Field-evolved resistance to Cry1F maize by Spodoptera frugiperda (Lepidoptera: Noctuidae) in Brazil

Crop Protection

Volumn 64, Issue , 2014, Pages 150-158

  Farias, Juliano Ricardo ^a   Andow, David A ^b   Horikoshi, Renato Jun ^a   Sorgatto, Rodrigo José ^a   Fresia, Pablo ^a   dos Santos, Antonio Cesar ^c   Omoto, Celso ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF MINNESOTA   (United States)

^c DOW AGROSCIENCES LLC   (United States)

Author keywords

Bacillus thuringiensis; Cry1F; Fall armyworm; Genetic basis; Plant survival

Indexed keywords

BACTERIUM; BIOASSAY; BIOLOGICAL CONTROL; GENE EXPRESSION; MAIZE; MOTH; PROTEIN; SURVIVAL;

BAHIA; BRAZIL;

EID: 84904113806     PISSN: 02612194     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cropro.2014.06.019     Document Type: Article

References (55)

1. Abbott W.S. Amethod of computing the effectiveness of an insecticide. J.Econ. Entomol. 1925, 18:265-267.
2. Andow D.A. The risk of resistance evolution in insects to transgenic insecticidal crops. Colln. Biosaf. Rev. 2008, 4:142-199.
3. Andow D.A., Alstad D.N. F2 screen for rare resistance alleles. J.Econ. Entomol. 1998, 91:572-578.
4. Ashley T.R., Wiseman B.R., Davis F.M., Andrews K.L. The fall armyworm: a bibliography. Fla. Entomol. 1989, 72:152-202. 10.2307/3494982.
5. Bernardi O., Malvestiti G.S., Dourado P.M., Oliveira W.S., Martinelli S., Berger G.U., Head G.P., Omoto C. Assessment of the high-dose concept and level of control provided by MON 87701×MON 89788 soybean against Anticarsia gemmatalis and Pseudoplusia includens (Lepidoptera: Noctuidae) in Brazil. Pest Manag. Sci. 2012, 68:1083-1091. 10.1002/ps.3271.
6. Blanco C.A., Portilla M., Jurat-Fuentes J.L., Sánchez J.F., Viteri D., Vega-Aquino P., Terán-Vargas A.P., Azuara-Domínguez A., López J.D., Arias R., Zhu Y.C., Lugo-Barrera D., Jackson R. Susceptibility of isofamilies of Spodoptera frugiperda (Lepidoptera: Noctuidae) to Cry1Ac and Cry1Fa proteins of Bacillus thuringiensis. Southwest Entomol. 2010, 35:409-415. 10.3958/059.035.0325.
7. Bourguet D., Genissel A., Raymond M. Insecticide resistance and dominance levels. J.Econ. Entomol. 2000, 93:1588-1595.
8. Curtis C.F., Cook L.M., Wood R.J. Selection for and against insecticide resistance and possible methods of inhibiting the evolution of resistance in mosquitoes. Ecol. Entomol. 1978, 3:273-287. 10.1111/j.1365-2311.1978.tb00928.x.
9. Dow Agrosciences Industrial Ltda Commercial Release of Genetically Modified Corn, Herculex Corn (TC1507) 2008, Technical Opinion No. 1679/2008. Comissão Técnica Nacional de Biossegurança (CTNBio). [Online]. Available at:, (accessed 20.10.13.). http://www.ctnbio.gov.br/index.php/content/view/12818.html.
10. Dhurua S., Gujar G.T. Field-evolved resistance to Bt toxin Cry1Ac in the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), from India. Pest Manag. Sci. 2011, 67:898-903. 10.1002/ps.2127.
11. Fabrick J.A., Tabashnik B.E. Similar genetic basis of resistance to Bt toxin Cry1Ac in boll-selected and diet-selected strains of pink bollworm. PLoS One 2012, 7:e35658. 10.1371/journal.pone.0035658.
12. Ffrench-Constant R.H., Steichen J., Rocheleau T.A., Aronstein K., Roush R.T. Asingle amino acid substitution in a gamma-aminobutyric acid subtype A receptor locus is associated with cyclodiene insecticide resistance in Drosophila populations. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:1957-1961. 10.1073/pnas.90.5.1957.
13. Finney D.J. Probit Analysis 1971, Cambridge University Press, London, UK. third ed.
14. Gassmann A.J., Petzold-Maxwell J.L., Keweshan R.S., Dunbar M.W. Field-evolved resistance to Bt maize by western corn rootworm. PLoS One 2011, 6:e22629.
15. Giolo F.P., Grützmacher A.D., Garcia M.S., Busato G.R. Parâmetros biológicos de Spodoptera frugiperda (J. E. Smith, 1797) (Lep.: Noctuidae), oriundas de diferentes localidades e hospedeiros. Rev. Bras. Agrociênc. 2002, 8:219-224.
16. 2 screening for resistance to pyramided Bacillus thuringiensis maize in Louisiana and Mississippi populations of Diatraea saccharalis (Lepidoptera: Crambidae). Pest Manag. Sci. 2011, 67:1269-1276. 10.1002/ps.2182.
17. 2 screen for resistance to a Bacillus thuringiensis-maize hybrid in the sugarcane borer (Lepidoptera: Crambidae). Bull. Entomol. Res. 2007, 97:437-444.
18. Huang F., Leonard B.R., Andow D.A. Sugarcane borer (Lepidoptera: Crambidae) resistance to transgenic Bacillus thuringiensis maize. J.Econ. Entomol. 2007, 100:164-171. 10.1603/0022-0493(2007)100[164:SBLCRT]2.0.CO;2.
19. Huang F., Parker R., Leonard R., Yong Y., Liu J. Frequency of resistance alleles to Bacillus thuringiensis-corn in Texas populations of the sugarcane borer, Diatraea saccharalis (F.) (Lepidoptera: Crambidae). Crop Prot. 2009, 28:174-180. 10.1016/j.cropro.2008.10.002.
20. Kasten Júnior P., Preceti A.C.M., Parra J.R.P. Dados biológicos comparativos de Spodoptera frugiperda (JE Smith, 1797) em duas dietas artificiais e substrato natural. Rev. Agric. 1978, 53:68-78.
21. Lewis E.B. Pseudoallelism and gene evolution. Cold Spring Harbor Symp. Quant. Biol. 1951, 16:159-174. 10.1101/SQB.1951.016.01.014.
22. Liu F., Xu Z., Zhu Y.C., Huang F., Wang Y., Li H., Li H., Gao C., Zhou W., Shen J. Evidence of field-evolved resistance to Cry1Ac-expressing Bt cotton in Helicoverpa armigera (Lepidoptera: Noctuidae) in northern China. Pest Manag. Sci. 2010, 66:155-161.
23. Luo K.E., Banks D., Adang M.J. Toxicity, binding, and permeability analyses of four Bacillus thuringiensis Cry1D-Endotoxins using brush border membrane vesicles of Spodoptera exigua and Spodoptera frugiperda. Appl. Microbiol. 1999, 65:457-464.
24. Mahon R.J., Downes S., James B. Vip3A resistance alleles exist at high levels in Australian targets before release of cotton expressing this toxin. PLoS One 2012, 7:e39192. 10.1371/journal.pone.0039192.
25. Mahon R.J., Downes S., James W., Parker T. Why do F1 screens estimate higher frequencies of Cry2ab resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) than do F2 screens?. J.Econ. Entomol. 2010, 103:472-481. 10.1603/EC09225.
26. Marçon P.C.R.G., Young L.J., Steffey K.L., Siegfried B.D. Baseline susceptibility of European corn borer (Lepidoptera: Crambidae) to Bacillus thuringiensis toxins. J.Econ. Entomol. 1999, 92:279-285.
27. Martinelli S., Barata R.M., Zucchi M.I., Silva-Filho M.C., Omoto C. Molecular variability of Spodoptera frugiperda (Lepidoptera: Noctuidae) populations associated to maize and cotton crops in Brazil. J.Econ. Entomol. 2006, 99:519-526. 10.1603/0022-0493-99.2.519.
28. Martinelli S., Clark P.L., Zucchi M.I., Silva-Filho M.C., Foster J.E., Omoto C. Genetic structure and molecular variability of Spodoptera frugiperda (Lepidoptera: Noctuidae) collected in maize and cotton fields in Brazil. Bull. Entomol. Res. 2007, 97:225-231. 10.1017/S0007485307004944.
29. Mcgaughey W.H., Whalon M.E. Managing insect resistance to Bacillus thuringiensis toxins. Science 1992, 258:1451-1555. 10.1126/science.258.5087.1451.
30. McKenzie J.A., Batterham P. The genetic, molecular and phenotypic consequences of selection for insecticide resistance. Trends Ecol. Evol. 1994, 9:166-169. 10.1016/0169-5347(94)90079-5.
31. Nagoshi R.N., Meagher R.L. Review of fall armyworm (Lepidoptera: Noctuidae) genetic complexity and migration. Fla. Entomol. 2008, 91:546-554.
32. Nagoshi R.N., Meagher R.L., Jenkins D.A. Puerto Rico fall armyworm has only limited interactions with those from Brazil or Texas but could have substantial exchanges with Florida populations. J.Econ. Entomol. 2010, 103:360-367. 10.1603/EC09253.
33. Raymond M., Callaghan A., Fort P., Pasteur N. Worldwide migration of amplified insecticide resistance genes in mosquitoes. Nature 1991, 350:151-153. 10.1038/350151a0.
34. Ritchie W., Hanway J.J., Benson G.O. How a Corn Plant Develops 1997, Special Report No. 48, Iowa State University, Ames, IA. J.C. Herman (Ed.).
35. Robertson J.L., Preisler H.K. Pesticide Bioassays with Arthropods 1992, CRC Press, London.
36. Robertson J., Preisler H., Russell R. PoloPlus User's Guide 2003, Version 1.0, LeOra Software, Petaluma, CA.
37. Saeglitz C., Bartsch D., Eber S., Gathmann A., Priesnitz K.U., Schuphan I. Monitoring the Cry1Ab susceptibility of European corn borer in Germany. J.Econ. Entomol. 2006, 99:1768-1773. 10.1603/0022-0493-99.5.1768.
38. Santos L.M., Redaelli L.R., Diefenbach L.M.G., Efrom C.F.S. Larval and pupal stage of Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) in sweet and field corn genotypes. Braz. J. Biol. 2003, 63:627-633.
39. SAS Institute Inc. SAS/STAT: Statistical Analysis System: Getting Started with the SAS Learning 2004, SAS Institute Inc., Cary, NC.
40. ® 10 Discovering JMP 2012, SAS Institute Inc., Cary, NC.
41. Siebert M.W., Babock J.M., Nolting S., Santos A.C., Adamczyk J.J., Neese P.A., King J.E., Jenkins J.N., Mccarty J., Lorenz G.M., Fromme D.D., Lassiter R.B. Efficacy of Cry1F insecticidal protein in maize and cotton for control of fall armyworm (Lepidoptera: Noctuidae). Fla. Entomol. 2008, 91:555-565.
42. Siegfried B.D., Spencer T., Crespo A.L., Storer N.P., Head G.P., Owens E.D., Guyer D. Ten years of Bt resistance monitoring in the European corn borer: what we know, what we don't know, and what we can do better. Am. Entomol. 2007, 53:208-214.
43. Sparks A.N. Areview of the biology of the fall armyworm. Fla. Entomol. 1979, 62:82-87. 10.2307/3494083.
44. Storer N.P., Babcock J.M., Schlenz M., Meade T., Thompson G.D., Bing J.W., Huckaba R.M. Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J.Econ. Entomol. 2010, 103:1031-1038. 10.1603/EC10040.
45. Storer N.P., Kubiszak M.E., King J.E., Thompson G.D., Santos A.C. Status of resistance to Bt maize in Spodoptera frugiperda: lessons from Puerto Rico. J.Invertebr. Pathol. 2012, 110:294-300. 10.1016/j.jip.2012.04.007.
46. Tabashnik B.E., Liu Y., Dennehy T.J., Sims M.A., Sisterson M.S., Biggs R.W., Carrière Y. Inheritance of resistance to Bt toxin Cry1Ac in a field-derived strain of pink bollworm (Lepidoptera: Gelechiidae). J.Econ. Entomol. 2002, 95:1018-1026. 10.1603/0022-0493-95.5.1018.
47. Tabashnik B.E., Liu Y., Malvar T., Heckel D.G., Masson L., Ballester V., Granelo F., Mensura J.L., Ferré J. Global variation in the genetic and biochemical basis of diamondback moth resistance to Bacillus thuringiensis. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:12780-12785. 10.1073/pnas.94.24.12780.
48. Tabashnik B.E., Liu Y., Malvar T., Heckel D.G., Masson L., Ferré J. Insect resistance to Bacillus thuringiensis: uniform or diverse?. Philos. Trans. R. Soc. B 1998, 353:1751-1756.
49. Tabashnik B.E., Liu Y., Unnithan D.C., Carrière Y., Dennehy T.J., Morin S. Shared genetic basis of resistance to Bt toxin Cry1ac in independent strains of pink bollworm. J.Econ. Entomol. 2004, 97:721-726. 10.1603/0022-0493(2004)097[0721:SGBORT]2.0.CO;2.
50. Van Rensburg J.B.J. First report of field resistance by the stem borer, Busseola fusca (Fuller) to Bt-transgenic maize. S.Afr. J. Plant. Soil 2007, 24:147-151. 10.1080/02571862.2007.10634798.
51. Waquil J.M., Vilella F.M.F., Foster J.E. Resistência de milho (Zea mays L.) transgênico à lagarta-do-cartucho, Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae). Rev. Bras. Milho Sorgo 2002, 1:1-11.
52. Waquil J.M., Vilella F.M.F., Siegfried B.D., Foster J.E. Atividade biológica das toxinas do Bt, Cry1A(b) e Cry1F em Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae). Rev. Bras. Milho Sorgo 2004, 3:161-171.
53. 2 screen to monitor frequency of resistance alleles to Bt cotton in field populations of Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae). Pest Manag. Sci. 2009, 65:391-397. 10.1002/ps.1703.
54. Yue B., Huang F., Leonard B.R., Moore S., Parker R., Andow D.A., Cook D., Emfinger K., Lee D.R. Verifying an F1 screen for identification and quantification of rare Bacillus thuringiensis resistance alleles in field populations of sugarcane borer, Diatraea saccharalis. Entomol. Exp. Appl. 2008, 129:172-180. 10.1111/j.1570-7458.2008.00761.x.
55. Zhang H., Tian W., Zhao J., Jin L., Yang J., Liu C., Yang Y., Wu S., Wu K., Cui J., Tabashnik B.E., Wu Y. Diverse genetic basis of field-evolved resistance to Bt cotton in cotton bollworm from China. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:10275-10280. 10.1073/pnas.1200156109.