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Comparative fitness of a wild squash species and three generations of hybrids between wild × virus-resistant transgenic squash

Published online by Cambridge University Press:  15 March 2004

Marc Fuchs
Affiliation:
Department of Plant Pathology, Cornell University, New York State Agricultural Experiment Station, Geneva, NY 14456, USA
Ellen M. Chirco
Affiliation:
Department of Horticultural Sciences, Cornell University, New York State Agricultural Experiment Station, Geneva, NY 14456, USA
Jim R. Mcferson
Affiliation:
Plant Genetic Resources, USDA-ARS, Cornell University, Geneva, NY 14456, USA
Dennis Gonsalves
Affiliation:
Department of Plant Pathology, Cornell University, New York State Agricultural Experiment Station, Geneva, NY 14456, USA

Abstract

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We compared some fitness components of the wild squash species Cucurbita pepo spp. ovifera var. texana (C. texana) and three generations of hybrids (F1, BC1, and BC2) between C. texana and commercial transgenic squash CZW-3 over three consecutive years under field conditions of low (LDP) and high disease pressure (HDP) by Cucumber mosaic virus (CMV), Zucchini yellow mosaicvirus (ZYMV) and Watermelon mosaic virus (WMV). Transgenic squash CZW-3 expresses the coat protein (CP) genes of CMV, ZYMV, and WMV, and is resistant to these three aphid-borne viruses. Across all HDP trials, transgenic BC1 and BC2 hybrids expressing the three CP genes grew more vigorously, displayed resistance to CMV, ZYMV, and WMV, and produced a greater number of mature fruits and viable seeds than nontransgenic hybrid segregants and C. texana. Transgenic F1 hybrids behaved similarly to BC1 and BC2 hybrids but grew less vigorously than C. texana. In contrast, across all LDP trials, C. texana outperformed the transgenic and nontransgenic hybrid segregants. Further, only one back cross was necessary to recover individuals with most of the C. texana characteristics and yet maintain virus resistance. Our data suggest that C. texana acquiring CP transgenes upon hybridization and introgression could have a selective advantage if CMV, ZYMV, and WMV are severely limiting the growth and reproductibility of wild squash populations.

Type
Research Article
Copyright
© ISBR, EDP Sciences, 2004

References

Acord, BD (1996) Availability of determination of nonregulated status for a squash line genetically engineered for virus resistance. Fed. Reg. 61: 3348433485
Bartsch, D, Schmidt, M, Pohl-Orf, M, Haag, C, Schuphan, I (1996) Competitiveness of transgenic sugar beet resistant to beet necrotic yellow vein virus and potential impact on wild beet populations. Mol. Ecol. 5: 199205 CrossRef
Bartsch D, Brand U, Morak C, Pohl-Orf M, Schuphan I, Ellstrand NC (2001) Biosafety of hybrids between transgenic virus-resistant sugar beet and Swiss Chard. Ecol. Appl. 11: 142–147
Blancard D, Lecoq H, Pitrat M (1994) Cucurbit Diseases: Observation, identification and control. Wiley and Sons, New York, NY
Boyette G, Templeton E, Oliver LR (1984) Texas gourd (Cucurbita texana) control. Weed Sci. 32: 649–655
Burke, JM, Rieseberg, LH (2003) Fitness effects of transgenic disease resistance in sunflowers. Science 300: 1250 CrossRef
Dale J (1992) Spread of engineered genes to wild relatives. Plant Physiol. 100: 13–15 CrossRef
Decker, DS (1988) Origin(s), evolution, and systematics of Cucurbita pepo (Cucurbitaceae). Econ. Bot. 42: 415 CrossRef
Dietz-Pfeilestetter A, Kirchner M (1998) Analysis of gene inheritance and expression in hybrids between transgenic sugar beet and wild beets. Mol. Ecol. 7: 1693–1700
Duffus JE (1971) Role of weeds in the incidence of virus diseases. Annu. Rev. Phytopathol. 9: 319–340 CrossRef
Ellstrand, NC, Schierenbeck, KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc. Natl. Acad. Sci. USA 97: 70437050 CrossRef
Ellstrand NC, Prentice HC, Hancock JF (1999) Gene flow and introgression from domesticated plants into their wild relatives. Annu. Rev. Ecol. Syst. 30: 539–563
Friess, N, Maillet, J (1996) Influence of cucumber mosaic virus infection on the intraspecific competitive ability and fitness of purslane. New Phytol. 132: 103111 CrossRef
Friess N, Maillet J (1997) Influence of cucumber mosaic virus infection on the competitive ability and reproduction of chickweed (Stellaria media). New Phytol. 135: 887–674 CrossRef
Fuchs M, Gonsalves D (1995) Resistance of transgenic hybrid squash ZW-20 expressing the coat protein genes of zucchini yellow mosaic virus and watermelon mosaic virus 2 to mixed infections by both potyviruses. Bio/Tech. 13: 14466–14473 CrossRef
Fuchs M, Gonsalves D (1997) Genetic Engineering. In Rechcigl NA, Rechcigl JE, eds, Environmentally Safe Approcahes to Crop Disease Control, CRC Press, Boca Raton, FL, pp 333–368
Fuchs, M, Tricoli, DM, McMaster, JR, Carney, KJ, Schesser, M, McFerson, JR, Gonsalves, D (1998) Comparative virus resistance and fruit yield of transgenic squash with single and multiple coat protein genes. Plant Dis. 82: 13501356 CrossRef
Fuchs M, Chirco EM, Gonsalves D (2004) Movement of coat protein genes from a commercial virus-resistant transgenic squash into a wild relative. Environ. Biosafety Res. 3: 5–16 CrossRef
Gonsalves, D (1998) Control of papaya ringspot virus in papaya: A case study. Annu. Rev. Phytopathol. 36: 415437 CrossRef
Grumet R (1994) Development of virus resistant plants via genetic engineering. Plant Breeding Rev. 12: 47–79 CrossRef
Gueritaine G, Sester M, Eber F, Chèvre AM, Darmency H (2002) Fitness of backcross six of hybrids between transgenic oildseed rape (Brassica napus) and wild radish (Raphanus raphanistrum). Mol. Ecol. 11: 1419–1426 CrossRef
Hancock, JF, Grumet, R, Hokanson, SC (1996) The opportunity of escape of engineered genes from transgenic crops. HortSci. 31: 10801085
Hokanson, SC, Hancock, JF, Grumet, R (1997) Direct comparison of pollen-mediated movement of native and engineered genes. Euphytica 96: 397403 CrossRef
Kareiva P, Morris W, Jacobi CM (1994) Studying and managing the risk of cross-fertilization between transgenic crops and wild relatives. Mol. Ecol. 3: 15–21
Kelley SE (1993) Viruses and the advantage of sex in Anthoxanthum odoratum: A review. Plant Species Biol. 8: 217–223 CrossRef
Kirkpatrick, KJ, Wilson, H (1988) Interpecific gene flow in Cucurbita: C. texana vs. C. pepo. Am. J. Bot. 75: 519527 CrossRef
Klas, FE, Fuchs, M, Gonsalves, D (1994) Spatial analysis as a tool to evaluate virus resistance in a transgenic crop. Phytopathol. 84: 1372
Maskell, LC, Raybould, AF, Cooper, JI, Edwards, ML, Gray, AJ (1999) Effects of turnip mosaic virus and turnip yellow mosaic virus on the survival, growth and reproduction of wild cabbage (Brassica oleracea). Ann. appl. Biol. 135: 401407 CrossRef
McClement, WD, Richards, M (1956) Virus in wild plants. Can. J. Bot. 24: 793799 CrossRef
McCreight JD, Staub J (1999) Report of the Cucurbit working group. In Traynor P, Westwood JH, eds, Proceedings of a Workshop on Ecological Effects of Pest Resistance Genes in Managed Ecosystems, Jan. 31-Feb. 3, ISB, Blacksburg, VA, pp 79–87
Medley, TL (1994) Availability of determination of nonregulated status for virus resistant squash. Fed. Reg. 59: 6418764189
Mikkelsen TR, Andersen B, Jørgensen RB (1996) The risk of crop transgene spread. Nature 380: 31 CrossRef
Munger HM (1993) Breeding for viral resistance in cucurbits. In Resistance to viral diseases of vegetables: Genetics and breeding, Timber Press, Portland, OR, pp 8–43
Oliver LR, Harrison SA, McClelland M (1983) Germination of Texas gourd (Cucurbita texana) and its control in soybean (Glycine max). Weed Sci. 31: 700–706
Pallett DW, Thurston MI, Cortina-Borja M, Edwards ML, Alexander M, Mitchell E, Raybould AF, Cooper JI (2002) The incidence of viruses in wild Brassica rapa ssp. sylvestris in southern England. Ann. Appl. Biol. 141: 163–170
Powell, CA, Mountain, WL, Derr, MA (1992) Tomato ringspot virus reduces dandelion top weight and flower production under field conditions. HortScience 27: 273
Quemada H (1998) The use of coat protein technology to develop virus-resistant cucurbits. In Ives CL, Bedford BM, eds, Agricultural Biotechnology in International Development, CAB International, Wallingford, UK, pp 147–160
Quemada H, Strehlow L, Decker-Walters D, Staub J (2002) Case Study: Gene flow from commercial transgenic Cucurbita pepo to “wild” C. pepo populations. In Proceedings of the Scientific Methods Workshop on Ecological and Agronomic Consequences of Gene Flow from Transgenic Crops to Wild Relatives, March 5–6, 2002, Columbus, OH, pp 65–70, http://www.biosci.ohio-state.edu/~lspencer/gene_flow.htm
Quiot JB, Marchoux G, Douine L, Vigouroux A (1979) Écologie et épidémiologie du virus de la mosaïque du concombre dans le sud-est de la France. V. Rôle des espèces spontanées dans la conservation du virus. Ann. Phytopath. 11: 325–348
Raybould, A (1999) Transgenes and agriculture – going with the flow? Trends Plant Sci. 4: 247248 CrossRef
Raybould AF, Maskell LC, Cooper JI, Edwards ML, Gray AJ (1999) The prevalence and spatial distribution of viruses in natural populations of Brassica oleracea. New Physiol. 141: 265–275 CrossRef
Rissler J, Mellon M (1996) The Ecological Risks of Engineered Crops, MIT Press, Cambridge, MA, pp 159
Sanford, JC, Johnston, SA (1985) The concept of parasite-derived resistance – deriving resistance genes from the parasite’s own genome. J. Theor. Biol. 113: 395405 CrossRef
Snow, AA, Palma, PM (1997) Commercialization of transgenic plants: Potential ecological risks. BioScience 47: 8696 CrossRef
Snow, AA, Pilson, D, Rieseberg, LH, Paulsen, MJ, Pleskac, N, Reagon, MR, Wolf, DE, Selbo, SM (2003) A Bt-transgene reduces herbivory and enhances fecundity in wild sunflowers. Ecol. Appl. 13: 279286 CrossRef
Spencer, LJ, Snow, A (2001) Fecundity of transgenic wild-crop hybrids of Cucurbita pepo (Cucurbitaceae): implications for crop-to-wild gene flow. Heredity 86: 694702 CrossRef
Thurston MI, Pallett DW, Cortina-Borja M, Edwards ML, Raybould AF, Cooper JI (2001) The incidence of viruses in wild Brassica nigra in Dorset (UK). Ann. Appl. Biol. 139: 277–284 CrossRef
Tricoli, DM, Carney, KJ, Russell, PF, McMaster, JR, Groff, DW, Hadden, KC, Himmel, PT, Hubbard, JP, Boeshore, ML, Quemada, HD (1995) Field evaluation of transgenic squash containing single and multiple coat protein gene constructs for resistance to cucumber mosaic virus, watermelon mosaic virus 2, and zucchini yellow mosaic virus. Bio/Tech. 13: 14581465
Weidemann, GJ, Templeton, GE (1988) Efficacy and soil persistence of Fusarium solani f. sp. cucurbitae for control of Texas gourd (Cucurbita texana). Plant Dis. 72: 3638 CrossRef
Wilson, HD (1990) Gene flow in squash species. BioScience 40: 449455 CrossRef
Zitter TA, Hopkins DL, Thomas CE (1996) Compendium of cucurbit diseases, APS Press, St Paul, MN