Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-26T15:32:34.977Z Has data issue: false hasContentIssue false

Effect of protein extracts of Amaranthus retroflexus (Amaranthaceae) and Cuminum cyminum (Apiaceae) on digestive proteinases and biological characters of Helicoverpa (Heliothis) armigera (Hübner) (Lepidoptera: Noctuidae)

Published online by Cambridge University Press:  05 June 2020

Solmaz Azimi*
Affiliation:
1Department of Plant Protection, Azarbaijan Shahid Madani University, Tabriz, Iran
Shima Rahmani
Affiliation:
2Department of Plant Protection, Science and Research Branch, Islamic Azad University, Tehran, Iran
Maghsoud Pazhouhandeh
Affiliation:
3Department of Biotechnology, Azarbaijan Shahid Madani University, Tabriz, Iran
*
*Corresponding author. Email: [email protected]

Abstract

Plant proteinase inhibitors are among the promising biopesticides which are induced in plants tissues against the several Lepidoptera pests to inhibit digestive proteases. In this study, protein extracts of two nonhost plant seeds, Amaranthus retroflexus Linnaeus (Amaranthaceae) and Cuminum cyminum Linnaeus (Apiaceae), were examined on Helicoverpaarmigera (Hübner) (Lepidoptera: Noctuidae). The results obtained by using azocasein as a substrate showed that inhibitory activity of general proteases of the larvae fed on a diet incorporated with both inhibitors was dose dependent. Seed extracts of A. retroflexus and C. cyminum at the highest concentration showed that inhibition activities of chymotrypsin-like proteinase and trypsin-like proteinase were between 31–45% and 28–61%, respectively. Based on polyacrylamide gel electrophoresis, all of the proteinase isoforms, including those of A. retroflexus seed extracts, disappeared entirely, and only one band was detected in the seed extracts of C. cyminum. Larval mortality in the larvae fed on A. retroflexus and C. cyminum seed extracts was 56 ± 2.15 and 68 ± 2.23, respectively, but mortality in control (no seed protein extract) was 12 ± 2.34 individuals. Also, the life table parameters were affected significantly by A. retroflexus and C. cyminum protein seed extracts. Therefore, A. retroflexus and C. cyminum seed protein extracts showed inhibitory effect on H. armigera digestive proteinases and adverse effects on survival and fitness of the pest; hence, they could be introduced as a successful biopesticide in the near future.

Type
Research Papers
Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of the Entomological Society of Canada

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Subject editor: Zhen Zou

References

Annapurna, S.S., Ramadoss, C.S., and Prasad, D.S. 1991. Characterization of a trypsin/chymotrypsin inhibitor from jack fruit (Artocarpus integrifolia) seeds. Journal of the Science Food and Agriculture, 54: 605618. https://doi.org/10.1002/jsfa.2740540412.CrossRefGoogle Scholar
Bown, D.P., Wilkinson, H.S., and Gatehouse, J.A. 1997. Differentially regulated inhibitor-sensitive and insensitive protease genes from the phytophagous insect pest, Helicoverpa armigera, are members of complex multigene families. Insect Biochemistry and Molecular Biology, 27: 625638.Google ScholarPubMed
Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72: 248254.CrossRefGoogle ScholarPubMed
Chi, H. 1988. Life-table analysis incorporating both sexes and variable development rates among individuals. Environmental Entomology, 17(1): 2634. http://doi.org/:10.1093/ee/17.1.26.CrossRefGoogle Scholar
Chi, H. 2016. TWOSEX-MSCHART: a computer program for the age stage two sex life table analysis [online]. Available from http://140.120.197.173/Ecology/products.htm [accessed 22 March 2020].Google Scholar
Chi, H. and Liu, H. 1985. Two new method for the study of insect population ecology. Bulletin of the Institute of Zoology, Academia Sinica, 24: 224240.Google Scholar
Chi, H. and Su, H.Y. 2006. Age stage two sex life table of Aphidius gifuensis (Hymenoptera: Braconidae) with mathematical proof of relationship between female fecundity and net reproduction rate. Environmental Entomology, 35: 1021.CrossRefGoogle Scholar
Chi, H. and Yang, T. 2003. Two-sex life table and predation rate of Propylaea japonica Thunberg (Coleoptera: Coccinellidae) fed on Myzus persicae (Sulzer) (Homoptera: Aphididae). Environmental Entomology, 32: 327e333.CrossRefGoogle Scholar
Chougule, N.P., Giri, A.P., Sainani, M.N., and Gupta, V.S. 2005. Gene expression patterns of Helicoverpa armigera gut proteases. Insect Biochemistry and Molecular Biology, 35: 355367.CrossRefGoogle ScholarPubMed
Czepak, C., Albernaz, K.C., Vivan, L.M., Oliveira, H.O., and Carvalhais, T. 2013. First reported occurrence of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in Brazil. Pesquisa Agropecuaria Tropical, 43: 110113.CrossRefGoogle Scholar
Dastranj, M., Bandani, A.R., and Mehrabadi, M. 2013. Age-specific digestion of Tenebrio molitor (Coleoptera: Tenebrionidae) and inhibition of proteolytic and amylolytic activity by plant proteinaceous seed extracts. Journal of Asia-Pacific Entomology, 16: 309315.CrossRefGoogle Scholar
Dunse, K.M., Kaas, Q., Guarino, R.F., Barton, P.A., Craik, D.J., and Anderson, M.A. 2010a. Molecular basis for the resistance of an insect chymotrypsin to a potato type II proteinase inhibitor. Proceeding of the National Academy of Sciences, 107: 1501615021. http://doi.org/10.1073/pnas.1009327107.CrossRefGoogle ScholarPubMed
Dunse, K.M., Stevens, J.A., Lay, F.T., Gaspar, Y.M., Heath, R.L., and Anderson, M.A. 2010b. Coexpression of potato type I and II proteinase inhibitors gives cotton plants protection against insect damage in the field. Proceeding of the National Academy of Sciences, 107: 1501115015.CrossRefGoogle ScholarPubMed
Efron, B. and Tibshirani, R.J. 1993. An introduction to the bootstrap. Chapman and Hall, New York, New York, United States of America.CrossRefGoogle Scholar
Fitt, G.P. 1989. The ecology of Heliothis species in relation to agroecosystems. Annual Review of Entomology, 34: 1752.Google Scholar
Garcia-Olmedo, G., Salcedo, G., Sanchez-Monge, R., Gornez, L.J., and Carbonero, P. 1987. Plant proteinaceous inhibitors of proteinases and alpha-amylases. Plant Molecular Cell Biology, 4: 275284.Google Scholar
Gatehouse, L.N., Shannon, A.L., Burgess, E.P.J., and Christeller, J.T. 1997. Characterization ofmajor midgut proteinase cDNAs from Helicoverpa armigera larvae and changes in gene expression in response to four proteinase inhibitors in the diet. Insect Biochemistry Molecular Biology, 27: 929944.CrossRefGoogle Scholar
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. Photochemistry, 63: 523532.CrossRefGoogle Scholar
Godbole, S.A., Krishna, T.G., and Bhatia, C.R. 1994. Further characterisation of protease inhibitors from pigeon pea (Cajanus cajan L. millsp) seeds. Journal of the Science Food and Agriculture, 64: 331335.CrossRefGoogle Scholar
Goodman, D. 1982. Optimal life histories, optimal notation, and the value of reproductive value. The American Naturalist, 119: 803823.CrossRefGoogle Scholar
Guo, Y.Y. 1997. Progress in the researches on migration regularity of Helicoverpa armigera and relationships between the pest and its host plants. Acta Entomologica Sinica, 40: 16.Google Scholar
Hivrale, V.K., Lomate, P.R., Basaiyye, S.H., and Kalve, S. 2013. Compensatory proteolytic responses to dietary proteinase inhibitors from Albizia lebbeck seeds in the Helicoverpa armigera larvae. Arthropod-Plant Interactions, 7: 259266. https://doi.org/10.1007/s11829-012-9240-1.CrossRefGoogle Scholar
Jamal, F., Pandey, P., Singh, D., and Ahmed, W. 2015. A Kunitz-type serine protease inhibitor from Butea monosperma seed and its influence on developmental physiology of Helicoverpa armigera. Gene, 403: 2938.Google Scholar
Jha, R.K., Chi, H., and Tang, L.-C. 2012. Life table of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) with a discussion on jackknife vs. bootstrap techniques and variations on the Euler-Lotka Equation. Formosan Entomology, 32: 355375.Google Scholar
Johnston, K.A., Lee, M.J., Gatehouse, J.A., and Anstee, J.H. 1991. The partial purification and characterization of serine protease activity in midgut of larval Helicoverpa armigera. Insect Biochemistry, 21: 389397.CrossRefGoogle Scholar
Jongsma, M.A., Bakker, P.L., Peters, J., Bosch, D., and Stiekema, W.J. 1995. Adaptation of Spodoptera exigua larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition. Proceedings of National Academy of Sciences, 97: 80418045.CrossRefGoogle Scholar
Jongsma, M.A. and Bolter, C. 1997. The adaptation of insects to plant protease inhibitors. Journal of Insect Physiology, 43: 885895.CrossRefGoogle Scholar
Kuwar, S.S., Pauchet, Y., Vogel, H., and Heckel, D.G. 2015. Adaptive regulation of digestive serine proteases in the larval midgut of Helicoverpa armigera in response to a plant protease inhibitor. Insect Biochemistry and Molecular Biology, 59: 1829. https://doi.org/10.1016/j.ibmb.2015.01.016.CrossRefGoogle ScholarPubMed
Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227: 680685.CrossRefGoogle ScholarPubMed
Lammers, J.W. and Macleod, A. 2007. Report of a pest risk analysis: Helicoverpa armigera (Hübner, 1808). Available from https://secure.fera.defra.gov.uk/phiw/riskRegister/downloadExternalPra.cfm?id=3879 [accessed 22 March 2020].Google Scholar
Lawrence, P.K. and Koundal, K.R. 2002. Plant protease inhibitors in control of phytophagous insects. Electronic Journal of Biotechnology, 5: 93109. https://doi.org/10.2225/vol5-issue1-fulltext-3.Google Scholar
Liu, Y., Sui, Y.P., Wang, J.X., and Zhao, X.F. 2009. Characterization of the trypsin-like protease (Ha-TLP2) constitutively expressed in the integument of the cotton bollworm, Helicoverpa armigera. Archives of Insect Biochemistry and Physiology, 72: 7487. https://doi.org/10.1002/arch.20324.CrossRefGoogle ScholarPubMed
Lomate, P.R. and Hivrale, V.K. 2013. Effect of Bacillus thuringiensis (Bt) Cry1Ac toxin and protease inhibitor on growth and development of Helicoverpa armigera (Hübner). Pesticide Biochemistry and Physiology, 105: 7783.CrossRefGoogle Scholar
Melo, F.R., Sales, M.P., Silva, L.S., Franco, O.L., Bloch, J. C., and Ary, M.B. 1999. α-amylase inhibitors from cowpea seeds. Protein Peptide Letter, 6: 387392.Google Scholar
Mittal, A., Kansal, R., Kalia, V., Tripathi, M., and Gupta, V. 2014. A kidney bean trypsin inhibitor with an insecticidal potential against Helicoverpa armigera and Spodoptera litura. Acta Physiologiae Plantarum, 36: 525539.CrossRefGoogle Scholar
Moral Garcia, F.J. 2006. Analysis of the spatiotemporal distribution of Helicoverpa armigera (Hübner) in a tomato field using a stochastic approach. Biosystems Engineering, 93: 253259.CrossRefGoogle Scholar
Murdock, L.L. and Shade, R.E. 2002. Lectins and protease inhibitors as plant defenses against insects. Journal of Agricultural and Food Chemistry, 50: 66056611. https://doi.org/10.1021/jf020192c.CrossRefGoogle ScholarPubMed
Naseri, B., Fathipour, Y., Moharramipour, S., Hosseininaveh, V., and Gatehouse, A.M.R. 2010. Digestive proteolytic and amylolytic activities of Helicoverpa armigera in response to feeding on different soybean cultivars. Pest Management Science, 66: 13161323. https://doi.org/10.1002/ps.2017.CrossRefGoogle ScholarPubMed
Özgür, E., Yücel, M., and Öktem, H.A. 2009. Identification and characterization of hydrolytic enzymes from the midgut of the cotton bollworm, Helicoverpa armigera Hübner (Lepidoptera: Noctuidae). Turkish Journal of Agriculture and Forestry, 33: 285294.Google Scholar
Parde, V.D., Sharma, H.C., and Kachole, M.S. 2010. In vivo inhibition of Helicoverpa armigera gut pro-proteinase activation by non-host plant protease inhibitors. Journal of Insect Physiology, 56: 13151324. https://doi.org/10.1016/j.jinsphys.2010.04.003.CrossRefGoogle ScholarPubMed
Patankar, A.G., Giri, A.P., Harsulkar, A.M., Sainani, M.N., Deshpande, V.V., Ranjekar, P.K., and Gupta, V.S. 2001. Complexity in specificities and expression of Helicoverpa armigera gut proteases explains polyphagous nature of the insect pest. Insect Biochemistry Molecular Biology, 31: 453464.CrossRefGoogle ScholarPubMed
Pogue, M.G. 2004. A new synonym of Helicoverpa zea (Boddie) and differentiation of adult males of H. zea and H. armigera (Hübner) (Lepidoptera: Noctuidae: Heliothinae). Annals of the Entomological Society of America, 97: 12221226.CrossRefGoogle Scholar
Polat-Akköprü, E., Atlihan, R., Okut, H., and Chi, H. 2015. Demographic assessment of plant cultivar resistance to insect pests: a case study of the dusky-veined walnut aphid (Hemiptera: Callaphididae) on five walnut cultivars. Journal of Economic Entomology, 108: 378387. https://doi.org/10.1093/jee/tov011.CrossRefGoogle Scholar
Rahmani, S. and Bandani, A.R. 2013. Sublethal concentrations of thiamethoxam adversely affect life table parameters of the aphid predator, Hippodamia variegata (Goeze) (Coleoptera: Coccinellidae). Crop Protection, 54: 168175. https://doi.org/10.1016/j.cropro.2013.08.002.CrossRefGoogle Scholar
Ramos, R., Ramírez, F., Sanpera, C., Jover, L., and Ruiz, X. 2009. Feeding ecology of yellow-legged gulls Larus michahellis in the western Mediterranean: a comparative assessment using conventional and isotopic methods, Marine Ecology Progress Series, 377: 289297. http://doi.org/10.3354/meps07792.CrossRefGoogle Scholar
Ryan, C.A. 1990. Protease inhibitors in plants: genes for improving defenses against insects and pathogens, Annual Review Phytopathology, 28: 425449. https://doi.org/10.1016/bs.abr.2017.11.004.CrossRefGoogle Scholar
Saadati, F. and 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: article 72, 112. https://doi.org/10.1673/031.011.7201.CrossRefGoogle ScholarPubMed
SAS Institute. 2003. SAS/STAT, Release 9.1. SAS Institute, Cary, North Carolina, United States of America.Google Scholar
Shorey, H.H. and Hale, R.L. 1965. Mass rearing of the larvae of nine noctuid species on a simple artificial medium. Journal of Economic Entomology, 58: 522524.CrossRefGoogle Scholar
Siow, H.-L. and Gan, C.Y. 2014. Functional protein from cumin seed (Cuminum cyminum): optimization and characterization studies. Food Hydrocolloid, 41: 178187. https://doi.org/10.1016/j.foodhyd.2014.04.017.CrossRefGoogle Scholar
Siow, H.-L. and Gan, C.Y. 2016. Optimization study in extracting anti-oxidative and α-amylase inhibitor peptides from cumin seeds (Cuminum cyminum). Journal of Food Biochemistry, 107: 1501115015. https://doi.org/10.1111/jfbc.12280.Google Scholar
Srinivasan, A., Giri, A., and Gupta, V. 2006. Structural and functional diversities in lepidopteran serine proteases. Cellular and Molecular Biology Letters, 11: 132154.CrossRefGoogle ScholarPubMed
Stevens, J.A., Dunse, K.M., Guarino, R.F., Barbeta, B.L., Evans, S.C., West, J.A., and Anderson, M.A. 2013. The impact of ingested potato type II inhibitors on the production of the major serine proteases in the gut of Helicoverpa armigera. Insect Biochemistry and Molecular Biology, 43: 197208. http://doi.org/10.1016/j.ibmb.2012.11.006.CrossRefGoogle ScholarPubMed
Tamhane, V.A., Chougule, N.P., Giri, A.P., Dixit, A.R., Sainani, M.N., and Gupta, V.S. 2005. In vivo and in vitro effect of Capsicum annum proteinase inhibitors on Helicoverpa armigera gut proteinases. Biochimica et Biophysica Acta; 1722: 156167. http://doi.org/10.1016/j.bbagen.2004.12.017.CrossRefGoogle ScholarPubMed
Telang, M., Srinivasan, A., Patankar, A., Harsulkar, A., Joshi, V., Damle, A., et al. 2003. Bitter gourd proteinase inhibitors: potential growth inhibitors of Helicoverpa armigera and Spodoptera litura. Phytochemistry, 63: 643652.CrossRefGoogle ScholarPubMed
Terra, W.R. and Ferreira, C. 1994. Insect digestive enzymes: properties, compartmentalization and function. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 109: 162.CrossRefGoogle Scholar
Valdes-Rodriguez, S., Blanco-Labra, A., Gutierrez-Benicio, G., Boradenenko, A., Herrera-Estrella, A., and Simpson, J. 1999. Cloning and characterization of a trypsin inhibitor cDNA from amaranth (Amaranthus hypochondriacus) seeds. Plant Molecular Biology, 41: 1523.Google ScholarPubMed
Valdes-Rodriguez, S., Segura-Nieto, M., Chagolla-Lopez, A., Vargas-Cortina, A., Martinez-Callardo, N., and Blanco-Labra, A. 1993. Purification, characterization, and complete amino acid sequence of a trypsin inhibitor from amaranth (Amaranthus hypochondriacus) seeds. Plant Physiology, 103: 14071412.CrossRefGoogle ScholarPubMed
Walker, A.J., Ford, L., Majerus, M.E.N., Geoghegan, I.E., Birch, N., Gatehouse, J.A., and Gatehouse, A.M.R. 1998. Characterisation of the mid-gut digestive proteinase activity of the two-spot ladybird (Adalia bipunctata L.) and its sensitivity to proteinase inhibitors. Insect Biochemistry and Molecular Biology, 28: 173180.CrossRefGoogle Scholar
Zalucki, M.P., Daghlish, G., Firempong, S., and Twine, P. 1986. The biology and ecology of Helicoverpa armigera (Hübner) and H. punctigera Wallengren (Lepidoptera: Noctuidae) in Australia: what do we know? Australian Journal of Zoology, 34: 779814.CrossRefGoogle Scholar
Zhao, X.-F., Wang, J.-X., Xu, X.-L., Schmid, R., and Wieczorek, H. 2002. Molecular cloning and characterization of the cathepsin B-like proteinase from the cotton boll worm, Helicoverpa armigera. Insect Molecular Biology, 11: 567575.CrossRefGoogle ScholarPubMed
Zhu, Y.C., Abel, C.A., and Chen, M.S. 2007. Interaction of Cry1Ac toxin (Bacillus thuringiensis) and proteinase inhibitors on the growth, development, and midgut proteinase activities of the bollworm, Helicoverpa zea. Pesticide Biochemistry Physiology, 87: 3946. https://pubag.nal.usda.gov/download/28045/PDF.CrossRefGoogle Scholar