Title | Targeted modification of homogalacturonan by transgenic expression of a fungal polygalacturonase alters plant growth |
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Publication Type | Articolo su Rivista peer-reviewed |
Year of Publication | 2004 |
Authors | Capodicasa, Cristina, Vairo D., Zabotina O., McCartney L., Caprari C., Mattei B., Manfredini C., Aracri B., Benen J., Knox J.P., De Lorenzo G., and Cervone F. |
Journal | Plant Physiology |
Volume | 135 |
Pagination | 1294 - 1304 |
Date Published | 2004 |
ISBN Number | 00320889 (ISSN) |
Keywords | Antibodies, Ara, Arabidopsis, article, Aspergillus, Aspergillus niger, Base Sequence, Cell walls, Cells, development and aging, DNA Primers, endopolygalacturonase II, enzymology, Fungi, Genes, Genetically Modified, genetics, growth, isolation and purification, metabolism, Nicotiana, Nicotiana obtusifolia, Nicotiana tabacum, nucleotide sequence, pectin, Pectins, plant stem, Plant Stems, Plants, Plants (botany), polygalacturonase, polygalacturonic acid, primer DNA, recombinant protein, Recombinant Proteins, Tobacco, transgenic plant |
Abstract | Pectins are a highly complex family of cell wall polysaccharides comprised of homogalacturonan (HGA), rhamnogalacturonan I and rhamnogalacturonan II. We have specifically modified HGA in both tobacco (Nicotiana tabacum) and Arabidopsis by expressing the endopolygalacturonase II of Aspergillus niger (AnPGII). Cell walls of transgenic tobacco plants showed a 25% reduction in GalUA content as compared with the wild type and a reduced content of deesterified HGA as detected by antibody labeling. Neutral sugars remained unchanged apart from a slight increase of Rha, Ara, and Gal. Both transgenic tobacco and Arabidopsis were dwarfed, indicating that unesterified HGA is a critical factor for plant cell growth. The dwarf phenotypes were associated with AnPGII activity as demonstrated by the observation that the mutant phenotype of tobacco was completely reverted by crossing the dwarfed plants with plants expressing PGIP2, a strong inhibitor of AnPGII. The mutant phenotype in Arabidopsis did not appear when transformation was performed with a gene encoding AnPGII inactivated by site directed mutagenesis. |
Notes | Cited By :34Export Date: 29 September 2015CODEN: PLPHACorrespondence Address: Cervone, F.; Dipartimento di Biologia Vegetale, Lab. Genomica Funzionale Proteomica, Univ. di Roma La Sapienza, 00185 Rome, Italy; email: felice.cervone@uniroma1.itChemicals/CAS: pectin, 9000-69-5; polygalacturonase, 9023-92-1, 9032-75-1; polygalacturonic acid, 25249-06-3; DNA Primers; endopolygalacturonase II, EC 3.2.1.-; Pectins; Polygalacturonase, EC 3.2.1.15; polygalacturonic acid, 9046-38-2; Recombinant ProteinsReferences: Allen, R.L., Lonsdale, D.M., Molecular characterization of one of the maize polygalacturonase gene family members which are expressed during late pollen development (1993) Plant J, 3, pp. 261-271;Analysis of the genome sequence of the flowering plant Arabidopsis thaliana (2000) Nature, 408, pp. 796-815; Armand, S., Wagemaker, M.J., Sanchez-Torres, P., Kester, H.C.M., Van Santen, Y.D.W., Visser, J., Benen, J.A.E., The active site topology of Aspergillus niger endopolygalacturonase II as studied by site-directed mutagenesis (2000) J Biol Chem, 275, pp. 691-696; Atkinson, R.C., Schröder, R., Hallett, I.C., Cohen, D., MacRae, E.A., Overexpression of polygalacturonase in transgenic apple leads to a range of novel phenotypes involving changes in cell adhesion (2002) Plant Physiol, 129, pp. 122-133; Baron-Epel, O., Gharyal, P.K., Schindler, M., Pectins as mediators of wall porosity in soybean cells (1988) Planta, 175, pp. 389-395; Bellincampi, D., Forrest, R., Nuss, L., Salvi, G., De Lorenzo, G., Cervone, F., Extracellular accumulation of an auxin-regulated protein in Phaseolus vulgaris L. cells is inhibited by oligogalacturonides (1995) J Plant Physiol, 147, pp. 367-370; Bergmann, C., Ito, Y., Singer, D., Albersheim, P., Darvill, A.G., Benhamou, N., Nuss, L., De Lorenzo, G., Polygalacturonase-inhibiting protein accumulates in Phaseolus vulgaris L. in response to wounding, elicitors and fungal infection (1994) Plant J, 5, pp. 625-634; Bouton, S., Leboeuf, E., Mouille, G., Leydecker, M.T., Talbotec, J., Granier, F., Lahaye, M., Truong, H.N., QUASIMODO1 encodes a putative membrane-bound glycosyltransferase required for normal pectin synthesis and cell adhesion in Arabidopsis (2002) Plant Cell, 14, pp. 2577-2590; Cervone, F., De Lorenzo, G., Degrà, L., Salvi, G., Elicitation of necrosis in Vigna unguiculata Walp. by homogeneous Aspergillus niger endo-polygalacturonase and by α-D-galacturonate oligomers (1987) Plant Physiol, 85, pp. 626-630; Clausen, M.H., Willats, W.G.T., Knox, J.P., Synthetic methyl hexagalacturonate hapten inhibitors of anti-homogalacturonan monoclonal antibodies LM7, JIM5 and JIM7 (2003) Carbohydr Res, 338, pp. 1797-1800; Clough, S.J., Bent, A.F., Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana (1998) Plant J, 16, pp. 735-743; Cosgrove, D.J., Enzymes and other agents that enhance cell wall extensibility (1999) Annu Rev Plant Physiol Plant Mol Biol, 50, pp. 391-417; De Lorenzo, G., D’Ovidio, R., Cervone, F., The role of polygacturonase-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., De Lorenzo, G., Polygalacturonase-inhibiting proteins (PGIPs) with different specificities are expressed in Phaseolus vulgaris (1997) Mol Plant Microbe Interact, 10, pp. 852-860; Federici, L., Caprari, C., Mattei, B., Savino, C., Di Matteo, A., De Lorenzo, G., Cervone, F., Tsernoglou, D., Structural requirements of endopolygalacturonase for the interaction with PGIP (polygalacturonase-inhibiting protein) (2001) Proc Natl Acad Sci USA, 98, pp. 13425-13430; Femenia, A., Garosi, P., Roberts, K., Waldron, K.W., Selvendran, R.R., Robertson, J.A., Tissue-related changes in methyl-esterification of pectic polysaccharides in cauliflower (Brassica oleracea L. var. botrytis) stems (1998) Planta, 205, pp. 438-444; Giovannoni, J.J., DellaPenna, D., Bennett, A.B., Fischer, R.L., Expression of a chimeric polygalacturonase gene in transgenic rin (ripening inhibitor) tomato fruit results in polyuronide degradation but not fruit softening (1989) Plant Cell, 1, pp. 53-63; Gobom, J., Nordhoff, E., Mirgorodskaya, E., Ekman, R., Roepstorff, P., Sample purification and preparation technique based on nano-scale reversed-phase columns for the sensitive analysis of complex peptide mixtures by matrix-assisted laser desorption/ionization mass spectrometry (1999) J Mass Spectrom, 34, pp. 105-116; Hansen, G., Das, A., Chilton, M.D., Constitutive expression of the virulence genes improves the efficiency of plant transformation by Agrobacterium (1994) Proc Natl Acad Sci USA, 91, pp. 7603-7607; Jarvis, M.C., Self-assembly of plant cell walls (1992) Plant Cell Environ, 15, pp. 1-5; Kalaitzis, P., Solomos, T., Tucker, M.L., Three different polygalacturonases are expressed in tomato leaf and flower abscission, each with a different temporal expression pattern (1997) Plant Physiol, 113, pp. 1303-1308; Kim, J.B., Carpita, N.C., Changes in esterification of the uronic acid groups of cell wall polysaccharides during elongation of maize coleoptiles (1992) Plant Physiol, 98, pp. 646-653; Knox, J.P., Linstead, P.J., King, J., Cooper, C., Roberts, K., Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apices (1990) Planta, 181, pp. 512-521; Lao, N.T., Long, D., Kiang, S., Coupland, G., Shoue, D.A., Carpita, N.C., Kavanagh, T.A., Mutation of a family 8 glycosyltransferase gene alters cell wall carbohydrate composition and causes a humidity-sensitive semi-sterile dwarf phenotype in Arabidopsis (2003) Plant Mol Biol, 53, pp. 687-701; 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; Limberg, G., Korner, R., Buchholt, H.C., Christensen, T.M., Roepstorff, P., Mikkelsen, J.D., Analysis of different de-esterification mechanisms for pectin by enzymatic fingerprinting using endopectin lyase and endopolygalacturonase II from A. niger (2000) Carbohydr Res, 327, pp. 293-307; O’Neill, M.A., Eberhard, S., Albersheim, P., Darvill, A.G., Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth (2001) Science, 294, pp. 846-849; Oomen, R.J., Doeswijk-Voragen, C.H., Bush, M.S., Vincken, J.P., Borkhardt, B., Van Den Broek, L.A., Corsar, J., McCann, M.C., In muro fragmentation of the rhamnogalacturonan I backbone in potato (Solanum tuberosum L.) results in a reduction and altered location of the galactan and arabinan side-chains and abnormal periderm development (2002) Plant J, 30, pp. 403-413; Orfila, C., Seymour, G.B., Willats, W.G., Huxham, I.M., Jarvis, M.C., Dover, C.J., Thompson, A.J., Knox, J.P., Altered middle lamella homogalacturonan and disrupted deposition of (1→5)-alpha-L-arabinan in the pericarp of Cnr, a ripening mutant of tomato (2001) Plant Physiol, 126, pp. 210-221; Osteryoung, K.W., Toenjes, K., Hall, B., Winkler, V., Bennett, A.B., Analysis of tomato polygalacturonase expression in transgenic tobacco (1990) Plant Cell, 2, pp. 1239-1248; Oxenboll, S.S., Pauly, M., Bush, M., Skjot, M., McCann, M.C., Borkhardt, B., Ulvskov, P., Pectin engineering: Modification of potato pectin by in vivo expression of an endo-1,4-beta-D-galactanase (2000) Proc Natl Acad Sci USA, 97, pp. 7639-7644; Peretto, R., Favaron, F., Bettini, V., De Lorenzo, G., Marini, S., Alghisi, P., Cervone, F., Bonfante, P., Expression and localization of polygalacturonase during the outgrowth of lateral roots in Allium porrum L. (1992) Planta, 188, pp. 164-172; Pilling, J., Willmitzer, L., Fisahn, J., Expression of a Petunia inflata pectin methyl esterase in Solanum tuberosum L. enhances stem elongation and modifies cation distribution (2000) Planta, 210, pp. 391-399; Rhee, S.Y., Somerville, C.R., Tetrad pollen formation in quartet mutants of Arabidopsis thaliana is associated with persistence of pectic polysaccharides of the pollen mother cell wall (1998) Plant J, 15, pp. 79-88; Ridley, B.L., O’Neill, M.A., Mohnen, D., Pectins: Structure, biosynthesis, and oligogalacturonide-related signaling (2001) Phytochemistry, 57, pp. 929-967; Ried, J.L., Collmer, A., Comparison of pectic enzymes produced by Erwinia chrysanthemi, Erwinia carotovora subsp. carotovora, and Erwinia carotovora subsp. atroseptica (1986) Appl Environ Microbiol, 52, pp. 305-310; Schols, H.A., Vierhuis, E., Bakx, E.J., Voragen, A.G.J., Different populations of pectic hairy regions occur in apple cell walls (1995) Carbohydr Res, 275, pp. 343-360; Shevell, D.E., Kunkel, T., Chua, N.H., Cell wall alterations in the arabidopsis emb30 mutant (2000) Plant Cell, 12, pp. 2047-2060; Skjot, M., Kauppinen, S., Kofod, L.V., Fuglsang, C., Pauly, M., Dalboge, H., Andersen, L.N., Functional cloning of an endo-arabinanase from Aspergillus aculeatus and its heterologous expression in A. oryzae and tobacco (2001) Mol Genet Genomics, 265, pp. 913-921; Smith, C.J., Watson, C.F., Bird, C.R., Ray, J., Schuch, W., Grierson, D., Expression of a truncated tomato polygalacturonase gene inhibits expression of the endogenous gene in transgenic plants (1990) Mol Gen Genet, 224, pp. 477-481; Steele, N.M., McCann, M.C., Roberts, K., Pectin modification in cell walls of ripening tomatoes occurs in distinct domains (1997) Plant Physiol, 114, pp. 373-381; Stolle-Smits, T., Beekhuizen, J.G., Recourt, K., Voragen, A.G.J., Van Dijk, C., Changes in pectic and hemicellulosic polymers of green beans (Phaseolus vulgaris L.) during industrial processing (1997) J Agric Food Chem, 45, pp. 4790-4799; 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; Thompson, A.J., Tor, M., Barry, C.S., Vrebalov, J., Orfila, C., Jarvis, M.C., Giovannoni, J.J., Seymour, G.B., Molecular and genetic characterization of a novel pleiotropic tomato-ripening mutant (1999) Plant Physiol, 120, pp. 383-389; Toubart, P., Desiderio, A., Salvi, G., Cervone, F., Daroda, L., De Lorenzo, G., Bergmann, C., Albersheim, P., Cloning and characterization of the gene encoding the endopolygalacturonase-inhibiting protein (PGIP) of Phaseolus vulgaris L. (1992) Plant J, 2, pp. 367-373; Wang, Z.Y., MacRae, E.A., Wright, M.A., Bolitho, K.M., Ross, G.S., Atkinson, R.G., Polygalacturonase gene expression in kiwifruit: Relationship to fruit softening and ethylene production (2000) Plant Mol Biol, 42, pp. 317-328; Wen, F.S., Zhu, Y.M., Hawes, M.C., Effect of pectin methylesterase gene expression on pea root development (1999) Plant Cell, 11, pp. 1129-1140; Willats, W.G., Gilmartin, P.M., Mikkelsen, J.D., Knox, J.P., Cell wall antibodies without immunization: Generation and use of de-esterified homogalacturonan block-specific antibodies from a naive phage display library (1999) Plant J, 18, pp. 57-65; Willats, W.G., Limberg, G., Buchholt, H.C., Van Alebeek, G.J., Benen, J., Christensen, T.M., Visser, J., Knox, J.P., Analysis of pectic epitopes recognised by hybridoma and phage display monoclonal antibodies using defined oligosaccharides, polysaccharides, and enzymatic degradation (2000) Carbohydr Res, 327, pp. 309-320; Willats, W.G., Orfila, C., Limberg, G., Buchholt, H.C., Van Alebeek, G.J., Voragen, A.G., Marcus, S.E., Murray, B.S., Modulation of the degree and pattern of methyl esterification of pectic homogalacturonan in plant cell walls: Implications for pectin methyl esterase action, matrix properties and cell adhesion (2001) J Biol Chem, 276, pp. 19404-19413 |
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Citation Key | 5445 |