Abstract
Genes representative of three gene classes encoding proteinase inhibitor proteins, with distinct spatial expression patterns, were isolated and characterized from Pisum.Under standard plant growth conditions, one class is expressed exclusively in seeds, whereas the other two make minor contributions to seed inhibitor proteins but are also expressed in other organs, predominantly in root endodermal and floral reproductive tissues. Two of the gene classes contain few genes and are genetically linked at the Tri locus, whereas the third class displays complex hybridization patterns to genomic DNA and maps to diverse genetic loci. Expression analysis of this last class suggests that only a small number of these genes are expressed. The quantitative effect of the Tri locus on root and floral inhibitor gene expression was examined in near-isogenic lines of pea. The proteins encoded by the three classes are all members of the same family (Bowman-Birk) of enzyme inhibitors but are distinct in terms of overall sequence, active site sequences and inhibitor function.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Altabella, T. and Chrispeels, M.J. 1990. Tobacco plants transformed with the bean ?ai gene express an inhibitor of insect ?-amylase in their seeds. Plant Physiol. 93: 805–810.
Aubourg, S., Boudet, N., Kreis, M. and Lecharny, A. 2000. In Arabidopsis thaliana, 1% of the genome codes for a novel protein family unique to plants. Plant Mol. Biol. 42: 603–613.
Charity, J.A., Anderson, M.A., Bittisnich, D.J., Whitecross, M. and Higgins, T.J.V. 1999. Transgenic tobacco and peas expressing a proteinase inhibitor from Nicotiana alata have increased insect resistance. Mol. Breed. 5: 357–365.
Domoney, C., Welham, T., Ellis, N. and Hellens, R. 1994. Inheritance of qualitative and quantitative trypsin inhibitor variants in Pisum. Theor. Appl. Genet. 89: 387–391.
Domoney, C., Welham, T., Sidebottom, C. and Firmin, J.L. 1995. Multiple isoforms of Pisum trypsin inhibitors result from modification of two primary gene products. FEBS Lett. 360: 15–20.
Domoney, C. and Welham, T. 1998. Limited proteolysis of enzyme inhibitor proteins during seed desiccation in Pisum. J. Plant Physiol. 152: 692–695.
Domoney, C. 1999. Inhibitors of legume seeds. In: P.R. Shewry and R. Casey (Eds.) Seed Proteins, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 635–655.
Duan, X., Li, X., Xue, Q., Abo-El-Saad, M., Xu, D. and Wu, R. 1996. Transgenic rice plants harboring an introduced potato proteinase inhibitor II gene are insect resistant. Nature Biotechnol. 14: 494–498.
Dubbs, W.E. and Grimes, H.D. 2000. The mid-pericarp cell layer in soybean pod walls is a multicellular compartment enriched in specific lipoxygenase isoforms. Plant Physiol. 123: 1281–1288.
Ellis, T.H.N., Domoney, C., Castleton, J., Cleary, W. and Davies, D.R. 1986. Vicilin genes of Pisum. Mol. Gen. Genet. 205: 164–169.
Forster, C., Knox, M., Domoney, C. and Casey, R. 1994. lox1: Ps:2, a Pisum sativum seed lipoxygenase gene. Plant Physiol. 106: 1227–1228.
Garcia-Olmedo, F., Salcedo, G., Sanchez-Monge, R., Gomez, L., Royo, J. and Carbonero, P. 1987. Plant proteinaceous inhibitors of proteinases and ?-amylases. Oxford Surv. Plant Mol. Cell Biol. 4: 275–334.
Gariani, T., McBride, J.D. and Leatherbarrow, R.J. 1999. The role of the P'2 position of Bowman-Birk proteinase inhibitor in the inhibition of trypsin. Studies on P'2 variation in cyclic peptides encompassing the reactive site loop. Biochim. Biophys. Acta 1431: 232–237.
Graham, J., Gordon, S.C. and McNicol, R.J. 1997. The effect of the CpTi gene in strawberry against attack by vine weevil (Otiorhynchus sulcatus F. Coleoptera: Curculionidae). Ann. Appl. Biol. 131: 133–139.
Grossi de Sa, M.F., Mirkov, T.E., Ishimoto, M., Colucci, G., Bateman, K.S. and Chrispeels, M.J. 1997. Molecular characterization of a bean ?-amylase inhibitor that inhibits the ?-amylase of the Mexican bean weevil Zabrotes subfasciatus. Planta 203: 295–303.
Hedemann, M.S., Welham, T., Boisen, S., Canibe, N., Bilham, L. and Domoney, C. 1999. Studies on the biological responses of rats to seed trypsin inhibitors using near-isogenic lines of Pisum sativum L (pea). J. Sci. Food Agric. 79: 1647–1653.
Hilder, V.A., Barker, R.F., Samour, R.A., Gatehouse, A.M.R., Gatehouse, J.A. and Boulter, D. 1989. Protein and cDNA sequences of Bowman-Birk protease inhibitors from the cowpea (Vigna unguiculata Walp.). Plant Mol. Biol. 13: 701–710.
Laucou, V., Haurogné, K., Ellis, N. and Rameau, C. 1998. Genetic mapping in pea. 1. RAPD-based genetic linkage map of Pisum sativum. Theor. Appl. Genet. 97: 905–915.
Lee, M.C.S., Scanlon, M.J., Craik, D.J. and Anderson, M.A. 1999. A novel two-chain proteinase inhibitor generated by circularization of a multidomain precursor protein. Nature Struct. Biol. 6: 526–530.
McGurl, B., Mukherjee, S., Kahn, M. and Ryan, C.A. 1995. Characterization of two proteinase inhibitor (ATI) cDNAs from alfalfa leaves (Medicago sativa var. Vernema): the expression of ATI genes in response to wounding and soil microorganisms. Plant Mol. Biol. 27: 995–1001.
Miller, E.A., Lee, M.C.S., Atkinson, A.H.O. and Anderson, M.A. 2000. Identification of a novel four-domain member of the proteinase inhibitor II family from the stigmas of Nicotiana alata. Plant Mol. Biol. 42: 329–333.
Mirkov, T.E., Wahlstrom, J.M., Hagiwara, K., Finardi-Filho, F., Kjemtrup, S. and Chrispeels, M.J. 1994. Evolutionary relationships among proteins in the phytohemagglutinin-arcelin-?-amylase inhibitor family of the common bean and its relatives. Plant Mol. Biol. 26: 1103–1113.
Mirkov, T.E., Evan, S.V., Wahlstrom, J., Gomez, L., Young, N.M. and Chrispeels, M.J. 1995. Location of the active site of the bean ?-amylase inhibitor and involvement of a Trp, Arg, Tyr triad. Glycobiology 5: 45–50.
Muel, F., Carrouee, B. and Grosjean, F. 1998. Trypsin inhibitor activity of pea cultivars: new data and a proposal strategy for breeding programmes. In: AEP (Association Européenne de recherche sur les Protéagineux) (Eds.) Proceedings of the Third European Conference on Grain Legumes (Valladolid, Spain), AEP, Paris, pp. 164–165.
Schroeder, H.E., Gollasch, S., Moore, A., Tabe, L.M., Craig, S., Hardie, D.C., Chrispeels, M.J., Spencer, D. and Higgins, T.J.V. 1995. Bean ?-amylase inhibitor confers resistance to the pea weevil (Bruchus pisorum) in transgenic peas (Pisum sativum L.). Plant Physiol. 107: 1233–1239.
Shewry, P.R. and Lucas, J.A. 1997. Plant proteins that confer resistance to pests and pathogens. Adv. Bot. Res. 26: 135–192.
Takakura, Y., Ito, T., Saito, H., Inoue, T., Komari, T. and Kuwata, S. 2000. Flower-predominant expression of a gene encoding a novel class I chitinase in rice (Oryza sativa L.). Plant Mol. Biol. 42: 883–897.
Taylor, S., Hofer, J. and Murfet, I. 2001. Stamina pistilloida, the pea ortholog of Fim and UFO, is required for normal development of flowers, inflorescences, and leaves. Plant Cell 13: 31–46.
Ware, J.H., Wan, X.S. and Kennedy, A.R. 1999. Bowman-Birk inhibitor suppresses production of superoxide anion radicals in differentiated HL-60 cells. Nutr. Cancer 33: 174–177.
Welham, T., O'Neill, M., Johnson, S., Wang, T.L. and Domoney, C. 1998. Expression patterns of genes encoding seed trypsin inhibitors in Pisum sativum. Plant Sci. 131: 13–24.
Welham, T. and Domoney, C. 2000. Temporal and spatial activity of a promoter from a pea enzyme inhibitor gene and its exploitation for seed quality improvement. Plant Sci. 159: 289–299.
Xu, D., Xue, Q., McElroy, D., Mawal, Y., Hilder, V.A. and Wu, R. 1996. Constitutive expression of a cowpea trypsin inhibitor gene, CpTi, in transgenic rice plants confers resistance to two major rice insect pests. Mol. Breed. 2: 167–173.
Zhang, L., Wan, X.S., Donahue, J.J., Ware, J.H. and Kennedy, A.R. 1999. Effects of the Bowman-Birk inhibitor on clonogenic survival and cisplatin-or radiation-induced cytotoxicity in human breast, cervical, and head and neck cancer cells. Nutr. Cancer 33: 165–173.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Domoney, C., Welham, T., Ellis, N. et al. Three classes of proteinase inhibitor gene have distinct but overlapping patterns of expression in Pisum sativum plants. Plant Mol Biol 48, 319–329 (2002). https://doi.org/10.1023/A:1013379430582
Issue Date:
DOI: https://doi.org/10.1023/A:1013379430582