Sequence variation and differential splicing of the midgut cadherin gene in trichoplusia ni

Insect Biochemistry and Molecular Biology

Volumn 43, Issue 8, 2013, Pages 712-723

  Zhang, Xin ^a   Kain, Wendy ^a   Wang, Ping ^a  

^a New York State Agricultural Experiment Station   (United States)

Author keywords

Bt resistance; Cadherin; Midgut; Trichoplusia ni

Indexed keywords

BACTERIAL PROTEIN; CADHERIN; COMPLEMENTARY DNA; ENDOTOXIN; HEMOLYSIN; INSECT PROTEIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS;

ALLELE; ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BT RESISTANCE; CHEMISTRY; COMPARATIVE STUDY; CROSS BREEDING; DNA SEQUENCE; GASTROINTESTINAL TRACT; GENETICS; INDEL MUTATION; INSECTICIDE RESISTANCE; METABOLISM; MIDGUT; MOLECULAR GENETICS; MOTH; NUCLEOTIDE SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; TRICHOPLUSIA NI;

BT RESISTANCE; CADHERIN; MIDGUT; TRICHOPLUSIA NI;

ALLELES; ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; CADHERINS; CROSSES, GENETIC; DNA, COMPLEMENTARY; ENDOTOXINS; GASTROINTESTINAL TRACT; HEMOLYSIN PROTEINS; INDEL MUTATION; INSECT PROTEINS; INSECTICIDE RESISTANCE; MOLECULAR SEQUENCE DATA; MOTHS; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ANALYSIS, DNA;

BACILLUS THURINGIENSIS; HEXAPODA; LEPIDOPTERA; TRICHOPLUSIA NI;

EID: 84879472325     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2013.05.007     Document Type: Article

References (66)

1. Abedin M., King N. The premetazoan ancestry of cadherins. Science 2008, 319:946-948.
2. Aimanova K.G., Zhuang M., Gill S.S. Expression of Cry1Ac cadherin receptors in insect midgut and cell lines. J.Invertebr. Pathol. 2006, 92:178-187.
3. Baxter S.W., 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.
4. Baxter S.W., Badenes-Pérez 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.
5. Bell R.A., Owens C.D., Shapiro M., Tardif J.R. Development of mass-rearing technology. The Gypsy Moth: Research toward Integrated Pest Management 1981, 599-633. U.S. Dep. Agric, Washington, DC. C.C. Doane, M.L. McManus (Eds.).
6. Bravo A., Gomez I., Conde J., Munoz-Garay C., Sanchez J., Miranda R., Zhuang M., Gill S.S., Soberon M. Oligomerization triggers binding of a Bacillus thuringiensis Cry1Ab pore-forming toxin to aminopeptidase N receptor leading to insertion into membrane microdomains. Biochim. Biophys. Acta. 2004, 1667:38-46.
7. Carrière Y., Showalter A.M., Fabrick J.A., Sollome J., Ellers-Kirk C., Tabashnik B.E. Cadherin gene expression and effects of Bt resistance on sperm transfer in pink bollworm. J.Insect Physiol. 2009, 55:1058-1064.
8. Chen J., Brown M.R., Hua G., Adang M.J. Comparison of the localization of Bacillus thuringiensis Cry1A delta-endotoxins and their binding proteins in larval midgut of tobacco hornworm, Manduca sexta. Cell Tissue Res. 2005, 321:123-129.
9. Coates B.S., Sumerford D.V., Hellmich R.L., Lewis L.C. Sequence variation in the cadherin gene of Ostrinia nubilalis: a tool for field monitoring. Insect Biochem. Mol. Biol. 2005, 35:129-139.
10. 2 larval weights when fed a diet containing Cry1Ab. J.Insect Sci. 2008, 8:21.
11. Dorsch J.A., Candas M., Griko N.B., Maaty W.S., Midboe E.G., Vadlamudi R.K., Bulla L.A. Cry1A toxins of Bacillus thuringiensis bind specifically to a region adjacent to the membrane-proximal extracellular domain of BT-R(1) in Manduca sexta: involvement of a cadherin in the entomopathogenicity of Bacillus thuringiensis. Insect Biochem. Mol. Biol. 2002, 32:1025-1036.
12. Duan J., Li R., Cheng D., Fan W., Zha X., Cheng T., Wu Y., Wang J., Mita K., Xiang Z., Xia Q. SilkDB v2.0: a platform for silkworm (Bombyx mori ) genome biology. Nucleic Acids Res. 2010, 38:D453-D456.
13. 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.
14. Fabrick J., Oppert C., Lorenzen M.D., Morris K., Oppert B., Jurat-Fuentes J.L. Anovel Tenebrio molitor cadherin is a functional receptor for Bacillus thuringiensis Cry3Aa toxin. J.Biol. Chem. 2009, 284:18401-18410.
15. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:783-791.
16. Flannagan R.D., Yu C.G., Mathis J.P., Meyer T.E., Shi X., Siqueira H.A., Siegfried B.D. Identification, cloning and expression of a Cry1Ab cadherin receptor from European corn borer, Ostrinia nubilalis (Hubner) (Lepidoptera: Crambidae). Insect Biochem. Mol. Biol. 2005, 35:33-40.
17. Fung S., Wang F., Chase M., Godt D., Hartenstein V. Expression profile of the cadherin family in the developing Drosophila brain. J.Comp. Neurol. 2008, 506:469-488.
18. Gahan L.J., Gould F., Heckel D.G. Identification of a gene associated with Bt resistance in Heliothis virescens. Science 2001, 293:857-860.
19. Gahan L.J., Gould F., Lopez J.D., Micinski S., Heckel D.G. Apolymerase chain reaction screen of field populations of Heliothis virescens for a retrotransposon insertion conferring resistance to Bacillus thuringiensis toxin. J.Econ. Entomol. 2007, 100:187-194.
20. 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.
21. Gomez I., Oltean D.I., Gill S.S., Bravo A., Soberon M. Mapping the epitope in cadherin-like receptors involved in Bacillus thuringiensis Cry1A toxin interaction using phage display. J.Biol. Chem. 2001, 276:28906-28912.
22. 1 receptor with loop 2 of domain II of Bacillus thuringiensis Cry1A toxins. J.Biol. Chem. 2002, 277:30137-30143.
23. Gomez I., Dean D.H., Bravo A., Soberon M. Molecular basis for Bacillus thuringiensis Cry1Ab toxin specificity: two structural determinants in the Manduca sexta Bt-R1 receptor interact with loops alpha-8 and 2 in domain II of Cy1Ab toxin. Biochemistry 2003, 42:10482-10489.
24. Gomez I., Arenas I., Benitez I., Miranda-Rios J., Becerril B., Grande R., Almagro J.C., Bravo A., Soberon M. Specific epitopes of domains II and III of Bacillus thuringiensis Cry1Ab toxin involved in the sequential interaction with cadherin and aminopeptidase-N receptors in Manduca sexta. J.Biol. Chem. 2006, 281:34032-34039.
25. 1 receptor in Manduca sexta. BIOS 2005, 76:153-161.
26. Hua G., Jurat-Fuentes J.L., Adang M.J. Bt-R1a extracellular cadherin repeat 12 mediates Bacillus thuringiensis Cry1Ab binding and cytotoxicity. J.Biol. Chem. 2004, 279:28051-28056.
27. Hua G., Zhang R., Abdullah M.A., Adang M.J. Anopheles gambiae cadherin AgCad1 binds the Cry4Ba toxin of Bacillus thuringiensis israelensis and a fragment of AgCad1 synergizes toxicity. Biochemistry 2008, 47:5101-5110.
28. Hulpiau P., van Roy F. Molecular evolution of the cadherin superfamily. Int. J. Biochem. Cell Biol. 2009, 41:349-369.
29. Hulpiau P., van Roy F. New insights into the evolution of metazoan cadherins. Mol. Biol. Evol. 2011, 28:647-657.
30. Janmaat A.F., Myers J. Rapid evolution and the cost of resistance to Bacillus thuringiensis in greenhouse populations of cabbage loopers, Trichoplusia ni. Proc. Biol. Sci. 2003, 270:2263-2270.
31. Kain W.C., Zhao J.Z., Janmaat A.F., Myers J., Shelton A.M., Wang P. Inheritance of resistance to Bacillus thuringiensis Cry1Ac toxin in a greenhouse-derived strain of cabbage looper (Lepidoptera: Noctuidae). J.Econ. Entomol. 2004, 97:2073-2078.
32. Kashyap L., Tabish M. Alternatively spliced isoforms encoded by cadherin genes from C.elegansgenome. Bioinformation 2007, 2:50-56.
33. Midboe E.G., Candas M., Bulla L.A. Expression of a midgut-specific cadherin BT-R1 during the development of Manduca sexta larva. Comp. Biochem. Physiol. B., Biochem. Mol. Biol. 2003, 135:125-137.
34. Morin S., Biggs R.W., Sisterson M.S., Shriver L., Ellers-Kirk C., Higginson D., Holley D., Gahan L.J., Heckel D.G., Carriere 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.
35. Morin S., Henderson S., Fabrick J.A., Carriere Y., Dennehy T.J., Brown J.K., Tabashnik B.E. DNA-based detection of Bt resistance alleles in pink bollworm. Insect Biochem. Mol. Biol. 2004, 34:1225-1233.
36. Mutanen M., Wahlberg N., Kaila L. Comprehensive gene and taxon coverage elucidates radiation patterns in moths and butterflies. Proc. R. Soc. B 2010, 277:2839-2848.
37. Nagamatsu Y., Koike T., Sasaki K., Yoshimoto A., Furukawa Y. The cadherin-like protein is essential to specificity determination and cytotoxic action of the Bacillus thuringiensis insecticidal CryIAa toxin. FEBS Lett. 1999, 460:385-390.
38. Pardo-Lopez L., Soberon M., Bravo A. Bacillus thuringiensis insecticidal three-domain cry toxins: mode of action, insect resistance and consequences for crop protection. FEMS Microbiol. Rev. 2013, 37:3-22.
39. Patel S.D., Chen C.P., Bahna F., Honig B., Shapiro L. Cadherin-mediated cell-cell adhesion: sticking together as a family. Curr. Opin. Struct. Biol. 2003, 13:690-698.
40. Pigott C.R., Ellar D.J. Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol. Mol. Biol. Rev. 2007, 71:255-281.
41. Regier J.C., Zwick A., Cummings M.P., Kawahara A.Y., Cho S., Weller S., Roe A., Baixeras J., Brown J.W., Parr C., Davis D.R., Epstein M., Hallwachs W., Hausmann A., Janzen D.H., Kitching I.J., Solis M.A., Yen S.H., Bazinet A.L., Mitter C. Toward reconstructing the evolution of advanced moths and butterflies (Lepidoptera: Ditrysia): an initial molecular study. BMC. Evol. Biol. 2009, 9:280. 10.1186/1471-2148-9-280.
42. Roe A.D., Weller S.J., Baixeras-Almela J., Brown J., Cummings M., Davis D., Horak M., Kawahara A., Mitter C., Parr C., Regier J., Rubinoff D., Simonsen T.J., Wahlberg N., Zwick A. Evolutionary framework for Lepidoptera model systems. Molecular Biology and Genetics of the Lepidoptera 2010, 1-24. CRC Press, Boca Raton, FL. M. Goldsmith, F. Marec (Eds.).
43. Rokas A. The origins of multicellularity and the early history of the genetic toolkit for animal development. Annu. Rev. Genet. 2008, 42:235-251.
44. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406-425.
45. Sayed A., Nekl E.R., Siqueira H.A., Wang H.C., Ffrench-Constant R.H., Bagley M., Siegfried B.D. Anovel cadherin-like gene from western corn rootworm, Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae), larval midgut tissue. Insect Mol. Biol. 2007, 16:591-600.
46. Shelton A.M., Robertson J.L., Tang J.D., Perez C., Eigenbrode S.D., Preisler H.K., Wilsey W.T., Cooley R.J. Resistance of diamondback moth (Lepidoptera: Plutellidae) to Bacillus thuringiensis subspecies in the field. J.Econ. Entomol. 1993, 86:697-705.
47. Soberon M., Pardo-Lopez L., Lopez I., Gomez I., Tabashnik B.E., Bravo A. Engineering modified Bt toxins to counter insect resistance. Science 2007, 318:1640-1642.
48. Soberon M., Pardo L., Munoz-Garay C., Sanchez J., Gomez I., Porta H., Bravo A. Pore formation by Cry toxins. Adv. Exp. Med. Biol. 2010, 677:127-142.
49. Tabashnik B.E., Finson N., Johnson M.W., Moar W.J. 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. 1993, 59:1332-1335.
50. Tabashnik B.E., Fabrick J.A., Henderson S., Biggs R.W., Yafuso C.M., Nyboer M.E., Manhardt N.M., Coughlin L.A., Sollome J., Carriere Y., Dennehy T.J., Morin S. DNA screening reveals pink bollworm resistance to Bt cotton remains rare after a decade of exposure. J.Econ. Entomol. 2006, 99:1525-1530.
51. Tabashnik B.E., Huang F., Ghimire M.N., Leonard B.R., Siegfried B.D., Rangasamy M., Yang Y., Wu Y., Gahan L.J., Heckel D.G., Bravo A., Soberon M. Efficacy of genetically modified Bt toxins against insects with different genetic mechanisms of resistance. Nat. Biotechnol. 2011, 29:1128-1131.
52. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
53. The Heliconius Genome Consortium Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 2012, 487:94-98.
54. 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. U S A 2011, 108:14037-14042.
55. Vachon V., Laprade R., Schwartz J.-L. Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: a critical review. J.Invertebr. Pathol. 2012, 111:1-12.
56. Vadlamudi R.K., Ji T.H., Bulla L.A. Aspecific binding protein from Manduca sexta for the insecticidal toxin of Bacillus thuringiensis subsp. berliner. J.Biol. Chem. 1993, 268:12334-12340.
57. Vadlamudi R.K., Weber E., Ji I., Ji T.H., Bulla L.A. Cloning and expression of a receptor for an insecticidal toxin of Bacillus thuringiensis. J.Biol. Chem. 1995, 270:5490-5494.
58. Wang G., Wu K., Liang G., Guo Y. Gene cloning and expression of cadherin in midgut of Helicoverpa armigera and its Cry1A binding region. Sci. China C. Life Sci. 2005, 48:346-356.
59. Wang P., Zhao J.-Z., Rodrigo-Simon A., Kain W., Janmaat A.F., Shelton A.M., Ferre J., Myers J. Mechanism of resistance to Bacillus thuringiensis toxin Cry1Ac in a greenhouse population of the cabbage looper, Trichoplusia ni. Appl. Environ. Microbiol. 2007, 73:1199-1207.
60. Xie R., Zhuang M., Ross L.S., Gomez I., Oltean D.I., Bravo A., Soberon M., Gill S.S. Single amino acid mutations in the cadherin receptor from Heliothis virescens affect its toxin binding ability to Cry1A toxins. J.Biol. Chem. 2005, 280:8416-8425.
61. Xu X., Yu L., Wu Y. Disruption of a cadherin gene associated with resistance to Cry1Ac δ-endotoxin of Bacillus thuringiensis in Helicoverpa armigera. Appl. Environ. Microbiol. 2005, 71:948-954.
62. Yang Y., Chen H., Wu S., Yang Y., Xu X., Wu Y. Identification and molecular detection of a deletion mutation responsible for a truncated cadherin of Helicoverpa armigera. Insect Biochem. Mol. Biol. 2006, 36:735-740.
63. 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.
64. 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.
65. Zhao J., Jin L., Yang Y., Wu Y. Diverse cadherin mutations conferring resistance to Bacillus thuringiensis toxin Cry1Ac in Helicoverpa armigera. Insect Biochem. Mol. Biol. 2010, 40:113-118.
66. Zuckerkandl E., Pauling L. Evolutionary divergence and convergence in proteins. Evolving Genes and Proteins 1965, 97-166. Academic Press, New York. V. Bryson, H.J. Vogel (Eds.).