Legume Research

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Legume Research, volume 41 issue 5 (october 2018) : 639-646

Legumes: Potential source of entomotoxic proteins- A review

D. Sagar, Heena Dhall
1Division of Entomology, ICAR- Indian Agricultural Research Institute, New Delhi-110 012, India.
  • Submitted20-06-2017|

  • Accepted17-11-2017|

  • First Online 15-02-2018|

  • doi 10.18805/LR-3903

Cite article:- Sagar D., Dhall Heena (2018). Legumes: Potential source of entomotoxic proteins- A review. Legume Research. 41(5): 639-646. doi: 10.18805/LR-3903.
To meet the food demand of the ever-expanding world population there is a need for research and development for protecting crops against insect pests and pathogens. The way could be exploring the plant’s own defense mechanism by manipulating the expression of their endogenous defense proteins or introducing an insect control gene derived from another plants. The wild and resistant gene pools are the potential source of beneficial gene that offers considerable resistance to the insect pests. Insecticidal proteins viz., lectins, a-amylase inhibitor, urease, protease inhibitor, arcelins and cyclotides present in the seeds of pulses, especially in wild and resistance germplasms have been suggested to play a major role in insect resistance which are considered as most promising weapons that confer resistance against insects and which will be eco-friendly alternative to synthetic pesticides. Thus, it is very important to characterize these proteins and their encoding genes so that they can be used as viable means of producing pest resistant transgenic crops. This review deals with the biochemical features and mechanism of action of legume insecticidal proteins involved in defense mechanism against insect pests. 
  1. Atwal, A. S. and Dhaliwal, G. S. (2008). Agricultural Pests of South Asia and their Management. Kalyani Publishers, New Delhi. pp.487
  2. Azzouz, H., Cherqui A., Campan, E. D. M., Rahbe, Y., Duport, G. and Jouanin, L. (2005). Effects of plant protease inhibitors, oryzacystatin I and soybean Bowman-Birk inhibitor, on the aphid, Macrosiphum euphorbiae (Homoptera, Aphididae) and its parasitoid, Aphelinus abdominalis (Hymenoptera: Aphelinidae). J. Insect Physiol. 51:75-86.
  3. Barbeta, B. L., Marshall, A. T., Gillon, A. D., Craik, D. J. and Anderson, M. A. (2008). Plant cyclotides disrupt epithelial cells in the midgut of lepidopteran larvae. Proc. Natl. Acad. Sci. USA. 105:1221-1225.
  4. Barrett, A. J. (1987).The cystatins: a new class of peptidase inhibitors. Trends Biochem. Sci. 12: 193-196.
  5. Basse, C. W. (2005). Dissecting defense-related and developmental transcriptional responses of maize during Ustilago maydis infection and subsequent tumor formation. Plant Physiol. 138: 1774-1784.
  6. Becker-Ritt A. B., Martinelli A. H., Mitidieri S., Feder V., Wassermann G. E., Santi L., et. al, (2007). Antifungal activity of plant and bacterial ureases. Toxicon, 50: 971-983.
  7. Bode, W. and Huber, R. (1992). Natural protein proteinase inhibitors and their interaction with proteinases. Eur. J. Biochem. 204: 433-445.
  8. Boulter, D., Edwards, G. A., Gatehouse, A. M. R., Gatehouse, J. A. and Hilde, V. A. (1990). Additive protective effects of incorporating two different higher plants derived insect resistance genes in transgenic tobacco plants. Crop Prot. 9: 351-354.
  9. Bown, D. P., Wilkinson, H. S. and Gatehouse, J. A. (1997). Differentially regulated inhibitory sensitive protease genes from the phytophagous insect pest, Helicoverpa armigera, are members of complex multigene families. Insect Biochem Mol Biol. 27:625-638.
  10. Broadway, R. M. (1995). Are insects resistant to plant proteinase inhibitors? J. Insect Physiol. 2: 107-116.
  11. Burgess, E. P. J. and Gatehouse, A. M. R.(1997). Engineering for insect pest resistance: In: Biotechnology and the Improvement of Forage Legumes (eds McKersie, B. D. and Brown, D. C. W.), CAB International, Wallingford. pp. 229-258.
  12. Candido Ede, S., Pinto, M. F., Pelegrini, P. B., Lima, T. B., Silva, O. N., Pogue, R., et.al. (2011). Plant storage proteins with antimicrobial activity: novel insights into plant defense mechanisms. FASEB J. 10: 3290-305.
  13. Cardona, C., Kornegay, J., Posso, C. E., Morales, F. and 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: 197-206.
  14. Carlini C. R. and Polacco J. C. (2008). Toxic properties of urease. Crop Science, 48: 1665-1672.
  15. Chakraborti, D., Sarkar, A., Mondal, H. A. and Das, S. (2009). Tissue specific expression of potent insecticidal, Allium sativum leaf agglutinin (ASAL) in important pulse crop, chickpea (Cicer arietinum L.) to resist the phloem feeding Aphis craccivora. Transgenic Res.18: 529-544.
  16. Chiche, L., Heitz, A., Gelly, J. C., Gracy, J. Chau, P. T., Ha, P. T., Hernandez, J. F. and Le-Nguyen, D. (2004). Squash inhibitors: From structural motifs to macrocyclic knottins. Curr Protein Pept. Sci. 5:341-349.
  17. Chouabe, C., Eyraud, V., Da Silva, P., Rahioui, I., Royer, C., Soulage, C., Bonvallet, R., Huss, M. and Gressent, F. (2011). New mode of action for a knottin protein bioinsecticide: pea albumin 1 subunit b (PA1b) is the first peptidic inhibitor of V-ATPase. J. Biol. Chem. 286: 36291-36296.
  18. Colgrave, M. L. and Craik, D. J. (2004). Thermal, chemical, and enzymatic stability of the cyclotide Kalata B1: The importance of the cyclic cystine knot. Biochem. 43: 5965-5975.
  19. Colgrave, M. L., Kotze, A. C., Huang, Y. H., Grady, J. O., Simonsen, S. M. and Craik, D. J. (2008). Cyclotides: Natural, circular plant peptides that possess significant activity against gastrointestinal nematode parasites of sheep. Biochem. 47: 5581–5589.
  20. Connors, B. J., Laun, N. P., Maynard, C. A. and Powell, W. A. (2002). Molecular characterization of gene encoding a cystatin expressed in the stems of American Chestnut (Castanea dentate). Planta, 215: 510-514.
  21. Craik, D. J., Daly, N. L., Bond, T. and Waine, C. (1999). Plant cyclotides: A unique family of cyclic and knotted proteins that defines the cyclic cystine knot structural motif. J. Mol. Biol. 294: 1327-1336.
  22. Craik, D. J., Cemazar, M., Wang, C. K. and Daly, N. L. (2006). The cyclotide family of circular miniproteins: Nature’s combinatorial peptide template. Biopolymers, 84: 250-266.
  23. Damme, V. E. J. M., Lannoo, N., Peumans, W. J. (2008). Plant lectins. Adv. Bot. Res. 48: 107-209.
  24. Dixon, N. E., Gazzola, T. C., Blakeley, R. L. and Zermer, B. (1975). Jack bean urease (EC 3.5.1.5). A metalloenzyme. A simple biological role for nickel. J. Am. Chem. Soc. 97: 4131–4133.
  25. Fabrick, J., Behnke, C., Czapla, T., Beta, K., Rao, A. G., Kramer, K. J. and Reeck, G. R. (2002). Effect of a potato cysteine proteinase inhibitor on midgut proteolysis enzyme activity and growth of the southern corn root worm, Diabrotica undecimpunctata Howardi (Coleoptera: Chrysomelidae), Insect Biochem. Mol. Biol. 32: 405-415.
  26. Feng, G. H., Richardson, M., Chem, M. S., Kramer, K. J., Morgan, T. D. and Reeck, G. R. (1996). Alpha-amylase inhibitor from wheat: Amino acid sequences and patterns of inhibition of insect and human alpha-amylases. Insect Biochem. Mol. Biol. 26: 419-426.
  27. Ferreira-DaSilva, C. T., Gombarovits, M. E., Masuda, H., Oliveira, C. M. and Carlini, C. R. (2000). Proteolytic activation of canatoxin, a plant toxic protein, by insect cathepsin-like enzymes. Arch. Insect Biochem. Physiol. 44: 162–171.
  28. Frédéric Gressent, Pedro Da Silva, Vanessa Eyraud, Lamis Karaki and Corinne Royer (2011). Pea Albumin 1 Subunit b (PA1b), a Promising Bio-insecticide of Plant Origin. Toxins(Basel), 3: 1502-1517.
  29. Giri, A. P., Harsulkar, A. M., Ku, M. S. B., Gupta, V. S., Deshpande, V. V., Ranjekar, P. K. and Franceschi, V. R. (2003). Identification of potent inhibitors of Helicoverpa armigera gut proteinases from winged bean seeds. Phytochem. 63: 523-532.
  30. Grossi de Sa, M. F. and Chrispeels, M. J. (1997). Molecular cloning of bruchid (Zabrotes subfasciatus) á-amylase cDNA and interactions of the expressed enzyme with bean amylase inhibitors. Insect Biochem. Mol. Biol. 27: 271-281.
  31. Gunasekera, S., Foley, F. M., Clark, R. J., Sando, L., Fabri, L. J., Craik, D. J. and Daly, N. L. (2008). Engineering stabilized vascular endothelial growth factor-A antagonists: Synthesis, structural characterization and bioactivity of grafted analogues of cyclotides. J. Med. Chem. 51: 7697-7704.
  32. Habibi, J., Backus, E. A. and Czapla, T. H. (1993). Plant lectins affect survival of the potato leaf-hopper (Homoptera-Cicadellidae). J. Econ. Entomol. 86: 945-951.
  33. Heiser, C. B. (1990). Seed to Civilization: The Story of Food. Harvard University Press, pp. 228.
  34. Hilder, V. A., Gatehouse, A. M. R., Sheerman, S. E., Barker, R. F. and Boulter, D. (1987). A novel mechanism of insect resistance engineered into tobacco. Nature, 300: 160-163.
  35. Huesing, J. E., Shade, R. E., Chrispeels, M. J. and Mirclock, L. L. (1991). a-Amylase inhibitor, Not phytohemagglutinin, Explains resistance of common bean seeds to cowpea weevil. Plant Physiol. 96: 993-996.
  36. Ishimoto, M., Sato, T., Chripeels, M. J. and Kitamura, K. (1996). Bruchid resistance of transgenic azuki bean expressing seed alpha amylase inhibitor of common bean. Entomol. Exp. Appl. 79: 309-315.
  37. Janzen, D. H., Juster, H. B. and Liener, I. E. (1976). Insecticidal action of the phytohemagglutinin in black bean on a bruchid beetle. Science, 192: 795-796.
  38. Kansal, R., Kumar, M., Kuhar K., Gupta, R. N., Subrahmanyam, B., Koundal, K. R. and Gupta, V. K. (2008). Purification and characterization of trypsin inhibitor from Cicer arietineum L. and its efficacy against Helicoverpa armigera. Brazil. Soc. Plant Physiol. 20: 313-322.
  39. Kirsi, M. (1974). Proteinase inhibitors in germinating barley embryos. Physiol. Plant. 32: 89-93.
  40. Kluh, I., Horn, M., Hblový´, J., Hubert, J., Dole-ý‘kový´-Mareý´ový´, L., Voburka. Z.,et.al. (2005). Inhibitory specificity and insecticidal selectivity of a-amylase inhibitor from Phaseolus vulgaris. Phytochem. 66: 31-39.
  41. Kosslak, R. M., Chamberlin, M. A., Palmer, R. G. and Bowen, B. A. ( 1997). Programmed Cell Death in the Root Cortex of Soybean Root Necrosis Mutants. Plant J. 11: 729-745.
  42. Koundal, K. R. and Rajendran, P. (2003). Plant insecticidal proteins and their potential for developing transgenics resistant to insect pests. Indian J. Biotech. 2: 110-120.
  43. Kuroda, M., Ishimoto, M., Suzuki, K., Kondo, H., Abe, K., Kitamura, K. and Arai, S. (1996). Oryzacystatins Exhibit Growth-inhibitory and lethal effects on different species of bean insect pests, Callosobruchus chinensis (Coleoptera) and Riptortus clavatus (Hemiptera). Biosci. Biotechnol. Biochem. 60: 209-212.
  44. Lam, J. M., Pwe, K. H., Sun, W. Q., Chua, Y. L. and Wang, X. J.( 1999). Enzyme stabilizing activity of seed trypsin inhibitors during desiccation. Plant Sci. 142: 209-218.
  45. Lee, S. I., Lee, S. H., Koo, J. C., Chun, H. J., Lim, C. O., Mun, J. H., Song, Y. H. and Cho, M.J. (1999). Soybean Kunitz trypsin inhibitor (SKTI) confers resistance to the brown planthopper (Nilaparvata lugens Stal) in transgenic rice. Mol. Breed. 5: 1-9.
  46. Leple, J. C., Bonadebottino, M., Augustin, S., Pilate, G., Letan, V. D., Delplanque, A., Cornu, D. and Jouanin, L. (1995). Toxicity to Chrysomela tremulae (Coleoptera: Chrysomelidae) of transgenic poplars expressing a cysteine proteinase inhibitor. Mol. Breed. 1: 319-328.
  47. Lipke, H., Fraenkel, G. S. and Liener, I. E. (1954). Effects of soybean inhibitors on growth of Tribolium confusum. J. Sci. Food Agri. 2: 410-415.
  48. Liu, B., Bian, H. J. and Bao, J. K. (2010). Plant lectins: potential antineoplastic drugs from bench to clinic. Cancer Lett. 287: 1-12.
  49. Lu, X. F., Xia,Y. X. and Pei, Y. (1998). Roles of plant proteinase inhibitors in the resistance of plant against insects and pathogens. Prog. Biochem. Biophys. 25: 328-333.
  50. Macedo, M. L., Freire, M. D. G. M., Da Silva, M. B. and Coelho, L. C. (2007). Insecticidal action of Bauhinia monandra leaf lectin (BmoLL) against Anagasta kuehniella (Lepidoptera: Pyralidae), Zabrotes subfasciatus and Callosobruchus maculatus (Coleoptera: Bruchidae). Comp. Biochem. Physiol. Mol. Integr. Physiol. 146: 486-498.
  51. Meiners, J. P. and Elden, T. C. (1978). Resistance to insects and diseases in Phaseolus. In: Advances in Legume Science. International Legume Conference, (Summerfield, R. S and Bunting, A.H. (Eds.)). Kew Surrey, UK. pp. 359-364.
  52. Mickel, C. E. and Standish, J. (1947). Susceptibility of processed soy flour and soy grits in storage to attack by Tribolium castaneum. University of Minnesota Agricultural Experimental Station Technical Bulletin. 178: 1-20.
  53. Mirkov, T. E., Wahlstrom, J. E., Hagiwara, K., Finardi-Filho, F., Kjemtrup, S. and Chrispeels, M. J. (1994). Evolutionary relationships among proteins in the phytohemagglutininin arcelin-á-amylase inhibitor family of the common bean and its relatives. Plant Mol. Biol. 26: 1103-111.
  54. Mittal, A., Kansal, R., Kalia, V., Tripathi, M. and Gupta,V. K. (2014). A kidney bean trypsin inhibitor with an insecticidal potential against Helicoverpa armigera and Spodoptera litura. Acta. Physiol. Plant. 36: 525-539.
  55. Mulinari, F., Staniscuaski F., Bertholdo-Vargas L. R., Postal, M., Oliveira-Neto O. B., et.al, (2007). Jaburetox-2Ec: an insecticidal peptide derived from an isoform of urease from the plant Canavalia ensiformis. Peptides. 28: 2042-2050.
  56. Piovesan, A. R., Staniscuaski, F., Marco-Salvadori, J., Real-Guerra, R., Defferrari, M. S. and Carlini, C. R. (2008). Stage-specific gut proteinases of the cotton stainer bug, Dysdercus peruvianus: role in the release of entomotoxic peptides from Canavalia ensiformis urease. Insect Biochem. Mol. Biol. 38: 1023-1032.
  57. Plan, M. R. R., Saska, I., Cagauan, A.G. and Craik, D.J. (2008). Backbone cyclised peptides from plants show molluscicidal activity against the rice pest Pomacea canaliculata (golden apple snail). J. Agric. Food Chem. 56:5237–5241.
  58. Poth, A. G., Colgrave, M. L., Philip, R., Kerenga, B., Daly, N. L., Anderson, M. A. and Craik, D. J. (2011). Discovery of cyclotides in the Fabaceae plant family provides new insights into the cyclization, evolution and distribution of circular proteins. ACS Chem. Biol. 6: 345-355.
  59. Pusztai, A., Ewen, S.W., Grant, G., Brown, D. S., Stewart, J. C., Peumans, W. J., Van Damme, E. J. and Bardocz, S. (1993). Antinutritive effects of wheat-germ agglutinin and other N-acetylglucosamine specific lectins. Br. J. Nutr. 70: 313-321.
  60. Puttamadappa, S. S., Jagadish, K., Shekhtman, A. and Camarero, J. A. (2010). Backbone dynamics of cyclotide MCoTI-I free and complexed with trypsin. Angew Chem Int Ed Engl 49: 7030-7034.
  61. Rahbe, Y. and Febvay, G. (1993). Protein toxicity to aphids: an in vitro test on Acyrthosiphon pisum. Entomol. Exp. Appl. 67:149-160.
  62. Ramesh Babu and Subrahmanyam, B. (2012). Effect of french bean seed proteinase inhibitors (fbpis) on trypsin and chymotrypsin activity, growth and development of Helicoverpa armigera (hubner). The Bioscan. 7: 653-659.
  63. Read, J. W. and Haas, L.W. (1938). Studies on the baking quality of flour as affected by certain enzyme actions. Cereal Chem. 45: 59-68.
  64. Robert, N., Roche, K., Lebeau, Y., Breda, C., Boulay, M., Esnault, R. and Buffard, D. (2002). Expression of grapevine chitinase genes in berries and leaves infected by fungal or bacterial pathogens. Plant Sci. 162: 389-400.
  65. Rouge´, P., Richardson, M., Ranfaing, P., Yarwood, A. and Sousa- Cavada, B. (1987). Single- and two-chain legume lectins as phylogenetic markers of speciation. Bio. Syst. Econ. 15: 341-348.
  66. Ryan, C. A. (1981). The Biochemistry of Plants (ed. Marcus, A.), Academic Press, New York. 6: 351-370.
  67. Ryan, C. A. (1990). Proteinase inhibitors in plants: genes for improving defenses against insects and pathogens. Ann. Rev. Phytophathol. 28: 425-449.
  68. Saha, P., Majumder, P., Dutta, I., Ray, T., Roy, S. C. and Das, S. (2006). Transgenic rice expressing Allium sativum leaf lectin with enhanced resistance against sap-sucking insect pests. Planta. 223: 1329-1343.
  69. Sane, V. A., Nath, P., Aminuddin and Sane, P. V. (1997). Development of insect resistant transgenic plants used in plant genes: Expression of cowpea trypsin inhibitor in transgenic tobacoo plants. Curr. Sci. 72: 741-747.
  70. Sauvion, N., Rahbe, Y., Pneumans, W. J., van Damme, E. J. M., Gatehouse, J. A. and Gatehouse A. M. R. (1996). Effect of GNA and other mannose binding lectins on development and fecundity of the peach potato aphids Myzus persicae. Entomol. Exp. Appl.79: 285-293.
  71. Schroeder, H. E., Gollasch, S., Moore, A., Tabe, L. M., Craig, S., Hardie, D., Chrispeels, M. J., Spencer, D. and Higgins, T. J. V. (1995). Bean á-amylase inhibitor confers resistance to the pea weevil, Bruchus pisorum, in genetically engineered peas (Pisum sativum L.). Plant Physiol. 107: 1233-1239.
  72. Schuler, T. H., Poppy, G. M., Kerry, B. R. and Denholm, I. (1998). Insect-resistant transgenic plants. Biotechnol. 16: 168-175.
  73. Staniscuaski, F., Ferreira-Dasilva, C. T., Mulinari, F., Pires-Alves, M. and Carlini, C. R. (2005). Insecticidal effects of canatoxin on the cotton stainer bug, Dysdercus peruvianus (Hemiptera: Pyrrhocoridae). Toxicon. 45: 753-760.
  74. Stanley-Samuelson, D. W. J. (1994). Assessing the significance of prostaglandins and other eicosanoids in insect physiology. Insect Physiol, 40: 3-11.
  75. Ussuf, K. K., Laxmi, N. H. and Mitra, R. (2001). Proteinase inhibitors: Plant-derived genes of insecticidal protein for developing insect-resistant transgenic plants. Curr. Sci. 80: 847-85.
  76. Vandenborre, G., Smagghe, G. and Van Damme, E. J. M. (2011). Plant lectins as defense proteins against phytophagous insects. Phytochem. 72: 1538-50.
  77. Vasconcelos, I. M. and Oliveira, J. T. A. (2004). Antinutritional properties of plant lectins. Toxicon. 44: 385-403.
  78. Verma, J. and Dubey, N., (1999). Perspectives of botanical and microbial products as pesticides of tomorrow. Curr. Sci.76: 172-179.

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