Skip to main content
Log in

Serine proteinase inhibitor proteins: Exogenous and endogenous functions

  • Published:
In Vitro Cellular & Developmental Biology - Plant Aims and scope Submit manuscript

Summary

Proteinase inhibitor II (PIN2) proteins from the Solanaceae family have been previously used in plant transformation to acquire protection against caterpillars. Some of these PIN2 proteins have been shown to exhibit exogenous activities against trypsin and/or chymotrypsin in vitro. Despite their application in conferring insect resistance in transgenic plants, the endogenous roles of this family of proteins in various plant species have not been well defined. To investigate the exogenous and endogenous functions of PIN2 proteins, cDNAs encoding PIN2 proteins from the weed Solanum americanum (American black nightshade), designated SaPIN2a and SaPIN2b, were cloned and characterized. The localization of S. americanum SaPIN2a and SaPIN2b mRNAs and proteins in the reproductive tissues destined to undergo developmental programmed cell death subsequently led to investigations into their function during seed development. Using plant transformation of lettuce and S. americanum, it was evident that: (1) the expression of SaPIN2a in transgenic lettuce conferred resistance to cabbage looper (Trichoplusia ni) caterpillars; and (2) the expression of siRNAs from a PIN2-RNAi construct resulted in transgenic S. americanum that were impaired in seed development. These results suggest that S. americanum PIN2 proteins not only enhance resistance to caterpillars (when expressed exogenously) but they function in inhibiting endogenous proteases that are expressed during seed development. Specifically, the aborted seeds of PIN2-RNAi lines showed abnormal endothelium that subsequently affected endosperm and embryo development.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Applebaum, S. W.; Konijn, A. M. The presence of a Tribolium-protease inhibitor in wheat. J. Insect. Physiol. 12:665–669; 1966.

    Article  CAS  Google Scholar 

  • Atkinson, A. H.; Heath, R. L.; Simpson, R. J.; Clarke, A. E.; Anderson, M. A. Proteinase inhibitors in Nicotiana alata stigmas are derived from a precursor protein which is processed into five homologous inhibitors. Plant Cell 5:203–213; 1993.

    Article  PubMed  CAS  Google Scholar 

  • Balandin, T.; van der Does, C.; Albert, J.-M. B.; Bol, J. F.; Linthorst, H. J. M. Structure and induction pattern of a novel proteinase inhibitor class II gene of tobacco. Plant Mol. Biol. 27:1197–1204; 1995.

    Article  PubMed  CAS  Google Scholar 

  • Barbour, J. D. Vegetable crops: search for arthropod resistance in genetic resources. In: Clement, S. L.; Quisenberry, S. S., eds. Global plant genetic resources for insect-resistant crops. Boca Raton, FL: CRC Press; 1999:171–189.

    Google Scholar 

  • Barrett, A. J.; Rawlings, N. D.; Woessner, J. F. Handbook of proteolytic enzymes. New York: Academic Press; 1998.

    Google Scholar 

  • Baumgartner, B.; Chrispeels, M. J. Partial characterization of a proteinase inhibitor which inhibits the major endopeptidases present in the cotyledons of mung beans. Plant Physiol. 58:1–6; 1976.

    PubMed  CAS  Google Scholar 

  • Birch, R. G. Plant transformation: problems and strategies for practical application. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:297–326; 1997.

    Article  PubMed  CAS  Google Scholar 

  • Birk, Y.; Gertler, A.; Khalef, S. Separation of a Tribolium-protease inhibitor from soybeans on a calcium phosphate column. Biochim. Biophys. Acta 67:326–328; 1963.

    Article  PubMed  CAS  Google Scholar 

  • Boesewinkel, F. D. Development of ovule and testa of Linum usitatissimum L. Acta Bot. Neerl. 29:17–32; 1980.

    Google Scholar 

  • Boesewinkel, F. D.; Bouman, F. The seed; structure In: Johri, B. M., ed. Embryology of angiosperms. Berlin, Heidelberg: Springer-Verlag; 1984:567–610.

    Google Scholar 

  • Botella, M. A.; Xu, Y.; Prabha, T. N.; Zhao Y.; Narasimhan, M. L.; Wilson, K. A.; Nielsen, S. S.; Bressan, R. A.; Hasegawa, P. M. Differential expression of soybean cysteine proteinase inhibitor genes during development and in response to wounding and methyl jasmonate. Plant Physiol. 112:1201–1210; 1996.

    Article  PubMed  CAS  Google Scholar 

  • Boulter, D.; Edwards, G. A.; Gatehouse, A. M. R.; Gatehouse, J. A.; Hilder, V. A. Additive protective effects of incorporating two different higher plant derived insect resistance genes in transgenic tobacco plants. Crop Prot. 9:351–354; 1990.

    Article  Google Scholar 

  • Bowman, D. E. Fractions derived from soybeans and navy beans which retard the tryptic digestion of casein. Proc. Soc. Exptl Biol. Med. 57:139–140; 1944.

    CAS  Google Scholar 

  • Brandstädter, J.; Roßbach, C.; Theres, K. Expression of genes for a defensin and a proteinase inhibitor in specific areas of the shoot apex and the developing flower in tomato. Mol. Gen. Genet. 252:146–154; 1996.

    Article  PubMed  Google Scholar 

  • Bryant, J.; Green, T. R.; Gurusaddaiah, T.; Ryan, C. A. Proteinase inhibitor II from potatoes: Isolation and characterization of its promoter components. Biochemistry 15:3418–3424; 1976.

    Article  PubMed  CAS  Google Scholar 

  • Brzin, J.; Kidric, M. Proteinases and their inhibitors in plants: role in normal growth and in response to various stress conditions. Biotechnol. Genet. Eng. Rev. 13:421–467; 1995.

    Google Scholar 

  • Charity, J. A.; Anderson, M. A.; Bittisnich, D. J.; Whitecross, M.; Higgins, T. J. V. Transgenic tobacco and peas expressing a proteinase inhibitor from Nicotiana alata have increased insect resistance. Mol. Breed. 5:357–365; 1999.

    Article  CAS  Google Scholar 

  • Chen, F.; Foolad, M. R. Molecular organization of a gene in barley which encodes a protein similar to aspartic protease and its specific expression in nucellar cells during degeneration. Plant Mol. Biol. 35:821–831; 1997.

    Article  PubMed  CAS  Google Scholar 

  • Choi, D.; Park, J. A.; Seo, Y. S.; Chun, Y. J.; Kim, W.T. Structure and stress-related expression of two cDNAs encoding proteinase inhibitor II of Nicotiana glutinosa L. Biochim. Biophys. Acta 1492:211–215; 2000.

    PubMed  CAS  Google Scholar 

  • Cleveland, T. E.; Thornburg, R. W.; Ryan, C. A. Molecular characterization of a wound-inducible Inhibitor I gene from potato and the processing of its mRNA and protein. Plant Mol. Biol. 8:199–207; 1987.

    Article  CAS  Google Scholar 

  • Colombo, L.; Franken, J.; Van der Krol, A. R.; Wittich, P. E.; Dons, H. J. M.; Angenent, G. C. Downregulation of ovule-specific MADS box genes from Petunia results in maternally controlled defects in seed development. Plant Cell 9:703–715; 1997.

    Article  PubMed  CAS  Google Scholar 

  • Cordero, M. J.; Raventos, D.; Segundo, B. S. Expression of a maize proteinase inhibitor gene is induced in response to wounding and fungal infection: systemic wound-response of a monocot gene. Plant J. 6:141–150; 1994.

    Article  PubMed  CAS  Google Scholar 

  • Costa, L. M.; Gutièrrez-Marcos, J. F.; Dickinson, H. G. More than a yolk: the short life and complex times of the plant endosperm. Trends Plant Sci. 9:507–514; 2004.

    Article  PubMed  CAS  Google Scholar 

  • Curtis, I. S.; Power, J. B.; Blackhall, N. W.; de Laat, A. M. M.; Davey, M. R. Genotype-independent transformation of lettuce using Agrobacterium tumefaciens. J. Exp. Bot. 45:1441–1449; 1994.

    Article  CAS  Google Scholar 

  • Domínguez, F.; Cejudo, F. J. Germination-related genes encoding proteolytic enzymes are expressed in the nucellus of developing wheat grains. Plant J. 15:569–574; 1998.

    Article  Google Scholar 

  • Duan, X.; Li, X.; Xue, Q.; Abo-El-Saad, M.; Xu, D.;, Wu, R. Transgenic rice plants harboring an introduced potato proteinase inhibitor II gene are insect resistant. Nat. Biotechnol. 14:494–498; 1996.

    Article  PubMed  CAS  Google Scholar 

  • Felton, G. W.; Gatehouse, J. A. Antinutritive plant defence mechanisms. In: Lehane, M. J.; Billingsley P. F. eds. Biology of the insect midgut. London: Chapman & Hall; 1996:373–416.

    Google Scholar 

  • Fritz, H. Foreword. In: von der Helm, K.; Korant, B. D.; Cheronis, J. C., eds. Proteases as targets for therapy. Berlin: Springer-Verlag; 2000:5–6.

    Google Scholar 

  • Gadea, J.; Mayda, M. E.; Conejero, V.; Vera, P. Characterization of defense-related genes ectopically expressed in viroid-infected tomato plants. Mol. Plant-Microbe Interact. 9:409–415; 1996.

    PubMed  CAS  Google Scholar 

  • Gatehouse, A. M. R. Biotechnological applications of plant genes in the production of insect-resistant crops. In: Clement, S. L.; Quisenberry, S. S., eds. Global plant genetic resources for insect-resistant crops. Boca Raton, FL: CRC Press; 1999:263–280.

    Google Scholar 

  • Gatehouse, A. M. R.; Davison, G. M.; Newell, C. A.; Merryweather, A.; Hamilton, W. D. O.; Burgess, E. P. J.; Gilbert, R. J. C.; Gatehouse, J. A. Transgenic potato plants with enhanced resistance to the tomato moth, Lacanobia oleracea: growth room trials. Mol. Breed. 3:49–63; 1997.

    Article  CAS  Google Scholar 

  • Graham, J. S.; Pearce, G.; Merryweather, J.; Titani, K.; Ericsson, L. H.; Ryan, C. A. 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. 260:6555–6560; 1985a.

    PubMed  CAS  Google Scholar 

  • Graham, J. S.; Pearce, G.; Merryweather, J.; Titani, K.; Ericsson, L. H.; Ryan, C. A. Wound-induced proteinase inhibitors from tomato leaves. II. The cDNA-deduced primary structure of pre-inhibitor II. J. Biol. Chem. 260:6561–6564; 1985b.

    PubMed  CAS  Google Scholar 

  • Greenblatt, H. M.; Ryan, C. A.; James, M. N. G. Structure of the complex of Streptomyces griseus proteinase B and polypeptide chymotrypsin inhibitor-I from Russet Burbank potato tubers at 2.1 Å resolution. J. Mol. Biol. 205:201–228; 1989.

    Article  PubMed  CAS  Google Scholar 

  • Gustafson, G.; Ryan, C. A. Specificity of protein turnover in tomato leaves. J. Biol. Chem. 251:7004–7010; 1976.

    PubMed  CAS  Google Scholar 

  • Ham, W. E.; Sandstedt, R. M. A proteolytic inhibitory substance in the extract from unheated soybean meal. J. Biol. Chem. 154:505–506; 1944.

    CAS  Google Scholar 

  • Hendriks, T.; Vreugdenhil, D.; Stiekema, W. J. Patatin and four serine proteinase inhibitor genes are differentially expressed during potato tuber development. Plant Mol. Biol. 17:385–394; 1991.

    Article  PubMed  CAS  Google Scholar 

  • Hilder, V. A.; Gatehouse, A. M. R.; Boulter, D. Transgenic plants conferring insect tolerance: proteinase inhibitor approach. In: Kung, S. D.; Wu, R. eds. Transgenic plants, vol. 1. New York: Academic Press; 1993:317–338.

    Google Scholar 

  • 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 330:160–163; 1987.

    Article  CAS  Google Scholar 

  • Hollaender-Czytko, H.; Andersen, J. K.; Ryan, C. A. Vacuolar localization of wound-induced carboxypeptidase inhibitor in potato leaves. Plant Physiol. 78:76–79, 1985.

    Google Scholar 

  • Horisberger, M.; Tacchini-Vonlanthen, M. Ultrastructural localization of Kunitz inhibitor on thin sections of soybean (Glycine max cv. Maple Arrow) by the gold method. Histochemistry 77:37–50; 1983a.

    Article  PubMed  CAS  Google Scholar 

  • Horisberger, M.; Tacchini-Vonlanthen, M. Ultrastructural localization of Bowman-Birk inhibitor on thin sections of Glycine max (soybean) cv. Maple Arrow by the gold method. Histochemistry 77:313–321; 1983b.

    Article  PubMed  CAS  Google Scholar 

  • Horsch, R. B.; Fry, J. E.; Hoffmann, N. L.; Eichholtz, D.; Rogers S. G.; Fraley, R. T. A simple and general method for transferring genes into plants. Science 227:1229–1231; 1985.

    Article  CAS  Google Scholar 

  • Jofuku, K. D.; Goldberg, R. B. Kunitz trypsin inhibitor genes are differentially expressed during the soybean life cycle and in transformed tobacco plants. Plant Cell 1:1079–1093; 1989.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, R.; Narvaez, J.; Anm, G.; Ryan, C. Expression of proteinase inhibitors I and II in transgenic tobacco plants: effects on natural defense against Manduca sexta larvae. Proc. Natl Acad. Sci. USA 86:9871–9875; 1989.

    Article  PubMed  CAS  Google Scholar 

  • Kenny, A. J. Introduction: Nomenclature and classes of peptidases. In: Sterchi, E. E.; Stocker, W., eds. Proteolytic enzymes. Tools and targets. Berlin: Springer-Verlag; 1999:1–8.

    Google Scholar 

  • Klopfenstein, N. B.; Allen, K. K.; Avila, F. J.; Heuchelin, S. A.; Martinez, J.; Carman, R. C.; Hall, R. B.; Hart, E. R.; McNabb, H. S. Proteinase inhibitor II gene in transgenic poplar: chemical and biological assays. Biomass Bioener. 12:299–311; 1997.

    Article  CAS  Google Scholar 

  • Kunitz, M. Crystallization of a trypsin inhibitor from soybeans. Science 101:668–669; 1945.

    Article  CAS  PubMed  Google Scholar 

  • Laskowski, M. Jr; Kato, I. Protein inhibitors of proteinases Annu. Rev. Biochem. 49:593–626; 1980.

    Article  PubMed  CAS  Google Scholar 

  • Laskowski, M. Jr.; Sealock, R. W. Protein proteinase inhibitors-molecular aspects. In: Boyer, P., ed. The enzymes, vol. 3. New York: Academic Press; 1971:375–473.

    Google Scholar 

  • Liener, I. E.; Kakade, M. L.; Protease inhibitors. In: Liener, I. E., ed. Toxic constituents of plant foodstuffs. New York: Academic Press; 1969:7–68.

    Google Scholar 

  • Lopes, M. A.; Larkins, B. A. Endosperm origin, development, and function. Plant Cell 5:1383–1399; 1993.

    Article  PubMed  CAS  Google Scholar 

  • Lorberth, R.; Dammann, C.; Ebneth, M.; Amati, S.; Sanchez-Serrano, J. J. Promoter elements involved in environmental and developmental control of potato proteinase inhibitor II expression. Plant J. 2:477–486; 1992.

    PubMed  CAS  Google Scholar 

  • Ma, J. K.-C.; Drake, P. M. W.; Christou, P. The production of recombinant pharmaceuticals proteins in plants. Nat. Rev. Genet. 4:794–805; 2003.

    Article  PubMed  CAS  Google Scholar 

  • Margossian, L. J.; Federman, A. D.; Giovannoni, J. J.; Fischer, R. L. 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. USA 85:8012–8016; 1988.

    Article  PubMed  CAS  Google Scholar 

  • Meinke, D. W. Molecular genetics of plant embryogenesis. Annu. Rev. Plant Physiol. Plant. Mol. Biol. 46:369–394; 1995.

    Article  CAS  Google Scholar 

  • Michelmore, R. W.; Marsh, E.; Seely, S.; Landry, B. Transformation of lettuce (Lactuca sativa) mediated by Agrobacterium tumefaciens. Plant Cell Rep. 6:439–442; 1987.

    CAS  Google Scholar 

  • Miller, E. A.; Lee, M. C. S.; Atkinson, A. H. O.; Anderson, M. A. Identification of a novel four-domain member of the proteinase inhibitor II family from the stigmas of Nicotiana alata. Plant Mol. Biol. 42:329–333; 2000.

    Article  PubMed  CAS  Google Scholar 

  • Murray, D. R. Nutrition of the angiosperm embryo. Somerset England: Research Studies Press; 1988.

    Google Scholar 

  • Norton, G. Proteinase inhibitors. In: D'Mello, J. P. F., Duffus, C. M.; Duffus, J. H., eds. Toxic substances in crop plants. Cambridge: Royal Society of Chemistry; 1991:68–106.

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Pearce, G.; Ryan, C. A.; Liljegren, D. Proteinase inhibitors I and II in fruit of wild tomato species: transient components of a mechanism for defense and seed dispersal. Planta 175:527–531; 1988.

    Article  CAS  Google Scholar 

  • Peňa-Cortés, H.; Sanchez-Serrano, J.; Rocha-Sosa, M.; Willmitzer, L. Systemic induction of proteinase-inhibitor II gene expression in potato plants by wounding. Planta 174:84–89; 1988.

    Article  Google Scholar 

  • Peňa-Cortés, H.; Willmitzer, L.; Sánchez-Serrano, J. J. Abscisic acid mediates wound induction but not developmental-specific expression of the proteinase inhibitor II gene family. Plant Cell 3:963–972; 1991.

    Article  PubMed  Google Scholar 

  • Read, J. W.; Haas, L. W. Studies on the baking quality of flour as affected by certain enzyme actions. V. Further studies concerning potassium bromate and enzyme activity. Cereal Chem. 15:59–68; 1938.

    CAS  Google Scholar 

  • Reeck, G. R.; Kramer, K. J.; Baker, J. E.; Kanost, M. R.; Fabrick, J. A.; Behnke, C. A. Proteinase inhibitors and resistance of transgenic plants to insects. In: Carozzi, N.; Koziel, M., eds. Advances in insect control: the role of transgenic plants. London: Taylor & Francis; 1997:157–183.

    Google Scholar 

  • Richardson, M. The proteinase inhibitors of plants and micro-organisms. Phytochemistry 16:159–169; 1977.

    Article  CAS  Google Scholar 

  • Richardson, M. The complete amino acid sequence and trypsin reactive (inhibitory) site of the major proteinase inhibitor from the fruits of aubergine (Solanum melongena L.). FEBS Lett. 104:322–326; 1979.

    Article  PubMed  CAS  Google Scholar 

  • Richardson, M. Seed storage proteins: The enzyme inhibitors. In: Rogers, L. J., ed. Methods in plant biochemistry, vol. 5. Amino acids, proteins and nucleic acids, New York: Academic Press; 1991:259–305.

    Google Scholar 

  • Rosahl, S.; Eckes, P.; Schell, J.; Willmitzer L. Organ-specific gene expression in potato: isolation and characterization of tuber-specific cDNA sequences. Mol. Gen. Genet. 202:368–373; 1986.

    Article  CAS  Google Scholar 

  • Ryan, C. A. Proteinase inhibitors. In: Marcus, A., ed. The biochemistry of plants, vol. 6. New York: Academic Press; 1981:351–370.

    Google Scholar 

  • Ryan, C. A. Proteinase inhibitor gene families: strategies for transformation to improve plant defenses against herbivores. BioEssays 10:20–24; 1989.

    Article  PubMed  CAS  Google Scholar 

  • Ryan, C. A. Protease inhibitors in plants: genes for improving defenases against insects and pathogens. Annu. Rev. Phytopathol. 28:425–449; 1990.

    Article  CAS  Google Scholar 

  • Ryder, E. J. Lettuce, endive and chicory. New York: CABI Publishing; 1999.

    Google Scholar 

  • Sanchez-Serrano, J. J.; Schmidt, R.; Schell, J.; Willmitzer, L. Nucleotide sequence of proteinase inhibitor II encoding cDNA of potato (Solanum tuberosum) and its mode of expression. Mol. Gen. Genet. 203:15–20; 1986.

    Article  CAS  Google Scholar 

  • Sin, S. F.; Chye, M. L. Expression of proteinase inhibitor II proteins during floral development in Solanum americanum. Planta 219:1010–1022; 2004.

    Article  PubMed  CAS  Google Scholar 

  • Sin, S. F.; Yeung, E. C.; Chye, M. L. Down-regulation of Solanum americanum genes encoding proteinase inhibitor II causes defective seed development. Plant J. 45:58–70; 2006.

    Article  PubMed  CAS  Google Scholar 

  • Solomon, M.; Belenghi, B.; Delledonne, M.; Menachem, E.; Levine, A. The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 11:431–443; 1999.

    Article  PubMed  CAS  Google Scholar 

  • Srinivasan, A.; Giri, A. P.; Harsulkar, A. M.; Gatehouse, J. A.; Gupta, V. S. A Kunitz trypsin inhibitor from chickpea exerts anti-metabolic effect on podborer (Helicoverpa armigera) larvae. Plant Mol. Biol. 57:359–374; 2005.

    Article  PubMed  CAS  Google Scholar 

  • Stevens, L. H.; Stoopen, G. M.; Elbers, I. J.; Molthoff, J. W.; Baker, H. A.; Lommen, A.; Bosch, D.; Jordi, W. Effect of climate conditions and plant developmental stage on the stability of antibodies expressed in transgenic tobacco. Plant Physiol. 124:73–182; 2000.

    Article  Google Scholar 

  • Stiekema, W. J.; Heidekamp, F.; Dirkse, W. G.; van Beckum, J.; de Haan, P.; ten Bosch, C.; Louwerse, J. D. Molecular cloning and analysis of four potato tuber mRNAs. Plant Mol. Biol. 11:255–269; 1988.

    Article  CAS  Google Scholar 

  • Tamayo, M. C.; Rufat, M.; Bravo, J. M.; Segundo, B. S. Accumulation of a maize proteinase inhibitor in response to wounding and insect feeding, and characterization of its activity toward digestive proteinases of Spodoptera littoralis larvae. Planta 211:62–71; 2000.

    Article  PubMed  CAS  Google Scholar 

  • Taylor, B. H.; Young, R. J.; Scheuring, C. F. Induction of a proteinase inhibitor II-class gene by auxin in tomato roots. Plant Mol. Biol. 23:1005–1014; 1993.

    Article  PubMed  CAS  Google Scholar 

  • Thornburg, R. W.; An, G.; Cleveland, T. E.; Johnson, R.; Ryan, C. A. Wound-inducible expression of a potato inhibitor II-chloramphenicol acetyl-transferase gene fusion in transgenic tobacco plants. Proc. Natl Acad. Sci. USA 84:744–748; 1987.

    Article  PubMed  CAS  Google Scholar 

  • Turk, V. Proteases: new perspectives Basel: Birkhauser Verlag; 1999.

    Google Scholar 

  • Vielle-Calzada, J. P.; Thomas, J.; Spillane, C. Coluccio, A.; Hoeppner, M. A.; Grossniklaus, U. Maintenance of genomic imprinting at the Arabidopsis medea locus requires zygotic DDM1 activity. Genes Dev. 13:2971–2982; 1999.

    Article  PubMed  CAS  Google Scholar 

  • Walker, N. A.; Patrick, J. W.; Zhang, W. H.; Fiew, S. Efflux of photosynthate and acid from developing seed coats of Phaseolus vulgaris L.: a chemiosomotic analysis of pump-driven efflux. J. Exp. Bot. 46: 539–549; 1995.

    Article  CAS  Google Scholar 

  • Walker-Simmons, M.; Ryan, C. A. Wound-induced accumulation of trypsin inhibitor activities in plant leaves Plant Physiol. 59:437–439; 1977.

    Article  PubMed  CAS  Google Scholar 

  • Walsh, T. A.; Strickland, J. A. Proteolysis of the 85-kilodalton crystalline proteinase inhibitor from potato releases functional cystain domains. Plant Physiol. 103:1227–1234; 1993.

    Article  PubMed  CAS  Google Scholar 

  • Wan, L.; Xia, Q.; Qiu, X.; Selvaraj, G. Early stages of seed development in Brassica napus: a seed coat-specific cysteine proteinase associated with programmed cell death of the inner integument. Plant J. 30:1–10; 2002.

    Article  PubMed  CAS  Google Scholar 

  • Wingate, V. P. M.; Franceschi, V. R.; Ryan, C. A. Tissue and cellular localization of proteinase inhibitors I and II in the fruit of the wild tomato, Lycopersicon peruvianum (L.) Mill. Plant Physiol. 97:490–495; 1991.

    CAS  Google Scholar 

  • Wu, H. M.; Cheung, A. Y. Programmed cell death in plant reproduction. Plant Mol. Biol. 44:267–281; 2000.

    Article  PubMed  Google Scholar 

  • Xu, F. X.; Chye, M. L. Expression of cysteine proteinase during developmental events associated with programmed cell death in brinjal. Plant J. 17:321–327; 1999.

    Article  PubMed  CAS  Google Scholar 

  • Xu, H.; Kermode, A. R. Proleases associated with programmed cell death of megagametophyte cells after germination of white spruce (Picea glauca) seeds. Plant Mol. Biol. 52:729–744; 2003.

    Article  Google Scholar 

  • Xu, Z. F.; Qi, W. Q.; Ouyang, X. Z.; Yeung, E.; Chye, M. L. A proteinase inhibitor II of Solanum americanum is expressed in phloem. Plant Mol. Biol. 47:727–738; 2001.

    Article  PubMed  CAS  Google Scholar 

  • Xu, Z. F.; Teng, W. L.; Chye, M. L. Inhibition of endogenous trypsin-and chymotrypsin-like activities in transgenic lettuce expressing hetero-geneous proteinase inhibitor SaPIN2a. Planta 218:623–629; 2004.

    Article  PubMed  CAS  Google Scholar 

  • Yamauchi, Y.; Ejiri, Y.; Sugimoto, T.; Sueyoshi, K.; Oji, Y.; Tanaka, K. A high molecular weight glutamyl endopeptidase and its endogenous inhibitors from cucumber leaves. J. Biochem. 130:257–261; 2001.

    PubMed  CAS  Google Scholar 

  • Yeung, E. C. Developmental-changes in the branched parenchyma cells of bean-seed coat. Protoplasma 118:225–229; 1983.

    Article  Google Scholar 

  • Yeung, E. C.; Cavey, M. J. Developmental-changes in the inner epidermis of the bean seed coat. Protoplasma 154:45–52; 1990.

    Article  Google Scholar 

  • Yeung, E. C.; Meinke, D. W.; Nickle, T. C. Embryology of flowering plants—an overview. Phytomorphology Golden Jubilee Issue 2001:289–304.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. -L. Chye.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chye, M.L., Sin, S.F., Xu, Z.F. et al. Serine proteinase inhibitor proteins: Exogenous and endogenous functions. In Vitro Cell.Dev.Biol.-Plant 42, 100–108 (2006). https://doi.org/10.1079/IVP2005741

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1079/IVP2005741

Key words

Navigation