Vol.12_No.2 - Pesticide Alternatives Lab - Michigan State University

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Spring 2003 Resistant Pest Management Newsletter Vol. 12, No.2development (Georghiou & Taylor 1977) and thetheoretical potential for spraying crops with extremelyhigh doses of one or more insecticides has beendiscussed often (Roush 1989, Tabashnik & Croft1982). The "high-dose refuge" strategy is the mostwidely used and has been implemented in NorthAmerica (Alstad & Andow 1995). When an insecticidespray kills 95% of the susceptible (SS) individuals, thesurvival of RS individuals is likely to be significantlyhigher, unless the alleles governing resistance happento be phenotypically recessive (i.e, the RS and SSinsects are physiologically identical). Instead of hopingthat resistance is phenotypically recessive, the highdose approach attempts to make resistance alleles"effectively recessive" even if they are notphenotypically recessive (Gould 1998). Similarly, dosethat is insufficient to kill the insects bearing one copyof a major resistance allele renders resistancefunctionally partially dominant. Hence, the onlycommercially available approach to reduce thelikelihood of resistance development is the use of ahigh dose of a single gene, producing 25 times thetoxin concentration needed to kill susceptible insects incombination with a refuge.High concentrations of Cry1Ac in bolls oftransgenic cotton are essential for achievingfunctionally recessive inheritance of resistance (Liu etal. 2001). Further, extensive planting of transgenic cornhybrids having sub-optimal production of the toxin andresulting in only moderate effects on H. zea wouldraise concerns about the rapid evolution of resistance(Storer et al. 2001). If transgenic plants could be madeto express enough toxins to overcome all homozygousresistance alleles, the crop in question would become anon-host. The lack of a "high dose" in current Bt cottoncultivars for H. armigera and the small scaleproduction systems of cotton indicates that the "highdose/refuge" resistance management strategy is notfeasible for Bt cotton in northern China (Zhao et al.2000a). Under these circumstances, supplementalcontrol of H. armigera with insecticides is essential togrow Bt cotton for a longer period (Ru et al. 2002).Resistance in insects to Bt can be dramatically reducedthrough the genetic engineering of chloroplasts inplants. Several copies of the Bt genes could beexpressed per cell via the chloroplast genome asopposed to only two copies via the nuclear genome in adiploid cell. The Cry2Aa2 protoxin levels inchloroplast-transformed tobacco leaves are between 2to 3% of total soluble protein, and are 20-to-30-foldhigher than current commercial transgenic plants (Kotaet al. 1999). If a toxin is consistently produced by aplant at a highly toxic concentration without having anegative effect on yield, and the toxin does not affectnon-target organisms, then the constraints on high dosestrategy would be quite low.Another serious concern regarding the success ofhigh dose strategy is that the hypothesis of resistancebeing recessive does not hold in different insectspecies. Inheritance of resistance showed incompletedominance in O. nubilalis to a commercial preparationof Bt (Huang et al. 1999), and in H. virescens toCry1Ab (Sims & Stone 1991). While, Tabashnik etal.(1998) demonstrated dominant resistance to Cry1Aain a strain of P. xylostella having field-evolved Btresistance.CONTROLLED EXPRESSION of TOXINS Mono-cultivationof Bt transgenic crops is likely to select intensely forresistance because pests will be exposed to Bt evenwhen they are not causing economic damage (Mallet &Porter 1992). The degree of yield reduction caused by apest population is dependent on its density, as well ason when and where insects feed on the plants.Expression of toxin coding genes could be limited tovulnerable plant parts, and at times when toxicity isneeded most. If a pest causes no damage when it feedson mature leaves, but causes severe stunting when itfeeds on buds and developing leaves, then toxinproduction only in buds would be useful. Having Btexpressed in plants so that the insect population issubjected to selection pressure for particular periods oftime (e.g., through an inducible promoter) or inparticular plant parts (e.g., through tissue-specificpromoters) may provide larger refuges for susceptiblealleles both within the field and within a region whileat the same time minimizing the crop loss (Roush1997b). This can be achieved by using gene constructshaving a tissue specific promoter.In P. xylostella, resistance to Bt declined whenexposure to insecticide ceased (mean R = -0.19). Infour other pests (H. virescens, L. decemlineata, Muscadomestica and P. interpunctella), resistance to Btdeclined slowly or not at all (mean R = -0.02) in theabsence of exposure to Bt (Tabashnik et al. 1994 ).Similar loss of resistance in O. nubilalis was observedin the absence of selection pressure (Bolin et al. 1999).This can be exploited for formulating resistancemanagement strategies by enforcing completerestriction on cultivation of certain Bt cultivars for aspecified period.Solutions to resistance management involvecomplex strategies. The track record of resistancemanagement for chemical pesticides is notencouraging. The wisdom gained from previouspesticide failures should provide impetus for theproactive development and implementation ofmanagement strategies for transgenic crops. Keepingthis in view, Cohen (2000) made four practicalrecommendations for promoting the sustainable use ofBt crops, based on existing knowledge of the principlesof resistance management:22
Spring 2003 Resistant Pest Management Newsletter Vol. 12, No.2Do not release Bt varieties that do not have a highdose of toxin. Toxin titers of 2 µg/g of leaf freshweight or 0.2 % of soluble leaf protein have beenshown to act as high doses against most insectpests of crops.Release only Bt cultivars that have two Bt toxingenes, which are not closely related to each other,and both should be expressed at a high dose.Do not release Bt-transformed versions of allpopular crop varieties. Some popular non-Btvarieties should remain available to improvechances that some non-Bt fields (refuges) willexist.Implement resistance monitoring programs toserve as an early warning system for governmentsand farmers and provide valuable information forimproved deployment of future pest-resistantcultivars.However, the farm-level implementation ofresistance management will face practical and socialobstacles. A survey conducted by US maize growershas shown that in the year 2000, almost 30% of thefarmers failed to comply with the refuge protocolsdesigned to prevent or delay the emergence of insectsresistant to Bt toxins (Dove 2001). Ensuring effectiveresistance management practices is a challenge thatwill require coordination from all sectors (public andprivate) concerned with crop protection, and willrequire the commitment of growers and advisers thatcurrent technology for crop protection is a preciousresource vital to profitable production. There is acontinuing need for interaction between ecologists,geneticists, and plant breeders in determining systemwideimpacts and devising optimal ways of deployinginsect-resistant crops. The current state of knowledge isnot sufficient to support any single proven resistancemanagement strategy that may be recommended as ageneral approach to avoid resistance to transgenic Btplants, and demands thorough examination of thetritrophic interactions that occur between insecticidalproteins, the plant, and the insect.REFERENCESAdamczyk Jr, J.J., Adams, L.C. & Hardee, D.D. 2001. Field efficacy andseasonal expression profiles for terminal leaves of single and doubleBacillus thuringiensis toxin cotton genotypes. J. Econ. Entomol. 94:1589 -1593.Alstad, D.N. & Andow, D.A. 1995. Managing the evolution of insectresistance to transgenic plants. Science 268: 1894-1896.Attathom, T., Chanpaisang, J. & Chongrattanameteekul, W. 1994.Bacillus thuringiensis isolation, identification, and bioassay. InBacillus thuringiensis biotechnology and environmental benefits(eds Feng, T. Y. et al.,). Hua Shiang Yuan Publishing Co., Taipei,Taiwan. pp 68-86.Ballester, V., Escriche, B., Mensua, J. L., Riethmacher, G. W. & Ferre, J.1994. Lack of cross-resistance to other Bacillus thuringiensiscrystal proteins in a population of Plutella xylostella highly resistantto Cry1A(b). Biocontrol Sci. Technol. 4: 437-443Bolin, C.P., Hutchison, W.D. & Andow, D.A. 1999. Long-term selectionfor resistance to Bacillus thuringiensis Cry1Ac endotoxin in aMinnesota population of European corn borer (Lepidoptera:Crambidae). J. Econ. Entomol. 92: 1021-1030.Cannon, R.J.C. 2000. Bt transgenic crops: risks and benefits. IntegratedPest Management Review 5 (3): 151-173.Cohen, M. B. 2000. Bt rice: practical steps to sustainable use. IRRI News.25: 4-10.Denolf, P., Jansens, S., Peferoen, M., Degheele, D. & VanRie, J. 1993.Two different Bacillus thuringiensis delta-endotoxin receptors inthe midgut brush border membrane of the European corn borer,Ostrinia nubilalis (Hubner) (Lepidoptera: Pyralidae). Appl.Environ. Microbiol. 59: 1828-1837.Dove, A. 2001. Survey raises concerns about Bt resistance management.Nat. Biotechnol. 19: 293-294. Environmental Protection Agency/US Department of Agriculture (EPA/ USDA). 1999.EPA and USDA position paper on insect resistance management in Btcrops. http://www.epa.gov/pesticides/ biopesticides/otherdocs/bt_position_paper_618. htm(1999, December 2).Estada, U. & Ferre, J. 1994. Binding of insecticidal crystal proteins ofBacillus thuringiensis to the midgut brush border of the cabbagelooper, Trichoplusia ni (Hubner) (Lepidoptera: Noctuidae) andselection for resistance to one of the crystal proteins. Appl. EnvironMicrobiol. 60: 3840-3846.Ferre, J. & VanRie, J. 2002. Biochemistry and genetics of insectresistance to Bacillus thuringiensis. Ann. Rev. Entomol. 47: 501-533.Ferre, J., Real, M. D., VanRie, J., Jansens, S. & Peferoen, M. 1991.Resistance to the Bacillus thuringiensis bioinsecticide in a fieldpopulation of Plutella xylostella is due to a change in a membranemidgut receptor. Proc. Natl. Acad. Sci. USA 88: 5119-5123.Forcada, C., Alcacer, E., Garcera, M. D. & Martinez-Ramirez, A. 1996.Differences in the midgut proteolytic activity of two Heliothisvirescens strains, one susceptible and one resistant to Bacillusthuringiensis toxins. Arch. Insect Biochem. Physiol. 31:257-272.Forcada, C., Alcacer, E., Garcera, M. D., Tato, A. & Martinez-RamirezA. 1999. Resistance to Bacillus thuringiensis Cry1Ac toxin in threestrains of Heliothis virescens: proteolytic and SEM study of thelarval midgut. Arch. Insect Biochem. Physiol. 42: 51-63.Gelernter, W.D. 1997. Resistance to microbial insecticides: the scale ofthe problem and how to manage it. Microbial insecticides: noveltyor necessity? Proceedings of a symposium held at the University ofWarwick, Coventry, UK, 16-18 April 1997. 25: 201-212.Georghiou, G. P. & Taylor. C. E. 1977. Operational influences in theevolution of insecticide resistance. J. Econ. Entomol. 70: 653-658.Gill, S. S., Cowles, E. S. & Pietrantonio, P.V. 1992. The mode of actionof Bacillus thuringiensis endotoxins. Ann. Rev. Entomol. 37: 615-636.Gould, F. & Tabashnik, B. 1998. Bt-cotton resistance management. InNow or never serious new plans to save a natural pest control (eds.Mellon, M. & Rissler, J.) Cambridge (Massachusetts): Union ofConcerned Scientists. pp 67-105.Gould, F. 1998. Sustainability of transgenic insecticidal cultivars:integrating pest genetics and ecology. Ann. Rev. Entomol. 43: 701-26.Gould, F., Anderson, A., Reynolds, A., Bumgarner, L. & Moar, W. 1995.Selection and genetic analysis of a Heliothis virescens(Lepidoptera: Noctuidae) strain with high levels of resistance toBacillus thuringiensis toxins. J. Econ. Entomol. 88: 1545-1559.Gould, F., Martinez-Ramirez, A., Anderson, A., Ferre, J., Silva, F.J.,Moar, W.J. 1992. Broad-spectrum resistance to Bacillusthuringiensis toxins in Heliothis virescens. Proc. Natl. Acad. Sci.USA 89 (17): 7986-7990.Greenplate, J. T., Penn, S. R., Shappley, Z., Oppenhuizen, M., Mann, J.,Reich, B. & Osborn, J. 2000a. Bollgard II efficacy: quantification oftotal lepidopteran activity in a 2-gene product. ProceedingsBeltwide Cotton Conference ( eds. Dugger, P. & Richter, D.).National Cotton Council of America, Memphis, Tennesse, USA. pp1041-1043.Greenplate, J. T., Penn, S.R., Mullins, J.W. & Oppenhuizen, M. 2000b.Seasonal Cry 1Ac levels in DP50B: The "Bollgard basis" for23
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