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Theoretical and Applied Genetics

, Volume 114, Issue 4, pp 755–764 | Cite as

Assessment of the importance of α-amylase inhibitor-2 in bruchid resistance of wild common bean

  • Keito Nishizawa
  • Masayoshi Teraishi
  • Shigeru Utsumi
  • Masao IshimotoEmail author
Original Paper

Abstract

Both α-amylase inhibitor-2 (αAI-2) and arcelin have been implicated in resistance of wild common bean (Phaseolus vulgaris L.) to the Mexican bean weevil (Zabrotes subfasciatus Boheman). Near isogenic lines (NILs) for arcelin 1–5 were generated by backcrossing wild common bean accessions with a cultivated variety. Whereas seeds of a wild accession (G12953) containing both αAI-2 and arcelin 4 were completely resistant to Z. subfasciatus, those of the corresponding NIL were susceptible to infestation, suggesting that the principal determinant of resistance was lost during backcrossing. Three independent lines of transgenic azuki bean [Vigna angularis (Willd.) Ohwi and Ohashi] expressing αAI-2 accumulated high levels of this protein in seeds. The expression of αAI-2 in these lines conferred protection against the azuki bean weevil (Callosobruchus chinensis L.), likely through inhibition of larval digestive α-amylase. However, although the seed content of αAI-2 in these transgenic lines was similar to that in a wild accession of common bean (G12953), it did not confer a level of resistance to Z. subfasciatus similar to that of the wild accession. These results suggest that αAI-2 alone does not provide a high level of resistance to Z. subfasciatus. However, αAI-2 is an effective insecticidal protein with a spectrum of activity distinct from that of αAI-1, and it may prove beneficial in genetic engineering of insect resistance in legumes.

Keywords

Common Bean Wild Accession Azuki Bean Wild Parent Tepary Bean 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This research was supported by the Project for Development of Innovative Transgenic Plants of the Ministry of Agriculture, Forestry, and Fisheries of Japan. We thank Koichi Fujii (University of Tsukuba) for providing colonies of Z. subfasciatus, Elizabeth E. Hood (ProdiGene, College Station, TX) for providing A. tumefaciens strain EHA105, and Yumi Nakamoto for technical assistance.

References

  1. Acosta-Gallegos JA, Quintero C, Vargas J, Toro O, Tohme J, Cardona C (1998) A new variant of arcelin in wild common bean, Phaseolus vulgaris L., from southern Mexico. Genet Resour Crop Evol 45:235–242CrossRefGoogle Scholar
  2. Andreas JR, Yandell BS, Bliss FA (1986) Bean arcelin 1. Inheritance of a novel seed protein of Phaseolus vulgaris L. and its effect on seed composition. Theor Appl Genet 72:123–128CrossRefGoogle Scholar
  3. Bernfeld P (1955) Amylases, α- and β-. Methods Enzymol 1:149–158CrossRefGoogle Scholar
  4. Cardona C, Kornegay J, Posso CE, Morales F, Ramirez H (1990) Comparative value of four arcelin variants in the development of dry bean lines resistant to the Mexican bean weevil. Entomol Exp Appl 56:197–206CrossRefGoogle Scholar
  5. Chen R, Tsuda S, Matsui K, Fukuchi-Mizutani M, Ochiai M, Shimizu S, Sakuradani E, Aoki T, Imaizumi R, Ayabe S, Tanaka Y (2005) Production of γ-linolenic acid in Lotus japonicus and Vigna angularis by expression of the Δ6-fatty-acid desaturase gene isolated from Mortierella alpina. Plant Sci 169:599–605CrossRefGoogle Scholar
  6. Chrispeels MJ, Raikhel NV (1991) Lectins, lectin genes, and their role in plant defense. Plant Cell 3:1–9PubMedCrossRefGoogle Scholar
  7. Duke-Ras A, Hookyaas PJJ (1995) Electroporation of Agrobacterium tumefaciens. In: Nickloff JA (ed) Plant cell electroporation and electrofusion protocols. Humana, Totowa, NJ, pp 63–72CrossRefGoogle Scholar
  8. Fory LF, Finardi-Filho F, Quintero CM, Osborn TC, Cardona C, Chrispeels MJ, Mayer JE (1996) α-Amylase inhibitor in resistance of common beans to the Mexican bean weevil and the bean weevil (Coleoptera: Bruchidae). J Econ Entomol 89:204–210Google Scholar
  9. Goossens A, Quintero C, Dillen W, Rycke RD, Valor JF, Clercq JD, Montagu MV, Cardona C, Angenon G (2000) Analysis of bruchid resistance in the wild common bean accession G02771: no evidence for insecticidal activity of arcelin 5. J Exp Bot 51:1229–1236PubMedCrossRefGoogle Scholar
  10. Hanafy MS, Rahman SM, Khalafalla MM, El-Shemy HA, Nakamoto Y, Ishimoto M, Wakasa K (2006) Accumulation of free tryptophan in azuki bean (Vigna angularis) induced by expression of a gene (OASA1D) for a modified α subunit of rice anthranilate synthase. Plant Sci 171:670–676CrossRefGoogle Scholar
  11. Hood EE, Gelvin SB, Melchers LS, Hoekema A (1993) New Agrobacterium helper plasmids for gene transfer to plants. Transgen Res 2:208–218CrossRefGoogle Scholar
  12. Ishimoto M, Kitamura K (1989) Growth inhibitory effects of an α-amylase inhibitor from kidney bean, Phaseolus vulgaris (L.), on three species of bruchids (Coleoptera: Bruchidae). Appl Entomol Zool 24:281–286Google Scholar
  13. Ishimoto M, Kitamura K (1991) Effects of absence of seed α-amylase inhibitor on the growth inhibitory activity to azuki bean weevil (Callosobruchus chinensis) in common bean (Phaseolus vulgaris L.). Jpn J Breed 41:231–240Google Scholar
  14. Ishimoto M, Suzuki K, Iwanaga M, Kikuchi F, Kitamura K (1995) Variation of seed α-amylase inhibitors in the common bean. Theor Appl Genet 90:762–766CrossRefGoogle Scholar
  15. Ishimoto M, Sato T, Chrispeels MJ, Kitamura K (1996) Bruchid resistance of transgenic azuki bean expressing seed α-amylase inhibitor of common bean. Entomol Exp Appl 79:309–315CrossRefGoogle Scholar
  16. Ishimoto M, Yamada T, Kaga A (1999) Insecticidal activity of an α-amylase inhibitor-like protein resembling a putative precursor of α-amylase inhibitor in the common bean, Phaseolus vulgaris L. Biochim Biophys Acta 1432:104–112PubMedGoogle Scholar
  17. Kornegay J, Cardona C, Posso CE (1993) Inheritance of resistance to the Mexican bean weevil in common bean, determined by bioassay and biochemical tests. Crop Sci 33:589–594CrossRefGoogle Scholar
  18. Lioi L, Bollini R (1989) Identification of a new arcelin variant in wild bean seeds. Annu Rep Bean Improv Coop 32:28Google Scholar
  19. Minney BHP, Gatehouse AMR, Dobie P, Dendy J, Cardona C, Gatehouse JA (1990) Biochemical basis of seed resistance to Zabrotes subfasciatus (bean weevil) in Phaseolus vulgaris (common bean); a mechanism for arcelin toxicity. J Insect Physiol 36:757–767CrossRefGoogle Scholar
  20. Mirkov TE, Wahlstrom JM, Hagiwara K, Finardi-Filho F, Kjemtrup S, Chrispeels MJ (1994) Evolutionary relationships among proteins in the phytohemagglutinin-arcelin-α-amylase inhibitor family of the common bean and its relatives. Plant Mol Biol 26:1103–1113PubMedCrossRefGoogle Scholar
  21. Morton RL, Schroeder HE, Bateman KS, Chrispeels MJ, Armstrong E, Higgins TJV (2000) Bean α-amylase inhibitor 1 in transgenic peas (Pisum sativum) provides complete protection from pea weevil (Bruchus pisorum) under field conditions. Proc Natl Acad Sci USA 97:3820–3825PubMedCrossRefGoogle Scholar
  22. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325PubMedCrossRefGoogle Scholar
  23. Nakaguchi T, Arakawa T, Philo JS, Wen J, Ishimoto M, Yamaguchi H (1997) Structural characterization of an α-amylase inhibitor from a wild common bean (Phaseolus vulgaris): insight into the common structural features of leguminous α-amylase inhibitors. J Biochem (Tokyo) 121:350–354Google Scholar
  24. Nishizawa K, Maruyama K, Satoh R, Fuchikami Y, Higasa T, Utsumi S (2003) A C-terminal sequence of soybean β-conglycinin α′ subunit acts as a vacuolar sorting determinant in seed cells. Plant J 34:647–659PubMedCrossRefGoogle Scholar
  25. Nodari RO, Tsai SM, Gilbertson RL, Gepts P (1993) Towards an integrated linkage map of common bean. 2. Development of an RFLP-based linkage map. Theor Appl Genet 85:513–520CrossRefGoogle Scholar
  26. Osborn TC, Blake T, Gepts P, Bliss FA (1986) Bean arcelin. 2. Genetic variation, inheritance and linkage relationships of a novel seed protein of Phaseolus vulgaris L. Theor Appl Genet 71:847–855CrossRefGoogle Scholar
  27. Osborn TC, Alexander DC, Sun SSM, Cardona C, Bliss FA (1988) Insecticidal activity and lectin homology of arcelin seed protein. Science 240:207–210CrossRefGoogle Scholar
  28. Pueyo JJ, Hunt DC, Chrispeels MJ (1993) Activation of bean (Phaseolus vulgaris) α-amylase inhibitor requires proteolytic processing of the proprotein. Plant Physiol 101:1341–1348PubMedCrossRefGoogle Scholar
  29. Santino A, Valsasina B, Lioi L, Vitale A, Bollini R (1991) Bean (Phaseolus vulgaris L.) seed lectins: a novel electrophoretic variant of arcelin. Plant Physiol 10:7–11Google Scholar
  30. Sarmah BK, Moore A, Tate W, Molvig L, Morton RL, Rees DP, Chiaiese P, Chrispeels MJ, Tabe LM, Higgins TJV (2004) Transgenic chickpea seeds expressing high levels of a bean α-amylase inhibitor. Mol Breed 14:73–82CrossRefGoogle Scholar
  31. Schoonhoven AV, Cardona C, Valor J (1983) Resistance to the bean weevil and the Mexican bean weevil (Coleoptera: Bruchidae) in noncultivated common bean accessions. J Econ Entomol 76:1255–1259Google Scholar
  32. Schroeder HE, Gollash S, Moore A, Craig S, Hardie DC, Chrispeels MJ, Spencer D, Higgins TVJ (1995) Bean α-amylase inhibitor confers resistance to the pea weevil (Bruchus pisorum) in transgenic peas (Pisum sativum L.). Plant Physiol 107:1233–1239PubMedGoogle Scholar
  33. Shade RE, Schroeder HE, Pueyo JJ, Tabe LM, Murdock LL, Higgins TJV, Chrispeels MJ (1994) Transgenic pea seeds expressing the α-amylase inhibitor of the common bean are resistant to bruchid beetles. Biotechnology (NY) 12:793–796CrossRefGoogle Scholar
  34. Silva CP, Terra WR, Xavier-Filho J, Grossi de Sà MF, Lopes AR, Pontes EG (1999) Digestion in larvae of Callosobruchus maculatus and Zabrotes subfasciatus (Coleoptera: Bruchidae) with emphasis on α-amylases and oligosaccharidases. Insect Biochem Mol Biol 29:355–366CrossRefGoogle Scholar
  35. Silva CP, Terra WR, Grossi de Sa MF, Samuels RI, Isejima EM, Bifano TD, Almeida JS (2001) Induction of digestive α-amylases in larvae of Zabrotes subfasciatus (Coleoptera: Bruchidae) in response to ingestion of common bean α-amylase inhibitor 1. J Insect Physiol 47:1283–1290PubMedCrossRefGoogle Scholar
  36. Suzuki K, Ishimoto M, Kikuchi F, Kitamura K (1993) Growth inhibitory effect of an α-amylase inhibitor from the wild common bean resistant to the Mexican bean weevil (Zabrotes subfasciatus). Jpn J Breed 43:257–265Google Scholar
  37. Suzuki K, Ishimoto M, Kitamura K (1994) cDNA sequence and deduced primary structure of an α-amylase inhibitor from a bruchid-resistant wild common bean. Biochim Biophys Acta 1206:289–291PubMedGoogle Scholar
  38. Suzuki K, Ishimoto M, Iwanaga M, Kikuchi F, Kitamura K (1995) Inheritance of seed α-amylase inhibitor in the common bean and genetic relationship to arcelin. Theor Appl Genet 90:762–766CrossRefGoogle Scholar
  39. Yamada T, Hattroi K, Ishimoto M (2001a) Purification and characterization of two α-amylase inhibitors from seeds of tepary bean (Phaseolus acutifolius A. Gray). Phytochemistry 58:59–66CrossRefGoogle Scholar
  40. Yamada T, Teraishi M, Hattori K, Ishimoto M (2001b) Transformation of azuki bean by Agrobacterium tumefaciens. Plant Cell Tissue Organ Cult 64:47–54CrossRefGoogle Scholar
  41. Yamada T, Moriyama R, Hattori K, Ishimoto M (2005) Isolation of two α-amylase inhibitor genes of tepary bean (Phaseolus acutifolius A.Gray) and their functional characterization in genetically engineered azuki bean. Plant Sci 169:502–511CrossRefGoogle Scholar
  42. Young NM, Thibault P, Watson DC, Chrispeels MJ (1999) Post-translational processing of two α-amylase inhibitors and an arcelin from the common bean, Phaseolus vulgaris. FEBS Lett 446:203–206PubMedCrossRefGoogle Scholar
  43. Zambre M, Goossens A, Cardona C, Van Montagu M, Terryn N, Angenon G (2005) A reproducible genetic transformation system for cultivated Phaseolus acutifolius (tepary bean) and its use to assess the role of arcelins in resistance to the Mexican bean weevil. Theor Appl Genet 110:914–924PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Keito Nishizawa
    • 1
    • 2
  • Masayoshi Teraishi
    • 3
  • Shigeru Utsumi
    • 2
  • Masao Ishimoto
    • 1
    Email author
  1. 1.National Agricultural Research Center for Hokkaido RegionSapporoJapan
  2. 2.Laboratory of Food Quality Design and Development, Graduate School of AgricultureKyoto UniversityUjiJapan
  3. 3.Laboratory of Plant Production Control, Graduate School of AgricultureKyoto UniversityTakatsukiJapan

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