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Limited ecological risk of insect-resistance transgene flow from cultivated rice to its wild ancestor based on life-cycle fitness assessment

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Abstract

Ecological impact caused by transgene flow from genetically engineered (GE) crops to their wild relatives is largely determined by the fitness effect brought by a transgene. To estimate such impact is critical for the ecological risk assessment prior to the commercialization of GE crops. We produced F1 and F2 hybrid descendants from crosses of two insect-resistant GE rice lines (Bt, Bt/CpTI) and their non-GE rice parent with a wild rice (Oryza rufipogon) population to estimate the transgenic fitness. Insect damages and life-cycle fitness of GE and non-GE crop–wild hybrid descendants as well as their wild parent were examined in a common-garden experiment. No significant differences in insect damages were observed between the wild rice parent and GE hybrid descendants under high-insect pressure. The wild parent showed significantly greater relative survival-regeneration ratios than its GE and non-GE hybrid descendants under both high- and low-insect pressure. However, more seeds were produced in GE hybrid descendants than their non-GE counterparts under high-insect pressure. Given that the introduction of Bt and Bt/CpTI transgenes did not provide greater insect resistance to crop–wild hybrid descendants than their wild parent, we predict that transgene flow from GE insect-resistant rice to wild rice populations may not cause considerable ecological risks.

摘要

转基因渐渗到作物野生近缘种带来的生态影响取决于其适合度效应, 而对生态影响的评价是转基因作物商品化应用的安全保障。利用抗虫转基因 (Bt, Bt/CpTI) 水稻及其非转基因亲本与普通野生稻 (Oryza rufipogon) 杂交而产生F1和F2代杂种群体, 我们在同质园实验条件下分析了转基因对杂种抗虫能力和适合度的影响。结果表明: 即使在高虫压条件下野生稻亲本与转基因杂种的虫害水平无显著差异; 野生亲本的生存和再生能力显著高于杂种后代; 在高虫压条件下转基因杂种的种子生产能力显著高于非转基因杂种。鉴于抗虫转基因并未给杂种植株带来高于野生稻亲本的抗虫能力, 我们预测抗虫转基因渐渗到野生稻不带来明显生态风险。

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References

  1. James C (2014) Global status of commercialized biotech/GM crops: ISAAA Brief No. 49. ISAAA, Ithaca

  2. 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 

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

    Article  CAS  PubMed  Google Scholar 

  4. Lu B-R (2008) Transgene escape from GM crops and potential biosafety consequences: an environmental perspective. In: International Centre for Genetic Engineering and Biotechnology (ICGEB), collection of biosafety reviews. ICGEB Press, Trieste, vol 4, pp 66–141

  5. Ellstrand NC (2003) Current knowledge of gene flow in plants: implications for transgene flow. Philos Trans R Soc B 358:1163–1170

    Article  Google Scholar 

  6. Stewart CN, Halfhill MD, Warwick SI (2003) Transgene introgression from genetically modified crops to their wild relatives. Nat Rev Genet 4:806–817

    Article  CAS  PubMed  Google Scholar 

  7. Kling J (1996) Could transgenic supercrops one day breed superweeds? Science 274:180–181

    Article  ADS  CAS  Google Scholar 

  8. Lu B-R, Song Z, Chen J (2003) Can transgenic rice cause ecological risks through transgene escape? Prog Nat Sci 13:17–24

    Google Scholar 

  9. Lu B-R, Snow AA (2005) Gene flow from genetically modified rice and its environmental consequences. Bioscience 55:669–678

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  11. 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  CAS  PubMed  PubMed Central  Google Scholar 

  12. Wang W, Xia H, Yang X et al (2014) A novel 5-enolpyruvoylshikimate-3-phosphate (EPSP) synthase transgene for glyphosate resistance stimulates growth and fecundity in weedy rice (Oryza sativa) without herbicide. New Phytol 202:679–688

    Article  CAS  PubMed  Google Scholar 

  13. Lu B-R, Yang X, Ellstrand NC (2016) Fitness correlates of crop transgene flow into weedy populations: a case study of weedy rice in China and other examples. Evol Appl 9:857–870

    Article  PubMed  PubMed Central  Google Scholar 

  14. 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 

  15. 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  CAS  PubMed  Google Scholar 

  16. Crone EE (2001) Is survivorship a better fitness surrogate than fecundity? Evolution 55:2611–2614

    Article  CAS  PubMed  Google Scholar 

  17. Silvertown J, Mendoza A (1993) Comparative plant demography-relative importance of life cycle components to the finite rate of increase in woody and herbaceous perennials. J Ecol 81:465–476

    Article  Google Scholar 

  18. Yang X, Li L, Cai XX et al (2015) 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 18:1–9

    Google Scholar 

  19. Xia H, Zhang H, Wang W et al (2016) Ambient insect pressure and recipient genotypes determine fecundity of transgenic crop-weed rice hybrid progeny: implications for environmental biosafety assessment. Evol Appl 9:847–856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Vaughan DA, Lu B-R, Tomooka N (2008) The evolving story of rice evolution. Plant Sci 174:394–408

    Article  CAS  Google Scholar 

  21. Song ZP, Xu X, Wang B et al (2003) Genetic diversity in the northernmost Oryza rufipogon populations estimated by SSR markers. Theor Appl Genet 107:1492–1499

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  23. Xiao J, Li J, Grandillo S et al (1996) A wild species contains genes that may significantly increase the yield of rice. Nature 384:223–224

    Article  ADS  CAS  Google Scholar 

  24. Bellon MR, Brar DS, Lu B-R et al (1998) Rice genetic resources. In: Dwoling NG, Greenfield SM, Fischer KS (eds) Sustainability of rice in the global food system, chap 16, Davis, California (USA). Pacific Basin Study Center and IRRI, Manila, pp 251–283

  25. Lu B-R (2013) Introgression of transgenic crop alleles: its evolutionary impacts on conserving genetic diversity of crop wild relatives. J Syst Evol 51:245–262

    Article  Google Scholar 

  26. Song ZP, Li B, Chen JK et al (2005) Genetic diversity and conservation of common wild rice (Oryza rufipogon) in China. Plant Spec Biol 20:83–92

    Article  Google Scholar 

  27. Zhao Y, Vrieling K, Liao H et al (2013) Are habitat fragmentation, local adaptation and isolation-by-distance driving population divergence in wild rice Oryza rufipogon? Mol Ecol 22:5531–5547

    Article  CAS  PubMed  Google Scholar 

  28. Lu B-R (2016) Challenges of transgenic crop commercialization in China. Nat Plants 2:1–2

    ADS  Google Scholar 

  29. Song ZP, Lu B-R, Zhu YG et al (2003) Gene flow from cultivated rice to the wild species Oryza rufipogon under experimental field conditions. New Phytol 157:657–665

    Article  CAS  Google Scholar 

  30. Song ZP, Zhu WY, 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 

  31. 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  CAS  PubMed  PubMed Central  Google Scholar 

  32. Wang L, Haccou P, Lu B-R (2016) High-resolution gene flow model for assessing environmental impacts of transgene escape based on biological and climatic parameters. PLoS One 11:e0149563

    Article  PubMed  PubMed Central  Google Scholar 

  33. Xia H, Lu B-R, Su J et al (2009) Normal expression of insect-resistant transgene in progeny of common wild rice crossed with genetically modified rice: its implication in ecological biosafety assessment. Theor Appl Genet 119:635–644

    Article  CAS  PubMed  Google Scholar 

  34. Song ZP, Lu B-R, Wang B et al (2004) Fitness estimation through performance comparison of F1 hybrids with their parental species Oryza rufipogon and O. sativa. Ann Bot 93:311–316

    Article  PubMed  PubMed Central  Google Scholar 

  35. Dong SS, Xiao MQ, Rong J et al (2011) No effect of transgene and strong wild parent effects on seed dormancy in crop–wild hybrids of rice: implications for transgene persistence in wild populations. Ann Appl Biol 159:348–357

    Article  Google Scholar 

  36. Xiao MQ, Dong SS, Li ZL et al (2015) Effects of water management practices on residue decomposition and degradation of Cry1Ac protein from crop–wild Bt rice hybrids and parental lines during winter fallow season. Ecotoxicol Environ Saf 122:275–289

    Article  CAS  PubMed  Google Scholar 

  37. Rong J, Song ZP, 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  CAS  PubMed  Google Scholar 

  38. 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 

  39. 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  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  40. Ramachandran R, Khan ZR (1991) Mechanisms of resistance in wild rice Oryza brachyantha to rice leaffolder Cnaphalocrocis medinalis (Guenée) (Lepidoptera: Pyralidae). J Chem Ecol 17:41–65

    Article  CAS  PubMed  Google Scholar 

  41. Vaughan DA (1994) The wild relatives of rice: a genetic resources handbook. International Rice Research Institute (IRRI) Press, Los Baños

    Google Scholar 

  42. Padhi G, Sen P (2002) Evaluation of wild rice species against yellow stem borer (Scirpophaga incertulas Walk.). J Appl Zool Res 13:147–148

    Google Scholar 

  43. Du B, Zhang W, Liu B et al (2009) Identification and characterization of Bph14, a gene conferring resistance to brown planthopper in rice. Proc Natl Acad Sci USA 106:22163–22168

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  44. Huang D, Qiu Y, Zhang Y et al (2013) Fine mapping and characterization of BPH27, a brown planthopper resistance gene from wild rice (Oryza rufipogon Griff.). Theor Appl Genet 126:219–229

    Article  CAS  PubMed  Google Scholar 

  45. Brar DS, Virk PS, Jena KK et al (2009) Breeding for resistance to planthoppers in rice. In: Heong KL, Hardy B (eds) Planthoppers: new threats to the sustainability of intensive rice production systems in Asia. IRRI, Los Baños, pp 401–409

    Google Scholar 

  46. Sarwar M (2012) Management of rice stem borers (Lepidoptera: Pyralidae) through host plant resistance in early, medium and late plantings of rice (Oryza sativa L.). J Cereals Oilseeds 3:10–14

    Article  MathSciNet  Google Scholar 

  47. Carbonari JJ, Martins JFDH (1998) Chemical and morphological factors of rice plants associated with insect resistance. Agropecuria Clima Temperado 1:107–115

    Google Scholar 

  48. Chand DS, Muralirangan MC (2000) Silica of rice cultivars, Oryza sativa (Linn.) versus feeding by Oxya nitidula (Wlk.). Uttar Pradesh. J Zool 20:29–35

    Google Scholar 

  49. Foissac X, Loc NT, Christou P et al (2000) Resistance to green leafhopper (Nephotettix virescens) and brown planthopper (Nilaparvata lugens) in transgenic rice expressing snowdrop lectin (Galanthus nivalis agglutinin; GNA). J Insect Physiol 46:573–583

    Article  CAS  PubMed  Google Scholar 

  50. Ge S, Sang T, Lu B-R et al (1999) Phylogeny of rice genomes with emphasis on origins of allotetraploid species. Proc Natl Acad Sci USA 96:14400–14405

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  51. Oka HI (1988) Origin of Cultivated rice. Elsevier, Amsterdam

    Google Scholar 

  52. Pan JJ, Price JS (2002) Fitness and evolution in clonal plants: the impact of clonal growth. Evol Ecol 15:583–600

    Article  Google Scholar 

  53. Sang T, Ge S (2007) The puzzle of rice domestication. J Integr Plant Biol 49:760–768

    Article  CAS  Google Scholar 

  54. Sagers CL, Londo JP, Bautista N et al (2015) Benefits of transgenic insect resistance in Brassica hybrids under selection. Agronomy 5:21–34

    Article  CAS  Google Scholar 

  55. Chen YH, Welter SC (2002) Abundance of a native moth Homoeosoma electellum (Lepidoptera: Pyralidae) and activity of indigenous parasitoids in native and agricultural sunflower habitats. Environ Entomol 31:626–636

    Article  Google Scholar 

  56. Chen YH, Bernal CC (2011) Arthropod diversity and community composition on wild and cultivated rice. Agric For Entomol 13:181–189

    Article  Google Scholar 

  57. 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 Biosaf Res 7:73–85

    Article  Google Scholar 

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Acknowledgments

This work is supported by the National Natural Science Foundation of China (31330014) and the National Program of Development of Transgenic New Species of China (2016ZX08011-006).

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Correspondence to Bao-Rong Lu.

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Li, L., Yang, X., Wang, L. et al. Limited ecological risk of insect-resistance transgene flow from cultivated rice to its wild ancestor based on life-cycle fitness assessment. Sci. Bull. 61, 1440–1450 (2016). https://doi.org/10.1007/s11434-016-1152-5

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  • DOI: https://doi.org/10.1007/s11434-016-1152-5

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