Biotechnology Letters

, Volume 39, Issue 5, pp 647–666 | Cite as

Structural and functional characteristics of plant proteinase inhibitor-II (PI-II) family

  • Shazia Rehman
  • Ejaz Aziz
  • Wasim Akhtar
  • Muhammad Ilyas
  • Tariq Mahmood


Plant proteinase inhibitor-II (PI-II) proteins are one of the promising defensive proteins that helped the plants to resist against different kinds of unfavorable conditions. Different roles for PI-II have been suggested such as regulation of endogenous proteases, modulation of plant growth and developmental processes and mediating stress responses. The basic knowledge on genetic and molecular diversity of these proteins has provided significant insight into their gene structure and evolutionary relationships in various members of this family. Phylogenetic comparisons of these family genes in different plants suggested that the high rate of retention of gene duplication and inhibitory domain multiplication may have resulted in the expansion and functional diversification of these proteins. Currently, a large number of transgenic plants expressing PI-II genes are being developed for enhancing the defensive capabilities against insects, bacteria and pathogenic fungi. Much emphasis is yet to be given to exploit this ever expanding repertoire of genes for improving abiotic stress resistance in transgenic crops. This review presents an overview about the current knowledge on PI-II family genes, their multifunctional role in plant defense and physiology with their potential applications in biotechnology.


Multifunctional role Proteinase inhibitor-II (PI-II) proteins Stress responses Transgenic plants 



This work was financially supported by the Higher Education Commission, Islamabad, Pakistan.

Compliance with ethical standards

Conflict of interest

The authors declared that they have no conflict of interest.


  1. Abdeen A, Virgós A, Olivella E, Villanueva J, Avilés X, Gabarra R, Prat S (2005) Multiple insect resistance in transgenic tomato plants over-expressing two families of plant proteinase inhibitors. Plant Mol Biol 57:189–202PubMedCrossRefGoogle Scholar
  2. Abuereish GM (1998) Pepsin inhibitor from roots of Anchusa strigosa. Phytochemistry 48:217–221PubMedCrossRefGoogle Scholar
  3. 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 annuum) seeds. Biochim Biophys Acta 1298:95–101PubMedCrossRefGoogle Scholar
  4. Atkinson AH, Heath RL, Simpson RJ, Clarke AE, Anderson MA (1993) Proteinase inhibitors in Nicotiana alata stigmas are derived from a precursor protein which is processed into five homologous inhibitors. Plant Cell 5:203–213PubMedPubMedCentralCrossRefGoogle Scholar
  5. Balandin T, van der Does C, Albert JMB, Bol JF, Linthorst HJM (1995) Structure and induction pattern of a novel proteinase inhibitor class II gene of tobacco. Plant Mol Biol 27:1197–1204PubMedCrossRefGoogle Scholar
  6. Barta E, Pintar A, Pongor S (2002) Repeats with variations: accelerated evolution of the Pin2 family of proteinase inhibitors. Trends Genet 18:600–603PubMedCrossRefGoogle Scholar
  7. Beekwilder J, Schipper B, Bakker P, Bosch D, Jongsma M (2000) Characterization of potato proteinase inhibitor II reactive site mutants. Eur J Biochem 267:1975–1984PubMedCrossRefGoogle Scholar
  8. Benchabane M, Schluter U, Vorster J, Goulet MC, Michaud D (2010) Plant cystatins. Biochimie 92:1657–1666PubMedCrossRefGoogle Scholar
  9. Berger A, Schechter I (1970) Mapping the active site of papain with the aid of peptide substrates and inhibitors. Philos Trans R Soc Lond B Biol Sci 257:249–264PubMedCrossRefGoogle Scholar
  10. Bergey DR, Howe GA, Ryan CA (1996) Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. Proc Natl Acad Sci USA 93:12053–12058PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bhattacharjee C, Prasad DT, Manjunath NH, Sanyal D, Zarga SM (2012) Exploring plant proteinase inhibitors. Genom Appl Biol 3:8–21. doi: 10.3969/gab.2012.03.0002 Google Scholar
  12. Birk Y (2003) Plant protease inhibitors: significance in nutrition, plant protection, cancer prevention and genetic engineering. Springer, Berlin, p 170Google Scholar
  13. Bishop PD, Makus DJ, Pearce G, Ryan CA (1981) Proteinase inhibitor-inducing factor activity in tomato leaves resides in oligosaccharides enzymatically released from cell walls. Proc Natl Acad Sci USA 78:3536–3540PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bryant J, Green TR, Gurusaddaiah T, Ryan CA (1976) Proteinase inhibitor II from potatoes: isolation and characterization of its protomer components. Biochemistry 15:3418–3424PubMedCrossRefGoogle Scholar
  15. Brzin J, Kidric M (1995) Proteinases and their inhibitors in plants: role in normal growth and in response to various stress conditions. Biotechnol Genet Eng Rev 13:421–467CrossRefGoogle Scholar
  16. Cançado GMA, Nogueira FTS, Camargo SR, Drummond RD, Jorge RA, Menossi M (2008) Gene expression profiling in maize roots under aluminum stress. Biol Plant 52:475–485CrossRefGoogle Scholar
  17. Cao FY, Yoshioka K, Desveaux D (2011) The roles of ABA in plant-pathogen interactions. J Plant Res 124:489–499PubMedCrossRefGoogle Scholar
  18. Charity JA, Hughes P, Anderson MA, Bittisnich DJ, Whitecross M, Higgins TJV (2005) Pest and disease protection conferred by expression of barley ß-hordothionin and Nicotiana alata proteinase inhibitor genes in transgenic tobacco. Funct Plant Biol 32:35–44CrossRefGoogle Scholar
  19. Choi D, Park JA, Seo YS, Chun YJ, Kim WT (2000) Structure and stress-related expression of two cDNAs encoding proteinase inhibitor II of Nicotiana glutinosa L. Biochim Biophys Acta 1492:211–215PubMedCrossRefGoogle Scholar
  20. Christeller JT, Farley PC, Ramsay RJ, Sullivan PA, Laing WA (1998) Purification, characterization and cloning of an aspartic proteinase inhibitor from squash phloem exudates. Eur J Biochem 254:160–167PubMedCrossRefGoogle Scholar
  21. Chung HS, Koo AJ, Gao X, Jayanty S, Thines B, Jones AD, Howe GA (2008) Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory. Plant Physiol 146(3):952–964PubMedPubMedCentralCrossRefGoogle Scholar
  22. Chye ML, Sin SF, Xu ZF, Yeung EC (2006) Serine proteinase inhibitor proteins: exogenous and endogenous functions. Vitro Cell Dev Biol Plant 42:100–108CrossRefGoogle Scholar
  23. Clark AM, Jacobsen KR, Bostwick DE, Dannenhoffer JM, Skaggs MI, Thompson GA (1997) Molecular characterization of a phloem-specific gene encoding the filament protein, phloem protein 1 (PP1), from Cucurbita maxima. Plant J 12:49–61PubMedCrossRefGoogle Scholar
  24. Conconi A, Smerdon MJ, Howe GA, Ryan CA (1996) The octadecanoid signalling pathway in plants mediates a response to ultraviolet radiation. Nature 383:826–829PubMedCrossRefGoogle Scholar
  25. Delano-Frier JP, Aviles-Arnaut H, Casarrubias-Castillo K, Casique-Arroyo G, Castrillon-Arbelaez PA, Herrera-Estrella L et al (2011) Transcriptomic analysis of grain amaranth (Amaranthus hypochondriacus) using 454 pyrosequencing: comparison with A. tuberculatus, expression profiling in stems and in response to biotic and abiotic stress. BMC Genom 12:363CrossRefGoogle Scholar
  26. Doares SH, Narváez-Vásquez J, Conconi A, Ryan CA (1995) Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol 108:1741–1746PubMedPubMedCentralCrossRefGoogle Scholar
  27. Domash VI, Sharpio TP, Zabreiko SA, Sosnovskaya TF (2008) Proteolytic enzymes and trypsin inhibitors of higher plants under stress conditions. Russ J Inorg Chem 34:318–322Google Scholar
  28. Dombrowski JE (2003) Sodium chloride stress activation of wound related genes in tomato plants. Plant Physiol 132:2098–2107PubMedPubMedCentralCrossRefGoogle Scholar
  29. Dunaevskii YE, Gladysheva IP, Pavlukova EB, Beliakova GA, Gladysheva DP, Papisova AI, Larionova NI, Belozersky MA (1997) The anionic protease inhibitor BBWI-I from buckwheat seeds—kinetic properties and possible biological role. Plant Physiol 100:483–488CrossRefGoogle Scholar
  30. Dunaevsky YE, Pavlukova EB, Beliakova GA, Tsybina TA, Gruban TN, Belozersky MA (1998) Protease inhibitors in buckwheat seeds: comparison of anionic and cationic inhibitors. J Plant Physiol 152:696–702CrossRefGoogle Scholar
  31. Dunse KM, Stevens JA, Lay FT, Gaspar YM, Heath RL, Anderson MA (2010) Coexpression of potato type I and II proteinase inhibitors gives cotton plants protection against insect damage in the field. Proc Natl Acad Sci USA 25:1–5Google Scholar
  32. Falco MC, Marbach PAS, Pompermayer P, Lopes FCC, Silva-Filho MC (2001) Mechanisms of sugarcane response to herbivory. Genet Mol Biol 24:113–122CrossRefGoogle Scholar
  33. Fan S, Wu G (2005) Characteristics of plant proteinase inhibitors and their applications in compating phytophagous insets. Bot Bull Acad Sin 46:273–292Google Scholar
  34. Fan X, Shi X, Zhao J, Zhao R, Fan Y (1999) Insecticidal activity of transgenic tobacco plants expressing both Bt and CpTI genes on cotton bollworm (Helicoverpa armigera). Chin J Biotechnol 15:1PubMedGoogle Scholar
  35. Farmer EE, Ryan CA (1990) Interplant communication: airborne methyl jasmonate induces synthesis of preoteinase inhibitors in plant leaves. Proc Natl Acad Sci USA 87:7713–7716PubMedPubMedCentralCrossRefGoogle Scholar
  36. Farmer EE, Johnson RR, Ryan CA (1992) Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic acid. Plant Physiol 98:995–1002PubMedPubMedCentralCrossRefGoogle Scholar
  37. Fischer M, Kuckenberg M, Kastilan R, Muth J, Gebhardt C (2015) Novel in vitro inhibitory functions of potato tuber proteinaceous inhibitors. Mol Genet Genom 290:387–398CrossRefGoogle Scholar
  38. Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LS, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876PubMedCrossRefGoogle Scholar
  39. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442PubMedCrossRefGoogle Scholar
  40. Fürstenberg-Hägg J, Zagrobelny M, Bak S (2013) Plant defense against insect herbivores. Int J Mol Sci 14:10242–10297PubMedPubMedCentralCrossRefGoogle Scholar
  41. Gaddour K, Vicente-Carbajosa J, Lara P, Isabel-Lamoneda I, Díaz I, Carbonero P (2001) A constitutive cystatin-encoding gene from barley (Icy) responds differentially to abiotic stimuli. Plant Mol Biol 45:599–608PubMedCrossRefGoogle Scholar
  42. Gadea J, Mayda ME, Conejero V, Vera P (1996) Characterization of defense-related genes ectopically expressed in viroid-infected tomato plants. Mol Plant Microb Interact 9(5):409–415CrossRefGoogle Scholar
  43. Galleschi L, Friggeri M, Repiccioli R, Come D (1993) Aspartic proteinase inhibitor from wheat: some properties. In: Proceedings of the fourth international workshop on seeds, Angers, France, pp 207–211Google Scholar
  44. Gatehouse AMR (1999) In: Clement SL, Quisenberry SS (eds) Global plant genetic resources for insect resistant crops. CRC Press, Boca RatonGoogle Scholar
  45. Gosti F, Bertauche N, Vartanian N, Giraudat J (1995) Abscisic acid-dependent and -independent regulation of gene expression by progressive drought in Arabidopsis thaliana. Mol Gen Genet 246:10–18PubMedCrossRefGoogle Scholar
  46. Graham JS, Pearce G, Merryweather J, Titani K, Ericsson L, Ryan CA (1985a) Wound-induced proteinase inhibitors from tomato leaves. I. The cDNA-deduced primary structure of pre-inhibitor I and its post-translational processing. J Biol Chem 260(11):6555–6560PubMedGoogle Scholar
  47. Graham JS, Pearce G, Merryweather J, Titani K, Ericsson LH, Ryan CA (1985b) Wound-induced proteinase inhibitors from tomato leaves. II. The cDNA-deduced primary structure of pre-inhibitor II. J Biol Chem 260:6561–6564PubMedGoogle Scholar
  48. Grativol C, Hemerly AS, Ferreira PC (2012) Genetic and epigenetic regulation of stress responses in natural plant populations. Biochim Biophys Acta 1819(2):176–185PubMedCrossRefGoogle Scholar
  49. Green T, Ryan C (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175:776–777PubMedCrossRefGoogle Scholar
  50. Grosse‐Holz FM, Hoorn RAL (2016) Juggling jobs: roles and mechanisms of multifunctional protease inhibitors in plants. New Phytol, pp 1–14Google Scholar
  51. Gruden K, Strukelj B, Ravnikar M, Poljsak-Prijatelj M (1997) Potato cysteine proteinase inhibitor gene family: molecular cloning, characterisation and immunocytochemical localisation studies. Plant Mol Biol 34:317–323PubMedCrossRefGoogle Scholar
  52. Guerra F, Duplessis S, Kohler A, Martin F, Tapia J, Lebed P, Zamudio F, González E (2009) Gene expression analysis of Populus deltoides roots subjected to copper stress. Environ Exp Bot 67:335–344CrossRefGoogle Scholar
  53. Guerra FP, Reyes L, Vergara-Jaque A, Campos-Hernández C, Gutiérrez A, Pérez-Díaz J, Pérez-Díaz R, Blaudez D, Ruíz-Lara S (2015) Populus deltoides Kunitz trypsin inhibitor 3 confers metal tolerance and binds copper, revealing a new defensive role against heavy metal stress. Environ Exp Bot 115:28–37CrossRefGoogle Scholar
  54. Habib H, Fazili KM (2007) Plant protease inhibitors: a defense strategy in plants. Biotechnol Mol Biol Rev 2:068–085Google Scholar
  55. Haq SK, Atif SM, Khan RH (2004) Protein proteinase inhibitor genes in combat against insects, pests, and pathogens: natural and engineered phytoprotection. Arch Biochem Biophys 431:145–159PubMedCrossRefGoogle Scholar
  56. Hartl M, Giri AP, Kaur H, Baldwin IT (2010) Serine protease inhibitor specifically defend Solanum nigrum against generalist herbivores but do not influence plant growth and development. Plant Cell 22:4158–4175PubMedPubMedCentralCrossRefGoogle Scholar
  57. Heath RL, Barton PA, Simpson RJ, Reid GE, Lim G, Anderson MA (1995) Characterization of the protease processing sites in a multidomain proteinase inhibitor precursor from Nicotiana alata. Eur J Biochem 230:250–257PubMedCrossRefGoogle Scholar
  58. Heath RL, McDonald G, Christeller JT, Lee M, Bateman K, West J, Van Heeswijck R, Anderson MA (1997) Proteinase inhibitors from Nicotiana alata enhance plant resistance to insect pests. J Insect Physiol 43:833–842PubMedCrossRefGoogle Scholar
  59. Heibges A, Glaczinski H, Ballvora A, Salamini F, Gebhardt C (2003) Structural diversity and organization of three gene families for Kunitz-type enzyme inhibitors from potato tubers (Solanum tuberosum L.). Mol Genet Genom 269:526–534CrossRefGoogle Scholar
  60. Herde O, Atzorn R, Fisahn J, Wasternack C, Willmitzer L, Peña-Cortés H (1996) Localized wounding by heat initiates the accumulation of proteinase inhibitor II in abscisic acid-deficient plants by triggering jasmonic acid biosynthesis. Plant Physiol 112:853–860PubMedPubMedCentralCrossRefGoogle Scholar
  61. Hermosa MR, Turrà D, Fogliano V, Monte E, Lorito M (2006) Identification and characterization of potato protease inhibitors able to inhibit pathogenicity and growth of Botrytis cinerea. Physiol Mol Plant Pathol 68:138–148CrossRefGoogle Scholar
  62. Hilder VA, Gatehouse AMR, Sherman SE, Barker RF, Boulter D (1987) A novel mechanism of insect resistance engineered into tobacco. Nature 300:160–163CrossRefGoogle Scholar
  63. Holländer-Czytko H, Andersen JK, Ryan CA (1985) Vacuolar localization of wound-induced carboxypeptidase inhibitor in potato leaves. Plant Physiol 78:76–79PubMedPubMedCentralCrossRefGoogle Scholar
  64. Horn M, Patankar AG, Zavala JA, Wu J, Doleckova-Maresova L, Vujtechova M, Mares M, Baldwin IT (2005) Differential elicitation of two processing proteases controls the processing pattern of the trypsin proteinase inhibitor precursor in Nicotiana attenuata. Plant Physiol 139:375–388PubMedPubMedCentralCrossRefGoogle Scholar
  65. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587. doi: 10.1093/nar/gkm259 PubMedPubMedCentralCrossRefGoogle Scholar
  66. Huang Y, Xiao B, Xiong L (2007) Characterization of a stress responsive protease inhibitor gene with positive effect in improving drought resistance in rice. Planta 226:73–85PubMedCrossRefGoogle Scholar
  67. Hubbard KE, Siegel RS, Valerio G, Brandt B, Schroeder JI (2012) Abscisic acid and CO2 signalling via calcium sensitivity priming in guard cells, new CDPK mutant phenotypes and a method for improved resolution of stomatal stimulus-response analyses. Ann Bot 109:5–17PubMedCrossRefGoogle Scholar
  68. Jamal F, Pandey PK, Singh D, Khan MY (2013) Serine protease inhibitors in plants: nature’s arsenal crafted for insect predators. Phytochem Rev 12:1–34CrossRefGoogle Scholar
  69. Johnson R, Ryan CA (1990) Wound-inducible potato inhibitor II genes: enhancement of expression by sucrose. Plant Mol Biol 14:527–536PubMedCrossRefGoogle Scholar
  70. Johnson R, Narvaez J, An G, Ryan C (1989) Expression of proteinase inhibitors I and II in transgenic tobacco plants: effects on natural defense against Manduca sexta larvae. Proc Natl Acad Sci USA 86:9871–9875PubMedPubMedCentralCrossRefGoogle Scholar
  71. Joshi BN, Sainani MN, Bastawade KB, Deshpande VV, Gupta VS, Ranjekar PK (1999) Pearl millet cysteine protease inhibitor. Evidence for the presence of two distinct sites responsible for anti-fungal and anti-feedent activities. Eur J Biochem 265:556–563PubMedCrossRefGoogle Scholar
  72. Joshi RS, Tanpure RS, Singh RK, Gupta VS, Giri AP (2014) Resistance through inhibition: ectopic expression of serine protease inhibitor offers stress tolerance via delayed senescence in yeast cell. Biochem Biophys Res Commun 452:361–368PubMedCrossRefGoogle Scholar
  73. Katoch M, Rani S, Kumar S, Chahota RK (2014) plant protection with the use of protease inhibitors- a scientific review. Life Sci Leafl 53:1–21Google Scholar
  74. Keil M, Sanchez-Serrano J, Schell J, Willmitzer L (1986) Primary structure of a proteinase inhibitor II gene from potato (Solanum tuberosum). Nucleic Acid Res 14:5641–5650PubMedPubMedCentralCrossRefGoogle Scholar
  75. Keilova H, Tomasek V (1976) Isolation and some properties of cathepsin D inhibitor from potatoes. Collect Czech Chem Commun 41:489–497CrossRefGoogle Scholar
  76. Kernan A, Thornburg RW (1989) Auxin levels regulate the expression of a wound-inducible proteinase inhibitor II chloramphenicol acetyl transferase gene fusion in vitro and in vivo. Plant Physiol 9:73–78CrossRefGoogle Scholar
  77. Kidrič M, Kos J, Sabotič J (2014) Proteases and their endogenous inhibitors in the plant response to abiotic stress. Bot Serbica 38:139–158Google Scholar
  78. Kieffer P, Dommes J, Hoffmann L, Hausman JF, Renaut J (2008) Quantitative changes in protein expression of cadmium-exposed poplar plants. Proteomics 8:2514–2530PubMedCrossRefGoogle Scholar
  79. Kim S, Hong Y, An CS, Lee K (2001) Expression characteristics of serine proteinase inhibitor II under variable environmental stresses in hot pepper (Capsicum annuum L.). Plant Sci 161:27–33CrossRefGoogle Scholar
  80. Kim JY, Park SC, Kim MH, Lim HT, Park Y, Hahm KS (2005) Antimicrobial activity studies on a trypsin-chymotrypsin protease inhibitor obtained from potato. Biochem Biophys Res Commun 330:921–927PubMedCrossRefGoogle Scholar
  81. Koiwa H, Bressan RA, Hasegawa PM (1997) Regulation of protease inhibitors and plant defense. Trends Plant Sci 2:379–384CrossRefGoogle Scholar
  82. Konarev AV, Griffin J, Konechnaya GY, Shewry PR (2004) The distribution of serine proteinase inhibitors in seeds of the Asteridae. Phytochemistry 65:3003–3020PubMedCrossRefGoogle Scholar
  83. Kong L, Ranganathan S (2008) Tandem duplication, circular permutation, molecular adaptation: how Solanaceae resist pests via inhibitors. BMC Bioinform 9:S22CrossRefGoogle Scholar
  84. Kulkarni A, Rao M (2009) Differential elicitation of an aspartic protease inhibitor: regulation of endogenous protease and initial events in germination in seeds of Vigna radiate. Peptides 30:2118–2126PubMedCrossRefGoogle Scholar
  85. Kunitz M (1945) Crystallization of a trypsin inhibitor from soybean. Science 101:668–669PubMedCrossRefGoogle Scholar
  86. Larrieu A, Vernoux T (2016) Q&A: how does jasmonate signaling enable plants to adapt and survive? BMC Biol 14:79PubMedPubMedCentralCrossRefGoogle Scholar
  87. Lawrence PK, Koundal KR (2002) Plant protease inhibitors in control of phytophagous insects. Electron J Biotechnol 5:93–109CrossRefGoogle Scholar
  88. Lee JS, Brown WE, Graham JS, Pearce G, Fox EA, Dreher TW, Ahern KG, Pearson GD, Ryan CA (1986) Molecular characterization and phylogenetic studies of a wound-inducible proteinase inhibitor I gene in Lycopersicon species. Proc Natl Acad Sci USA 83:7277–7281PubMedPubMedCentralCrossRefGoogle Scholar
  89. Li XQ, Zhang T, Donnelly D (2011) Selective loss of cysteine residues and disulphide bonds in a potato proteinase inhibitor II family. PLoS ONE 6:e18615PubMedPubMedCentralCrossRefGoogle Scholar
  90. Liu J, Xia KF, Deng YG, Huang XL, Hu BL, Xu X, Xu ZF (2006) The nightshade proteinase inhibitor IIb gene is constitutively expressed in glandular trichomes. Plant Cell Physiol 47:1274–1284PubMedCrossRefGoogle Scholar
  91. Lopez F, Vansuyt G, Derancourt J, Fourcroy P, Casse-Delbart F (1994) Identifcation by 2D-page analysis of sodium chloride-stress induced proteins in radish (Raphanus sativus). Cell Mol Biol 40:85–90PubMedGoogle Scholar
  92. Lopez-Otin C, Bond JS (2008) Proteases: multifunctional enzymes in life and disease. J Biol Chem 283:30433–30437PubMedPubMedCentralCrossRefGoogle Scholar
  93. Lorito M, Broadway RM, Hayes CK, Woo SL, Noviello C, Williams DL, Harman GE (1994) Proteinase inhibitors from plants as a novel class of fungicides. Mol Plant Microbe Interact 7:525–527CrossRefGoogle Scholar
  94. Luo M, Wang Z, Li H, Xia KF, Cai Y, Xu ZF (2009) Overexpression of a Weed (Solanum americanum) Proteinase inhibitor in transgenic tobacco results in increased glandular trichome density and enhanced resistance to Helicoverpa armigera and Spodoptera litura. Int J Mol Sci 10:1896–1910PubMedPubMedCentralCrossRefGoogle Scholar
  95. Majeed A, Makhdoom R, Husnain T, Riazuddin S (2011) Assessment of potato proteinase inhibitor-II gene as an antifungal and insecticidal agent. Acta Agric Scand Sect B 61:92–96Google Scholar
  96. 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 146:888–903PubMedPubMedCentralCrossRefGoogle Scholar
  97. Malone M, Alarcon JJ (1995) Only xylem-borne factors can account for systemic wound signalling in the tomato plant. Planta 196:740–746CrossRefGoogle Scholar
  98. Martinez M, Diaz I (2008) The origin and evolution of plant cystatins and their target cysteine proteinases indicate a complex functional relationship. BMC Evol Biol 8:198PubMedPubMedCentralCrossRefGoogle Scholar
  99. Martinez M, Abraham Z, Gambardella M, Echaide M, Carbonero P, Diaz I (2005) The strawberry gene Cyf1 encodes a phytocystatin with antifungal properties. J Exp Bot 56:1821–1829PubMedCrossRefGoogle Scholar
  100. Massange-Sanchez JA, Palmeros-Suarez PA, Martinez-Gallardo NA, Castrillon-Arbelaez PA, Avilés-Arnaut H, Alatorre-Cobos F, Tiessen A, Délano-Frier JP (2015) The novel and taxonomically restricted Ah24 gene from grain amaranth (Amaranthus hypochondriacus) has a dual role in development and defense. Front Plant Sci 6:602PubMedPubMedCentralCrossRefGoogle Scholar
  101. Miller EA, Lee MCS, Atkinson AHO, Anderson MA (2000) Identification of a novel four-domain member of the proteinase inhibitor II family from the stigmas of Nicotiana alata. Plant Mol Biol 42:329–333PubMedCrossRefGoogle Scholar
  102. Mishra M, Mahajan N, Tamhane VA, Kulkarni MJ, Baldwin IT, Gupta VS, Giri AP (2012) Stress inducible proteinase inhibitor diversity in Capsicum annuum. BMC Plant Biol 12:217PubMedPubMedCentralCrossRefGoogle Scholar
  103. Mosolov VV, Loginova MD, Fedurkina NV, Benken II (1976) The biological significance of proteinase inhibitors in plants. Plant Sci Lett 7:77–80CrossRefGoogle Scholar
  104. Moura DS, Ryan CA (2001) Wound-inducible proteinase inhibitors in pepper. Differential regulation upon wounding, systemin and methyl jasmonate. Plant Physiol 126:289–298PubMedPubMedCentralCrossRefGoogle Scholar
  105. Munir F, Naqvi SMS, Mahmood T (2013) In vitro and in silico characterization of Solanum lycopersicum wound-inducible proteinase inhibitor-II gene. Turk J Biol 37:1–10Google Scholar
  106. Narvaez-Vasquez J, Orozco-Cardenas ML, Ryan CA (2007) Systemic wound signaling in tomato leaves is cooperatively regulated by systemin and hydroxyproline-rich glycopeptide signals. Plant Mol Biol 65:711–718PubMedCrossRefGoogle Scholar
  107. Narváez-Vásquez J, Franceschi VR, Ryan CA (1993) Proteinase-inhibitor synthesis in tomato plants: evidence for extracellular deposition in roots through the secretory pathway. Planta 189:257–266CrossRefGoogle Scholar
  108. 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 68–106CrossRefGoogle Scholar
  109. O’Donnell PJ, Calvert C, Atzorn R, Wasternack C, Leyser HMO, Bowles DJ (1996) Ethylene as a signal mediating the wound response of tomato plants. Science 274:1914–1917PubMedCrossRefGoogle Scholar
  110. Odeny DA, Stich B, Gebhardt C (2010) Physical organization of mixed protease inhibitor gene clusters, coordinated expression and association with resistance to late blight at the StKI locus on potato chromosome III. Plant Cell Env 33:2149–2161CrossRefGoogle Scholar
  111. Paiva PMG, Pontual EV, Coelho LCBB, Napoleão TH (2013) Protease inhibitors from plants: Biotechnological insights with emphasis on their effects on microbial pathogens. In: Méndez-Vilas A (ed) Microbial pathogens and strategies for combating them: science, technology and education. Formatex Research Center, Badajoz, pp k641–k649Google Scholar
  112. Pautot V, Holzer FM, Walling LL (1991) Differential expression of tomato proteinase inhibitor I and II genes during bacterial pathogen invasion and wounding. Mol Plant Microb Interact 4:284–292CrossRefGoogle Scholar
  113. Pearce G, Sy L, Russell C, Ryan CA, Hass GM (1982) Isolation and characterization from potato tubers of two polypeptide inhibitors of serine proteinases. Arch Biochem Biophys 213:456–462PubMedCrossRefGoogle Scholar
  114. Pearce G, Ryan CA, Liljegren D (1988) Proteinase inhibitor-I and inhibitor-II in fruit of wild tomato species—transient components of a mechanism for defense and seed dispersal. Planta 175:527–531PubMedCrossRefGoogle Scholar
  115. Pearce G, Strydom D, Johnson S, Ryan CA (1991) A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253:895–898PubMedCrossRefGoogle Scholar
  116. Pearce G, Johnson S, Ryan CA (1993a) Purification and characterization from tobacco (Nicotina tabacum) leaves of six small, wound-inducible, proteinase iso inhibitors of the potato inhibitor II family. Plant Physol 102:639–644CrossRefGoogle Scholar
  117. Pearce G, Johnson S, Ryan CA (1993b) Purification and characterization from tobacco (Nicotiana tabacum) leaves of six small, wound-inducible, proteinase isoinhibitors of the potato inhibitor II family. Plant Physiol 102:639–644PubMedPubMedCentralCrossRefGoogle Scholar
  118. Pekkarinen AI, Longstaff C, Jones BL (2007) Kinetics of the inhibition of Fusarium serine proteinases by barley (Hordeum vulgare L.) inhibitors. J Agric Food Chem 55:2736–2742. doi: 10.1021/jf0631777 PubMedCrossRefGoogle Scholar
  119. Peña-Cortés H, Albrecht T, Prat S, Weiler EW, Willmitzer L (1993) Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191:123–128CrossRefGoogle Scholar
  120. Peña-Cortés H, Fisahn J, Willmitzer L (1995) Signals involved in wound-induced proteinase inhibitor II gene expression in tomato and potato plants. Proc Natl Acad Sci USA 92:4106–4113PubMedPubMedCentralCrossRefGoogle Scholar
  121. Pernas M, Sanchez-Monge R, Salcedo G (2000) Biotic and abiotic stress can induce cystatin expression in chestnut. FEBS Lett 467:206–210PubMedCrossRefGoogle Scholar
  122. Plunkett G, Senear DF, Zuroske G, Ryan CA (1982) Proteinase inhibitors I and II from leaves of wounded tomato plants: purification and properties. Arch Biochem Biophys 213:463–472PubMedCrossRefGoogle Scholar
  123. Rawlings ND, Tolle DP, Barrett AJ (2004) Evolutionary families of peptidase inhibitors. Biochem J 378:705–716PubMedPubMedCentralCrossRefGoogle Scholar
  124. Rawlings ND, Morton FR, Kok CY, Kong J, Barrett AJ (2008) MEROPS: the peptidase database. Nucleic Acid Res 34:D320–D325Google Scholar
  125. Rawlings ND, Barrett AJ, Bateman A (2010) MEROPS: the peptidase database. Nucleic Acid Res 38:D227–D233PubMedCrossRefGoogle Scholar
  126. Rawlings ND, Barrett AJ, Bateman A (2012) MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acid Res 40:343–350CrossRefGoogle Scholar
  127. Rehman S, Mahmood T (2015) Functional role of DREB and ERF transcription factors: regulating stress-responsive network in plants. Acta Physiol Plant 37:178CrossRefGoogle Scholar
  128. Rejeb IB, Pastor V, Mauch-Mani B (2014) Plant responses to simultaneous biotic and abiotic stress: molecular mechanisms. Plants 3:458–475PubMedPubMedCentralCrossRefGoogle Scholar
  129. Richardson M (1977) The protease inhibitors of plants and micro- organisms. Phytochemistry 16:159–169CrossRefGoogle Scholar
  130. Richardson M (1979) The complete amino acid sequence and the trypsin reactive (inhibitory) site of the major proteinase inhibitor from the fruits of aubergine (Solanum melongena L.). FEBS Lett 104:322–326PubMedCrossRefGoogle Scholar
  131. Rickauer M, Fournier J, Esquerre-Tugaye MT (1989) Induction of proteinase inhibitors in tobacco cell suspension culture by elicitors of Phytophthora parasitica var. nicotianae. Plant Physiol 90:1065–1070PubMedPubMedCentralCrossRefGoogle Scholar
  132. Rosahl S, Feussner I (2005) Oxylipins. In: Murphy DJ (ed) Plant lipids: biology, utilization, and manipulation. Blackwell Publishing, Oxford, pp 329–354Google Scholar
  133. Roszkowska-Jakimiec W, Bankowska A (1998) Cathepsin D inhibitor from Vicia sativa L. Rocz Akad Med Bialymst 43:245–249PubMedGoogle Scholar
  134. Ryan CA (1990) Protease inhibitors in plants: genes for improving defenses against insect and pathogens. Annu Rev Phytopathol 28:425–449CrossRefGoogle Scholar
  135. Ryan CA (1992) The search for proteinase inhibitor inducing factor, PIIF. Plant Mol Biol 19:123–133PubMedCrossRefGoogle Scholar
  136. Ryan CA (2000) The systemin-signaling pathway: differential activation of plant defensive genes. Biochim Biophys Acta 1477:112–121PubMedCrossRefGoogle Scholar
  137. Santamaria ME, Diaz-Mendoza M, Diaz I, Martinez M (2014) Plant protein peptidase inhibitors: an evolutionary overview based on comparative genomics. BMC Genom 15:812–826CrossRefGoogle Scholar
  138. Sasaki Y, Asamizu E, Shibata D, Nakamura Y, Kaneko T, Awai K, Amagai M, Kuwata C, Tsugane T, Masuda T, Shimada H, Takamiya K, Ohta H, Tabata S (2001) Monitoring of methyl jasmonate-responsive genes in Arabidopsis by cDNA macroarray: self-activation of jasmonic acid biosynthesis and crosstalk with other phytohormone signaling pathways. DNA Res 8:153–161PubMedCrossRefGoogle Scholar
  139. Scalschi L, Sanmartin M, Camanes G, Troncho P, Sanchez-Serrano JJ, Garcia-Agustin P, Vicedo B (2015) Silencing of OPR3 in tomato reveals the role of OPDA in callose deposition during the activation of defense responses against Botrytis cinerea. Plant J 81:304–315PubMedCrossRefGoogle Scholar
  140. Schirra HJ, Craik DJ (2005) Structure and folding of potato type II proteinase inhibitors: circular permutation and intramolecular domain swapping. Protein Pept Lett 12(5):421–431PubMedCrossRefGoogle Scholar
  141. Selitrennikoff CP (2001) Antifungal proteins. Appl Environ Microbiol 67:2883–2894PubMedPubMedCentralCrossRefGoogle Scholar
  142. Shewry PR (2003) Tuber storage proteins. Ann Bot 91:755–769PubMedPubMedCentralCrossRefGoogle Scholar
  143. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227PubMedCrossRefGoogle Scholar
  144. Sin SF, Chye ML (2004) Expression of proteinase inhibitor II proteins during floral development in Solanum americanum. Planta 219:1010–1022PubMedCrossRefGoogle Scholar
  145. Sin SF, Yeung EC, Chye ML (2006) Downregulation of Solanum americanum genes encoding proteinase inhibitor II causes defective seed development. Plant J 45(1):58–70PubMedCrossRefGoogle Scholar
  146. Snowden KC, Richards KD, Gardner RC (1995) Aluminum-induced genes (induction by toxic metals, low calcium, and wounding and pattern of expression in root tips). Plant Physiol 107:341–348PubMedPubMedCentralCrossRefGoogle Scholar
  147. Soares-Costa A, Beltramini L, Thieman O, Henrique- Silva F (2002) A sugarcane cystatin: recombinant expression, purification, and antifungal activity. Biochem Biophys Res Commun 296:1194–1199PubMedCrossRefGoogle Scholar
  148. Srinivasan T, Kumar KR, Kirti PB (2009) Constitutive expression of a trypsin protease inhibitor confers multiple stress tolerance in transgenic tobacco. Plant Cell Physiol 50(3):541–553PubMedCrossRefGoogle Scholar
  149. Stiekema WJ, Heidekamp F, Dirkse WG, van Beckum J, de Haan P, ten Bosch C, Louwerse JD (1988) Molecular cloning and analysis of four potato tuber mRNAs. Plant Mol Biol 11:255–269PubMedCrossRefGoogle Scholar
  150. Sun JQ, Jiang HL, Li CY (2011) Systemin/Jasmonate-mediated systemic defense signaling in tomato. Mol Plant 4:607–615PubMedCrossRefGoogle Scholar
  151. Tamhane VA, Giri AP, Sainani MN, Gupta VS (2007) Diverse forms of Pin-II family proteinase inhibitors from Capsicum annuum adversely affect the growth and development of Helicoverpa armigera. Gene 403:29–38PubMedCrossRefGoogle Scholar
  152. Tamhane VA, Giri AP, Kumar P, Gupta VS (2009) Spatial and temporal expression patterns of diverse Pin-II proteinase inhibitor genes in Capsicum annuum Linn. Gene 442:88–98PubMedCrossRefGoogle Scholar
  153. Tamhane VA, Mishra M, Mahajan NS, Gupta VS, Giri AP (2012) Plant PinII family proteinase inhibitor: structural and functional diversity. Funct Plant Sci Biotechnol 6:42–58Google Scholar
  154. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acid Res 22:4673–4680PubMedPubMedCentralCrossRefGoogle Scholar
  155. Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14:S153–S164PubMedPubMedCentralGoogle Scholar
  156. Valueva TA, Revina TA, Kladnitskaya GV, Mosolov VV (1998) Kuntz-type proteinase inhibitors from intact and Phytophthora infected potato tubers. FEBS Lett 426:131–134PubMedCrossRefGoogle Scholar
  157. Valueva TA, Revina TA, Gvozdeva EL, Gerasimova NG, Ozeretskovskaya OL (2003) Role of proteinase inhibitors in potato protection. Russ J Bioorg Chem 29:454–458CrossRefGoogle Scholar
  158. Vanjildorj E, Song SY, Yang ZH, Choi JE, Noh YS, Park S, Lim WJ, Cho KM, Yun HD, Lim YP (2009) Enhancement of tolerance to soft rot disease in the transgenic Chinese cabbage (Brassica rapa L. ssp. pekinensis) inbred line, Kenshin. Plant Cell Rep 28:1581–1591PubMedCrossRefGoogle Scholar
  159. Verma V, Ravindran P, Kumar PP (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biol 16:86PubMedPubMedCentralCrossRefGoogle Scholar
  160. War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7(10):1306–1320PubMedPubMedCentralCrossRefGoogle Scholar
  161. Wasternack C, Parthier B (1997) Jasmonate-signalled plant gene expression. Trend Plant Sci 2:302–307CrossRefGoogle Scholar
  162. Werner R, Guitton MC, Muhlbach HP (1993) Nucleotide sequence of a cathepsin D inhibitor protein from tomato. Plant Physiol 103:1473PubMedPubMedCentralCrossRefGoogle Scholar
  163. Wildon DC, Thain JF, Minchin PEH, Gubb IR, Reilly AJ, Skipper YD, Doherty HM, O’Donnell PJ, Bowles DJ (1992) Electrical signaling and systemic proteinase inhibitor induction in the wounded plant. Nature 360:62–65CrossRefGoogle Scholar
  164. Wingate VPM, Franceschi VR, Ryan CA (1991) Tissue and cellular localization of proteinase inhibitors I and II in the fruit of the wild tomato, Lycopersicon peruvianum (L.) Mill. Plant Physiol 97:490–495PubMedPubMedCentralCrossRefGoogle Scholar
  165. Xie J, Ouyang XZ, Xia KF, Huang YF, Pan WB, Cai YP, Xu X, Li B, Xu ZF (2007) Chloroplast-like organelles were found in enucleate sieve elements of transgenic plants overexpressing a proteinase inhibitor. Biosci Biotech Biochem 71:2759–2765CrossRefGoogle Scholar
  166. Xu ZF, Qi WQ, Ouyang XZ, Yeung E, Chye ML (2001) A proteinase inhibitor II of Solanum americanum is expressed in phloem. Plant Mol Biol 47:727–738PubMedCrossRefGoogle Scholar
  167. Ye XY, Ng TB, Rao PF (2001) A Bowman–Birk-type trypsinchymotrypsin inhibitor from broad beans. Biochem Biophys Res Commun 289:91–96PubMedCrossRefGoogle Scholar
  168. Young RJ, Scheuring CF, Harris-Haller L, Taylor BH (1994) An auxin-inducible proteinase inhibitor gene from tomato. Plant Physiol 104:811–812PubMedPubMedCentralCrossRefGoogle Scholar
  169. Yu CS, Chen YC, Lu CH, Hwang JK (2006) Prediction of protein subcellular localization. Protein Struct Funct Bioinform 64:643–651CrossRefGoogle Scholar
  170. Zavala JA, Patankar AG, Gase K, Hui D, Baldwin IT (2004) Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses. Plant Physiol 134:1181–1190PubMedPubMedCentralCrossRefGoogle Scholar
  171. Zhang HY, Xie XZ, Xu YZ, Wu NH (2004) Isolation and functional assessment of a tomato proteinase inhibitor II gene. Plant Physiol Biochem 42:437–444PubMedCrossRefGoogle Scholar
  172. Zhang J, Liu F, Yao L, Luo C, Yin Y, Wang G, Huang Y (2012) Development and bioassay of transgenic Chinese cabbage expressing potato proteinase inhibitor II gene. Breed Sci 62:105–112PubMedPubMedCentralCrossRefGoogle Scholar
  173. Zhu YC, Abel CA, Chen MS (2007) Interaction of Cry1Ac toxin (Bacillus thuringiensis) and proteinase inhibitors on the growth, development and midgut proteinase activities of the bollworm, Helicoverpa zea. Pestic Biochem Physiol 87:39–46CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • Shazia Rehman
    • 1
  • Ejaz Aziz
    • 1
  • Wasim Akhtar
    • 2
  • Muhammad Ilyas
    • 1
  • Tariq Mahmood
    • 1
  1. 1.Department of Plant SciencesQuaid-i-Azam UniversityIslamabadPakistan
  2. 2.Department of BiotechnologyUniversity of Azad Jammu and KashmirMuzaffarabadPakistan

Personalised recommendations