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Purified winged bean protease inhibitor affects the growth of Bactrocera cucurbitae

Published online by Cambridge University Press:  20 December 2018

A.P. Kaur  and
S.K. Sohal
A.P. Kaur
Affiliation:
Department of Zoology, Guru Nanak Dev University, Amritsar 143 005, India
S.K. Sohal*
Affiliation:
Department of Zoology, Guru Nanak Dev University, Amritsar 143 005, India
*
*Author for correspondence Phone: 91-183-2258802-09; Extn. 3398 Fax: 91-183-2258819 E-mail: [email protected]
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Abstract

The melon fruit fly, Bactrocera cucurbitae (Coquillett), is a serious agricultural pest which has defied the various control measures employed against it. Protease inhibitors present in plants which have the potential to inhibit the growth and development of associated insect pests can be a possible alternative which can be manipulated for developing resistance in plants to the pest. In the present study, winged bean (Psophocarpus tetragonolobus) protease inhibitor isolated through affinity chromatography was explored for its potential to disrupt the development of melon fruit fly, B. cucurbitae. Different concentrations (12.5, 25, 50, 100, 200, and 400 µg ml−1) of the winged bean protease inhibitor (WBPI) were incorporated into the artificial diet of the second instar (64–72 h old) larvae of B. cucurbitae. The WBPI significantly delayed the larval, pupal, and total development period. The percentage pupation and adult emergence of the treated larvae was reduced as compared with control. The activities of major digestive enzymes (trypsin, chymotrypsin, leucine aminopeptidase, and elastase) decreased significantly in the larvae treated with different concentrations (50, 100, 200, and 400 µg ml−1) of WBPI. The findings reveal that the inhibitor holds considerable promise for the management of the melon fruit fly.

Keywords

Bactrocera cucurbitaePsophocarpus tetragonolobusmelon fruit flyprotease inhibitorswinged beans
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 109 , Issue 4 , August 2019 , pp. 550 - 558
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Copyright
Copyright © Cambridge University Press 2018 

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References

Azzouz, H., Cherqui, A., Campman, E.D.M., Duport, G., Jouanin, L., Kaiser, L. & Giordanango, P. (2005) Effects of plant protease inhibitors, oryzacystatin I and soybean Bowman-Birk inhibitor, on the aphid Macrosaphium euphorbiae (Homoptera: Aphididae) and its parasitoid Aphelinus abdominalis (Hymenoptera: Aphelinidae). Journal of Insect Physiology 51, 75–86.Google Scholar
Barrett, A.J., Rawlings, N.D. & Woessner, J.F. (1998) Handbook of Proteolytic Enzymes. London, UK, Academic Press.Google Scholar
Bhattacharyya, A., Mazumdar, S., Leighton, S.M. & Babu, C.R. (2006) A Kunitz proteinase inhibitor from Archidendron ellipticum seeds: purification, characterization, and kinetic properties. Phytochemistry 67, 232–241.Google Scholar
Birk, Y. (1996) Protein proteinase inhibitors in legume seeds – overview. Archivos latinoamericanos de nutrición 44 (4 Suppl 1) 26S–30S.Google Scholar
Broadway, R.M. & Duffey, S.S. (1986) Plant proteinase inhibitors: mechanism of action and effect on the growth and digestive physiology of larval Heliothis zea and Spodoptera exigua. Journal of Insect Physiology 32, 827–833.Google Scholar
Christeller, J.T., Laing, W.A., Shaw, B.D. & Burgess, E.P.J. (1990) Characterization and partial purification of the digestive proteases of the black field cricket, Telleogryllus commodus (Walker): elastase is a major component. Insect Biochemistry 20, 157–164.Google Scholar
Christeller, J.T., Laing, W.A., Markwic, N.P. & Burgess, E.P.J. (1992) Midgut protease activities in 12 phytophagous lepidopteran larvae: dietary and protease inhibitor interactions. Insect Biochemistry and Molecular Biology 22, 735–746.Google Scholar
Clausen, C.P., Clancey, D.W. & Chock, Q.C. (1965) Biological control of the Oriental fruit fly (Dacus dorsalis Hendel) and other fruit flies in Hawaii. U.S. Department of Agriculture Bulletin No. 1322, Washington DC.Google Scholar
Dunse, K.M., Stevens, J.A., La, F.T., Gaspar, Y.M., Heath, R.L. & Anderson, M.A. (2010) Coexpression of potato type I and II proteinase inhibitors gives cotton plants protection against insect damage in the field. Proceedings of the National Academy of Sciences USA 107, 15011–15015.Google Scholar
Fitt, G.P. (1994) Cotton pest management: part 3, an Australian perspective. Annual Reviews of Entomology 39, 543–562.Google Scholar
Forget, G. (1993) Balancing the need for pesticides with the risk to human health. p. 2 in Forget, G., Goodman, T. & de Villiers, A. (Eds) Impact of Pesticide Use on Health in Developing Countries. Ottawa, IDRC.Google Scholar
Garcia, V.A., Freire, M.G.M., Novello, J.C., Marangoni, S. & Macedo, M.L.R. (2004) Trypsin inhibitor from Poecilanthe parviflora seeds: purification, characterization, and activity against pest proteases. Protein Journal 23, 343–350.Google Scholar
Gatehouse, A.M., Hilder, V.A., Powell, K.S., Wang, M., Davison, G.M., Gatehouse, L.N., Down, R.E., Edmonds, H.S., Boulter, D., Newell, C.A., Merryweather, A., Hamilton, W.D.O. & Gatehouse, J.A. (1994) Insect-resistant transgenic plants: choosing the gene to do the ‘job’. Biochemical Society Transactions 22, 944–949.Google Scholar
Ge, Z.Y., Wan, P.J. & Han, Z.J. (2012) Cloning and characterization of trypsin and chymotrypsin-like genes in the striped rice stem borer, Chilo suppressalis. Genome 55, 281–288.Google Scholar
Giri, A.P., Harsulkar, A.M., Ku, M.S., Gupta, V.S., Deshpande, V.V., Ranjekar, P.K. & Franceschi, V.R. (2003) Identification of potent inhibitors of Helicoverpa armigera gut proteinases from winged bean seeds. Phytochemistry 63, 523–532.Google Scholar
Gomes, A.P.G., Dias, S.C., Broch, C. Jr., Melo, F.R., Furtado, J.R. Jr., Monnert, R.G., Grossi-de-Sa, M.F. & Franco, O.L. (2005) Toxicity to cotton boll weevil Anthonomus grandis of a trypsin inhibitor from chick pea seeds. Comparative Biochemistry and Physiology 140, 313–319.Google Scholar
Gunning, R.V., Easton, C.S., Balfe, M.E. & Ferris, I.G. (1991) Pyrethroid resistance mechanisms in Australian Helicoverpa armigera. Pesticide Science 33, 473–490.Google Scholar
Gupta, J.N., Verma, A.N. & Kashyap, R.K. (1978) An improved method for mass rearing for melon fruit fly Dacus cucurbitae Coquillett. Indian Journal of Entomology 40, 470–471.Google Scholar
Gupta, P., Dhawan, K., Malhotra, S.P. & Singh, R. (2000) Purification and characterization of trypsin inhibitor from seeds of faba bean (Vicia faba L.). Acta Physiologiae Plantarum 22, 433–438.Google Scholar
Gupta, G.P., Birah, A. & Rani, S. (2008) Growth-inhibitory effects of winged bean (Psophocarpus tetragonolobus) proteinase inhibitors on two problematic lepidopteran pests. Indian Journal of Agricultural Sciences 78, 159–162.Google Scholar
Haq, S.K., Atif, S.M. & Khan, R.H. (2004) Protein proteinase inhibitor genes in combat against insects, pests, and pathogens: natural and engineered phytoprotection. Archives of Biochemistry and Biophysics 431, 145–159.Google Scholar
Haq, I., Cáceres, C., Hendrichs, J., Teal, P.E.A., Wornoayporn, V., Stauffer, C. & Robinson, A.S. (2010) Effects of the juvenile hormone analogue methoprene and dietary protein on male melon fly Bactrocera cucurbitae (Diptera: Tephritidae) mating success. Journal of Insect Physiology 56, 1503–1509.Google Scholar
Harsulkar, A.M., Giri, A.P. & Kothekar, V.S. (1997) Protease inhibitors of chickpea (Cicer arietinum L.) during seed development. Journal of the Science of Food and Agriculture 74, 509–512.Google Scholar
Harsulkar, A.M., Giri, A.P., Patankar, A.G., Gupta, V.S., Sainani, M.N., Ranjekar, P.K. & Deshpande, V.V. (1999) Successive use of non-host plant proteinase inhibitors required for effective inhibition of gut proteinases and larval growth of Helicoverpa armigera. Plant Physiology 121, 497–506.Google Scholar
Heath, R.L., McDonald, G., Christeller, J.T., Lee, M., Bateman, K., West, J., Heeswijck, R.V. & Anderson, M.A. (1997) Proteinase inhibitors from Nicotiana alata enhance plant resistance to insect pests. Journal of Insect Physiology 9, 833–842.Google Scholar
Hoffman, M.P., Zalom, F.G., Smilanick, J.M., Malyj, L.D., Kiser, J., Wilson, L.T., Hilder, V.A. & Barnes, W.M. (1991) Field evaluation of transgenic tobacco containing genes encoding Bacillus thuringiensis δ-endotoxin or cowpea trypsin inhibitor: efficacy against Helicoverpazea (lepidoptera: Noctuidae). Journal ofEconomic Entomology 85, 2516–2522.Google Scholar
Igbedioh, S.O. (1991) Effects of agricultural pesticides on humans, animals and higher plants in developing countries. Archives of Environmental Health 46, 218.Google Scholar
Jeyaratnam, J. (1985) Health problems of pesticide usage in the third world. British Journal of Industrial Medicine 42, 505–506.Google Scholar
Kansal, R., Kumar, M., Kuhar, K., Gupta, R.N., Subhrahmanyam, B., Koundal, K.R. & Gupta, V.K. (2008) Purification and characterization of trypsin inhibitor from Cicer arietinum L. and its efficacy against Helicoverpa armigera. Brazilian Journal of Plant Physiology 20, 313–322.Google Scholar
Kaur, A.P. & Sohal, S.K. (2016) Pea protease inhibitor inhibits protease activity and development of Bactrocera cucurbitae. Journal of Asia Pacific Entomology 19, 1183–1189.Google Scholar
Kaur, H., Kaur, A.P., Sohal, S.K., Rup, P.J. & Kaur, A. (2009) Effect of soybean trypsin inhibitor on development of immature stages of Bactrocera cucurbitae (Coquillett). Biopesticide International 5, 114–124.Google Scholar
Kaur, H., Sohal, S.K., Rup, P.J. & Kaur, A. (2010) Growth and development of melon fruit fly larvae under the influence of soybean trypsin inhibitors. International Journal ofTropical Insect Sciences 30, 200–206.Google Scholar
Koyama, T., Kakinohana, H. & Miyatake, T. (2004) Eradication of the melon fly Bactrocera cucurbitae in Japan: importance of behaviour, ecology, genetics and evolution. Annual Review of Entomology 49, 331–349.Google Scholar
Laemmli, U.K. (1970) Cleavage of structural protein during assembly of the head of bacteriophage T4. Nature 227, 680–668.Google Scholar
Lawrence, P.K. & Koundal, K.R. (2002) Plant protease inhibitors in control of phytophagous insects. Journal of Biotechnology 5, 93–109.Google Scholar
Lipke, H., Fraenkel, G.S. & Liener, I.E. (1954) Effects of soybean inhibitors on growth of Tribolium confusum. Journal of Science and Food Agriculture 2, 410–415.Google Scholar
Lowry, O.H., Rosebrough, A., Lewis, F.A. & Randall, R.J. (1951) Protein measurement with the Folin Phenol reagent. Journal of Biological Chemistry 193, 263–275.Google Scholar
Macedo, M.L.R., Durigan, R.A., da Silva, D.S., Marangoni, S., Freire, M.D.G.M. & Parra, J.R.P. (2010) Adenanthera pavonina trypsin inhibitor retard growth of Anagasta kuehniella (Lepidoptera: Pyralidae). Archives of Insect Biochemistry and Physiology 73, 213–231.Google Scholar
Markwick, N.P., Reid, S.J., Laing, W.A. & Christeller, J.T. (1995) Effect of dietary protein and protease inhibitors on codling moth (Lepidoptera: Tortricidae). Journal of Economic Entomology 88, 33–39.Google Scholar
McManus, M.T. & Burgess, E.P.J. (1995) Effects of the soybean (Kunitz) trypsin inhibitor on growth and digestive proteases of larvae of Spodoptera litura. Journal of Insect Physiology 41, 731–738.Google Scholar
Mello, G.C., Oliva, M.L.V., Sumikawa, J.T., Machado, O.L.T., Marangoni, S., Novello, J.C. & Macedo, M.L.R. (2001) Purification and characterization of a new trypsin inhibitor from Dimorphandra mollis seeds. Journal of Protein Chemistry 20, 625–632.Google Scholar
Mochizuki, A., Nishizawa, Y., Onodera, H., Tabei, Y., Toki, S., Habu, Y., Ugaki, M. & Ohashi, Y. (1999) Transgenic rice plants expressing a trypsin inhibitor are resistant against rice stem borers, Chilo suppressalis. Entomologia Experimentalis et Applicata 93, 173–178.Google Scholar
Narayanan, E.S. & Batra, H.N. (1960) Fruit Flies and Their Control. New Delhi, India, Indian Council of Agricultural Research, pp. 1–68.Google Scholar
Pandey, P.K., Singh, D., Singh, S., Khan, M.Y. & Jamal, F. (2014) A non-host peptidase inhibitor of~14 kDa from Butea monosperma (Lam.) Taub. seeds affects negatively the growth and developmental physiology of Helicoverpa armigera. Biochemistry Research International 2014, 1–11.Google Scholar
Paulino da Silva, L., Leite, J.R.S.A., Bloch, C. Jr. & Maria de Freitas, S. (2001) Stability of a blackeyed pea trypsin/chymotrypsin inhibitor (BTCI). Protein Peptide Letters 8, 33–38.Google Scholar
Pompermayer, P., Lopes, A.R., Terra, W.R., Parra, J.R.P., Falco, M.C. & Silva-Filho, M.C. (2001) Effects of soybean proteinase inhibitor on development, survival and reproductive potential of the sugarcane borer, Diatraea saccharalis. Entomologia Experimentalis et Applicata 99, 79–85.Google Scholar
Ponnuvel, K.M., Nithya, K., Sirigineedi, S., Awasthi, A.K. & Yamakawa, M. (2012) “In vitro antiviral activity of an alkaline trypsin from the digestive juice of bombyx mori larvae against nucleopolyhedrovirus: antiviral activity of an alkaline trypsin from Bombyx mori against Nucleopolyhedrovirus”. Archives of Insect Biochemistry and Physiology 81, 90–104.Google Scholar
Prasad, E.R., Dutta-Gupta, A. & Padmasree, K. (2010) Insecticidal potential of Bowman–Birk proteinase inhibitors from red gram (Cajanus cajan) and black gram (Vigna mungo) against lepidopteran insect pests. Pesticide Biochemistry and Physiology 98, 80–88.Google Scholar
Rahbe, Y., Ferrasson, E., Rabesona, H. & Quillies, L. (2003) Toxicity to the pea aphid Acyrthosiphon pisum of anti-chymotrypsin isoforms and fragments of Bowman-Birk protease inhibitors from pea seeds. Insect Biochemistry and Molecular Biology 33, 299–306.Google Scholar
Roessler, Y. (1989) Insecticidal bait and cover sprays. pp. 329–336 in Robinson, A.S. & Hooper, G. (Eds) Fruit Flies, Their Biology, Natural Enemies and Control. The Netherlands, Amsterdam, Elsevier.Google Scholar
Roy, S. & Dutta, S.K. (2009) Purification of chymotrypsin-trypsin inhibitor from winged bean seeds using single step immunoaffinity column. American Journal of Biochemistry and Biotechnology 5, 142–146.Google Scholar
Saadati, F. & Bandani, A.R. (2011) Effects of serine protease inhibitors on growth and development and digestive serine proteinases of the Sunn pest, Eurygaster integriceps. Journal of Insect Science 11, 72.Google Scholar
Schluter, U., Benchabane, M., Munger, A., Kiggundu, A., Vorster, J., Goulet, M.C., Cloutier, C. & Michaud, D. (2010) Recombinant protease inhibitors for herbivore pest control: a multirophic perspective. Journal of Experimental Botany 61, 41–69.Google Scholar
Shukle, R.H., Murdock, L.L. & Gallun, R.L. (1985) Identification and partial characterization of a major gut proteinase from larvae of the Hessian fly, Mayetiola destructor (Say) (Diptera: Cecidomyiidae). Insect Biochemistry 15, 93–101.Google Scholar
Slansky, F. Jr. & Scriber, J.M. (1985) Food consumption and utilization. pp. 87–163 in Kerkut, G.A. & Gilbert, L.I. (Eds) Comprehensive Insect Physiology, Biochemistry and Pharmacology. Oxford, Pergamon Press.Google Scholar
Srinivasan, A., Chougule, N.P., Giri, A.P., Gatehouse, J.A. & Gupta, V.S. (2005) Pod borer (Helicoverpa armigera Hubn.) does not show specific adaptations in gut proteinases to dietary Cicer arietinum Kunitz proteinase inhibitor. Journal of Insect Physiology 51, 1268–1276.Google Scholar
Srivastava, B.G. (1975) A chemically defined diet for Dacus cucurbitae (Coq.) larvae under aseptic conditions. Entomology Newsletters 5, 24.Google Scholar
Steffens, R., Fox, F.R. & Kassell, B. (1978) Effect of trypsin inhibitors on growth and metamorphosis of corn borer larvae Ostrinia nubilolis (Hubner). Journal of Agriculture and Food Chemistry 26, 170–174.Google Scholar
Tamhane, V.A., Giri, A.P., Sainani, M.N. & Gupta, V.S. (2007) Diverse forms of Pin-II family proteinase inhibitors from Caspicum annuum adversely affect the growth and development of Helicoverpa armigera. Gene 403, 29–38.Google Scholar
White, I.M. & Elson-Harris, M.M. (1992) Fruit Flies of Economic Significance: Their Identification and Bionomics. Wallingford, UK, CAB International, p. 601.Google Scholar
Zhu-Salzman, K. & Zeng, R.S. (2015) Insect response to plant defensive protease inhibitors. Annual Reviews of Entomology 60, 233–252.Google Scholar