ANNUAL REPORT
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ANNUAL REPORT
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SIPPE <strong>REPORT</strong><br />
<strong>ANNUAL</strong> <strong>REPORT</strong><br />
2010-2011<br />
Shanghai Institute of Plant Physiology & Ecology<br />
Chinese Academy of Sciences
SIPPE <strong>REPORT</strong><br />
Director’s Report<br />
Shanghai Institute of Plant Physiology and Ecology (SIPPE), Chinese<br />
Academy of Science (CAS), was formed by integration of the former<br />
Shanghai Institute of Plant Physiology and Shanghai Institute of<br />
Entomology on May 19 th , 1999. The mission of SIPPE is to achieve<br />
breakthrough in cutting knowledge of plant, insect and microbiology<br />
sciences and in the industrialization of agriculture and industrial<br />
biotechnology, to play a leading role in innovation in the national<br />
science and technology innovation system. Currently, SIPPE focuses on deciphering physiology<br />
and genetic basis of rice yield and quality, physiology and biotechnology in plant stress resistance<br />
improvement, systems biology of microbial metabolism and synthetic biology.<br />
SIPPE is always adhering to the “people-oriented” concept and pays a great attention to recruit<br />
the distinguished scientists. In 2010 and 2011, SIPPE made remarkable achievements in<br />
recruiting new principle investigators and organizing the research teams. Professor Jian-Kang<br />
Zhu (member of National Academy of Science in USA) obtained the national “Top One-Thousand-<br />
Outstanding-Talents Program” fund. Totally 9 principle investigators are supported by various<br />
funds including “Outstanding Young Investigator Fund” from NSFC, national “One-Thousand-<br />
Young-Talents Program” or CAS “One-Hundred-Talents Program”. One scientist was elected as<br />
the member of Academy of Sciences of Developing Countries and one has won the HLHL prize.<br />
With a good academic atmosphere, SIPPE has gained a number of important achievements in the<br />
last two years. More than 160 research papers including 13 papers in leading scientific journals<br />
such as Nature Genetics, Science, PNAS, Plant Cell and PLOS Genetics were published and 23<br />
patents have been authorized and a new crop variety has obtained the protection of new varieties.<br />
In addition, National Center of Plant Gene Research (Shanghai) was formally established, which<br />
will speed up the industrialization of plant biotechnology. The National Key Laboratory of Plant<br />
Molecular Genetics (NKLPMG) was evaluated as one of the "Excellent" laboratories by the<br />
Ministry of Science and Technology.<br />
In the next few years, SIPPE will allocate resources rationally, improve the supporting system and<br />
do its best to create new research mechanisms to build a first-class institution.<br />
On behalf of the Institute, I would like to acknowledge the enormous supports from our sponsor<br />
and funding agencies and thank our staff and students for their persistent hard working. I hope<br />
that we will make a new chapter in SIPPE history with greater degrees of enthusiasm, scientific<br />
ideas, pragmatic attitudes and morale.<br />
HongWei Xue
Content<br />
Introduction<br />
Introduction of SIPPE<br />
Institute Organization<br />
2010-2011 Progress<br />
Highlights of Achivements<br />
Projects<br />
Research Team Construction<br />
Cooperation and Extention<br />
2<br />
3<br />
12<br />
24<br />
25<br />
28<br />
INTRODUCTION<br />
Appendix<br />
Publication<br />
Major Event<br />
Representative Publications<br />
Committee<br />
30<br />
37<br />
41<br />
54
SIPPE<br />
Academic Degree Committee<br />
Advisory Committee Academic Committee<br />
Research Sector Administration Sector Supporting Sector<br />
Introduction<br />
SIPPE <strong>REPORT</strong><br />
研 究 所 介 绍<br />
Introduction of SIPPE<br />
2010-2011 SIPPE Report<br />
Institute Organization<br />
Shanghai Institute of Plant Institute Physiology Introduction<br />
and Ecology (SIPPE) is one of the institutions of the Shanghai Institutes<br />
for Biological Sciences (SIBS), Chinese Academy of Science (CAS). SIPPE was established by the integration<br />
of the former Shanghai Institute of Plant Physiology (SIPP) and Shanghai Institute of Entomology (SIE) on May<br />
Shanghai Institute of Plant Physiology and Ecology (SIPPE), Chinese Academy of Science (CAS),<br />
19 th , 1999. The former SIPP was initially evolved from the laboratory of Plant Physiology, Institute of Botany<br />
was formed by the integration of the former Shanghai Institute of Plant Physiology (SIPP) and<br />
of the Academia Sinica, which was founded at the town of Beipei, Chongqing on May 1 st , 1944. On January<br />
Shanghai Institute of Entomology (SIE) on May 19 th , 1999. The former SIPP was developed from the<br />
laboratory of Plant Physiology, Institute of Botany of the Academia Sinica, which was founded in<br />
23 rd , 1953, Institute of Experimental Biology, CAS, was separated from the Academia Sinica and became the<br />
Chongqing Beipei on May 1 st , 1944. On January 23 rd , 1953, Institute of Experimental Biology of<br />
predecessor of SIPP. It was the cradle of plant physiology and biochemistry in China, and one of the pioneer<br />
Chinese Academy of Science was separated from the Academia Sinica and became the predecessor<br />
institutions that carried out molecular genetic researches in plants and microbes. Tremendous achievements have<br />
of SIPP. Many famous plant physiologists worked in SIPP. It was the cradle of plant physiology and<br />
been made in the fields of photosynthesis and nitrogen fixation in the early years. Former SIE, one of the main<br />
biochemistry research in China, and one of the pioneer institutes that carried out molecular genetic<br />
researches in plants and microbes.Tremendous success has been achieved in the field of<br />
research institutions on entomology in China, was founded in 1959 and once made great progresses in insect<br />
photosynthesis and nitrogen fixation, etc. The former SIE, one of the main research institutes in<br />
taxonomy, physiology, toxicology, co-evolution, pesticide resistance and sex pheromones.<br />
entomology of China was founded in 1959 and has made great progress in insect taxonomy,<br />
physiology, toxicology, co-evolution, resistance and sex pheromone.<br />
The mission of SIPPE is to generate knowledge of plants,<br />
microbes and insects through creative research, to train scientists<br />
for the future, and to benefit the sustainable agriculture, ecological<br />
environments, bio-energy and bio-manufacturing requirements<br />
in China. Our research topics include, if not all, functional<br />
genomics and physiology, synthetic biology, developmental<br />
and evolutionary biology, and biotechnologies by using plants,<br />
microbes and insects as model organisms.<br />
National Key Laboratory of Plant Molecular Genetics<br />
National Center of Plant Gene Research (Shanghai)<br />
National Center for Gene Research,CAS<br />
Key Laboratory of Insect Development and Evolutionary Biology, CAS<br />
Key Laboratory of Synthetic Biology, CAS<br />
Laboratory of Photosynthesis and Environmental Biology<br />
Executive Office<br />
Aiming at the cutting edge of biological sciences in important physiological processes and<br />
interaction between plants, microorganisms and insects, SIPPE focus on original systematic and<br />
applied basic research to meet strategic requirements for sustainable agriculture, ecological<br />
By the end of 2011, there are 403 research scientists working at<br />
SIPPE including 51 professors, 55 associate professors and senior<br />
technicians. SIPPE now has 9 CAS academicians, 11 winners for<br />
the NSFC “National Outstanding Young Investigator Award”, three awardees for “the One-Thousand-Talents”<br />
environment, bio-energy and bio-manufacturing in China. The goal of SIPPE is to achieve<br />
schemes, and 28 awardees for the CAS “One-Hundred-Talents” program. The research capacity of SIPPE has<br />
breakthrough in deciphering molecular physiology and genetic basis of rice yield and quality,<br />
been continuously strengthened by the supports from the funding agencies of the National Natural Science<br />
physiology and biotechnology in plant stress resistance improvement, systems biology study of<br />
microbial metabolism and synthesis of artificial life system; to achieve substantial progress in functional<br />
Foundation of China (NSFC) and the Ministry of Science and Technology (MOST), Ministry of Agriculture<br />
genomics of important traits formation of plant, insects and micro-organisms, fine regulation of plants<br />
and CAS. In particular, three innovative research teams including “The system and synthetic biology research<br />
and insects development, metabolic and biosynthetic pathways in plant, insect and micro-organisms,<br />
of microbial metabolism” have been funded by NSFC, and three projects have won the MOST’s National Basic<br />
plant gene regulation in insect, disease and stress resistance, advanced biotechnology, etc.; to<br />
Research Program (“973”) and National Science and Technology Infrastructure Program supports.<br />
In the next five to ten years, SIPPE will continue to strengthen its research team by recruiting outstanding young<br />
scientists, to improve its institutional managements, and to improve its national and international competitiveness<br />
in plant, microbe and insect sciences. The Institute will expand its collaborations with local and international<br />
institutions and enterprises for related basic and translational research. In general, SIPPE will devote its efforts to<br />
establish itself as a world-recognized institution by reinforcing its both basic and applied research capacities.<br />
7<br />
Projects Management Office<br />
Crop Cultivation and Breeding Base<br />
Core Facility Center<br />
Phytotron<br />
Shanghai Entomological Museum<br />
2<br />
3
Introduction<br />
SIPPE <strong>REPORT</strong><br />
National Key Laboratory of Plant Molecular Genetics<br />
The National Key Laboratory of Plant Molecular Genetics (NKLPMG), the first national key laboratory for plant<br />
molecular biological research, was approved for its organization in 1986 and was officially founded in 1988.<br />
NKLPMG mainly focuses on the following research areas: (1) plant functional genomics; (2) plant molecular<br />
physiology and development; (3) plant biotechnology and genetic engineering. The current director of NKLPMG<br />
is Professor Hong-Wei Xue and the chairman of academic board is Professor Zhi-Hong Xu, an academician of<br />
the Chinese Academy of Sciences (CAS).<br />
NKLPMG comprises of an active and energetic research team. Currently, there are 24 research groups and 120<br />
staff in NKLPMG, including 5 academicians of the CAS, 1 honored as “the One-Thousand-Talents”, 6 honored<br />
as “National Outstanding Young Investigator” by NSFC, and 14 honored as “the One-Hundred-Talents”.<br />
In the past two years, through unremitting efforts of all members, NKLPMG has been undertaking a total of 205<br />
research projects, among which 78 were newly approved from the Ministry of Sciences and Technology (973<br />
and 863 programs), the National Plant Transgenic Program, the National Natural Science Foundation of China,<br />
etc. Moreover, NKLPMG has made great progress in the research of rice functional genomes, plant development<br />
and cell biology, plant hormone and signal conduction, plant nutrition and metabolism, and plant biotechnology.<br />
NKLPMG published 103 scientific papers, of which 67 appeared on the SCI indexed journals including Plant<br />
Cell, PNAS, EMBO J, Cell Res, Plant J, Plant Physiol, etc. In the same period of time, NKLPMG obtained 12<br />
patent licenses and is currently applying for additional 40 national and international patents.<br />
In 2011, NKLPMG obtained the top record of “Excellence” in the national key laboratory assessment organized<br />
by the Ministry of Science and Technology, representing considerable accumulations of systematic scientific<br />
researches and comprehensive advantages in plant molecular biology and molecular physiology for NKLPMG.<br />
NKLPMG will make further effort to produce innovative contributions to plant and agricultural sciences and aim<br />
to be a world-class laboratory of plant Science.<br />
Homepage of NKLPMG: http://www.nlpmg.labs.gov.cn/<br />
XiaoYa Chen Academician Plant Secondary Metabolism and Cotton Biology<br />
YuDa Fang Professor Cell Biology of Plant Genome and Epigenome<br />
JiMing Gong Professor Mineral Nutrition and Phytoremediation<br />
FangQing Guo Professor Nitric Oxide Signal Transduction and Mechanisms of Senescence<br />
YuKe He Professor Plant Morphogenesis and Molecular Breeding<br />
ZuHua He Professor Plant Disease Resistance and Rice Functional Genomics<br />
Hai Huang Professor Plant Developmental Biology<br />
JiRong Huang Professor G-protein Signaling and Chloroplast Development<br />
LaiGeng Li Professor Cell Wall Formation and Biomass Biosynthesis Studies<br />
HongXuan Lin Academician The Genetics and Functional Genomics of Crop<br />
HongTao Liu Professor Light Regulated Development and Light Signal Transduction<br />
HuaLing Mi Professor Protein-Protein Interactions in Chloroplasts<br />
WeiHua Tang Professor Plant-Fungal Interaction and Plant Reproductive Biology<br />
JiaWei Wang Professor Plant Small Regulatory RNAs<br />
YongFei Wang Professor Ion Channel and Signal Transduction in Plant Cells<br />
QiGuang Wen Professor Ethylene Signal Transduction<br />
Han Xiao Professor Fruit Developmental Biology<br />
Fang Xie Professor Legume-Rhizobium Symbiotic Nitrogen Fixation<br />
HongWei Xue Professor Plant Hormones and Seed Development<br />
ZhenBiao Yang Professor Plant Cell Biology and Signal Transduction<br />
HongXia Zhang Professor Engineering Salt Tolerant Plants<br />
Peng Zhang Professor Cassava and Sweetpotato Biotechnology<br />
Peng Zhang Professor Structural Biology<br />
4<br />
5
Introduction<br />
SIPPE <strong>REPORT</strong><br />
Key Laboratory of Synthetic Biology, CAS<br />
The Key Laboratory of Synthetic Biology (KLSynB) is a key laboratory of the Chinese Academy of Sciences<br />
(CAS), established in December 2008 through reorganization of the Laboratory of Molecular Microbiology.<br />
KLSynB focuses on developing the theory of synthetic biology under the guidance of systems biology via<br />
integrative analysis and comprehensive characterization of various levels of biological systems, integrating the<br />
theory of systems biology with the tools of synthetic biology in order to guide the production of biomaterial,<br />
biomedical and bio-fuel molecules through modification and/or synthesis of novel or improved biosystems (cell<br />
factory and molecular machine), and innovating synthetic biology technologies and transforming the cuttingedge<br />
core techniques into engineering-oriented platform and related resource banks/databases for research and<br />
application. The current director of KLSynB is academician Guo-Ping Zhao and the chairman of academic board<br />
is academician Sheng-Li Yang.<br />
KLSynB currently consists of 67 permanent staffs including 12 principal investigators, 9 associated professors,<br />
21 assistant professors and 9 technicians. One professor is honored as academician, three as “the Distinguished<br />
Young Investigator” by NSFC, six as “the One-Hundred-Talents” of CAS, and four as the Pujiang Scholars of<br />
Shanghai. KLSynB has been supported by 104 grants with RMB 42 million from various sources of funding<br />
agencies during 2010-2011, including one from the National “973” program and one from the Creative Research<br />
Group of NSFC. Fifty-eight peer-reviewed SCI-sourced papers have been published. In 2011, KLSynB hosted an<br />
international conference of the Six-Academy Synthetic Biology Symposium.<br />
Key Laboratory of Insect Developmental and<br />
Evolutionary Biology, CAS<br />
The Key Laboratory of Insect Developmental and Evolutionary Biology (IDEB), CAS, was founded in 2009.<br />
The research topics conducted at IDEB are mainly focused on the genomics and functional genomics studies of<br />
insects, primarily the Bombyx mori and Drosophila melanogaster. The main mission of IDEB is to reveal the<br />
complexity of insect systematics, development, the interactions between insects and insects, and between insects<br />
and other organisms at the molecular and genetic levels. The acquired knowledge can be used for innovative<br />
insect pest managements and effective use of beneficial insects. In addition, IDEB will work together with the<br />
Shanghai Entomological Museum to train and educate graduates for advanced insect sciences, and to spread and<br />
broaden insect knowledge for public audience. The current director of IDEB is Professor Cheng-Shu Wang and<br />
the chairman of academic board is Professor Le Kang, a CAS academician.<br />
Currently, there are one academician, 8 professors and 8 associate professors plus more than 100 staff, postdocs<br />
and graduate students at IDEB. During 2010-2011, the scientists at IDEB have been involved in 60 research<br />
programs from the Ministry of Sciences and Technology (973 and 863 programs), National Natural Sciences<br />
Foundation of China, and CAS. More than 60 high profile papers have been published by IDEB members on<br />
the journals of PNAS, PLoS Genetics, Genome Biology, Development, Cell Research, JBC, etc. IDEB has<br />
established a close relationship with the Shanghai Key Lab of Chemical Biology, East China University of<br />
Science and Technology. IDEB successfully organized “The 3 rd International Symposium on Insect Physiology,<br />
Biochemistry and Molecular Biology” in 2011 in Shanghai.<br />
WeiHong Jiang Professor Microbial Metabolic Regulation and Enzyme Engineering Group<br />
LaiGeng Li Professor Group of Cell Wall Formation and Biomass Biosynthesis Studies<br />
Xuan Li Professor Bioinformatics Research<br />
ZhongJun Qin Professor Molecular Genetics of Actinomycetes and Genomic Engineering Group<br />
Yong Wang Professor Synthetic Biology for Natural products Development<br />
LiYou Xiao Professor Chemical Biology and Enzymology<br />
Chen Yang Professor Microbial Metabolic Engineering and Comparative Genomics Group<br />
Sheng Yang Professor Microbial Metabolic Regulation and Enzyme Engineering Group<br />
Peng Zhang Professor Cassava and Sweetpotato Biotechnology Group<br />
GuoPing Zhao Academician Microbial Functional Genomics Group<br />
ZhiHua Zhou Professor Microbial Metagenomics and Bioenergy Conversion Group<br />
YongPing Huang Professor Insect Functional Genomics<br />
Sheng Li Professor Insect Development and Metamorphosis<br />
ErJun Ling Professor Insect Innate Immunology and Pest Control<br />
JianHua Shen Professor Molecular Toxicology<br />
ChengShu Wang Professor Insect Molecular Pathology<br />
YongZhen Xu Professor Insect RNA Splicing and Development<br />
WenYing Yin Academician Insect Taxonomy and Systematics<br />
6<br />
7
Introduction<br />
SIPPE <strong>REPORT</strong><br />
WeiMing Cai Professor Molecular Mechanism of Stress Tolerance of Plants and Space Biology<br />
JiRong Huang Professor G-protein Signaling and Chloroplast Development<br />
HuaLing Mi<br />
YunGang Shen<br />
Laboratory of Photosynthesis and Environmental Biology<br />
The Laboratory of Photosynthesis and Environmental Biology was reconstituted from the former two laboratories<br />
for photosynthesis and environmental biology in 2008. The former photosynthesis laboratory founded by the<br />
famous Academician Hong-Zhang Yin in 1956 was the first laboratory in this field in China, and had splendid<br />
achievements. Currently, the laboratory is interested in physiological and molecular mechanisms underlying<br />
photosynthesis, plant water and stress, gravity and sugar signaling. The long-term mission of the Lab is to provide<br />
crop breeders with genetic resources and technology to improve yield and food quality. The current director of the<br />
Lab is Professor Ji-Rong Huang, and chairman of academic board is Academician Yun-Gang Shen.<br />
The Lab has 38 researchers including two academicians, 8 principal investigators, 28 associate and assistant<br />
professors, 42 graduate students, and 4 postdoctoral researchers. Professor Ji-Rong Huang was supported by<br />
the “National Science Fund for Distinguished Young Investigator” in 2010. The Lab has 42 scientific research<br />
projects (more than RMB 20 million) from the Ministry of Sciences and Technology (973 and 863 programs),<br />
National Natural Science Foundation of China, and the National Plant Transgenic Program. In the past two<br />
years, the Lab published 70 papers, 58 of which in SCI journals, applied 7 patents, and made significant and<br />
substantial progresses on understanding of Rubisco activation, NAD(P)H dehydrogenase and its relationship<br />
with respiration of chloroplasts and cyclic electron transport, molecular basis of chloroplast development,<br />
regulation of photosynthetic efficiency, the resistance to abiotic stress; the development of techniques related to<br />
plant proteomic study, space biology and application of controlled agriculture. In terms of international scientific<br />
communication, the lab was involved to organize “The 15 th International Conference on Photosynthesis” and “The<br />
2 nd International Conference on Plant Metabolism”.<br />
Professor<br />
Academician<br />
Regulation of Photosynthetic Electron Transports in the Operation of<br />
Photosynthetic Apparatus<br />
Photophosphorylation and Regulation of the Operation of Photosynthetic<br />
Apparatus<br />
HuiQiong Zheng Professor Biology and Biotechnology in Microgravity<br />
National Center of Plant Gene Research (Shanghai)<br />
The National Center of Plant Gene Research (NCPGRS, Shanghai), a key state project of crop molecular<br />
breeding and commercialization, was authorized to be launched in 2009, and was formally inaugurated on<br />
June 25 th , 2011. NCPGRS consists of the well-established scientific research units in Shanghai, Zhejiang and<br />
Jiangsu, including Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences,<br />
Shanghai Jiaotong University, Fudan University, Zhejiang University, Nanjing Agricultural University, Yangzhou<br />
University, Chinese National Rice Research Institute, Zhejiang Academy of Agricultural Sciences, Shanghai<br />
Academy of Agricultural Sciences, Jiangsu Academy of Agricultural Sciences, as well as the leading seed<br />
company Longping High-Tech Industry Group, to format the R & D strategic alliances. The current director of<br />
NCPGRS is Academician Xiao-Ya Chen and the Chair of Advisory Committee is Academician Zhi-Hong Xu.<br />
NCPGRS serves national agricultural demand, and focuses on gene discovery and molecular breeding application<br />
of pest and disease resistance, yield, quality, stress tolerance, and nutrition and water efficiency in the major<br />
crops such as rice, cotton, wheat and soybean. Several technique platforms will be established, including (1)<br />
large-scale gene discovering systems; (2) high-throughput gene function analysis and application evaluation; (3)<br />
crop metabolism and synthetic biology. The major objective of NCPGRS is to establish a world-class integrity<br />
research center from gene discovery, genetic resource innovation, to crop improvement evaluation.<br />
National Center for Gene Research, CAS<br />
In 1992, the National Center for Gene Research (NCGR) was established jointly by the Ministry of Science and<br />
Technology, the Chinese Academy of Sciences (CAS), and the Shanghai local government to provide a major focus in<br />
China for mapping and sequencing the rice genome, and genomes of other organisms. Since 1998, NCGR has been a<br />
member of the International Rice Genome Sequencing Project (IRGSP) to completely sequence the entire rice japonica<br />
genome. NCGR has been working on the chromosome 4 sequencing in close collaboration with the IRGSP members,<br />
the Chinese National Human Genome Center at Shanghai, and Institute of Genetics and Developmental Biology of<br />
CAS. The current director of NCGR is Professor Bin Han.<br />
NCGR has a staff size of 40, consists of three research groups: sequencing department, large-scale platform and<br />
bioinformatics department. NCGR has a high-performance DNA sequencing facility with 16 DNA sequencers. There<br />
are many other types of equipment such as SGI-3800 server, lots of SUN workstations, PCR amplifiers, real-time PCR,<br />
DNA synthesizers, automatic workstation, fluorescent microscope, ultra centrifuge, incubators, and ultra-low temperature<br />
freezers. NCGR has also various rice clone resources, including two rice japonica BAC/PAC clone libraries, three rice<br />
indica BAC/PAC clone libraries, rice indica full-length cDNA library, and some other BAC and cDNA libraries.<br />
Uncovering the genetic basis of agronomic traits in crop landraces that have adapted to various agro-climatic conditions<br />
is important to world food security. NCGR sequenced 517 rice landraces, constructed a high-density haplotype map of<br />
rice genome by using a novel data imputation method and also performed genome-wide association studies (GWAS)<br />
for fourteen agronomic traits in the population of indica subspecies. The loci identified through GWAS explained<br />
~36% of the phenotypic variance on average. This study thus demonstrates that an integrated approach of secondgeneration<br />
genome sequencing and GWAS can be used as a powerful complementary strategy to classical bi-parental<br />
cross mapping for dissecting complex traits in rice, and provides a fundamental resource for rice genetics research and<br />
breeding. NCGR further developed an analytical framework for haplotype-based de novo assembly of the low-coverage<br />
sequencing data in rice. This study thus demonstrates that the integrated approach of sequence-based GWAS and<br />
functional genome annotation has the potential to resolve complex traits to their causal polymorphisms in rice.<br />
8<br />
9
Introduction<br />
SIPPE <strong>REPORT</strong><br />
Crop Cultivation and Breeding Base<br />
Experimental and Breeding Base is located at Wushe Modern Agricultural<br />
Zone, Songjiang District in Shanghai. It includes a biosafety-controlled<br />
nursery for genetically modified crops and plant trial fields.There is<br />
an indoor space of 2000 m 2 , equited with complete research and living<br />
facilities including laboratories, offices, conference room, staff dormitory,<br />
warehouses, etc. The base was already an experiment and platform for<br />
functional genomic research and crop breeding.<br />
2010-2011 PROGRESS<br />
Core Facility Center<br />
Taking advantage of the international leading equipments available in<br />
the institute, SIPPE make every effort on the studies of cell biology,<br />
metabolism, functional genomics and proteomics. There are many<br />
facilities including laser scanning confocal microscopes, scanning<br />
electron microscopes, transmission electron microscope, real-time PCR<br />
instruments, fluorescence spectrophotometers, HPLC-MS, GC-MS, etc.<br />
Phytotron<br />
A phytotron with 4700 m 2 was built on the campus. The environmentally<br />
controlled area (1650 m 2 ) is divided into 83 units, with rooms equipped<br />
for full climate control.<br />
Shanghai Entomological Museum<br />
The Insect Specimen Gallery in the Shanghai Entomological Museum<br />
is one of the largest insect museums in China with a broad collection<br />
of insect specimens. The collection is composed of over 1,000,000<br />
specimens from across the country, including 400,000 soil animals (over<br />
1,000 types of insects). This collection provides valuable resources for<br />
studying the insect fauna of China.<br />
10<br />
11
2010-2011 Progress 研 究 所 介 绍<br />
2010-2011 SIPPE SIPPE <strong>REPORT</strong> Report<br />
Highlights of Achivements<br />
In 2010 and 2011, scientists of SIPPE made great contributions in many research fields, and published 161<br />
papers in leading scientific journals including Nature Genetics, Science, PNAS, PLoS Genetics, Genome<br />
Research, Plant Cell, ect. Sixty patents were applied, twenty-three inventions have been granted, including one<br />
from South Africa. A new variety of sweet potato “Taizhong No.9” was examined and approved by Crop Variety<br />
Authorization Committee of Shandong Province (No. 2010041).<br />
The achievements in the following fields:<br />
Crop Functional Genomics<br />
Analysis of Rice Functional Genomics Based on High-Throughput Sequencing Technology<br />
Research on Genes Controlling Important Agronomic Traits<br />
Molecular Mechanisms Underlying Important Processes in Plant Physiology<br />
Plant Hormone and Signal Transduction<br />
Plant Development<br />
Study of Plant Cell Biology<br />
Plant Metabolic Regulation and Biotechnology<br />
Mineral Nutrition and Metabolism in Plants<br />
Analysis of Rice Functional Genomics Based on High-Throughput<br />
Analysis of Rice Functional Genomics Based on High-Throughput<br />
Sequencing Technology<br />
Rice (Oryza sativa L) is an economically important crop that accounts for ~20% of the world’s caloric<br />
intake. To be grown successfully under a variety of climatic conditions across the globe, breeders maintain<br />
rice at high genetic diversity. Second-generation sequencing technologies have enabled resequencing of a<br />
large number of genomes and have provided the possibility of high-throughput genotyping and large-scale<br />
genetic variation surveys. Identification of allelic variations underpinning the phenotypic diversity<br />
observed in rice will have enormous practical implications in rice breeding.<br />
Professor Bin Han’s group sequenced 517 rice landraces and constructed a high-density haplotype map of<br />
rice genome by using a novel data imputation method. They performed genome-wide association studies<br />
(GWAS) for fourteen agronomic traits in the population of indica subspecies. The loci identified through<br />
GWAS explained ~36% of the phenotypic variance on average. The peak signals at six loci tied closely to<br />
the previously identified genes. This study thus demonstrates that an integrated approach of<br />
second-generation genome sequencing and GWAS can be used as a powerful complementary strategy to<br />
classical bi-parental cross mapping for dissecting complex traits in rice, and provides a fundamental<br />
resource for rice genetics research and breeding (Nature Genetics, 2010).<br />
Their group further extended the sample to 950 world-wide rice varieties, and constructed a high-density<br />
haplotype map by the imputation method. They identified a total of 32 new loci associated with flowering<br />
time and ten grain-related traits, indicating that the larger sample dramatically lifted the power of GWAS in<br />
rice. They developed an analytical framework for haplotype-based de novo assembly of the low-coverage<br />
sequencing data in rice. This study thus demonstrates that the integrated approach of sequence-based<br />
GWAS and functional genome annotation has the potential to resolve complex traits to their causal<br />
polymorphisms in rice (Nature Genetics, 2011).<br />
Biomass and Bioenergy Plants<br />
Insect Developmental and Evolutionary Biology<br />
Comparative Genomics of Insect Pathogenic Fungi<br />
Insect Development and Evolutionary Biology<br />
Synthetic Biology<br />
Systems and Synthetic Biology of Microbial Metabolism<br />
Microbial Industrial Biotechnology<br />
Genome analysis of low-coverage sequencing of rice varieties<br />
Genetic diversity of rice germplasm<br />
1<br />
12<br />
13
2010-2011 Progress SIPPE <strong>REPORT</strong><br />
Research on Genes Controlling Important Agronomic Traits<br />
Research on Genes Controlling Important Agronomic Traits<br />
During 2010 to 2011, the institute made great progress in discovery, innovation and application of genetic<br />
resources that control important agronomic traits in crops such as rice.<br />
Rice productivity is highly associated with its architectural pattern, including plant height, which is mainly<br />
attributable to stem internode elongation. The uppermost internode is of particular importance for rice<br />
productivity, since the elongation of the uppermost internode promotes panicle emergence and subsequent<br />
grain filling. Professor ZuHua He’s group has been devoted to dissecting the rice internode development<br />
and identified Eui gene which controls rice uppermost internode<br />
elongation by modulation of the bioactive GA levels. Thereafter they<br />
find that a new gene BUI1, which encodes the class II formin FH5.<br />
Mutation of BUI1 results in severely disruption of the actin<br />
cytoskeleton and consequently inhibition of cell expansion. They<br />
found that BUI1 could efficiently promote actin filament assembly<br />
and actin bundling. Thus, their study identified a rice formin protein<br />
BUI1 that regulates de novo actin nucleation and spatial organization<br />
of the actin filaments, which are important for proper cell expansion<br />
and rice morphogenesis. The identification of BUI1 also reveals a<br />
new regulatory mechanism underlying the development of rice<br />
internodes (Plant Cell, 2011).<br />
Domestication has played important roles in crop breeding. Many important agronomic trait-related genes<br />
are subjected to domestication. Previous study in Zuhua He’s lab has demonstrated that GIF1 encodes a<br />
cell-wall invertase required for grain filling. Sequence analysis of GIF1 region revealed significant<br />
domestication signatures in its promoter, which restricted GIF1 expression specifically to the ovular trace.<br />
Their further study identified another cell-wall invertase gene OsCIN1. GIF1 and OsCIN1 constitute a pair<br />
of duplicate genes with differentiated expression and function through independent selection (BMC Evol<br />
Biol, 2010). Using a genetic population constructed by a cross between O. rufipogon W1943 (black hull)<br />
and O. sativa indica cv Guangluai 4 (straw-white hull), Professor Bin Han’s group cloned Bh4, an a amino<br />
acid transporter protein, which plays a critical role in controlling seed hull color during grain ripening. Bh4<br />
sequence alignment revealed a significant reduction in nucleotide diversity in rice cultivars probably due to<br />
artificial selection, suggesting that straw-white hull was selected as an important visual phenotype of<br />
nonshattered grains during rice domestication (Plant Physiol, 2011).<br />
As the predominant component of milled rice, the physicochemical properties of starch determine the<br />
eating, cooking, and milling qualities of rice. To systemically identify the genes that regulate rice starch<br />
biosynthesis, Professor HongWei Xue’s group performed gene co-expression analysis to identify candidate<br />
regulators for starch biosynthesis. They isolated 61<br />
transcription factors predicted to be involved in starch<br />
synthesis, including Rice Starch Regulator1 (RSR1).<br />
Mutation of RSR1 results in increased amylose<br />
content, altered fine structure of amylopectin, and<br />
decreased gelatinization temperature. The results<br />
demonstrate the potential of co-expression analysis<br />
for studying rice starch biosynthesis and the<br />
regulation of a complex metabolic pathway, and<br />
provide informative clue to facilitate the improvement<br />
of rice quality and nutrition (Plant Physiol, 2010).<br />
WT<br />
rsr1<br />
Plant Hormone and Signal Transduction<br />
Plant Hormone and Signal Transduction<br />
Plant hormones play crucial regulatory roles in plant growth and development. Studies of the<br />
corresponding functional mechanism are significant and helpful to understand how plants grow and<br />
develop, and contribute to the agricultural development. With the technological development of genetics<br />
and molecular biology, some important progresses on the molecular mechanism of plant hormones have<br />
been gained. However, the metabolism of different hormones, the signaling transduction pathway,<br />
functional mechanism, and interactions between different hormones or with other signaling pathways, need<br />
further studies.<br />
GA is crucial for multiple aspects of plant growth and development. Prof. HongWei Xue’s group identified<br />
a rice T-DNA insertion mutant earlier flowering1 (el1), which is deficient in a casein kinase I that plays<br />
critical roles in both plants and animals. el1 had an enhanced GA response including the elongated second<br />
leaf sheaths and α-amylase activities. Transcription of GA biosynthesis-related genes was reduced in el1,<br />
which is consistent with the stimulated GA signaling.<br />
No. of flowering plants<br />
16<br />
14<br />
12<br />
10<br />
8<br />
6<br />
4<br />
2<br />
0<br />
WT<br />
WT<br />
el1<br />
el1<br />
60~62 63~65 66~68 69~71 72~74<br />
Heading time (days)<br />
WT<br />
el1<br />
WT<br />
el1<br />
Biochemical characterization showed that EL1<br />
specifically phosphorylates rice DELLA protein<br />
SLR1, a key negative regulator of GA signaling,<br />
providing a direct evidence for SLR1<br />
phosphorylation. The severe dwarf phenotype and<br />
suppressed GA signaling by SLR1 overexpression<br />
was significantly reduced by EL1 deficiency,<br />
indicating the negative effect of SLR1 on GA<br />
signaling requires the EL1 function. Further studies<br />
revealed that the phosphorylation of SLR1 is<br />
important for maintaining its activity and stability,<br />
which provided important clues of casein kinase I<br />
effects in regulation of GA signaling and plant<br />
development (EMBO J, 2010).<br />
Rice ABI5-like1 (ABL1) encodes a bZIP transcription factor and participates in the stress responses by<br />
regulating the expression of a series of ABRE-containing WRKY family genes. Expression of rice ABL1<br />
could be significantly enhanced by hormones ABA and IAA, and the abl1 mutant is hypersensitive to<br />
exogenous IAA. These shed informative lights on the interaction of ABA-auxin signaling (Plant Physiol,<br />
2010).<br />
Key enzyme of Arabidopsis phosphatidylinositol signaling,<br />
PIP5K2, and its product, PtdIns(4,5)P2, is disclosed to<br />
regulate the lateral root formation and root gravity response<br />
through modulating auxin accumulation and polar auxin<br />
transport by enhancing the vesicular trafficking and cycling<br />
of PIN proteins(Cell Research, 2011).<br />
Dr. Sheng Teng and other researchers disclosed that eight<br />
fructose-sensing quantitative trait loci (QTLs) (FSQ1–8)<br />
existed in Arabidopsis fructose-specific signaling pathway.<br />
FSQ6-associated fructose-signaling pathway functions<br />
independently of the hexokinase1 glucose sensor and its<br />
downstream signaling interacts with abscisic acid (ABA) -<br />
and ethylene-signaling pathways (PNAS, 2011).<br />
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2010-2011 Progress SIPPE <strong>REPORT</strong><br />
研 究 所 介 绍<br />
2010-2011 SIPPE Report<br />
Plant Development<br />
Plant Development<br />
Leaves are the plant organs for photosynthesis, through which the free carbon dioxide isassimilated. The<br />
molecular regulatory mechanism of leaf development is therefore of significance. Researches in this field<br />
have been advanced substantially by several groups during 2010-2011.<br />
Arabidopsis AS1 and AS2 are important genes in specifying leaf adaxial identity, and ribosome and 26S<br />
proteasome, which are the essential proteins for living organisms, are also involved in leaf polarity<br />
establishment. The characterization of a novel as2 enhancer mutant ae7, which exhibits developmental<br />
defects in the leaf adaxial side, partly answered how Ribosome and 26S proteasomegenes regulate leaf<br />
polarity. The ae7 leaves contained the reduced cell number with the enlarged cell size, indicating that AE7<br />
is required for cell proliferation.The AE7 gene is expressed in a spotted pattern in plant tissues, similar to<br />
some cell-cycle marker genes, further support the notion that the basic function of AE7 may be involved in<br />
cell division.<br />
Both double mutants, combine as1 (or as2) with Elongator and grf mutants, showed the enhanced defects<br />
in the leaf adaxial-abaxial axis. These results indicate that defective cell division could generally affect leaf<br />
adaxial-abaxial polarity. It was proposed that the newly initiated leaf primordium is an abaxialized<br />
structure, and differentiation toan abaxial identityisthe default pattern in the absence of actionsof the<br />
adaxially-promoting factors. Hence, because the adaxially featured cells initiate and accumulate later than<br />
the abaxially featured cells, for the final balanced adaxial and abaxial domains in mature leaves, the<br />
adaxial cells must proliferate more rapidly than the abaxial cells at certain leaf developmental stages.<br />
Although all leaf cells in both adaxial and abaxial domains are affected in the cell proliferation defective<br />
mutants, the adaxial domain must suffer more severely than the abaxial one (Plant J, 2010, 2011).<br />
The production and distribution of plant trichomes is temporally and spatially regulated. After entering into<br />
the flowering stage, Arabidopsis thaliana plants have progressively reduced numbers of trichomes on the<br />
inflorescence stem, and the floral organs are nearly glabrous. SQUAMOSA PROMOTER BINDING<br />
PROTEIN LIKE (SPL) genes, which define an endogenous flowering pathway and are targeted by<br />
microRNA 156 (miR156), temporally control the trichome distribution during flowering. During plant<br />
development, the increase in SPL transcript levels is coordinated with the gradual loss of trichome cells on<br />
the stem. The MYB transcription factor genes<br />
TRICHOMELESS1 (TCL1) and TRIPTYCHON (TRY) are<br />
negative regulators of trichome development. Prof. XiaoYa<br />
Chen’s group showed that SPL9 directly activates TCL1 and<br />
TRY expression through binding to their promoters and that<br />
this activation is independent of GLABROUS1 (GL1). The<br />
phytohormones cytokinin and gibberellin were reported to<br />
induce trichome formation on the stem and inflorescence via<br />
the C2H2 transcription factors GIS, GIS2, and ZFP8, which<br />
promote GL1 expression. The GIS-dependent pathway does<br />
not affect the regulation of TCL1 and TRY by miR156-targeted<br />
SPLs, represented by SPL9. These results demonstrate that the miR156-regulated SPLs establish a direct<br />
link between developmental programming and trichome distribution (Plant Cell, 2011).<br />
Plant Cell Biology<br />
Studies of Plant Cell Biology<br />
The basic unit of packaging of chromatin is the nucleosome. Its core domain is a compact histone octamer<br />
which contains two molecules of each core histones H2A, H2B, H3 and H4. In addition to the canonical<br />
histones, there exist diverse variants of histones through addition, deletion or substitution of specific amino<br />
acid residues. The incorporation of histone variants into nucleosomes produces various forms of<br />
nucleosomes with divergent structures and functions, which play important roles in epigenetics and<br />
regulation of genome functions. The family of histone H3 includes the canonical histone H3.1, variant<br />
H3.3 and centromere-specific CenH3, which are highly conservative from fly to human and plant. Plant<br />
H3.3 differs in four amino acid residues from H3.1, these are residue 31 (with Thr in H3.3 instead of Gly<br />
in H3.1) and 41 (with Tyr in H3.3 instead of Phe in H3.1) in the N-terminal tail and residues 87 (with His<br />
in H3.3 instead of Cys in H3.1) and 90 (with Leu in H3.3 instead of Gly in H3.1) in the histone folding<br />
domain (HFD). By live-cell imaging, it was found that H3.1-GFP is mainly loaded into heterchromatin,<br />
while H3.3 is incorporated into euchromatin and highly enriched in rDNA arrays. Having investigated the<br />
dynamic loading or unloading of Arabidopsis histone H3.1, H3.3 and their mutated proteins into<br />
nucleoluar rDNA, Prof. YuDa Fang’s group revealed that amino acid residue 87, and to some extent<br />
residue 90, of Arabidopsis histone H3.3 is critical for its deposition into rDNA arrays. When RNA<br />
polymerase I directed nucleolar transcription is inhibited, wild type H3.3 and H3.3 containing mutations at<br />
residues 87 and 90, but not H3.3 containing mutations at residues 31 and 41, is depleted from the rDNA<br />
arrays. Based on these results, they put forward a model in which amino acids 87 and 90 in the core<br />
domain of H3.3 guide nucleosome assembly, while amino acids 31 and 41 in the N-terminal tail of<br />
Arabidopsis H3.3 guide nucleosome disassembly in nucleolar rDNA. As histone variant H3.3 is highly<br />
conserved in various organisms, the result may have broad biological significance (PNAS, 2011).<br />
In the studies on plant germ cells, Prof. WeiHua Tang’s group profiled laser-captured rice pollen mother<br />
cells by microarrays, and found that 59% of genes express in pollen mother cells (PMCs). Among these<br />
genes expressed in PMCs, 127 genes are not expressed in tricellular pollen or seedling (Plant Physiol,<br />
2010). In an invited review article in Semin Cell Dev Bio<br />
(2011), Prof. ZhenBiao Yang’s group updated the recent<br />
studies on pollen tip growth from aspects of the structure and<br />
signal regulation system, and summarized the mechanisms of<br />
regulating the rapid growth of pollen tip by integrating<br />
cellular and ex-cellular signals and coordinating membrane<br />
dynamics and recombination of cell wall in a manner of<br />
self-organization. In another study, Prof. HuiQiong Zheng’s<br />
group has investigated the structural events associated with<br />
vacuole biogenesis in root tip cells of tobacco seedlings<br />
preserved by high-pressure freezing and freeze-substitution<br />
techniques, and demonstrated that the lytic vacuoles (LVs) of<br />
root tip cells are derived from protein storage vacuoles (PSVs) by cell type-specific sets of transformation<br />
events (Plant Physiol, 2011).<br />
16<br />
5<br />
17
2010-2011 Progress SIPPE <strong>REPORT</strong><br />
植 物 生 理 生 态 研 究 所 年 报<br />
2010-2011 SIPPE Report<br />
Mineral Nutrition and Metabolism in in Plants<br />
Mineral nutrition and metabolism are essential processes that determine growth and economical output of<br />
plants,which enable plants to provide massive biomass and energy to plants themselves and also the<br />
secondary consumers in the food chain. Substantial progresses in this field have been obtained by serveral<br />
groups during 2010-2011.<br />
Nitrogen is one of the most studied macronutrients. Nitrate represents the major nitrogen source for most<br />
terrestrial plants, functioning as mineral<br />
nutrient as well as an important signal<br />
molecule to regulate plant development.<br />
Once taken up into plant roots, nitrate is<br />
subjected to long-distance transport to<br />
aerial parts, where nitrate assimilation<br />
and photosynthesis are directly coupled<br />
in chloroplast, and conferring plants<br />
increased energy efficiency than root<br />
assimilation. However, environmental<br />
stresses including low temperature, dim<br />
light, high salt and heavy metals tend to<br />
retain proportionally more nitrate in<br />
roots. How this happens and if it is of<br />
physiological improtance remain largely<br />
to be addressed, and Prof. JiMing Gong’s group contributes substantially to a better understanding of these<br />
questions by functional characterizing a nitrate transporter gene NRT1.8 (Plant Cell, 2010). NRT1.8 is the<br />
only one gene in nitrate assimilation pathway which is strongly responsive to Cd 2+ stress. Physiological<br />
analyses showed that NRT1.8 is a pH-dependent nitrate uptake transporter, and it functions primarily to<br />
transport nitrate across plasma membrane into xylem<br />
parenchyma cells, thus unloading nitrate from xylem sap<br />
and mediating nitrate long-distance transport from roots<br />
to shoots. Under Cd 2+ stress, NRT1.8 expression is<br />
upregulated and helps to retain more nitrates in roots, and<br />
consequently mediates the nitrate distribution between<br />
roots and shoots. In the loss-of-function mutant nrt1.8-1,<br />
nitrate redistribution under Cd 2+ stress was disrupted and<br />
plants showed increased sensitivity to Cd 2+ . These results<br />
reveal that nitrate reallocation into roots is actively<br />
regulated by NRT1.8 and plays an essential role in stress<br />
tolerance, rather than a passive consequence of inhibited<br />
transpiration rate as previously proposed.<br />
In addition, Prof. HongWei Xue’s group revealed that<br />
KASI is an essential regulator in the interaction between<br />
de novo fatty acid biosynthesis and chloroplast<br />
development (Plant Cell, 2010). Prof. JiRong Huang’s<br />
group discovered that GDPD1 plays an essential role in<br />
plant tolerance to environmental Pi deficiency (Plant J,<br />
2011).<br />
Biomass and Bioenergy Plants<br />
Biomass and Bioenergy Plants<br />
The institute focuses on the key biological questions and biotechnologies of starch and fiber-based<br />
bioenergy plants by exploring the molecular mechanism of biomass biosynthesis, verifying gene functions,<br />
and enhancing germplasm.<br />
Cassava (Manihot esculenta Crantz) and<br />
sweet potato (Ipomoea batatas [L.] Lam.)<br />
are important starchy root crops for<br />
bioenergy development. The development<br />
of novel germplasms with high yield and<br />
starch content and improving capacity of<br />
resistance to various stresses could<br />
promote their industrialization. In order to<br />
further increase yield, analysis of storage root formation and developmental mechanism is of importance.<br />
Using the microarray technology, thousands of differential expressed genes related to storage root<br />
development was analyzed. Metabolic pathways, such as glycolysis/gluconeogenesis, starch and sucrose<br />
metabolism etc., were actively regulated during the biological process. Based on the structural scenario and<br />
carbon flux, the first molecular model for the development of starchy storage root in cassava was<br />
suggested. These studies should not only facilitate our understanding of the storage root formation, but also<br />
explore a number of genes of interest for genetic improvement of cassava and sweet potato.<br />
Wild-type Transgenic<br />
Starch quality, an important agronomic trait of root crops,<br />
determines the conversion efficiency from biomass to<br />
bioenergy and the potency of novel bioproducts. Using the<br />
constitutive or vascular-specific promoters, expression of the<br />
amylase biosynthetic gene GBSSI was silenced in transgenic<br />
cassava, leading to the development of various waxy plants<br />
with amylopectin up to 98%. The alternation of starch<br />
property was further verified by different physico-chemical<br />
characterizations, including structural, viscosity and<br />
thermodynamics analyses. The well performance of these<br />
transgenic plant lines in the field trial also indicates a great<br />
potential of these waxy cassava for providing new materials<br />
in industrial applications (Biotech & Bioen, 2011).<br />
Significant progress has also been made in sweet potato<br />
traditional breeding, collaborated with Tai’an Academy of Agricultural Sciences. “TaiZhong No.9”, a<br />
recently released variety approved by the Crop Variety Authorization Committee of Shandong Province<br />
(No. 2010041), is a high-starch cultivar suitable for cultivation in Shandong and other Huanghuai regions.<br />
The cultivar has been planted for more than 100,000 hectares to promote local development, which<br />
significantly supports the development of bioenergy plants and regional agricultural economy.<br />
For woody plants, Prof. LaiGeng Li’s group identified a number of important new plasma membrane<br />
proteins which are closely associated with regulating secondary vascular differentiation in poplar. A<br />
functional study of rice 4-coumarate: CoA ligase (4CL, EC 6.2.1.12), a key enzyme involved in<br />
monolignol biosynthesis, revealed that different biosynthetic pathways might exist in dicotyledons and<br />
monocotyledons. This study showed a cooperated evolution of plants and lignin biosynthesis (Plant<br />
Physiol, 2011).<br />
18<br />
19<br />
6
2010-2011 Progress SIPPE <strong>REPORT</strong><br />
Comparative Genomics of Insect Pathogenic Fungi<br />
There are about one thousand fungal species that can infect and kill insects. The species like Metarhizium<br />
spp. and Beauveria spp. have been developed as promising insect biocontrol agents while the Cordyceps<br />
species like C. militaris and C. sinensis are traditional Chinese medicines. Before our studies, the genome<br />
information of these fungi is unknown.<br />
Prof. ChengShu Wang’s group is focusing on the<br />
functional genomics and comparative genomics<br />
studies of insect pathogenic fungi. They initiated and<br />
finished the genome studies of Metarhizium robertsii,<br />
M. acridum and Cordyceps militaris. Comparative<br />
genomics study of the generalist species M. robertsii<br />
and acridid-specific M. acridum indicated that the<br />
genus Metarhizium may have evolved from plant<br />
endophytes or pathogens. Both M. robertsii and M.<br />
acridum have a strikingly larger proportion of genes<br />
encoding proteases, chitinases and lipases than other<br />
sequenced fungi to target insect cuticles. Relative to<br />
M. acridum, M. robertsii has acquired many<br />
additional genes for these and other functions that<br />
may facilitate its ability to adapt to heterogenous environments such as plant root surfaces and multiple<br />
insect hosts. Unlike M. acridum, M. robertsii has lost the repeat-induced point mutation genomic defense<br />
system and this loss may have facilitated lineage specific gene duplications and increased niche<br />
adaptability. RNA-seq transcriptional analysis of both fungi during early infection processes provided<br />
further insights into the genes and pathways involved in infectivity and specificity. Of particular note, M.<br />
acridum but not M. robertsii transcribed different G-protein coupled receptors on host but not non-host<br />
cuticles, thus the fine-tuning mechanisms in association with insect host species (PLoS Genetics, 2011).<br />
Further genome study of the model species of C. militaris<br />
found that different species in the Cordyceps/Metarhizium<br />
genera have evolved into insect pathogens independently of<br />
each other. The lineage leading to Cordyceps spp. diverged<br />
130 million year before Metarhizium. However, their<br />
similar gene family expansions suggest a convergent<br />
evolution. Consistent with its long track record of safe<br />
usage as a medicine, the Cordyceps genome does not<br />
contain genes for known human mycotoxins. C. militaris is<br />
sexually heterothallic but, very unusually, fruiting can occur<br />
without an opposite mating-type partner. High throughput<br />
transcriptional profiling indicated that the fruiting of C.<br />
militaris involved induction of MAPK pathway and the<br />
PKA pathway is not activated. As well as providing fundamental new information on the evolution of<br />
insect pathogens, their studies will facilitate the identification of genes involved in fungal virulence,<br />
development, sexuality and the biosynthesis of secondary metabolites (Genome Biology, 2011).<br />
Insect Development and Evolutionary Biology<br />
Animal cells require extrinsic cues for growth, proliferation and survival. The propagation of Drosophila<br />
imaginal disc cells in vitro, for example, requires the<br />
supplementation of fly extract, the composition of which<br />
remains largely undefined. Prof. Sheng Li’s group reported the<br />
biochemical purification of iron-loaded ferritin as an active<br />
ingredient of fly extract that is required for promoting the<br />
growth of Cl8 imaginal disc cells. They concluded that<br />
iron-loaded ferritin is an essential mitogen for cell proliferation<br />
and postembryonic development in Drosophila through<br />
maintaining iron homeostasis and antagonizing starvation<br />
response (Cell Research, 2010).<br />
Sericulture has been greatly advanced by applying hybrid breeding techniques to the domesticated<br />
silkworm, Bombyx mori, but has reached a plateau during the last decades. For the first time, they report<br />
improved silk yield in a GAL4/UAS transgenic silkworm. Overexpression of the Ras1 CA oncogene<br />
specifically in the posterior silk gland improved fibroin production and silk yield 60%, while increasing<br />
food consumption only 20%. Ras activation by Ras1 CA overexpression in the posterior silk gland enhanced<br />
phosphorylation levels of Ras downstream effector proteins, up-regulated fibroin mRNA levels, increased<br />
total DNA content, and stimulated endoreplication. Moreover, Ras1 activation increased cell and nuclei<br />
sizes, enriched subcellular organelles related to protein synthesis, and stimulated ribosome biogenesis for<br />
mRNA translation (Cell Research, 2011).<br />
Insects exhibit the richest diversity of all animals, and the rapid evolution of their phenotypic patterns<br />
suggests strong selective forces that promote and maintain variation. The pigmentation of insects has<br />
served as an excellent model for the study of morphological trait evolution and developmental biology.<br />
The melanism (mln) mutant of the silkworm Bombyx mori is notable for its strong black coloration,<br />
phenotypic differences between larval and adult stages, and its widespread use in strain selection. Prof.<br />
YongPing Huang’s group reported the genetic and molecular bases for the formation of the mln<br />
morphological trait. Fine mapping revealed that an arylalkylamine N-acetyltransferase (AANAT) gene<br />
co-segregates with the black coloration patterns.<br />
Coding sequence variations and expression<br />
profiles of AANAT are also associated with the<br />
melanic phenotypes. An enzymatic assay<br />
demonstrated the absolute loss of AANAT<br />
activity in the mutant proteins. They also<br />
performed RNA interference of AANAT in<br />
wild-type pupae and observed a significant<br />
proportion of adults with ectopic black coloration.<br />
AANAT is also involved in a parallel melanin<br />
synthesis pathway in which ebony plays a role,<br />
whereas no pigmentation defect has been<br />
reported in the Drosophila model or in other<br />
insects to date. The mln mutation might be the first characterized mutant phenotype of insects with<br />
AANAT, and this result contributes to our understanding of dopamine metabolism and melanin pattern<br />
polymorphisms (Development, 2010).<br />
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2010-2011 Progress SIPPE <strong>REPORT</strong><br />
Systems and and Synthetic Biology of Microbial Metabolism<br />
Delineatig microbial metabolic network and regulatory mechnisms based on functional genomic and<br />
comparative genomic techniques has been an important theme of Laboratory of Synthetic Biology<br />
(LSynB). Recently great progress has been made by Prof. GuoPing Zhao’s group in deciphering the global<br />
regulatory role of post-translational modification in microbial metabolism.<br />
Lysine acetylation regulates many eukaryotic cellular processes, but its function in prokaryotes is largely<br />
unknown. Aiming to answer whether acetylation is a conserved universal modification of metabolic<br />
enzymes, the groups from Prof. Zhao and Prof. Chen Yang demonstrated that central metabolism enzymes<br />
in Salmonella were acetylated extensively and differentially in response to different carbon sources,<br />
concomitantly with changes in cell growth and metabolic fluxes, by integrating the MS and 13 C-based<br />
metabolic flux analysis techniques. They found almost 200 acetylated proteins in S. enterica., almost every<br />
intermediary metabolic enzyme was acetylated. For example, the relative activities of key enzymes<br />
controlling the direction of glycolysis versus gluconeogenesis and the branching between citrate cycle and<br />
glyoxylate bypass were all regulated by acetylation. This modulation is mainly controlled by a pair of<br />
protein acetyltransferase (Pat) and NAD + -dependent deacetylase (CobB), whose expressions are<br />
coordinated with growth status. Reversible acetylation of metabolic enzymes ensures that cells respond<br />
environmental changes via promptly sensing cellular energy status and flexibly altering reaction rates or<br />
directions. The identification of extensively acetylated metabolic enzymes in both prokaryotes and human<br />
indicate that reversible lysine acetylation may represent an evolutionarily conserved mechanism of<br />
metabolic regulation in both eukaryotes and prokaryotes. (Science, 2010)<br />
In addition, Prof. Zhao’s group has sequenced the whole genome of Amycolatopsis mediterranei, an<br />
industrial microorganism for rifamycin production, and delineated the metabolic network related to the<br />
secondary antibiotic synthesis. Prof. WeiHong Jiang’s group has elucidated the molecular mechanism of a<br />
two-component regulatory system involved in antibiotic biosynthesis in Streptomyces coelicolor. Prof.<br />
Yang’s group combined a comparative genomic reconstruction of arabinose utilization regulons in nine<br />
Clostridium species with the detailed experimental characterization of arabinose pathways and regulatory<br />
mechanisms in Clostridium acetobutylicum.<br />
Industrial Microbial Industrial Biotechnology Biotechnology Research<br />
Clostridium acetobutylicum is an important industrial butanol-producing bacterium. Genetic modification<br />
of C. acetobutylicum, through metabolic engineering and synthetic biology method, for efficient butanol<br />
production from hydrolysates of different lignocellulosic materials (e.g. corn stover) and higher butanol<br />
selectivity has attracted increasing interests. The bio-butanol research group performed a series of research<br />
around these two aspects with a focus on: studying genetic, physiological and biochemical characteristics<br />
of C. acetobutylicum, developing new genetic tools, constructing engineered C. acetobutylicum strains<br />
with improved performance.<br />
C. acetobutylicum EA 2018 is a patent strain (patent number CN 1143677A) with high butanol-producing<br />
ability, which was previously obtained through butanol resistance screening by the bio-butanol research<br />
group. This Clostridium strain exhibits improved fermentative performance than the C. acetobutylicum<br />
model strain ATCC 824, such as higher butanol ratio, non-sporulation and enhancement of xylose<br />
utilization. Through cooperation with Chinese National Human Genome Center, the bio-butanol research<br />
group performed intensive molecular-level studies on this strain by using genome sequencing, comparative<br />
genomic and transcriptomic analysis, thus discovering and confirming molecular mechanisms underlying<br />
EA2018’s excellent characteristics.<br />
C. acetobutylicum normally produces, besides 60%-70% butanol, 20%-30% acetone and 10% ethanol as<br />
low-value byproducts among the fermentation products.<br />
Reconstruction and optimization of butanol-synthetic<br />
pathway in C. acetobutylicum is expected to decrease<br />
acetone and ethanol formation, and simultaneously, enhance<br />
butanol ratio without impacting solvents yield, thus<br />
increasing economical viability for bio-butanol production.<br />
The bio-butanol research group blocked the acetone<br />
formation by knockout of acetoacetate decarboxylase gene,<br />
which located in acetone-synthetic pathway, and then, by the<br />
following chemical mutagenesis, screening and fermentation<br />
conditions optimization, further increased the butanol ratio to<br />
over 85% among the total solvent products.<br />
Lignocellulose is the most abundant renewable resource in nature. However, C. acetobutylicum is not able<br />
to efficiently co-utilize mixed sugars in lignocellulosic hydrolysates because of the catabolite repression<br />
glucose exerts on pentose (xylose and arabinose)<br />
metabolism. The bio-butanol research group discovered<br />
Promoter 1<br />
Gene1<br />
gene2<br />
and identified genes responsible for key enzymes,<br />
gene3<br />
Promoter 2<br />
gene4<br />
xylose transporters and regulators involved in xylose<br />
gene5<br />
Titer (g/L)<br />
gene6<br />
Xylose pathway genes<br />
Butanol<br />
pathway through comparative transcriptomic analysis<br />
Xylose<br />
overexpression<br />
Arabinose Clostridium<br />
Acetone<br />
and genetic and biochemical analysis. On this basis,<br />
Ethanol<br />
they attenuated glucose phosphoenolpyruvate<br />
Glucose<br />
Time<br />
X<br />
dependent phosphotransferase system (PTS),<br />
confirmed and eliminated xylose pathway bottlenecks,<br />
X<br />
and gained Clostridium strains capable of efficiently<br />
Glucose PTS attenuation<br />
co-fermenting the mixture of glucose, xylose and<br />
arabinose, thus overcoming a technical bottleneck in<br />
the lignocellulose based butanol production.<br />
22<br />
23
2010-2011 Progress SIPPE <strong>REPORT</strong><br />
植 物 生 理 生 态 研 究 所 年 报<br />
Project Name Description Director<br />
Mechanisms of Plant Immunity and Practice of Molecular Design<br />
for Crop Disease Resistance /2011CB100700<br />
Molecular Regulatory Mechanisms of Endosperm Development<br />
and Accumulation of Storage Substances in Higher Plants<br />
/2012CB944800<br />
Artificial Biology Devices with Special Functions: Designing,<br />
Construction and Assembly /2012CB721100<br />
The System and Synthetic Biology Research of Microbial<br />
Metabolism/31121001<br />
G-protein Signaling in Plants / 30925005<br />
Projects<br />
There has been a steady increase in our research grants from both national and CAS programs.The funds of<br />
annual new scientific contracts reached RMB 100 million. Among the new scienfic programs, 64 were funded by<br />
the National Nature Science Foundation of China (NSFC), 3 programs and 13 sub-projects by the National Basic<br />
Reasearch Program, 8 by scientifc & technological programs of Shanghai. SIPPE also obstained 8 Innovation<br />
Direction Programs and 2 Province-Institutes Cooperation Programs from CAS, got 9 Competent Young Talents<br />
Program and a Chief Scientist Program from SIBS. The capacity of SIPPE on organization and commitment of<br />
importment national research tasks has been continually strengthened.<br />
973 Project ZuHua He<br />
973 Project HongWei Xue<br />
973 Project GuoPing Zhao<br />
Foundation for Creative<br />
Research Groups of NSFC<br />
Distinguished Young<br />
Investigator Foundation<br />
Distinguished Young<br />
Investigator Foundation<br />
GuoPing Zhao<br />
JiRong Huang<br />
Mechanisms of Insects Abnormal Development by the Coregulation<br />
of Juvenile Hormone and Molting Hormone<br />
ShengLi<br />
Silkworm as the Model for Researching Target Genes of<br />
YongPing<br />
Key project of NSFC<br />
Lepidopteran Pest Management /31030060<br />
Huang<br />
Mechanism of Fast-growing Fiber Ttimber Cultivating /31130012 Key project of NSFC LaiGengLi<br />
Mechanism of Rice Hybird Reproductive Isolation /31130071 Key project of NSFC HongXuan Lin<br />
Studies on the Function of Phosphatidylinositol(PI) Signaling Pathway in<br />
Regulation of Plant Growth and Development /31130060<br />
Key project of NSFC<br />
2010-2011 SIPPE Report<br />
HongWei Xue<br />
Research Team Construction<br />
As usual, SIPPE pays a great attention to recruit the outstanding scientists. SIPPE takes a series of<br />
measures As usual, SIPPE to ensure pays the a great success attention of talents to recruit recruitment the outstanding subsequent scientists. SIPPE training. takes By a providing series of<br />
comprehensive measures to ensure facilities, the success the Institute of talents tries recruitment to ensure the and new subsequent PI focusing training. on their By providing own research comprehensive works. The<br />
Institute facilities, maintains SIPPE tries its to suitable ensure the systems new PIs and focusing culture on atmosphere their own to research inspire works. their SIPPE innovative maintains research its<br />
enthusiasms.<br />
suitable systems and culture atmosphere to inspire their innovative research enthusiasms.<br />
In the past two years, 125 staff including 7 principle investigators joined SIPPE. Of these, the remarkable<br />
achievements included that one PI won the national “Top One-Thousand-Talents Program” award and one<br />
for the “One-Thousand-Young-Talents Program” fund. In addition, one was elected as the member of<br />
Academy of Sciences of Developing Countries, one won the HLHL prize, two won the “National<br />
Outstanding Young Investigator Fund”, etc.<br />
Academician Prof. Guo-Ping Prof. Guo-Ping Zhao was Zhao elected was the Elected Member as of Academy the Member of Sciences of<br />
Academy of Sciences of Developing of Developing Countries Countries<br />
Dr. Guo-Ping Zhao was elected as the Member of Chinese Academy of Sciences (CAS) in<br />
2005 and the Member of the Academy of Sciences of Developing Countries (TWAS) in<br />
2011. He is the chairmen of academic committee in SIPPE, the Director of the Key<br />
Laboratory of Synthetic Biology, the chief scientists of MOST’s 973 program and the<br />
NSFC innovative research team. His lab is engaged in exploring the metabolism and<br />
physiological regulation of microbes, establishing the research system of synthetic biology<br />
by the combination of genomics, molecular genetics, proteomics and protein structural<br />
biology. More than 200 papers have been published by Prof. Zhao in the leading scientific journals<br />
including Nature, Science, PNAS, Genome Res, J Biol Chem, J Bacteriol, etc. He was also awarded the<br />
second prize of National Natural Science, the second prize of National Science and Technology Progress,<br />
HLHL award in Science and Technology and the first prize of Shanghai Natural Science.<br />
Academician Prof. Hong-Xuan Lin Won the HLHL Award<br />
Academician Prof. Hong-Xuan Lin Won the HLHL Award<br />
Dr. Hong-Xuan Lin joined SIPPE as a principle investigator in March, 2001. Eight years<br />
later, he was elected as the Member of Chinese Academy of Sciences in 2009. His group is<br />
studying the molecular mechanism of important and complicated agronomic traits and has<br />
made big progresses in the genetic mechanisms of rice yielding and abiotic stress, including<br />
salt resistance and drought tolerance. His lab cloned and functionally studied several key<br />
genes that regulate abiotic stress and yielding in rice. The discoveries made by Prof. Lin<br />
contribute to our understanding of molecular mechanisms of agronomic traits. Meanwhile,<br />
the important genes he found with independent intellectual properties were licensed for use for the crop<br />
molecular breeding.<br />
Distribution of New Grants (2010-2011)<br />
24<br />
2010-2011 New Contracted Funding Structure<br />
25
2010-2011 Progress SIPPE <strong>REPORT</strong><br />
Promote the Construction of “Shanghai Center for Plant Stress<br />
Promote the Construction of Biology, “Shanghai CAS” Center for Plant Stress Biology,<br />
CAS”<br />
Outstanding Young Investigator from NSFC<br />
Following the scientific and technological development strategy, SIPPE<br />
explores the new mechanism for recruiting talented people. In 2010, Dr.<br />
Hong-Wei Xue, the director of SIPPE, and Dr. Xiao-Ya Chen, the director of<br />
SIBS wrote the letter together to sincerely invite Dr. Jian-Kang Zhu to return<br />
home from abroad to conduct research work in Shanghai. SIPPE and SIBS<br />
worked together to help Prof. Zhu successfully applied and won the support of<br />
“the One-Thousand-Outstanding-Talents Program”. In 2011, Prof. Jian-Kang<br />
Zhu started to set up the laboratory of plant stress biology at SIPPE. SIPPE will<br />
continue to help the construction of “Shanghai Center for Plant Stress Biology” in the future.<br />
Professor Jian-Kang Zhu received his Ph. D in plant physiology from the Purdue University in 1993 and<br />
became a professor in the Department of Plant Biology, University of Arizona in 2000. He has previously<br />
worked as the Director of the Institute for Integrative Genome Biology at University of California,<br />
Riverside, the Director of the Plant Stress Genomic and Technology Research Center, the Professor of<br />
Molecular Biology and Plant Physiology at KAUST, and the Jane S. Johnson Professor of Plant Biology at<br />
UC Riverside. From 2010 he serves as the distinguished professor in the Department of Horticulture and<br />
Landscape, Purdue University. He focuses on the research of abiotic stress biology, and has made<br />
tremendous contribution in the field of plant tolerance against salt, drought and cold. He has published<br />
more than 200 articles in top journals including Cell, Nature, Science, etc. , and has been recognized as<br />
the most cited plant scientist in the United States. In 2002, Professor JianKang Zhu was recognized as the<br />
Researcher of the Year in the College of Agriculture and Life Sciences at the University of Arizona and<br />
received the Charles Albert Shull Award from the American Society of Plant Biologists. In 2010, he was<br />
elected as the member of National Academy of Science (NAS) in USA. He is the third NAS member who<br />
finished his bachelor study in China mainland.<br />
Professor Ji-Rong Huang (2010)<br />
G-protein Signaling and<br />
Chloroplast Development<br />
One-Thousand-Young-Tanlents supported by the Central<br />
Organisation Department<br />
Professor Jia-Wei Wang (2011)<br />
Plant Small Regulatory RNAs<br />
One-Hundred-Talents supported by the Chinese Academy of Science<br />
Professor Han Xiao (2010)<br />
Fruit Developmental Biology<br />
Professor Yu-Da Fang (2010)<br />
Cell Biology of Plant<br />
Genome and Epigenome<br />
Professor Sheng Li (2010)<br />
Insect Development and<br />
Metamorphosis<br />
Professor Er-Jun Ling (2010)<br />
Insect Innate Immunology<br />
and Pest Control<br />
Professor Xuan Li (2010)<br />
Bioinformatics Research<br />
Professor Yong-Fei Wang (2011)<br />
Ion Channel and Signal<br />
Transduction in Plant Cells<br />
Professor Yang Zhao (2011)<br />
Chemical Genetics<br />
26<br />
27
2010-2011 Progress<br />
SIPPE <strong>REPORT</strong><br />
Cooperation and Extension<br />
SIPPE stays active in the international academic exchanges in 2010 and 2011, co-organized "The 2nd<br />
International Conference on Plant Metabolism" and other five influential international conferences. There<br />
were 169 overseas visits of our scientists and staff and 70 incoming visits of foreign scientists to our institute,<br />
including Dr. Dale Sanders, the<br />
director of John Innes Centre and the<br />
senior editor of Nature, Dr. Magdalena<br />
Skipper. The institute obtained two<br />
projects co-funded by the national<br />
natural science foundation (NSFC)<br />
and Dutch Organization for Scientific<br />
Research (NWO).<br />
APPENDIX<br />
The Huzhou biotechnology center, SIBS, constantly increased investment on equipments and had the productive<br />
capacity from test tubes to 2 tons fermentation tanks, those equipments could satisfy not only industrial technology<br />
research and development but also commercial production demand. In 2011, the center signed 7 new technology<br />
contracts, amount to RMB 4.3 million and put two new projects into operation. The Huzhou modern agricultural<br />
biotechnology innovation center, SIBS, signed 9 technology development contracts with Coca-Cola beverage (Shanghai)<br />
Co., Ltd., and involved in 8 projects from national and provincial sources. At present, these projects are progressing well.<br />
It is expected that after the transformation in 2012-2013, these projects would bring RMB 40 million for enterprise. The<br />
joint research centre of Zhejiang Academy of Agricultural Science and SIPPE was established in 2007, this centre made<br />
significant achievements in 2011 after several years’ collaboration. Both parties co-applied for the the National Plant<br />
Transgenic Program and also are applying for a prize of national Science from Shanghai.<br />
Through deepening cooperation with enterprise, the institute dramatically promotes transformation of the<br />
scientific research achievements. The project "Genetic Engineering and Industrialization Demonstration of<br />
Butanol Production Strains" cooperated with Songyuan Laihe chemicals Co., Ltd was supported by CAS-<br />
JiLin province foundation, and would achieve new production value RMB 80 million after the industrialization<br />
in 2012. The cooperation with ChangChun DaCheng fermentation technology development Co., Ltd, would<br />
increase the production of lysine to about 5000 tons, and bring direct economic benefits of RMB 75 million.<br />
The new sweet potato varieties "ThaiZhong No.9”, collaborated with the Institute of TaiAn Agricultural science<br />
research, was approved by Crop<br />
Variety Authorization Committee of<br />
Shandong Province (No. 2010041)<br />
and produced economic benefits of<br />
RMB 56.3 million.<br />
28<br />
29
Appendix<br />
SIPPE <strong>REPORT</strong><br />
研 究 所 介 绍<br />
Publication<br />
Publication<br />
2010-2011 SIPPE Report<br />
1. Aileni M, Abbagani S, Zhang P*. (2011). Highly efficient production of transgenic Scoparia dulcis L. mediated by<br />
Agrobacterium tumefaciens: plant regeneration via shoot organogenesis. Plant Biotechnol Rep 5: 147-156.<br />
2. Bi HP, Aileni M, Zhang P*. (2010). Evaluation of cassava varieties for cassava mosaic disease resistance jointly by<br />
agro-inoculation screening and molecular markers. Afr J Plant Sci 4: 330-338.<br />
3. Bu Y, Yin WY*. (2010). The Protura from Liupan Mountain, northwest China. Acta Zootaxonomica Sinica 35:<br />
278-286.<br />
4. Bu Y, Yin WY*. (2010). Two new species of the genus Kenyentulus Tuxen, 1981 from Shaanxi Province, Northwest<br />
China (Protura: Berberentulidae). Acta Zoologica Cracoviensia 53B: 65-71.<br />
5. Chen AM, Wang YB, Sun J, Yu AY, Luo L, Yu GQ, Zhu JB, Wang YZ*. (2010). Identification of a TRAP transporter<br />
for malonate transport and its expression regulated by GtrA from Sinorhizobium meliloti. Res Microbiol 161: 556-564.<br />
6. Chen F, Gao MJ, Miao YS, Yuan YX, Wang MY, Li Q, Mao BZ, Jiang LW, He ZH*. (2010). Plasma membrane<br />
localization and potential endocytosis of constitutively expressed XA21 proteins in transgenic rice. Mol Plant 3:<br />
917-926.<br />
7. Chen FF, Lin L, Wang L, Tan Y, Zhou HX, Wang YG, Wang Y* and WQ He*. (2011). Distribution and diversity of<br />
glycosylated natural product genes in marine bacteria genomes. Appl Microbiol Biotechnol. 90: 1347-1359.<br />
8. Chen HY, Ying L, Jin J, Li Q, Cai WM*. (2010). Determining the transcriptional regulation pattern of PgTIP1 in<br />
transgenic Arabidopsis thaliana by constructing gene coexpression networks. Adv Bio Biotech 1: 384-390.<br />
9. Chen J, Wang P, Mi HL, Chen GY*, Xu DQ. (2010). Reversible association of ribulose-1, 5-bisphosphate<br />
carboxylase/oxygenase activase with the thylakoid membrane depends upon the ATP level and pH in rice without heat<br />
stress. J Exp Bot 61: 2930-2950.<br />
10. Chen WH and Qin ZJ*. (2011). Development of a gene cloning system in a fast-growing and moderately thermophilic<br />
Streptomyces species and heterologous expression of Streptomyces antibiotic biosynthetic gene clusters. BMC Microbiol.<br />
11: 243.<br />
11. Cheng YX, Zhou WB, El Sheery NI, Peters C, Li MY, Wang XM, Huang JR*. (2011). Characterization of the<br />
Arabidopsis glycerophosphodiester phosphodiesterase (GDPD) family reveals a role of the plastid-localized AtGDPD1<br />
in maintaining cellular phosphate homeostasis under phosphate starvation. Plant J 66: 781-795.<br />
12. Dai C, Xue HW*. (2010). Rice EARLY FLOWERING1, a CKI, phosphorylates DELLA protein SLR1 to negatively<br />
regulate GA signaling. EMBO J 29: 1916-1927.<br />
13. Dallai R, Mercati D, Bu Y, Yin WY*. (2010). Spermatogenesis and sperm structure of Acerella muscorum, (Ionescu,<br />
1930) (Hexapoda, Protura). Tissue and Cell 42: 97-104.<br />
14. Fang X, Yang CQ, Wei YK, Ma QX, Yang L, Chen XY*. (2011). Genomics grand for diversified plant secondary<br />
metabolites. Plant Diversity and Resources 33: 53-64.<br />
15. Fang YD, Spector DL. (2010). “Live Cell Imaging of Plants,” in Live Cell Imaging: A Laboratory Manual, 2th ed.,<br />
Robert D. Goldman, Jason R. Swedlow, David L. Spector, Eds. New York: Cold Spring Harbor Laboratory Press<br />
pp.371-386.<br />
16. Fu FF, Xue HW*. (2010). Co-expression Analysis Identifies Rice Starch Regulator1 (RSR1), a rice AP2/EREBP family<br />
transcription factor, as a novel rice starch biosynthesis regulator. Plant Physiol 154: 927-938.<br />
17. Gao LL, Xue HW*. (2011). Global analysis of expression profiles of rice receptor-like kinase genes. Mol Plant<br />
doi:10.1093/mp/ssr062.<br />
18. Gao Q, Jin K, Ying SH, Zhang Y, Xiao G, Shang Y, Duan Z, Hu X, Xie XQ, Zhou G, Peng G, Luo Z, Huang W, Wang<br />
B, Fang W, Wang S, Zhong Y, Ma LJ, St Leger RJ, Zhao GP, Pei Y, Feng MG, Xia Y, Wang C*. (2011).Genome<br />
sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M.<br />
acridum. PLoS Genet. 7: e1001264.<br />
19. Geng AL, He YL, Qian CL, Yan X, Zhou ZH*. (2010). Effect of key factors on hydrogen production from cellulose in a<br />
co-culture of Clostridium thermocellum and C. thermopalmarium. Bioresource Technol 101: 4029-4033.<br />
20. Gruntenko NЕ, Wen D, Karpova EK, Adonyeva NV, Liu Y, He Q, Faddeeva NV, Fomin AS, Li S*, Rauschenbach IY.<br />
(2010). Altered juvenile hormone metabolism, reproduction and stress resistance in Drosophila adults with genetic<br />
ablation of the corpus allatum cells. Insect Biochem Mol Biol 40: 891-897.<br />
21. Gu XL, Wang H, Huang H, Cui XF*. (2011). SPT6L encoding a putative WG/GW-repeat protein regulates apical-basal<br />
polarity of embryo in Arabidopsis. Mol Plant doi:10.1093/mp/ssr073.<br />
22. Gu Y, Ding Y, Ren C, Sun Z, Dmitry AR, Zhang WW, Yang S, Yang C*, Jiang WH*. (2010). Reconstruction of<br />
xylose utilization pathway and regulons in Firmicutes. BMC Genomics 11: 255-268.<br />
植 物 生 理 生 态 研 究 所 年 报<br />
2010-2011 SIPPE Report<br />
23. Gui JS, Shen JH, Li LG*. (2011). Functional characterization of evolutionarily divergent 4-coumarate: CoA ligases in<br />
rice. Plant Physiol 157: 574-586.<br />
24. Hao P, Zheng HJ, Yu Y, Ding GH, Gu WY, Chen ST, Yu ZH, Ren SX, Oda M, Konno T, Wang SY, Li X*, Ji ZS* and<br />
Zhao GP*. (2011). Complete Sequencing and Pan-Genomic Analysis of Lactobacillus delbrueckii subsp. bulgaricus<br />
Reveal Its Genetic Basis for Industrial Yogurt Production. PLoS ONE. 6(1): e15964.<br />
25. Hao W, Lin HX*. (2010). Toward understanding genetic mechanisms of complex traits in rice. J Genet Genomics 37:<br />
1-14.<br />
26. He ZQ, Li K, Fang Y, Liu XW*. (2010). A taxonomic study of the genus Amusurgus Brunner von Wattenwyl from<br />
China (Orthoptera, Gryllidae, Trigonidiinae). Zootaxa 2423: 55-62.<br />
27. Horvath B, Peralta P, Peszlen I, Divos F, Kasal B, Li L*. (2010). Elastic modulus of transgenic aspen. Wood Research<br />
55: 1-10.<br />
28. Horvath B, Peszlen I, Peralta P, Horvath L, Kasal B, Li L*. (2010). Elastic modulus determination of transgenic aspen<br />
trees using a dynamic mechanical analyzer in static bending mode. Forest Products J 60: 296-300.<br />
29. Horvath B, Peszlen I, Peralta P, Kasal B, Li L*. (2010). Effect of lignin genetic modification on wood anatomy of aspen<br />
trees. IAWA J 31: 29-38.<br />
30. Hou S, Li LG*. (2011). Rapid characterization of woody biomass digestibility and chemical composition using<br />
near-infrared spectroscopy. J Integr Plant Biol 53: 166-175.<br />
31. Hu SY, Chen J, Yang ZY, Shao LJ, Bai H, Luo JL, Jiang WH, Yang YL*. (2010). Coupled bioconversion for<br />
preparation of N-acetyl-Dneuraminic acid using immobilized N-acetyl-D-glucosamine-2-epimerase and<br />
N-acetyl-Dneuraminic acid lyase. Appl Microbio Biotechnol 85: 1383-1391.<br />
32. Hu SY, Zheng HJ, Gu Y, Zhao JB, Zhang WW, Yang YL, Wang SY, Zhao GP, Yang S*, Jiang WH*. (2011).<br />
Comparative genomic and transcriptomic analysis revealed genetic characteristics related to solvent formation and<br />
xylose utilization in Clostridium acetobutylicum EA 2018. BMC Genomics 12: 93.<br />
33. Huang CW, Potapov M, Gao Y*. (2010). Taxonomy of the Proisotoma complex. III. A revision of the genus Narynia<br />
(Collembola: Isotomidae) with a description of a new species from China. Zootaxa 2410: 45-52.<br />
34. Huang W, Bi T, Sun W*. (2010). Comparative analysis of panicle proteomes of two upland rice varieties upon<br />
hyper-osmotic stress. Front Biol 5: 546-555.<br />
35. Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T, Zhang Z, Li M, Fan D, Guo Y, Wang A, Wang<br />
L, Deng L, Li W, Lu Y, Weng Q, Liu K, Huang T, Zhou T, Jing Y, Li W, Lin Z, Buckler ES, Qian Q, Zhang Q, Li J,<br />
Han B*. (2010). Genome-wide association studies of 14 agronomic traits in rice landraces. Nature Genet 42: 961-967.<br />
36. Huang X, Zhao Y, Wei X, Li C, Wang A, Zhao Q, Li W, Guo Y, Deng L, Zhu C, Fan D, Lu Y, Weng Q, Liu K, Zhou T,<br />
Jing Y, Si L, Dong G, Huang T, Lu T, Feng Q, Qian Q, Li J, Han B*. (2011). Genome-wide association study of<br />
flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 44:32-39.<br />
37. Huang Y, Zong WM, Yang X, Wang RF, Hemme CL, Zhou JZ, Zhou ZH*. (2010) Succession of the bacterial<br />
community and dynamics of hydrogen producers in a hydrogen-producing bioreactor. Appl Environ Microbiol 76:<br />
3387-3390.<br />
38. Huang, J., Tian, L., Abdou, M., Wen, D., Wang, Y., Li, S.*, Wang, J. (2011). DPP-mediated TGF-β signaling regulates<br />
juvenile hormone biosynthesis by upregulating expression of JH acid methyltransferase. Development. 138:2283-91.<br />
39. Hwang JU, Wu G, Yan A, Lee YJ, Grierson CS, Yang ZB*. (2010). Pollen-tube tip growth requires a balance of lateral<br />
propagation and global inhibition of Rho-family GTPase activity. J Cell Sci 123: 340-350.<br />
40. Khalid KA, Teixeira da Silva JA, Cai WM*. (2010). Water deficit and polyethylene glycol 6000 affects morphological<br />
and biochemical characters of Pelargonium odoratissimum (L.). Scientia Horticulturae 125: 159-166.<br />
41. Li J, Zhao LJ, Zhao M, Yang YL, Zhang WW, Yang S*. (2010). Screening and characterization of butanol tolerant<br />
microorganisms. Lett Appl Microbiol 50: 373-379.<br />
42. Li JY, Gong JM*. (2010). Nitrate signal sensing and transduction in higher plants. J Plant Physiol 47: 111-118.<br />
43. Li JY, Fu YL, Pike SM, Bao J, Tian W, Zhang Y, Chen CZ, Zhang Y, Li HM, Huang J, Li LG, Schroeder JI, Gassmann<br />
W, Gong JM*. (2010). The Arabidopsis nitrate transporter NRT1.8 functions in nitrate removal from the xylem sap and<br />
mediates cadmium tolerance. Plant Cell 22: 1633-1646.<br />
44. Li K, He ZQ, Liu XW*. (2010). A taxonomic study of the genus Metiochodes Chopard from China (Orthoptera,<br />
Gryllidae, Trigonidiinae). Zootaxa 2506: 43-50.<br />
45. Li K, He ZQ, Liu XW*. (2010). Four new species of Nemobiinae from China (Orthoptera, Gryllidae, Nemobiinae).<br />
Zootaxa 2540: 59-64.<br />
46. Li L, Shi ZY, Li L, Shen GZ, Wang XQ, An LS, Zhang JL*. (2010). Over-expression of ACL1 (abaxially curled leaf)<br />
increased bulliform cells and induced abaxial curling of leaf blade in rice. Mol Plant 3: 807-817.<br />
47. Li P, Julia JW, Shi XL, Zhang HL, Johannes H, Sjef CS, and Teng S*. (2011). Fructose sensitivity is suppressed in<br />
Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain. Proc Natl Acad Sci U S A.<br />
108:3436-41.<br />
30<br />
1<br />
2<br />
31
Appendix<br />
SIPPE <strong>REPORT</strong><br />
研 究 所 介 绍<br />
2010-2011 SIPPE Report<br />
植 物 生 理 生 态 研 究 所 年 报<br />
2010-2011 SIPPE Report<br />
48. Li S*. (2010). Identification of iron-loaded ferritin as an essential mitogen for cell proliferation and postembryonic<br />
development in Drosophila. Cell Res. 20: 1148-1157.<br />
49. Li TX, Zhang Y, Liu H, Wu YT, Zhang HX*. (2010). Stable expression of Arabidopsis vacuolar Na + /H + antiporter gene<br />
AtNHX1, and its salt tolerance in the transgenic soybean for over six generations. Chinese Sci Bull 55: 1127-1134.<br />
50. Li W, Zhong SH, Li GJ, Li Q, Mao BZ, Deng YW, Zhang HJ, Zeng LJ, Song FM, He ZH*. (2011). Rice RING protein<br />
OsBBI1 with E3 ligase activity confers broad-spectrum resistance against Magnaporthe oryzae by modifying the cell<br />
wall defence. Cell Res 21: 835-848.<br />
51. Li XF, Liu T, Wu YQ, Zhao GP, Zhou ZH*. (2010). Derepressive effect of NH 4 + on hydrogen production by deleting<br />
the glnA1 gene in Rhodobacter sphaeroides. Biotechnol and Bioen 106: 564-572.<br />
52. Lin GF, Du H, Chen JG, Lu HC, Guo WC, Golka K, Shen JH*. (2010). Association of XPD/ERCC2 G 23591 A and<br />
A 35931 C polymorphisms with skin lesion prevalence in a multiethnic, arseniasis-hyperendemic village exposed to indoor<br />
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53. Lin GF, Meng H, Du H, Lu HC, Zhou YS, Chen JG, Golka K, Lu JC, Shen JH*. (2010). Factors impacting on the<br />
excess arseniasis prevalence due to indoor combustion of high arsenic coal in a hyperendemic village. Int Arch Occup<br />
Environ Health 83: 433-440.<br />
54. Liu H, Tang RJ, Zhang Y, Wang CT, Lv QD, Gao XS, Li WB, Zhang HX*. (2010). AtNHX3 is a vacuolar K + /H +<br />
antiporter required for low-potassium tolerance in Arabidopsis thaliana. Plant Cell Environ 33: 1989-1999.<br />
55. Liu J, Zheng QJ, Ma QX, Gadidasu KK, Zhang P*. (2011). Cassava genetic transformation and its application in<br />
breeding. J Integr Plant Biol 53: 552-569.<br />
56. Liu Q, Shi LL, Fang YD*. (2011). Dicing Bodies. Plant Physiol doi:10.1104/pp.111.186734.<br />
57. Liu Q, Xu C, Wen CK*. (2010). Genetic and transformation studies reveal negative regulation of ERS1 ethylene<br />
receptor signaling in Arabidopsis. BMC Plant Biol 10: 60-73.<br />
58. Liu T, Li XF, Zhou ZH*. (2010). Improvement of hydrogen yield by hupr gene knock-out and nifa gene overexpression<br />
in Rhodobacter sphaeroides 6016. Int J. Hydrogen Energy. 35: 9603-9610.<br />
59. Liu W, Luo L, Sun J, Cao LP, Yu GQ, Zhu JB, Wang YZ*. (2010). Characterization and expression analysis of<br />
Medicago truncatula ROP GTPase family during the early stage of symbiosis. J Integr Plant Biol 52: 639-652.<br />
60. Liu Y, Zhou S, Ma L, Tian L, Wang S, Sheng Z, Jiang R-J, Bendena WG, Li S*. (2010). Transcriptional regulation of<br />
the insulin signaling pathway genes by starvation and 20-hydroxyecdysone in the Bombyx fat body. J Insect Physiol 56:<br />
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61. Liu ZY, Jia LG, Mao YF, He YK*. (2010). Classification and quantification of leaf curvature. J Exp Bot 61: 2757-2767.<br />
62. Liu ZY, Jia LG, Wang H, He YK*. (2011). HYL1 regulates the balance between adaxial and abaxial identity for leaf<br />
flattening via miRNA-mediated pathways. J Exp Bot 62: 4367-4381.<br />
63. Long YH, Xie L, Liu N, Yan X, Fan MZ, Wang Q*. (2010). Comparison of gut-associated and nest-associated<br />
microbial communities of a fungus-growing termite (Odontotermes yunnanensis). Insect science 17: 265-276.<br />
64. Lu LD, Sun Q, Fan XY, Zhong Y, Yao YF*, Zhao GP*. (2010). Mycobacterial MazG is a novel NTP<br />
pyrophosphohydrolase involved in oxidative stress response. J Biol Chem 285: 28076-28085.<br />
65. Lu T, Lu G, Fan D, Zhu C, Li W, Zhao Q, Feng Q, Zhao Y, Guo Y, Li W, Huang X, Han B*. (2010). Function<br />
annotation of the rice transcriptome at single-nucleotide resolution by RNA-seq. Genome Res 20: 1238-1249.<br />
66. Lu YH, He JM, Zhu H, Yu ZY, Wang R, Chen YL, Dang FJ, Zhang WW, Yang S, and Jiang WH*. (2011). An Orphan<br />
Histidine Kinase, OhkA, Regulates Both Secondary Metabolism and Morphological Differentiation in Streptomyces<br />
coelicolor. J. Bacteriol. 193: 3020-3032.<br />
67. Lu ZQ, Xie PF, Qin ZJ*. (2010). Promotion of markerless deletion of the actinorhodin biosynthetic gene cluster in<br />
Streptomyces coelicolor. Acta Biochimica et Biophysica Sinica 42: 717-721.<br />
68. Ma L, Xu HF, Zhu JQ, Ma SY, Liu Y, Jiang RJ, Xia QY and Li S*. (2011). Ras1 CA overexpression in the posterior silk<br />
gland improves silk yield. Cell Res. 21:934-43.<br />
69. Ma L, Jun Z, Zou G, Wang CS, Zhou ZH*. (2011). Improvement of cellulase activity in Trichoderma reesei by<br />
heterologous expression of a beta-glucosidase gene from Penicillium decumbens. Enzyme Microb. Technol. 49:<br />
366-371.<br />
70. Mao YB, Tao XY, Xue XY, Wang LJ, Chen XY*. (2011). Cotton plants expressing CYP6AE14 double-stranded RNA<br />
show enhanced resistance to bollworms. Transgenic Res 20: 665-673.<br />
71. Mei Y, Jia WJ, Chu YJ, Xue HW*. (2011). Arabidopsis PIPK2 is involved in root gravitropism through regulating auxin<br />
polar transport by affecting the cycling of PIN proteins. Cell Res doi:10.1038/cr.2011.<br />
72. Peng Z, Lu T, Li L, Liu X, Gao Z, Hu T, Yang X, Feng Q, Guan J, Weng Q, Fan D, Zhu C, Lu Y, Han B*, Jiang Z*.<br />
(2010). Genome-wide characterization of the biggest grass, bamboo, based on 10,608 putative full-length cDNA<br />
sequences. BMC Plant Biol 10: 116.<br />
73. Potapov MB, Bu Y, Huang CW, Gao Y, Luan YX*. (2010). Generic switch-over during ontogenesis in<br />
Dimorphacanthella gen. n. (Collembola, Isotomidae) with barcoding evidence. Zookeys 73: 13-23.<br />
74. Qin Y, Yang ZB*. (2011). Rapid tip growth: Insights from pollen tubes. Semin Cell Dev Biol 22: 816-824.<br />
75. Rao XJ*, Ling EJ*, Yu XQ. (2010) The role of lysozyme in the prophenoloxidase activation system of Manduca sexta:<br />
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76. Ren C, Gu Y, Hu SY, Wu Y, Wang P, Yang YL, Yang C, Yang S*, Jiang WH*. (2010). Identification and inactivation<br />
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77. Shangguan XX, Yu N, Wang LJ, Chen XY*. (2010). Recent advances in molecular biology research on cotton fiber<br />
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78. Shi LL, Fang YD*. (2011). Histone variants: making structurally and functionally divergent nucleosomes and linkers in<br />
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79. Shi LL, Wang J, Hong F, Spector DL, Fang YD*. (2011). Four amino acids guide the assembly or disassembly of<br />
Arabidopsis histone H3.3-containing nucleosomes. P Natl Acad Sci USA 108: 10574-10578.<br />
80. Shi QM, Yang X, Song L, Xue HW*. (2011). Arabidopsis MSBP1 is activated by HY5 and HYH and is involved in<br />
photomorphogenesis and brassinosteroid sensitivity regulation. Mol Plant 4: 1092-1104.<br />
81. Song DL, Shen JH, Li L*. (2010) Characterization of cellulose synthase complexes in Populus xylem differentiation.<br />
New Phytologist 187: 777-790.<br />
82. Song DL, Xi W, Shen JH, Bi T, Li LG*. (2011). Characterization of the plasma membrane proteins and receptor-like<br />
kinases associated with secondary vascular differentiation in poplar. Plant Mol Biol 76: 97-115.<br />
83. Sun CB, Du XM, He YK*. (2010). A novel method for constructing pathogen-regulated small RNA cDNA library.<br />
Biochem Bioph Res Co 397: 532-536.<br />
84. Sun Q, Xiao W, Xin D, Shi JP, Yan X, Zhou ZH*. (2010). Statistical optimization of process parameters on<br />
biohydrogen production from sucrose by co-culture of Clostridium acidisoli sp. Nov and Rhodobacter sphaeroides. Int J.<br />
Hydrogen Energy. 35: 4076-4084.<br />
85. Tang RJ, Liu H, Bao Y, Lv QD, Yang L, Zhang HX*. (2010). The woody plant poplar has a functionally conserved<br />
salt overly sensitive pathway in response to salinity stress. Plant Mol Biol 74: 367-380.<br />
86. Tang X, Zhang ZY, Zhang WJ, Zhao XM, Li X, Zhang D, Liu QQ, Tang WH*. (2010). Global gene profiling of<br />
laser-captured pollen mother cells indicates molecular pathways and gene subfamilies involved in rice meiosis. Plant<br />
Physiol 154: 1855-1870.<br />
87. Tao YZ, Liu D, Yan X, Zhou ZH, Jeong KL, and Yang C*. (2011). Network identification and flux quantification of<br />
glucose metabolism in Rhodobacter sphaeroides under photoheterotrophic H 2 -producing conditions. J. Bacteriol.<br />
Accepted.<br />
88. Tian L, Guo E, Diao Y, Wang S, Liu S, Cao Y, Jiang R-J, Ling E, Li S*. (2010). Developmental regulation of<br />
glycolysis by 20-hydroxyecdysone and juvenile hormone in fat body tissues of the silkworm, Bombyx mori. J Mol Cell<br />
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89. Tian L, Guo E, Diao Y, Zhou S, Peng Q, Cao Y, Ling E, Li S*. (2010). Genome-wide regulation of innate immunity by<br />
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90. Wang CL, Wang ZX, Ling QZ, Kariuki MM, Kiguchi K, Ling EJ*. (2010). Physiological functions of hemocytes<br />
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91. Wang CT, Liu H, Gao XS, Zhang HX*. (2010). Overexpression of G10H and ORCA3 in the hairy roots of<br />
Catharanthus roseus improves catharanthine production of Catharanthus roseus improves catharanthine production.<br />
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92. Wang ET, Xu X, Zhang L, Zhang H, Lin L, Wang Q, Li Q, Ge S, Lu BR, Wang W, He ZH*. (2010). Duplication and<br />
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93. Wang HH, Wang CT, Liu H, Tang RJ, Zhang HX*. (2011). An efficient Agrobacterium-mediated transformation and<br />
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94. Wang J, Gao XY, Shi XY, Zhang JL, Shi ZY*. (2010). Over expression of ta-siR2141 in rice resulted in adaxialization<br />
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95. Wang J, Wang Y, Luo D*. (2011). LjCYC genes constitute floral dorsoventral asymmetry in Lotus japonicus. J Integr<br />
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96. Wang K, Xiang XH, He F, Lin LB, Zhang R, Ping XJ, Han JS, Guo N, Zhang QH, Cui CL, Zhao GP*. (2010).<br />
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32<br />
3<br />
4<br />
33
Appendix<br />
SIPPE <strong>REPORT</strong><br />
研 究 所 介 绍<br />
2010-2011 SIPPE Report<br />
植 物 生 理 生 态 研 究 所 年 报<br />
2010-2011 SIPPE Report<br />
97. Wang L, Gu XL, Xu DY, Wang W, Wang H, Zeng MH, ZhaoY, Huang H, Cui XF*. (2010). miR396-targeted AtGRF<br />
transcription factors are required for coordination of cell division and differentiation during leaf development in<br />
Arabidopsis. J Exp Bot 62: 761-773.<br />
98. Wang L, Li XR, Lian H, Ni DA, He YK, Chen XY, Ruan YL*. (2010). Evidence that high activity of vacuolar<br />
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99. Wang L, Yu X, Wang H, Lu YZ, de Ruiter M, Prins M, He YK*. (2011). A novel class of heat-responsive small RNAs<br />
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100. Wang QJ, Zhang YK, Yang C, Xiong H, Lin Y, Yao J, Li H, Xie L, Zhao W, Yao YF, Ning ZB, Zeng R, Xiong Y,<br />
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101. Wang S, Liu S, Liu H, Wang J, Zhou S, Liu Y, Jiang R-J, Bendena WG, Li S*. (2010). The insect steroid hormone<br />
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102. Wang W, Xu B, Wang H, Li JQ, Huang H, Xu L*. (2010). YUCCA genes are expressed in response to leaf<br />
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103. Wang Y, Xu J, Shen J, Luo Y, Scheu S, Ke X*. (2010). Tillage, residue burning and crop rotation alter soil fungal<br />
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104. Wang YW, Xu J, Chen AM, Wang YZ, Zhu JB, Yu GQ, Xu L, Luo L*.(2010). GGDEF and EAL proteins play<br />
different roles in the control of Sinorhizobium meliloti growth, motility, exopolysaccharide production, and competitive<br />
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105. Wei JL, Xu M, Zhang DB*, Mi HL*. (2010). The role of carotenoid isomerase in maintenance of photosynthetic<br />
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106. Wei N, Tan C, Qi B, Zhang Y, Xu G, Zheng HQ*. (2010). Changes in gravitational forces induce the modification of<br />
Arabidopsis thaliana silique pedicel positioning. J Exp Bot 61: 3874-3884.<br />
107. Wei WQ, Liu FQ, Liu L, Li ZF, Zhang XY, Jiang F, Shi Q, Zhou XY, Sheng WQ, Cai SJ, Li X*, Xu Y*, Nan P*.<br />
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108. Shao W, Kim HS, Cao Y, Xu YZ*, and Query CC*. (2012). A U1–U2 snRNP interaction network during intron<br />
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109. Weng L, Tian Z, Feng X, Li X, Xu S, Hu X, Luo D*, Yang J*. (2011). Petal development in Lotus japonicus. J Integr<br />
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110. Wu GZ, Xue HW*. (2010). Arabidopsis β-ketoacyl-[acyl carrier protein] synthase I (KASI) is crucial for fatty acid<br />
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111. Wu S, Zhang XF, Chen XM, Cao PS, Ling EJ*. (2010). BmToll9, an Arthropods conservative Toll, is probably<br />
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112. Wu S, Zhang XF, He YQ, Shuai JB, Chen XM, Ling EJ*. (2010) Expression of antimicrobial peptide genes in Bombyx<br />
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113. Wu WJ, Elsheery N, Wei Q, Zhang LG, Huang JR*. (2011). Defective etioplasts observed in variegation mutants may<br />
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114. Wu Y, Zheng F, Ma W, Han Z, Gu Q, Shen Y, Mi HL*. (2011). Regulation of NAD(P)H dehydrogenase-dependent<br />
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115. Xiao H, Gu Y, Ning YY, Yang YL, Wilfrid JM, Yang S*, and Jiang WH*. (2011). Confirmation and Elimination of<br />
Xylose Metabolism Bottlenecks in Glucose Phosphoenolpyruvate-Dependent Phosphotransferase System-Deficient<br />
Clostridium acetobutylicum for Simultaneous Utilization of Glucose, Xylose, and Arabinose. Appl Environ Microbiol.<br />
77: 7886-7895.<br />
116. Xiong CH, Xia YL, Zheng P, Shi SH, Wang CS*. (2010). Developmental stage-specific gene expression profiling for a<br />
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117. Xu DY, Huang WH, Li Y, Wang H, Huang H, Cui XF*. (2011). Elongator complex is critical for cell cycle progression<br />
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118. Xu J, Aileni M, Abbagani S, Zhang P*. (2010). A reliable and efficient method for total RNA isolation from various<br />
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119. Xu J, Zhao Q, Du P, Xu C, Wang B, Feng Q, Liu Q, Tang S, Gu M, Han B*, Liang G*. (2010). Developing high<br />
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120. Xu T, Ping J, Yu Y, Yu FD, Yu YT, Hao P*, Li X*. (2010). Revealing parasite influence in metabolic pathways in<br />
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121. Yan J, Cai XF, Luo JH, Sato S, Jiang QY, Yang J, Cao XL, Hu XH, Tabata S, Gresshoff PM, Luo D*. (2010). The<br />
REDUCED LEAFLET genes encode key components of the trans-acting small interfering rna pathway and regulate<br />
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122. Yang CQ, Lu S, Mao YB, Wang LJ, Chen XY*. (2010). Characterization of two NADPH: Cytochrome P450<br />
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123. Yang J, An D, Zhang P*. (2011). Expression profiling of cassava storage roots reveals an active process of<br />
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124. Yang J, Bi HP, Fan WJ, Zhang M, Wang HX, Zhang P*. (2011). Efficient embryogenic suspension culturing and rapid<br />
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125. Yang JW, Xu J, Chen XY, Zhang YX, Jiang XC, Guo XK, Zhao GP*. (2010). Decrease of plasma platelet-activating<br />
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126. Yang WB, Ren SL, Zhang XM, Gao MJ, Ye SH, Qi YB, Zheng YY, Zeng LJ, Li Q, Huang SJ, He ZH*. (2011).<br />
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127. Yang X, Yang YN, Xue LJ, Zou MJ, Liu JJ, Chen F, Xue HW*. (2011). Rice ABI5-like1 regulates ABA and auxin<br />
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128. Zhong Yi, Chang Xiao, Cao Xingjun, Zhang Yan, Zheng Huajun, Zhu Yongzhang, Cai Chengsong, Cui Zelin, Zhang<br />
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129. Yao HY, Xue HW*. (2011). Invited review: Signals and mechanisms affecting vesicular trafficking during root<br />
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130. Yu N, Cai WJ, Wang SC, Shan CM, Wang LJ, Chen XY*. (2010). Temporal control of trichome distribution by<br />
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131. Yu X, Wang H , Lu YZ, de Ruiter M, Cariaso M, Prins M, van Tunen A, He YK*. (2011). Identification of conserved<br />
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132. Yu Y, Xu T, Yu YT, Hao P*, Li X*. (2010). Association of tissue lineage and gene expression: conservatively and<br />
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133. Yuan ZH, Luo DX, Li G, Yao XZ, Wang H, Zeng MH, Huang H, Cui XF*. (2010). Characterization of the AE7 gene<br />
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134. Wang YB, Zhang H, Li H, Miao XX*. Second-Generation Sequencing Supply an Effective Way to Screen RNAi<br />
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135. Zang AP, Xue XJ, Neill S, Cai WM*. (2010). Overexpression of OsRAN2 in rice and Arabidopsis renders transgenic<br />
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136. Zhang DL, Zhu FY, Fan WC, Tao RZ, Yu H, Yang YL, Jiang WH, Yang S*. (2011). Gradually accumulating<br />
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137. Zhan S, Guo QH, Li MH, Li MW, Li JY, Miao XX, Huang YP*. (2010). Deletion of an N-acetyltransferase gene of<br />
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138. Zhang J, Wei YJ, Xiao W, Zhou ZH, Yan X*. (2011). Performance and spatial community succession of an anaerobic<br />
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139. Zhang L, Wang L, Wang J, Ou XJ, Zhao GP*, Ding XM*. (2010). DNA cleavage is independent of synapsis during<br />
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140. Zhang M, Li G., Huang W, Bi T, Tang Z, Su W, Sun W*. (2010). Proteomic study of Carissa spinarum in response to<br />
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141. Zhang M, Lü S, Li G, Mao Z, Yu X, Sun W, Tang Z, Long M*, Su W*. (2010). Identification of a residue in helix 2 of<br />
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142. Zhang P*, Wang WQ, Zhang GL, Kaminek M, Dobrev P, Xu J, Gruissem W. (2010). Senescence-inducible expression<br />
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143. Zhang R, Peng SY, Qin ZJ. (2010). Two Internal Origins of Replication on Streptomyces Linear Plasmid pFRL1.<br />
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144. Zhang W, Hu WL, Wen CK*. (2010). Ethylene preparation and its application to physiological experiments. Plant<br />
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34<br />
5<br />
6<br />
35
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SIPPE <strong>REPORT</strong><br />
研 究 所 介 绍<br />
2010-2011 SIPPE Report<br />
145. Zhang W, Wen CK*. (2010). Preparation of ethylene gas and comparison of ethylene responses induced by ethylene,<br />
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146. Zhang YY, Zhang BC, Yan DW, Dong WX, Yang WB, Li Q, Zeng LJ, Wang JJ, Wang LY, Hicks LM, He ZH*.<br />
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147. Zhang ZZ, Wang H, Luo DX, Zeng MH, Huang H, Cui XF*. (2010). Convergence of the 26S proteasome and the<br />
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148. Zhao Q, Huang X, Lin Z, Han B*. (2010). SEG-Map: A novel software for genotype calling and genetic map<br />
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149. Zhao SQ, Hu J, Guo LB, Qian Q, Xue HW*. (2010). Rice leaf inclination 2 (LC2), a VIN3-like protein, regulates leaf<br />
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150. Zhao SS, Dufour D, Sánchez T, Ceballos H, Zhang P*. (2011). Development of waxy cassava with different biological<br />
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151. Zhao W, Zhong Y, Yuan H, Wang J, Zheng HJ, Wang Y, Cen XF, Xu F, Bai J, Han XB, Lu G, Zhu YQ, Shao ZH, Yan<br />
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152. Zhao XL, Shi ZY, Peng LT, Shen GZ, Zhang JL*. (2011). An atypical HLH protein OsLF protein participates in<br />
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153. Zheng HQ*, L. Andrew S. (2011). L Andrew Staehelin. Protein storage vacuoles are transformed into lytic vacuoles in<br />
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154. Zheng P, Xia YL, Xiao GH, Xiong CH, Hu X, Zhang SW, Zheng HJ, Huang Y, Zhou Y, Wang SY, Zhao GP, Liu XZ,<br />
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155. Zhong L, Cheng QX, Tian XL, Zhao LiQ, Qin ZJ*. (2010). Characterization of the Replication, Transfer and<br />
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156. Zhou B, Yang XN, Jiang JH, Wang YB, Li MH, Li MW, Miao XX, Huang YP*. (2010). Silkworm (Bombyx mori)<br />
BmLid is a more prevalent histone lysine demethylase than its homologues in drosophila and mammals. Cell Research<br />
20: 1079-1082.<br />
157. Zhou M*, Bi WX, Liu XW. (2010). The genus Conocephalus (Orthoptera, Tettigonioidea) in China. Zootaxa 2527:<br />
49-60.<br />
158. Zhou S, Zhou Q, Liu Y, Wang S, Wen D, He Q, Wang W, Bendena WG, Li S*. (2010). Two Tor genes in the silkworm,<br />
Bombyx mori. Insect Mol Biol 19: 727-735.<br />
159. Sun ZT, Ning YY, Liu LX, Liu YM, Sun BB, Jiang WH, Yang C, Yang S*. (2011). Metabolic engineering of the<br />
L-phenylalanine pathway in Escherichia coli for the production of S- or R-mandelic acid. Microb Cell Fact. 13: 10-71.<br />
160. Zhu L, Tao RS, Wang Y, Jiang Y, Lin X, Yang YL, Zheng HB, Jiang WH, Yang S*. (2011). Removal of L: -alanine<br />
from the production of L: -2-aminobutyric acid by introduction of alanine racemase and D: -amino acid oxidase. Appl<br />
Microbiol Biotechnol. 90:903-910.<br />
161. Zhu Q, Zhang JT, Gao XS, Tong JH, Xiao LT, Li WB, Zhang HX*. (2010). The Arabidopsis AP2/ERF transcription<br />
factor R AP2.6 participates in ABA, salt and osmotic stress responses. Gene 457:1-12<br />
2010-2011 Major Event<br />
Year 2010<br />
1.19 The Advisory Committee of "Molecular Mechanism of Plant<br />
Hormone", funded by Key Project of Major Resarch Plan from NSFC,<br />
visited SIPPE twice in January.<br />
2.7 A Forum for "Mechanism of Plant Immunity and Crop Productivity"<br />
was held in Shanghai Institute of Advanced Studies.<br />
4.8 The International Partner Creative Research Group of "Metabolic<br />
Basis of Crop Yield" sponsored by SIPPE passed through the evaluation<br />
organized by Chinese Academy of Science, CAS.<br />
4.20 A new variety of sweet potato "Taizhong No.9" was examined and<br />
approved by Crop Variety Authorization Committee of Shandong Province<br />
(No. 2010041).<br />
5.16 The Unveiling Ceremony for Key Laboratory of Insect<br />
Developmental and Evolutionary Biology was held in the institute.<br />
5.19 National Center of Plant Gene Research (Shanghai) was launched<br />
in Shanghai.<br />
6.18 The annual impact factor of Molecular Plant which is sponsored by<br />
SIPPE and Chinese Society of Plant Biology reached 2.784 in 2009.<br />
7.7 Shanghai Entomological Museum was awarded the title of "National<br />
Science Education Base”.<br />
9.6 The Agricultural Biotechnology Department of DuPont Pioneer Hi-<br />
Bred International Corporation visited SIPPE.<br />
9.26 The 1 st Synthetic Microbiology Symposium organized by SIPPE<br />
was held in Shanghai.<br />
9.30 Dr. Julian I. Schroeder visited SIPPE and gave a lecture.On behalf<br />
of Chinese Academy of Science, Dr. HongWei Xue, the director of SIPPE,<br />
honored him as the distinguished research fellow of Foreign Experts.<br />
10.21 Dr. Pamela F. Colosimo, deputy chief editor of Nature Genetics,<br />
visited SIPPE.<br />
10.25 Dr. HongWei Xue, together with a delegation from SIPPE visited<br />
South China Botanical Garden by their invitation.<br />
36<br />
7<br />
37
2011 period<br />
ject "Mechanisms of plant immunity and practice of molecular design for crop disease<br />
ed by SIPPE was launched<br />
Appendix<br />
in Shanghai.<br />
SIPPE <strong>REPORT</strong><br />
Year 2011<br />
ation office of SIPPE was awarded the 2009-2010 National Advanced Women Collective<br />
ence and Technology System<br />
2.26 The 973 program "Mechanisms of Plant Immunity and Practice<br />
of Molecular Design for Crop Disease Resistance" hosted by SIPPE was<br />
launched in Shanghai.<br />
3.8 The executive office of SIPPE was awarded the 2009-2010<br />
Advanced Women Collective of Shanghai Science and Technology<br />
cience visited SIPPE twice on 17th and 29th March.<br />
System.<br />
3.17 Bayer Crop Science visited SIPPE twice on 17th and 29th March.<br />
5.3 Dr. XiuLing Cai, associate professor of SIPPE, won the third prize<br />
of Shanghai Technological Invention Award for her research of "Screening<br />
Methods for Low Amylose Content of Rice Seeds".<br />
Cai, associate professor of SIPPE, won the third prize 5.5 of Dr. Shanghai XuHong Technological Qian, president of East China University of Science<br />
for her research of "Screening methods for low amylose content of rice seeds".<br />
and Technology, with a delegation from Shanghai Key Laboratory of<br />
ian, director of East China University of Science and Technology, with a delegation<br />
Key Laboratory of Chemical Biology, visited the Chemical Key Laboratory Biology, visited of Insect the Key Laboratory of Insect Developmental and<br />
and Evolutionary Biology, CAS.<br />
Evolutionary Biology, CAS.<br />
n, the president of SIBS and Dr.HongWei Xue, the director of SIPPE, with a delegation<br />
ey Laboratory of Plant Molecular Genetics, National Center of Plant Gene Research<br />
5.6 Dr. XiaoYa Chen, the president of SIBS and Dr. HongWei Xue, the<br />
director of SIPPE, with a delegation from National Key Laboratory of Plant<br />
Molecular Genetics, National Center of Plant Gene Research (Shanghai)<br />
and Office of Projects Management visited Yangzhou University to carry<br />
out academic exchanges in rice genetics and breeding.<br />
5.10 The Strategy Symposium of Key Laboratory of Insect<br />
Developmental and Evolutionary Biology 2011 were held in SIPPE.<br />
5.26 The Development Strategy Seminar<br />
and Annual Academic Meeting of SIPPE was<br />
held in Fuyang, Zhejiang province. More than<br />
180 staff including the leading group, members<br />
of the academic committee, PIs, research and<br />
administrative personnel, as well as postdoctors<br />
and graduate students attended the meeting.<br />
6.9 Dr. Dale Sanders, the director of John Innes Centre, visited SIPPE<br />
and gave a lecture on"Cations in Plants: Losing Them and Using Them".<br />
6.24 The opening ceremony of National Center of Plant Gene Research<br />
(Shanghai) was held in SIPPE.<br />
6.30 “The 2 nd International Conference on Plant Metabolism” organized<br />
by SIPPE was held in Qingdao.<br />
7.2 “The 3 rd International Symposium on Insect Physiology, Biochemistry<br />
and Molecular Biology” was held in Shanghai by the organization of Key<br />
Laboratory of Insect Developmental and Evolutionary Biology, CAS.<br />
7.7 According to the annual journal citation report published by ISI in<br />
2010, the impact factor of Molecular Plant reached 4.296. For the first time,<br />
MP ranked in the top 8%, and first in plant science journals of Asia.<br />
7.21 In the evaluation of State Key Laboratories by the Ministry of<br />
Science and Technology, National Key Laboratory of Plant Molecular<br />
Genetics was ranked “Excellent".<br />
8.31 The opening ceremony for new graduate<br />
student was held in the institute.<br />
9.29 Dr. JiaYang Li, the associate president of<br />
Chinese Academy of Sciecnes, attended the midterm<br />
assessment of the leading group in SIPPE. Dr.<br />
HongWei Xue, the director of SIPPE, on behalf of the<br />
leading group, made the summing-up report for all the<br />
attendee. The leading group of SIPPE that assumed<br />
office in 2008 December faced the frontiers of life sciences and focused on<br />
the national strategy need of agriculture, environment and resource. All the<br />
members of the leading group united and cooperated to make an efficient<br />
exploration in the key developmental areas of SIPPE. The great efforts<br />
made by the leading group made brilliant achievements.<br />
38<br />
39
Appendix<br />
SIPPE <strong>REPORT</strong><br />
Representative Publications<br />
10.12 The “Enabling Technology for Synthetic-Six-<br />
Academy Synthetic Biology Symposium II” was held in<br />
Shanghai Institute of Biological Science.<br />
10.15 The 973 program "Study on Crop Nutrient<br />
Metabolism and Its Regulation Mechanism" organized by<br />
SIPPE was completed and passed the evaluation in Beijing.<br />
10.18 The celebration of the 65 years anniversary of academician<br />
Wenying Yin engaged in research and her 90 th birthday was held in SIPPE.<br />
11.1 During the launch of "Shenzhou-8", Dr. HongWei Xue, director of<br />
SIPPE and the designers of biotechnology system in space life sciences,<br />
with a delegation, visited the launch site and guided the preparation work.<br />
11.3 Mr.JingDun Jia, the director of China Rural Technology Development<br />
Center from Ministry of Science and Technology, visited SIPPE.<br />
11.15 Dr. Katharine Barnes, the chief editor of Nature Protocols, visited<br />
SIPPE.<br />
11.21 Dr. HongWen Huang, the head of South China Botanical Garden,<br />
with a delegation visited SIPPE. The academic exchanges activity is<br />
helpful to further expand and deepen the bilateral strategic and cooperative<br />
partnership.<br />
11.24The Creative Research group of “System and Synthetic Biology<br />
Research of Microbial Metabolism”funded by NSFC held a kick-off<br />
meeting in SIPPE.<br />
11.28The Annual Academic Meeting 2011 of the CAS National Key<br />
Laboratory of Plant Molecular Genetics was held in SIPPE.<br />
11.30 Dr. Magdalena Skipper, the chief editor of Nature, visited SIPPE.<br />
12.15 Dr. GuoPing Zhao was elected as the academician of the<br />
Academy of Sciences of Developing Country.<br />
12.18 The 973 program "Artifical Biology Devices with Special<br />
Functions: Designing, Construction and Assembly" hosted by SIPPE was<br />
launched in Shanghai.<br />
© 2010 Nature America, Inc. All rights reserved.<br />
Genome-wide association studies of 14 agronomic traits<br />
in rice landraces<br />
Xuehui Huang 1,2,10 , Xinghua Wei 3,10 , Tao Sang 4,10 , Qiang Zhao 1,2,10 , Qi Feng 1,10 , Yan Zhao 1 , Canyang Li 1 ,<br />
Chuanrang Zhu 1 , Tingting Lu 1 , Zhiwu Zhang 5 , Meng Li 5,6 , Danlin Fan 1 , Yunli Guo 1 , Ahong Wang 1 , Lu Wang 1 ,<br />
Liuwei Deng 1 , Wenjun Li 1 , Yiqi Lu 1 , Qijun Weng 1 , Kunyan Liu 1 , Tao Huang 1 , Taoying Zhou 1 , Yufeng Jing 1 ,<br />
Wei Li 1 , Zhang Lin 1 , Edward S Buckler 5,7 , Qian Qian 3 , Qi-Fa Zhang 8 , Jiayang Li 9 & Bin Han 1,2<br />
Uncovering the genetic basis of agronomic traits in crop landraces that have adapted to various agro-climatic conditions is<br />
important to world food security. Here we have identified ~3.6 million SNPs by sequencing 517 rice landraces and constructed<br />
a high-density haplotype map of the rice genome using a novel data-imputation method. We performed genome-wide association<br />
studies (GWAS) for 14 agronomic traits in the population of Oryza sativa indica subspecies. The loci identified through GWAS<br />
explained ~36% of the phenotypic variance, on average. The peak signals at six loci were tied closely to previously identified<br />
genes. This study provides a fundamental resource for rice genetics research and breeding, and demonstrates that an approach<br />
integrating second-generation genome sequencing and GWAS can be used as a powerful complementary strategy to classical<br />
biparental cross-mapping for dissecting complex traits in rice.<br />
Rice (Oryza sativa L.) is a staple food for more than half of the<br />
world population. Rice landraces have evolved from their wild progenitor<br />
under natural and human selection, leading to the maintenance<br />
of high genetic diversity 1,2 . These cultivated varieties also<br />
have a high capacity to tolerate biotic and abiotic stress, resulting<br />
in highly stable yields and an intermediate yield under a low-input<br />
agricultural system. Identifying the genetic basis of these diverse<br />
varieties will provide important insights for breeding elite varieties<br />
for sustainable agriculture.<br />
GWAS have emerged as a powerful approach for identifying<br />
genes underlying complex diseases at an unprecedented rate 3–6 .<br />
However, despite their promise, GWAS have largely not been<br />
applied to the dissection of complex traits in crop plants 7–9 . This<br />
is due mainly to the lack of effective genotyping techniques for<br />
plants and the limited resources for developing high-density haplotype<br />
maps like those seen in other well-developed systems, such<br />
as the human genome HapMap project 3,4 . Rice is an ideal candidate<br />
system for the application of GWAS because it is self-fertilizing<br />
and has a high-quality reference genome sequence 10 and phenotyping<br />
resources. Such a system should permit the identification of<br />
high-quality haplotypes necessary to accurately associate molecular<br />
markers with phenotypes.<br />
Here we have genotyped rice landraces through direct resequencing<br />
of their genomes by adopting sequencing-by-synthesis technology,<br />
which represents a step forward from the oligonucleotide array<br />
technology widely used for GWAS 11–13 . More than 500 diverse rice<br />
landraces, representing a large collection of rice accessions, were<br />
sequenced at approximately onefold genome coverage. The resulting<br />
data set captures more of the common sequence variation in cultivated<br />
rice than any other data set to date. Using a highly accurate<br />
imputation method, we constructed a high-density rice haplotype<br />
map and performed GWAS for 14 agronomic traits to identify a substantial<br />
number of loci potentially important for rice production and<br />
improvement. Some loci were mapped at close to gene resolution,<br />
indicating that GWAS of rice landraces could provide an effective<br />
approach for gene identification.<br />
RESULTS<br />
Genome sequencing and SNP identification<br />
From a collection of ~50,000 rice accessions originating in China,<br />
we have undertaken an effort to build a large sample of morphologically,<br />
genetically and geographically diverse landraces for genetic<br />
studies. In this study, a total of 517 landraces were selected and<br />
comprehensively phenotyped (see Online Methods). We genotyped<br />
1 National Center for Gene Research, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai,<br />
China. 2 CAS Key Laboratory of Genome Sciences and Information, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China. 3 State Key Laboratory<br />
of Rice Biology, China National Rice Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou, China. 4 Department of Plant Biology, Michigan State<br />
University, East Lansing, Michigan, USA. 5 Institute for Genomic Diversity, Cornell University, Ithaca, New York, USA. 6 National Center for Soybean Improvement,<br />
State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Agriculture, Nanjing Agricultural University, Nanjing, China. 7 US Department of<br />
Agriculture–Agricultural Research Service, Ithaca, New York, USA. 8 National Key Laboratory of Crop Genetic Improvement, National Center for Plant Gene Research<br />
(Wuhan), Huazhong Agricultural University, Wuhan, China. 9 National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese<br />
Academy of Sciences, Beijing, China. 10 These authors contributed equally to this work. Correspondence should be addressed to B.H. (bhan@ncgr.ac.cn).<br />
Received 10 May; accepted 27 September; published online 24 October 2010; doi:10.1038/ng.695<br />
Articles<br />
Nature GeNetics VOLUME 42 | NUMBER 11 | NOVEMBER 2010 961<br />
40<br />
41
Appendix<br />
SIPPE <strong>REPORT</strong><br />
Articles<br />
Fructose sensitivity is suppressed in Arabidopsis by<br />
the transcription factor ANAC089 lacking the<br />
membrane-bound domain<br />
© 2012 Nature America, Inc. All rights reserved.<br />
Genome-wide association study of flowering time and grain<br />
yield traits in a worldwide collection of rice germplasm<br />
Xuehui Huang 1,2,5 , Yan Zhao 1,2,5 , Xinghua Wei 3,5 , Canyang Li 1 , Ahong Wang 1 , Qiang Zhao 1 , Wenjun Li 1 ,<br />
Yunli Guo 1 , Liuwei Deng 1 , Chuanrang Zhu 1 , Danlin Fan 1 , Yiqi Lu 1 , Qijun Weng 1 , Kunyan Liu 1 , Taoying Zhou 1 ,<br />
Yufeng Jing 1 , Lizhen Si 1 , Guojun Dong 1,3 , Tao Huang 1 , Tingting Lu 1 , Qi Feng 1 , Qian Qian 3 , Jiayang Li 4 &<br />
Bin Han 1,2<br />
A high-density haplotype map recently enabled a genome-wide association study (GWAS) in a population of indica subspecies of<br />
Chinese rice landraces. Here we extend this methodology to a larger and more diverse sample of 950 worldwide rice varieties,<br />
including the Oryza sativa indica and Oryza sativa japonica subspecies, to perform an additional GWAS. We identified a total of<br />
32 new loci associated with flowering time and with ten grain-related traits, indicating that the larger sample increased the power<br />
to detect trait-associated variants using GWAS. To characterize various alleles and complex genetic variation, we developed an<br />
analytical framework for haplotype-based de novo assembly of the low-coverage sequencing data in rice. We identified candidate<br />
genes for 18 associated loci through detailed annotation. This study shows that the integrated approach of sequence-based GWAS<br />
and functional genome annotation has the potential to match complex traits to their causal polymorphisms in rice.<br />
Rice (Oryza sativa L) is an economically important crop that accounts<br />
for ~20% of the world’s caloric intake. To be grown successfully under<br />
a variety of climatic conditions across the globe, breeders maintain<br />
rice at high genetic diversity. Second-generation sequencing technologies<br />
have enabled resequencing of a large number of genomes<br />
and have provided the possibility of high-throughput genotyping and<br />
large-scale genetic variation surveys 1 . Identification of allelic variations<br />
underpinning the phenotypic diversity observed in rice will have<br />
enormous practical implications in rice breeding 2 .<br />
Recently we performed low-coverage sequencing of 517 Chinese<br />
rice landraces and imputed missing genotypes to construct a haplotype<br />
map of the rice genome. We then used this map to perform<br />
GWAS in the indica population in a previous study 3 . However, identifying<br />
the loci associated with complex traits in rice is challenging.<br />
This is because (i) O. sativa contains indica and japonica subspecies,<br />
which can be further divided into several divergent groups with high<br />
amounts of population differentiation 2,3 , and (ii) there is a low rate<br />
of linkage disequilibrium (LD) decay in rice 3 . Therefore, the interpretation<br />
of association signals and the identification of causal genes<br />
through GWAS requires a full incorporation of population structure<br />
and detailed follow-up analyses of associated loci for candidate genes<br />
and causal polymorphisms.<br />
In this study, we examined 950 worldwide rice cultivars, representing<br />
a much broader and larger sample than has previously been used.<br />
We developed a new analytical framework to assemble low-coverage<br />
sequences of different gene alleles 4 . This approach was then used to<br />
detect SNPs and complex polymorphisms such as insertions and deletions<br />
(indels). Using this new method, we were able to project a map<br />
of genic variation onto the rice genome. This facilitated the discovery<br />
of functional variation among rice varieties. We collected phenotypic<br />
data of flowering time (heading date) and grain-related traits and used<br />
them for a GWAS in the O. sativa indica and japonica subpopulations<br />
and in the full O. sativa population. The broader sampling greatly<br />
enhanced the power of the GWAS. In addition to the loci identified<br />
previously, we identified 32 new loci underlying flowering time and<br />
ten grain-related traits. In the follow-up analysis of these regions, we<br />
integrated detailed annotation, expression profiles and genetic variation<br />
to identify candidate genes and potential causal polymorphisms<br />
for the grain-related traits.<br />
RESULTS<br />
Genetic structure of worldwide rice germplasm<br />
The germplasm collection used in this study included a previous set<br />
of 520 Chinese landraces, plus a new set from China and other widespread<br />
countries (Supplementary Fig. 1). We sequenced the genomes<br />
of the plants in the new set, which included 100 additional Chinese<br />
japonica landraces and 330 diverse global cultivars from 33 countries,<br />
on the Illumina Genome Analyzer IIx to approximately onefold coverage.<br />
The resulting sequence dataset of 950 rice varieties consisted of<br />
4.6 billion 73-bp paired-end reads. After aligning these short reads<br />
1 National Center for Gene Research, National Center for Plant Gene Research (Shanghai), Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological<br />
Sciences, Chinese Academy of Sciences, Shanghai, China. 2 Chinese Academy of Sciences Key Laboratory of Genome Sciences and Information, Beijing Institute<br />
of Genomics, Chinese Academy of Sciences, Beijing, China. 3 State Key Laboratory of Rice Biology, China National Rice Research Institute, Chinese Academy of<br />
Agricultural Sciences, Hangzhou, China. 4 National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences,<br />
Beijing, China. 5 These authors contributed equally to this work. Correspondence should be addressed to B.H. (bhan@ncgr.ac.cn).<br />
Received 3 June; accepted 2 November; published online 4 December 2011; doi:10.1038/ng.1018<br />
32 VOLUME 44 | NUMBER 1 | JANUARY 2012 Nature GeNetics<br />
Ping Li a,1 , Julia J. Wind b,1 , Xiaoliang Shi a , Honglei Zhang a , Johannes Hanson b,c,d , Sjef C. Smeekens b,c ,<br />
and Sheng Teng a,b,c,2<br />
a Institute of Plant Physiology and Ecology, Shanghai Institute for Biological Sciences, The Chinese Academy of Sciences, Shanghai 200032, China; b Department<br />
of Molecular Plant Physiology, Utrecht University, 3584 CH, Utrecht, The Netherlands; c Centre for BioSystems Genomics, 6700 AB, Wageningen,<br />
The Netherlands; and d Umeå Plant Science Center (UPSC), Umeå University, 901 87 Umea, Sweden<br />
Edited by Maarten Koornneef, Max Planck Institute for Plant Breeding Research, Cologne, Germany, and approved January 19, 2011 (received for review<br />
December 16, 2010)<br />
In living organisms sugars not only provide energy and carbon<br />
skeletons but also act as evolutionarily conserved signaling molecules.<br />
The three major soluble sugars in plants are sucrose, glucose,<br />
and fructose. Information on plant glucose and sucrose signaling is<br />
available, but to date no fructose-specific signaling pathway has<br />
been reported. In this study, sugar repression of seedling development<br />
was used to study fructose sensitivity in the Landsberg<br />
erecta (Ler)/Cape Verde Islands (Cvi) recombinant inbred line population,<br />
and eight fructose-sensing quantitative trait loci (QTLs)<br />
(FSQ1–8) were mapped. Among them, FSQ6 was confirmed to be<br />
a fructose-specific QTL by analyzing near-isogenic lines in which Cvi<br />
genomic fragments were introgressed in the Ler background. These<br />
results indicate the existence of a fructose-specific signaling pathway<br />
in Arabidopsis. Further analysis demonstrated that the FSQ6-<br />
associated fructose-signaling pathway functions independently<br />
of the hexokinase1 (HXK1) glucose sensor. Remarkably, fructosespecific<br />
FSQ6 downstream signaling interacts with abscisic acid<br />
(ABA)- and ethylene-signaling pathways, similar to HXK1-dependent<br />
glucose signaling. The Cvi allele of FSQ6 acts as a suppressor<br />
of fructose signaling. The FSQ6 gene was identified using mapbased<br />
cloning approach, and FSQ6 was shown to encode the transcription<br />
factor gene Arabidopsis NAC (petunia No apical meristem<br />
and Arabidopsis transcription activation factor 1, 2 and Cup-shaped<br />
cotyledon 2) domain containing protein 89 (ANAC089). The Cvi allele<br />
of FSQ6/ANAC089 is a gain-of-function allele caused by a premature<br />
stop in the third exon of the gene. The truncated Cvi FSQ6/<br />
ANAC089 protein lacks a membrane association domain that is<br />
present in ANAC089 proteins from other Arabidopsis accessions.<br />
As a result, Cvi FSQ6/ANAC089 is constitutively active as a transcription<br />
factor in the nucleus.<br />
sugar signaling | natural variation | fructose quantitative trait locus | map<br />
based cloning<br />
n plants, sugars provide the energy and carbon skeletons needed<br />
Ifor growth and in addition act as crucial signaling molecules that<br />
affect growth, development, and response to the (a)biotic environment<br />
(1–3). Plant cells harbor sugar-sensing and -signaling systems<br />
that regulate the expression of thousands of genes and control the<br />
metabolic processes needed for growth (2–4). These sugar-response<br />
systems are known to interact with other signaling pathways, such<br />
as those for light, phytohormones, stress, and nutrients (1).<br />
The neutral sugars sucrose, glucose, and fructose are central to<br />
metabolism in plants and in other organisms as well. So far, detailed<br />
information is available only on glucose sensing, and it has<br />
been shown that the hexokinase 1 (HXK1) enzyme acts as a glucose<br />
sensor (5, 6). Sucrose-specific signaling also was demonstrated<br />
because the effect of sucrose cannot be mimicked by<br />
glucose and/or fructose (7), but so far no information on sucrosesensing<br />
systems is available. A signaling function for fructose has<br />
been proposed (8, 9), but no convincing experimental evidence on<br />
such fructose-specific signaling is available.<br />
In Arabidopsis early seedling development is arrested by high<br />
concentrations of exogenous glucose or sucrose. This observation<br />
has been used in several screens to identify mutants defective in<br />
sugar sensing or signaling (10, 11). This rapid and convenient<br />
phenotypic screen allowed the isolation of many mutants with<br />
altered sugar responses and the subsequent identification of the<br />
genes involved. In this way the glucose-insensitive (gin) phenotype<br />
of the hxk1/gin2 mutant (6) was established, and a network of<br />
HXK1-dependent glucose signaling and abscisic acid (ABA) and<br />
ethylene biosynthesis and signaling was identified (10–17).<br />
Fructose is a major soluble monosaccharide in plant. Fructose<br />
is produced from sucrose by invertases and sucrose synthases.<br />
Like glucose, fructose can repress the expression of photosynthesis<br />
genes (18). Most likely, fructose is phosphorylated mainly<br />
by fructokinases (FRKs), and a member of that gene family is<br />
present in Arabidopsis. The putative regulatory role of FRK in<br />
fructose signaling was investigated first in tomato (9, 19). Inhibition<br />
of the tomato fructokinase 2 (LeFRK2) interferes with<br />
development of phloem and xylem by impairing callose deposition,<br />
thus reducing transport of sugars and water (20). In this<br />
way LeFRK2 affects tomato stem and root growth and the normal<br />
development of flowers, fruits, and seeds. These experiments<br />
illustrate the important role of FRK in metabolism, but a signaling<br />
function for FRKs or for fructose could not be established.<br />
Here, a fructose-specific signaling pathway is proposed by the<br />
identification of Arabidopsis quantitative trait loci (QTLs) in the<br />
Landsberg erecta (Ler)/Cape Verde Islands (Cvi) recombinant<br />
inbred line (RIL) population that displays altered fructose-specific<br />
sensitivity. This fructose-signaling pathway is HXK1 independent,<br />
but, remarkably, the fructose signal feeds into the same downstream<br />
ABA-signaling pathway as the glucose/HXK signal. The<br />
Cvi fructose-sensing QTL allele 6 (FSQ6) was cloned by a mapbased<br />
cloning approach and shown to encode the Arabidopsis<br />
NAC (petunia No apical meristem and Arabidopsis transcription<br />
activation factor 1, 2 and Cup-shaped cotyledon 2) domain containing<br />
protein 89 (ANAC089) gene. Functional analysis indicates<br />
that the Cvi FSQ6/ANAC089 allele is a gain-of-function allele that<br />
represses the fructose-induced ABA-signaling pathway.<br />
Results<br />
Identification of Fructose-Sensitivity QTLs in the Ler/Cvi RIL<br />
Population. High concentrations of glucose and sucrose repress<br />
Arabidopsis seedling development. The identified gin and sugarinsensitive<br />
(sis) mutants are insensitive to glucose and/or sucrose<br />
Author contributions: S.T. designed research; P.L., J.J.W., X.S., and H.Z. performed research;<br />
J.H. and S.C.S. analyzed data; and S.C.S. and S.T. wrote the paper.<br />
The authors declare no conflict of interest.<br />
This article is a PNAS Direct Submission.<br />
1 P.L., and J.J.W. contributed equally to this work.<br />
2 To whom correspondence should be addressed. E-mail: steng@sippe.ac.cn.<br />
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.<br />
1073/pnas.1018665108/-/DCSupplemental.<br />
3436–3441 | PNAS | February 22, 2011 | vol. 108 | no. 8 www.pnas.org/cgi/doi/10.1073/pnas.1018665108<br />
42<br />
43
Appendix<br />
SIPPE <strong>REPORT</strong><br />
Four amino acids guide the assembly or disassembly of<br />
Arabidopsis histone H3.3-containing nucleosomes<br />
Leilei Shi a,1 , Jing Wang a,1,2 , Fang Hong a , David L. Spector b , and Yuda Fang a,3<br />
a National Key Laboratory of Plant Molecular Genetics, Shanghai Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese<br />
Academy of Sciences, Shanghai 200032, China; and b Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724<br />
Edited* by Steven Henikoff, Fred Hutchinson Cancer Research Center, Seattle, WA, and approved May 17, 2011 (received for review November 30, 2010)<br />
The histone variant H3.3 and the canonical histone H3.1, which<br />
differ in only 4- to 5-aa positions, are coexpressed in complex<br />
multicellular eukaryotes from fly to human and plant. H3.3 is mainly<br />
associated with active chromatin by replacing H3.1 through chaperones<br />
such as histone regulator A, death domain associated protein<br />
DAXX, thalassemia/mental retardation syndrome X-linked homolog<br />
ATRX, or proto-oncogene protein DEK and plays important roles in<br />
the germline, epigenetic memory, and reprogramming. However,<br />
the signals within H3.3 that serve as a guide for its dynamic deposition<br />
or depletion in plant chromatin are not clear. Here, we show<br />
that Arabidopsis histone H3.3 differs from H3.1 by 4-aa sites: amino<br />
acids 31, 41, 87, and 90. Although histone H3.1 is highly enriched in<br />
chromocenters, H3.3 is present in nucleolar foci in addition to being<br />
diffusely distributed in the nucleoplasm. We have evaluated the<br />
function of the 4 aa that differ between H3.1 and H3.3. We show<br />
that amino acid residue 87, and to some extent residue 90, of<br />
Arabidopsis histone H3.3 are critical for its deposition into rDNA<br />
arrays. When RNA polymerase I-directed nucleolar transcription is<br />
inhibited, wild type H3.3, but not H3.3 containing mutations at residues<br />
31 and 41, is depleted from the rDNA arrays. Together, our<br />
results are consistent with a model in which amino acids 87 and 90<br />
in the core domain of H3.3 guide nucleosome assembly, whereas<br />
amino acids 31 and 41 in the N-terminal tail of Arabidopsis H3.3<br />
guide nucleosome disassembly in nucleolar rDNA.<br />
H3 dynamics | histone code | nucleolar dominance | chromatin remodeling<br />
he fundamental repeat unit of packaging of eukaryotic ge-<br />
DNA is predominantly the nucleosome where DNA is<br />
Tnomic<br />
wrapped around a histone octamer that contains two molecules<br />
of each core histone: H2A, H2B, H3, and H4. The four core<br />
histones share the common histone folding domain (HFD), which<br />
is composed of three α-helices (α1, α2, and α3) separated by two<br />
loops (L1 and L2) (1). The N- and C-terminal tails stretch out of<br />
the nucleosome core and are subject to diverse posttranslational<br />
modifications (PTMs) including methylation, acetylation, phosphorylation,<br />
ubiquitination, and poly-ADP ribosylation (2, 3). In<br />
addition, the incorporation of histone variants into nucleosomes<br />
has been proposed to provide another mechanism for modifying<br />
chromatin structure (4).<br />
In addition to the centromere-specific histone 3 variant (CenH3),<br />
which can be deposited into the centromeric nucleosomes in tetrameric<br />
(5, 6) or hexameric states (7), the histone H3 family<br />
includes another universal histone H3 variant H3.3 (4) or H3.2 in<br />
alfalfa, a plant histone H3.3 (8). In most animals, histone variant<br />
H3.3 differs by 4-aa residues from H3.1, which are residue 31 in the<br />
N-terminal tail and residues 87, 89, and 90 in the HFD near the<br />
beginning of α2 (1, 9). In contrast to the replication-coupled<br />
deposition of H3.1 during S-phase mediated by chromatin-assembly<br />
factor 1 (CAF1) (4), H3.3 in eukaryotes incorporates into nucleosomes<br />
mostly in a replication-independent manner (9)<br />
through the histone chaperones, including the histone regulator<br />
A (HIRA), ATRX, death-associated protein DAXX, and DEK<br />
(10–17). H3.3 is deposited primarily in promoters, gene regulatory<br />
sites, and regions with PTMs that are associated with transcribed<br />
genes (18). H3.3 has been shown to play roles in epigenetic<br />
reprogramming (19) and memory (20). When the H3.3 gene was<br />
knocked out in Drosophila melanogaster, flies exhibited sterility,<br />
and the transcriptional defects were able to be rescued by overexpression<br />
of H3.1, which shows that H3.3 is not necessary for<br />
somatic development (21, 22). In addition, H3.3 mutants display<br />
meiotic defects in chromosome condensation in spermatocytes,<br />
which is dependent on residues 87, 89, and/or 90 but not on<br />
methylation of H3.3K4 or phosphorylation of Ser31, suggesting<br />
a role of H3.3 in the germline (22).<br />
H3.3 can be displaced dynamically by H3.1 and reloaded at<br />
the site of transcription in D. melanogaster (23). The nucleosome<br />
turnover might have functional significance in epigenome maintenance,<br />
gene regulation, and DNA replication (24). However,<br />
the signals within H3.3 that serve as a guide for its dynamic deposition<br />
or depletion in plant chromatin are not clear. Here, we<br />
have evaluated the function of 4 aa that differ between Arabidopsis<br />
histone H3.1 and H3.3, and we have identified the specific signals<br />
within H3.3 that serve as guides for its dynamic deposition into or<br />
depletion from the H3.3-containing nucleosomes.<br />
Results and Discussion<br />
Arabidopsis Histone H3.3 Is Highly Enriched at Nucleolar rDNA Foci<br />
in Addition to Being Diffusely Distributed in the Nucleoplasm. The<br />
Arabidopsis genome encodes six H3.3 or H3.3-like genes, including<br />
histone three related 4(HTR4, At4g40030), HTR5(At4g40040),<br />
HTR6(At1g13370), HTR8(At5g10980), HTR14(At1g75600), and<br />
the male gamete-specific HTR10/AtMGH3(At1g19890) (25). To<br />
investigate the regions in the plant histone H3.3 variant that are<br />
responsible for guiding its incorporation into and its depletion<br />
from nucleosomes, we first examined the sequence alignment of<br />
canonical Arabidopsis histone H3.1(HTR1) and variant H3.3<br />
(HTR4) proteins and compared them with corresponding sequences<br />
from other organisms (Fig. 1). The difference between<br />
histone H3.1 and H3.3 is defined by 4-aa residues at the sites 31<br />
(Ala vs. Ser), 87 (Ser vs. Ala), 89 (Val vs. Ile), and 90 (Met vs. Gly)<br />
in Drosophila (26), and an additional site at 96 (Cys vs. Ser) is<br />
included in humans (27, 28). The difference of 4-aa residues between<br />
Arabidopsis histone H3.1/HTR1 and H3.3/HTR4 was observed<br />
at the sites 31 (Ala vs. Thr), 41 (Phe vs. Tyr), 87 (Ser vs.<br />
His), and 90 (Ala vs. Leu); they lack the amino acid change at<br />
residue 89 observed in other organisms, but contain an additional<br />
amino acid difference at residue 41. This plant-specific feature<br />
is conserved in both dicot and monocot plant species such as rice<br />
and maize (Figs. S1–S3) (19).The amino acid residues 87 and 90<br />
are located in the α2-helix of the H3 core domain and residues<br />
Author contributions: D.L.S. and Y.F. designed research; L.S., J.W., F.H., and Y.F. performed<br />
research; L.S., J.W., and Y.F. analyzed data; and L.S. and Y.F. wrote the paper.<br />
The authors declare no conflict of interest.<br />
*This Direct Submission article had a prearranged editor.<br />
1 L.S. and J.W. contributed equally to this work.<br />
2 Present address: Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724.<br />
3 To whom correspondence should be addressed. E-mail: yfang@sippe.ac.cn.<br />
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.<br />
1073/pnas.1017882108/-/DCSupplemental.<br />
<strong>REPORT</strong>S<br />
1004<br />
mammalian cells with CobB deacetylase increased<br />
ASL activity (Fig. 3H), supporting a direct role of<br />
acetylation in ASL inactivation. The dual regulation<br />
of ASL by both amino acids and glucose<br />
indicates that acetylation may have an important<br />
role in the coordination of metabolic pathways.<br />
In the presence of sufficient glucose, amino acid<br />
catabolism for energy production and gluconeogenesis<br />
would be inhibited. In the presence of<br />
abundant amino acids and low glucose, cells would<br />
switch to using amino acids for energy production<br />
with enhanced urea cycle activity. Cells may use<br />
acetylation to coordinate multiple pathways in<br />
order to achieve these metabolic adaptations<br />
Phosphoenolpyruvate carboxykinase 1(PEPCK1;<br />
EC code 4.1.1.32) is a key regulatory enzyme in<br />
gluconeogenesis (Fig. 1D) (9, 10). Three acetylated<br />
lysine residues were identified in PEPCK1 by MS<br />
analysis (Lys 70 , Lys 71 , and Lys 594 ; table S2). Acetylation<br />
of PEPCK1 was enhanced in cells treated<br />
with high concentrations of glucose (Fig. 4A) but<br />
was decreased by addition of amino acids in glucosefree<br />
medium (Fig. 4B). These results suggest a potential<br />
mechanism by which cells could regulate<br />
gluconeogenesis through regulating acetylation<br />
of PEPCK1 in response to the availability of<br />
extracellular fuels.<br />
In searching for an effect of acetylation on the<br />
regulation of PEPCK1, we noticed that levels of<br />
endogenous PEPCK1 protein were decreased by<br />
high glucose (Fig. 4C). Furthermore, treatment<br />
with TSA and NAM caused a 70% reduction in<br />
the amount of PEPCK1 protein in both HEK293T<br />
and Chang liver cells (Fig. 4D). PEPCK1 was stable<br />
in cells in glucose-free medium but unstable<br />
in high-glucose medium (Fig. 4E). When cells<br />
were treated with TSA and NAM, PEPCK1 was<br />
unstable even in glucose-free medium or in the<br />
presence of amino acids. These results indicate that<br />
acetylation may regulate the stability of PEPCK1.<br />
We replaced the three putative acetylation lysine<br />
residues by arginine (PEPCK1 3KR ) or glutamine<br />
(PEPCK1 3KQ ) to abolish or mimic acetylation,<br />
respectively. The PEPCK1 3KR mutant was more<br />
stable than the wild type, whereas the PEPCK1 3KQ<br />
mutant remained unstable (Fig. 4F). Moreover,<br />
treatment of cells with TSA and NAM failed to<br />
destabilize the PEPCK1 3KR mutant.<br />
The importance of lysine acetylation in the<br />
regulation of chromatin dynamics and gene expression<br />
is well appreciated. Our study and others<br />
extend the scope of cell regulation by lysine acetylation<br />
to an extent comparable to that of other<br />
major posttranslational modifications such as phosphorylation<br />
and ubiquitination. We show that most<br />
intermediate metabolic enzymes are acetylated and<br />
that acetylation can directly affect the enzyme activity<br />
or stability. We found that acetylation of<br />
metabolic enzymes changed in response to the<br />
alterations of extracellular nutrient availability, providing<br />
evidence for a physiological role of dynamic<br />
acetylation in metabolic regulation. The<br />
mechanism of acetylation in regulating metabolism<br />
may be conserved during evolution. Many<br />
metabolic enzymes in Escherichia coli are acetylated,<br />
although the functional importance of these<br />
acetylations has not been investigated (11). We<br />
propose that lysine acetylation is an evolutionarily<br />
conserved mechanism involved in regulation of<br />
metabolism in response to nutrient availability<br />
Acetylation of Metabolic Enzymes<br />
Coordinates Carbon Source Utilization<br />
and Metabolic Flux<br />
Qijun Wang, 1 Yakun Zhang, 2 Chen Yang, 3 Hui Xiong, 1,2 Yan Lin, 4 Jun Yao, 4 Hong Li, 3 Lu Xie, 3<br />
Wei Zhao, 3 Yufeng Yao, 5 Zhi-Bin Ning, 3 Rong Zeng, 3 Yue Xiong, 4,6 Kun-Liang Guan, 4,7<br />
Shimin Zhao, 1,4 * Guo-Ping Zhao 1,2,3,8 *<br />
Lysine acetylation regulates many eukaryotic cellular processes, but its function in prokaryotes is largely<br />
unknown. We demonstrated that central metabolism enzymes in Salmonella were acetylated extensively<br />
and differentially in response to different carbon sources, concomitantly with changes in cell growth<br />
and metabolic flux. The relative activities of key enzymes controlling the direction of glycolysis<br />
versus gluconeogenesis and the branching between citrate cycle and glyoxylate bypass were all<br />
regulated by acetylation. This modulation is mainly controlled by a pair of lysine acetyltransferase<br />
and deacetylase, whose expressions are coordinated with growth status. Reversible acetylation of<br />
metabolic enzymes ensure that cells respond environmental changes via promptly sensing cellular<br />
energy status and flexibly altering reaction rates or directions. It represents a metabolic regulatory<br />
mechanism conserved from bacteria to mammals.<br />
P<br />
CORRECTED 21 MAY 2010; SEE LAST PAGE<br />
rotein lysine acetylation regulates wide<br />
range of cellular functions in eukaryotes,<br />
especially transcriptional control in the<br />
nucleus (1, 2). It also plays an extensive role in<br />
regulation of metabolic enzymes through various<br />
mechanisms in human liver (3). In prokaryotes<br />
such as Salmonella enterica, reversible lysine<br />
acetylation is known to regulate the activity of<br />
acetyl–coenzyme A (CoA) synthetase (4). To determine<br />
how lysine acetylation globally regulates<br />
19 FEBRUARY 2010 VOL 327 SCIENCE www.sciencemag.org<br />
and cellular metabolic status. Acetylation may<br />
play a key role in the coordination of different<br />
metabolic pathways in response to extracellular<br />
conditions.<br />
References and Notes<br />
1. X. J. Yang, E. Seto, Mol. Cell 31, 449 (2008).<br />
2. S. C. Kim et al., Mol. Cell 23, 607 (2006).<br />
3. C. Choudhary et al., Science 325, 834 (2009).<br />
4. K. Alvares et al., Cancer Res. 54, 2303 (1994).<br />
5. C. S. Yeh et al., Cancer Lett. 233, 297 (2006).<br />
6. P. A. Watkins et al., J. Clin. Invest. 83, 771<br />
(1989).<br />
7. E. Trevisson et al., Hum. Mutat. 28, 694 (2007).<br />
8. R. L. Jungas, M. L. Halperin, J. T. Brosnan, Physiol. Rev.<br />
72, 419 (1992).<br />
9. H. Lardy, P. E. Hughes, Curr. Top. Cell. Regul. 24, 171<br />
(1984).<br />
10. P. She et al., Mol. Cell. Biol. 20, 6508 (2000).<br />
11. J. Zhang et al., Mol. Cell. Proteomics 8, 215 (2009).<br />
12. We thank members of Fudan MCB laboratory for their<br />
valuable inputs throughout this study and S. Jackson for<br />
reading the manuscript. Supported by the 985 program<br />
from the Chinese Ministry of Education, state key<br />
development programs of basic research of China<br />
(grants 2009CB918401 and 2006CB806700), the<br />
national high technology research and development<br />
program of China (grant 2006AA02A308), Chinese<br />
National Science Foundation grants 30600112 and<br />
30871255, Shanghai key basic research projects<br />
(grants 06JC14086, 07PJ14011, 08JC1400900),<br />
and NIH grants R01GM51586, R01CA108941, and<br />
R01CA65572 (K.L.G., X.C., and Y.X.).<br />
Supporting Online Material<br />
www.sciencemag.org/cgi/content/full/327/5968/1000/DC1<br />
Materials and Methods<br />
Figs. S1 to S3<br />
Tables S1 to S3<br />
References<br />
27 July 2009; accepted 7 January 2010<br />
10.1126/science.1179689<br />
the metabolism in prokaryotes, we determined the<br />
overall acetylation status of S. enterica proteins<br />
under either fermentable glucose-based glycolysis<br />
or under oxidative citrate-based gluconeogenesis.<br />
By immunopurification of acetylated peptides with<br />
antibody to acetyllysine and peptide identification<br />
1 State Key Laboratory of Genetic Engineering, Department of<br />
Microbiology, School of Life Sciences and Institute of<br />
Biomedical Sciences, Fudan University, Shanghai 200032,<br />
China. 2 MOST-Shanghai Laboratory of Disease and Health<br />
Genomics, Chinese National Human Genome Center at<br />
Shanghai, Shanghai 201203, China.<br />
3 Key Laboratory of<br />
Synthetic Biology, Bioinformatics Center and Laboratory of<br />
Systems Biology, Institute of Plant Physiology and Ecology,<br />
Shanghai Institutes for Biological Sciences, Chinese Academy<br />
of Sciences, Shanghai 200032, China. 4 Molecular Cell Biology<br />
Laboratory, Institute of Biomedical Sciences, Fudan University,<br />
Shanghai 200032, China. 5 Laboratory of Human Bacterial<br />
Pathogenesis, Department of Medical Microbiology and<br />
Parasitology, Institute of Medical Sciences, Shanghai Jiao<br />
Tong University School of Medicine, Shanghai 200025, China.<br />
6 Department of Biochemistry and Biophysics and Lineberger<br />
Comprehensive Cancer Center, University of North Carolina at<br />
Chapel Hill, Chapel Hill, NC 27599, USA. 7 Department of<br />
Pharmacology and Moores Cancer Center, University of<br />
California San Diego, La Jolla, CA 92093, USA. 8 Department<br />
of Microbiology and Li Ka Shing Institute of Health Sciences,<br />
The Chinese University of Hong Kong, Prince of Wales<br />
Hospital, Shatin, New Territories, Hong Kong SAR, China.<br />
*To whom correspondence should be addressed. E-mail:<br />
zhaosm@fudan.edu.cn (S.Z.); gpzhao@sibs.ac.cn (G.-P.Z.)<br />
Downloaded from www.sciencemag.org on February 27, 2012<br />
10574–10578 | PNAS | June 28, 2011 | vol. 108 | no. 26 www.pnas.org/cgi/doi/10.1073/pnas.1017882108<br />
44<br />
45
Appendix<br />
SIPPE <strong>REPORT</strong><br />
Research<br />
Downloaded from genome.cshlp.org on September 1, 2010 - Published by Cold Spring Harbor Laboratory Press<br />
Function annotation of the rice transcriptome<br />
at single-nucleotide resolution by RNA-seq<br />
Tingting Lu, 1,4 Guojun Lu, 1,4 Danlin Fan, 1 Chuanrang Zhu, 1 Wei Li, 1 Qiang Zhao, 1,2<br />
Qi Feng, 1 Yan Zhao, 1 Yunli Guo, 1 Wenjun Li, 1 Xuehui Huang, 1 and Bin Han 1,3,5<br />
1 National Center for Gene Research & Institute of Plant Physiology and Ecology, Shanghai Institutes of Biological Sciences, Chinese<br />
Academy of Sciences, Shanghai 200233, China; 2 College of Life Science & Biotechnology, Shanghai Jiaotong University, Shanghai<br />
200240, China; 3 Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing 100029, China<br />
The functional complexity of the rice transcriptome is not yet fully elucidated, despite many studies having reported the<br />
use of DNA microarrays. Next-generation DNA sequencing technologies provide a powerful approach for mapping and<br />
quantifying the transcriptome, termed RNA sequencing (RNA-seq). In this study, we applied RNA-seq to globally sample<br />
transcripts of the cultivated rice Oryza sativa indica and japonica subspecies for resolving the whole-genome transcription<br />
profiles. We identified 15,708 novel transcriptional active regions (nTARs), of which 51.7% have no homolog to public<br />
protein data and >63% are putative single-exon transcripts, which are highly different from protein-coding genes (
Appendix<br />
SIPPE <strong>REPORT</strong><br />
COPLBI-888; NO. OF PAGES 9<br />
Available online at www.sciencedirect.com<br />
The Plant Cell, Vol. 22: 1633–1646, May 2010, www.plantcell.org ã 2010 American Society of Plant Biologists<br />
Signals and mechanisms affecting vesicular trafficking during<br />
root growth<br />
Hong-Yan Yao and Hong-Wei Xue<br />
Vesicular trafficking is mediated by distinct exocytic and<br />
endocytic routes in eukaryotic cells. These pathways involve<br />
RAB family proteins, ADP-ribosylation factor, RHO proteins of<br />
the Ras superfamily, and SNAREs (soluble N-ethylmaleimidesensitive<br />
factor adaptors). Studies have shown that vesicular<br />
trafficking plays a crucial role in protein localization and<br />
movement, signal transduction, and multiple developmental<br />
processes. Here we summarize the role of vesicular trafficking<br />
in root and root hair growth and in auxin-mediated root<br />
development, focusing on the regulation of the polarized<br />
subcellular distribution of the PIN proteins (auxin efflux<br />
carriers).<br />
Address<br />
National Key Laboratory of Plant Molecular Genetics, Shanghai Institute<br />
of Plant Physiology and Ecology, Chinese Academy of Sciences, 300,<br />
Fenglin Road, 200032 Shanghai, China<br />
Corresponding author: Xue, Hong-Wei (hwxue@sibs.ac.cn)<br />
Current Opinion in Plant Biology 2011, 14:1–9<br />
This review comes from a themed issue on<br />
Cell signalling and gene regulation<br />
Edited by Sean Cutler and Christa Testerink<br />
1369-5266/$ – see front matter<br />
# 2011 Elsevier Ltd. All rights reserved.<br />
DOI 10.1016/j.pbi.2011.06.009<br />
Introduction<br />
Vesicular trafficking maintains cellular homeostasis by<br />
delivering newly synthesized proteins from the endoplasmic<br />
reticulum (ER) to the correct destination: for<br />
example, the trans-Golgi network (TGN), for retrograde<br />
transport; the plasma membrane (PM), for recycling by<br />
transport vesicles; or the lysosomes and vacuoles, for<br />
degradation. Vesicular trafficking is also important in<br />
maintaining compartment identity and fidelity in eukaryotic<br />
cells. Furthermore, cell endocytosis and exocytosis<br />
are dependent on vesicular trafficking.<br />
Studies in yeast (Saccharomyces cerevisiae), mammals,<br />
and plants have indicated that regulatory molecules<br />
are required for efficient and accurate vesicular trafficking<br />
[1]. Specifically, the successive steps from the ER to<br />
the Golgi, intra-Golgi, post-Golgi, and endocytic trafficking<br />
are mediated by five gene families [RAS, RHO,<br />
RAB/YPT, ADP-ribosylation factor (ARF), and Rasrelated<br />
nuclear proteins (RAN)] of the Ras superfamily<br />
and the soluble N-ethylmaleimide-sensitive factor<br />
adaptor (SNARE) machinery [2,3]. However, no homologue<br />
of the mammalian RAS has been identified in<br />
plants, whereas RAB, ARF, RHO and RAN GTPases<br />
have been well characterized. Only the RAS and RHO<br />
GTPases are considered to be signaling proteins,<br />
whereas RAB/YPT and ARF are directly involved in<br />
the regulation of vesicular trafficking [3], and RAN has<br />
been implicated in nuclear trafficking [4].<br />
The RAB GTPases function in the regulation of vesicle<br />
formation on donor membranes. These proteins also<br />
direct vesicles to dock on target membranes [5]. The<br />
57 Arabidopsis RAB sequences fall into eight clades<br />
named RAB-A to RAB-H [6]. The RAB11/A and<br />
RAB2/RABB GTPases members have been implicated<br />
in the regulation of tip growth through polarized secretion<br />
of new cell wall components or through control of polar<br />
recycling events during pollen tube growth [7] (Table 1).<br />
RAB5/F2 is involved in endocytosis and is important for<br />
the biosynthetic vacuolar transport pathway [8].<br />
ARF GTPases are major regulators of vesicle biogenesis<br />
[9]. The most studied small GTPase in vesicular trafficking<br />
in tobacco BY-2 cells is ARF1, which controls the<br />
assembly of COPI- and AP1, AP3, and AP4/clathrincoated<br />
vesicles and recruits other proteins to membranes<br />
[10]. ARF1p controls COPI transport and influences the<br />
BP-80-mediated transport route to the lytic vacuole in<br />
tobacco leaf protoplasts [11].<br />
ARF-guanine exchange factors (ARF-GEFs) increase<br />
levels of the active GTP-bound ARF protein, which<br />
are tethered to the membrane by a myristoylated tail.<br />
An Arabidopsis GEF called GNOM (also called EMB30 or<br />
VAN7) was identified as a GBF protein that plays a key<br />
role during embryo development by regulating the endosomal<br />
cycling of the auxin efflux carrier PIN1 [12,13]<br />
(Table 1).<br />
ARF-GTPase-activating proteins (ARF-GAPs) regenerate<br />
the inactive, soluble GDP-bound ARF protein by<br />
stimulating GTP hydrolysis. These ARF-GAPs modulate<br />
intracellular trafficking from multiple sites, including the<br />
Golgi, TGN and the endosome in Arabidopsis [14]. Interactions<br />
of ARF-GAPs with lipids, coat proteins and cargo<br />
receptors promote the efficient loading of cargo into<br />
vesicles and remodeling of the actin cytoskeleton [15].<br />
www.sciencedirect.com Current Opinion in Plant Biology 2011, 14:1–9<br />
The Arabidopsis Nitrate Transporter NRT1.8 Functions in<br />
Nitrate Removal from the Xylem Sap and Mediates<br />
Cadmium Tolerance C W<br />
Jian-Yong Li, a,1 Yan-Lei Fu, a,1 Sharon M. Pike, b Juan Bao, a Wang Tian, c Yu Zhang, a Chun-Zhu Chen, a Yi Zhang, a<br />
Hong-Mei Li, a Jing Huang, a Le-Gong Li, c Julian I. Schroeder, d Walter Gassmann, b and Ji-Ming Gong a,2<br />
a<br />
National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for<br />
Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, People’s Republic of China<br />
b<br />
Division of Plant Sciences, C.S. Bond Life Sciences Center and Interdisciplinary Plant Group, University of Missouri, Columbia,<br />
Missouri 65211-7310<br />
c<br />
College of Life Sciences, Capital Normal University, Beijing 100037, People’s Republic of China<br />
d<br />
Division of Biological Sciences and Center for Molecular Genetics, Cell and Developmental Biology Section, University of<br />
California, San Diego, California 92093-0116<br />
Long-distance transport of nitrate requires xylem loading and unloading, a successive process that determines nitrate<br />
distribution and subsequent assimilation efficiency. Here, we report the functional characterization of NRT1.8, a member of<br />
the nitrate transporter (NRT1) family in Arabidopsis thaliana. NRT1.8 is upregulated by nitrate. Histochemical analysis using<br />
promoter-b-glucuronidase fusions, as well as in situ hybridization, showed that NRT1.8 is expressed predominantly in xylem<br />
parenchyma cells within the vasculature. Transient expression of the NRT1.8:enhanced green fluorescent protein fusion in<br />
onion epidermal cells and Arabidopsis protoplasts indicated that NRT1.8 is plasma membrane localized. Electrophysiological<br />
and nitrate uptake analyses using Xenopus laevis oocytes showed that NRT1.8 mediates low-affinity nitrate uptake.<br />
Functional disruption of NRT1.8 significantly increased the nitrate concentration in xylem sap. These data together suggest<br />
that NRT1.8 functions to remove nitrate from xylem vessels. Interestingly, NRT1.8 was the only nitrate assimilatory pathway<br />
gene that was strongly upregulated by cadmium (Cd 2+ ) stress in roots, and the nrt1.8-1 mutant showed a nitrate-dependent<br />
Cd 2+ -sensitive phenotype. Further analyses showed that Cd 2+ stress increases the proportion of nitrate allocated to wildtype<br />
roots compared with the nrt1.8-1 mutant. These data suggest that NRT1.8-regulated nitrate distribution plays an<br />
important role in Cd 2+ tolerance.<br />
INTRODUCTION<br />
The nitrate assimilation pathway has been extensively studied. It<br />
consists of several steps, beginning with uptake into roots.<br />
Nitrate concentrations in soil vary considerably, mainly as a result<br />
of two microbial processes, mineralization and nitrification, that<br />
are highly sensitive to environmental conditions (Marschner,<br />
1995). To cope with highly variable nitrate concentrations in soil,<br />
plants have developed both a high-affinity transport system<br />
(HATS) and a low-affinity transport system (LATS) (Glass et al.,<br />
1992; Crawford, 1995; Crawford and Glass, 1998; Forde, 2000).<br />
When the external nitrate concentration is high (>1 mM), LATS is<br />
preferentially used. When nitrate availability is limited, HATS is<br />
1<br />
These authors contributed equally to this work.<br />
2<br />
Address correspondence to jmgong@sibs.ac.cn.<br />
The author responsible for distribution of materials integral to the<br />
findings presented in this article in accordance with the policy described<br />
in the Instructions for Authors (www.plantcell.org) is: Ji-Ming Gong<br />
( jmgong@sibs.ac.cn).<br />
C<br />
Some figures in this article are displayed in color online but in black<br />
and white in the print edition.<br />
W<br />
Online version contains Web-only data.<br />
www.plantcell.org/cgi/doi/10.1105/tpc.110.075242<br />
activated and takes over the nitrate uptake process (Glass et al.,<br />
1992; Crawford and Glass, 1998).<br />
To date, two nitrate transporter gene families, NRT1 and<br />
NRT2, were identified as responsible for LATS and HATS,<br />
respectively (Glass et al., 1992; Orsel et al., 2002b; Tsay et al.,<br />
2007). In the Arabidopsis thaliana NRT1 family, the 53 NRT1<br />
(PTR, peptide transporter) members include both nitrate and<br />
oligopeptide transporters. Among the characterized nitrate<br />
transporters, CHLorate resistant 1 (CHL1/NRT1.1) is the most<br />
studied and represents a major low-affinity uptake mechanism<br />
for nitrate (Tsay et al., 1993, 2007). Furthermore, CHL1/NRT1.1<br />
functions as a dual-affinity transporter with regulation by phosphorylation<br />
(Wang et al., 1998; Liu et al., 1999). The NRT2 family<br />
consists of seven members in the Arabidopsis genome. NRT2.1<br />
and NRT2.2 are involved in inducible high-affinity nitrate uptake<br />
(Cerezo et al., 2001; Li et al., 2007). Though functionally and<br />
phylogenetically distinct, the nitrate transport functions of both<br />
NRT1 and NRT2 are believed to be proton dependent (Paulsen<br />
and Skurray, 1994; Orsel et al., 2002a).<br />
Once taken up into the root cytoplasm, nitrate is either translocated<br />
across the tonoplast and stored in the vacuoles, or it is<br />
reduced to nitrite and then partitioned to plastids where it is<br />
further assimilated to organic nitrogen (Orsel et al., 2002a).<br />
Please cite this article in press as: Yao H-Y, Xue H-W. Signals and mechanisms affecting vesicular trafficking during root growth, Curr Opin Plant Biol (2011), doi:10.1016/j.pbi.2011.06.009<br />
48<br />
49
Appendix<br />
SIPPE <strong>REPORT</strong><br />
The Plant Cell, Vol. 22: 2322–2335, July 2010, www.plantcell.org ã 2010 American Society of Plant Biologists<br />
The Plant Cell, Vol. 22: 3726–3744, November 2010, www.plantcell.org ã 2010 American Society of Plant Biologists<br />
Temporal Control of Trichome Distribution by<br />
MicroRNA156-Targeted SPL Genes in Arabidopsis thaliana W OA<br />
Nan Yu, a,b,1 Wen-Juan Cai, a,b,1 Shucai Wang, c Chun-Min Shan, a,b Ling-Jian Wang, a and Xiao-Ya Chen a,2<br />
a<br />
National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for<br />
Biological Sciences, 200032 Shanghai, P.R. China<br />
b<br />
Graduate School of Chinese Academy of Sciences, 200032 Shanghai, P.R. China<br />
c<br />
Department of Botany, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada<br />
Arabidopsis b-Ketoacyl-[Acyl Carrier Protein] Synthase I Is<br />
Crucial for Fatty Acid Synthesis and Plays a Role in<br />
Chloroplast Division and Embryo Development C W OA<br />
Guo-Zhang Wu and Hong-Wei Xue 1<br />
National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for<br />
Biological Science, Chinese Academy of Sciences, 200032 Shanghai, China<br />
The production and distribution of plant trichomes is temporally and spatially regulated. After entering into the flowering<br />
stage, Arabidopsis thaliana plants have progressively reduced numbers of trichomes on the inflorescence stem, and the<br />
floral organs are nearly glabrous. We show here that SQUAMOSA PROMOTER BINDING PROTEIN LIKE (SPL) genes, which<br />
define an endogenous flowering pathway and are targeted by microRNA 156 (miR156), temporally control the trichome<br />
distribution during flowering. Plants overexpressing miR156 developed ectopic trichomes on the stem and floral organs. By<br />
contrast, plants with elevated levels of SPLs produced fewer trichomes. During plant development, the increase in SPL<br />
transcript levels is coordinated with the gradual loss of trichome cells on the stem. The MYB transcription factor genes<br />
TRICHOMELESS1 (TCL1) and TRIPTYCHON (TRY) are negative regulators of trichome development. We show that SPL9<br />
directly activates TCL1 and TRY expression through binding to their promoters and that this activation is independent of<br />
GLABROUS1 (GL1). The phytohormones cytokinin and gibberellin were reported to induce trichome formation on the stem<br />
and inflorescence via the C2H2 transcription factors GIS, GIS2, and ZFP8, which promote GL1 expression. We show that the<br />
GIS-dependent pathway does not affect the regulation of TCL1 and TRY by miR156-targeted SPLs, represented by SPL9.<br />
These results demonstrate that the miR156-regulated SPLs establish a direct link between developmental programming and<br />
trichome distribution.<br />
Lipid metabolism plays a pivotal role in cell structure and in multiple plant developmental processes. b-Ketoacyl-[acyl<br />
carrier protein] synthase I (KASI) catalyzes the elongation of de novo fatty acid (FA) synthesis. Here, we report the functional<br />
characterization of KASI in the regulation of chloroplast division and embryo development. Phenotypic observation of an<br />
Arabidopsis thaliana T-DNA insertion mutant, kasI, revealed multiple morphological defects, including chlorotic (in netted<br />
patches) and curly leaves, reduced fertility, and semidwarfism. There are only one to five enlarged chloroplasts in the<br />
mesophyll cells of chlorotic sectors of young kasI rosette leaves, indicating suppressed chloroplast division under KASI<br />
deficiency. KASI deficiency results in a significant change in the polar lipid composition, which causes the suppressed<br />
expression of FtsZ and Min system genes, disordered Z-ring placement in the oversized chloroplast, and inhibited<br />
polymerization of FtsZ protein at mid-site of the chloroplast in kasI. In addition, KASI deficiency results in disrupted embryo<br />
development before the globular stage and dramatically reduces FA levels (;33.6% of the wild type) in seeds. These results<br />
demonstrate that de novo FA synthesis is crucial and has pleiotropic effects on plant growth. The polar lipid supply is<br />
important for chloroplast division and development, revealing a key function of FA synthesis in plastid development.<br />
INTRODUCTION<br />
1<br />
These authors contributed equally to this work.<br />
2<br />
Address correspondence to xychen@sibs.ac.cn.<br />
The author responsible for distribution of materials integral to the<br />
findings presented in this article in accordance with the policy described<br />
in the Instructions for Authors (www.plantcell.org) is: Xiao-Ya Chen<br />
(xychen@sibs.ac.cn).<br />
W<br />
Online version contains Web-only data.<br />
OA<br />
Open Access articles can be viewed online without a subscription.<br />
www.plantcell.org/cgi/doi/10.1105/tpc.109.072579<br />
Trichomes are specialized epidermal cells that act as barriers to<br />
protect plants from herbivores, UV irradiation, and excessive<br />
transpiration (Johnson, 1975; Mauricio and Rausher, 1997). In<br />
Arabidopsis thaliana, the distribution of trichomes is spatially and<br />
temporally regulated. During the early vegetative phase, trichomes<br />
are evenly distributed on the adaxial side of juvenile<br />
rosette leaves. As trichome production initiates on the abaxial<br />
side of leaves, the plant prepares for the transition from the<br />
vegetative to the reproductive stage (Telfer et al., 1997). After<br />
entering into the reproductive stage, the number of trichomes<br />
produced on the main inflorescence stem is gradually reduced.<br />
Floral organs are nearly glabrous except for a few trichomes<br />
present on the abaxial surface of sepals.<br />
Previous studies of Arabidopsis trichome development have<br />
focused on rosette leaves (Marks, 1997; Hülskamp et al., 1999;<br />
Larkin et al., 2003; Ishida et al., 2008). A series of genes positively<br />
regulating trichome initiation and development have been identified,<br />
including TRANSPARENT TESTA GLABRA1 (TTG1)<br />
(Galway et al., 1994; Walker et al., 1999; Bouyer et al., 2008),<br />
GLABRA1 (GL1) (Oppenheimer et al., 1991), GL3, and EN-<br />
HANCER OF GLABRA3 (EGL3) (Payne et al., 2000; Szymanski<br />
et al., 2000; Zhang et al., 2003). TTG1, GL1, and GL3+EGL3<br />
encode a WD40 protein, an R2R3 MYB transcription factor, and<br />
two basic helix-loop-helix–type transcription factors, respectively,<br />
and they form a ternary complex that initiates trichome cell<br />
development by activating GL2, which encodes a homeodomain/leucine<br />
zipper t ranscription factor (Rerie et al., 1994;<br />
Masucci et al., 1996; Schiefelbein, 2003; Pesch and Hülskamp,<br />
2004; Ramsay and Glover, 2005). Another group of genes<br />
encode the single-repeat R3 MYB factors TRIPTYCHON (TRY),<br />
CAPRICE (CPC), ENHANCER OF TRY AND CPC1 (ETC1), ETC2,<br />
ETC3, and TRICHOMELESS1 (TCL1) (Wada et al., 1997; Esch<br />
et al., 2004; Kirik et al., 2004a, 2004b; Schellmann et al., 2002;<br />
Simon et al., 2007; Wang et al., 2007). They suppress trichome<br />
initiation in a redundant manner, although TRY, TCL1, and CPC<br />
exert a major influence on rosette leaves, inflorescences, and<br />
roots (root hairs), respectively (Wada et al., 1997; Schnittger<br />
et al., 1998; 1999; Schellmann et al., 2002; Wang et al., 2007). It<br />
was suggested that expression of some of the negative regulator<br />
genes, including TRY, CPC, ETC1, and ETC3, was completely or<br />
partially dependent on the GL1-GL3-TTG1 protein complex<br />
(Morohashi et al., 2007), whereas TCL1 and ETC2 were regulated<br />
by yet unidentified mechanisms (Wang et al., 2008b). The singlerepeat<br />
MYB proteins can move from the trichome into neighboring<br />
cells where they compete with GL1 for the binding site of<br />
INTRODUCTION<br />
Studies have demonstrated the crucial roles of fatty acids (FAs) in<br />
plant development, cell signaling, and stress responses. The de<br />
novo biosynthesis of FAs starts with the formation of the direct<br />
substrate malonyl-coenzyme A (CoA), which is catalyzed by<br />
acetyl-CoA carboxylase (Guchhait et al., 1974; Gornicki and<br />
Haselkorn, 1993). As the initiation enzyme of FA chain elongation,<br />
b-ketoacyl-[acyl carrier protein] synthase III (KASIII) is responsible<br />
for the condensation reaction of malonyl-acyl carrier protein<br />
(ACP) and acetyl-ACP (Jackowski and Rock, 1987; Clough et al.,<br />
1992), and KASI and KASII are the condensing enzymes for the<br />
elongation of the carbon chain from C4 to C18. KASI has high<br />
activity when butyryl- to myristyl-ACP (C4:0-C14:0 ACP) is used<br />
as the substrate to produce hexanoyl- to palmitoyl-ACP (C6:0-<br />
C16:0 ACP), whereas KASII mainly uses palmitoyl-ACP as the<br />
substrate to produce stearoyl-ACP (Shimakata and Stumpf,<br />
1982b). After the condensing reaction, the 3-ketoacyl-ACP is<br />
reduced at the carbonyl group by 3-ketoacyl-ACP reductase<br />
(KAR), dehydrated by hydroxyacyl-ACP dehydratase (HAD), and<br />
completed by enoyl-ACP reductase (ENR; which reduces the<br />
1<br />
Address correspondence to hwxue@sibs.ac.cn.<br />
The author responsible for distribution of materials integral to the<br />
findings presented in this article in accordance with the policy described<br />
in the Instructions for Authors (www.plantcell.org) is: Hong-Wei Xue<br />
(hwxue@sibs.ac.cn).<br />
C<br />
Some figures in this article are displayed in color online but in black<br />
and white in the print edition.<br />
W<br />
Online version contains Web-only data.<br />
OA<br />
Open Access articles can be viewed online without a subscription.<br />
www.plantcell.org/cgi/doi/10.1105/tpc.110.075564<br />
trans-2 double bond to form a saturated FA; Mou et al., 2000).<br />
Subsequently, the mature palmitoyl-ACP and stearoyl-ACP participate<br />
in eukaryotic or prokaryotic FA processing pathway.<br />
These 16:0 and 18:0 FAs are involved in multiple biological<br />
processes, including producing glycerolipids and phospholipids<br />
that are important in cell signaling, forming very-long-chain fatty<br />
acids (VLCFAs) for cuticular waxes and plant development or<br />
being converted to plant hormones, such as jasmonic acid, that<br />
participate in stress responses (Ohlrogge and Browse, 1995).<br />
Several Arabidopsis thaliana mutants that are deficient in<br />
different steps of the FA biosynthesis pathway have been identified,<br />
and genetic studies have revealed that FAs participated in<br />
multiple aspects of plant growth (Ohlrogge and Browse, 1995).<br />
An Arabidopsis mutant that has a deficiency in acyl-ACP thioesterases<br />
(FATB) shows dramatically reduced eukaryotic lipids<br />
(lipids species mainly existing outside of the plastid, such as<br />
phosphatidylcholine [PC] and phosphatidylethanolamine [PE]),<br />
and fatb seedlings are semidwarf, exhibit altered morphology,<br />
and produce seeds with low viability (Bonaventure et al., 2003). A<br />
point mutation in the sixth exon of MOD1, which encodes the<br />
ENR in Arabidopsis, causes significantly decreased ENR activity,<br />
defective development of the chloroplast grana, premature<br />
cell death in mesophyll cells, and reduced fertility (Mou et al.,<br />
2000). The VLCFAs have been demonstrated to participate<br />
in many aspects of plant growth, development, and stress<br />
response. Enoyl-CoA reductase has been identified as an important<br />
enzyme that is involved in the synthesis of all VLCFAs. An<br />
enoyl-CoA reductase knockout mutant, cer10, exhibits severe<br />
morphological abnormalities and reduced size of aerial organs,<br />
demonstrating the important roles of VLCFAs in endocytic<br />
50<br />
51
Appendix<br />
SIPPE <strong>REPORT</strong><br />
The Plant Cell, Vol. 23: 661–680, February 2011, www.plantcell.org ã 2011 American Society of Plant Biologists<br />
BENT UPPERMOST INTERNODE1 Encodes the Class II<br />
Formin FH5 Crucial for Actin Organization and<br />
Rice Development W OA<br />
The EMBO Journal (2010) 29, 1916–1927 | & 2010 European Molecular Biology Organization | Some Rights Reserved 0261-4189/10<br />
www.embojournal.org<br />
Rice early flowering1, a CKI, phosphorylates<br />
DELLA protein SLR1 to negatively regulate<br />
gibberellin signalling<br />
THE<br />
EMBO<br />
JOURNAL<br />
EMBO<br />
open<br />
Weibing Yang, a,1 Sulin Ren, b,1 Xiaoming Zhang, c,1 Mingjun Gao, a Shenghai Ye, c Yongbin Qi, c Yiyan Zheng, b<br />
Juan Wang, b Longjun Zeng, a Qun Li, a Shanjin Huang, b,2 and Zuhua He a,2,3<br />
a<br />
National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences,<br />
Shanghai 200032, China<br />
b<br />
Key Laboratory of Photosynthesis and Environmental Molecular Physiology, Institute of Botany, Chinese Academy of<br />
Sciences, Beijing 100093, China<br />
c<br />
State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Zhejiang Academy of Agricultural<br />
Sciences, Hangzhou 310021, China<br />
The actin cytoskeleton is an important regulator of cell expansion and morphogenesis in plants. However, the molecular<br />
mechanisms linking the actin cytoskeleton to these processes remain largely unknown. Here, we report the functional<br />
analysis of rice (Oryza sativa) FH5/BENT UPPERMOST INTERNODE1 (BUI1), which encodes a formin-type actin nucleation<br />
factor and affects cell expansion and plant morphogenesis in rice. The bui1 mutant displayed pleiotropic phenotypes,<br />
including bent uppermost internode, dwarfism, wavy panicle rachis, and enhanced gravitropic response. Cytological<br />
observation indicated that the growth defects of bui1 were caused mainly by inhibition of cell expansion. Map-based cloning<br />
revealed that BUI1 encodes the class II formin FH5. FH5 contains a phosphatase tensin-like domain at its amino terminus<br />
and two highly conserved formin-homology domains, FH1 and FH2. In vitro biochemical analyses indicated that FH5 is<br />
capable of nucleating actin assembly from free or profilin-bound monomeric actin. FH5 also interacts with the barbed end of<br />
actin filaments and prevents the addition and loss of actin subunits from the same end. Interestingly, the FH2 domain of FH5<br />
could bundle actin filaments directly and stabilize actin filaments in vitro. Consistent with these in vitro biochemical<br />
activities of FH5/BUI1, the amount of filamentous actin decreased, and the longitudinal actin cables almost disappeared<br />
in bui1 cells. The FH2 or FH1FH2 domains of FH5 could also bind to and bundle microtubules in vitro. Thus, our study<br />
identified a rice formin protein that regulates de novo actin nucleation and spatial organization of the actin filaments, which<br />
are important for proper cell expansion and rice morphogenesis.<br />
INTRODUCTION<br />
Rice (Oryza sativa) is a major food resource for nearly half of the<br />
world human population. Rice productivity is highly associated<br />
with its architectural pattern, including plant height, which is<br />
attributable mainly to stem internode elongation (Sasaki et al.,<br />
2002; Wang and Li, 2008). The uppermost internode is of<br />
particular importance for rice productivity, since the elongation<br />
of the uppermost internode promotes panicle emergence<br />
(Zhu et al., 2006). The phytohormones gibberellins (GAs) and<br />
brassinosteroids are the two major factors that affect rice<br />
internode length by modulating cell expansion (Wang and Li,<br />
2008). The cytoskeleton, including microtubules and actin<br />
1<br />
These authors contributed equally to this work.<br />
2<br />
These authors contributed equally to this work.<br />
3<br />
Address correspondence to zhhe@sibs.ac.cn.<br />
The authors responsible for distribution of materials integral to the<br />
findings presented in this article in accordance with the policy described<br />
in the Instructions for Authors (www.plantcell.org) are: Shanjin Huang<br />
(sjhuang@ibcas.ac.cn) and Zuhua He (zhhe@sibs.ac.cn).<br />
W<br />
Online version contains Web-only data.<br />
OA<br />
Open Access articles can be viewed online without a subscription.<br />
www.plantcell.org/cgi/doi/10.1105/tpc.110.081802<br />
microfilaments, is also essential for plant development and<br />
morphogenesis by modulation of cell expansion. For example,<br />
loss of function of DWARF AND GLADIUS LEAF1, which<br />
encodes an ATPase katanin-like protein in rice, caused disorganization<br />
of microtubule arrays and inhibited cell elongation,<br />
resulting in a dwarf phenotype (Komorisono et al., 2005).<br />
However, the information about the functions of the actin cytoskeleton<br />
in cell elongation and rice morphogenesis is rather<br />
limited.<br />
Pharmacological perturbation of actin organization indicates<br />
that the actin cytoskeleton is a major regulator of cell elongation<br />
in Arabidopsis thaliana and other plant species (Baluska et al.,<br />
2001; Collings et al., 2006). Simultaneous downregulation of<br />
ACTIN2 and ACTIN7 reduced cell elongation in Arabidopsis<br />
hypocotyls (Kandasamy et al., 2009). Misexpression of actin<br />
regulatory proteins, such as profilin and actin-depolymerizing<br />
factors, also perturbs cell elongation (Ramachandran et al.,<br />
2000; Dong et al., 2001; Kandasamy et al., 2009). In addition,<br />
the actin cytoskeleton plays pivotal roles in polar cell expansion<br />
and the establishment of cell division planes by governing<br />
cytoplasmic streaming, organelle movement, and vesicle transport<br />
(Martin et al., 2001; Staiger and Blanchoin, 2006). However,<br />
This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits<br />
distribution, and reproduction in any medium, provided the original authorand source are credited. This license does not<br />
permit commercial exploitation or the creation of derivative works without specific permission.<br />
Cheng Dai and Hong-Wei Xue*<br />
National Key Laboratory of Plant Molecular Genetics, Institute of Plant<br />
Physiology and Ecology, Shanghai Institutes for Biological Sciences,<br />
Chinese Academy of Sciences, Shanghai, PR China<br />
The plant hormone gibberellin (GA) is crucial for multiple<br />
aspects of plant growth and development. To study the<br />
relevant regulatory mechanisms, we isolated a rice mutant<br />
earlier flowering1, el1, which is deficient in a casein<br />
kinase I that has critical roles in both plants and animals.<br />
el1 had an enhanced GA response, consistent with the<br />
suppression of EL1 expression by exogenous GA 3 .<br />
Biochemical characterization showed that EL1 specifically<br />
phosphorylates the rice DELLA protein SLR1, proving a<br />
direct evidence for SLR1 phosphorylation. Overexpression<br />
of SLR1 in wild-type plants caused a severe dwarf phenotype,<br />
which was significantly suppressed by EL1 deficiency,<br />
indicating the negative effect of SLR1 on GA<br />
signalling requires the EL1 function. Further studies<br />
showed that the phosphorylation of SLR1 is important<br />
for maintaining its activity and stability, and mutation of<br />
the candidate phosphorylation site of SLR1 results in the<br />
altered GA signalling. This study shows EL1 a novel and<br />
key regulator of the GA response and provided important<br />
clues on casein kinase I activities in GA signalling and<br />
plant development.<br />
The EMBO Journal (2010) 29, 1916–1927. doi:10.1038/<br />
emboj.2010.75; Published online 16 April 2010<br />
Subject Categories: genome stability & dynamics; plant<br />
biology<br />
Keywords: casein kinase I; EL1; flowering time; GA<br />
response; rice<br />
Introduction<br />
The switch from vegetative to reproductive growth is a<br />
critical event in the life cycle of flowering plants and is<br />
essential for their maximum reproductive success (Bernier,<br />
1988). In Arabidopsis, a model plant for eudicots, four major<br />
pathways are involved in the control of flowering time: the<br />
*Corresponding author. National Key Laboratory of Plant Molecular<br />
Genetics, Shanghai Institute of Plant Physiology and Ecology, Chinese<br />
Academy of Sciences, 300 Fenglin Road, 200032 Shanghai, PR China.<br />
Tel.: þ 86 21 54924059; Fax: þ 86 21 54924060;<br />
E-mail: hwxue@sibs.ac.cn<br />
Received: 11 February 2010; accepted: 26 March 2010; published<br />
online: 16 April 2010<br />
photoperiod, autonomous, vernalization, and gibberellin<br />
(GA) pathways. In contrast to Arabidopsis, rice is a shortday<br />
plant. Several rice genes in the photoperiod pathway<br />
controlling heading date (Hd) (flowering time) have been<br />
genetically characterized, including Se1 (photoperiod sensitivity<br />
1; Yokoo et al, 1980; Yamagata et al, 1986), Se3–Se7<br />
(Yamagata et al, 1986; Poonyarit et al, 1989; Sano, 1992;<br />
Yokoo and Okuno, 1993), and E1–E3 (Hd 1–3, Tsai, 1995;<br />
Kinoshita, 1998). Some rice genes encode proteins similar to<br />
those in the Arabidopsis long-day pathway. Specifically, the<br />
products of Hd 1, 3a, and 6 are homologous to Arabidopsis<br />
CO (Yano et al, 2000), FT (FLOWERING LOCUS T, Kojima<br />
et al, 2002), and a subunit of kinase CK2 (a regulator of<br />
circadian rhythm and flowering time, Takahashi et al, 2001),<br />
respectively. In addition, rice phytochromes are also involved<br />
in the regulation of flowering time in response to day length<br />
(Izawa et al, 2000). Similar to Arabidopsis, circadian-regulated<br />
OsGI expression in transgenic rice has striking effects on<br />
flowering time (Hayama et al, 2003).<br />
Arabidopsis mutants defective in GA biosynthesis or<br />
signalling show severe delayed flowering (Moon et al, 2003;<br />
Yu et al, 2004); however, the role of GA in rice flowering is less<br />
clear. Biochemical and genetic studies have characterized key<br />
components, especially DELLA proteins, in the GA signalling<br />
cascade in both Arabidopsis (Peng et al, 1997; Dill and Sun,<br />
2001; Lee et al, 2002; Hussain et al, 2005) and rice (Ikeda et al,<br />
2001). The Arabidopsis DELLA proteins GAI, RGA, and RGL1<br />
negatively regulate flowering time in the absence of GA<br />
(Mouradov et al, 2002). Recently, the GA receptor GID1 was<br />
identified in Arabidopsis (Griffiths et al, 2006; Nakajima et al,<br />
2006) and rice (Ueguchi-Tanaka et al, 2005), and found<br />
to interact with DELLA proteins (GAI, RGA, or SLR1) in a<br />
GA-dependent manner both in vitro and in vivo (Willige et al,<br />
2007; Ueguchi-Tanaka et al, 2007a, b). The GA–GID1–SLR1<br />
complex is targeted for ubiquitination by SCF GID2 , an F-box<br />
protein, and degraded by the ubiquitin-dependent proteasome<br />
pathway (Sasaki et al, 2003; Gomi et al, 2004; Ueguchi-Tanaka<br />
et al, 2005, 2007a, b), which in turn results in the activated<br />
GA response.<br />
Casein kinase I, a serine/threonine protein kinase, is a<br />
multifunctional protein kinase detected in most eukaryotic<br />
cells (Gross and Anderson, 1998). In mammalian cells, there<br />
are five isoforms of casein kinase I: a, b, g, d, and e (Fish et al,<br />
1995). They are involved in multiple signalling pathways,<br />
including vesicular trafficking (Panek et al, 1997; Murakami<br />
et al, 1999), growth and morphogenesis (Robinson et al,<br />
1993), circadian rhythm (Kloss et al, 1998; Peters et al,<br />
1999), DNA-repair (Dhillon and Hoekstra, 1994), and cell<br />
cycle progression, and cytokinesis (Behrend et al, 2000).<br />
Previous studies showed that CKI regulates BR signalling<br />
1916 The EMBO Journal VOL 29 | NO 11 | 2010 & 2010 European Molecular Biology Organization<br />
52<br />
53
Appendix<br />
SIPPE <strong>REPORT</strong><br />
Committee<br />
Advisory Committee<br />
XiaoYa Chen MengMin Hong HongXuan Lin ShanJiong Shen<br />
YunGang Shen JiaoNai Shi ZhiHong Xu WenYing Yin<br />
GuoPing Zhao<br />
Academic Committee<br />
Chair: GuoPing Zhao<br />
Vice-Chair: ZuHua He YongPing Huang HongWei Xue ChengShu Wang<br />
Members: XiaoYa Chen Bin Han YuKe He Hai Huang<br />
Secretary: LaiGeng Li<br />
JiRong Huang WeiHong Jiang LaiGeng Li Xuan Li<br />
HongXuan Lin ZhongJun Qin QiGuang Wen ZhenBiao Yang<br />
Academic Degree Committee<br />
Chair: QiGuang Wen<br />
JiaMin Fang<br />
Members: WeiMing Cai JiMing Gong FangQing Guo Bin Han<br />
YuKe He ZuHua He Hai Huang JiRong Huang<br />
YongPing Huang WeiHong Jiang LaiGeng Li HongXuan Lin<br />
HuaLing Mi ZhongJun Qin WeiHua Tang ChengShuWang<br />
HongWei Xue<br />
Academic Committee of National Key Laboratory of Plant Molecular Genetics<br />
Chair: ZhiHong Xu<br />
Vice-Chair: Bin Han<br />
Hong Ma<br />
Members: XiaoYa Chen Chong Kong Yan Guo Hongxuan Lin<br />
YaoGuang Liu Qian Qian LiJia Qu JianMin Wan<br />
DaoXin Xie HongWei Xue YongBiao Xue zhenBiao Yang<br />
DaBing Zhang<br />
Academic Committee of Key Laboratory of Synthetic Biology<br />
Chair: ShengLi Yang<br />
Members: ZiXin Deng GuoPing Zhao LuHua Lai Li Huang<br />
HaiYan Liu JiaRui Wu SiLiang Zhang DaiJie Chen<br />
Lei Wang ZhiHao Sun YiXue Li Wen Liu<br />
WeiHong Jiang<br />
HongWei Xue<br />
Academic Committee of Key Laboratory of Insect Developmental and Evolutionary<br />
Biology<br />
Chair: Le Kang<br />
Members: KongMing Wu WenYing Yin GuoPing Zhao WenJun Bu<br />
JiaAn Chen FangQing Guo ZhaoJun Han WeiHua Xu<br />
XiaoFan Zhao ZhangWu Zhao<br />
54<br />
55
Appendix<br />
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