1932

Abstract

Insecticidal proteins from the bacterium () are used in sprayable formulations or produced in transgenic crops as the most successful alternatives to synthetic pesticides. The most relevant threat to sustainability of insecticidal proteins (toxins) is the evolution of resistance in target pests. To date, high-level resistance to sprays has been limited to one species in the field and another in commercial greenhouses. In contrast, there are currently seven lepidopteran and one coleopteran species that have evolved practical resistance to transgenic plants producing insecticidal proteins. In this article, we present a review of the current knowledge on mechanisms of resistance to toxins, with emphasis on key resistance genes and field-evolved resistance, to support improvement of technology and its sustainability.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-052620-073348
2021-01-07
2024-12-09
Loading full text...

Full text loading...

/deliver/fulltext/ento/66/1/annurev-ento-052620-073348.html?itemId=/content/journals/10.1146/annurev-ento-052620-073348&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Adang M, Crickmore N, Jurat-Fuentes JL 2014. Diversity of Bacillus thuringiensis crystal toxins and mechanism of action. Insect Midgut and Insecticidal Proteins TS Dhadialla, S Gill 39–87 Adv. Insect Physiol. 47 Amsterdam: Elsevier
    [Google Scholar]
  2. 2. 
    Atsumi S, Miyamoto K, Yamamoto K, Narukawa J, Kawai S et al. 2012. Single amino acid mutation in an ATP-binding cassette transporter gene causes resistance to Bt toxin Cry1Ab in the silkworm. Bombyx mori. PNAS 109:E1591–98Germline transformation of Bombyx mori to prove the role of ABCC2 in Cry1Ab resistance.
    [Google Scholar]
  3. 3. 
    Ballester V, Granero F, Tabashnik BE, Malvar T, Ferré J 1999. Integrative model for binding of Bacillus thuringiensis toxins in susceptible and resistant larvae of the diamondback moth (Plutella xylostella). Appl. Environ. Microbiol. 65:1413–19
    [Google Scholar]
  4. 4. 
    Banerjee R, Hasler J, Meagher R, Nagoshi R, Hietala L et al. 2017. Mechanism and DNA-based detection of field-evolved resistance to transgenic Bt corn in fall armyworm (Spodoptera frugiperda). Sci. Rep. 7:10877First description of a gene mutation (ABCC2) for resistance to a Bt transgenic crop.
    [Google Scholar]
  5. 5. 
    Barkhade UP, Thakare AS. 2010. Protease mediated resistance mechanism to Cry1C and Vip3A in Spodoptera litura. Egypt. Acad. J. Biol. Sci 3:43–50
    [Google Scholar]
  6. 6. 
    Baxter SW, Badenes-Perez FR, Morrison A, Vogel H, Crickmore N et al. 2011. Parallel evolution of Bacillus thuringiensis toxin resistance in Lepidoptera. Genetics 189:675–79
    [Google Scholar]
  7. 7. 
    Baxter SW, Zhao JZ, Gahan LJ, Shelton AM, Tabashnik BE, Heckel DG 2005. Novel genetic basis of field-evolved resistance to Bt toxins in Plutella xylostella. Insect Mol. Biol 14:327–34
    [Google Scholar]
  8. 8. 
    Bergamasco VB, Mendes DRP, Fernandes OA, Desidério JA, Lemos MVF 2013. Bacillus thuringiensis Cry1Ia10 and Vip3Aa protein interactions and their toxicity in Spodoptera spp. (Lepidoptera). J. Invertebr. Pathol. 112:152–58
    [Google Scholar]
  9. 9. 
    Bernardi D, Salmeron E, Horikoshi RJ, Bernardi O, Dourado PM et al. 2015. Cross-resistance between Cry1 proteins in fall armyworm (Spodoptera frugiperda) may affect the durability of current pyramided Bt maize hybrids in Brazil. PLOS ONE 10:e0140130
    [Google Scholar]
  10. 10. 
    Bernardi O, Bernardi D, Amado D, Sousa RS, Fatoretto J et al. 2015. Resistance risk assessment of Spodoptera frugiperda (Lepidoptera: Noctuidae) and Diatraea saccharalis (Lepidoptera: Crambidae) to Vip3Aa20 insecticidal protein expressed in corn. J. Econ. Entomol. 108:2711–19
    [Google Scholar]
  11. 11. 
    Bernardi O, Bernardi D, Horikoshi RJ, Okuma DM, Miraldo LL et al. 2016. Selection and characterization of resistance to the Vip3Aa20 protein from Bacillus thuringiensis in Spodoptera frugiperda. Pest Manag. Sci 72:1794–802
    [Google Scholar]
  12. 12. 
    Boaventura D, Ulrich J, Lueke B, Bolzan A, Okuma D et al. 2020. Molecular characterization of Cry1F resistance in fall armyworm, Spodoptera frugiperda from Brazil. Insect Biochem. Mol. Biol. 116:103280
    [Google Scholar]
  13. 13. 
    Bretschneider A, Heckel DG, Pauchet Y 2016. Three toxins, two receptors, one mechanism: mode of action of Cry1A toxins from Bacillus thuringiensis in Heliothis virescens. Insect Biochem. Mol. Biol 76:109–17
    [Google Scholar]
  14. 14. 
    Caccia S, Moar WJ, Chandrashekhar J, Oppert C, Anilkumar KJ et al. 2012. Association of Cry1Ac toxin resistance in Helicoverpa zea (Boddie) with increased alkaline phosphatase levels in the midgut lumen. Appl. Environ. Microbiol. 78:5690–98
    [Google Scholar]
  15. 15. 
    Camargo AM, Castanera P, Farinos GP, Huang F 2017. Comparative analysis of the genetic basis of Cry1F resistance in two strains of Spodoptera frugiperda originated from Puerto Rico and Florida. J. Invertebr. Pathol. 146:47–52
    [Google Scholar]
  16. 16. 
    Carriere Y, Williams JL, Crowder DW, Tabashnik BE 2018. Genotype-specific fitness cost of resistance to Bt toxin Cry1Ac in pink bollworm. Pest Manag. Sci. 74:2496–503
    [Google Scholar]
  17. 17. 
    Castagnola A, Jackson J, Perera OP, Oppert C, Eda S, Jurat-Fuentes JL 2017. Alpha-arylphorin is a mitogen in the Heliothis virescens midgut cell secretome upon Cry1Ac intoxication. PeerJ 5:e3886
    [Google Scholar]
  18. 18. 
    Chakroun M, Banyuls N, Walsh T, Downes S, James B, Ferre J 2016. Characterization of the resistance to Vip3Aa in Helicoverpa armigera from Australia and the role of midgut processing and receptor binding. Sci. Rep. 6:24311
    [Google Scholar]
  19. 19. 
    Chakroun M, Ferré J. 2014. In vivo and in vitro binding of Vip3Aa to Spodoptera frugiperda midgut and characterization of binding sites using 125I-radiolabeling. Appl. Environ. Microbiol. 80:6258–65
    [Google Scholar]
  20. 20. 
    Chandrasena DI, Signorini AM, Abratti G, Storer NP, Olaciregui ML et al. 2018. Characterization of field-evolved resistance to Bacillus thuringiensis-derived Cry1F delta-endotoxin in Spodoptera frugiperda populations from Argentina. Pest Manag. Sci. 74:746–54
    [Google Scholar]
  21. 21. 
    Coates BS, Siegfried BD. 2015. Linkage of an ABCC transporter to a single QTL that controls Ostrinia nubilalis larval resistance to the Bacillus thuringiensis Cry1Fa toxin. Insect Biochem. Mol. Biol. 63:86–96
    [Google Scholar]
  22. 22. 
    Crickmore N. 2016. Bacillus thuringiensis resistance in Plutella—too many trees. Curr. Opin. Insect Sci. 15:84–88
    [Google Scholar]
  23. 23. 
    Crickmore N, Berry C, Panneerselvam S, Mishra R, Connor TR, Bonning BC 2020. A structure-based nomenclature for Bacillus thuringiensis and other bacteria-derived pesticidal proteins. J. Invertebr. Pathol. In press
    [Google Scholar]
  24. 24. 
    Daniel A, Sangadala S, Dean DH, Adang MJ 2002. Denaturation of either Manduca sexta aminopeptidase N or Bacillus thuringiensis Cry1A toxins exposes binding epitopes hidden under nondenaturing conditions. Appl. Environ. Microbiol. 68:2106–12
    [Google Scholar]
  25. 25. 
    de Bortoli C, Banerjee R, Huang F, Hasler J, Reay-Jones F et al. 2019. Identification and frequency of an allele linked to resistance against Cry1Fa corn in Spodoptera frugiperda from Florida Paper presented at the Annual Meeting of the Entomological Society of America St. Louis, MO: Nov 17–20
    [Google Scholar]
  26. 26. 
    Dhurua S, Gujar GT. 2011. Field-evolved resistance to Bt toxin Cry1Ac in the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), from India. Pest Manag. Sci. 67:898–903
    [Google Scholar]
  27. 27. 
    Endo H, Azuma M, Adegawa S, Kikuta S, Sato R 2017. Water influx via aquaporin directly determines necrotic cell death induced by the Bacillus thuringiensis Cry toxin. FEBS Lett 591:56–64
    [Google Scholar]
  28. 28. 
    Escriche B, Tabashnik B, Finson N, Ferré J 1995. Immunohistochemical detection of binding of CryIA crystal proteins of Bacillus thuringiensis in highly resistant strains of Plutella xylostella (L.) from Hawaii. Biochem. Biophys. Res. Commun. 212:388–95
    [Google Scholar]
  29. 29. 
    Estada U, Ferre J. 1994. Binding of insecticidal crystal proteins of Bacillus thuringiensis to the midgut brush border of the cabbage looper, Trichoplusia ni (Hubner) (Lepidoptera: Noctuidae), and selection for resistance to one of the crystal proteins. Appl. Environ. Microbiol. 60:3840–46
    [Google Scholar]
  30. 30. 
    Fabrick JA, Mathew LG, LeRoy DM, Hull JJ, Unnithan GC et al. 2020. Reduced cadherin expression associated with resistance to Bt toxin Cry1Ac in pink bollworm. Pest Manag. Sci. 76:67–74
    [Google Scholar]
  31. 31. 
    Fabrick JA, Ponnuraj J, Singh A, Tanwar RK, Unnithan GC et al. 2014. Alternative splicing and highly variable cadherin transcripts associated with field-evolved resistance of pink bollworm to Bt cotton in India. PLOS ONE 9:e97900First description of alternative splicing (cadherin) in resistance to a Bt transgenic crop.
    [Google Scholar]
  32. 32. 
    Farias JR, Andow DA, Horikoshi RJ, Sorgatto RJ, Fresia P et al. 2014. Field-evolved resistance to Cry1F maize by Spodoptera frugiperda (Lepidoptera: Noctuidae) in Brazil. Crop Prot 64:150–58
    [Google Scholar]
  33. 33. 
    Flagel L, Lee YW, Wanjugi H, Swarup S, Brown A et al. 2018. Mutational disruption of the ABCC2 gene in fall armyworm, Spodoptera frugiperda, confers resistance to the Cry1Fa and Cry1A.105 insecticidal proteins. Sci. Rep. 8:7255
    [Google Scholar]
  34. 34. 
    Flagel LE, Swarup S, Chen M, Bauer C, Wanjugi H et al. 2015. Genetic markers for Western corn rootworm resistance to Bt toxin. G3 5:399–405
    [Google Scholar]
  35. 35. 
    Forcada C, Alcácer E, Garcerá MD, Martínez R 1996. Differences in the midgut proteolytic activity of two Heliothis virescens strains, one susceptible and one resistant to Bacillus thuringiensis toxins. Arch. Insect Biochem. Physiol. 31:257–72
    [Google Scholar]
  36. 36. 
    Forcada C, Alcacer E, Garcera MD, Tato A, Martinez R 1999. Resistance to Bacillus thuringiensis Cry1Ac toxin in three strains of Heliothis virescens: proteolytic and SEM study of the larval midgut. Arch. Insect Biochem. Physiol. 42:51–63
    [Google Scholar]
  37. 37. 
    Gahan LJ, Gould F, Heckel DG 2001. Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293:857–60First report of a gene mutation (cadherin) in Cry1A resistance.
    [Google Scholar]
  38. 38. 
    Gahan LJ, Pauchet Y, Vogel H, Heckel DG 2010. An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1Ac toxin. PLOS Genet 6:e1001248First description of an ABC transporter in Cry1A resistance.
    [Google Scholar]
  39. 39. 
    Gassmann AJ, Shrestha RB, Kropf AL, St Clair CR, Brenizer BD 2020. Field-evolved resistance by western corn rootworm to Cry34/35Ab1 and other Bacillus thuringiensis traits in transgenic maize. Pest Manag. Sci. 76:268–76
    [Google Scholar]
  40. 40. 
    Gomis-Cebolla J, Ruiz de Escudero I, Vera-Velasco NM, Hernandez-Martinez P, Hernandez-Rodriguez CS et al. 2017. Insecticidal spectrum and mode of action of the Bacillus thuringiensis Vip3Ca insecticidal protein. J. Invertebr. Pathol. 142:60–67
    [Google Scholar]
  41. 41. 
    Gomis-Cebolla J, Wang Y, Quan Y, He K, Walsh T et al. 2018. Analysis of cross-resistance to Vip3 proteins in eight insect colonies, from four insect species, selected for resistance to Bacillus thuringiensis insecticidal proteins. J. Invertebr. Pathol. 155:64–70
    [Google Scholar]
  42. 42. 
    Gong Y, Wang C, Yang Y, Wu S, Wu Y 2010. Characterization of resistance to Bacillus thuringiensis toxin Cry1Ac in Plutella xylostella from China. J. Invertebr. Pathol. 104:90–96
    [Google Scholar]
  43. 43. 
    Gonzalez-Cabrera J, Garcia M, Hernandez-Crespo P, Farinos GP, Ortego F, Castanera P 2013. Resistance to Bt maize in Mythimna unipuncta (Lepidoptera: Noctuidae) is mediated by alteration in Cry1Ab protein activation. Insect Biochem. Mol. Biol. 43:635–43
    [Google Scholar]
  44. 44. 
    Gunning RV, Dang HT, Kemp FC, Nicholson IC, Moores GD 2005. New resistance mechanism in Helicoverpa armigera threatens transgenic crops expressing Bacillus thuringiensis Cry1Ac toxin. Appl. Environ. Microbiol. 71:2558–63
    [Google Scholar]
  45. 45. 
    Guo Z, Kang S, Chen D, Wu Q, Wang S et al. 2015. MAPK signaling pathway alters expression of midgut ALP and ABCC genes and causes resistance to Bacillus thuringiensis Cry1Ac toxin in diamondback moth. PLOS Genet 11:e1005124
    [Google Scholar]
  46. 46. 
    Hayakawa T, Shitomi Y, Miyamoto K, Hori H 2004. GalNAc pretreatment inhibits trapping of Bacillus thuringiensis Cry1Ac on the peritrophic membrane of Bombyx mori. FEBS Lett 576:331–35
    [Google Scholar]
  47. 47. 
    Hernández-Martínez P, Gomis-Cebolla J, Ferré J, Escriche B 2017. Changes in gene expression and apoptotic response in Spodoptera exigua larvae exposed to sublethal concentrations of Vip3 insecticidal proteins. Sci. Rep. 7:16245
    [Google Scholar]
  48. 48. 
    Hernández-Martínez P, Navarro-Cerrillo G, Caccia S, de Maagd RA, Moar WJ et al. 2010. Constitutive activation of the midgut response to Bacillus thuringiensis in Bt-resistant Spodoptera exigua. PLOS ONE 5:e12795
    [Google Scholar]
  49. 49. 
    Herrero S, Ansems M, Van Oers MM, Vlak JM, Bakker PL, de Maagd RA 2007. REPAT, a new family of proteins induced by bacterial toxins and baculovirus infection in Spodoptera exigua. Insect Biochem. Mol. Biol 37:1109–18
    [Google Scholar]
  50. 50. 
    Herrero S, Gechev T, Bakker PL, Moar WJ, de Maagd RA 2005. Bacillus thuringiensis Cry1Ca-resistant Spodoptera exigua lacks expression of one of four aminopeptidase N genes. BMC Genom 6:96
    [Google Scholar]
  51. 51. 
    Horikoshi RJ, Bernardi O, Bernardi D, Okuma DM, Farias JR et al. 2016. Near-isogenic Cry1F-resistant strain of Spodoptera frugiperda (Lepidoptera: Noctuidae) to investigate fitness cost associated with resistance in Brazil. J. Econ. Entomol. 109:854–59
    [Google Scholar]
  52. 52. 
    Huang F, Qureshi JA, Meagher RL Jr., Reisig DD, Head GP et al. 2014. Cry1F resistance in fall armyworm Spodoptera frugiperda: single gene versus pyramided Bt maize. PLOS ONE 9:e112958
    [Google Scholar]
  53. 53. 
    Jakka SR, Ferré J, Jurat-Fuentes JL 2015. Cry toxin binding sites and their use in strategies to delay resistance evolution. Bt Resistance: Characterization and Strategies for GM Crops Producing Bacillus thuringiensis Toxins M Soberón, Y Gao, A Bravo 138–49 Boston: CAB Int.
    [Google Scholar]
  54. 54. 
    Jakka SR, Gong L, Hasler J, Banerjee R, Sheets JJ et al. 2015. Field-evolved Mode 1 resistance of the fall armyworm to transgenic Cry1Fa-expressing corn associated with reduced Cry1Fa toxin binding and midgut alkaline phosphatase expression. Appl. Environ. Microbiol. 82:1023–34
    [Google Scholar]
  55. 55. 
    Jakka SR, Knight VR, Jurat-Fuentes JL 2014. Fitness costs associated with field-evolved resistance to Bt maize in Spodoptera frugiperda (Lepidoptera: Noctuidae). J. Econ. Entomol. 107:342–51
    [Google Scholar]
  56. 56. 
    Jakka SR, Knight VR, Jurat-Fuentes JL 2014. Spodoptera frugiperda (J. E. Smith) with field-evolved resistance to Bt maize are susceptible to Bt pesticides. J. Invertebr. Pathol. 122:52–54
    [Google Scholar]
  57. 57. 
    Jakka SR, Shrestha RB, Gassmann AJ 2016. Broad-spectrum resistance to Bacillus thuringiensis toxins by western corn rootworm (Diabrotica virgifera virgifera). Sci. Rep. 6:27860
    [Google Scholar]
  58. 58. 
    James C. 2017. Global status of commercialization of biotech/GM crops in 2017: Biotech crop adoption surges as economic benefits accumulate in 22 years. ISAAA Brief No. 53 ISAAA 1–4 Ithaca, NY: ISAAA
    [Google Scholar]
  59. 59. 
    Janmaat AF, Myers J. 2003. Rapid evolution and the cost of resistance to Bacillus thuringiensis in greenhouse populations of cabbage loopers. Trichoplusia ni. Proc. Biol. Sci. 270:2263–70
    [Google Scholar]
  60. 60. 
    Jiang K, Hou X-y, Tan T-t, Cao Z-l, Mei S-q et al. 2018. Scavenger receptor-C acts as a receptor for Bacillus thuringiensis vegetative insecticidal protein Vip3Aa and mediates the internalization of Vip3Aa via endocytosis. PLOS Pathog 14:e1007347
    [Google Scholar]
  61. 61. 
    Jiang K, Mei SQ, Wang TT, Pan JH, Chen YH, Cai J 2016. Vip3Aa induces apoptosis in cultured Spodoptera frugiperda (Sf9) cells. Toxicon 120:49–56
    [Google Scholar]
  62. 62. 
    Jin L, Wang J, Guan F, Zhang J, Yu S et al. 2018. Dominant point mutation in a tetraspanin gene associated with field-evolved resistance of cotton bollworm to transgenic Bt cotton. PNAS 115:11760–65First report of a dominant gene mutation (tetraspanin) in Cry1A resistance.
    [Google Scholar]
  63. 63. 
    Jin T, Chang X, Gatehouse AM, Wang Z, Edwards MG, He K 2014. Downregulation and mutation of a cadherin gene associated with Cry1Ac resistance in the Asian corn borer, Ostrinia furnacalis (Guenee). Toxins 6:2676–93
    [Google Scholar]
  64. 64. 
    Jin T, Duan X, Bravo A, Soberon M, Wang Z, He K 2016. Identification of an alkaline phosphatase as a putative Cry1Ac binding protein in Ostrinia furnacalis (Guenee). Pestic. Biochem. Physiol. 131:80–86
    [Google Scholar]
  65. 65. 
    Jurat-Fuentes JL, Gahan LJ, Gould FL, Heckel DG, Adang MJ 2004. The HevCaLP protein mediates binding specificity of the Cry1A class of Bacillus thuringiensis toxins in Heliothis virescens. Biochemistry 43:14299–305
    [Google Scholar]
  66. 66. 
    Jurat-Fuentes JL, Karumbaiah L, Jakka SR, Ning C, Liu C et al. 2011. Reduced levels of membrane-bound alkaline phosphatase are common to lepidopteran strains resistant to Cry toxins from Bacillus thuringiensis. PLOS ONE 6:e17606
    [Google Scholar]
  67. 67. 
    Kahn TW, Chakroun M, Williams J, Walsh T, James B et al. 2018. Efficacy and resistance management potential of a modified Vip3C protein for control of Spodoptera frugiperda in maize. Sci. Rep. 8:16204
    [Google Scholar]
  68. 68. 
    Kain W, Song X, Janmaat AF, Zhao JZ, Myers J et al. 2015. Resistance of Trichoplusia ni populations selected by Bacillus thuringiensis sprays to cotton plants expressing pyramided Bacillus thuringiensis toxins Cry1Ac and Cry2Ab. Appl. Environ. Microbiol. 81:1884–90
    [Google Scholar]
  69. 69. 
    Kain WC, Zhao JZ, Janmaat AF, Myers J, Shelton AM, Wang P 2004. Inheritance of resistance to Bacillus thuringiensis Cry1Ac toxin in a greenhouse-derived strain of cabbage looper (Lepidoptera: Noctuidae). J. Econ. Entomol. 97:2073–78
    [Google Scholar]
  70. 70. 
    Kalmykova G, Burtseva L, Milne R, Van Frankenhuyzen K 2009. Activity of spores and extracellular proteins from six Cry+ strains and a Cry− strain of Bacillus thuringiensis subsp. kurstaki against the western spruce budworm, Choristoneura occidentalis (Lepidoptera: Tortricidae). Can. J. Microbiol 55:536–43
    [Google Scholar]
  71. 71. 
    Karabörklü S, Azizoglu U, Azizoglu ZB 2018. Recombinant entomopathogenic agents: a review of biotechnological approaches to pest insect control. World J. Microbiol. Biotechnol. 34:14
    [Google Scholar]
  72. 72. 
    Karumbaiah L, Oppert B, Jurat-Fuentes JL, Adang MJ 2007. Analysis of midgut proteinases from Bacillus thuringiensis-susceptible and -resistant Heliothis virescens (Lepidoptera: Noctuidae). Comp. Biochem. Physiol. B 146:139–46
    [Google Scholar]
  73. 73. 
    Lee MK, Rajamohan F, Gould F, Dean DH 1995. Resistance to Bacillus thuringiensis CryIA δ-endotoxins in a laboratory-selected Heliothis virescens strain is related to receptor alteration. Appl. Environ. Microbiol. 61:3836–42
    [Google Scholar]
  74. 74. 
    Lee MK, Walters FS, Hart H, Palekar N, Chen JS 2003. The mode of action of the Bacillus thuringiensis vegetative insecticidal protein Vip3A differs from that of Cry1Ab delta-endotoxin. Appl. Environ. Microbiol. 69:4648–57
    [Google Scholar]
  75. 75. 
    Li H, Oppert B, Higgins RA, Huang F, Zhu KY, Buschman LL 2004. Comparative analysis of proteinase activities of Bacillus thuringiensis-resistant and -susceptible Ostrinia nubilalis (Lepidoptera: Crambidae). Insect Biochem. Mol. Biol. 34:753–62
    [Google Scholar]
  76. 76. 
    Liu JG, Yang AZ, Shen XH, Hua BG, Shi GL 2011. Specific binding of activated Vip3Aa10 to Helicoverpa armigera brush border membrane vesicles results in pore formation. J. Invertebr. Pathol. 108:92–97
    [Google Scholar]
  77. 77. 
    Liu YB, Tabashnik BE, Masson L, Escriche B, Ferré J 2000. Binding and toxicity of Bacillus thuringiensis protein Cry1C to susceptible and resistant diamondback moth (Lepidoptera: Plutellidae). J. Econ. Entomol. 93:1–6
    [Google Scholar]
  78. 78. 
    Ma G, Roberts H, Sarjan M, Featherstone N, Lahnstein J et al. 2005. Is the mature endotoxin Cry1Ac from Bacillus thuringiensis inactivated by a coagulation reaction in the gut lumen of resistant Helicoverpa armigera larvae. Insect Biochem. Mol. Biol. 35:729–39
    [Google Scholar]
  79. 79. 
    Mahon RJ, Downes SJ, James B 2012. Vip3A resistance alleles exist at high levels in Australian targets before release of cotton expressing this toxin. PLOS ONE 7:e39192Comprehensive F2 screen for rare recessive Vip3A resistance alleles.
    [Google Scholar]
  80. 80. 
    Martínez-Ramírez AC, Gould F, Ferré J 1999. Histopathological effects and growth reduction in a susceptible and a resistant strain of Heliothisvirescens (Lepidoptera: Noctuidae) caused by sublethal doses of pure Cry1A crystal proteins from Bacillus thuringiensis. Biocontrol Sci. Technol 9:239–46
    [Google Scholar]
  81. 81. 
    Masson L, Mazza A, Brousseau R, Tabashnik B 1995. Kinetics of Bacillus thuringiensis toxin binding with brush border membrane vesicles from susceptible and resistant larvae of Plutella xylostella. J. Biol. Chem 270:11887–96
    [Google Scholar]
  82. 82. 
    Mathew LG, Ponnuraj J, Mallappa B, Chowdary LR, Zhang J et al. 2018. ABC transporter mis-splicing associated with resistance to Bt toxin Cry2Ab in laboratory- and field-selected pink bollworm. Sci. Rep. 8:13531
    [Google Scholar]
  83. 83. 
    Mohan KS, Ravi KC, Suresh PJ, Sumerford D, Head GP 2016. Field resistance to the Bacillus thuringiensis protein Cry1Ac expressed in Bollgard® hybrid cotton in pink bollworm, Pectinophora gossypiella (Saunders), populations in India. Pest Manag. Sci. 72:738–46
    [Google Scholar]
  84. 84. 
    Monnerat R, Martins E, Macedo C, Queiroz P, Praça L et al. 2015. Evidence of field-evolved resistance of Spodoptera frugiperda to Bt corn expressing Cry1F in Brazil that is still sensitive to modified Bt toxins. PLOS ONE 10:e0119544
    [Google Scholar]
  85. 85. 
    Morin S, Biggs RW, Sisterson MS, Shriver L, Ellers-Kirk C et al. 2003. Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. PNAS 100:5004–9
    [Google Scholar]
  86. 86. 
    Nagoshi RN, Htain NN, Boughton D, Zhang L, Xiao Y et al. 2020. Southeastern Asia fall armyworms are closely related to populations in Africa and India, consistent with common origin and recent migration. Sci. Rep. 10:1421
    [Google Scholar]
  87. 87. 
    Nagoshi RN, Koffi D, Agboka K, Tounou KA, Banerjee R et al. 2017. Comparative molecular analyses of invasive fall armyworm in Togo reveal strong similarities to populations from the eastern United States and the Greater Antilles. PLOS ONE 12:e0181982
    [Google Scholar]
  88. 88. 
    Naik VC, Kumbhare S, Kranthi S, Satija U, Kranthi KR 2018. Field-evolved resistance of pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), to transgenic Bacillus thuringiensis (Bt) cotton expressing crystal 1Ac (Cry1Ac) and Cry2Ab in India. Pest Manag. Sci. 74:2544–54
    [Google Scholar]
  89. 89. 
    Nair R, Kalia V, Aggarwal KK, Gujar GT 2013. Variation in the cadherin gene sequence of Cry1Ac susceptible and resistant Helicoverpa armigera (Lepidoptera: Noctuidae) and the identification of mutant alleles in resistant strains. Curr. Sci. 104:215–23
    [Google Scholar]
  90. 90. 
    Nair R, Kamath SP, Mohan KS, Head G, Sumerford DV 2016. Inheritance of field-relevant resistance to the Bacillus thuringiensis protein Cry1Ac in Pectinophora gossypiella (Lepidoptera: Gelechiidae) collected from India. Pest Manag. Sci. 72:558–65
    [Google Scholar]
  91. 91. 
    Natl. Acad. Sci. Eng. Med. 2016. Genetically Engineered Crops: Experiences and Prospects Washington, DC: Natl. Acad.
    [Google Scholar]
  92. 92. 
    Ojha A, Sree KS, Sachdev B, Rashmi MA, Ravi KC et al. 2014. Analysis of resistance to Cry1Ac in field-collected pink bollworm, Pectinophora gossypiella (Lepidoptera: Gelechiidae), populations. GM Crops Food 5:280–86
    [Google Scholar]
  93. 93. 
    Olson S. 2015. An analysis of the biopesticide market now and where it is going. Outlooks Pest Manag 26:203–6
    [Google Scholar]
  94. 94. 
    Omoto C, Bernardi O, Salmeron E, Sorgatto RJ, Dourado PM et al. 2016. Field-evolved resistance to Cry1Ab maize by Spodoptera frugiperda in Brazil. Pest Manag. Sci. 72:1727–36
    [Google Scholar]
  95. 95. 
    Oppert B, Kramer KJ, Beeman RW, Johnson D, McGaughey WH 1997. Proteinase-mediated insect resistance to Bacillus thuringiensis toxins. J. Biol. Chem. 272:23473–76
    [Google Scholar]
  96. 96. 
    Oppert B, Kramer KJ, Johnson DE, MacIntosh SC, McGaughey WH 1994. Altered protoxin activation by midgut enzymes from a Bacillus thuringiensis resistant strain of Plodia interpunctella. Biochem. Biophys. Res. Commun 198:940–47
    [Google Scholar]
  97. 97. 
    Palma L, Scott DJ, Harris G, Din SU, Williams TL et al. 2017. The Vip3Ag4 insecticidal protoxin from Bacillus thuringiensis adopts a tetrameric configuration that is maintained on proteolysis. Toxins 9:165
    [Google Scholar]
  98. 98. 
    Park Y, Gonzalez-Martinez RM, Navarro-Cerrillo G, Chakroun M, Kim Y et al. 2014. ABCC transporters mediate insect resistance to multiple Bt toxins revealed by bulk segregant analysis. BMC Biol 12:46
    [Google Scholar]
  99. 99. 
    Pauchet Y, Bretschneider A, Augustin S, Heckel DG 2016. A P-glycoprotein is linked to resistance to the Bacillus thuringiensis Cry3Aa toxin in a leaf beetle. Toxins 8:362First report in Coleoptera of a gene mutation (ABCB1) in Cry3A resistance.
    [Google Scholar]
  100. 100. 
    Pickett BR, Gulzar A, Ferre J, Wright DJ 2017. Bacillus thuringiensis Vip3Aa toxin resistance in Heliothis virescens (Lepidoptera: Noctuidae). Appl. Environ. Microbiol. 83:e03506-16
    [Google Scholar]
  101. 101. 
    Pigott CR, Ellar DJ. 2007. Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol. Mol. Biol. Rev. 71:255–81
    [Google Scholar]
  102. 102. 
    Pinos D, Chakroun M, Millán-Leiva A, Jurat-Fuentes JL, Wright DJ et al. 2020. Reduced membrane-bound alkaline phosphatase does not affect binding of Vip3Aa in a Heliothis virescens resistant colony. Toxins 12:409
    [Google Scholar]
  103. 103. 
    Pinos D, Martínez-Solís M, Herrero S, Ferré J, Hernández-Martínez P 2019. The Spodoptera exigua ABCC2 acts as a Cry1A receptor independently of its nucleotide binding domain II. Toxins 11:172
    [Google Scholar]
  104. 104. 
    Qi L, Qiu X, Yang S, Li R, Wu B et al. 2020. Cry1Ac protoxin and its activated toxin from Bacillus thuringiensis act differentially during the pathogenic process. J. Agric. Food Chem. 68:5816–24
    [Google Scholar]
  105. 105. 
    Rajagopal R, Arora N, Sivakumar S, Rao NG, Nimbalkar SA, Bhatnagar RK 2009. Resistance of Helico-verpa armigera to Cry1Ac toxin from Bacillus thuringiensis is due to improper processing of the protoxin. Biochem. J. 419:309–16
    [Google Scholar]
  106. 106. 
    Raymond B, Johnston PR, Nielsen-LeRoux C, Lereclus D, Crickmore N 2010. Bacillus thuringiensis: an impotent pathogen. Trends Microbiol 18:189–94
    [Google Scholar]
  107. 107. 
    Shabbir MZ, Zhang T, Prabu S, Wang Y, Wang Z et al. 2020. Identification of Cry1Ah-binding proteins through pull down and gene expression analysis in Cry1Ah-resistant and susceptible strains of Ostrinia furnacalis. Pestic. Biochem. Physiol 163:200–8
    [Google Scholar]
  108. 108. 
    Singh G, Sachdev B, Sharma N, Seth R, Bhatnagar RK 2010. Interaction of Bacillus thuringiensis vegetative insecticidal protein with ribosomal S2 protein triggers larvicidal activity in Spodoptera frugiperda. Appl. Environ. Microbiol 76:7202–9
    [Google Scholar]
  109. 109. 
    Song X, Kain W, Cassidy D, Wang P 2015. Resistance to Bacillus thuringiensis toxin Cry2Ab in Trichoplusia ni is conferred by a novel genetic mechanism. Appl. Environ. Microbiol. 81:5184–95
    [Google Scholar]
  110. 110. 
    Storer NP, Babcock JM, Schlenz M, Meade T, Thompson GD et al. 2010. Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J. Econ. Entomol. 103:1031–38
    [Google Scholar]
  111. 111. 
    Tabashnik BE, Carriere Y. 2019. Evaluating cross-resistance between Vip and Cry toxins of Bacillus thuringiensis. J. Econ. Entomol 113:553–61
    [Google Scholar]
  112. 112. 
    Tabashnik BE, Finson N, Johnson MW, Moar WJ 1993. Resistance to toxins from Bacillus thuringiensis subsp. kurstaki causes minimal cross-resistance to B. thuringiensis subsp. aizawai in the diamondback moth (Lepidoptera: Plutellidae). Appl. Environ. Microbiol 59:1332–35
    [Google Scholar]
  113. 113. 
    Tabashnik BE, Liu YB, Malvar T, Heckel DG, Masson L et al. 1997. Global variation in the genetic and biochemical basis of diamondback moth resistance to Bacillus thuringiensis. PNAS 94:12780–85
    [Google Scholar]
  114. 114. 
    Tabashnik BE, Malvar T, Liu YB, Finson N, Borthakur D et al. 1996. Cross-resistance of the diamondback moth indicates altered interactions with domain II of Bacillus thuringiensis toxins. Appl. Environ. Microbiol. 62:2839–44
    [Google Scholar]
  115. 115. 
    Tabashnik BE, Schwartz JM, Finson N, Johnson MW 1992. Inheritance of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera, Plutellidae). J. Econ. Entomol. 85:1046–55
    [Google Scholar]
  116. 116. 
    Tanaka S, Miyamoto K, Noda H, Jurat-Fuentes JL, Yoshizawa Y et al. 2013. The ATP-binding cassette transporter subfamily C member 2 in Bombyx mori larvae is a functional receptor for Cry toxins from Bacillus thuringiensis. FEBS J 280:1782–94First demonstration of cadherin and ABC protein synergism in Cry1A pore formation.
    [Google Scholar]
  117. 117. 
    Tay WT, Mahon RJ, Heckel DG, Walsh TK, Downes S et al. 2015. Insect resistance to Bacillus thuringiensis toxin Cry2Ab is conferred by mutations in an ABC transporter subfamily A protein. PLOS Genet 11:e1005534
    [Google Scholar]
  118. 118. 
    Tiewsiri K, Wang P. 2011. Differential alteration of two aminopeptidases N associated with resistance to Bacillus thuringiensis toxin Cry1Ac in cabbage looper. PNAS 108:14037–42
    [Google Scholar]
  119. 119. 
    Vachon V, Laprade R, Schwartz JL 2012. Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: a critical review. J. Invertebr. Pathol. 111:1–12
    [Google Scholar]
  120. 120. 
    Vélez AM, Spencer TA, Alves AP, Crespo ALB, Siegfried BD 2013. Fitness costs of Cry1F resistance in fall armyworm. Spodoptera frugiperda. J. Appl. Entomol. 138:315–25
    [Google Scholar]
  121. 121. 
    Vélez AM, Spencer TA, Alves AP, Moellenbeck D, Meagher RL et al. 2013. Inheritance of Cry1F resistance, cross-resistance and frequency of resistant alleles in Spodoptera frugiperda (Lepidoptera: Noctuidae). Bull. Entomol. Res. 103:700–13
    [Google Scholar]
  122. 122. 
    Walsh T, James B, Chakroun M, Ferré J, Downes S 2018. Isolating, characterising and identifying a Cry1Ac resistance mutation in field populations of Helicoverpa punctigera. Sci. Rep 8:2626
    [Google Scholar]
  123. 123. 
    Wang J, Ma H, Zhao S, Huang J, Yang Y et al. 2020. Functional redundancy of two ABC transporter proteins in mediating toxicity of Bacillus thuringiensis to cotton bollworm. PLOS Pathog 16:e1008427
    [Google Scholar]
  124. 124. 
    Wang J, Wang H, Liu S, Liu L, Tay WT et al. 2017. CRISPR/Cas9 mediated genome editing of Helicoverpa armigera with mutations of an ABC transporter gene HaABCA2 confers resistance to Bacillus thuringiensis Cry2A toxins. Insect Biochem. Mol. Biol. 87:147–53
    [Google Scholar]
  125. 125. 
    Wang J, Zhang H, Wang H, Zhao S, Zuo Y et al. 2016. Functional validation of cadherin as a receptor of Bt toxin Cry1Ac in Helicoverpa armigera utilizing the CRISPR/Cas9 system. Insect Biochem. Mol. Biol. 76:11–17
    [Google Scholar]
  126. 126. 
    Wang L, Ma Y, Guo X, Wan P, Liu K et al. 2019. Pink bollworm resistance to Bt toxin Cry1Ac associated with an insertion in cadherin exon 20. Toxins 11:186
    [Google Scholar]
  127. 127. 
    Wang L, Ma Y, Wan P, Liu K, Xiao Y et al. 2018. Resistance to Bacillus thuringiensis linked with a cadherin transmembrane mutation affecting cellular trafficking in pink bollworm from China. Insect Biochem. Mol. Biol. 94:28–35
    [Google Scholar]
  128. 128. 
    Wang L, Wang J, Ma Y, Wan P, Liu K et al. 2019. Transposon insertion causes cadherin mis-splicing and confers resistance to Bt cotton in pink bollworm from China. Sci. Rep. 9:7479
    [Google Scholar]
  129. 129. 
    Wang P, Zhao JZ, Rodrigo-Simón A, Kain W, Janmaat AF et al. 2007. Mechanism of resistance to Bacillus thuringiensis toxin Cry1Ac in a greenhouse population of the cabbage looper. Trichoplusia ni. Appl. Environ. Microbiol. 73:1199–207
    [Google Scholar]
  130. 130. 
    Wei W, Pan S, Ma Y, Xiao Y, Yang Y et al. 2020. GATAe transcription factor is involved in Bacillus thuringiensis Cry1Ac toxin receptor gene expression inducing toxin susceptibility. Insect Biochem. Mol. Biol. 118:103306
    [Google Scholar]
  131. 131. 
    Wolfersberger MG. 1990. The toxicity of two Bacillus thuringiensis delta-endotoxins to gypsy moth larvae is inversely related to the affinity of binding sites on midgut brush border membranes for the toxins. Experientia 46:475–77
    [Google Scholar]
  132. 132. 
    Xiao Y, Dai Q, Hu R, Pacheco S, Yang Y et al. 2017. A single point mutation resulting in cadherin mislocalization underpins resistance against Bacillus thuringiensis toxin in cotton bollworm. J. Biol. Chem. 292:2933–43
    [Google Scholar]
  133. 133. 
    Xu C, Wang B-C, Yu Z, Sun M 2014. Structural insights into Bacillus thuringiensis Cry, Cyt and para-sporin toxins. Toxins 6:2732–70
    [Google Scholar]
  134. 134. 
    Xu X, Yu L, Wu Y 2005. Disruption of a cadherin gene associated with resistance to Cry1Ac δ-endotoxin of Bacillus thuringiensis in Helicoverpa armigera. Appl. Environ. Microbiol 71:948–54
    [Google Scholar]
  135. 135. 
    Yamazaki T, Ishikawa T, Pandian GN, Okazaki K, Haginoya K et al. 2011. Midgut juice of Plutella xylostella highly resistant to Bacillus thuringiensis Cry1Ac contains a three times larger amount of glucosinolate sulfatase which binds to Cry1Ac compared to that of susceptible strain. Pestic. Biochem. Physiol. 101:125–31
    [Google Scholar]
  136. 136. 
    Yang F, Huang F, Qureshi JA, Leonard BR, Niu Y et al. 2013. Susceptibility of Louisiana and Florida populations of Spodoptera frugiperda (Lepidoptera: Noctuidae) to transgenic Agrisure® Viptera™ 3111 corn. Crop Prot 50:37–39
    [Google Scholar]
  137. 137. 
    Yang F, Morsello S, Head GP, Sansone C, Huang F et al. 2018. F2 screen, inheritance and cross-resistance of field-derived Vip3A resistance in Spodoptera frugiperda (Lepidoptera: Noctuidae) collected from Louisiana, USA. Pest Manag. Sci. 74:1769–78
    [Google Scholar]
  138. 138. 
    Yang F, Santiago Gonzalez JC, Little N, Reisig D, Payne G et al. 2020. First documentation of major Vip3Aa resistance alleles in field populations of Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) in Texas, USA. Sci. Rep. 10:5867
    [Google Scholar]
  139. 139. 
    Yang X, Chen W, Song X, Ma X, Cotto-Rivera RO et al. 2019. Mutation of ABC transporter ABCA2 confers resistance to Bt toxin Cry2Ab in Trichoplusia ni. Insect Biochem. Mol. Biol 112:103209
    [Google Scholar]
  140. 140. 
    Yang Y, Chen H, Wu S, Yang Y, Xu X, Wu Y 2006. Identification and molecular detection of a deletion mutation responsible for a truncated cadherin of Helicoverpa armigera. Insect Biochem. Mol. Biol 36:735–40
    [Google Scholar]
  141. 141. 
    Yang Y, Zhu YC, Ottea J, Husseneder C, Leonard BR et al. 2011. Down regulation of a gene for cadherin, but not alkaline phosphatase, associated with Cry1Ab resistance in the sugarcane borer Diatraea saccharalis. PLOS ONE 6:e25783
    [Google Scholar]
  142. 142. 
    Zhang H, Tang M, Yang F, Yang Y, Wu Y 2013. DNA-based screening for an intracellular cadherin mutation conferring non-recessive Cry1Ac resistance in field populations of Helicoverpa armigera. Pestic. Biochem. Physiol 107:148–52
    [Google Scholar]
  143. 143. 
    Zhang H, Wu S, Yang Y, Tabashnik BE, Wu Y 2012. Non-recessive Bt toxin resistance conferred by an intracellular cadherin mutation in field-selected populations of cotton bollworm. PLOS ONE 7:e53418
    [Google Scholar]
  144. 144. 
    Zhang L, Liu B, Zheng W, Liu C, Zhang D et al. 2019. High-depth resequencing reveals hybrid population and insecticide resistance characteristics of fall armyworm (Spodoptera frugiperda) invading China. bioRxiv 813154. https://doi.org/10.1101/813154
    [Crossref]
  145. 145. 
    Zhang M, Wei J, Ni X, Zhang J, Jurat-Fuentes JL et al. 2019. Decreased Cry1Ac activation by midgut proteases associated with Cry1Ac resistance in Helicoverpa zea. Pest Manag. Sci 75:1099–106
    [Google Scholar]
  146. 146. 
    Zhang S, Cheng H, Gao Y, Wang G, Liang G, Wu K 2009. Mutation of an aminopeptidase N gene is associated with Helicoverpa armigera resistance to Bacillus thuringiensis Cry1Ac toxin. Insect Biochem. Mol. Biol. 39:421–29
    [Google Scholar]
  147. 147. 
    Zhang X, Tiewsiri K, Kain W, Huang L, Wang P 2012. Resistance of Trichoplusia ni to Bacillus thuringiensis toxin Cry1Ac is independent of alteration of the cadherin-like receptor for Cry toxins. PLOS ONE 7:e35991
    [Google Scholar]
  148. 148. 
    Zhao J, Jin L, Yang Y, Wu Y 2010. Diverse cadherin mutations conferring resistance to Bacillus thuringiensis toxin Cry1Ac in Helicoverpa armigera. Insect Biochem. Mol. Biol 40:113–18
    [Google Scholar]
  149. 149. 
    Zhao JZ, Collins HL, Tang JD, Cao J, Earle ED et al. 2000. Development and characterization of diamondback moth resistance to transgenic broccoli expressing high levels of Cry1C. Appl. Environ. Microbiol. 66:3784–89
    [Google Scholar]
  150. 150. 
    Zhao JZ, Oneal MA, Richtman NM, Thompson SD, Cowart MC et al. 2016. mCry3A-selected Western corn rootworm (Coleoptera: Chrysomelidae) colony exhibits high resistance and has reduced binding of mCry3A to midgut tissue. J. Econ. Entomol. 109:1369–77
    [Google Scholar]
  151. 151. 
    Zhao Z, Meihls LN, Hibbard BE, Ji T, Elsik CG, Shelby KS 2019. Differential gene expression in response to eCry3.1Ab ingestion in an unselected and eCry3.1Ab-selected western corn rootworm (Diabrotica virgifera virgifera LeConte) population. Sci. Rep. 9:4896
    [Google Scholar]
  152. 152. 
    Zheng M, Evdokimov AG, Moshiri F, Lowder C, Haas J 2019. Crystal structure of a Vip3B family insecticidal protein reveals a new fold and a unique tetrameric assembly. Protein Sci 29:824–29
    [Google Scholar]
  153. 153. 
    Zhu B, Sun X, Nie X, Liang P, Gao X 2020. MicroRNA-998–3p contributes to Cry1Ac-resistance by targeting ABCC2 in lepidopteran insects. Insect Biochem. Mol. Biol. 117:103283
    [Google Scholar]
/content/journals/10.1146/annurev-ento-052620-073348
Loading
/content/journals/10.1146/annurev-ento-052620-073348
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error