An overview of viruses infecting Dioscorea yams in ... - ResearchGate

Plant virology in sub-Saharan AfricaAn overview of viruses infecting Dioscorea yamsin sub-Saharan AfricaL. Kenyon a , S.A. Shoyinka b , J.d’A. Hughes c , and B.O. Odu caNatural Resources Institute, Central Avenue, Chatham, Kent, ME4 4TB, UKbInstitute of Agricultural Research and Training, Obafemi Awolowo UniversityMoor Plantation, Ibadan, NigeriacInternational Institute of Tropical Agriculture, c/o L.W. Lambourn and Co., 26 Dingwall Road,Croydon CR9 3EE, UKAbstractViruses of the genera Potyvirus, Potexvirus, Badnavirus, Cucumovirus, and Carlavirusinfect yams of different species worldwide. These viruses cause a range of symptomsincluding mosaics, mottle, vein clearing, chlorosis, stunting, and distortion. These leadto a chronic and sometimes severe disease situation in all yam growing areas.In sub-Saharan Africa, where more than 90% of the world’s yams are produced, Yammosaic virus (YMV), genus Potyvirus is an ubiquitous pathogen. It is the only wellcharacterizedvirus infecting yams. Other viruses infecting yams in sub-Saharan Africaare Dioscorea alata virus (DAV), genus Potyvirus; Dioscorea alata bacilliform virus(DaBV), genus Badnavirus; Cucumber mosaic virus (CMV), genus Cucumovirus; andDioscorea dumetorum virus (DdV), genus Potyvirus. Dioscorea mottle virus (DMoV),a possible member of the genus Comovirus, was recently isolated from Dioscoreaalata in Nigeria.Transmission studies show that YMV, DAV, DaBV, and CMV are mechanicallytransmissible between yam plants. All these viruses are transmitted by aphids, exceptDaBV, which is transmitted by mealybugs (Planococcus citri). Although tuber yieldlosses have been attributed to virus infection, the influence of these viruses on yieldand growth of the yam plant has not been well studied. Tremendous improvement hasbeen achieved in the detection of yam viruses with the development of highly sensitiveand more specific diagnostic techniques such as enzyme-linked immunosorbent assays(ELISA), immunosorbent electron microscopy (ISEM), and polymerase chain reaction(PCR). The reliability of these diagnostic tools has enabled the production of virus-testedin-vitro germplasm which can be safely distributed internationally.432

An overview of viruses infecting Dioscorea yamsRésuméLes virus des genres Potyvirus, Potexvirus, Badnavirus, Cucumovirus et Carlaviruss’attaquent à différentes espèces d’igname de par le monde. Ils sont responsables dedivers symptômes dont la mosaïque, la marbrure, l’éclaircissement des nervures, lachlorose, le rabougrissement et la déformation. Ceux-ci sont à l’origine d’affectionschroniques, voire graves dans toutes les zones de culture d’igname.En Afrique subsaharienne où plus de 90% des ignames du monde sont produites, levirus de la mosaïque de l’igname, YMV du genre potyvirus est un pathogène omniprésent.C’est le seul virus de l’igname qui ait été bien caractérisé. Les autres virusqui infectent l’igname en Afrique subsaharienne sont : le virus de Dioscorea alata(DAV), du genre Potyvirus; le virus bacilliforme de Dioscorea alata (DaBV), du genreBadnavirus; le virus de la mosaïque du concombre (CMV), du genre Cucumovirus etle virus de Dioscorea dumetorum (DdV), du genre Potyvirus. Le virus de la marbrurede Dioscorea (DMoV), membre possible du genre Comovirus, fut récemment isolé deDioscorea alata au Nigeria.Des études conduites sur la transmission de ces virus montrent que YMV, DAV, DaBV,et CMV se transmettent de façon mécanique d’un pied d’igname à un autre. Tous lesvirus sont transmis par des pucerons, sauf le DaBV qui est transmis par les cochenilles(Planococcus citri). Bien que les pertes de rendement en tubercules soient attribuéesaux viroses, l’impact de ces virus sur le rendement et le développement de l’igname n’apas encore fait l’objet d’une étude approfondie. Des améliorations considérables ont étéobtenues dans la détection des virus de l’igname avec la mise au point de techniquesde diagnostic très sensibles et plus spécifiques telles que l’essai par l’immunosorbantlié à une enzyme (ELISA), la microscopie électronique immunosorbante (ISEM), et laréaction en chaîne polymérase (PCR). Très fiables, ces outils de diagnostic ont permisla production de matériel végétal in vitro, testé contre les virus et pouvant être distribuésans risque à l’échelle internationale.IntroductionYams are the starchy tubers produced by various Dioscorea species (Dioscoreaceae).They are a traditional crop and an important staple food over much of sub-SaharanAfrica. Of the 600 or so species of Dioscorea recognized, only about 10 species aregrown for food in different tropical and subtropical parts of the world. About 30 otherspecies are grown on a small-scale for extraction of the pharmaceutical compoundsdioscorin and diosgenin. Species of Dioscorea are native to a wide range of tropicaland subtropical ecologies from semiarid scrub land to tropical rain forests. Most areclimbing vines found in tropical forests and forest margins. Approximately 95% of all433

Plant virology in sub-Saharan Africafood yam production occurs in the equatorial “yam-belt” of sub-Saharan Africa, withabout three quarters of this being confined to the south and central states of Nigeria.The preferred yam species in West Africa is the white yam (D. rotundata) since thisgenerally produces tubers with a high dry-matter content that is good for pounding.This is thought to be a tetraploid (2n = 40) which resulted from hybridization betweenweedy species (Dumont and Vernier 2000). Some authorities regard the yellow yamas a separate species (D. cayenensis), while others group it with the white yam inthe D. rotundata–cayenensis complex. There is some evidence that domesticationof this species (complex) is an ongoing process since in some countries (e.g., BeninRepublic), there appears to be a replenishment of the germplasm of cultivated typesby the collection of wild types from forests (Berthaud et al. 2001).Water yam (D. alata, native to southeast Asia) is gaining popularity in sub-SaharanAfrica because it is easier to propagate than the native white yam. However, it is lessacceptable to many consumers because of the higher water content of the tubers, whichmeans it cannot be pounded to produce fufu of the right consistency. Other species grown(or sometimes harvested from the wild) for other culinary uses in West Africa includethe aerial yam (D. bulbifera) and the bitter yam (D. dumetorum).Most of the edible yam species are relatively infertile and if or when they do set trueseed, most seed is not viable. Thus, most propagation and multiplication of yam is byvegetative means through the planting of small tubers (seed yams) or pieces of tuber(setts). This vegetative propagation allows the perpetuation and accumulation of somediseases, including those caused by viruses. The planting of smaller tubers saved fromthe previous harvest may in effect be selection of the most infected lines.There is a desire for increased international movement and exchange of yamgermplasm to facilitate selection and breeding for improved genotypes adapted tolocal conditions and uses. However, the presence of any virus in the vegetative plantingmaterial poses a great risk as new viruses or strains may be distributed to new siteswhere their effects on tuber yield or quality may be catastrophic. There is thus the needto develop sensitive and robust methods for detecting and diagnosing yam-infectingviruses that can be used to prevent the international movement of these viruses.Virus species from at least six different genera identified infecting yam in differentparts of the world have been characterized to a greater or lesser extent (Table 1). Thevirus species most commonly encountered in yam in sub-Saharan Africa are Yam mosaicpotyvirus, Dioscorea alata potyvirus, and the badnaviruses.434

Table 1. Identifi ed virus species infecting Dioscorea yams.Virus Reported geographical distribution Susceptible Dioscorea spp. Antiserum435Chinese yam necrotic mosaic virus (ChYNMV),genus Macluravirus (?) Asia (JP) D. batatasSynonym: Naga-Imo virus D. batatas, f. typicaCucumber mosaic virus (CMV), genus Cucumovirus Africa (CI, NG) D. alataD. trifi da Dioscorea alata badnavirus (DaBV), genus Badnavirus Africa (BJ, GH, NG, TG), Asia (JP) D. alata, D. dumetorum Caribbean (BB, GD)D. nummularia, D. oppositaPacifi c (PG, VU)D. pentaphylla, D. trifi daSouth America (BR, GY) D. rotundata–cayenensis Dioscorea alata virus (DAV), genus Potyvirus Africa (BJ, CM, GH, GN, NG) D. alata Synonyms: Yam virus I (YVI) Asia (ID, LK) Caribbean (BB, PR) D. esculentaYam mild mosaic virus (YMMV)Pacifi c (PG, SB, VU)Dioscorea bulbifera badnavirus (DbBV), genusAfrica (NG, GH)Badnavirus Caribbean (PR) D. bulbifera Dioscorea dumetorum virus (DDV), genus (?)Potyvirus Africa (NG) D. alataAsia (BD, LK) D. dumetorum Dioscorea esculenta virus (DEV), genus (?)Potyvirus Asia (LK) D. esculentaDioscorea latent virus (DLV), genus Potexvirus Caribbean (PR) D. bulbifera, D. composita Pacifi c (VU)D. fl oribunda, D. nummulariaDioscorea mottle virus (DMoV), genus (?)Comovirus Africa (NG) D. alataSyn: Dioscorea mild chlorosis virusDioscorea trifi da virus (DTV), genus (?)Potyvirus Caribbean (GP) D. alata, D. rotundata–cayenensisD. trifi daJapanese yam mosaic virus (JYMV), genus Potyvirus Asia (JP) D. japonica Yam internal brown spot virus (IBSV), genus (?) Caribbean (BB) D. alataBadnavirus D. rotundata–cayenensis?Yam mosaic virus (YMV), genus Potyvirus Africa (BJ, CM, CI, GH, NG, TG) D. alata, D. dumetorumSynonyms: Dioscorea rotundata potyvirus (DRPV) Asia (ID, MY, PH) D. esculentaDioscorea green-banding mosaic potyvirus (DGMV) Caribbean (BB, GP, PR) D. praehensilisPacifi c (PG, SB) South America (GY) D. preussii, D. rotundata–cayenensis An overview of viruses infecting Dioscorea yams

Plant virology in sub-Saharan AfricaGenus Potyvirus, family PotyviridaeYam mosaic virus (YMV)Yam mosaic virus (YMV) is one of the most important viruses infecting yams in sub-Saharan Africa. It was first isolated and characterized in the Côte d’Ivoire by Thouveneland Fauquet (1979), and has since been detected throughout the yam growing regionsof Africa (Goudou-Urbino et al. 1996), the Caribbean, and the Pacific. Potyviruses areflexuous rods 650–900 nm in length and with a single stranded RNA genome of 9–12kbp. Typical symptoms of YMV are mosaic, green-vein banding, green spotting orflecking, blistering and leaf mottling, vein yellowing, and leaf deformation (curling).YMV can be transmitted in a nonpersistent manner by a wide range of aphid species.It can also be mechanically transmitted in sap, though the main means of spread isprobably in infected planting material. Thus, the main method of control is to useclean planting material collected from uninfected plants. Some resistance to YMV hasbeen identified in some breeding lines of D. rotundata and attempts are being made toincorporate this into more agronomically useful varieties. Monoclonal and polyclonalantisera are available for use in ELISA, and RT-PCR using specific YMV primers hasbeen shown to be reliable for testing for the virus. Nicotiana benthamiana is a goodtest plant for YMV.Dioscorea alata virus (DAV)Dioscorea alata virus (DAV) (= yam virus I, YVI) probably occurs in all areas wherewater yam is grown. Symptoms in water yam range from very mild chlorosis throughleaf mosaic to severe stunting, though the most common symptom is a mild mosaic. Thishas led some authors to name the virus Yam mild mosaic virus (YMMV). Sequencingpart of the genome of potyviruses from yam suggests that there are two related cladesof DAV, one from Africa and the other from southeast Asia, but that isolates from boththese clades have been found infecting other Dioscorea species as well as D. alata. Sofar, it has proved impossible to transmit DAV mechanically by sap inoculation, thoughseveral aphid species are efficient vectors (Odu et al. 2001). Polyclonal antisera andDAV-specific PCR primers are available for detection of DAV.Other PotyviridaeSequence analysis of part of the genome of the potyviruses isolated from yam indicatesthat as well as YMV and DAV, there are several other distinct potyviruses that infectyam. These include Dioscorea esculenta virus (DEV), Dioscorea dumetorum virus(DDV), Dioscorea trifida virus (DTV), and Japanese yam mosaic virus (JYMV), each436

An overview of viruses infecting Dioscorea yamsnamed after the host species where they are most commonly detected. Chinese yamnecrotic mosaic virus (ChYNMV) from Japan has recently been shown to be in thegenus Macluravirus of the Potyviridae. Details of the geographical distributions, hostrange, symptoms, and transmission characteristics of each of these remain sparse.Genus Badnavirus, family CaulimoviridaeThe badnaviruses are a genetically and serologically diverse genera of virus havingbacilliform particles of 25–30 × 120 nm and a circular double stranded DNA genomeof 7.3–8.3 kbp. Several bacilliform viruses have been associated with yam disease. Inthe Caribbean, a bacilliform virus was associated with internal brown spot disease.Dioscorea alata badnavirus (DaBV) and the serologically related Dioscorea bulbiferabadnavirus (DbBV) have been detected in a range of yam species from West Africa usingspecific antisera. It was also demonstrated that they can be mechanically transmittedfrom partially purified samples and also in a semipersistent manner by some mealybugspecies including the citrus mealybug Planococcus citri. Sequencing and phylogeneticanalysis of part of the genome of badnaviruses isolated from yam indicates that awide range of genetically diverse strains or quasi-species of Badnavirus infects yamin different parts of the world. Symptoms of badnavirus infection in yam depend onthe virus strain, host genotype, and environmental conditions and can range from nosymptoms to severe chlorosis and leaf distortion and curling.Cucumber mosaic virus genus CucumovirusCucumber mosaic virus (CMV), genus Cucumovirus, is a species with several serologicallyand genetically distinct strains or subspecies. The virus particles are isometricand about 30 nm in diameter. The species as a whole has a very wide host range, butthere tends to be some specialization within strains or subspecies. CMV infectionsof yam tend to be sporadic, suggesting they arise from a chance encounter betweena viruliferous vector and the yam plant. However occasionally, CMV incidence inyam can be high locally. Strains of CMV have been reported infecting D. alata, D.trifi da, and D. rotundata in West Africa, the Caribbean, South America, and the SouthPacific (Migliori and Cadilhac 1976). Typically, CMV infection of yam causes severeleaf chlorosis and mosaic symptoms; it may also cause leaf distortions and stunting.CMV is efficiently transmitted in nature in a nonpersistent manner by a wide rangeof aphid species. Experimentally, it is mechanically transmitted to a wide range ofindicator plants. Mechanical transmission of CMV produces chlorotic local lesions onChenopodium amaranticolor and C. quinoa, systemic mosaic symptoms on Cucumissativus and necrotic local lesions on Vigna unguiculata. Numerous different more orless strain-specific antisera are available for use in ELISA.437

Plant virology in sub-Saharan AfricaDioscorea latent virus genus PotexvirusDioscorea latent virus (DLV) is the only member of the Potexvirus genus known to infectyams. It is known to spread in Puerto Rico and causes no symptoms in D. compositaor D. fl oribunda (Lawson et al. 1973). It can be transmitted mechanically to variousherbaceous indicator species such as N. benthamiana and N. megalosiphon, again causingsymptomless infection. DLV is often found in association with DAV, and detectionis usually by ELISA using polyclonal antiserum.Dioscorea mottle virus genus ComovirusDioscorea mottle virus (DMoV) belongs to the genus Comovirus having particles thatare isometric, 20–30 nm in diameter, and a bipartite genome of single stranded RNA.DMoV has been found infecting D. alata in Nigeria, and is likely to be distributedacross West Africa. Symptoms in D. alata include mild chlorosis (mild chlorosisstrain), mottling (mottle strain), and necrosis (necrosis strain). DMoV is mechanicallytransmissible from D. alata, and the natural vector is thought to be a beetle. DMoV canbe mechanically transmitted to the indicator plants Vigna unguiculata, Glycine max,Chenopodium murale, C. amaranticolor, and C. quinoa. Antisera are being developedfor use in diagnosis.ConclusionWith the great range of virus species and strains that commonly affect yams, and thefinding that nutrient or trace element deficiencies can mimic or enhance the symptomscaused by virus infections, it has up to now been extremely difficult to assess how muchdamage in terms of the yield or quality reduction infection by a specific virus can cause.Multiple infections with different species or strains of virus are also relatively common.Generally, the effect of the mixture is greater than that of the strains/species alone. Thus,it is important not to move viruses between different regions so as to avoid the risk ofcreating even more devastating mixtures. Since most of the spread of these viruses isfrom one generation and season to the next through the vegetative propagation of theyams, one of the main methods to limit the spread is to ensure that only virus-testedplanting materials are used. These can be plantlets derived directly from tissue culture orfrom mini-tubers produced in vector-proof conditions. If virus-tested planting materialsare not available, farmers should ensure that their planting setts are derived from parentmaterial that at least looked healthy during the growing season.ReferencesBerthaud, J., M. Bousalem, O. Daïnau, J. Dubern, B. Malaurie, and S. Tostain. 2001. Can yamdomestication and participatory breeding be new ways to improve this crop and conserve its438

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