Introgression of a cry1Ab transgene into open pollinated maize and its effect on Cry protein concentration and target pest survival

English version

Autoři: Reynardt Erasmus ^aff001; Rialet Pieters ^aff001; Hannalene Du Plessis ^aff001; Angelika Hilbeck ^aff002; Miluse Trtikova ^aff002; Annemie Erasmus ^aff003; Johnnie Van den Berg ^aff001
Působiště autorů: Unit for Environmental Sciences and Management, North-West University, Potchefstroom, South Africa ^aff001; ETH Zurich, IBZ, Plant Ecological Genetics, Zurich, Switzerland ^aff002; ARC-Grain Crops, Potchefstroom, South Africa ^aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0226476

Souhrn

In Africa, the target pests of genetically modified Bt maize are lepidopteran stem borers, notably Busseola fusca (Lepidoptera: Noctuidae). Gene flow between Bt maize hybrids and open pollinated varieties (OPVs) that do not contain the Bt trait is highly likely in areas where both types of maize are cultivated. Consequently, introgression of the cry1Ab transgene into local OPVs will result in unknown patterns of Cry1Ab protein expression in plants during follow-up seasons when recycled seed of OPVs is planted. Too low concentrations of Cry protein in such plants may result in selection for resistant alleles and accelerate resistance evolution. The aim of this study was to determine the effects of introgression of the cry1Ab transgene into an OPV, on Cry protein concentration levels and pest survival. Bt transgene introgression was done by crossing a transgenic donor hybrid containing the cry1Ab gene with a non-Bt OPV as well as with a non-Bt near-isogenic hybrid. F1 and F2 crosses as well as back crosses were done yielding 11 genotypes (treatments). Cry1Ab protein concentrations in leaf tissue of these crosses were determined by means of ELISAs. All crosses that contained the transgene had similar or higher Cry1Ab concentrations when compared to the Bt parental hybrid, except for the Bt x OPV F1-cross that had a significantly lower Cry1Ab concentration. Survival B. fusca larvae were evaluated in assays in which larvae were reared for 14 days on whorl leaf tissue of the different treatments. Larval survival did not differ between any of the maize plant treatments which contained the Bt gene. Results suggest that Bt transgene introgression into OPVs may produce plant progenies that express Cry1Ab protein at sufficient concentrations, at last up to the F2 seed, to control B. fusca larvae. Resistance evolution is however not only influenced by the frequency of pest individuals that survive exposure to the Cry proteins but also by factors such as genetics of the pest and recipient OPV, pest biology and migration behaviour.

Klíčová slova:

Agricultural workers – Evolutionary genetics – Gene flow – Genetically modified plants – Introgression – Larvae – Maize – Seeds

Zdroje

1. Tabashnik B. Evolution of resistance to Bacillus thuringiensis. Annu Rev Entomol. 1994;39(1): 47–79.

2. Gould F. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu Rev Entomol. 1998;43: 70–726.

3. Chandrasena DI, Signorini AM, Abratti G, Storer NP, Olaciregui ML, Alves AP, et al. Characterization of field-evolved resistance to Bacillus thuringiensis-derived Cry1F δ-endotoxin in Spodoptera frugiperda populations from Argentina. Pest Manag Sci 2018;74: 746–754. doi: 10.1002/ps.4776 29072821

4. Grimi DA, Parody B, Ramos ML, Machado M, Ocampo F, Willse A, et al. Field-evolved resistance to Bt maize in sugarcane borer (Diatraea saccharalis) in Argentina. Pest Manag Sci. 2018;74: 905–913. doi: 10.1002/ps.4783 29095565

5. Jin L, Wang J, Guan F, Zang J, Yu S, Liu S, et al. Dominant point mutation in a tetraspanin gene associated with field-evolved resistance if cotton bollworm to transgenic Bt cotton. Proc. Natl. Acad. Sci. U.S.A. 2018;116: 1816–1818.

6. Smith JL, Lepping MD, Rule DM, Farhan Y, Schaafsma AW. Evidence for field-evolved resistance of Striacosta albicosta (Lepidoptera : Noctuidae) to Cry1F Bacillus thuringiensis Protein and Transgenic Corn Hybrids in Ontario, Canada. 2017;110: 2217–2228.

7. Tabashnik BE, Carrière Y. Success and failures of transgenic crops: Global patterns of field-evolved resistance. In: Soberón M, Gao Y, Bravo A., editors. Characterization and strategies for GM crops producing Bacillus thuringiensis. Wallingford, UK: CAB International; 2015. pp. 1–14.

8. Tabashnik BE, Carrière Y. Surge in insect resistance to transgenic crops and prospects for sustainability. Nat Biotechnol. 2017;35(10): 926–935. doi: 10.1038/nbt.3974 29020006

9. Calatayud PA, Le Ru BP, Van den Berg J, Schulthess F. Ecology of the African maize stalk borer, Busseola fusca (Lepidoptera: Noctuidae) with special reference to insect-plant interactions. Insects. 2014;5: 539–563. doi: 10.3390/insects5030539 26462824

10. Kruger M, Van Rensburg JBJ, Van den Berg J. Resistance to Bt maize in Busseola fusca (Lepidoptera: Noctuidae) form Vaalharts, South Africa. Environ Entomol. 2011;40: 477–483.

11. Kruger M, Van Rensburg JBJ, Van den Berg J. Transgenic Bt maize: Farmers’ perceptions, refuge compliance and reports of stem borer resistance in South Africa. J Appl Entomol. 2012;136: 38–50.

12. Tabashnik BE, Van Rensburg JBJ, Carrière Y. Field-evolved insect resistance to Bt crops: definition, theory, and data. J Econ Entomol. 2009;102(6): 2011–2025. doi: 10.1603/029.102.0601 20069826

13. Aheto DW, Bøhn T, Breckling B, Van den Berg J, Ching LL, Wikmark O. Implications of GM crops in subsistence-based agricultural systems in Arica. In: Breckling B, Verhoeven R, editors. GM Crop Cultivation-Ecological effects in a landscape scale. Frankfurt: Peter Lang; 2013. pp. 93–103.

14. Bøhn T, Aheto DW, Mwangala FS, Fisher K, Bones IL, Simoloka C, et al. Pollen-mediated gene flow and seed exchange in smallscale Zambian maize farming, implications for biosafety assessment. Sci Rep. 2016. 6:34483. doi: 10.1038/srep34483 27694819

15. Ellstrand NC, Hoffman CA. Hybridization as an avenue of escape for engineered genes—strategies for risk reduction. Biosci. 1990;40: 438–442.

16. Ellstrand NC, Prentice HC, Hancock JF. Gene flow and introgression from domesticated plants into their wild relatives. Annu Rev Ecol Syst. 1999;30: 539–63.

17. Johnston J, Blancas L, Borem A. Gene flow and its consequences: a case study of Bt maize in Kenya. In: Hilbeck A, Andow DA, editors. Environmental risk assessment of genetically modified organisms. Wallingford, UK: CAB International; 2004. pp. 187–209.

18. Quist D, Chapela IH. Transgenic DNA introgressed into traditional maize landraces in Oaxaca, Mexico. Nature. 2001;414: 541–543. doi: 10.1038/35107068 11734853

19. Mercer KL, Wainwright JD. Gene flow from transgenic maize to landraces in Mexico: An analysis. Agric Ecosyst and Environ. 2007;123: 109–115.

20. Iversen M, Grønsberg IM, Van den Berg J, Fischer K, Aheto DW, Bøhn T. Detection of transgenes in local maize varieties of small-scale farmers in Eastern Cape, South Africa. PLoS ONE. 2014. 9(12): e116147. doi: 10.1371/journal.pone.0116147 25551616

21. Glaum PR, Ives AR, Andow DA. Contamination and management of resistance evolution to high-dose transgenic insecticidal crops. Theor Ecol. 2012;5: 195–209.

22. Van den Berg J. Socio-economic factors affecting adoption of improved agricultural practices by small scale farmers in South Africa. Afr J of Agric Res. 2013;8: 4490–4500.

23. Fatoretto JC, Michel AP, Silva-Filho MC, Silva N. Adaptive potential of fall armyworm (Lepidoptera: Noctuidae) limits Bt trait durability in Brazil. J Integr Pest Manag. 2017;8: 1–10.

24. Lu B. Transgene escape from GM crops and potential biosafety consequences: an environmental perspective. International Centre for Genetic Engineering and Biotechnology (ICGEB), Collection of Biosafety Reviews. Trieste: ICGEB Press. 2008;4: 66–141.

25. Roush RL. Managing pests and their resistance to Bacillus thuringiensis: Can transgenic plants be better than crop sprays? Biocontrol Sci Technol. 1994;4: 501–516.

26. Carroll MW, Head G, Caprio M. When and where a seed mix refuge makes sense for managing insect resistance to Bt plants. Crop Prot. 2012;38: 74–79.

27. Kotey D, Assefa Y, Obi A, Van den Berg J. Disseminating genetically modified (GM) maize technology to smallholder farmers in the Eastern Cape province of South Africa: Extension personnel’s’ awareness of stewardship requirements and dissemination practices. S Afr J Agric Ext. 2016;44: 59–74.

28. Kotey DA, Assefa Y, Van den Berg J. Enhancing smallholder farmers’ awareness of GM maize technology, management practices and compliance to stewardship requirements in the Eastern Cape Province of South Africa: the role of public extension and advisory services. S Afr J Agric Ext. 2017a;45: 49–63.

29. Assefa Y, Van den Berg J. Genetically modified maize: adoption practices of small-scale farmers in South Africa and implications for resource poor farmers on the continent. Asp Appl Biol. 2010;96: 215–224.

30. Azadi H, Samiee A, Moahmoudi H, Jouzi Z, Kachak PR, De Maeyer P, et al. Genetically modified crops and small-scale farmers: main opportunities and challenges. Crit Rev Biotech. 2015;36: 434–446.

31. Jacobson K, Myhr AI. GM crops and smallholders: biosafety and local practice. J Environ Dev. 2013;221: 104–124.

32. Bates SL, Zhao JZ, Roush RT, Shelton AM. Insect resistance management in GM crops: Past, present and future. Nat Biotechnol. 2005;23: 57–62. doi: 10.1038/nbt1056 15637622

33. Chilcutt CF, Tabashnik BE. Contamination of refuges by Bacillus thuringiensis toxin genes from transgenic maize. Proc Natl Acad Sci USA. 2004;101: 7526–7529. doi: 10.1073/pnas.0400546101 15136739

34. Burkness EC, O’Rourke PK, Hutchison WD. Cross-pollination of nontransgenic corn ears with transgenic Bt corn: efficacy against lepidopteran pests and implications for resistance management. J Econ Entomol. 2011;104: 1476–1479. doi: 10.1603/ec11081 22066174

35. Huang F, Ghimire MN, Leonard BR, Daves C, Levy R, Baldwin J. Extended monitoring of resistance to Bacillus thuringiensis Cry1Ab maize in Diatraea saccharalis (Lepidoptera: Crambidae). GM Crops Food. 2012;3: 245–254. doi: 10.4161/gmcr.20539 22688686

36. Krupke C, Marquardt P, Johnson W, Weller S, Conley SP. Volunteer corn presents new challenges for insect resistance management. Agron J. 2009;101: 797–799.

37. South African National Biodiversity Institute. Monitoring the environmental impacts of GM maize in South Africa. The outcomes of the South Africa-Norway Biosafety Collaboration Project (2008–2010). 2011. Department of Environmental Affairs, South Africa & South African National Biosafety Institute, Pretoria, South Africa. https://www.sanbi.org/sites/default/files/documents/documents/sanbimaizereportlr.pdf. Cited 20 April 2016.

38. Abel CA, Adamzcyk JJ. Relative concentration of Cry1A in maize leaves and cotton bolls with diverse chlorophyll content and corresponding larval development of fall armyworm (Lepidoptera: Noctuidae) and southwestern corn borer (Lepidoptera: Crambidae) on maize whorl leaf profiles. J Econ Entomol. 2004;97: 1737–1744. doi: 10.1603/0022-0493-97.5.1737 15568367

39. Fearing PL, Brown D, Vlachos D, Meghji M, Privalle L. 1997. Quantitative analysis of CryIA(b) expression in Bt maize plants, tissues, and silage and stability of expression over successive generations. Mol Breed. 1997;3: 169–176.

40. Kruger M, Van Rensburg JBJ, Van den Berg J. No fitness costs associated with resistance of Busseola fusca (Lepidoptera: Noctuidae) to genetically modified Bt maize. Crop Prot. 2014; 55: 1–6.

41. Kotey DA, Obi A, Assefa Y, Erasmus A, Van den Berg J. Monitoring resistance to Bt maize in field populations of Busseola fusca (Fuller) (Lepidoptera: Noctuidae) from smallholder farms in the Eastern Cape Province of South Africa. Afr Entomol 2017b,25: 200–209.

42. Strydom E, Erasmus A, Du Plessis H, Van den Berg J. Resistance status of Busseola fusca (Lepidoptera: Noctuidae) populations to single- and stacked-gene Bt maize in South Africa. J Econ Entomol. 2019;112: 305–315. doi: 10.1093/jee/toy306 30321350

43. Park J, Kim H, Lee G, Yu J, Park Y. Stable inheritance of an integrated transgene and its expression in phenylethylisothiocyanate-enriched transgenic Chinese cabbage. Korean J Hortic Sci. 2015;34: 112–121.

44. Wu G, Cui H, Ye G, Xia Y, Sardana R, Cheng X, et al. Inheritance and expression of the cry1Ab gene in Bt (Bacillus thuringiensis) transgenic rice. Theor Appl Genet. 2002;104: 727–734. doi: 10.1007/s001220100689 12582680

45. Canming T, Jing S, Xiefi Z, Wangzhen G, Tianzhen Z, Jinlian S, et al. Inheritance of resistance to Helicoverpa armigera of 3 kinds of transgenic Bt maize strains available in upland cotton in China. Chin Sci Bull. 2000;45: 363–367.

46. Christou P, Swain WF, Yang N, McCabe DE. Inheritance and expression of foreign genes in transgenic soybean plants. Proc Natl Acad Sci USA. 1989;86: 7500–7504. doi: 10.1073/pnas.86.19.7500 16594073

47. Duan X, Li X, Xue Q, Abo-El-Saad M, Xu D, Wu R. Transgenic rice plants harbouring an introduced potato proteinase inhibitor II gene are insect resistant. Nat Biotechnol. 1996;14: 494–498. doi: 10.1038/nbt0496-494 9630927

48. Ivo NL, Nascimento CP, Vieira LS, Campos FAP, Aragão FJA. Biolistic-mediated genetic transformation of cowpea (Vigna unguiculata) and stable Mendelian inheritance of transgenes. Plant Cell Rep. 2008;27: 1475–1483. doi: 10.1007/s00299-008-0573-2 18587583

49. Micallef MC, Austin S, Bingham ET. Improvement of transgenic alfalfa by backcrossing. In Vitro Cell Dev Biol Plant. 1995;31: 187–192.

50. Xia H, Lu BR, Su J, Chen R, Rong J, Song, Z, et al. 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. 2009;119: 635–644. doi: 10.1007/s00122-009-1075-5 19504082

51. Zhang B, Guo T, Wang Q. Inheritance and segregation of exogenous genes in transgenic cotton. J Genet. 2000;79: 71–75.

52. Tritikova M, Wikmark OG, Zemp N, Widmer A, Hilbeck A. Transgene expression and Bt protein content in transgenic Bt maize (MON810) under optimal and stressful environmental conditions. 2015. PLoS ONE 10(4): e0123011. doi: 10.1371/journal.pone.0123011 25853814

53. Wang Z, Yu C, Jaing L. Segregation and expression of transgenes in the progenies of Bt transgenic rice crossed to conventional rice varieties. Afr J Biotechnol. 2012;11: 7812–7818.

54. Khan ZR, Midega CAO, Wadhams LJ, Pickett JA, Mumini A. Evaluation of Napier grass (Pennisetum purpureum) varieties for use as trap plants for the management of African stemborer (Busseola fusca) in a push–pull strategy. Entomol Exp Appl. 2007;124: 201–211.

55. Van den Berg J, De Bruyn AJM, Van Hamburg H. Oviposition preference and survival of the maize stem borer, Busseola fusca (Lepidoptera: Noctuidae) on Napier grasses (Pennisetum spp.) and maize. Afr Entomol. 2006;14: 211–218.

56. Jarvis DJ, Hodgkin T. Wild relatives and crop cultivars: detecting natural introgression and farmer selection of new genetic combination in agro-ecosystems. Mol Ecol. 1999;8: 159–173. doi: 10.1046/j.1365-294x.1999.00799.x

57. Sachs ES, Benedict JH, Stelly DM, Taylor JF, Altman DW, Berberich SA, et al. Expression and segregation of genes encoding Cry1A insecticidal proteins in cotton. Crop Sci. 1998;38: 1–11.

58. Bakó A, Gell G, Zambó A, Spitkó T, Pók I, Pintér J, et al. Monitoring transgene expression levels in different genotypes of field grown maize (Zea mays L.). S Afr J Bot. 2013;84: 6–10.

59. Bellon M, Berthaud J. Transgenic maize and the evolution of landrace diversity in Mexico. The importance of farmers’ behaviour. Plant Physiol. 2004;134: 883–888. doi: 10.1104/pp.103.038331 15020750

60. Llewellen D, Cousin Y, Mathews A, Hartweck L, Lyon B. Expression of Bacillus thuringiensis insecticidal protein genes in transgenic crop plants. Agric Ecosyst Environ. 1994;49: 85–93.

61. Tabashnik BE, Brévault T, Carrière Y. Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol. 2013;31: 510–52. doi: 10.1038/nbt.2597 23752438

Introgression of a cry1Ab transgene into open pollinated maize and its effect on Cry protein concentration and target pest survival

Souhrn

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