Plant Serine Protease Inhibitors: Biotechnology Application in Agriculture and Molecular Farming
<p>Mechanisms of protease-inhibitor interactions. (<b>A</b>) Irreversible “trapping” reactions. The protease–inhibitor interaction induces the cleavage of an internal peptide bond in the inhibitor triggering a conformational change. This reaction is not reversible, and the inhibitor never recovers its initial structure. For this reason, the inhibitors that participate in trapping reactions are also known as suicide inhibitors. The inhibitors never recover the initial structure. (<b>B</b>) Reversible tight-binding interactions. The inhibitor interacts with the protease active site in a similar way to the enzyme-substrate interaction. The protease-inhibitor complex co-exists in a stable equilibrium among the intact form of the inhibitor and the modified forms of the inhibitor where the peptide bond of the reactive site is cleaved. Therefore, the inhibitor in the complex is dissociated to its intact or its modified form. P1: PI reactive site; RL: reactive loop.</p> "> Figure 2
<p>Serine proteases inhibitors identified in plants (endogenous SPIs) or in other organisms (exogenous SPIs) can be introduced by conventional transformation (<span class="html-italic">Agrobacterium tumefaciens</span> or gene gun transformation) or by novel editing technologies to increase the resistance to insect pest and phytopathogenic microorganisms. The application of these technologies can be used to produce new resistant sources of important crops.</p> "> Figure 3
<p>Co-expression of serine protease inhibitors could help to minimize the proteolytic activity and to avoid the recombinant protein degradation in transplastomic, transgenic plants or in plants that transiently express recombinant proteins. The protease inhibitor can be targeted in the same organelle (chloroplast transformation) where the recombinant protein would be expressed or co-expressed. Transgenic plants over-expressing protease inhibitors would be more suitable to express recombinant proteins by agroinfiltration.</p> ">
Abstract
:1. Introduction
2. Classification of Protease Inhibitors
3. Mechanisms of Inhibition of Protease Inhibitors
4. Plant Serine Protease Inhibitors (SPIs)
5. SPI as Protein Defense in Plants
6. Plant SPIs: Biotechnology Application in Agriculture
7. Challenges and Perspectives in Pathogen Resistance
8. Plant SPIs: Biotechnology Application in Molecular Farming
9. Challenges and Perspectives in Preventing Proteolysis in Plant Protein Factories
10. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Santamaría, M.E.; Diaz-Mendoza, M.; Diaz, I.; Martinez, M. Plant protein peptidase inhibitors: An evolutionary overview based on comparative genomics. BMC Genom. 2014, 15, 812. [Google Scholar] [CrossRef] [PubMed]
- Ivanov, D.; Emonet, C.; Foata, F.; Affolter, M.; Delley, M.; Fisseha, M.; Blum-Sperisen, S.; Kochhar, S.; Arigoni, F. A serpin from the gut bacterium Bifidobacterium longum inhibits eukaryotic elastase-like serine proteases. J. Biol. Chem. 2006, 281, 17246–17252. [Google Scholar] [CrossRef] [PubMed]
- Rawlings, N.D.; Tolle, D.P.; Barrett, A.J. Evolutionary families of peptidase inhibitors. Biochem. J. 2004, 378, 705–716. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Qi, R.F.; Song, Z.W.; Chi, C.W. Structural features and molecular evolution of Bowman-Birk protease inhibitors and their potential application. Acta Biochim. Biophys. Sin. (Shanghai) 2005, 37, 283–292. [Google Scholar] [CrossRef] [PubMed]
- Bitoun, E.; Chavanas, S.; Irvine, A.D.; Lonie, L.; Bodemer, C.; Paradisi, M.; Hamel-Teillac, D.; Ansai, S.; Mitsuhashi, Y.; Taïeb, A.; et al. Netherton syndrome: Disease expression and spectrum of SPINK5 mutations in 21 families. J. Investig. Dermatol. 2002, 118, 352–361. [Google Scholar] [CrossRef] [PubMed]
- Lomas, D.A.; Lourbakos, A.; Cumming, S.A.; Belorgey, D. Hypersensitive mousetraps, alpha1-antitrypsin deficiency and dementia. Biochem. Soc. Trans. 2002, 30, 89–92. [Google Scholar] [CrossRef] [PubMed]
- Ritchie, B.C. Protease inhibitors in the treatment of hereditary angioedema. Transfus. Apher. Sci. 2003, 29, 259–267. [Google Scholar] [CrossRef] [PubMed]
- Ryan, C.A. Protease inhibitor in plants: Genes for improving defenses against insects and pathogens. Ann. Rev. Phytopathol. 1990, 28, 425–449. [Google Scholar] [CrossRef]
- Lawrence, P.K.; Koundal, K.R. Plant protease inhibitors in control of phytophagous insects. Electron. J. Biotechnol. 2002, 5, 93–109. [Google Scholar] [CrossRef]
- Haq, S.K.; Atif, S.M.; Khan, R.H. Protein proteinase inhibitor genes in combat against insects, pests, and pathogens: Natural and engineered phytoprotection. Arch. Biochem. Biophys. 2004, 431, 145–159. [Google Scholar] [CrossRef] [PubMed]
- Schaller, A. A cut above the rest: The regulatory function of plant proteases. Planta 2004, 220, 183–197. [Google Scholar] [CrossRef] [PubMed]
- Valueva, T.A.; Mosolov, V.V. Role of inhibitors of proteolytic enzymes in plant defense against phytopathogenic microorganisms. Biochemistry (Moscow) 2004, 69, 1305–1309. [Google Scholar] [CrossRef] [PubMed]
- Van der Hoorn, R.A.; Jones, J.D. The plant proteolytic machinery and its role in defence. Curr. Opin. Plant Biol. 2004, 7, 400–407. [Google Scholar] [CrossRef] [PubMed]
- Mosolov, V.V.; Valueva, T.A. Proteinase Inhibitors and Their Function in Plants: A Review. Appl. Biochem. Microbiol. 2005, 41, 227–246. [Google Scholar] [CrossRef]
- Salas, C.E.; Gomes, M.T.; Hernandez, M.; Lopes, M.T. Plant cysteine proteinases: Evaluation of the pharmacological activity. Phytochemistry 2008, 69, 2263–2269. [Google Scholar] [CrossRef] [PubMed]
- Santamaria, M.E.; Cambra, I.; Martinez, M.; Pozancos, C.; González-Melendi, P.; Grbic, V.; Castañera, P.; Ortego, F.; Diaz, I. Gene pyramiding of peptidase inhibitors enhances plant resistance to the spider mite Tetranychus urticae. PLoS ONE 2012, 7, e43011. [Google Scholar] [CrossRef] [PubMed]
- Horger, A.C.; van der Hoorn, R.A. The structural basis of specific protease-inhibitor interactions at the plant-pathogen interface. Curr. Opin. Struct. Biol. 2013, 23, 842–850. [Google Scholar] [CrossRef] [PubMed]
- Volpicella, M.; Leoni, C.; Costanza, A.; De Leo, F.; Gallerani, R.; Ceci, L.R. Cystatins, serpins and other families of protease inhibitors in plants. Curr. Protein Pept. Sci. 2011, 12, 386–398. [Google Scholar] [CrossRef] [PubMed]
- Laskowski, M.; Kato, I. Protein inhibitors of proteinases. Annu. Rev. Biochem. 1980, 49, 593–626. [Google Scholar] [CrossRef] [PubMed]
- Birk, Y. Plant Protease Inhibitors: Plant Protease Inhibitors: Significance in Nutrition, Plant Protection, Cancer Prevention, and Genetic Engineering; Springer: Berlin/Heidelberg, Germany, 2003; pp. 1–170. [Google Scholar]
- Rustgi, S.; Boex-Fontvieille, E.; Reinbothe, C.; von Wettstein, D.; Reinbothe, S. The complex world of plant protease inhibitors: Insights into a Kunitz-type cysteine protease inhibitor of Arabidopsis thaliana. Commun. Integr. Biol. 2018, 11, e1368599. [Google Scholar] [CrossRef] [PubMed]
- Chothia, C.; Lesk, A.M. The relation between the divergence of sequence and structure in proteins. EMBO J. 1986, 5, 823–826. [Google Scholar] [CrossRef] [PubMed]
- Rawlings, N.D. Peptidase inhibitors in the MEROPS database. Biochimie 2010, 92, 1463–1483. [Google Scholar] [CrossRef] [PubMed]
- Rawlings, N.D.; Barrett, A.J.; Finn, R. Twenty years of the MEROPS database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res. 2016, 44, 343–350. [Google Scholar] [CrossRef] [PubMed]
- Rawlings, N.D.; Barrett, A.J.; Thomas, P.D.; Huang, X.; Bateman, A.; Finn, R.D. The MEROPS database of proteolytic enzymes, their substrates and inhibitors in 2017 and a comparison with peptidases in the PANTHER database. Nucleic Acids Res. 2018, 46, 624–632. [Google Scholar] [CrossRef] [PubMed]
- Bateman, K.S.; James, M.N. Plant protein proteinase inhibitors: Structure and mechanism of inhibition. Curr. Protein Pept. Sci. 2011, 12, 340–347. [Google Scholar] [CrossRef] [PubMed]
- Joshi, R.S.; Mishra, M.; Suresh, C.G.; Gupta, V.S.; Giri, A.P. Complementation of intramolecular interactions for structural-functional stability of plant serine proteinase inhibitors. Biochim. Biophys. Acta 2013, 1830, 5087–5094. [Google Scholar] [CrossRef] [PubMed]
- Laskowski, M.; Qasim, M.A. What can the structures of enzyme-inhibitor complexes tell us about the structures of enzyme substrate complexes? Biochim. Biophys. Acta 2000, 1477, 324–337. [Google Scholar] [CrossRef]
- Farady, C.J.; Craik, C.S. Mechanisms of macromolecular protease inhibitors. ChemBioChem 2010, 11, 2341–2346. [Google Scholar] [CrossRef] [PubMed]
- Richardson, M. Seed storage proteins: The enzyme inhibitors. In Methods in Plant Biochemistry; Rogers, L.J., Ed.; Academic Press: New York, NY, USA, 1991; Volume 5, pp. 259–305. [Google Scholar]
- Srikanth, S.; Chen, Z. Plant Protease Inhibitors in Therapeutics-Focus on Cancer Therapy. Front. Pharmacol. 2016, 7, 470. [Google Scholar] [CrossRef] [PubMed]
- De Leo, F.; Volpicella, M.; Licciulli, F.; Liuni, S.; Gallerani, R.; Ceci, L.R. PLANT-PIs: A database for plant protease inhibitors and their genes. Nucleic Acids Res. 2002, 30, 347–348. [Google Scholar] [CrossRef] [PubMed]
- Grosse-Holz, F.M.; van der Hoorn, R.A. Juggling jobs: Roles and mechanisms of multifunctional protease inhibitors in plants. New Phytol. 2016, 210, 794–807. [Google Scholar] [CrossRef] [PubMed]
- Antao, C.M.; Malcata, F.X. Plant serine proteases: Biochemical, physiological and molecular features. Plant Physiol. Biochem. 2005, 43, 637–650. [Google Scholar] [CrossRef] [PubMed]
- Roberts, T.H.; Hejgaard, J. Serpins in plants and green algae. Funct. Integr. Genom. 2008, 8, 1–27. [Google Scholar] [CrossRef] [PubMed]
- Jamal, F.; Pandey, P.K.; Singh, D.; Khan, M.Y. Serine protease inhibitors in plants: Nature’s arsenal crafted for insect predators. Phytochem. Rev. 2013, 12, 1–34. [Google Scholar] [CrossRef]
- Silverstein, K.A.; Moskal, W.A., Jr.; Wu, H.C.; Underwood, B.A.; Graham, M.A.; Town, C.D.; VandenBosch, K.A. Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants. Plant J. 2007, 51, 262–280. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martinez, M.; Cambra, I.; González-Melendi, P.; Santamaría, M.E.; Díaz, I. C1A cysteine-proteases and their inhibitors in plants. Physiol. Plant. 2012, 145, 85–94. [Google Scholar] [CrossRef] [PubMed]
- Pak, C.; van Doorn, W.G. Delay of Iris flower senescence by protease inhibitors. New Phytol. 2005, 165, 473–480. [Google Scholar] [CrossRef] [PubMed]
- Joshi, R.S.; Tanpure, R.S.; Singh, R.K.; Gupta, V.S.; Giri, A.P. Resistance through inhibition: Ectopic expression of serine protease inhibitor offers stress tolerance via delayed senescence in yeast cell. Biochem. Biophys. Res. Commun. 2014, 452, 361–368. [Google Scholar] [CrossRef] [PubMed]
- Diaz, I.; Santamaria, M.E. Biotechnological approaches to combat phytophagous arthropods. In Arthropod-Plant Interactions: Novel Insights and Approaches for IPM; Smagghe, G., Diaz, I., Eds.; Springer: Amsterdam, The Netherlands, 2012; Volume 14, pp. 159–176. [Google Scholar]
- Arnaiz, A.; Talavera-Mateo, L.; Gonzalez-Melendi, P.; Martinez, M.; Diaz, I.; Santamaria, M.E. Arabidopsis Kunitz Trypsin Inhibitors in Defense Against Spider Mites. Front. Plant Sci. 2018, 9, 986. [Google Scholar] [CrossRef] [PubMed]
- Fluhr, R.; Lampl, N.; Roberts, T.H. Serpin protease inhibitors in plant biology. Physiol. Plant. 2012, 145, 95–102. [Google Scholar] [CrossRef] [PubMed]
- Bendre, A.D.; Ramasamy, S.; Suresh, C.G. Analysis of Kunitz inhibitors from plants for comprehensive structural and functional insights. Int. J. Biol. Macromol. 2018, 113, 933–943. [Google Scholar] [CrossRef] [PubMed]
- Roberts, T.H.; Ahn, J.W.; Lampl, N.; Fluhr, R. Plants and the study of serpin biology. Methods Enzymol. 2011, 499, 347–366. [Google Scholar] [PubMed]
- Savelkoul, F.H.; van der Poel, A.F.; Tamminga, S. The presence and inactivation of trypsin inhibitors, tannins, lectins and amylase inhibitors in legume seeds during germination. A review. Plant Foods Hum. Nutr. 1992, 42, 71–85. [Google Scholar] [CrossRef] [PubMed]
- Rustgi, S.; Boex-Fontvieille, E.; Reinbothe, C.; von Wettstein, D.; Reinbothe, S. Serpin1 and WSCP differentially regulate the activity of the cysteine protease RD21 during plant development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2017, 114, 2212–2217. [Google Scholar] [CrossRef] [PubMed]
- Boex-Fontvieille, E.; Rustgi, S.; Reinbothe, S.; Reinbothe, C. A Kunitz-type protease inhibitor regulates programmed cell death during flower development in Arabidopsis thaliana. J. Exp. Bot. 2015, 66, 6119–6135. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.Y.; Park, S.C.; Hwang, I.; Cheong, H.; Nah, J.W.; Hahm, K.S.; Park, Y. Protease inhibitors from plants with antimicrobial activity. Int. J. Mol. Sci. 2009, 10, 2860–2872. [Google Scholar] [CrossRef] [PubMed]
- Roy-Downing, W.L.; Mauxion, F.; Fauvarque, M.O.; Reviron, M.P.; de Vienne, D.; Vartanian, N.; Giraudat, J. A Brassica napus transcript encoding a protein related to the Künitz protease inhibitor family accumulates upon water stress in leaves, not in seeds. Plant J. 1992, 2, 685–693. [Google Scholar]
- Srinivasan, T.; Kumar, K.R.; Kirti, P.B. Constitutive expression of a trypsin protease inhibitor confers multiple stress tolerance in transgenic tobacco. Plant Cell Physiol. 2009, 50, 541–553. [Google Scholar] [CrossRef] [PubMed]
- Dramé, K.N.; Passaquet, C.; Repellin, A.; Zuily-Fodil, Y. Cloning, characterization and differential expression of a Bowman-Birk inhibitor during progressive water deficit and subsequent recovery in peanut (Arachis hypogaea) leaves. J. Plant Physiol. 2013, 170, 225–229. [Google Scholar] [CrossRef] [PubMed]
- Jones, J.D.; Dangl, J.L. The plant immune system. Nature 2006, 444, 323–329. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Spoel, S.H.; Dong, X. How do plants achieve immunity? Defence without specialized immune cells. Nat. Rev. Immunol. 2012, 12, 89–100. [Google Scholar] [CrossRef] [PubMed]
- Khadeeva, N.V.; Kochieva, E.Z.; Tcherednitchenko, M.Y.; Yakovleva, E.Y.; Sydoruk, K.V.; Bogush, V.G.; Dunaevsky, Y.E.; Belozersky, M.A. Use of buckwheat seed protease inhibitor gene for improvement of tobacco and potato plant resistance to biotic stress. Biochemistry (Mosc) 2009, 74, 260–267. [Google Scholar] [CrossRef] [PubMed]
- Katagiri, F.; Tsuda, K. Understanding the plant immune system. Mol. Plant Microbe Interact. 2010, 23, 1531–1536. [Google Scholar] [CrossRef] [PubMed]
- Schwessinger, B.; Zipfel, C. News from the frontline: Recent insights into PAMP-triggered immunity in plants. Curr. Opin. Plant Biol. 2008, 11, 389–395. [Google Scholar] [CrossRef] [PubMed]
- Kalashnikova, E.E.; Chernyshova, M.P.; Ignatov, V.V. The extracellular proteases of the phytopathogenic bacterium Xanthomonas campestris. Mikrobiologiia 2003, 72, 498–502. [Google Scholar] [PubMed]
- Cheng, Z.; Li, J.F.; Niu, Y.; Zhang, X.C.; Woody, O.Z.; Xiong, Y.; Djonović, S.; Millet, Y.; Bush, J.; McConkey, B.J.; et al. Pathogen-secreted proteases activate a novel plant immune pathway. Nature 2015, 521, 213–216. [Google Scholar] [CrossRef] [PubMed]
- Habib, H.; Fazili, K.M. Plant protease inhibitors: A defense strategy in plants. Biotechnol. Mol. Biol. Rev. 2007, 2, 68–85. [Google Scholar]
- Gatehouse, A.M.; Norton, E.; Davison, G.M.; Babbé, S.M.; Newell, C.A.; Gatehouse, J.A. Digestive proteolytic activity in larvae of tomato moth, Lacanobia oleracea; effects of plant protease inhibitors in vitro and in vivo. J. Insect Physiol. 1999, 45, 545–558. [Google Scholar] [CrossRef]
- van der Hoorn, R.A.L. Plant Proteases: From Phenotypes to Molecular Mechanisms. Annu. Rev. Plant Biol. 2008, 59, 191–223. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jashni, M.K.; Mehrabi, R.; Collemare, J.; Mesarich, C.H.; de Wit, P.J. The battle in the apoplast: Further insights into the roles of proteases and their inhibitors in plant-pathogen interactions. Front. Plant Sci. 2015, 6, 584. [Google Scholar] [CrossRef] [PubMed]
- Halitschke, R.; Baldwin, I.T. Antisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata. Plant J. 2003, 36, 794–807. [Google Scholar] [CrossRef] [PubMed]
- Boex-Fontvieille, E.; Rustgi, S.; Von Wettstein, D.; Pollmann, S.; Reinbothe, S.; Reinbothe, C. Jasmonic acid protects etiolated seedlings of Arabidopsis thaliana against herbivorous arthropods. Plant Signal. Behav. 2016, 11, e1214349. [Google Scholar] [CrossRef] [PubMed]
- Farmer, E.E.; Ryan, C.A. Interplant communication: Airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc. Natl. Acad. Sci. USA 1990, 87, 7713–7716. [Google Scholar] [CrossRef] [PubMed]
- Howe, G.A.; Jander, G. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 2008, 59, 41–66. [Google Scholar] [CrossRef] [PubMed]
- Turra, D.; Bellin, D.; Lorito, M.; Gebhardt, C. Genotype-dependent expression of specific members of potato protease inhibitor gene families in different tissues and in response to wounding and nematode infection. J. Plant Physiol. 2009, 166, 762–774. [Google Scholar] [CrossRef] [PubMed]
- Qu, L.J.; Chen, J.; Liu, M.; Pan, N.; Okamoto, H.; Lin, Z.; Li, C.; Li, D.; Wang, J.; Zhu, G.; et al. Molecular cloning and functional analysis of a novel type of Bowman-Birk inhibitor gene family in rice. Plant Physiol. 2003, 133, 560–570. [Google Scholar] [CrossRef] [PubMed]
- Birk, Y. Protein proteinase inhibitors in legume seeds—Overview. Arch. Latinoam. Nutr. 1996, 44, 26–30. [Google Scholar]
- Pouvreau, L.; Gruppen, H.; Piersma, S.R.; van den Broek, L.A.; van Koningsveld, G.A.; Voragen, A.G. Relative abundance and inhibitory distribution of protease inhibitors in potato juice from cv. Elkana. J. Agric. Food Chem. 2001, 49, 2864–2874. [Google Scholar] [CrossRef] [PubMed]
- Christeller, J.; Laing, W. Plant serine proteinase inhibitors. Protein Pept. Lett. 2005, 12, 439–447. [Google Scholar] [CrossRef] [PubMed]
- Yoo, B.C.; Aoki, K.; Xiang, Y.; Campbell, L.R.; Hull, R.J.; Xoconostle-Cázares, B.; Monzer, J.; Lee, J.Y.; Ullman, D.E.; Lucas, W.J. Characterization of cucurbita maxima phloem serpin-1 (CmPS-1). A developmentally regulated elastase inhibitor. J. Biol. Chem. 2000, 275, 35122–35128. [Google Scholar] [CrossRef] [PubMed]
- La Cour Petersen, M.; Hejgaard, J.; Thompson, G.A.; Schulz, A. Cucurbit phloem serpins are graft-transmissible and appear to be resistant to turnover in the sieve element-companion cell complex. J. Exp. Bot. 2005, 56, 3111–3120. [Google Scholar] [CrossRef] [PubMed]
- Zhu, Y.; Wang, Y.; Gorman, M.J.; Jiang, H.; Kanost, M.R. Manduca sexta serpin-3 regulates prophenoloxidase activation in response to infection by inhibiting prophenoloxidase-activating proteinases. J. Biol. Chem. 2003, 278, 46556–46564. [Google Scholar] [CrossRef] [PubMed]
- Hilder, V.A.; Gatehouse, M.R.; Boulter, D. Transgene plants conferring insect tolerance: Protease inhibitor approach. Transgenic Plants 1993, 1, 317–338. [Google Scholar]
- Baldwin, I.T.; Schultz, J.C. Rapid changes in tree leaf chemistry induced by damage: Evidence for communication between plants. Science 1983, 221, 277–279. [Google Scholar] [CrossRef] [PubMed]
- Lingling, L.; Lei, J.; Song, M.; Li, L.; Cao, B. Study on transformation of cowpea trypsin inhibitor gene into cauli flower (Brassica oleracea L. var. botrytis). Afr. J. Biotechnol. 2005, 4, 45–49. [Google Scholar]
- Pujol, M.; Hernandez, C.A.; Armas, R.; Coll, Y.; Alfonso-Rubi, J.; Perez, M.; Ayra, C.; González, A. Inhibition of Heliothis virescens larvae growth in transgenic tobacco plants expressing cowpea trypsin inhibitor. Biotechnol. Appl. 2005, 22, 27–130. [Google Scholar]
- Quilis, J.; Meynard, D.; Vila, L.; Aviles, F.X.; Guiderdoni, E.; Segundo, B.S. A potato carboxypeptidase inhibitor gene provides pathogen resistance in transgenic rice. Plant Biotechnol. J. 2007, 5, 537–553. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Quilis, J.; López-García, B.; Meynard, D.; Guiderdoni, E.; San Segundo, B. Inducible expression of a fusion gene encoding two proteinase inhibitors leads to insect and pathogen resistance in transgenic rice. Plant Biotechnol. J. 2014, 12, 367–377. [Google Scholar] [CrossRef] [PubMed]
- Down, R.E.; Ford, L.; Mosson, H.J.; Fitches, E.; Gatehouse, J.A.; Gatehouse, A.M. Protease activity in the larval stage of the parasitoid wasp, Eulophus pennicornis (Nees) (Hymenoptera: Eulophidae); effects of protease inhibitors. Parasitology 1999, 119, 157–166. [Google Scholar] [CrossRef] [PubMed]
- Azzouz, H.; Cherqui, A.; Campan, E.D.; Rahbé, Y.; Duport, G.; Jouanin, L.; Kaiser, L.; Giordanengo, P. Effects of plant protease inhibitors, oryzacystatin I and soybean Bowman-Birk inhibitor, on the aphid Macrosiphum euphorbiae (Homoptera, Aphididae) and its parasitoid Aphelinus abdominalis (Hymenoptera, Aphelinidae). J. Insect Physiol. 2005, 51, 75–86. [Google Scholar] [CrossRef] [PubMed]
- Williamson, V.M.; Hussey, R.S. Nematode pathogenesis and resistance in plants. Plant Cell 1996, 8, 1735–1745. [Google Scholar] [CrossRef] [PubMed]
- Sharma, H.C.; Sharma, K.K.; Seetharama, N.; Ortiz, R. Prospects for using transgenic resistance to insects in crop improvement. Electron. J. Biotechnol. 2000, 3, 21–22. [Google Scholar] [CrossRef]
- Major, I.T.; Constabel, C.P. Functional analysis of the Kunitz trypsin inhibitor family in poplar reveals biochemical diversity and multiplicity in defense against herbivores. Plant Physiol. 2008, 146, 888–903. [Google Scholar] [CrossRef] [PubMed]
- Botelho-Junior, S.; Machado, O.L.; Fernandes, K.V.; Lemos, F.J.; Perdizio, V.A.; Oliveira, A.E.; Monteiro, L.R.; Filho, M.L.; Jacinto, T. Defense response in non-genomic model species: Methyl jasmonate exposure reveals the passion fruit leaves’ ability to assemble a cocktail of functionally diversified Kunitz-type trypsin inhibitors and recruit two of them against papain. Planta 2014, 240, 345–356. [Google Scholar] [CrossRef] [PubMed]
- Migliolo, L.; de Oliveira, A.S.; Santos, E.A.; Franco, O.L.; de Sales, M.P. Structural and mechanistic insights into a novel non-competitive Kunitz trypsin inhibitor from Adenanthera pavonina L. seeds with double activity toward serine- and cysteine-proteinases. J. Mol. Graph. Model. 2010, 29, 148–156. [Google Scholar] [CrossRef] [PubMed]
- da Silva, D.S.; de Oliveira, C.F.; Parra, J.R.; Marangoni, S.; Macedo, M.L. Short and long-term antinutritional effect of the trypsin inhibitor ApTI for biological control of sugarcane borer. J. Insect Physiol. 2014, 61, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Valueva, T.A.; Revina, T.A.; Gvozdeva, E.L.; Gerasimova, N.G.; Il’inskaia, L.I.; Ozeretskovakaia, O.L. Effect of elicitors on accumulation of protease inhibitors in injured potato tubers. Prikl. Biokhim. Mikrobiol. 2001, 37, 601–606. [Google Scholar] [PubMed]
- Laluk, K.; Mengiste, T. The Arabidopsis extracellular unusual serine proteinase inhibitor functions in resistance to necrotrophic fungi and insect herbivory. Plant J. 2011, 68, 480–494. [Google Scholar] [CrossRef] [PubMed]
- Smigocki, A.C.; Ivic-Haymes, S.; Li, H.; Savić, J. Pest protection conferred by a Beta vulgaris serine proteinase inhibitor gene. PLoS ONE 2013, 8, e57303. [Google Scholar] [CrossRef] [PubMed]
- Hilder, V.A.; Gatehouse, A.M.R.; Sheerman, S.E.; Barker, R.F.; Boulter, D. A novel mechanism of insect resistance engineered into tobacco. Nature 1987, 330, 160–163. [Google Scholar] [CrossRef]
- Altpeter, F.; Diaz, I.; McAuslane, H.; Gaddour, K.; Carbonero, P.; Vasil, I.K. Increased insect resistance in transgenic wheat stably expressing trypsin inhibitor CMe. Mol. Breed. 1999, 5, 53–63. [Google Scholar] [CrossRef]
- Lee, I.; Lee, S.H.; Koo, C.; Jin, C.H.; Lim, C.O.; Mun, H.; Han, S.Y.; Cho, J. Soybean Kunitz trypsin inhibitor (SKTI) confers resistance to the brown planthopper Nilaparvata lugens Stal in transgenic rice. Mol. Breed. 1999, 5, 1–9. [Google Scholar] [CrossRef]
- Vila, L.; Quilis, J.; Meynard, D.; Breitler, J.C.; Marfa, V.; Murillo, I.; Vassal, J.M.; Messeguer, J.; Guiderdoni, E.; San Segundo, B. Expression of the maize proteinase inhibitor (mpi) gene in rice plants enhances resistance against the striped stem borer (Chilo suppressalis): Effects on larval growth and insect gut proteinases. Plant Biotechnol. J. 2005, 3, 187–202. [Google Scholar] [CrossRef] [PubMed]
- Dunse, K.M.; Stevens, J.A.; Lay, F.T.; Gaspar, Y.M.; Heath, R.L.; Anderson, M.A. Coexpression of potato type I and II proteinase inhibitors gives cotton plants protection against insect damage in the field. Proc. Natl. Acad. Sci. USA 2010, 107, 15011–15015. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hartl, M.; Giri, A.P.; Kaur, H.; Baldwin, I.T. Serine protease inhibitors specifically defend Solanum nigrum against generalist herbivores but do not influence plant growth and development. Plant Cell 2010, 22, 4158–4175. [Google Scholar] [CrossRef] [PubMed]
- Gatehouse, J.A. Prospects for using proteinase inhibitors to protect transgenic plants against attack by herbivorous insects. Curr. Protein Pept. Sci. 2011, 12, 409–416. [Google Scholar] [CrossRef] [PubMed]
- Luo, M.; Ding, L.W.; Ge, Z.J.; Wang, Z.Y.; Hu, B.L.; Yang, X.B.; Sun, Q.Y.; Xu, Z.F. The Characterization of SaPIN2b, a Plant Trichome-Localized Proteinase Inhibitor from Solanum americanum. Int. J. Mol. Sci. 2012, 13, 15162–15176. [Google Scholar] [CrossRef] [PubMed]
- Alfonso-Rubí, J.; Ortego, F.; Castañera, P.; Carbonero, P.; Díaz, I. Transgenic expression of trypsin inhibitor CMe from barley in indica and japonica rice, confers resistance to the rice weevil Sitophilus oryzae. Transgenic Res. 2003, 12, 23–31. [Google Scholar] [CrossRef] [PubMed]
- Hamza, R.; Pérez-Hedo, M.; Urbaneja, A.; Rambla, J.L.; Granell, A.; Gaddour, K.; Beltrán, J.P.; Cañas, L.A. Expression of two barley proteinase inhibitors in tomato promotes endogenous defensive response and enhances resistance to Tuta absoluta. BMC Plant Biol. 2018, 18, 24. [Google Scholar] [CrossRef] [PubMed]
- Stuiver, M.H.; Custers, J.H. Engineering disease resistance in plants. Nature 2001, 411, 865–868. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dunaevsky, Y.E.; Gladysheva, I.P.; Pavlukova, E.B.; Beliakova, G.A.; Gladyshev, D.P.; Papisova, A.I.; Larionova, N.I.; Belozersky, M.A. The anionic protease inhibitor BWI-1 from buckwheat seeds. Kinetic properties and possible biological role. Physiol. Plant. 1997, 101, 483–488. [Google Scholar] [CrossRef]
- Valueva, T.A.; Revina, T.A.; Kladnitskaya, G.V.; Mosolov, V.V. Kunitz-type proteinase inhibitors from intact and Phytophthora-infected potato tubers. FEBS Lett. 1998, 426, 131–134. [Google Scholar] [CrossRef]
- Ye, X.Y.; Ng, T.B.; Rao, P.F. A Bowman-Birk-type trypsin-chymotrypsin inhibitor from broad beans. Biochem. Biophys. Res. Commun. 2001, 289, 91–96. [Google Scholar] [CrossRef] [PubMed]
- Pekkarinen, A.I.; Longstaff, C.; Jones, B.L. Kinetics of the inhibition of fusarium serine proteinases by barley (Hordeum vulgare L.) inhibitors. J. Agric. Food Chem. 2007, 55, 2736–2742. [Google Scholar] [CrossRef] [PubMed]
- Pariani, S.; Contreras, M.; Rossi, F.R.; Sander, V.; Corigliano, M.G.; Simón, F.; Busi, M.V.; Gomez-Casati, D.F.; Pieckenstain, F.L.; Duschak, V.G.; et al. Characterization of a novel Kazal-type serine proteinase inhibitor of Arabidopsis thaliana. Biochimie 2016, 123, 85–94. [Google Scholar] [CrossRef] [PubMed]
- Castilho, A.; Windwarder, M.; Gattinger, P.; Mach, L.; Strasser, R.; Altmann, F.; Steinkellner, H. Proteolytic and N-glycan processing of human α1-antitrypsin expressed in Nicotiana benthamiana. Plant Physiol. 2014, 166, 1839–1851. [Google Scholar] [CrossRef] [PubMed]
- Goulet, C.; Khalf, M.; Sainsbury, F.; D’Aoust, M.A.; Michaud, D. A protease activity-depleted environment for heterologous proteins migrating towards the leaf cell apoplast. Plant Biotechnol. J. 2012, 10, 83–94. [Google Scholar] [CrossRef] [PubMed]
- Robert, S.; Khalf, M.; Goulet, M.C.; D’Aoust, M.A.; Sainsbury, F.; Michaud, D. Protection of recombinant mammalian antibodies from development-dependent proteolysis in leaves of Nicotiana benthamiana. PLoS ONE 2013, 8, e70203. [Google Scholar] [CrossRef] [PubMed]
- Grosse-Holz, F.; Madeira, L.; Zahid, M.A.; Songer, M.; Kourelis, J.; Fesenko, M.; Ninck, S.; Kaschani, F.; Kaiser, M.; van der Hoorn, R.A.L. Three unrelated protease inhibitors enhance accumulation of pharmaceutical recombinant proteins in Nicotiana benthamiana. Plant Biotechnol. J. 2018, 16, 1797–1810. [Google Scholar] [CrossRef] [PubMed]
- Komarnytsky, S.; Borisjuk, N.; Yakoby, N.; Garvey, A.; Raskin, I. Cosecretion of protease inhibitor stabilizes antibodies produced by plant roots. Plant Physiol. 2006, 141, 1185–1193. [Google Scholar] [CrossRef] [PubMed]
- Kim, T.G.; Kim, H.M.; Lee, H.J.; Shin, Y.J.; Kwon, T.H.; Lee, N.J.; Jang, Y.S.; Yang, M.S. Reduced protease activity in transformed rice cell suspension cultures expressing a proteinase inhibitor. Protein Expr. Purif. 2007, 53, 270–274. [Google Scholar] [CrossRef] [PubMed]
- Boulter, D. Insect pest control by copying nature using genetically engineered crops. Phytochemistry 1993, 34, 1453–1466. [Google Scholar] [CrossRef]
- Urwin, P.E.; McPherson, M.J.; Atkinson, H.J. Enhanced transgenic plant resistance to nematodes by dual proteinase inhibitor constructs. Planta 1998, 204, 472–479. [Google Scholar] [CrossRef] [PubMed]
- Alvarez-Alfageme, F.; Maharramov, J.; Carrillo, L.; Vandenabeele, S.; Vercammen, D.; Van Breusegem, F.; Smagghe, G. Potential use of a serpin from Arabidopsis for pest control. PLoS ONE 2011, 6, e20278. [Google Scholar] [CrossRef]
- Ferry, N.; Edwards, M.G.; Gatehouse, J.; Capell, T.; Christou, P.; Gatehouse, A.M.R. Transgenic plants for insect pest control: A forward looking scientific perspective. Transgenic Res. 2006, 15, 13–19. [Google Scholar] [CrossRef] [PubMed]
- Jongsma, M.A.; Bakker, P.L.; Peters, J.; Bosch, D.; Stiekema, W.J. Adaptation of Spodoptera exigua larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition. Proc. Natl. Acad. Sci. USA 1995, 92, 8041–8045. [Google Scholar] [CrossRef] [PubMed]
- Cloutier, C.; Jean, C.; Fournier, M.; Yelle, S.; Michaud, D. Adult Colorado potato beetles, Leptinotarsa decemlineata compensate for nutritional stress on oryzacystatin I-transgenic potato plants by hypertrophic behavior and over-production of insensitive proteases. Arch. Insect Biochem. Physiol. 2000, 44, 69–81. [Google Scholar] [CrossRef]
- Harsulkar, A.M.; Giri, A.P.; Patankar, A.G.; Gupta, V.S.; Sainani, M.N.; Ranjekar, P.K.; Deshpande, V.V. Successive use of non-host plant proteinase inhibitors required for effective inhibition of Helicoverpa armigera gut proteinases and larval growth. Plant Physiol. 1999, 121, 497–506. [Google Scholar] [CrossRef] [PubMed]
- Martínez-Trujillo, M.; Simpson, J.; Herrera-Estrella, L.R. Transgenic plants in modern agriculture. J. New Seeds 2002, 4, 1–23. [Google Scholar] [CrossRef]
- Ahmad, P.; Ashraf, M.; Younis, M.; Hu, X.; Kumar, A.; Akram, N.A.; Al-Qurainy, F. Role of transgenic plants in agriculture and biopharming. Biotechnol. Adv. 2012, 30, 524–540. [Google Scholar] [CrossRef] [PubMed]
- Nejat, N.; Rookes, J.; Mantri, N.L.; Cahill, D.M. Plant-pathogen interactions: Toward development of next-generation disease-resistant plants. Crit. Rev. Biotechnol. 2017, 37, 229–237. [Google Scholar] [CrossRef] [PubMed]
- Hiatt, A.; Cafferkey, R.; Bowdish, K. Production of antibodies in transgenic plants. Nature 1989, 342, 76–78. [Google Scholar] [CrossRef] [PubMed]
- Hood, E.E.; Witcher, D.R.; Maddock, S.; Meyer, T.; Baszczynski, C.; Bailey, M.; Flynn, P.; Register, J.; Marshall, L.; Bond, D.; et al. Commercial production of avidin from transgenic maize: Characterization of transformant, production, processing, extraction and purification. Mol. Breed. 1997, 3, 291–306. [Google Scholar] [CrossRef]
- Hood, E.E.; Howard, J.A. Commercial plant-produced recombinant avidin. In Commercial Plant-Produced Recombinant Protein Products; Howard, J.A., Hood, E.E., Eds.; Springer: Berlin/Heidelberg, Germany, 2014; Volume 68, pp. 15–25. [Google Scholar]
- Webster, D.E.; Thomas, M.C. Post-translational modification of plant-made foreign proteins; glycosylation and beyond. Biotechnol. Adv. 2012, 30, 410–418. [Google Scholar] [CrossRef] [PubMed]
- Yao, J.; Weng, Y.; Dickey, A.; Wang, K.Y. Plants as Factories for Human Pharmaceuticals: Applications and Challenges. Int. J. Mol. Sci. 2015, 16, 28549–28565. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tschofen, M.; Knopp, D.; Hood, E.; Stoger, E. Plant molecular farming: Much more than medicines. Annu. Rev. Anal. Chem. (Palo Alto Calif) 2016, 9, 271–294. [Google Scholar] [CrossRef] [PubMed]
- Twyman, R.M.; Schillberg, S.; Fischer, R. Optimizing the yield of recombinant pharmaceutical proteins in plants. Curr. Pharm. Des. 2013, 19, 5486–5494. [Google Scholar] [CrossRef] [PubMed]
- Stoger, E.; Fischer, R.; Moloney, M.; Ma, J.K. Plant molecular pharming for the treatment of chronic and infectious diseases. Annu. Rev. Plant Biol. 2014, 65, 743–768. [Google Scholar] [CrossRef] [PubMed]
- Mandal, M.K.; Ahvari, H.; Schillberg, S.; Schiermeyer, A. Tackling unwanted proteolysis in plant production hosts used for molecular farming. Front. Plant Sci. 2016, 7, 267. [Google Scholar] [CrossRef] [PubMed]
- Doran, P.M. Foreign protein degradation and instability in plants and plant tissue cultures. Trends Biotechnol. 2006, 24, 426–432. [Google Scholar] [CrossRef] [PubMed]
- Pillay, P.; Schlüter, U.; van Wyk, S.; Kunert, K.J.; Vorster, B.J. Proteolysis of recombinant proteins in bioengineered plant cells. Bioengineered 2014, 5, 15–20. [Google Scholar] [CrossRef] [PubMed]
- Pillay, P.; Kibido, T.; du Plessis, M.; van der Vyver, C.; Beyene, G.; Vorster, B.J.; Kunert, K.J.; Schlüter, U. Use of transgenic oryzacystatin-I-expressing plants enhances recombinant protein production. Appl. Biochem. Biotechnol. 2012, 168, 1608–1620. [Google Scholar] [CrossRef] [PubMed]
- Faye, L.; Boulaflous, A.; Benchabane, M.; Gomord, V.; Michaud, D. Protein modifications in the plant secretory pathway: Current status and practical implications in molecular pharming. Vaccine 2005, 23, 1770–1778. [Google Scholar] [CrossRef] [PubMed]
- Rivard, D.; Anguenot, R.; Brunelle, F.; Le, V.Q.; Vézina, L.P.; Trépanier, S.; Michaud, D. An in-built proteinase inhibitor system for the protection of recombinant proteins recovered from transgenic plants. Plant Biotechnol. J. 2006, 4, 359–368. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Benchabane, M.; Goulet, C.; Rivard, D.; Faye, L.; Gomord, V.; Michaud, D. Preventing unintended proteolysis in plant protein biofactories. Plant Biotechnol. J. 2008, 6, 633–648. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hein, M.B.; Tang, Y.; McLeod, D.A.; Janda, K.D.; Hiatt, A. Evaluation of immunoglobulins from plant cells. Biotechnol. Prog. 1991, 7, 455–461. [Google Scholar] [CrossRef] [PubMed]
- De Wilde, C.; De Rycke, R.; Beeckman, T.; De Neve, M.; Van Montagu, M.; Engler, G.; Depicker, A. Accumulation pattern of IgG antibodies and Fab fragments in transgenic Arabidopsis thaliana plants. Plant Cell Physiol. 1998, 39, 639–646. [Google Scholar] [CrossRef] [PubMed]
- Beyene, G.; Foyer, C.H.; Kunert, K.J. Two new cysteine proteinases with specific expression patterns in mature and senescent tobacco (Nicotiana tabacum L.) leaves. J. Exp. Bot. 2006, 57, 1431–1443. [Google Scholar] [CrossRef] [PubMed]
- Goulet, C.; Benchabane, M.; Anguenot, R.; Brunelle, F.; Khalf, M.; Michaud, D. A companion protease inhibitor for the protection of cytosol-targeted recombinant proteins in plants. Plant Biotechnol. J. 2010, 8, 142–154. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Van der Vyver, C.; Schneidereit, J.; Driscoll, S.; Turner, J.; Kunert, K.; Foyer, C.H. Oryzacystatin I expression in transformed tobacco produces a conditional growth phenotype and enhances chilling tolerance. Plant Biotechnol. J. 2003, 1, 101–112. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pagny, S.; Denmat-Ouisse, L.A.; Gomord, V.; Faye, L. Fusion with HDEL protects cell wall invertase from early degradation when N-glycosylation is inhibited. Plant Cell Physiol. 2003, 44, 173–182. [Google Scholar] [CrossRef] [PubMed]
- Pimpl, P.; Taylor, J.P.; Snowden, C.; Hillmer, S.; Robinson, D.G.; Denecke, J. Golgi-mediated vacuolar sorting of the endoplasmic reticulum chaperone BiP may play an active role in quality control within the secretory pathway. Plant Cell 2006, 18, 198–211. [Google Scholar] [CrossRef] [PubMed]
- Laguia-Becher, M.; Martín, V.; Kraemer, M.; Corigliano, M.; Yacono, M.L.; Goldman, A.; Clemente, M. Effect of codon optimization and subcellular targeting on Toxoplasma gondii antigen SAG1 expression in tobacco leaves to use in subcutaneous and oral immunization in mice. BMC Biotechnol. 2010, 10, 52. [Google Scholar] [CrossRef] [PubMed]
- Hehle, V.K.; Paul, M.J.; Drake, P.M.; Ma, J.K.; van Dolleweerd, C.J. Antibody degradation in tobacco plants: A predominantly apoplastic process. BMC Biotechnol. 2011, 11, 128. [Google Scholar] [CrossRef] [PubMed]
- Di Cola, A.; Frigerio, L.; Lord, J.M.; Roberts, L.M.; Ceriotti, A. Endoplasmic reticulum-associated degradation of ricin A chain has unique and plant-specific features. Plant Physiol. 2005, 137, 287–296. [Google Scholar] [CrossRef] [PubMed]
- Jha, S.; Agarwal, S.; Sanyal, I.; Jain, G.K.; Amla, D.V. Differential subcellular targeting of recombinant human α₁-proteinase inhibitor influences yield, biological activity and in planta stability of the protein in transgenic tomato plants. Plant Sci. 2012, 196, 53–66. [Google Scholar] [CrossRef] [PubMed]
- Pillay, P.; Kunert, K.J.; van Wyk, S.G.; Makgopa, M.E.; Cullis, C.A.; Vorster, B.J. Agroinfiltration contributes to VP1 recombinant protein degradation. Bioengineered 2016, 7, 459–477. [Google Scholar] [CrossRef] [PubMed]
- Stoger, E.; Sack, M.; Nicholson, L.; Fischer, R.; Christou, P. Recent progress in plantibody technology. Curr. Pharm. Des. 2005, 11, 2439–2457. [Google Scholar] [CrossRef] [PubMed]
- Delannoy, M.; Alves, G.; Vertommen, D.; Ma, J.; Boutry, M.; Navarre, C. Identification of peptidases in Nicotiana tabacum leaf intercellular fluid. Proteomics 2008, 8, 2285–2298. [Google Scholar] [CrossRef] [PubMed]
- Santos, R.B.; Chandrasekar, B.; Mandal, M.K.; Kaschani, F.; Kaiser, M.; Both, L.; van der Hoorn, R.A.L.; Schiermeyer, A.; Abranches, R. Low Protease Content in Medicago truncatula Cell Cultures Facilitates Recombinant Protein Production. Biotechnol. J. 2018, 13, e1800050. [Google Scholar] [CrossRef] [PubMed]
SPI Name | Origen | Role and Function | Biotechnology Application | References |
---|---|---|---|---|
A. thaliana Kunitz trypsin inhibitors (AtKTI4, AtKTI5) | Arabidopsis thaliana | Inhibitory activity against serine and cysteine protease; effect on mite performance (fecundity and mortality) | Protection against spider mite | [42] |
AtSerpin1 | Arabidopsis thaliana | Inhibition of digestive protease activity; inhibition of larval growth; inhibition of RD21 activity | Protection against insect disease | [47,103] |
Kunitz type protease inhibitor (AtWSCP) | Arabidopsis thaliana | Inhibition of cysteine RD21 activity; controlling cell death | Protection against herbivore attack | [45,47] |
Potato type 1 inhibitors | Solanum tuberosum | Differential expression pattern after wounding and nematode infection | Protection against nematodes | [68] |
Bowman-Birk-type inhibitor | Oryza sativa | Arrest fungal invasion; inhibition of fungal growth | Protection against fungal disease | [69] |
Phloem serpin-1 (CmPS-1) | Cucurbita maxima | Inhibition of elastase activity; increase of the aphid mortality | Protection against insect disease | [73,74] |
Cowpea trypsin inhibitor gene (CPTI) | Vigna unguiculata | Inhibition of larval growth | Protection against insect disease | [78,79,93] |
Potato carboxypeptidase inhibitor (PCI) | Solanum tuberosum | Antifungal activity; inhibition of larval growth | Protection against fungal and insect disease | [80,81] |
Maize proteinase inhibitor (mPI) | Zea mays | Inhibition of digestive serine proteinases; inhibition of larval and fungal growth | Protection against fungal and insect disease | [81,96] |
Soybean Kunitz inhibitor (SKTI) | Glycine max | Inhibition of digestive proteases present in insects and parasites | Protection against parasitic and insect disease | [83,86,95] |
Soybean Bowman-Birk inhibitor (SbBBI) | Glycine max | Inhibition of digestive protease activity; inhibition of aphid growth | Protection against aphid parasitoids | [83] |
Poplar Kunitz trypsin inhibitor | Populus trichocarpa x Populus deltoides | Inhibition of midgut protease present in lepidopteran pests | Protection against insect disease | [86] |
Passion fruit Kunitz type inhibitors (PfKI) | Passiflora edulis Sims | Inhibition of midgut proteases present in lepidopteran and coleopteran pests and Aedes aegypti | Protection against insect disease and Control of vectors of neglected tropical diseases | [87] |
Kunitz trypsin inhibitor (ApKTI) | Adenanthera pavonina | Inhibitory activity against trypsin and papain proteases; inhibition of midgut proteases and larval growth | Protection against insect disease | [88,89] |
Unusual serine protease inhibitor (UPI) | Arabidopsis thaliana | Chymotrypsin inhibitory activity; effect on the fungal and larval growth | Protection against fungal and insect disease | [91] |
Serine proteinase inhibitor (BvSTI) | Beta vulgaris | Trypsin inhibitor activity; effect on larval weights | Protection against lepidopteran insect disease | [92] |
Serine protease inhibitor CMe (BTI-CMe) | Barley (Hordeum vulgare) | Inhibition of midgut protease activity; effect on larval growth and survival of insects | Protection against insect disease | [94,101,102] |
Potato type I (StPin1A) inhibitor/Potato type II (NaPI) inhibitor | Solanum tuberosum Nicotiana alata | Protease inhibitory activity; effect on larval growth | Protection against Helicoverpa spp. | [97] |
PI-I and PI-II-class inhibitors | Solanum nigrum | Serine protease inhibitory activity | Protection against insect disease | [98] |
Potato Type II Proteinase Inhibitors (SaPIN2b) | Solanum americanum | Inhibition of midgut protease activity | Protection against insect disease | [97,100] |
Serine protease inhibitor (BWI-1a) | Fagopyrum sculentum | Inhibition of spore germination, mycelial growth, bacterial growth and survival of insects | Protection against insect, fungal and bacterial disease | [104,59] |
Serine protease inhibitors (PSPI-21, PSPI-22) | Solanum tuberosum | Trypsin and chymotrypsin inhibitory activity; inhibition of mycelial growth | Protection against fungal disease | [105] |
Bowman-Birk-type inhibitor | Vicia faba | Trypsin and chymotrypsin inhibitory activity; inhibition of mycelial growth | Protection against fungal disease | [106] |
Chymotrypsin/subtilisin inhibitor 2, amylase/subtilisin inhibitor, Bowman-Birk trypsin inhibitor | Hordeum vulgare | Inhibition of subtilisin and trypsin proteases of Fusarium culmorum | Protection against fungal disease | [107] |
Kazal type inhibitor (AtKPI-1) | Arabidopsis thaliana | Inhibition of conidial germination | Protection against fungal disease | [108] |
Tomato cathepsin D inhibitor (CDI) | Solanum tuberosum | Improvement of the stability of proteins in leaf crude extracts | Achieves high yields of recombinant proteins in the extraction/recovery process | [109,110,111,112] |
Bowman–Birk type protease inhibitor (BBI) | Glycine max | Reduction of the degradation of immunoglobulins in the secretion pathway | Achieves high yields of therapeutic proteins in transgenic plants | [113] |
Chymotrypsin and trypsin inhibitor | Nicotiana alata | Reduction of the extracellular protease activity | Achieves high yields of recombinant proteins in cell suspension culture | [114] |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Clemente, M.; Corigliano, M.G.; Pariani, S.A.; Sánchez-López, E.F.; Sander, V.A.; Ramos-Duarte, V.A. Plant Serine Protease Inhibitors: Biotechnology Application in Agriculture and Molecular Farming. Int. J. Mol. Sci. 2019, 20, 1345. https://doi.org/10.3390/ijms20061345
Clemente M, Corigliano MG, Pariani SA, Sánchez-López EF, Sander VA, Ramos-Duarte VA. Plant Serine Protease Inhibitors: Biotechnology Application in Agriculture and Molecular Farming. International Journal of Molecular Sciences. 2019; 20(6):1345. https://doi.org/10.3390/ijms20061345
Chicago/Turabian StyleClemente, Marina, Mariana G. Corigliano, Sebastián A. Pariani, Edwin F. Sánchez-López, Valeria A. Sander, and Víctor A. Ramos-Duarte. 2019. "Plant Serine Protease Inhibitors: Biotechnology Application in Agriculture and Molecular Farming" International Journal of Molecular Sciences 20, no. 6: 1345. https://doi.org/10.3390/ijms20061345