Skip to main content

Advertisement

SpringerLink
Log in

Serine protease inhibitors in plants: nature’s arsenal crafted for insect predators

  • Published:
Phytochemistry Reviews Aims and scope Submit manuscript

Abstract

Plant serine protease inhibitors are defense proteins crafted by nature for inhibiting serine proteases. Use of eco-friendly, sustainable and effective protein molecules which could halt or slow down metabolism of nutrients in pest would be a pragmatic approach in insect pest management of crops. The host-pest complexes that we observe in nature are evolutionary dynamic and inter-depend on other defense mechanisms and interactions of other pests or more generally speaking symbionts with the same host. Insects have co-evolved and adapted simultaneously, which makes it necessary to investigate serine protease inhibitors in non-host plants. Such novel serine protease inhibitors are versatile candidates with vast potential to overcome the host inhibitor-insensitive proteases. In a nutshell exploring and crafting plant serine proteinase inhibitors (PIs) for controlling pests effectively must go on. Non-host PI seems to be a better choice for coevolved insensitive proteases. Transgenic plants expressing wound inducible chimaeric PIs may be an outstanding approach to check wide spectrum of gut proteinases and overcome the phenomenon of resistance development. Thus, this article focuses on an entire array of plant serine protease inhibitors that have been explored in the past decade, their mode of action and biological implications as well as applications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adachi T, Izumi H, Yamada T et al (1993) Gene structure and expression of rice seed allergenic proteins belonging to the alpha-amylase/trypsin inhibitor family. Plant Mol Biol 21:239–248

    Article  PubMed  CAS  Google Scholar 

  • Aguirre C, Valdés-Rodríguez S, Mendoza-Hernández G et al (2004) A novel 8.7 kDa protease inhibitor from chan seeds (Hyptis suaveolens L.) inhibits proteases from the larger grain borer Prostephanus truncatus (Coleoptera: Bostrichidae). Comp Biochem Physiol B Biochem 138:81–89

    Article  CAS  Google Scholar 

  • Alfonso-Rubi J, Ortego F, Sanchez-Monge R et al (1997) Wheat and barley inhibitors active towards α-amylase and trypsin-like activities from Spodoptera frugiperda. J Chem Ecol 23:1729–1741

    Article  Google Scholar 

  • Alfonso-Rubí J, Ortego F, Castañera P et al (2003) Transgenic expression of trypsin inhibitor CMe from barley in indica and japonica rice, confers resistance to the rice weevil Sitophilus oryzae. Transgenic Res 12:23–31

    Article  PubMed  Google Scholar 

  • Al-Khunaizi M, Luke CJ, Askew YS et al (2002) The serpin SQN-5 is a dual mechanistic-class inhibitor of serine and cysteine proteinases. Biochemistry 41:3189–3199

    Article  PubMed  CAS  Google Scholar 

  • Altpeter F, Díaz I, McAuslane H et al (1999) Increased insect resistance in transgenic wheat stably expressing trypsin inhibitor CMe. Mol Breed 5:53–63

    Article  CAS  Google Scholar 

  • Annapurna SS, Ramadoss CS, Prasad DS (2006) Characterization of a trypsin/chymotrypsin inhibitor from jack fruit (Artocarpus integrifolia) seeds. J Sci Food Agric 54:605–618

    Article  Google Scholar 

  • Antcheva N, Patthy A, Athanasiadis A et al (1996) Primary structure and specificity of a serine proteinase inhibitor from paprika (Capsicum annuum) seeds. Biochim Biophys Acta 1298:95–101

    Article  PubMed  CAS  Google Scholar 

  • Antcheva N, Pintar A, Patthy A et al (2001) Proteins of circularly permuted sequence present within the same organism: the major serine proteinase inhibitor from Capsicum annuum seeds. Protein Sci 10:2280–2290

    Article  PubMed  CAS  Google Scholar 

  • Applebaum SW (1985) Biochemistry of digestion. In: Kerkot GA, Gilbert LI (eds) Comprehensive insect physiology; biochemistry and pharmacology, vol 4. Pergamon Press, New York, pp 279–311

    Google Scholar 

  • Araújo CL, Bezerra IWL, Oliveira AS et al (2005) In vivo bioinsecticidal activity toward Ceratitis capitata (fruit fly) and Callosobruchus maculatus (cowpea weevil) and in vitro bioinsecticidal activity toward different orders of insect pests of a trypsin inhibitor purified from tamarind tree (Tamarindus indica) seeds. J Agric Food Chem 53:4381–4387

    Article  PubMed  CAS  Google Scholar 

  • Argandona VH, Chaman M, Cardemil L et al (2001) Ethylene production and peroxidase activity in aphid infested barley. J Chem Ecol 27:53–68

    Article  PubMed  CAS  Google Scholar 

  • Atiwetin P, Harada S, Kamei K (2006) Serine protease inhibitor from Wax Gourd (Benincasa hispida[Thumb] seeds). Biosci Biotech Biochem 70(3):743–745

    Article  CAS  Google Scholar 

  • Atkinson AH, Heath RL, Simpson RJ et al (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

    PubMed  CAS  Google Scholar 

  • Babiychuk E, Fuangthong M, Van Montagu M et al (1997) Efficient gene tagging in Arabidopsis thaliana using a gene trap approach. Proc Natl Acad Sci USA 94:12722–12727

    Article  PubMed  CAS  Google Scholar 

  • Babu SR, Subrahmanyam B (2010) Bio-potency of serine proteinase inhibitors from Acacia senegal seeds on digestive proteinases, larval growth and development of Helicoverpa armigera (Hübner). Pesticide Biochem Physiol 98:349–358

    Article  CAS  Google Scholar 

  • Baker JE, Woo SM, Mullen MA (1984) Distribution of proteinases and carbohydrates in the midgut of the larvae of the sweet potato weevil Cyclas formicarius and response of proteinase to inhibitors from sweet potato. Entomol Exp Appl 36:97–105

    Article  CAS  Google Scholar 

  • Balestrazzi A, Confalonieri M, Odoardi M et al (2004) A trypsin inhibitor cDNA from a novel source, snail medic (Medicago scutellata L.): cloning and functional expression in response to wounding, herbivore, jasmonic and salicylic acid. Plant Sci 167:337–346

    Article  CAS  Google Scholar 

  • Barta E, Pintar A, Pongor S (2002) Repeats with variations: accelerated evolution of the Pin2 family of proteinase inhibitors. Trends Genet 18:600–603

    Article  PubMed  CAS  Google Scholar 

  • Batista IFC, Olivia MLV, Araújo MS et al (1996) Primary structure of a Kunitz-type trypsin inhibitor from Enterolobium contortisiliquum seeds. Action on blood clotting contact phase enzymes. Phytochem 41:1017–1022

    Article  CAS  Google Scholar 

  • Bayes A, Comellas-Bigler M, Vega MR et al (2005) Structural basis of the resistance of an insect carboxypeptidase to plant protease inhibitors. Proc Natl Acad Sci USA 102:16602–16607

    Article  PubMed  CAS  Google Scholar 

  • Belozersky MA, Dunaevsky YE, Musolyamov AX et al (1995) Complete amino acid sequence of the protease inhibitor from buckwheat seeds. FEBS Lett 371:264–266

    Article  PubMed  CAS  Google Scholar 

  • Bent AF (1996) Plant disease resistance genes: function meets structure. Plant Cell 8:1757–1771

    PubMed  CAS  Google Scholar 

  • Bergey DR, Orozco-Cardenas M, De Moura DS et al (1999) A wound- and systemin-inducible polygalacturonase in tomato leaves. Proc Natl Acad Sci USA 96:1756–1760

    Article  PubMed  CAS  Google Scholar 

  • Bhat AV, Pattabiraman PN (1989) Protease inhibitors from Jackfruit seeds. J Biosci 14:351–365

    Article  CAS  Google Scholar 

  • Bhattacharjee C, Manjunath NH, Prasad DT (2009) Purification of trypsin inhibitor from Cocculus hirsutus and identification of its biological activity. J Crop Sci Biotechnol 12:253–260

    Article  Google Scholar 

  • Bhattacharyya A, Rai S, Babu CR (2007) A trypsin and chymotrypsin inhibitor from Caesalpinia bonduc seeds: isolation, partial characterization and insecticidal properties. Plant Physiol Biochem 45:169–177

    Article  PubMed  CAS  Google Scholar 

  • Bhavani P, Bhattacherjee C, Prasad DT (2007) Bioevaluation of Subabul (Leucaena leucocephala) protease inhibitors on Helicoverpa armigera. Arthropod-Plant Inter 1:255–261

    Article  Google Scholar 

  • Bijina B, Chellapan S, Krishna JG et al (2011) Protease inhibitor from Moringa oleifera with potential use as therapeutic drug and as seafood preservative. Saudi J Biol Sci 18:273–281

    Article  CAS  Google Scholar 

  • Birk Y (1985) The Bowman-Birk inhibitor. Trypsin and chymotrypsin inhibitor from soybeans. Int J Pept Protein Res 25:113–131

    Google Scholar 

  • Birkenmeier GF, Ryan CA (1998) Wound signaling in tomato plants: evidence that ABA is not a primary signal for defense gene activation. Plant Physiol 117:687–693

    Article  PubMed  CAS  Google Scholar 

  • Blancolabra A, Martinez-Gallardo NA, Sandoval-Cardoso L (1996) Purification and characterization of a digestive cathepsin D proteinase isolated from Tribolium castaneum larvae (Herbst). Insect Biochem Mol Biol 26:95–100

    Article  CAS  Google Scholar 

  • Bode W, Papamokos E, Musil D et al (1986) Refined 1.2 Å crystal structure of the complex formed between subtilisin Carlsberg and the inhibitor eglin c. Molecular structure of eglin and its detailed interaction with subtilisin. EMBO J 5:813–818

    PubMed  CAS  Google Scholar 

  • Boulter D (1993) Insect pest control by copying nature using genetically engineered crops. Biochemistry 34:1453–1466

    CAS  Google Scholar 

  • Bown DP, Own DP, Wilkinson HS et al (1997) Differentially regulated inhibitor sensitive and insensitive protease genes from the phytophagous insect pest, Helicoverpa armigera, are members of complex multigene families. Insect Biochem Mol Biol 27:625–638

    Article  PubMed  CAS  Google Scholar 

  • Bradshaw HD Jr, Hollick JB, Parsons TJ et al (1990) Systemically wound-responsive genes in poplar trees encode proteins similar to sweet potato sporamins and legume Kunitz trypsin inhibitors. Plant Mol Biol 14:51–59

    Article  PubMed  CAS  Google Scholar 

  • Broadway RM, Duffey SS (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

    Article  CAS  Google Scholar 

  • Brovosky D (1986) Proteolytic enzymes and blood digestion in the mosquito Culex nigripalpus. Arch Insect Biochem Physiol 3:147–160

    Article  Google Scholar 

  • Cai M, Gong Y, Kao JL et al (1995) Three-dimensional solution structure of Cucurbita maxima trypsin inhibitor-V determined by NMR spectroscopy. Biochemistry 34(15):5201–5211

    Article  PubMed  CAS  Google Scholar 

  • Caillaud CM, Niemeyer HM (1996) Possible involvement of phloem sealing system in the acceptance of a plant as host by an aphid. Experientia 52:927–931

    Article  CAS  Google Scholar 

  • Ceci LR, Spoto N, de Virgilio M et al (1995) The gene coding for the mustard trypsin inhibitor-2 is discontinuous and wound-inducible. FEBS Lett 364:179–181

    Article  PubMed  CAS  Google Scholar 

  • Ceciliani F (1997) A trypsin inhibitor from snail medic seeds active against pest proteases. Phytochemistry 44:393–398

    Article  PubMed  CAS  Google Scholar 

  • Ceciliani F, Bortolloti F, Menegatti E et al (1994) Purification, inhibitory properties, amino acid sequence and identification of the reactive site of a new serine proteinase inhibitor from oil-rape (Brassica napus) seed. FEBS Lett 342:221–224

    Article  PubMed  CAS  Google Scholar 

  • Chang C-R, Tsen CC (1981) Characterization and heat stability of trypsin inhibitors from rye, triticale and wheat samples. Cereal Chem J 58:211–213

    CAS  Google Scholar 

  • Chaudhary NS, Shee C, Islam A et al (2008) Purification and characterization of a trypsin inhibitor from Putranjiva roxburghii seeds. Phytochemistry 69:2120–2126

    Article  PubMed  CAS  Google Scholar 

  • Chen P, Rose J, Love R (1992) Reactive sites of an anticarcinogenic Bowman-Birk proteinase inhibitor are similar to other trypsin inhibitors. J Biol Chem 267:1990–1994

    Google Scholar 

  • Chen ZY, Brown RL, Lax AR et al (1999) Inhibition of Plant-Pathogenic Fungi by a Corn Trypsin inhibitor overexpressed in Escherichia coli. Appl Environ Microbiol 65:1320–1324

    PubMed  CAS  Google Scholar 

  • Cheung AHK, Ng TB (2007) Isolation and characterization of a trypsin-chymotrypsin inhibitor from the seeds of green lentil (Lens culinaris). Protein Peptide Lett 14:859–864

    Article  CAS  Google Scholar 

  • Choi D, Park JA, Seo YS et al (2000) Structure and stress-related expression of two cDNAs encoding proteinase inhibitor II of Nicotiana glutinosa. Biochim Biophys Acta 1492(1):211–215

    Article  PubMed  CAS  Google Scholar 

  • Christeller J, Liang W (2005) Plant serine protease inhibitors. Protein Peptide Lett 12:439–447

    Article  CAS  Google Scholar 

  • Christopher ME, Miranda M, Major IT et al (2004) Gene expression profiling of systemically wound-induced defenses in hybrid poplar. Planta 219:936–947

    Article  PubMed  CAS  Google Scholar 

  • Chye ML, Sin SF, Xu ZF et al (2006) Serine proteinase inhibitor proteins: exogenous and endogenous functions. Plant 42:100–108

    CAS  Google Scholar 

  • Clementea A, Domoney C (2006) Biological significance of polymorphism in legume protease inhibitors from the Bowman-Birk family. Curr Protein Pept Sci 7(3):201–216

    Article  PubMed  Google Scholar 

  • Cleveland TE, Thornburg RW, Ryan CA (1987) Molecular characterization of a wound inducible inhibitor I gene from potato and the processing of its messenger RNA and protein. Plant Mol Biol 8:199–207

    Article  CAS  Google Scholar 

  • de Leo F, Bonadé-Bottino MA, Ceci LR et al (1998) Opposite effects on Spodoptera littoralis larvae of high expression level of a trypsin protease inhibitor in transgenic plants. Plant Physiol 118:997–1004

    Article  PubMed  Google Scholar 

  • Dennis MS, Herzka A, Lazrus RA (1994) Potent and selective Kunitz domain inhibitors of plasma kallikrein designed by phage display. J Biol Chem 270:25411–25417

    Google Scholar 

  • Devaraj VR, Manjunatha NH (1999) Purification and characterization of a protease inhibitor from field bean, Dolichos lablab perpureus L. J Protein Chem 18:47–54

    Article  PubMed  CAS  Google Scholar 

  • Dicke M, Beek TA, Posthumus MA et al (1990) Isolation and identification of volatile kairomone that affects acarine predator prey interactions. J Chem Ecol 16:381–396

    Article  CAS  Google Scholar 

  • Dunse KM, Kaas Q, Guarino RF et al (2010a) Molecular basis for the resistance of an insect chymotrypsin to a potato type II proteinase inhibitor. Proc Natl Acad Sci USA 107:15016–15021

    Article  PubMed  CAS  Google Scholar 

  • Dunse KM, Stevens JA, Laya FT et al (2010b) Coexpression of potato type I and II protease inhibitors give cotton plants protection against insect damage in the field. Proc Natl Acad Sci USA 107:15011–15015

    Article  PubMed  CAS  Google Scholar 

  • Ee KY, Zhao J, Rehman AU et al (2009) Purification and characterization of a Kunitz-type trypsin inhibitor from Acacia victoriae Bentham seeds. J Agric Food Chem 57:7022–7029

    Article  PubMed  CAS  Google Scholar 

  • Ee KY, Zhao J, Rehman A et al (2011) Glycosylation, amino acid analysis and kinetic properties of a major Kunitz-type trypsin inhibitor from Acacia victoriae Bentham seeds. Food Chem 129:1224–1227

    Article  CAS  Google Scholar 

  • Eguchi M, Iwamoto A, Yamaguhi K (1982) Interaction of proteases from the midgut lumen, epithelial and peritrophic membrane of the silkworm Bombyx mori L. Comp Biochem Physiol A 72:359–363

    Article  Google Scholar 

  • Epple P, Aprl K, Bohlmann H (1995) An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis related protein. Plant Physiol 109:813–820

    Article  PubMed  CAS  Google Scholar 

  • Evandro FF, Abdallah AH, Jack HW et al (2011) Isolation of a new trypsin inhibitor from the faba bean (Vicia faba cv. Giza 843) with potential medicinal applications. Protein Peptide Lett 18:64–72

    Article  Google Scholar 

  • Fang EF, Wong JH, Fern Bah CS et al (2010) Bauhinia variegata var. variegata trypsin inhibitor: from isolation to potential medicinal applications. Biochem Biophys Res Commun 396:806–811

    Article  PubMed  CAS  Google Scholar 

  • Felizmenio QME, Daly NL, Craik DJ (2001) Circular proteins in plants: solution structure of a novel macrocyclic trypsin inhibitor from Momordica cochinchinensis. J Biol Chem 276:22875–22882

    Article  Google Scholar 

  • Franco OL, Dos Santos RC, Batista JAN et al (2003) Effects of black-eyed pea trypsin/chymotrypsin inhibitor on proteolytic activity and on development of Anthonomus grandis. Phytochemistry 63:343–349

    Article  PubMed  CAS  Google Scholar 

  • Garcia VA, Freire MDGM, Novello JC et al (2004) Trypsin inhibitor from Poecilanthe parviflora seeds: purification, characterization, and activity against pest proteases. Protein J 23:343–350

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Olmedo SF, Sanchez MG, Gomez RL et al (1987) Plant proteinaceous inhibitors of proteinases and alpha-amylases. Oxford Survey Plant Mol Cell Biol 4:275–334

    CAS  Google Scholar 

  • Gautier MF, Alary R, Joudrier P (1990) Cloning and characterization of a cDNA encoding the wheat (Triticum durum Desf.) CM16 protein. Plant Mol Biol 14:313–322

    Article  PubMed  CAS  Google Scholar 

  • Giri AP, Harsulkar AM, Deshpande VV et al (1998) Chickpea defensive protease inhibitors can be inactivated by podborer gut proteases. Plant Physiol 116:393–401

    Article  CAS  Google Scholar 

  • Giri AP, Harsulkar AM, Ku MS et al (2003) Identification of potent inhibitors of Helicoverpa armigera gut proteinases from winged bean seeds. Phytochemistry 63(5):523–532

    Article  PubMed  CAS  Google Scholar 

  • Godbole SA, Krishna TG, Bhatia CR (1994) Further characterisation of protease inhibitors from pigeon pea (cajanus cajan (l) millsp) seeds. J Sci Food Agric 64:331–335

    Article  CAS  Google Scholar 

  • Gomes CEM, Barbosa AEAD, Macedo LLP et al (2005) Effect of trypsin inhibitor from Crotalaria pallida seeds on Callosobruchus maculatus (cowpea weevil) and Ceratitis capitata (fruit fly). Plant Physiol Biochem 43:1095–1102

    Article  PubMed  CAS  Google Scholar 

  • Gourinath S, Alam N, Srinivasan A et al (2000) Structure of the bifunctional inhibitor of trypsin and alpha-amylase from ragi seeds at 2.2 Å resolution. Acta Crystallogr Sect D 56(3):287–293

    Article  CAS  Google Scholar 

  • Graham JS, Ryan CA (1997) Accumulation of metallocarboxy-peptidase inhibitor in leaves of wounded potato plants. Biochem Biophys Res Commun 101:1164–1170

    Article  Google Scholar 

  • Green TR, Ryan CA (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175:776–777

    Article  PubMed  CAS  Google Scholar 

  • Greenblatt HM, Ryan CA, James MNG (1989) Structure of the complex Streptomyces griseus proteinase B and polypeptide chymotrypsin inhibitor-I at 2.1 Å resolution. J Mol Biol 205:201–228

    Article  PubMed  CAS  Google Scholar 

  • Gruden K, Strukelj B, Popovic T et al (1998) The cysteine protease activity of Colorado potato beetle (Leptinotarsa decemlineata Say) guts, which is insensitive to potato protease inhibitors, is inhibited by thyroglobulin type-1 domain inhibitors. Insect Biochem Mol Biol 28:549–560

    Article  PubMed  CAS  Google Scholar 

  • Gupta P, Dhawan K, Malhotra SP (2000) Purification and characterization of trypsin inhibitor from seeds of faba bean (Vicia faba L.). Acta Physiol Plant 22:433–438

    Article  CAS  Google Scholar 

  • Halitschke R, Gase K, Hui D et al (2003) Molecular interactions between the specialist herbivore Manduca sexta (lepidoptera, sphingidae) and its natural host Nicotiana attenuata. VI. Microarray analysis reveals that most herbivore-specific transcriptional changes are mediated by fatty acid-amino acid conjugates. Plant Physiol 131:1894–1902

    Article  PubMed  CAS  Google Scholar 

  • Hamato N, Koshiba T, Pham TN et al (1995) Trypsin and elastase inhibitors from bitter gourd (Momordica charantia LINN) seeds: purification, amino acid sequences, and inhibitory activities of four new inhibitors. J Biochem 117:432–437

    Article  PubMed  CAS  Google Scholar 

  • Haq SK, Khan RH (2003) Characterization of a Protease Inhibitor from Cajanus cajan (L.). J Protein Chem 22:543–554

    Article  PubMed  CAS  Google Scholar 

  • Hara S, Makino J, Ikenaka T (1989) Amino acid sequences and disulfide bridges of serine proteinase inhibitors from bitter gourd (Momordica charantia Linn) seeds. J Biochem 105:88–92

    PubMed  CAS  Google Scholar 

  • Harsulkar AM, Giri AP, Patankar AG et al (1999) Successive use of non-host plant protease inhibitors required for effective inhibition of Helicoverpa armigera gut proteases and larval growth. Plant Physiol 121:497–506

    Article  PubMed  CAS  Google Scholar 

  • Hartl M, Giri AP, Kaur H et al (2011) The multiple functions of plant serine protease inhibitors: defense against herbivores and beyond. Plant Signal Behav 6:1009–1011

    Article  PubMed  CAS  Google Scholar 

  • Haruta M, Major IT, Christopher ME et al (2001) A Kunitz trypsin inhibitor gene family from trembling aspen (Populus tremuloides Michx.): cloning, functional expression, and induction by wounding and herbivory. Plant Mol Biol 46:347–359

    Article  PubMed  CAS  Google Scholar 

  • Heath RL, Barton PA, Simpson RJ et al (1995) Characterization of the protease processing sites in a multidomain protease inhibitor precursor from Nicotiana alata. Eur J Biochem 230:250–257

    Article  PubMed  CAS  Google Scholar 

  • Heitz A, Hernandez JF, Gagnon J et al (2001) Solution structure of the squash trypsin inhibitor MCOTI-II. A new family for cyclic knottins. Biochemistry 40:7973–7983

    Article  PubMed  CAS  Google Scholar 

  • Hejgaard J, Hauge S (2002) Serpins of oat (Avena sativa) grain with distinct reactive centres and inhibitory specificity. Physiol Plant 116:155–163

    Article  PubMed  CAS  Google Scholar 

  • Holak TA, Bode W, Huber R et al (1989a) Nuclear magnetic resonance solution and X-ray structures of squash trypsin inhibitor exhibit the same conformation of the proteinase binding loop. J Mol Biol 210:649–654

    Article  PubMed  CAS  Google Scholar 

  • Holak TA, Gondol D, Otlewski J et al (1989b) Determination of the complete three-dimensional structure of the trypsin inhibitor from squash seeds in aqueous solution by nuclear magnetic resonance and a combination of distance geometry and dynamical simulated annealing. J Mol Biol 210:635–648

    Article  PubMed  CAS  Google Scholar 

  • Hollick JB, Gordon MP (1995) Transgenic analysis of a hybrid poplar wound-inducible promoter reveals developmental patterns of expression similar to that of storage protein genes. Plant Physiol 109:73–85

    Article  PubMed  CAS  Google Scholar 

  • Houseman JG, Thie NMR (1993) Difference in digestive proteolysis in stored maize beetles: Sitophilus zeamais (Coleoptera: Curculionidae) and Prostephanus truncatus (Coleoptera: Bustrichidae). J Econ Entomol 86:1049–1054

    CAS  Google Scholar 

  • Houseman JG, Downe AER, Philogene BJR (1989) Partial characterization of proteinase activity in the larval midgut of the European corn borer Ostrinia nubilalis Hubner (Lepidoptera: Pyralidae). Can J Zool 67:864–868

    Article  CAS  Google Scholar 

  • Huber R, Carrell RW (1989) Implications of the three-dimensional structure of alpha I -antitrypsin for structure and function of serpins. Biochemistry 28:8951–8966

    Article  PubMed  CAS  Google Scholar 

  • Hunt MD, Neuenschwander UH, Delaney TP et al (1996) Recent advances in systemic acquired resistance research-a review. Gene 179:89–95

    Article  PubMed  CAS  Google Scholar 

  • Huntington JA, Read RJ, Carrell RW (2000) Structure of a serpin–protease complex shows inhibition by deformation. Nature (London) 407:923–926

    Article  CAS  Google Scholar 

  • Irving JA, Pike RN, Dai W et al (2002) Evidence that serpin architecture intrinsically supports papain-like cysteine protease inhibition: engineering α1-antitrypsin to inhibit cathepsin proteases. Biochemistry 41:4998–5004

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa A, Ohta S, Matsuoka K et al (1994) A family of potato genes that encode Kunitz type proteinase inhibitors: structural comparisons and differential expression. Plant Cell Physiol 35:303–312

    PubMed  CAS  Google Scholar 

  • Iulek J, Franco OL, Silva M et al (2000) Purification, biochemical characterisation and partial primary structure of a new alpha-amylase inhibitor from Secale cereal (rye). Int J Biochem Cell Biol 32(1):195–204

    Article  Google Scholar 

  • Iwasaki T, Kiyohara T, Yoshikawa M (1971) Purification and partial characterization of two different types of proteinase inhibitors (inhibitors II-a and II-b) from potatoes. J Biochem 70:817–826

    PubMed  CAS  Google Scholar 

  • Jongsma MA, Bolter C (1997) The adaptation of insects to plant protease inhibitors. J Insect Physiol 43:885–895

    Article  PubMed  CAS  Google Scholar 

  • Jongsma MA, Bakker PL, Peters J et al (1995) Adaptation of Spodoptera exigua larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition. Proc Natl Acad Sci USA 92:8041–8045

    Article  PubMed  CAS  Google Scholar 

  • Joubert FJ, Merrifield EH, Dowdle EBD (1987) The reactive sites of protease inhibitors from Erythrina seeds. Int J Biochem 19:601–606

    Article  PubMed  CAS  Google Scholar 

  • Kansal R, Gupta RN, Koundal KR et al (2008) Purification, characterization and evaluation of insecticidal potential of trypsin inhibitor from mungbean (Vigna radiata L. Wilczek) seeds. Acta Physiol Plant 30:761–768

    Article  CAS  Google Scholar 

  • Khadeeva NV, Kochieva EZ, Tcherednitchenko MY et al (2009) Use of Buckwheat Seed Protease Inhibitor Gene for Improvement of Tobacco and Potato Plant Resistance to Biotic Stress. Biochemistry (Moscow) 74:260–267

    Article  CAS  Google Scholar 

  • Khadnair AH, Evans IR (2000) Molecular and microscopical detection of aster yellows phytoplasma associated with infected parsnip. Microbiol Res 155:53–57

    Article  Google Scholar 

  • Klinger J, Powell G, Thompson GA et al (1998) Phloem specific aphid resistance in Cucumis melo line AR 5: effects on feeding behaviour and performance of Aphis gossypii. Entomol Exper Appl 86:79–88

    Article  Google Scholar 

  • Knauper V, Reinke H, Tschesche H (1990) Inactivation of human plasma α1-proteinase inhibitor by human PMN leucocyte collagenase. FEBS Lett 263:355–357

    Article  PubMed  CAS  Google Scholar 

  • Koiwa H, Bressan RA, Hasegawa PM (1997) Regulation of protease inhibitors and plant defense. Trends Plant Sci 2:379–384

    Article  Google Scholar 

  • Koiwa K, Shade RE, Zhu-salzman K et al (1998) Phage display selection can differentiate insecticidal activity of soybean cystatins. Plant J 14:371–379

    Article  PubMed  CAS  Google Scholar 

  • Konarev AIV, Anisimova IN, Gavrilova VA et al (2000) Novel protease inhibitors in seeds of sunflower (Helianthus annuus L.): polymorphism, inheritance and properties. Theor Appl Genet 100:82–88

    Article  CAS  Google Scholar 

  • Konarev AIV, Anisimova IN, Gavrilova VA (2002) Serine protease inhibitors in the Compositae: distribution, polymorphism and properties. Phytochemistry 59:279–291

    Article  PubMed  CAS  Google Scholar 

  • Konarev AV, Griffin J, Konechnaya GY et al (2004) The distribution of serine protease inhibitors in the seed of Asteridae. Phytochemistry 65:3003–3020

    Article  PubMed  CAS  Google Scholar 

  • Kong L, Ranganathan S (2008) Tandem duplication, circular permutation, molecular adaptation: how Solanaceae resist pests via inhibitors. BMC Bioinform 9:22

    Article  CAS  Google Scholar 

  • Korth KL, Dixon RA (1997) Evidence for chewing insect specific molecular events distinct from a general wound response in leaves. Plant Physiol 115:1299–1305

    PubMed  CAS  Google Scholar 

  • Krishnamoorthi R, Gong Y, Richardson M (1990) A new protein inhibitor of trypsin and activated Hageman factor from pumpkin (Cucurbita maxima) seeds. FEBS Lett 273:163–167

    Article  PubMed  CAS  Google Scholar 

  • Kumar P, Sreerama YN, Gowda LR (2002) Formation of Bowman-Birk inhibitors during the germination of horsegram (Dolichos biflorus). Phytochemistry 60:581–588

    Article  PubMed  CAS  Google Scholar 

  • Kunitz M (1945) Crystallization of a trypsin inhibitor from soybean. Science 101:668–669

    Article  PubMed  CAS  Google Scholar 

  • Kuroda M, Kiyosaki T, Matsumoto I et al (2001) Molecular cloning, characterization and expression of wheat cystatins. Biosci Biotechnol Biochem 65:22–28

    Article  PubMed  CAS  Google Scholar 

  • Laing WA, McManus MT (2002) In: McManus MT, Laing WA and Allan AC (eds) Protein–protein interactions in plants, vol. 7. Academic Press, Sheffield, pp 77–119

  • Lam SK, Ng TB (2010) A dimeric high-molecular-weight chymotrypsin inhibitor with antitumor and HIV-1 reverse transcriptase inhibitory activities from seeds of Acacia confusa. Phytomed Int J Phytother Phytopharmacol 17:621–625

    Article  CAS  Google Scholar 

  • Lara P, Ortego F, Gonzalez-Hidalgo E et al (2000) Adaptation of Spodoptera exigua (Lepidoptera: Noctuidae) to barley trypsin inhibitor BTI-CMe expressed in transgenic tobacco. Transgenic Res 9:169–178

    Article  PubMed  CAS  Google Scholar 

  • Laskowski M Jr, Kato I (1980) Protein inhibitors of proteinases. Annu Rev Biochem 49:685–693

    Article  Google Scholar 

  • Laskowski M, Qasim MA (2000) What can the structures of enzyme-inhibitor complexes tell us about the structures of enzyme substrate complexes? Biochim Biophys Acta 1477:324–337

    Article  PubMed  CAS  Google Scholar 

  • Law R, Zhang Q, McGowan S et al (2006) An overview of the serpin superfamily. Genome Biol 7(5):216

    Article  PubMed  CAS  Google Scholar 

  • Lawrence PK, Koundal KR (2002) Plant protease inhibitors in control of phytophagous insects. Electron J Biotechnol 5:93–109

    Article  Google Scholar 

  • Lawrence SD, Novak NG (2001) A rapid method for the production and characterization of recombinant insecticidal proteins in plants. Mol Breed 8:139–146

    Article  CAS  Google Scholar 

  • Ledoigt G, Griffaut B, Debiton E et al (2006) Analysis of secreted protease inhibitors after water stress in potato tubers. Int J Biol Macromols 38:268–271

    Article  CAS  Google Scholar 

  • Lee CF, Lin JY (1995) Amino acid sequences of trypsin inhibitors from the melon Cucumis melo. J Biochem 118:18–22

    PubMed  CAS  Google Scholar 

  • Lee JS, Brown WE, Graham JS et al (1986) Molecular characterization and phylogenetic studies of a wound-inducible proteinase inhibitor I gene in Lycopersicon species). PNAS 83:7277–7281

    Article  PubMed  CAS  Google Scholar 

  • Lherminier J, Bonfiglioli RG, Daire X et al (1999) Oligodeoxynucleotides as probes for in situ hybridization with transmission electron microscopy to specifically localize phytoplasma in plant cells. Mol Cell Probes 13:41–47

    Article  PubMed  CAS  Google Scholar 

  • Li-Jia Qu, Chen J, Liu M et al (2003) Molecular cloning and functional analysis of a novel type of Bowman-Birk inhibitor gene family in rice. Plant Physiol 133:560–570

    Article  CAS  Google Scholar 

  • Lin GD, Bode W, Huber R et al (1993) The 0.25 nm X-ray structure of the Bowman-Birk type inhibitor from mung bean in ternary complex with porcine trypsin. Eur J Biochem 212:549–555

    Google Scholar 

  • Luo M, Wang Z, Li H et al (2009) Overexpression of a weed (Solanum americanum) protease inhibitor in transgenic tobacco results in increased glandular trichome density and enhanced resistance to Helicoverpa armigera and Spodoptera litura. Int J Mol Sci 10:1896–1910

    Article  PubMed  CAS  Google Scholar 

  • Macedo MLR, Freire MGM, Cabrini EC et al (2003) A trypsin inhibitor from Peltophorum dubium seeds active against pest proteases and its effect on the survival of Anagasta kuehniella (Lepidoptera: Pyralidae). Biochim Biophys Acta 1621:170–182

    Article  CAS  Google Scholar 

  • Macedo MRL, Sá CM, Freire MGM et al (2004) A Kunitz-type inhibitor of coleopteran proteases, isolated from Adenanthera pavonina L. seeds and its effect on Callosobruchus maculatus. J Agric Food Chem 52:2533–2540

    Article  PubMed  CAS  Google Scholar 

  • Macedo ML, Garcia VA, Freire MG et al (2007) Characterization of a Kunitz trypsin inhibitor with a single disulfide bridge from seeds of Inga laurina (SW.) Wild. Phyochemistry 68:1104–1111

    Article  CAS  Google Scholar 

  • Macedo MLR, Durigam RA, Soares da Silva D et al (2010) Adenanthera pavonina trypsin inhibitor retard growth of Anagasta kuehniella (Lepidoptera: Pyralidae). Insect Biochem Physiol 73:213–231

    CAS  Google Scholar 

  • Macedo MLR, Mariadas F, Freire GM et al (2011) A trypsin inhibitor from Sapindus saponaria L. seeds: purification, characterization, and activity towards pest insect digestive enzyme. Protein J 30:9–19

    Article  PubMed  CAS  Google Scholar 

  • Mahoney WC, Hermodson MA, Jones B et al (1984) Amino acid sequence and secondary structural analysis of the corn inhibitor of trypsin and activated Hageman Factor. J Biol Chem 259:8412–8416

    PubMed  CAS  Google Scholar 

  • Major IT, Constabel CP (2006) Molecular analysis of poplar defense against herbivory: comparison of wound- and insect elicitor-induced gene expression. New Phytol 172:617–635

    Article  PubMed  CAS  Google Scholar 

  • Major IT, Constabel CP (2008) Functional analysis of the Kunitz trypsin inhibitor family in poplar reveals biochemical diversity and multiplicity in defense against herbivores. Plant Physiol 146:888–903

    Article  PubMed  CAS  Google Scholar 

  • Malone M, Alarcon JJ (1995) Only xylem-borne factors can account for systemic wound signalling in the tomato plant. Planta 196:740–746

    Article  CAS  Google Scholar 

  • Margossian LJ, Federman AD, Giovannoni JJ et al (1988) Ethylene-regulated expression of a tomato fruit ripening gene encoding a proteinase inhibitor I with a glutamic residue at the reactive site. Proc Natl Acad Sci 85(21):8012–8016

    Article  PubMed  CAS  Google Scholar 

  • Mcgurl B, Orozco-Cardenas M, Pearce G (1994) Overexpression of the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase inhibitor synthesis. Proc Nat Acad Sci USA 91:9799–9802

    Article  PubMed  CAS  Google Scholar 

  • Meige M, Mascherpa J, Royer-Spierer A et al (1976) Analyse des crops proteiques isoles de Lablab Pupureus (L.) Sweet: localisation intracellulaire des globulines proteases et inhibiteurs de la trypsire. Planta 131:181–186

    Google Scholar 

  • Mello GC, Oliva ML, Sumikawa JT et al (2001) Purification and characterization of a new trypsin inhibitor from Dimorphandra mollis seeds. J Protein Chem 20:625–632

    Article  PubMed  CAS  Google Scholar 

  • Menegatti E, Sandro P, Peter W et al (1985) Isolation and characterization of a trypsin inhibitor from white mustard (Sinapis alba L.). J Agric Food Chem 33:784–789

    Article  CAS  Google Scholar 

  • Menegatti E, Boggian M, Ascenzi P et al (1987) Binding of the trypsin inhibitor from white mustard (Sinapis alba L.) seeds to bovine β-trypsin: thermodynamic study. J Enzyme Inhib Med Chem 2:67–71

    Article  CAS  Google Scholar 

  • Michaud D (1997) Avoiding protease mediated resistance in herbivorous pests. Trends Biotechnol 15:4–6

    Article  CAS  Google Scholar 

  • Michaud D, Nguyen-Quoc B, Vrain TC et al (1996) Response of digestive cysteine proteinases from the Colorado potato beetle (Leptinotarsa decemlineata) and the black vine weevil (Otiorynchus sulcatus) to a recombinant form of human stefin A. Arch Insect Biochem Physiol 31:451–464

    Article  PubMed  CAS  Google Scholar 

  • Miller EA, Lee MC, Atkinson AH et al (2000) Identification of a novel four-domain member of the proteinase inhibitor II family from the stigmas of Nicotiana alata. Plant Mol Biol 42(2):329–333

    Article  PubMed  CAS  Google Scholar 

  • Moura DS, Ryan CA (2001) Wound inducible proteinase inhibitors in pepper. Differential regulation upon wounding, systemin, and methyl jasmonate. Plant Physiol 126:289–298

    Article  PubMed  CAS  Google Scholar 

  • Moura DS, Bergey DR, Ryan CA (2001) Characterization and localization of a wound-inducible type I serine-carboxypeptidase from leaves of tomato plants (Lycopersicon esculentum Mill.). Planta 212:222–230

    Article  PubMed  CAS  Google Scholar 

  • Murdock LL, Brookhart G, Dunn PE (1987) Cysteine digestive proteinases in Coleoptera. Comp Biochem Physiol B 87:783–787

    Article  Google Scholar 

  • Murray C, Christeller JT (1995) Purification of a trypsin inhibitor (PFTI) from pumpkin fruit phloem exudate and isolation of putative trypsin and chymotrypsin inhibitor cDNA clones. Biol Chem Hoppe-Seyler 376(5):281–287

    Article  PubMed  CAS  Google Scholar 

  • Nandi AK, Basu D, Das S et al (1999) High level expression of soybean trypsin inhibitor gene in transgenic tobacco plants failed to confer resistance against damage caused by Helicoverpa armigera. J Biosci 24:445–452

    Article  CAS  Google Scholar 

  • Nilges M, Habazettl J, Brunger AT et al (1991) Relaxation matrix refinement of the solution structure of squash trypsin inhibitor. J Mol Biol 219:499–510

    Article  PubMed  CAS  Google Scholar 

  • Norton G (1991) Proteinase inhibitors. In: D’Mello JPF, Duffus CM, Duffus JH (eds) Toxic substances in crop plants. Royal Society of Chemistry, Cambridge, pp 68–106

    Chapter  Google Scholar 

  • Novillo C, Castanera P, Ortego F (1997) Inhibition of digestive trypsin like proteases from larvae of several lepidopteran species by the diagnostic cysteine protease inhibitor E64. Insect Biochem Mol Biol 27:247–254

    Article  CAS  Google Scholar 

  • Odani S, Ono T, Ikenak Τ (1980) The reactive site amino acid sequences of silk tree (Albizzia julibrissin) seed protease inhibitor. J Biochem 88:297–301

    PubMed  CAS  Google Scholar 

  • Odani S, Koide T, Ono T (1983) The complete amino acid sequence of barley trypsin inhibitor. J Biol Chem 258:7998–8003

    PubMed  CAS  Google Scholar 

  • Ogata F, Imamura H, Hirayama K et al (1986) Purification and characterization of four trypsin inhibitors from seeds of okra (Abelmoschus esculentus L.). Agric Biol Chem 50:2325–2333

    Article  CAS  Google Scholar 

  • Oliva MLV, Sampaio MU (2008) Bauhinia Kunitz-type protease inhibitors: structural characteristics and biological properties. J Biol Chem 389:1007–1013

    CAS  Google Scholar 

  • Oliva MLV, Sampaio MU, Sampaio CAM (1987) Serine and SH-protease inhibitors from Enterolobium contortisiliquum beans. Purification and preliminary characterization. Braz J Med Biol Res 20:767–770

    PubMed  CAS  Google Scholar 

  • Oliva MLV, Andrades S, Batista IFC et al (1999) Human plasma kallikrein and tissue kallikrein binding to a substrate based on the reactive site of a factor Xa inhibitor isolated from Bauhinia ungulate seeds. Immunopharmacology 45:145–149

    Article  PubMed  CAS  Google Scholar 

  • Oliva MLV, Andrades SA, Juliano MA et al (2003) Kinetic Characterization of Factor Xa Binding Using a Quenched Fluorescent Substrate Based on the Reactive Site of Factor Xa Inhibitor from Bauhinia ungulata Seeds. Curr Med Chem 10:1085–1093

    Article  PubMed  CAS  Google Scholar 

  • Oliveira AS, Migliolo L, Aquino RO et al (2007) Purification and characterization of a trypsin–papain inhibitor from Pithecelobium dumosum seeds and its in vitro effects towards digestive enzymes from insect pests. Plant Physiol Biochem 45:858–865

    Article  PubMed  CAS  Google Scholar 

  • Oppereman CH, Taylor CG, Conkling MA (1994) Rootknot nematode directed expression of a plant root specific gene. Science 263:221–223

    Article  Google Scholar 

  • Otlewski J, Krowarsch D (1996) Squash inhibitor family of serine proteinases. Acta Biochim Pol 43:431–444

    Google Scholar 

  • Paiva PMG, Oliva MLV, Fritz H et al (2006) Purification and primary structure determination of two Bowman–Birk type trypsin isoinhibitors from Cratylia mollis seeds. Phytochemistry 67:545–552

    Article  PubMed  CAS  Google Scholar 

  • Pandey PK, Jamal F (2010) Identification and evaluation of trypsin inhibitor in the seed extracts of Butea monosperma (Flame of Forest). Int J Biotechnol Biochem 6:513–520

    Google Scholar 

  • Pando SC, Oliva ML, Sampaio CA et al (2001) Primary sequence determination of a Kunitz inhibitor isolated from Delonix regia seeds. Phytochemistry 57:625–631

    Article  PubMed  CAS  Google Scholar 

  • Pannekoek H, Van Meijer M, Schleef RR et al (1993) Functional display of human plasminogen activator inhibitor 1 (PAI-1) on phages: novel perspectives for structure-function analysis by error-prone DNA synthesis. Gene 128:135–140

    Article  PubMed  CAS  Google Scholar 

  • Paolo A, Ruoppolo M, Amoresano A et al (1999) Characterization of low-molecular-mass trypsin isoinhibitors from oil rape (Brassica napus var oleifera) seed. FEBS J 261:275–284

    Google Scholar 

  • Park Y, Choi BH, Kwak JS et al (2005) Kunitz-type serine protease inhibitor from potato (Solanum tuberosum L. cv. Jopung). J Agric Food Chem 53:6491–6496

    Article  PubMed  CAS  Google Scholar 

  • Pearce G, Johnson S, Ryan CA (1993) Purification and characterization from tobacco (Nicotiana tabacum) leaves of six small, wound inducible, protease isoinhibitors of the potato inhibitor II family. Plant Physiol 102:639–644

    Article  PubMed  CAS  Google Scholar 

  • Plunkett G, Senear DF, Zuroske G et al (1982) Proteinase inhibitors I and II from leaves of wounded tomato plants: purification and properties. Arch Biochem Biophys 213:463–472

    Article  PubMed  CAS  Google Scholar 

  • Poerio E, Carrano L, Garzillo AM et al (1989) A trypsin inhibitor from the water soluble protein fraction of wheat kernel. Phytochemistry 28:1307–1311

    Article  CAS  Google Scholar 

  • Ponting CP, Russell RB (1995) Swaposins: circular permutations within genes encoding saposin homologues. Trends Biochem Sci 20:179–180

    Article  PubMed  CAS  Google Scholar 

  • Prakash B, Selvaraj S, Murthy MRN et al (1996) Analysis of the aminoacid sequences of plant Bowman-Birk inhibitors. J Mol Evol 42:560–569

    Google Scholar 

  • Prasad ER, Gupta AD, Padmasree K (2010) Purification and characterization of a Bowman-Birk proteinase inhibitor from the seeds of black gram (Vigna mungo). Phytochemistry 71:363–372

    Article  PubMed  CAS  Google Scholar 

  • Qi RF, Song Z, Chi C (2005) Structural features and molecular evolution of Bowman-Birk protease inhibitors and their potential application. Acta Biochemica et Biophysica 37:283–292

    Google Scholar 

  • Rai S, Aggarwal KK, Babu CR (2008) Isolation of a serine Kunitz trypsin inhibitor from leaves of Terminalia arjuna. Curr Sci 94:1509–1512

    CAS  Google Scholar 

  • Raj SS, Kibushi E, Kurasawa T et al (2002) Crystal structure of bovine trypsin and wheat germ trypsin inhibitor (I-2b) complex (2:1) at 2.3 a resolution. J Biochem 132:927–933

    Google Scholar 

  • Rakwak R, Agarwal KG, Jha NS (2001) Characterization of a rice (Oryza sativa L.) Bowman-Birk proteinase inhibitor: tightly light regulated induction in response to cut, jasmonic acid, ethylene and protein phosphatase 2A inhibitors. Gene 263:189–198

    Article  Google Scholar 

  • Ralph S, Oddy C, Cooper D et al (2006) Genomics of hybrid poplar (Populus trichocarpa x deltoides) interacting with forest tent caterpillars (Malacosoma disstria): normalized and full-length cDNA libraries, expressed sequence tags, and a cDNA microarray for the study of insect-induced defences in poplar. Mol Ecol 15:1275–1297

    Article  PubMed  Google Scholar 

  • Rawlings ND, Tolle DP, Barrett AJ (2004) Evolutionary families of peptidase inhibitors. Biochem J 378:705–716

    Article  PubMed  CAS  Google Scholar 

  • Reeck GR, Kramer KJ, Baker JE et al (1997) Proteinase inhibitors and resistance of transgenic plants to insects. In: Carozzi N, Koziel MM (eds) Advances in insect control: the role of transgenic plants. Taylor and Francis, London, pp 157–183

    Google Scholar 

  • Richardson M (1991) Seed storage proteins: the enzyme inhibitors. In: Rogers LJ (ed) Methods in plant biochemistry amino acids, proteins and nucleic acids. Academic Press, New York, pp 259–305

    Google Scholar 

  • Richardson M, Campos FAP, Xavier-Filho J et al (1986) The amino acid sequence and reactive (inhibitory) site of the major trypsin isoinhibitor (DE5) isolated from seeds of the Brazilian Carolina tree (Adenanthera pavonina L.). Biochim Biophys Acta 872:134–140

    Article  CAS  Google Scholar 

  • Ritonja A, Krizaj I, Mesko P et al (1990) The amino acid sequence of a novel inhibitor of cathepsin D from potato. FEBS Lett 267:1–15

    Article  Google Scholar 

  • Rottgen P, Collins JA (1995) Human pancreatic secretory trypsin inhibitor presenting a hypervariable highly constrained epitope via monovalent phagemid display. Gene 194:243–250

    Article  Google Scholar 

  • Roy S, Dutta SK (2009) Purification of chymotrypsin-trypsin from winged bean seeds using single step immunoaffinity column. Am J Biochem Biotechnol 5:142–146

    Article  CAS  Google Scholar 

  • Ryan CA (1990) Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annu Rev Phytopathol 28:425–449

    Article  CAS  Google Scholar 

  • Ryan CA (2000) The systemin signaling pathway: differential activation of plant defensive genes. Biochim Biophys Acta 1477:112–121

    Article  PubMed  CAS  Google Scholar 

  • Ryan CA, Balls AK (1962) An inhibitor of chymotrypsin from Solanum tuberosm and its behavior toward trypsin. Proc Natl Acad Sci USA 48:1839–1844

    Article  PubMed  CAS  Google Scholar 

  • Sampaio CA, Motta G, Sampaio MU et al (1992) Action of plant proteinase inhibitors on enzymes of the kallikrein kinin system. Agents Act Suppl 36:191–199

    Article  CAS  Google Scholar 

  • Sampaio CAM, Oliveira B, Marangoni S (1998) The complete amino acid sequence of a trypsin inhibitor from Bauhinia variegata var. candida seeds. J Protein Chem 17:827–834

    Article  PubMed  Google Scholar 

  • Sattar R, Ali SA, Kamal M et al (2004) Molecular mechanism of enzyme inhibition: prediction of the three-dimensional structure of the dimeric trypsin inhibitor from Leucaena leucocephala by homology modelling. Biochem Biophys Res Commun 314:755–776

    Article  PubMed  CAS  Google Scholar 

  • Schluter D, Marchinko KB, Barrett RDH (2010) Natural selection and the genetics of adaptation in threespine. Philos Trans Royal Soc B 365:2479–2486

    Article  Google Scholar 

  • Sharma U, Suresh CG (2011) Purification, crystallization and X-ray characterization of a Kunitz-type trypsin inhibitor protein from the seeds of chickpea (Cicer arietinum). Acta Cryst F67:714–717

    CAS  Google Scholar 

  • Shewry PR (1999) Enzyme inhibitors of seed: types and properties. In: Shewry PR, Casey P (eds) Seed proteins. Kluwer Academic Publishers, Netherlands, pp 587–615

    Chapter  Google Scholar 

  • Shibata H, Hara S, Ikenaka Τ et al (1986) Purification and Characterization of Protease Inhibitors from Winged Bean (Psophocarpus tetragonolobus (L.) seeds. J Biochem 99:1147–1155

    PubMed  CAS  Google Scholar 

  • Shivraj B, Pattabiraman TN (1981) Natural plant enzyme inhibitors. Characterization of an unusual alpha-amylase/trypsin inhibitor from ragi (Eleusine coracana Geartn.). Biochem J 193:29–36

    Google Scholar 

  • Shulke RH, Murdock LL (1983) Lipoxygenase trypsin inhibitor and lectin from soybeans: effects on larval growth of Manduca sexta (Lepidoptera: Sphingidae). Environ Entomol 12:787–791

    Google Scholar 

  • Silva AJ, Macedo MLR, Novello JC et al (2000) Biochemical characterization and N-terminal sequences of two new trypsin inhibitors from Copaifera langsdorffii seeds. J Protein Chem 20:1–7

    Article  Google Scholar 

  • Silva LP, Leite JRSA, Bloch JRC et al (2001) Stability of a black eyed pea trypsin/chymotrypsin inhibitor (BTCI). Protein Pept Lett 8:33–38

    Article  Google Scholar 

  • Silva AJ, Teles RC, Esteves GF et al (2008) Purification, crystallization and preliminary crystallographic studies of SPCI-chymotrypsin complex at 2.8 Å resolution. Acta Crystallogr, Sect F Struct Biol Cryst Commun 64:914–917

    Article  CAS  Google Scholar 

  • Silveira RV, Silva GS, Freire MGM et al (2008) Purification and characterization of a trypsin inhibitor from Plathymenia foliolosa seeds. J Agric Food Chem 56:11348–11355

    Article  CAS  Google Scholar 

  • Silverman GA, Bird PI, Carrell RW et al (2001) The serpins are an expanding superfamily of structurally similar but functionally diverse proteins, evolution, mechanism of evolution, novel functions, and revised nomenclature. J Biol Chem 276:33293–33296

    Article  PubMed  CAS  Google Scholar 

  • Simpson AJ, Maxwell AI, Govan JRW et al (1999) Elafin (elastase-specific inhibitor) has antimicrobial activity against Gram positive and Gram negative respiratory pathogens. FEBS Lett 452:309–313

    Article  PubMed  CAS  Google Scholar 

  • Socorro M, Cavalcanti M, Oliva ML et al (2002) Characterization of a Kunitz trypsin inhibitor with one disulfide bridge purified from Swartzia pickellii. Biochem Biophys Res Commun 29:635–639

    Google Scholar 

  • Souza EM, Mizuta K, Sampaio MU et al (1995) Purification and partial characterization of a Schizolobium parahyba chymotrypsin inhibitor. Phytochemistry 39:521–525

    Article  PubMed  CAS  Google Scholar 

  • Souza-Pinto JC, Oliva ML, Sampaio CA et al (1996) Effect of a serine protease inhibitor from Leucaena leucocephala on plasma kallikrein and plasmin. Immunopharmacology 33:330–332

    Article  PubMed  CAS  Google Scholar 

  • Sparber SB (1985) Insect resistance to biological insecticide Bacillus thuringiensis. Science 229:193–195

    Article  Google Scholar 

  • Sreedharan SK, Verma C, Caves LSD (1996) Demonstration that 1-trans-epoxysuccinyl-L-leucylamido-(4-guanidino) butane (E-64) is one of the most effective low Mr inhibitors of trypsin-catalysed hydrolysis. Characterization by kinetic analysis and by energy minimization and molecular dynamics simulation of the E-64–β-trypsin complex. Biochem J 316:777–786

    PubMed  CAS  Google Scholar 

  • Sterky F, Bhalerao RR, Unneberg P et al (2004) A Populus EST resource for plant functional genomics. Proc Nat Acad Sci USA 101:13951–13956

    Article  PubMed  Google Scholar 

  • Stintzi A, Weber H, Raymond P et al (2001) Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc Nat Acad Sci USA 98:12837–12842

    Article  PubMed  CAS  Google Scholar 

  • Stratmann JW, Scheer J, Ryan CA (2000a) Suramin inhibits initiation of defense signaling by systemin, chitosan, and a beta-glucan elicitor in suspension-cultured Lycopersicon peruvianum cells. Proc Nat Acad Sci USA 97:8862–8867

    Article  PubMed  CAS  Google Scholar 

  • Stratmann JW, Stelmach BA, Weiler EW et al (2000b) UVB/UVA radiation activates a 48 kDa myelin basic protein kinase and potentiates wound signaling in tomato leaves. Photochem Photobiol 71:116–123

    Article  PubMed  CAS  Google Scholar 

  • Strobl S, Maskos K, Wiegand G et al (1998) A novel strategy for inhibition of alpha amylases:yellow meal worm alpha-amylase in complex with the Ragi bifunctional inhibitor at 2.5 Å resolution. Structure 6:911–921

    Article  PubMed  CAS  Google Scholar 

  • Sumikawa JT, Brito MV, Araujo APU et al (2008) Action of Bauhinia-derivated compounds on Callosobruchus maculatus. In: Del Valle S, Escher E, Lubell WD (Org) (eds) Peptides for youth. American Peptide Society, New York, pp 611–613

  • Sun J, Wang H, Ng Tzi B (2010) Trypsin isoinhibitors with antiproliferative activity toward leukemia cells from Phaseolus vulgaris cv “White Cloud Bean”. J Biomed Biotechnol. doi:10.1155/2010/219793

    Google Scholar 

  • Tamhane VA, Chougule NP, Giri AP et al (2005) In vivo and in vitro effect of Capsicum annum proteinase inhibitors on Helicoverpa armigera gut proteinases. Biochim Biophys Acta 1722(2):156–167

    Article  PubMed  CAS  Google Scholar 

  • Tanaka AS, Sampaio MU, Sampaio CA (1989) Purification and preliminary characterization of Torresea cearensis trypsin inhibitor. Braz J Med Biol Res 22:1069–1071

    PubMed  CAS  Google Scholar 

  • Tanaka AS, Sampaio CA, Frith H et al (1995) Functional display and expression of chicken cystatin using a phagemid system. Biochem Biophys Res Commun 214:389–395

    Article  PubMed  CAS  Google Scholar 

  • Tanaka AS, Sampaio MU, Marangoni S et al (1997) Purification and primary structure determination of a Bowman-Birk trypsin inhibitor from Torresea cearensis seeds. Biol Chem 378:273–281

    Article  PubMed  CAS  Google Scholar 

  • Tashiro M, Asao T, Hitara C et al (1990) The complete amino acid sequence of a major trypsin inhibitor from seeds of foxtail millet (Setaria italica). J Biochem 108:669–672

    Google Scholar 

  • Taylor MAJ, Baker KC, Briggs GS et al (1995) Recombinant proregions from papain and papaya proteinase IV are selective high affinity inhibitors of the mature papaya enzymes. Protein Eng 8:59–62

    Article  PubMed  CAS  Google Scholar 

  • Thaimattam R, Tykarska E, Bierzynski A et al (2002) Atomic resolution structure of squash trypsin inhibitor: unexpected metal coordination. Acta Crystallogr D Biol Crystallogr 58:1448–1461

    Article  PubMed  CAS  Google Scholar 

  • Tian W-M, Peng S-Q, Wang X-C et al (2007) Vegetative storage protein in litchi chinensis, a subtropical evergreen fruit tree, possesses trypsin inhibitor activity. Ann Bot 100:1199–1208

    Article  PubMed  CAS  Google Scholar 

  • Titarenko E, Rojo E, Leon J et al (1997) Jasmonic acid-dependent and–independent signaling pathways control wound-induced gene activation in Arabidopsis thaliana. Plant Physiol 115:817–826

    Article  PubMed  CAS  Google Scholar 

  • Tong-xiang L, Jian-zhao N, Hui-yu X et al (2007) Separation and purification of mungbean trypsin inhibitor. Chin J Biochem Pharm. doi:CNKI:SUN:SHYW.0.2007-03-000

    Google Scholar 

  • Tsybina T, Dunaevsky Y, Musolyamov A et al (2004) New protease inhibitors from buckwheat seeds: properties, partial amino acid sequences and possible biological role. Biol Chem 385:429–434

    Article  PubMed  CAS  Google Scholar 

  • Tuskan GA, DiFazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  PubMed  CAS  Google Scholar 

  • Valdés-Rodríguez S, Segura-Nieto M, Chagolla-Lόpez A et al (1993) Purification, characterization, and complete amino acid sequence of a trypsin inhibitor from amaranth (Amaranthus hypochondriacus) seeds. Plant Physiol 103:1407–1412

    Article  PubMed  Google Scholar 

  • Vercammen D, Belenghi B, van de Cotte B et al (2006) Serpin1 of Arabidopsis thaliana is a suicide inhibitor for metacaspase 9. J Mol Biol 364:625–636

    Article  PubMed  CAS  Google Scholar 

  • Visal S, Taylor MAJ, Michaud D (1998) The pro-region of papaya IV inhibits colorado potato beetle digestive cysteine proteinases. FEBS Lett 434:401–405

    Article  PubMed  CAS  Google Scholar 

  • Volpicella M, Shipper A, Jongsma MA et al (2000) Characterization of recombinant mustard trypsin inhibitor 2 (MTI-2) expressed in Pichia pastoris. FEBS Lett 468:137–141

    Article  PubMed  CAS  Google Scholar 

  • Walker AJ, Ford L, Majerus MEN et al (1998) Characterisation of the midgut digestive proteinase activity of the two-spot ladybird (Adalia bipunctata L.) and its sensitivity to proteinase inhibitors. Insect Biochem Mol Biol 28:173–180

    Article  CAS  Google Scholar 

  • Wang HX, Ng TB (2006) Concurrent isolation of a Kunitz-type trypsin inhibitor with antifungal activity and a novel lectin from Pseudostellaria heterophylla roots. BBRC 342(1):349–353

    PubMed  CAS  Google Scholar 

  • Wang CI, Yang Q, Craik CS (1995) Isolation of a high affinity inhibitor of urokinase-type plasminogen activator by phage display of ecotin. J Biol Chem 270:12250–12256

    PubMed  CAS  Google Scholar 

  • Wang L, Halitschke R, Kang JH et al (2007a) Independently silencing two JAR family members impairs levels of trypsin proteinase inhibitors but not nicotine. Planta 226:159–167

    Article  PubMed  CAS  Google Scholar 

  • Wang ZY, Ding LW, Ge ZJ et al (2007b) Purification and characterization of native and recombinant SaPIN2a, a plant sieve element-localized protease inhibitor. Plant Physiol Biochem 45:757–766

    Article  PubMed  CAS  Google Scholar 

  • Wasternack C, Parthier B (1997) Jasmonate signalled plant gene expression. Trends Plant Sci 2:302–307

    Article  Google Scholar 

  • Wei R, Hai L, Lin-Fang DU (2007) Inhibitory effect of trypsin inhibitor from Cassia obtusifolia seeds against Pieris rapae larvae. Sichuan J Zool. doi:CNKI:SUN:SCDW.0.2007-03-054

    Google Scholar 

  • Wieczorek M, Otlewski J, Cook J et al (1985) The squash family of serine proteinase inhibitors. Amino acid sequences and association equilibrium constants of inhibitors from squash, summer squash, zucchini, and cucumber seeds. Biochem Biophys Res Commun 126:646–652

    Article  PubMed  CAS  Google Scholar 

  • Williamson MS, Forde J, Buxton B et al (1987) Nucleotide sequence of barley chymotrypsin inhibitor-2 (CI-2) and its expression in normal and high-lysine barley. Eur J Biochem 165:99–106

    Article  PubMed  CAS  Google Scholar 

  • Wingate VP, Broadway RM, Ryan CA (1989) Isolation and characterization of a novel, developmentally regulated proteinase inhibitor I protein and cDNA from the fruit of a wild species of tomato. J Biol Chem 264(30):17734–17738

    PubMed  CAS  Google Scholar 

  • Wojtaszek J, Kolaczkowska A, Kowalska J (2006) LTCI, a novel chymotrypsin inhibitor of the potato I family from the earthworm Lumbricus terrestris. Purification, cDNA cloning, and expression. Comp Biochem Physiol B: Biochem Mol Biol 143:465–472

    Article  CAS  Google Scholar 

  • Wolfson JL, Murdock LL (1990) Diversity in digestive proteinase activity among insects. J Chem Ecol 16:1089–1102

    Article  CAS  Google Scholar 

  • Yan K-M, Chang T, Soon S-A et al (2009) Purification and Characterization of Bowman-Birk Protease Inhibitor from Rice Coleoptiles. J Chin Chem Soc 56:949–960

    CAS  Google Scholar 

  • Yang DH, Hettenhausen C, Baldwin IT et al (2011) BAK1 regulates the accumulation of jasmonic acid and the levels of trypsin proteinase inhibitors in Nicotiana attenuata’s responses to herbivory. J Exp Bot 62:641–652

    Article  PubMed  CAS  Google Scholar 

  • Yoo B-C, Aoki K, Xiang Yu et al (2000) Characterization of Cucurbita maxima Phloem Serpin-1 (CmPS-1) A developmentally regulated elastase inhibitor. J Biol Chem 275:35122–35128

    Article  PubMed  CAS  Google Scholar 

  • Zhou JY, Liao H, Zhang NH et al (2008) Identification of a Kunitz inhibitor from Albizzia kalkora and its inhibitory effect against pest midgut proteases. Biotechnol Lett 30:495–1499

    Google Scholar 

  • Zhu-Salzman K, Salzman RA, Koiwa H et al (1998) Ethylene negatively regulates local expression of plant defense lectin genes. Physiol Plant 104:365–372

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors express their gratitude to Ministry of Science and Technology, Govt. of India and University Grants Commission, New Delhi for providing financial support to the department under the DST-FIST scheme for developing infrastructure to carry out work on such aspects. I am thankful to Council of Science and Technology, U.P. India for providing recurring financial support vide project CST/SERPD/D-1136.

Author information

Authors and Affiliations

  1. Department of Biochemistry (DST-FIST & UGC-SAP Supported), Dr. Ram Manohar Lohia, Avadh University, Faizabad, 224001, UP, India

    Farrukh Jamal, Prabhash K. Pandey & Dushyant Singh

  2. Department of Biotechnology, Babasaheb Bhimrao Ambedkar University, Lucknow, UP, India

    M. Y. Khan

Authors
  1. Farrukh Jamal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Prabhash K. Pandey
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dushyant Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Y. Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Farrukh Jamal.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jamal, F., Pandey, P.K., Singh, D. et al. Serine protease inhibitors in plants: nature’s arsenal crafted for insect predators. Phytochem Rev 12, 1–34 (2013). https://doi.org/10.1007/s11101-012-9231-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11101-012-9231-y

Keywords

Search

Navigation