PLANT PROTEASE INHIBITORS: STRATEGY FOR PEST CONTROL IN CROPS

  • R.S.DHANDE1 N.J.CHIKHALE2

Abstract

Proteinase inhibitors (PIs) are naturally occurring proteins in living organisms and are able to inhibit & control the activity of proteases. PIs are a diverse group of proteins that share a common biochemical activity. The role of plant proteinase inhibitors was investigated by Mickel and Standish in 1947 when they observed the insects larvae were unable to develop normally on soybean products. Subsequently, the soybean trypsin inhibitors were found to be lethal to the flour beetle larvae, Tribolium confusum (Lipke et. al., 1954). Now there are diverse examples of protease inhibitors active against many insect species both in vitro (Pannetier et. al., 1997; Koiwa et. al., 1998) and in vivo (Urwin et. al., 1997; Vain et. al., 1998) bioassays.

Author Biography

R.S.DHANDE1 N.J.CHIKHALE2

R.S.DHANDE1 & N.J.CHIKHALE2

1DEPARTMENT OF BOTANY, SHRI SHIVAJI COLLEGE, AKOT. DIST. AKOLA (M.S.) INDIA.

2SHRI SHIVAJI AGRICULTURE COLLEGE,

AMRAVATI (M.S.) INDIA.

Corresponding author’s e-mail:  ravi_dhande2005@yahoo.co.in

References

Abe, F. (1988). The thermochemical study of forest biomass. Forest Prod. Chem., 45: 1-95.
Abe, K., & Arai, S. (1985). Purification of a cysteine proteinase inhibitor from rice, Oryza sativa L. japonica. Agriculture Biology and Chemistry 49, 3349-3350.
Abe, K., Emori, Y., Kondo, H., Suzuki, K., & Arai, S. (1987). Molecular cloning of a cysteine proteinase inhibitor of rice (oryzacystatin). Homology with animal cystatins and transient expression in the ripening process of rice seeds. Journal of Biological Chemistry 262, No. 35, 16793-16797.
Abe, K., Kondo, H., & Arai, S. (1987). Purification and characterization of a rice cysteine proteinase inhibitor. Agricultural and Biological Chemistry 51, No.10, 2763-2768, ISSN 0002-1369.
Abe, M., Abe, K., Kuroda, M., & Arai, S. (1992). Corn kernel cysteine proteinase inhibitor as a novel cystatin superfamily member of plant origin. Molecular cloning and expression studies. European Journal of Biochemistry 209, No.3, 933–937, ISSN 0014-2956.
Amirhusin, B., Shade, R.E., Koiwa, H., Hasegawa, P.M., Bressan, R.A., & Murdock, L.L. (2007). Protease inhibitors from several clases work synergistically against Callosobruchus maculatus. J. Insect Physiol 53, 734-740.
Ana, C.S.M., Magnus, A., Ana, P.C.A.L., Marcos, A.V.S., and Scharfstein, J. (2001). Identification, characterization and localization of chagasin, a tight-binding cysteine protease inhibitor in Trypanosoma cruzi. J Cell Sci 114, 3933-3942.
Andras, P., Sumaira, A., Zulfiquar, M., Aprad, B., Jozsef, K., Bence, A., & Laszlo, G. (2002). Remarkable phylum selectivity of a Schistocerca gregaria trypsin inhibitor: The possible role of enzyme-inhibitor flexibility. Arch Biochem Biophys 398, 179-187.
Anna Azzolini, Sergio Daishi Sasaki, Ricardo José Soares Torquato, Renato Andreotti, Eliane Andreotti, and Aparecida Sadae Tanaka (2003). Rhipicephalus sanguineus trypsin inhibitors present in the tick larvae: isolation, characterization, and partial primary structure determination. Archives of Biochemistry and Biophysics, 417(2):176-82.
Annedi, S., Biabani, F., Poduch, E., Mannargudi, B., Majumder, K., Wei, L., Khayat, R., Tong, L., & Kotra, L. (2006). Engineering D-amino acid containing novel protease inhibitors using catalytic site architecture. Bioorg Med Chem Lett 14, 214-236.
Antcheva, N., Patthy, A., Athanasiadis, A., Tchorbanov, B., Zakhariev, S., & Pongor, S. (1996). Primary structure and specificity of a serine proteinase inhibitor from paprika (Capsicum annum) seeds. Biochem. Biophys. Acta 1298, No. 1, 95-101.
Applebaum S.W. (1985). Biochemistry of digestion. In: Kerkot G.A., & Gilbert L.I., Eds. Comprehensive insect physiology; Biochemistry and Pharmacology. New York, Pergamon Press, Vol. 4, 279-311.
Arai, S., Matsumoto, I., Emori, Y. and Abe, K. (2002). Plant seed cystatins and their target enzymes of endogenous and exogenous origin. J. Agric. Food Chem., 50: 6612-6617.
Arindam, B., Suman, M., Sudeshna, M. L., & Cherukuri, R. B. (2006). A Kunitz proteinase inhibitor from Archidendron ellipticum seeds: purification, characterization and kinetic properties. Phytochem 67, 232 -241.
Atchley, W.R., Lokot, T., Wollenberg, K., Dress, A., & Ragg, H. (2001). Phylogenetic analysis of amino acid variation in the serpin proteins. Mol Biol Evol 18, 1502-1511.
Atkinson, A.H., Health, R.L., Simpson, R.J., Clarke, A.E., & Anderson, M.A. (1993). Proteinase inhibitors in Nicotiana alata stigmas are derived from a precursor protein which is processed into five homologous inhibitors. Plant Cell 5, 203-213.
Barrett, A.L., & Salve san, G. (1986). Proteinase inhibitors. Academic press. New York.
Barrett, A.J. (1987). The cystatins, a new class of peptidase inhibitors. Trend Biochem. Sci 12, 193-196.
Barta, E., Pintar, A., & Pongor, S. (2002). Repeats with variations: accelerated evolution of the Pin2 family of proteinase inhibitors. Trends Genet 18, 600-603.
Batista, I.F.C., Oliva, M.L.V., Araujo, M.S., Sampaio, U.M., Richardson, M., Fritz, H., & Sampaio, C.A.M. (1996). Primary structure of a kunitz-type trypsin inhibitor from Enterolobium contortisiliquum seeds. Phytochemistry 41, No.4, 1017-1022, ISSN 0031-9422.
Baumgartner, B., & Chrispeels, M.J. (1976). Plant Physiol 58, 1-6.
Beuning, L.L., Spriggs, T.W., & Christeller, J.T. (1994). Evolution of the proteinase inhibitor I family and apparent lack of hypervariability in the proteinase contact loop. J Mol Evol 39, 644-654.
Bhattacharyya, A., Rai, S., & Babu, C. R. (2007). A trypsin and chymotrypsin inhibitor from Caesalpinia bonduc seeds: Isolation, partial characterization and insecticidal properties. Plant Physiology and Biochemistry 45, No.3-4, 169-177, ISSN 0981-9428.
Bhattacharyya, A., Cherukuri, R., & Babu, C. (2009). Purification and biochemical characterization of a serine proteinase inhibitor from Derris trifoliata Lour. seeds: Insight into structural and antimalarial features. Phytochemistry 70, No.6, 703-712, ISSN 1873-3700.
BjoErck, L., Grubb, A., & Kjellen, L. (1990). Cystatin C, a human CPI, the purified inhibitors have also been used to produce proteinase inhibitor, blocks replication of Herpes simplex virus, J Virol 64, 941-943.
Blankenvoorde, M.F., van't Hof, W., Walgreen-Weterings, E., van Steenbergen, T.J., Brand, H.S., Veerman, E.C. and Nieuw Amerongen, A.V. (1998). Cystatin and cystatin-derived peptides have antibacterial activity against the pathogen Porphyromonas gingivalis. Biol Chem., 379: 1371–1375.
Bode, W., & Huber, R. (1992). Natural protein proteinase inhibitors and their interaction with proteinases. Eur. J. Biochem 204, 433-451.
Bode, W., & Huber, R. (2000). Structural basis of the endoproteinase protein inhibitor interaction. Biochem Biophys Acta 1477, 241-252.
Bolter, C. J. (1993). Methyl jasmonate induces papain inhibitor(s) in tomato leaves. Plant Physiology 103, No.4, 1347–1353, ISSN 1532-2548.
Bosterling, B., & Quast, U. (1981). Soybean trypsin inhibitor (Kunitz) is double headed. Kinetics of the interaction of alpha-chymotrypsin with each side. Biochimica et Biophysica Acta 657, No.1, 58-72, ISSN 0006-3002.
Brito, L., Lopes, A.R., Parra, J.R.P., Terra, W.R., Silva-Filho, M.C. (2001). Adaptation of tobacco budworm Heliothis virescens to proteinase inhibitors may be mediated by synthesis of new proteinases. Comp. Biochem. Physiol 128B, 365-375.
Broadway, R.M. and 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. J Insect Physiol, 32: 827-833.
Broadway, R.M., & Duffey, S.S. (1988). The effect of plant protein quality on insect digestive physiology and the toxicity of plant proteinase inhibitors. Journal of Insect Physiology 34, 1111-1117.
Broadway, R.M. (1995). Are insects resistant to plant proteinase inhibitors? J. Insect Physiol 41, 107-116.
Brzin, J., & Kidric, M. (1995). Proteinases and their inhibitors in plants: role in normal growth and in response to various stress conditions. Biotechnology and Genetic Engineering Reviews 13, 421–467, ISSN 0264-8725.
Cai, M., Gong, Y., Kao, J.L., & Krishnamoorthi, R. (1995). Three dimensional crystal structure of Cucurbita maxima trypsin inhibitor-V determined by NMR spectroscopy. Biochemistry 34, No.15, 5201-5211.
Carlini, C., & Grossi-de-Sa M.F. (2002). Plant toxic proteins with inseticidal properties. A review on their potentialities as bioensecticides. Toxicon 40, 1515-1539.
Ceci, L.R., Spoto, N., De Virgilio, M., & Gallerani, R. (1995). FEBS Lett 364, 179-181.
Cesar, A., Silvia, V.R., Guillermo, M.H., Arturo, R.D., & Alejandro, L. (2004). A novel 8.7 kDa protease inhibitor from chan seeds (Hyptis suaveolens 1.) inhibits proteases from the larger grain borer Prostephanus truncatus (Coleoptera:Bostrichidae ). Comp Biochem Physiol Part B 138, 81 -89.
Chiaki, I. (2004). Enzyme inhibitors of marine microbial origin with pharmaceutical importance. Mar Biotechnol 6, 193-198.
Chrispeel, M.J., & Baumgartner, B. (1978). Trypsin inhibitors in Mung bean cotyledons: Purification, characteristics, subcellular localization, and metabolism. Plant Physiol 61, 617-623.
Christeller, J., & Liang, W. (2005). Plant serine protease inhibitors. Protein and Peptide Letters, 12, 439-447.
Christeller, J.T., Farley, P.C., Ramsay, R.J., Sullivan, P.A., & Laing, W.A. (1994). Midgut proteinase activities of three keratinolytic larvae, Hofmannophila pseudospretalla, Tineola bisselliella, and Anthrenocerus australis, and the effect of proteinase inhibitors on proteolysis. Arch. Insect Biochem. Physiol 25, 159-173.
Christeller, L.T., Farley, P.C., Ramsay, R.L., Sullivan, P.A., & Laing, W.A. (1998). Purification, characterization and cloning of an aspartic proteinase inhibitor from squash phloem exudate. Eur J Biochem 254, 160-167.
Chye, M.L., Sin, S.F., Xu, Z.F., & Yeung, E.C. (2006). Serine proteinase inhibitor proteins: exogenous and endogenous functions. Plant 42, 100-108.
Cleveland, T.E., Thornburg, R.W., & Ryan, C.A. (1987). Plant Mol. Biol 8, 199-207.
Collins, J.L., & Sanders, G.G. (1976). J. Food Sci 41, 168-172.
Daniel, C., Richard, D. B. I., Maureen, L., Lisa, M. H., Eva, C., Brian, F. J., Juliusz, M., Petr, K, & Michael, C. (2004). Molecular Characterization of Ancylostoma ceylanicum Kunitz-type serine protease inhibitor: Evidence for a role in hookworm-associated growth delay. Infect Immun 72, 2214-2221.
Diop, N.N., Kidric, M., Repellin, A., Gareil, M., D'arcy-Lameta, A., Pham, T.A.T., & Zuily Fodil, Y.A. (2004). Multicystatin is induced by drought-stress in cowpea (Vigna unguiculata (L.) Walp.) leaves. FEBS letters 577, No.3, 545-550, ISSN 1873-3468.
D Leo, F., Volpicella, M., Licciulli, F., Liuni, S., Gallerani, R., & Ceci, L.R. (2002). PLANT-PIs: A database for plant protease inhibitors and their genes. Nucl. Acids Res 30, 347-348.
Dohmae, N., Takio, K., Tsumuraya, Y., & Hashimoto, Y. (1995). The complete amino acid sequences of two serine proteinase inhibitors from the fruiting bodies of a basidiomycete, Pleurotus ostreatus. Arch Biochem Biophys 316, 498-506.
Domosey, C., Welham, T., Sidebottom, C., & Firmin, J.L. (1995). FEBS LETT 360, 15-20.
Downing, W.L., Mauxion, F., Fauvrque, M.O., Reviron, M.P., De-Vienne, D., Vartanian, N. & Giraudat, J. (1992). Plant J 2, 685-693.
Dubey, V.K., Pande, M., Singh, B.K., & Jagannadham, M.V. (2007). Papain-like proteases: Applications of their inhibitors. African J. Biotechnol 9, 1077-1086.
Dunaevskii, Y.E., Gladysheva, I.P., Pavlukova, E.B., Beliakova, G.A., Gladyschev, D.P., Papisova A.I., Larionova, N.I., & Belozersky, M.A. (1997). The anionic protease inhibitor BBWI –1 from buckwheat seeds. Kinetic properties and possible biological role. Physiologia plantarum 100, 483-488.
Erklund, H.V.R., Johansson, T., & Rinne, A. (1997). Rhabdovirus induced apoptosis in a fish cell line is inhibited by human endogenous acid cysteine proteinase inhibitor. J Virol 71, 5658-5662.
Faisal, M., Mac Intyre, E.A., Adam, K G., Tall, RD., Kothary, M. H., & Peyre, L.F.L. (1998). Evidence for the presence of protease inhibitors in eastern (Crassostrea virginicay and Pacific (Crassostrea gigas) oysters. Comp Biochem Physiol Part B 121, 161-168.
Fan, S., & Wu, G. (2005). Characteristics of plant proteinase inhibitors and their applications in compating phytophagous insets. Botanical Bulletin of Academia Sinica 46, No.4, 273-292, ISSN 0006-8063.
Felton, G.W., Donato, K., del Vecchio, R.J., & Duffey, S.S. (1989). Activation of plant foliar oxidases by feeding reduces nutritive quality of foliage for noctuid herbivores. J. Chem. Ecol 15, 2667-2694.
Fernandes, K.V.S., Sabelli, P.A., Barratt, D.H.P., Richardson, M., Xavier- Filho, J., & Shewry, P. R. (1993). The resistance of cowpea seeds to bruchid beetles is not related to levels of cysteine proteinase-inhibitors. Plant Molecular Biology, 23, No.1, 215–219, ISSN 1573-5028.
Frazao, C., Bento, L., Costa, L., Soares Claudio, M., Verissiorno, P., Faro, C., Pires, E., Cooper, L., & Carrondo, M. A. (1999). Crystal structure of cardosin A, a glycosylated and Arg-Gly-Asp- containing aspartic proteinase from the flowers of Cyanara cardunculus L. J Bioi Chem 274, 27694-27701.
Garcia-olmedo Salcedo, F., Sanchez Monge, G., Gomez, R.L., Royo, J., & Carbonero, P. (1987). Plant proteinaceous inhibitors of proteinases and amylases. Oxford Survey Plant Molecular and Cell Biology 4, 275-334.
Gourinath, S., Alam, N., Srinivasan, A., Betzel, C., & Singh, T.P. (2000). Structure of the bifunctional inhibitor of trypsin and alpha-amylase from ragi seeds at 2.2 A resolution. Acta Crystallographica Section D 56, No. 3, 287-293.
Graham, J.S. and Ryan, C.A. (1997). Accumulation of metallocarboxy-peptidase inhibitor in leaves of wounded potato plants. Biochemical and Biophysics Research Communication, vol. 101:1164-1170.
Greenblat, H.M., Ryan, C.A., & Lames, M.N.G. (1989). Structure of the complex Streptomyces griseus proteinase B and polypeptide chymotrypsin inhibitor-I at 2.1 A resolution. J Mol. Biol 205, 201-228.
Gregg, T. N., De, L.B.M., Sherry, D. P., & Ka, W. L. (2001): Structure, localization and potential role of a novel molluscan trypsin inhibitor in Lymnaea. EurJ Biochem 268, 1213-1221.
Havkioja, E., & Neuvonen, L. (1985). Induced long-term resistance to birch foliage against defoliators: defense or incidental. Ecology 66, 1303-1308.
Hershko, A., & Ciechanover, A. (1982). Mechanisms of intracellular protein breakdown. Annu Rev Biochem 51, 335-364.
Hollander-Czytko, H., Andersen, J.L., & Ryan, C.A. (1985). Vacuolar localization of wound-induced carboxy peptidase inhibitor in potato leaves. Plant Physiology 78, 76-79.
Hollick, J.B., & Gordon, M.P. (1993). Plant Mol. Biol 22, 561-572.
Horisberger, M., & Tacchini-Vonlanthen, M. (1983). Ultrastructural localization of Bowman-Brik inhibitor on thin sections of Glycine max (Soybean) cv. Maple arrow by the gold method. Histochemistry 77, 313-321.
Hung, C.H., Huang, C.C., Tsai, W.S., Wang, H.L., & Chen, Y.L. (2003). Purification and characterization of a trypsin inhibitor fron Brassica compestris seeds. J.Yuanpei Univ. Sci. Tech 10, 13-22.
Imada, C., Hara, S., Maeda, M., and Simidu, U. (1986a): Amino acid sequences of marinostatins C-1 and C-2 from marine Alteromonas sp. Bull Jpn Soc Sci Fish, 52: 1455–1459.
Imada, C., Maeda, M., and Taga, N. (1985c): Purification and characterization of the protease inhibitor ‘‘monastatin’’ from a marine Alteromonas sp . with reference to inhibition of the protease produced by a bacterium pathogenic to fish. Can J Microbiol, 31: 1089–1094.
Irving, J.A., Pike, R.N., Lesk, A.M., & Whisstock, J.C. (2000). Phylogeny of the serpin superfamily: implications of patterns of amino acid conservation for structure and function. Genome Res 10, 1845-1864.
Irving, J.A., Steenbakkers, P.J., Lesk, A.M., Op den Camp, H.J., Pike, R.N., & Whisstock, J.C. (2002). Serpins in prokaryotes. Mol Biol Evol 19, 1881-1890.
Jacinto, T., Fernandes, K. V. S., Machado, O. L. T., & Siqueira-Junior, C. L. (1998). Leaves of transgenic tomato plants overexpressing prosystemin accumulate high levels of cystatin. Plant Science 138, No.1, 35–42, ISSN 0168-9452.
Jackie Stevens, Kerry Dunse, Jennifer Fox, Shelley Evans and Marilyn Anderson (2012). Biotechnological Approaches for the Control of Insect Pests in Crop Plants. http://dx.doi.org/10.5772/46233.
Jackson, A.O., & Tailor, C.B. (1996): Plant-microbe interactions: Life and death at the interface. Plant Cell 8, 1651-1668.
Jongsma, M.A., & Bolter, C. (1997). The adaptation of insect to plant protease inhibitors. J Insect Physiol 43, 885-896.
Joshi, B., Sainani, M., Bastawad, E.K., Gupta, V.S., & Ranjekar, P.K. (1998): Cysteine protease inhibitor from pearl millet: A new class of antifungal protein. Biochem Biophys Res Commun 246, 382-387.
Jouanin, L., Bonade-Bottino, M., Girard, C., Morrot, G., & Giband, M. (1998). Transgenic plants for insect resistance. Plant Sci. 131, 1-11.
Keilova, H. & Tomasek, V. (1976). Isolation and properties of cathespin D inhibitor from potatoes. Collection of Czechoslovak Chemical Communication 41, 489-497.
Kervinen, J., Tobin, G.J., Costa, L., Waugh, D.S., Wlodawer, A., & Zdanov, A. (1999). Crystal structure of plant aspartic proteinase prophytepsin: Inactivation and vacuolar targeting. J Eur Mol Biol Org 18, 3947-3955.
Kirsi, M. (1974). Physiol. Plant 32, 89-93.
Koiwa, H., Bressan, R.A., & Hasegawa, P.M. (1997). Regulation of protease inhibitors and plant defense. Trends in Plant Science, 2, No.10, 379-384, ISSN 1360-1385.
Koiwa, K., Shade, R.E., Zhu-Salzman, K., Subramanian, L., Murdock, L.L., Nielsen, S.S., Bressan, R.A., & Hasegawa, P.M. (1998). Phage display selection can differentiate insecticidal activity of soybean cystatins. Plant Journal 14, 371-379.
Kos, L., & Lah, T. (1998). Cysteine proteinases and their endogenous inhibitors: Target proteins for prognosis, diagnosis and therapy in cancer. Oncol Reports 5, 1349-1361.
Kosslak, R.M., Chamberlin, M.A., Palmer, R.G., & Bowen, B.A. (1997). Plant J 11, 729-745.
Kouzuma, Y., Inanaga, H., Doi-Kawano, K., Yamasaki, N., & Kimura, M. (2000). Molecular cloning and functional expression of cDNA encoding the cysteine proteinase inhibitor with three cystatin domains from sunflower seeds. Journal of Biochemistry 128, No.2, 161-166, ISSN 0021-924X.
Krauchenco, S., Nagem, R.A.P., Silva, J.A., Marangoni, S., & Polikarpov, I. (2004). Threedimensional structure of na unusual kunitz (STI) type trypsin inhibitor from Copaifera langsdorfii. Biochimie 86, No.3, 167-172, ISSN 0300- 9084.
Lam, W., Coast, G. M., & Rayne, R. C. (1999). Isolation and characterization of two chymotrypsin from the midgut of Lacusta migratoria. Insect Biochemistry and Molecular Biology 29, No.7, 653-660, ISSN 0965-1748.
Laskowski, M. (1985). Protein inhibitors of serine proteinases: Mechanism and classification. In Friedman M (ed): Nutritional and Toxicological Significance of Enzyme inhibitors in Foods. New York: Plenum Press, 1-17.
Laskowski, M.J.R., & Kato, I. (1980). Protein inhibitors of proteinases. Annual Review of Biochemistry 49, 685-693.
Lawrence, P.L., & Koundal, K.R. (2002). Plant protease inhibitors in control of phytophagous insects. Electronic Journal of Biotechnology 5, No.1, 93-109, ISSN 0717-3458.
Lee, J.S., Brown, W.E., Grahm, J.S., Pearce, G., Fox, E.A., Dreher, T.W., Ahern, K.G., Pearson, D.G., & Ryan, C.A. (1986). Molecular characterization and phylogenic studies of a wound inducible proteinase inhibitor I gene in Lycopersicon species. PNAS 83, No.19, 7277-7281.
Leopoldo, G.G., Federico, U.C., Ana. L.S., Noelia, L.B., Faivovich, L., Lavilla, E., & Mario, R.E. (2004). A Kazal prolyl endopeptidase inhibitor isolated from the skin of Phyllomedusa sauvagii. Eur J Biochem 271, 2117-2126.
Levleva, E. V., Rudenskaya, Y. A., Dunaevsky, Y. E., & Mosolov, V. V. (1997). A 7.5-kD inhibitor of cysteine proteinases from pumpkin seeds. Biochemistry 62, No.5, 551-556, ISSN 0006-2979.
Lipke, H., Fraenkel, G.S. and Liener, I.E. (1954). Effects of soybean inhibitors on growth of Tribolium confusum. Journal of the Science of Food and Agriculture, vol. 2: 410-415.
Louise, F., David, B., Guiliano, Yelena, O., Asim, K., Debnath, Jing, L., Steven, A., Williams, Mark, L., Blaxter, & Sara, L. (2005). Characterization of a novel filarial serine protease inhibitor, Ov-SPI1, from Onchocerca volvulus, with potential multifunctional role during the parasites development. J Biol Chem 280, 49.
Macedo, M.R.L., Sa, C.M., Freire, M.G.M., & Parra, J.R.P. (2004). A Kunitz-type inhibitor of coleopteran proteases, isolated from Adenanthera pavonina L. seeds and its effect on Callosobruchus maculates. J. Agric. Food Chem 52, 2533-2540.
Macphalen, C.N., & James. M.N.G. (1987). Crystal and molecular structure of the serine proteinase inhibitor CI-2 from barley seeds. Biochem 26, 261-269.
Mahoney, W.C., Hermodson, M.A., Jones, B., & Powers, D.D. (1984). Amino acid sequence and secondary structural analysis of the corn inhibitor of trypsin and activated Hageman factor. J. Biol. Chem 259, 8412-8416.
Malek, K., & Dietrich, R.A. (1999). Defense on multiple fronts: How do plants cope with diverse enemies? Trends Plant Set 4, 215-219.
Manasi, T., Ajay, S., Aparna, P., Abhay, H., Vijay, L., Archana, D., Vasanti, D., Mohini, S., Prabhakar, R., Ashok, G., & Vidya, G. (2003). Bitter gourd protease inhibitors: Potential growth inhibitors of Helieoverpa armigera and Spodoptura litura. Phytochem 63, 643-652.
Marcela, G.A., Clelia, R.M., & La, C. (2000). A potent antifungal protein from Helianthus annuus flowers is a trypsin inhibitor. Plant Physiol Biochem 38, 881-888.
Marchetti, S., Delledonne, M., Fogher, C., Chiaba, C., Chiesa, F., & Savazzini, F. (2000). Soybean Kunitz, C-II and PI-IV inhibitor genes confer different levels of insect resistance to tobacco and potato transgenic plants. Theor. Appl. Genet 101, 519-526.
Mares, M., Meloun, B., Pavlik, M., Kostka, V., & Baudys, M. (1989). Primary structure of Cathepsin-D inhibitor from potatoes and its structural relationship to trypsin inhibitor family. FEBS Letters 251, 94-98.
Margis, R., Reis, E. M., & Villet, V. (1998). Structural and phylogenetic relationships among plant and animal cystatins. Archives of Biochemistry and Biophysics 359, No.1, 24-30, ISSN 1096-0384.
Margossian, L.J., Federman, A.D., Giovannoni, J.J., & Fischer, R.L. (1988). Ethylene regulated expression of a tomato fruit ripening gene encoding a proteinase inhibitor I with a glutamic acid residue at the reactive site. Proc. Natl. Acad. Sci 85, No. 21, 8012-8016.
Marshall, C.J. (1993). Evolutionary relationships among the serpins. Phil Trans R Soc Lond Series B Biol Sci 342, 101-119.
McGurl, B., Mukherjee, S., Kahn, M., & Ryan, C.A. (1995). Plant Mol. Biol 27, 995-1001.
Mello, M. O., Tanaka, A. S., & Silva-Filho, M. C. (2003). Molecular evolution of Bowman-Birk type proteinase inhibitors in flowering plants. Molecular Phylogenetics and Evolution 27, No.1, 103-112, ISSN 1095-9513.
Mickel, C.E., & 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.
Migliolo, L., Oliveira, S. O., Santos, E. A., Franco, O. L., & Sales, M. P. (2010). Structural and mechanistic insights into a novel non-competitive Kunitz trypsin inhibitor from Adenanthera pavonina L. seeds with double activity toward serine- and cysteineproteinases. Journal of molecular graphics & modeling 29, No.2, 148-156, ISSN 1093-3263.
Misaka, T., Kuroda, M., Iwabuchi, K., Abe, K., & Arai, S. (1996). Soyacystatin, a novel cysteine proteinase inhibitor in soybean, is distinct in protein structure and gene organization from other cystatins of animal and plant origin. European Journal of Biochemistry 240, No.3, 609-614, ISSN 0014-2956.
Mosolov, W., & Valueva, T.A. (2005). Proteinase inhibitors and their function in plant: a review. Appl. Biochem. Microbiol 41, 227-246.
Murao, S., Oda, K., & Koyama, T. (1978). New metallo proteinase inhibitor produced by Streptomyces nigrescens TK-23: S-MP1. Agric Biol Chem 42, 899-900.
Murray, C., Christeller, J.T. (1995). Purification of a trypsin inhibitor (PFTI) from pumpkin fruit phloem exudates and isolation of putative trypsin and chymotrypsin inhibitor cDNA clones. Biol. Chem. Hoppe-Seyler 376 No. 5, 281-287.
Nielsen, K.J., Heath, R.L., Anderson, M.A., & Craik, D.J. (1994). The three-dimensional solution structure by 1H NMR of a 6-kDa proteinase inhibitor isolated from the stigma of Nicotiana alata. J Mol Biol 242, 231-243.
Odani, S., Koide, T., & Ono, T. (1983). The complete amino acid sequence of barley trypsin inhibitor. J.Biol. Chem 258, 7998-8003.
Oliva, M.L.V., Souza-Pinto, J.C., Batista, I.F.C., Araujo, M.S., Silveira, V.F., Auerswald, E.A., Mentele, R., Eckerskorn, C., Sampaio, U.M., & Sampaio, C.A.M. (2000). Leucaena leucocephala serine proteinase inhibitor: prymary structure and action on blood coagulation, kinin release and paw edema. Biochimica et Biophysica Acta 1477, No.1-2, 64-74, ISSN 0006-3002.
Oliva, M.L.V., Silva, M.C.C., Sallai, R.C., Brito, M.V. and Sampaio M.U. (2010). A novel subclassification for Kunitz proteinase inhibitors from leguminous seeds. Biochimie, 92 (11): 1667–1673.
Oliveira, A.S., Xavier-Filho, J., & Sales, M.P. (2003). Cysteine proteinases and cystatins. Braz. Arch. Boil. Tecnol 46, 91-104.
Oppert, B., Morgan, T.D., Culbertson, C. & Kramer, K.J. (1993). Dietary mixtures of cysteine proteinase and serine proteinase inhibitors exhibit increased toxicity towards the red flour beetle, Tribolium castaneum. Comp. Biochem. Physiol 105C, 379-385.
Pando, S.C., Oliva, M.L.V., Sampaio, C.A.M., Di Ciero, L., Novello, J.C., & Marangoni, S. (2001). Prymary sequence determination of a Kunitz inhibitor siolated from Delonix regia seeds. Phytochemistry 57, No.5, 625-631, ISSN 0031-9422.
Pannetier, C., Giband, M., Couzi, P., Letan, V., Mazier, M., Tourneur, J., & Hau, B. (1997). Introduction of new traits into cotton through genetic engineering: insect resistance as example. Euphytica 96, 163-166.
Park, H., Yamanaka, N., Mikkonen, A., Kusakabe, L., & Kobayashi, H. (2000). Purification and characterization of aspartic proteinase from sunflower seeds. Biosci Biotech Biochem 64, 931-939.
Paulillo, L.C.M.S., Lopes, A.R., Cristofoletti, P.T., Parra, J.R.P., Terra, W.R., & Silva-Filho, M.C. (2000). Changes in midgutendopeptidases activity of Spodoptera frugiperda (Lepidoptera: Noctuidae) are responsible for adaptation to soybean proteinase inhibitors. J. Econ. Entomol 93, 892-896.
Pearce, G., Johnson, S., & Ryan, C.A. (1993). Purification and characterization from Tobacco (Nicotiana tabacum) leaves of six small, wound inducible, proeinase isoinhibitors of the potato inhibitor II family. Plant Physiol 102, 639-644.
Pearce, G., Sy, L., Russel, C., Ryan, C.A., & Hass, M. (1982). Arch. Biochem. Biophys 213, 456-462.
Pernas, M., Lopez-Solanilla, E., Sanchez-Monge, R., Salcedo, G., & Rodriguez-Palenzuela, P. (1999). Antifungal activity of a plant Cystatin. Mol Plant Microbe Interact 12, 624-627.
Pernas, M., Sanchez-Monge, R., Gómez, L., & Salcedo, G. A. (1998). Chestnut seed cystatin differentially effective against cysteine proteinases from closely related pests. Plant Molecular Biology 38, No.6, 1235–1242, ISSN 0167-4412.
Pierre, P., & Mcllman, L. (1998). Developmental regulation of invariant chain proteolysis controls MHC class II trafficking in mouse dendritic cells. Cell 93, 1135-1145.
Prakash, B., Selvaraj, S., Murthy, M.R., Sreerama, Y.N., Rao, D.R., & Gowda, L.R. (1996). Analysis of the amino acid sequences of plant Bowman-Birk inhibitors. J Mol Evol 42, 560-569.
Qi, R. F., Song, Z. W., & Chi, C. W. (2005). Structural features and molecular evolution of Bowman-Birk protease inhibitors and their potential application. Acta Biochimica et Biophysica Sinica 37, No.5, 283-292, ISSN 1745-7270.
Ramos, V.S., Freire, M.G.M., Parra, J.R.P., & Macedo, M.L.R. (2009). Regulatory effects of an inhibitor from Plathymenia foliolosa seeds on the larval development of Anagasta kuehniella (Lepidoptera). Comp. biochem. Physiol 152, 255-261.
Ramos, V.S., Silva, G.S., Freire, M.G.M., Parra, J.R.P. and Macedo, M.L.R. (2008). Purification and characterization of a trypsin inhibitor from Plathymenia foliolosa seeds. J. Agric. Food Chem., 10: 11348-11355.
Rancour, J.M., & Ryan, C.A. (1968). Isolation of a carboxypeptidase B inhibitor from potatoes. Archives of Biochemistry and Biophysics 125, 380-382.
Rawlings, N.D. & Barrett, A.J. (1990). Evolution of proteins of the cystatin superfamily. J Mol Evol 30, 60-71.
Rawlings, N.D., Tolle, D.P., & Barrett, A.J. (2004). Evolutionary families of peptidase inhibitors. Biochem J 378, 705-716.
Reeck, G.R., Kramer, K.J., Baker, J.E., Kanost, M.R., Fabrick, J.A., & Behnke, C.A. (1997). Proteinase inhibitors and resistance of transgenic plants to insect. In: Crozzi N and Koziel M, eds. Advances in insect control: the role of transgenic plants. London, Taylor and Francis, p. 157-183.
Richardson, M.J. (1991). Seed storage proteins: The enzyme inhibitors. In: Richardson, M.J, ed. Methods in Plant Biochemistry, New York, Academic Press, 259-305.
Rodriguez, E.V., Labra, A.B., Benicio, G.G., Boradenenko, A., Estrella, A.H., & Simpson, J. (1999). Plant Mol. Biol 41, 15-23.
Rohrmeier, T., Lehle, L., & Wijp, I. (1993). Plant Mol. Biol 22, 783-792.
Roston, D. (1996). Development of non-toxic protease inhibitors extracted from invertebrates for in vivo application. Int J Cardio 53, 11-37.
Ryan, C.A. (1981). In The Biochemistry of Plants (ed. Marcus, A.), Academic Press, New Yark Vol. 6, 351-370.
Ryan, C.A. (1990). Protease inhibitor in plants: Genes for improving defenses against insects and pathogens. Annual Review of Phytopathology 28, No.1, 425-449, ISSN 00664286.
Ryan, C.A., & Ball, A.K. (1962). An inhibitor of chymotrypsin from Solanum tuberosm and its behavior towards trypsin. Pro. Natl. Acad. Sci 48, 1839-44.
Sanchez-Serrano, J.J., Schmidt, R., Schell, J., & Willmitzer, L. (1986). Nucleotide sequence of proteinase inhibitor II encoding cDNA of potato (Solanum tuberosum) and its mode of expression. Mol. Gen. Genet 203, 15-20.
Sardana, R.K., Ganz, P.R., Duddani, A.K., Tackaberry, E.S., Cheng, X., & Altosaar, I. (1998). Synthesis of recombinant human cytoking GMCSF in the seeds of transgenic tobacco plants. In Cunningham, C. & Porter, A J R, eds. Recombinant proteins from plants. Production and isolation of clinically useful compounds. Totowa N J, Humama Press. p. 77-87.
Shoji, O., Kei, T., Satomi, K., Hiroshi, H., Takehiko, K., Saburo, H., Mamoru, I., & Susumu, T. (1999). The inhibitory properties and primary structure of a novel serine proteinase inhibitor from the fruiting body of the basidiomycete, Lentinus edodes. Eur J Biochem 262, 915-923.
Shulke, R.H. & Murdock, L.L. (1983). Lipoxygenase trypsin inhibitor and lectin from soybeans: effects on larval growth of Manduca sexta (Lepidoptera: Sphingidae). Environmental Entomology 12, 787-791.
Silverman, G.A., Bird. P.I., Carrell, R.W., Church, F.C., Coughlin, P.B., Gettins, P.G., Irving, J.A, Lomas, D.A, Luke, C.L., Moyer, R.W., Pemberton, P., Remold-O'Donnell, E., Salvesen, G.S., Travis, J., & Whisstock, L.C. (2001). Evolution, mechanism of inhibition, novel functions and a revised nomenclature. J Biol Chem 276, 33293-33296.
Silverman, G.A., Whisstock, J.C., Askew, D.J., Pak, S.C., Luke, C.J., Cataltepe, S., Irving, J.A., & Bird, P.I. (2004). Human clade B serpins (ov-serpins) belong to a cohort of evolutionarily dispersed intracellular proteinase inhibitor clades that protect cells from promiscuous proteolysis. Cell Mol Life Sci 61, 301-325.
Sin, S.F., & M.L. Chye. (2004). Expression of proteinase inhibitor II proteins during floral development in Solanum americanum. Planta 219, 1010-1022.
Solomon, M., Belenghi, B., Delledonne, M., Menachem, E., & Levine, A. (1999). Plant Cell, 11, 431-443.
Song, S.I., Kim, C.H., Back, S.J., & Choi, Y.D. (1991). Mol.Cells 1, 317-324.
Stephen, R.M., & Judy, A.S. (1994). Characterization of the serine protease and serine protease inhibitor from the tissue-penetrating nematode Anisakis simplex. J Biochem 269, 27650-27656.
Stotz, H.U., Kroymann, L., & Mitchell-Olds, T. (1999). Plant-insect interactions. Curl Opin Plant Bioi 2, 268-272.
Strobl, S., Muhlhahn, P., Bernstein, R., Wiltscheck, R., Maskos, K., & Wunderlich, M. (1995). Determination of the 3-dimensional structure of the bifunctional alpha-amylase/trypsin inhibitor from ragi seeds by NMR spectroscopy. Biochemistry 34, 8281-8293.
Stubbs, M.T., Laber, B., Bode, W., Huber, R., Jerala, R., & Lenarcic, B. (1990). The refined 2.4 A X-ray crystal structure of recombinant human stefm B in complex with the cysteine proteinase papain: A novel type of proteinase inhibitor interaction. EMBO J 9, 1939-1947.
Suh, Y., & Benedik, M. L. (1992). Production of active Serratia marcescens metalloprotease from Escherichia coli by a hemollysin HlyB and HlyD. J Bacteriol 174, 2261-2266.
Szyperski, T., Guntert, P., Stone, S. R., & Wuthrich, K. (1992). Nuclear magnetic resonance solution structure of hirudin. J Mol Bioi 228, 1193-1205.
Takeshi, K., Chiaki, L., Akira, H., Hiroshi, T., Katsushiro, M., Yoshihiko, L., Naoko, H., & Etsuo, W. (2003). Pseudoalteromonas sagamiensis sp. a novel marine bacterium that produces protease inhibitors. lnte J Syst Evol Microbiol 53, 1807-1811.
Tamir, S., Bell, J., Finlay, T.H., Sakal, E., Smirnoff, S., Gaur, S. and Birk, Y. (1996). Isolation, characterization and properties of a trypsin–chymotrypsin inhibitor from Amaranth seeds. J. Prot. Chem.15:219–229.
Turk, V., & Bode, W. (1991). The cystatins: protein inhibitors of cysteine proteinases. FEBS Letters 285, 213-219.
Ueda, Y., Kojima, S., Tsumoto, K., Takeda, S., Miura, K., & Kumagai, I. (1992). A protease inhibitor produced by Streptomyces lividans 66 exhibits inhibitory activities toward both subtilisin BPN' and trypsin. J Biochem 112, 204-11.
Urwin, P.E., Lilley, C.J., Mcpherson, M.J., & Atkinson, H.J. (1997). Resistance to both cyst and rootnot nematodes conferred by transgenic Arabidopsis expressing a modified plant cystatin. Plant Journal, 12, No.2, 455-461.
Vain, P., Worland, B., Clarke, M.C., Richard, G., Beavis, M., Liu, H., Kohli, A., Leech, M. Snape, J. & Christou, P. (1998). Expression of an engineered cysteine proteinase inhibitor (Oryzacystatin-I delta D86) for nematode resistance in transgenic rice plants. Theoretical and Applied Genetics 96, 266-271.
Valueva, T.A., Rcvina, T.A, Gvozdcva, E.L., Gerasimova, N.G., & Ozcrctskovskaya, O.L. (2003). Role of proteinase inhibitors in potato protection. Bioorg Khim 29, 499-504.
Valueva, T.A., Revina, T.A., & Mosolov, V.V. (1999). Reactive sites of the 21-kD protein inhibitor of serine proteinases from potato tubers. Biochemistry 64, No.9, 1074-1078, ISSN 0006-2979.
Van Gent, D., Sharp, P., Morgan, K., & Kalsheker, N. (2003). Serpins: structure, function and molecular evolution. Int J Biochem Cell Biol 35, 1536-1547.
Volpicella, M., Ceci, L.R., Cordewener, J., America, T., Gallerani, R., Bode, W. (2003). Properties of purified gut trypsin from Helicoverpa zea, adapted to proteinase inhibitors. Eur. J. Biochem 270, 10-19.
Waldron, C., Wegrich, L. M., Merlo, P.A.O., & Walsch, T.A. (1993). Characterization of a genomic sequence coding for potato multicystatin, an eight domain cysteine proteinase inhibitor. Plant Molecular Biology 23, No.4, 801–812, ISSN 0167-4412.
Williamson, V.M., & Hussey, R.S. (1996). Nematode pathogenesis and resistance in plants. Plant Cell 8, 1735-1745.
Wolfson, J.L., & Murdock, L.L. (1987). Suppression of larval Colorado beetle growth and development by digestive proteinase inhibitors. Entomologia Experimentaliset Applicata 44, 235-240.
Wu, J. & Haard, J.N. (2000). Purification and characterization of a cystatin from the leaves of methyl jasmonate treated tomato plants. Comparative Biochemistry and Physiology.Toxicology & Pharmacology 127, No.2, 209–220, ISSN 1532- 0456.
Xu, D., Duan, X., Wang, B., Hong, B., Ho, D.T., & Wu, R. (1996). Plant Physiol 110, 249-257.
Xu, Z.F., W.Q. Qi, X.Z. Ouyang, E. Yeung, & M.L. Chye. (2001). A proteinase inhibitor II of Solanum americanum is expressed in Phloem. Plant Mol. Biol 47, 727-738.
Yeh, K.W., Lin, M.I., Tuan, S.J., Chen, Y.M., Lin, C.Y., & Kao, S.S. (1997). Plant Cell Rep 16, 696-699.
How to Cite
N.J.CHIKHALE2, R.S.DHANDE1. PLANT PROTEASE INHIBITORS: STRATEGY FOR PEST CONTROL IN CROPS. LIFE SCIENCES LEAFLETS, [S.l.], v. 58, nov. 2014. ISSN 0976-1098. Available at: <http://petsd.org/ojs/index.php/lifesciencesleaflets/article/view/194>. Date accessed: 16 aug. 2017.