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Efficacy of insect-resistance Bt/CpTI transgenes in F5–F7 generations of rice crop–weed hybrid progeny: implications for assessing ecological impact of transgene flow

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  • Life & Medical Sciences
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Science Bulletin

Abstract

Ecological impact of transgene flow into populations of wild/weedy relatives is associated with fitness effects in hybrid progeny. Most studies assessing fitness effects focus essentially on early-generation hybrid progeny. However, whether the transgenes remain effective and durable in advanced generations of hybrid progeny remains unclear. We conducted a common garden experiment with F5–F7 hybrid progeny derived from crosses between insect-resistant transgenic (Bt/CpTI) rice and weedy rice, to examine their insect resistance and fitness effects of transgenes on progeny. Hybrid progeny were grown under different insect pressures and cultivation modes where insect damage and fitness-related traits were measured in the same growth season. Plants with transgenes showed significantly lower insect damage (10 % vs. 32 %) and higher fecundity (551 vs. 392 seeds/plant) than those without transgenes in F5–F7 populations, suggesting the efficacy of transgenes for insect resistance. Fitness benefits of the transgenes were similar among the F5–F7 populations, indicating the stability of transgenic effects. A positive correlation between insect index and fecundity change was detected, stressing the important role of ambient insect pressures in assessing fitness effects caused by insect-resistance transgenes. Our results have important implications for assessing ecological impacts caused by transgene flow to wild/weedy relatives. For cost-effectiveness, the experimental estimation of fitness effects is probably sufficient based on data from hybrids in early generations. Given that fitness effects of insect-resistance transgenes are associated with ambient insect pressure, ecological risk assessment on transgene flow should consider this variable in experimental design, reasonably reflecting actual situations in wild/weedy populations.

Abstract

本文报道了抗虫转基因 (Bt/CpTI) 对水稻与杂草稻杂种 F5–F7 分离世 代的抗虫性及适合度效应分析。在有害虫发生的环境中, 含转基因的 F5–F7 分离 群体比对应的非转基因群体虫害显著较低, 而结实性显著较高, 表明抗虫转基因 在高世代的杂种群体中仍非常有效, 且世代之间的适合度效应也比较稳定。因此, 抗虫转基因漂移生态风险的评价仅在早世代杂种群体中进行便可达到目的。转基 因的适合度效应与环境的虫压之间显著正相关, 表明正确的环境虫压设置对抗虫 转基因适合度效应的评价非常重要。

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References

  1. Ellstrand NC (2003) Current knowledge of gene flow in plants: implications for transgene flow. Proc R Soc B Biol Sci 358:1163–1170

    Google Scholar 

  2. Kwit C, Moon HS, Warwick SI et al (2011) Transgene introgression in crop relatives: molecular evidence and mitigation strategies. Trends Biotechnol 29:284–293

    Article  Google Scholar 

  3. Ellstrand NC, Meirmans P, Rong J et al (2013) Introgression of crop alleles into wild or weedy populations. Ann Rev Ecol Evol Syst 44:325–345

    Article  Google Scholar 

  4. Hansen LB, Siegismund HR, Jørgensen RB (2001) Introgression between oilseed rape (Brassica napus L.) and its weedy relative B. rapa L. in a natural population. Genet Resour Crop Evol 48:621–627

    Article  Google Scholar 

  5. Snow AA, Culley TM, Campbell LG et al (2010) Long-term persistence of crop alleles in weedy populations of wild radish (Raphanus raphanistrum). New Phytol 186:537–548

    Article  Google Scholar 

  6. Whitton J, Wolf DE, Arias DM et al (1997) The persistence of cultivar alleles in wild populations of sunflowers five generations after hybridization. Theor Appl Genet 95:33–40

    Article  Google Scholar 

  7. Cao QJ, Lu BR, Xia H et al (2006) Genetic diversity and origin of weedy rice (Oryza sativa f. spontanea) populations found in North-eastern China revealed by simple sequence repeat (SSR) markers. Ann Bot 98:1241–1252

    Article  Google Scholar 

  8. Song Z, Zhu W, Rong J et al (2006) Evidences of introgression from cultivated rice to Oryza rufipogon (Poaceae) populations based on SSR fingerprinting: implications for wild rice differentiation and conservation. Evol Ecol 20:501–522

    Article  Google Scholar 

  9. Xia HB, Wang W, Xia H et al (2011) Conspecific crop–weed introgression influences evolution of weedy rice (Oryza sativa f. spontanea) across a geographical range. PLoS One 6:e16189

    Article  Google Scholar 

  10. Barton NH (1993) The probability of fixation of a favored allele in a subdivided population. Genet Res 62:149–157

    Article  Google Scholar 

  11. Haygood R, Ives AR, Andow DA (2004) Population genetics of transgene containment. Ecol Lett 7:213–220

    Article  Google Scholar 

  12. Davis SA, Catchpole EA, Pech RP (1999) Models for the introgression of a transgene into a wild population within a stochastic environment, with applications to pest control. Ecol Model 119:267–275

    Article  Google Scholar 

  13. Snow AA, Pilson D, Rieseberg LH et al (2003) A Bt transgene reduces herbivory and enhances fecundity in wild sunflowers. Ecol Appl 13:279–286

    Article  Google Scholar 

  14. Hails RS, Morley K (2005) Genes invading new populations: a risk assessment perspective. Trends Ecol Evol 20:245–252

    Article  Google Scholar 

  15. Andow DA, Zwahlen C (2006) Assessing environmental risks of transgenic plants. Ecol Lett 9:196–214

    Article  Google Scholar 

  16. Warwick SI, Légère A, Simard MJ et al (2008) Do escaped transgenes persist in nature? The case of an herbicide resistance transgene in a weedy Brassica rapa population. Mol Ecol 17:1387–1395

    Article  Google Scholar 

  17. Wegier A, Piñeyro-Nelson A, Alarcón J et al (2011) Recent long-distance transgene flow into wild populations conforms to historical patterns of gene flow in cotton (Gossypium hirsutum) at its centre of origin. Mol Ecol 20:4182–4194

    Article  Google Scholar 

  18. Burke JM, Rieseberg LH (2003) Fitness effects of transgenic disease resistance in sunflowers. Science 300:1250

    Article  Google Scholar 

  19. Vacher C, Weis AE, Hermann D et al (2004) Impact of ecological factors on the initial invasion of Bt transgenes into wild populations of birdseed rape (Brassica rapa). Theor Appl Genet 109:806–814

    Article  Google Scholar 

  20. Halfhill MD, Sutherland JP, Moon HS et al (2005) Growth, productivity, and competitiveness of introgressed weedy Brassica rapa hybrids selected for the presence of Bt cry1Ac and gfp transgenes. Mol Ecol 14:3177–3189

    Article  Google Scholar 

  21. Guadagnuolo R, Clegg J, Ellstrand NC (2006) Relative fitness of transgenic vs. non-transgenic maize × teosinte hybrids: a field evaluation. Ecol Appl 16:1967–1974

    Article  Google Scholar 

  22. Magnussen LS, Hauser TP (2007) Hybrids between cultivated and wild carrots in natural populations in Denmark. Heredity 99:185–192

    Article  Google Scholar 

  23. Yang X, Xia H, Wang W et al (2011) Transgenes for insect resistance reduce herbivory and enhance fecundity in advanced generations of crop–weed hybrids of rice. Evol Appl 4:672–684

    Article  Google Scholar 

  24. Lu BR, Yang C (2009) Gene flow from genetically modified rice to its wild relatives: assessing potential ecological consequences. Biotechnol Adv 27:1083–1091

    Article  Google Scholar 

  25. Delouche JC, Burgos NR, Gealy DR et al (2007) Weedy rices—origin, biology, ecology and control. FAO of the United Nations, Rome

    Google Scholar 

  26. Londo JP, Schaal BA (2007) Origins and population genetics of weedy red rice in the USA. Mol Ecol 16:4523–4535

    Article  Google Scholar 

  27. Cohen MB, Arpaia S, Lan LP et al (2008) Shared flowering phenology, insect pests, and pathogens among wild, weedy, and cultivated rice in the Mekong Delta, Vietnam: implications for transgenic rice. Environ Biosafety Res 7:73–85

    Article  Google Scholar 

  28. Chen LJ, Lee DS, Song ZP et al (2004) Gene flow from cultivated rice (Oryza sativa) to its weedy and wild relatives. Ann Bot 93:67–73

    Article  Google Scholar 

  29. Shivrain VK, Burgos NR, Gealy DR et al (2009) Gene flow from weedy red rice (Oryza sativa L.) to cultivated rice and fitness of hybrids. Pest Manag Sci 65:1124–1129

    Article  Google Scholar 

  30. Song X, Liu L, Wang Z et al (2009) Potential gene flow from transgenic rice (Oryza sativa L.) to different weedy rice (Oryza sativa f. spontanea) accessions based on reproductive compatibility. Pest Manag Sci 65:862–869

    Article  Google Scholar 

  31. Lu BR, Snow AA (2005) Gene flow from genetically modified rice and its environmental consequences. BioScience 55:669–678

    Article  Google Scholar 

  32. Yang X, Wang F, Su J et al (2012) Limited fitness advantages of crop–weed hybrid progeny containing insect-resistant transgenes (Bt/CpTI) in transgenic rice field. PLoS One 7:e41220

    Article  Google Scholar 

  33. Cao QJ, Xia H, Yang X et al (2009) Performance of hybrids between weedy rice and insect-resistant transgenic rice under field experiments: implication for environmental biosafety assessment. J Integr Plant Biol 51:1138–1148

    Article  Google Scholar 

  34. Rong J, Song Z, Su J et al (2005) Low frequency of transgene flow from Bt/CpTI rice to its nontransgenic counterparts planted at close spacing. New Phytol 168:559–566

    Article  Google Scholar 

  35. Chen LY, Snow AA, Wang F et al (2006) Effects of insect-resistance transgenes on fecundity in rice (Oryza sativa, Poaceae): a test for underlying costs. Am J Bot 93:94–101

    Article  Google Scholar 

  36. Xia H, Chen LY et al (2010) Yield benefit and underlying cost of insect-resistance transgenic rice: Implication in breeding and deploying transgenic crops. Field Crops Res 118:215–220

    Article  Google Scholar 

  37. Xia H, Lu BR, Xu K et al (2011) Enhanced yield performance of Bt rice under target-insect attacks: implications for field insect management. Transgenic Res 20:655–664

    Article  Google Scholar 

  38. Snow AA, Andow DA, Gepts P et al (2005) Genetically engineered organisms and the environment: current status and recommendations 1. Ecol Appl 15:377–404

    Article  Google Scholar 

  39. Wu KM, Lu YH, Feng HQ et al (2008) Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin–containing cotton. Science 321:1676–1678

    Article  Google Scholar 

  40. Jenczewski E, Ronfort J, Chèvre AM (2003) Crop-to-wild gene flow, introgression and possible fitness effects of transgenes. Environ Biosafety Res 2:9–24

    Article  Google Scholar 

  41. Chandler S, Dunwell JM (2008) Gene flow, risk assessment and the environmental release of transgenic plants. Crit Rev Plant Sci 27:25–49

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the the National Basic Research Program of China (2011CB100401), the National Natural Science Foundation of China (31330014, 31271683), and National Program of Development of Transgenic New Species of China (2013ZX08011-006). Dr. B. E. Valverde edited the English language and provided constructive comments of the manuscript.

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Authors and Affiliations

  1. Ministry of Education, Key Laboratory for Biodiversity Science and Ecological Engineering, Department of Ecology and Evolutionary Biology, Fudan University, Shanghai, 200433, China

    Xiao Yang, Lei Li, XingXing Cai & Bao-Rong Lu

  2. Fujian Provincial Key Laboratory of Genetic Engineering for Agriculture, Fujian Academy of Agricultural Sciences, Fuzhou, 350003, China

    Feng Wang & Jun Su

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  1. Xiao Yang
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  2. Lei Li
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  3. XingXing Cai
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  4. Feng Wang
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  5. Jun Su
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  6. Bao-Rong Lu
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Correspondence to Bao-Rong Lu.

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Yang, X., Li, L., Cai, X. et al. Efficacy of insect-resistance Bt/CpTI transgenes in F5–F7 generations of rice crop–weed hybrid progeny: implications for assessing ecological impact of transgene flow. Sci. Bull. 60, 1563–1571 (2015). https://doi.org/10.1007/s11434-015-0885-x

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