Sorry, you need to enable JavaScript to visit this website.

The characterization of the soybean polygalacturonase-inhibiting proteins (Pgip) gene family reveals that a single member is responsible for the activity detected in soybean tissues

TitleThe characterization of the soybean polygalacturonase-inhibiting proteins (Pgip) gene family reveals that a single member is responsible for the activity detected in soybean tissues
Publication TypeArticolo su Rivista peer-reviewed
Year of Publication2006
AuthorsD’Ovidio, R., Roberti S., Di Giovanni M., Capodicasa Cristina, Melaragni M., Sella L., Tosi P., and Favaron F.
Pagination633 - 645
Date Published2006
ISBN Number00320935 (ISSN)
KeywordsAmino Acid Sequence, article, chemistry, Cloning, comparative study, DNA, DNA sequence, Endopolygalacturonase, fungal protein, Fungal Proteins, Fungi, fungus, Gene family, Genetic variability, genetics, Glycine, Glycine max, metabolism, microbiology, Molecular, molecular cloning, molecular genetics, Molecular Sequence Data, Multigene Family, PGIP protein, physiology, Plant, Plant Proteins, polygalacturonase, Polygalacturonase-inhibiting protein, Protein, Sclerotinia, Sclerotinia sclerotiorum, Sequence Alignment, Sequence Analysis, soybean, Soybeans, Variation (Genetics), vegetable protein

Polygalacturonase-inhibiting proteins (PGIPs) are leucine-rich repeat (LRR) proteins that inhibit fungal endopolygalacturonases (PGs). They are encoded by multigene families whose members show functional redundancy and subfunctionalization for recognition of fungal PGs. In order to expand the information on the structure and functional features of legume PGIP, we have isolated and characterized four members of the soybean Pgip gene family and determined the properties of the encoded protein products. Sequence analysis showed that these genes form two clusters: one cluster of about 5 kbp containing Gmpgip1 and Gmpgip2, and the other containing Gmpgip3 and Gmpgip4 within a 60 kb fragment of a separate BAC clone. Sequence diversification of the four members resides mainly in the xxLxLxx region that includes residues forming the β-sheet B1. When compared with other legume Pgip genes, Gmpgip3 groups with the bean genes Pvpgip1 and Pvpgip2, suggesting that these genes are closer to the ancestral gene. At the protein level, only GmPGIP3 shows the capability to inhibit fungal PGs. The spectrum of inhibition of GmPGIP3 against eight different fungal PGs mirrors that of the PGIP purified from soybean tissues and is similar to that of the bean PvPGIP2, one of the most efficient inhibitors so far characterized. We also report that the four Gmpgip genes are differentially regulated after wounding or during infection with the fungal pathogen Sclerotinia sclerotiorum. Following fungal infection Gmpgip3 is up regulated promptly, while Gmpgip2 is delayed. © Springer-Verlag 2006.


Cited By :30Export Date: 29 September 2015CODEN: PLANACorrespondence Address: D’Ovidio, R.; Dipartimento di Agrobiologia e Agrochimica, Università Della Tuscia, via San Camillo De Lellis, s.n.c, 01100, Viterbo, Italy; email: dovidio@unitus.itChemicals/CAS: polygalacturonase, 9023-92-1, 9032-75-1; Fungal Proteins; PGIP protein, plant; Plant Proteins; Polygalacturonase, EC Baulcombe, D., Chapman, S., Santa Cruz, S., Jellyfish green fluorescent protein as a reporter for virus infections (1995) Plant J, 7, pp. 1045-1053;Caprari, C., Mattei, B., Basile, M.L., Salvi, G., Crescenzi, V., De Lorenzo, G., Cervone, F., Mutagenesis of endopolygalacturonase from Fusarium moniliforme: Histidine residue 234 is critical for enzymatic and macerating activities and not for binding to polygalacturonase-inhibiting protein (PGIP) (1996) Mol Plant Microbe Interact, 9, pp. 617-624; Cervone, F., Castoria, R., Leckie, F., De Lorenzo, G., Perception of fungal elicitors and signal transduction (1997) Signal Transduction in Plants, pp. 153-177. , Aducci P (ed). Birkäuser Verlag, Basel/Switzerland; Cervone, F., De Lorenzo, G., Degrà, L., Salvi, G., Elicitation of necrosis in Vigna unguiculata Walp. by homogeneous Aspergillus niger endo-polygalacturonase and by a-D-galacturonate oligomers (1987) Plant Physiol, 85, pp. 626-630; Comeron, J.M., K-Estimator: Calculation of the number of nucleotide substitutions per site and the confidence intervals (1999) Bioinformatics, 15, pp. 763-764; D’Ovidio, R., Anderson, O.D., PCR analysis to distinguish between alleles of a member of a multigene family correlated with wheat quality (1994) Theor Appl Genet, 88, pp. 759-763; D’Ovidio, R., Raiola, A., Capodicasa, C., Devoto, A., Pontiggia, D., Roberti, S., Galletti, R., De Lorenzo, G., Characterization of the complex locus of Phaseolus vulgaris encoding polygalacturonase-inhibiting proteins (PGIPs) reveals sub-functionalization for defense against fungi and insects (2004) Plant Physiol, 135, pp. 2424-2435; De Lorenzo, G., D’Ovidio, R., Cervone, F., The role of polygalacturonase-inhibiting proteins (PGIPs) in defense against pathogenic fungi (2001) Annu Rev Phytopathol, 39, pp. 313-335; Desiderio, A., Aracri, B., Leckie, F., Mattei, B., Salvi, G., Tigelaar, H., Van Roekel, J.S., Cervone, F., Polygalacturonase-inhibiting proteins (PGIPs) with different specificities are expressed in Phaseolus vulgaris (1997) Mol Plant Microbe Interact, 10, pp. 852-860; Di Matteo, A., Federici, L., Mattei, B., Salvi, G., Johnson, K.A., Savino, C., De Lorenzo, G., Cervone, F., The crystal structure of PGIP (polygalacturonase-inhibiting protein), a leucine-rich repeat protein involved in plant defense (2003) Proc Natl Acad Sci USA, 100, pp. 10124-10128; Favaron, F., D’Ovidio, R., Porceddu, E., Alghisi, P., Purification and molecular characterization of a soybean polygalacturonase-inhibiting protein (PGIP) (1994) Planta, 195, pp. 80-87; Favaron, F., Castiglioni, C., D’Ovidio, R., Alghisi, P., Polygalacturonase-inhibiting proteins from Allium porrum L. and protection of plant tissue from fungal endo-polygalacturonase degradation (1997) Physiol Mol Plant Pathol, 50, pp. 403-417; Favaron, F., Destro, T., D’Ovidio, R., Transcript accumulation of polygalacturonase inhibiting protein (PGIP) following pathogen infections in soybean (2000) J Plant Pathol, 82, pp. 103-109; Favaron, F., Sella, L., D’Ovidio, R., Relationships among endo-polygalacturonase, oxalate, pH and plant polygalacturonase-inhibiting protein (PGIP) in the interaction between Sclerotinia sclerotiorum and soybean (2004) Mol Plant Microbe Interact, 17, pp. 1402-1409; Ferrari, S., Vairo, D., Ausubel, F.M., Cervone, F., De Lorenzo, G., Arabidopsis polygalacturonase-inhibiting proteins (PGIP) are regulated by different signal transduction pathways during fungal infection (2003) Plant Cell, 15, pp. 93-106; Huang, Q., Allen, C., Polygalacturonase are required for rapid colonization and full virulence of Ralstonia solanacearum on tomato plants (2000) Physiol Mol Plant Pathol, 57, pp. 77-83; Hulbert, S.H., Webb, C.A., Smith, S.M., Sun, Q., Resistance gene complexes: Evolution and utilization (2001) Annu Rev Phytopathol, 39, pp. 285-312; Isshiki, A., Akimitsu, K., Yamamoto, M., Yamamoto, H., Endopolygalacturonase is essential for citrus black rot caused by Alternaria citri but not brown spot caused by Alternaria alternata (2001) Mol Plant Microbe Interact, 14, pp. 749-757; Jang, S., Lee, B., Kim, C., Yim, J., Han, J.-J., Lee, S., Kim, S.-R., An, G., The OsFOR1 gene encodes a polygalacturonase-inhibiting protein (PGIP) that regulates floral organ number in rice (2003) Plant Mol Biol, 53, pp. 357-369; Jones, D.A., Jones, J.D.G., The roles of leucine rich repeats in plant defences (1997) Adv Bot Res, 24, pp. 90-167; Kemp, G., Bergmann, C.W., Clay, R., Van Der Westhuizen, A.J., Pretorius, Z.A., Isolation of a polygalacturonase-inhibiting protein (PGIP) from wheat (2003) Mol Plant Microbe Interact, 16, pp. 955-961; Leckie, F., Mattei, B., Capodicasa, C., Hemmings, A., Nuss, L., Aracri, B., De Lorenzo, G., Cervone, F., The specificity of polygalacturonase-inhibiting protein (PGIP): A single amino acid substitution in the solvent-exposed b-strand/b-turn region of the leucine-rich repeats (LRRs) confers a new recognition capability (1999) EMBO J, 18, pp. 2352-2363; Lehmann, P., Structure and evolution of plant disease resistance genes (2002) J Appl Genet, 43, pp. 403-414; Li, R., Rimmer, R., Yu, M., Sharpe, A.G., Seguin-Swartz, G., Lydiate, D., Hegedus, D.D., Two Brassica napus polygalacturonase inhibitory protein genes are expressed at different levels in response to biotic and abiotic stresses (2003) Planta, 217, pp. 299-308; Mahalingam, R., Wang, G., Knap, H.T., Polygalacturonase and Polygalacturonase Inhibitor Protein: Gene Isolation and Transcription in Glycine max-Heteroderaglycines Interactions (1999) Mol Plant Microbe Interact, 12, pp. 490-498; Mattei, B., Bernalda, M.S., Federici, L., Roepstorff, P., Cervone, F., Boffi, A., Secondary structure and post-translational modifications of the leucine-rich repeat protein PGIP (polygalacturonase-inhibiting protein) from Phaseolus vulgaris (2001) Biochemistry, 40, pp. 569-576; Meyers, B.C., Shen, K.A., Rohani, P., Gaut, B.S., Michelmore, R.W., Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection (1998) Plant Cell, 10, pp. 1833-1846; Milner, Y., Avigad, G., A copper reagent for the determination of hexuronic acids and certain ketohexoses (1967) Carbohydr Res, 4, pp. 359-361; Oeser, B., Heidrichm, P.M., Muller, U., Tudzynski, P., Tenberge, K.B., Polygalacturonase is a pathogenicity factor in the Claviceps purpurea/rye interaction (2002) Fungal Genet Biol, 36, pp. 176-186; Powell, A.L., Van Kan, J., Ten Have, A., Visser, J., Greve, L.C., Bennett, A.B., Labavitch, J.M., Transgenic expression of pear PGIP in tomato limits fungal colonization (2000) Mol Plant Microbe Interact, 13, pp. 942-950; Ridley, B.L., O’Neill, M.A., Mohnen, D., Pectins: Structure, biosynthesis, and oligogalacturonide-related signaling (2001) Phytochemistry, 57, pp. 929-967; Rodriguez-Palenzuela, P., Burr, T.J., Collmer, A., Polygalacturonase is a virulence factor in Agrobacterium tumefaciens biovar 3 (1991) J Bacteriol, 173, pp. 6547-6552; Sambrook, J., Fritsch, E.F., Maniatis, T., (1989) Molecular Cloning, a Laboratory Manual, , Cold Spring Harbor Laboratory Press, Cold Spring Harbor; Sella, L., Castiglioni, C., Roberti, S., D’Ovidio, R., Favaron, F., An endo-polygalacturonase (PG) of Fusarium moniliforme escaping inhibition by plant polygalacturonase-inhibiting proteins (PGIPs) provides new insights into the PG-PGIP interaction (2004) FEMS Microbiol Lett, 240, pp. 117-124; Szecsi, A., I. Analysis of pectic enzyme zymograms of Fusarium species. II. Comparison of polygalacturonase zymograms of Fusarium culmorum and Fusarium graminearum (1990) J Phytopathol, 130, pp. 188-196; Taylor, R.J., Secor, G.A., An improved diffusion assay for quantifying the polygalacturonase content of Erwinia culture filtrates (1988) Phytopathology, 78, pp. 1101-1103; Ten Have, A., Mulder, W., Visser, J., Van Kan, J.A., The endo-polygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea (1998) Mol Plant Microbe Interact, 11, pp. 1009-1016; Warren, R.F., Henk, A., Mowery, P., Holub, E., Innes, R.W., A mutation within the leucine-rich repeat domain of the Arabidopsis disease resistance gene RPS5 partially suppresses multiple bacterial and downy mildew resistance genes (1998) Plant Cell, 10, pp. 1439-1452; Worrall, D., Elias, L., Ashford, D., Smallwood, M., Sidebottom, C., Lillford, P., Telford, J., Bowles, D., A carrot leucine-rich-repeat protein that inhibits ice recrystallization (1998) Science, 282, pp. 115-117; Zhang, J., Kumar, S., Nei, M., Small-sample tests of episodic adaptive evolution: A case study of primate lysozymes (1997) Mol Biol Evol, 14, pp. 1335-1338

Citation Key5443