Linkage of an ABCC transporter to a single QTL that controls Ostrinia nubilalis larval resistance to the Bacillus thuringiensis Cry1Fa toxin

Insect Biochemistry and Molecular Biology

Volumn 63, Issue , 2015, Pages 86-96

  Coates, Brad S ^a   Siegfried, Blair D ^b  

^a IOWA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

Crystalline (Cry) toxin resistance; Genotyping by sequencing; QTL mapping

Indexed keywords

ABC TRANSPORTER; BACTERIAL PROTEIN; ENDOTOXIN;

ANIMAL; BACILLUS THURINGIENSIS; GENETIC LINKAGE; GENETICS; LARVA; MAIZE; MOTH; MUTATION; PHYSIOLOGY; QUANTITATIVE TRAIT LOCUS; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSGENIC PLANT;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; ENDOTOXINS; GENETIC LINKAGE; LARVA; MOTHS; MUTATION; PLANTS, GENETICALLY MODIFIED; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; ZEA MAYS;

EID: 84949304583     PISSN: 09651748     EISSN: 18790240     Source Type: Journal    
DOI: 10.1016/j.ibmb.2015.06.003     Document Type: Article

References (89)

1. Alstad D.N., Andow D.A. Managing the evolution of insect resistance to transgenic plants. Science 1995, 268:1894-1896.
2. Alvi A.H.K., Sayyed A.H., Naeem M., Ali M. Field evolved resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) to Bacillus thuringiensis toxin Cry1Ac in Pakistan. PLoS One 2012, 7:e47309.
3. Atsumi S., Miyamoto K., Yamamoto K., Narukawa J., Kawai S., Sezutsu H., Kobayashi I., et al. Single amino acid mutation in an ATP-binding cassette transporter gene causes resistance to Bt toxin Cry1Ab in the silkworm, Bombyx mori. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E1591-E1598.
4. Baird N.A., Etter P.D., Atwood T.S., Currey M.C., Shiver A.L., et al. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 2008, 3:e3376.
5. Bates S.L., Zhao J.Z., Roush R.T., Shelton A.M. Insect resistance management in GM crops: past, present and future. Nat. Biotechnol. 2005, 23:57-62.
6. Baxter S., Zhao J.Z., Gahan L.J., Shelton A.M., Tabashnik B.E., Heckel D.G. Novel genetic basis of field-evolved resistance to Bt toxins in Plutella xylostella. Insect Mol. Biol. 2005, 14:327-334.
7. Baxter S.W., Badenes-Perez F.R., Morrison A., Vogel H., Crickmore N., Kain W., Wang P., Heckel D.G., Jiggins C.D. Parallel evolution of Bacillus thuringiensis toxin resistance in Lepidoptera. Genetics 2011, 189:675-679.
8. Black W.C., Vontas J. Affordable assays for genotyping single nucleotide polymorphism in insects. Insect Mol. Biol. 2007, 16:377-387.
9. Bolin P.C., Hutchison W.D., Andow D.A. Long-term selection for resistance to Bacillus thuringiensis Cry1Ac endotoxin in a Minnesota population of European corn borer (Lepidoptera: Crambidae). J. Econ. Entomol. 1999, 92:1021-1030.
10. Bourguet D., Chaufaux J., Seguin J.M., Buisson C., Hinton J.L., Stodola T.J., et al. Frequency of alleles conferring resistance to Bt maize in French and US corn belt populations of the European corn borer. Theor. Appl. Genet. 2002, 106:1225-1233.
11. Bravo A., Gill S.S., Soberon M. Mode of action of Bacillus thuringiensis Cry1 and Cyt toxins and thir potential for insect control. Toxicon 2007, 49:423-435.
12. Campagne P., Kruger M., Pasquet R., Le Ru B., Van den Berg J. Dominant inheritance of field-evolved resistance to Bt corn in Busseola fusca. PLoS ONE 2013, 8:e69675.
13. Coates B.S., Sumerford D.V., Lewis L.C. A (β-1,3-galactosyltransferase and brainiac/bre5 homolog expressed in the midgut did not contribute to a Cry1Ab toxin resistance trait in Ostrinia nubilalis. Insect Biochem. Mol. Biol. 2007, 37:346-355.
14. 2 larval weights when fed on toxin-containing diet. J. Insect Sci. 2008, 8:21.
15. Coates B.S., Sumerford D.V., Lopez M.D., Wang H., Fraser L.M., Kroemer J.A., Spencer T., Kim K.S., Abel C.A., Hellmich R.L., Siegfried B.D. A single major QTL controls the expression of a larval Cry1F resistance trait in Ostrinia nubilalis (Lepidoptera: Crambidae). Genetica 2011, 139:961-972.
16. Coates B.S., Bayles D.O., Wanner K.W., Robertson H.M., Hellmich R.L., Sappington T.W. The application and performance of single nucleotide polymorphism (SNP) markers for population genetic analyses of Lepidoptera. Front. Genet. 2011, 2:38.
17. Coates B.S., Sumerford D.V., Hellmich R.L., Abel C.A. Unlinked genetic loci control the reduced transcription of aminopeptidase N 1 and 3 in the European corn borer and determine tolerance to Bacillus thuringiensis Cry1Ab toxin. Insect Biochem. Mol. Biol. 2013, 43:1152-1160.
18. Crava C.M., Bel Y., Jakubowska A.K., Ferre J., Escriche B. Midgut aminopeptidase N isoforms from Ostrinia nubilalis: activity characterization and differential binding to Cry1Ab and Cry1Fa proteins from Bacillus thuringiensis. Insect Biochem. Mol. Biol. 2013, 42:924-935.
19. Danecek P., Auton A., Abecasis G., Albers C.A., Banks E., DePristo M.A., Handsaker R., Lunter G., Marth G., Sherry S.T., McVean G., Durbin R. The variant call format and VCFtools. Bioinformatics 2011, 27:2156-2158. 1000 Genomes Project Analysis Group.
20. 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.
21. Downes S., Mahon R. Evolution, ecology and management of resistance in Helicoverpa spp. to Bt cotton in Australia. J. Invertebr. Pathol. 2012, 110:281-286.
22. Downes S., Mahon R. Successes and challenges of managing resistance in Helicoverpa armigera Bt cotton in Australia. Gm. Crops Food 2012, 3:228-234.
23. Elshire R.J., Glaubitz J.C., Sun Q., Poland J.A., Kawamoto K., Buckler E.S., Mitchell S.E. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PloS One 2011, 6:e19379.
24. Farias J.R., Andow D.A., Horiskoshi R.J., Sorgatto R.J., Fresia P.F., Santos A.C., Omoto C. Field-evolved resistance to Cry1F maize by Spodoptera frugiperda (Lepidoptera: Noctuidae) in Brazil. Crop Prot. 2014, 64:150-158.
25. ffrench-Constant R.H., Anthony N., Aronstein K., Rocheleau T., Stilwell G. Cyclodiene insecticide resistance: from molecular to population genetics. Ann. Rev. Entomol. 2000, 45:449-466.
26. Fu L., Niu B., Zhu Z., Wu S., Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 2012, 28:3150-3152.
27. Gahan L.J., Gould F., Heckel D.G. Identification of a gene associated with Bt resistance in Heliothis virescens. Science 2001, 293:857-860.
28. Gahan L.J., Ma Y.T., Coble M.L.M., Gould F., Moar W.J., Heckel D.G. Genetic basis of resistance to Cry1Ac and Cry2Aa in Heliothis virescens (Lepidoptera:Noctuidae). J. Econ. Entomol. 2005, 98:1357-1368.
29. Gahan L.J., Pauchet Y., Vogel H., Heckel D.G. An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1Ac toxin. PLoS Genet. 2010, 6:e1001248.
30. Gaspers C., Siegfried B.D., Spencer T., Alves A.P., Storer N.P., Schuphan I., Eber S. Susceptibility of European and North American populations of the European corn borer to the Cry1F insecticidal protein. J. Appl. Entomol. 2011, 135:7-16.
31. 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.
32. Gassmann A.J., Petzold-Maxwell J.L., Clifton E.H., Dunbar M.W., Hoffmann A.M., Ingber D.A., Keweshan R.S. Field-evolved resistance by western corn rootworm to multiple Bacillus thuringiensis toxins in transgenic maize. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:5141-5146.
33. Gould F. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu. Rev. Entomol. 1998, 43:701-726.
34. Greenplate J.T., Mullins J.W., Penn S.R., Dahm A., Reich B.J., Osborn J.A., Rahn P.R., Ruschke L., Shappley Z.W. Partial characterization of cotton plants expressing two toxin proteins from Bacillus thuringiensis: relative toxin contribution, toxin interaction, and resistance management. Appl. Entomol. 2003, 127:340-347.
35. Griffitts J.S., Aroian R.V. Many roads to resistance: how invertebrates adapt to Bt toxins. Bioessays 2005, 27:614-624.
36. Gunning R.V., Dang H.T., Kemp F.C., Nicholson I.C., Moores G.D. New resistance mechanism in Helicoverpa armigera threatens transgenic crops expressing Bacillus thuringiensis Cry1Ac toxin. Appl. Environ. Microbiol. 2005, 71:2558-2563.
37. Guo Z., Kang S., Chen D., Wu Q., Wang S., Xie W., Zhu X., Baxter S.W., Zhou X., Jurat-Fuentes J.L., Zhang Y. MAPK signaling pathway alters expression of midgut ALP and ABCC genes and causes resistance to Bacillus thuringiensis Cry1Ac toxin in Diamondback Moth. PLoS Genet. 2015, 11:e1005124.
38. Heckel D.G., Gahan L.J., Daly J.C., Trowell S. A genomic approach to understanding Heliothis and Helicoverpa resistance to chemical and biological insecticides. Phil. Trans. R. Soc. Lond. B 1998, 353:1713-1722.
39. Heckel D.G. Learning the ABCs of Bt: ABC transporters and insect resistance to Bacillus thuringiensis provide clues to a crucial step in toxin mode of action. Pestic. Biochem. Physiol. 2012, 104:103-110.
40. Herrero S., Gechev T., Bakker P.L., Moar W.J., de Maagd R.A. Bacillus thuringiensis Cry1Ca-resistant Spodoptera exigua lacks expression of one of four aminopeptidase N genes. BMC Genom. 2005, 6:96.
41. Hua G., Masson L., Jurat-Fuentes J.L., Schwab G., Adang M.J. Binding analyses of Bacillus thuringiensis Cry-endotoxins using brush border membrane vesicles of Ostrinia nubilalis. Appl. Environ. Microbiol. 2001, 67:872-879.
42. Huang F., Andow D.A., Buschman L.L. Success of the high-dose/refuge resistance management strategy after 15 years of Bt crop use in North America. Entomol. Exp. Appl. 2011, 140:1-16.
43. Huang F., Qureshi J.A., Meagher R.L., Reisig D.D., Head G.P., et al. Cry1F resistance in Fall armyworm Spodoptera frugiperda: single gene versus pyramided Bt maize. PLoS One 2014, 9:e112958.
44. Hutchison W.D., Burkness E.C., Mitchell P.D., Moon R.D., Leslie T.W., Fleischer S.J., Abrahamson M., Hamilton K.L., Steffey K.L., Gray M.E., Hellmich R.L., Kaster V., Hunt T.E., Wright R.J., Pecinovsky K.T., Rabaey T.L., Flood B.R., Raun E.S. Areawide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers. Science 2010, 330:222-225.
45. Jin L., Wei Y., Zhang L., Yang Y., Tabashnik B.E., Wu Y. Dominant resistance to Bt cotton and minor cross-resistance to Bt toxin Cry2Ab in cotton bollworm from China. Evol. Appl. 2013, 6:1222-1235.
46. Jurat-Fuentes J.L., Gould F.L., Adang M.J. Altered glycosylation of 63- and 68-kilodalton microvillar proteins in Heliothis virescens correlates with reduced Cry1 toxin binding, decreased pore formation, and increased resistance to Bacillus thuringiensis Cry1 toxins. Appl. Environ. Microbiol. 2002, 68:5711-5717.
47. Knaus B. Short Read Toolbox 2011, http://brianknaus.comlsoftware/srtoolboxlshortread.html.
48. Knowles B.H., Knight P.J.K., Ellar D.J. N-acetylgalactosamine is part of the receptor in insect gut epithelia that recognizes an insecticidal protein from Bacillus thuringiensis. Proc. R. Soc. Lond. Biol. 1991, 245:31-35.
49. Kruger M., Van Rensburg J.B.J., 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.
50. Langmead B., Salzberg S. Fast gapped-read alignment with Bowtie 2. Nat. Methods 2012, 9:357-359.
51. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. The sequence alignment/map format and SAMtools. Bioinformatics 2009, 25:2078-2079.
52. Lincoln S., Daly M., Lander E. Constructing Genetic Maps with MAPMAKER/EXP 3.0 1992, (Whitehead Institute Technical Report). third ed.
53. Mahon R.J., Downes S.J., James B. Vip3A resistance alleles exist at high levels in Australian targets before release of cotton expressing this toxin. PLoS ONE 2012, 7:e39192.
54. Matten R.S., Head G.P., MacIntoch S.C. How government regulation can help or hinder the integration of Bt crops within IPM programs. Integration of Insect Resistant Genetically Modified Crops with IPM Programs 2008, 27-39. Springer Science þ Business Media B. V, New York, USA. J. Romeis, A.M. Shelton, G.G. Kennedy (Eds.).
55. McGaughey W.H. Insect resistance to the biological insecticide Bacillus thuringiensis. Science 1985, 229:193-195.
56. Morin S., Biggs R.W., Sisterson M.S., Shriver L., Ellers-Kirk C., Higginson D., Holley D., Gahan L.J., Heckel D.G., Carrière Y., Dennehy T.J., Brown J.K., Tabashnik B.E. Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:5004-5009.
57. National Research Council Pesticide Resistance: Strategies and Tactics for Management 1986, National Academy Press, Washington, DC.
58. Onstad D.W., Guse C.A. Economic analysis of transgenic maize and nontransgenic refuges for managing European corn borer (Lepidoptera: Pyralidae). J. Econ. Entomol. 1999, 92:1256-1265.
59. Park Y., González-Martínez R.M., Navarro-Cerrillo G., Chakroun M., Kim Y., Ziarsolo P., Blanca J., Canizares J., Ferre J., Herrero S. ABCC transporters mediate insect resistance to multiple Bt toxins revealed by bulk segregant analysis. BMC Biol. 2014, 12:46.
60. Pereira E.J.G., Lang B.A., Storer N.P., Siegfried B.D. Selection for Cry1F resistance in the European corn borer and cross resistance to other Cry toxins. Entomol. Exper. Appl. 2008, 126:115-121.
61. Pereira E.J.G., Storer N.P., Siegfried B.D. Inheritance of Cry1F resistance in laboratory-selected European corn borer and its survival on transgenic corn expressing the Cry1F toxin. Bull. Entomol. Res. 2008, 98:621-629.
62. Piggot C.R., Ellar D.J. Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol. Mol. Biol. Rev. 2007, 71:255-281.
63. Riveron J.M., Yunta C., Ibrahim S.S., Djouaka R., Irving H., Menze B.D., Ismail H.M., Hemingway J., Ranson H., Albert A., Wondji C.S. The detailed molecular and structural basis through which candidate metabolic resistance genes confer resistance remains poorly characterized. Genome Biol. 2014, 15:R27.
64. Roush R.T., McKenzie J.A. Ecological genetics of insecticide and acaricide resistance. Ann. Rev. Entomol. 1987, 32:361-380.
65. Siegfried B.D., Hellmich R.L. Understanding successful resistance management: the European corn borer and Bt corn in the United States. Spec. Issue GM Crops Foods 2012, 3:184-193.
66. Siegfried B.D., Zoerb A., Spencer T. Effect of Event 176 transgenic maize on susceptibility and fitness of the European corn borer. Entomol. Exp. Appl. 2001, 100:15-20.
67. 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.
68. Siegfried B.D., Rangasamy M., Wang H., Spencer T., Haridas C.V., Tenhumberg B., Sumerford D.V., Storer N.P. Estimating the frequency of Cry1F resistance in field populations of the European corn borer (Lepidoptera: Crambidae). Pest Manag. Sci. 2014, 70:725-733.
69. Siqueira H.A.A., Moellenbeck D., Spencer T., Siegfried B.D. Cross-resistance of CrylAb-selected Ostrinia nubilalis (Lepidoptera: Crambidae) to Bacillus thuringiensis delta-endotoxins. J. Econ. Entomol. 2004, 97:1049-1057.
70. Soberon M., Gill S., Bravo A. Signaling versus punching hole: how do Bacillus thuringiensis toxins kill insect midgut cells. Cell. Mol. Life Sci. 2009, 66:1337-1349.
71. 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, 03:1031-1038.
72. Tabashnik B.E. Evolution of resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 1994, 39:47-79.
73. Tabashnik B.E. Delaying insect resistance to transgenic crops. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:19029-19030.
74. Tabashnik B.E., Carriere Y. Field-evolved resistance to Bt cotton: bollworm in the U.S. and pink bollworm in India. Southwest. Entomol. 2010, 35:417-424.
75. Tabashnik B.E., Cushing N.L., Finson N., Johnson M.W. Field development of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae). J. Econ. Entomol. 1990, 83:1671-1676.
76. Tabashnik B.E., Liu Y.B., Finson N., Masson L., Heckel D.G. One gene in diamondback moth confers resistance to four Bacillus thuringiensis toxins. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:1640-1644.
77. Tabashnik B.E., Gassmann A.J., Crowder D.W., Carriere Y. Insect resistance to Bt crops: evidence versus theory. Nat. Biotechnol. 2008, 26:199-202.
78. Tabashnik B.E., Ban Rensburg J.B.J., Carriere Y. Field-evolved insect resistance to Bt crops: definition, theory and data. J. Econ. Entomol. 2009, 102:2011-2025.
79. Tan S.Y., Cayabyab B.F., Alcantara E.P., Huang F., He K., Nickerson K.W., Siegfried B.D. Comparative binding of Cry1Ab and Cry1F Bacillus thuringiensis toxins to brush border membrane proteins from Ostrinia nubilalis, Ostrinia furnacalis and Diatraea saccharalis (Lepidoptera: Crambidae) midgut tissue. J. Invert. Pathol. 2013, 114:234-240.
80. Tiewsiri K., Wang P. Differential alteration of two aminopeptidases N associated with resistance to Bacillus thuringiensis toxin Cry1Ac in cabbage looper. Proc. Natl. Acad. Sci. USA 2011, 108:14037-14042.
81. Truong H.T., Ramos A.M., Yalcin F., de Ruiter M., van der Poel H.J.A., Huvenaars K.H.J., Hogers R.C.J., van Enckevort L.J.G., Janssen A., van Orsouw N.J., van Eijk M.J.T. Sequence-based genotyping for marker discovery and co-dominant scoring in germplasm and populations. PLoS One 2012, 7:e37565.
82. US EPA (United States Environmental Protection Agency, Washington, DC, USA) The Environmental Protection Agency's White Paper on Bt Plant-pesticide Resistance Management (EPA Publication 739-S-98-001) 1998, Available at:. http://www.epa.gov/EPA-PEST/1998/January/Day-14/paper.pdf.
83. US EPA (United States Environmental Protection Agency, Washington, DC, USA) Biopesticides Registration Action Document - Bacillus Thuringiensis Plant-incorporated Protestants. E: Benefits Assessment 2001, Available at:. http://www.epa.gov/oppbppd1/biopesticides/pips/bt_brad2/5-benefits.pdf.
84. van Rensburg J.B.J. First field report of field resistance by the stem borer, Busseola fusca (Fuller) to transgenic maize. S. Afr. J. Plant. Soil 2007, 24:147-151.
85. Vos P., Hogers R., Bleeker M., Reijans M., Lee T., Hornes M., Frijters A., Pot J., Peleman J., Kuiper M., et al. AFLP: a new technique for DNA fingerprinting. Nucl. Acids Res. 1995, 23:4407-4414.
86. Wang H., Coates B.S., Chen H., Sappington T.W., Guillemaud T., Siegfried B.D. Role of a gamma-aminobutryic acid (GABA) receptor mutation in the evolution and spread of Diabrotica virgifera virgifera resistance to cyclodiene insecticides. Insect Mol. Biol. 2013, 22:473-484.
87. Xie X., Cheng T., Wang G., Duan J., Niu W., Xia Q. Genome-wide analysis of the ATP-binding cassette (ABC) transporter gene family in the silkworm, Bombyx mori. Mol. Biol. Rep. 2012, 39:7281-7291.
88. Xu X., Yu L., Wu Y. Disruption of a cadherin gene associated with resistance of Cry1Ac δ-endotoxins of Bacillus thuringiensis in Helicoverpa armigera. Appl. Environ. Microbiol. 2005, 71:948-954.
89. Zhang X., Tiewsiri K., Kain W., Huang L., Wang P. Resistance of Trichoplusia ni to Bacillus thuringiensis toxin Cry1Ac is independent of alteration of the cadherin-like receptor for Cry toxins. PLoS ONE 2012, 7:e35991.