Abstract
Pectin is a major component of primary cell walls of all land plants and encompasses a range of galacturonic acid-rich polysaccharides. Three major pectic polysaccharides (homogalacturonan, rhamnogalacturonan-I and rhamnogalacturonan-II) are thought to occur in all primary cell walls. This review surveys what is known about the structure and function of these pectin domains. The high degree of structural complexity and heterogeneity of the pectic matrix is produced both during biosynthesis in the endomembrane system and as a result of the action of an array of wall-based pectin-modifying enzymes. Recent developments in analytical techniques and in the generation of anti-pectin probes have begun to place the structural complexity of pectin in cell biological and developmental contexts. The in muro de-methyl-esterification of homogalacturonan by pectin methyl esterases is emerging as a key process for the local modulation of matrix properties. Rhamnogalacturonan-I comprises a highly diverse population of spatially and developmentally regulated polymers, whereas rhamnogalacturonan-II appears to be a highly conserved and stable pectic domain. Current knowledge of biosynthetic enzymes, plant and microbial pectinases and the interactions of pectin with other cell wall components and the impact of molecular genetic approaches are reviewed in terms of the functional analysis of pectic polysaccharides in plant growth and development.
Similar content being viewed by others
References
Alagna, L., Prosperi, T., Tomlinson A.A.G. and Rizzo, R. 1986. Extended X-ray absoprtion fine structure investigation of solid and gel forms of calcium poly(α-D-galacturonate). J. Phys. Chem. 90: 6853–6857.
Albersheim, P., Darvill, A.G., O'Neill, M.A., Schols, H.A. and Vor-agen, A.G.J. 1996. An hypothesis: the same six polysaccharides are components of the primary cell walls of all higher plants. In: J. Visser and A.G.J. Voragen (Eds) Pectins and Pectinases, Elsevier Science, Amsterdam, pp. 47–55.
An, J., O'Neill, M.A., Albersheim, P. and Darvill, A.G. 1994. Isola-tion and structural characterization of β-D-glucosyluronic acid and 4-O-methyl β-D-glucosyluronic acid-containing oligosac-charides from the cell wall pectic polysaccharide, rhamnogalac-turonan I. Carbohydrate Res. 252: 235–243.
Atkins, E.D.T., Nieduszynski, I.A., Mackie, W., Parker, K.D. and Smolko E.E. 1973. Structural components of alginic acid. II. The crystalline structure of poly-α-L-guluronic acid. Results of X-ray diffraction and polarized infrared studies.Biopolymers 12: 1879–1887.
Barras, F., Van Gijsegem, F. and Chatterjee, A.K. 1994. Extracel-lular enzymes and pathogenesis of soft-rot Erwinia. Annu. Rev. Phytopath. 32: 201–234.
Bergey, D.R., Orozco-Cardenas, M., de Moura, D.S. and Ryan, C.A. 1999. A wound-and systemin-inducible polygalacturonase in tomato leaves. Proc. Natl. Acad. Sci. USA 96: 1756–1760.
Bonilla, I., Mergold-Villasenor, C., Campos, M.E., Sanchez, N., Pérez, H., Lopez, L., et al. 1997. The aberrant cell walls of boron-deficient bean root nodules have no covalently bound hydroxyproline/proline-rich proteins. Plant Physiol. 115: 1329–1340.
Bonnin E., Vigouroux J. and Thibault, J.F. 1997. Kinetic para-meters of hydrolysis and transglycosylation catalyzed by an exo-β-(1,4)-galactanase. Enzyme Microbial Tech. 20: 516–522.
Bordenave, M., Goldberg, R., Huet, J.C. and Pernollet, J.C. 1995. A novel protein from mung bean hypocotyl cell walls with acetyl esterase activity. Phytochemistry 38: 315–319.
Boudart, G., Lafitte, C., Barthe, J.P., Frassez, D. and Esquerré-Tugayé, M.-T. 1998. Differential elicitation of defense responses by pectic fragments in bean seedlings. Planta 206: 86–94.
Brisson, J.R., Uhrinova, S., Woods, R.J., van der Zwan, M., Jarrell, H.C., Paoletti, L.C., Kasper, D.L. and Jennings, H.J. 1997. NMR and molecular dynamics studies of the conformational epitope of the type III group B Streptococcus capsular polysaccharide and derivatives. Biochemistry 36: 3278–3292
Buckeridge, M.S. and Reid, J.S.G. 1994. Purification and properties of a novel β-galactosidase or exo-(1→4)-β-D-galactanase from the cotyledons of germinated Lupinus angustifolius L. seeds. Planta 192: 502–511.
Burton, R.A., Gibeaut, D.M., Bacic, A., Findlay, K., Roberts, K., Hamilton, A., Baulcombe, D.C. and Fincher, G.B. 2000. Virus-induced silencing of a plant cellulose synthase gene. Plant Cell 12: 691–705.
Bush, M.S. and McCann, M.C. 1999. Pectic epitopes are differen-tially distributed in the cell walls of potato (Solanum tuberosum) tubers. Physiol. Plant. 107: 201–213.
Camardella, L., Carratore, V., Ciardiello, M.A., Servillo, L., Balestrieri, C. and Giovane, A. 2000. Kiwi protein inhibitor of pectin methylesterase. Amino-acid sequence and structural importance of two disulfide bridges. Eur. J. Biochem. 267: 4561–4565.
Carey, A.T., Holt, K., Picard, S., Wilde, R., Tucker, G.A., Bird, C.R., Schuch, W. and Seymour, G.B. 1995. Tomato exo-(1→4)-. β-D-galactanase: isolation, changes during ripening in normal and mutant tomato fruit, and characterization of a related cDNA clone. Plant Physiol. 108: 1099–1107.
Carpita, N.C. 1996. Structure and biogenesis of the cell walls of grasses. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 445–476.
Carpita, N.C. and Gibeaut, D.M. 1993. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J. 3: 1–30.
Carrington, C.M.S., Greve, L.C. and Labavitch, J.M. 1993. Cell-wall metabolism in ripening fruit. 6. Effect of the antisense poly-galacturonase gene on cell-wall changes accompanying ripening in transgenic tomatoes. Plant Physiol. 103: 429–434.
Casero, P.J. and Knox, J.P. 1995. The monoclonal antibody JIM5 indicates patterns of pectin deposition in relation to pit fields at the plasma-membrane-face of tomato pericarp cell walls. Protoplasma 188: 133–137.
Catoire, L., Pierron, M., Morvan, C., Hervé du Penhoat, C. and Goldberg, R. 1998. Investigation of the action patterns of pect-inmethylesterase isoforms through kinetic analyses and NMR spectroscopy. Implications in cell wall expansion. J. Biol. Chem. 273273: 33150–33156.
Chanliaud, E. and Gidley, M.J. 1999. In vitro synthesis and properties of pectin/Acetobacter xylinus cellulose composites. Plant J. 20: 25–35.
Charnay, D., Nari, J. and Noat, G. 1992. Regulation of plant cell wall pectin methyl esterase by polyamines: interaction with the effect of metal ions. Eur. J. Biochem. 205: 711–714.
Chen, M.H., Sheng, J.S., Hind, G., Handa, A.K. and Citovsky, V. 2000. Interaction between the tobacco mosaic virus movement protein and host cell pectin methylesterases is required for viral cell-to-cell movement. EMBO J. 19: 913–920.
Christensen, T.M.I.E., Nielsen, J.E. and Mikkelsen, J.D. 1996. Iso-lation, characterization and immunolocalization of orange fruit acetyl esterase. In: J. Visser and A.G.J. Voragen (Eds.) Pectins and Pectinases, Elsevier Science, Amsterdam, pp. 723–730.
Collmer, A. and Keen, N.T. 1986. The role of pectic enzymes in plant pathogenesis. Annu. Rev. Phytopath. 24: 383–409.
Cook, B.J., Clay, R.P., Bergmann, C.W., Albersheim, P. and Darvill, A.G. 1999. Fungal polygalacturonases exhibit different substrate degradation patterns and differ in their susceptibilities to poly-galacturonase inhibiting proteins. Mol. Plant-Microbe Interact. 12: 703–711.
Cosgrove, D.J. 1999. Enzymes and other agents that enhance cell wall extensibility. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 391–417.
Cosgrove, D.J. 2000. Expansive growth of plant cell walls. Plant Physiol. Biochem. 38: 109–124.
Daas, P.J.H., Voragen, A.G.J. and Schols, H.A. 2000. Characterization of non-esterified galacturonic acid sequences in pectin with endopolygalacturonase. Carbohydrate Res. 326: 120–129.
Denès, J.-M., Baron, A., Renard, C.M.G.C., Péan, C. and Dril-leau, J.-F. 2000. Different action patterns for apple pectin methylesterase at pH 7.0 and 4.5. Carbohydrate Res. 327: 385–393.
Domingo, C., Roberts, K., Stacey, N.J., Connerton, I., Ruiz-Teran, F. and McCann, M.C. 1998. A pectate lyase from Zinnia elegans is auxin inducible. Plant J. 13: 17–28.
Doong, R.L. and Mohnen, D. 1998. Solubilization and characteri-zation of a galacturonosyltransferase that synthesizes the pectic polysaccharide homogalacturonan. Plant J. 13: 363–374.
Dorokhov, Y.L., Mäkinen, K., Frolova, O.Y., Merits, A., Saarinen, J., Kalkkinen, N., et al. 1999. A novel function for a unbiquitous plant enzyme pectin methylesterase: the host cell receptor for the tobacco mosaic virus movement protein. FEBS Lett. 461: 223–228.
Dumville, J.C. and Fry, S.C. 2000. Uronic acid-containing oligosac-charins: their biosynthesis, degradation and signalling roles in non-diseased plant tissues. Plant Physiol. Biochem. 38: 125–140.
du Penhoat, C.H., Gey, C., Pellerin, P. and Pérez, S. 1999. An NMR solution study of the mega-oligosaccharide, rhamnogalacturonan II. J. Biomol. NMR 14: 253–271.
Engelsen, S.B., Cros, S., Mackie, W. and Pérez, S. 1996. A molecular builder for carbohydrates: applications to polysaccharides and complex carbohydrates. Biopolymers 39: 417–433.
Ermel, F.F., Follet-Gueye, M.L., Cibert, C., Vian, B., Morvan, C., Catesson, A.N. and Goldberg, R. 2000. Differential localization of arabinan and galactan side chains of rhamnogalacturonan 1 in cambial derivatives. Planta 210: 732–740.
Esquerré-Tugayé, M.-T., Boudart, G. and Dumas, B. 2000. Cell wall degrading enzymes, inhibitory proteins, and oligosaccha-rides participate in the molecular dialogue between plants and pathogens. Plant Physiol. Biochem. 38: 157–163.
Fagard, M., Höfte, H. and Vernhettes, S. 2000. Cell wall mutants. Plant Physiol. Biochem. 38: 15–25.
Fischer, R.L. and Bennett, A.B. 1991. Role of cell wall hydrolases in fruit ripening.Annu. Rev. Plant Physiol. Plant Mol. Biol. 42: 675–703.
Fleischer, A., O'Neill, M.A. and Ehwald, R. 1999. The pore size of non-graminaceous plant cell walls is rapidly decreased by borate ester cross-linking of the pectic polysaccharide rhamnogalacturonan II. Plant Physiol. 121: 829–838.
Fleischer, A., Titel, C. and Ehwald, R. 1998. The boron requirement and cell wall properties of growing and stationary suspension-cultured Chenopodium album L. cells. Plant Physiol. 117: 1401–1410.
Foster, T.J., Ablett, S., McCann, M.C. and Gidley, M.J. 1996. Mobility resolved C-13 NMR spectroscopy of primary plant cell walls. Biopolymers 39: 51–66.
Freshour, G., Clay, R.P., Fuller, M.S., Albersheim, P., Darvill, A.G. and Hahn, M.G. 1996. Developmental and tissue-specific struc-tural alterations of the cell wall polysaccharides of Arabidopsis thaliana roots. Plant Physiol. 110: 1413–1429.
Geshi, N., Jorgensen, B., Scheller, H.V. and Ulvskov, P. 2000. In vitro biosynthesis of 1,4,-β-galactan attached to rhamnogalacturonan I. Planta 210: 622–629.
Gibeaut, D.M. 2000. Nucleotide sugars and glycosyltransferases for synthesis of cell wall matrix polysaccharides. Plant Physiol. Biochem. 38: 69–80.
Gillet, C., Voué, M. and Cambier, P. 1998. Site-specific counter-ion binding and pectic chains conformational transitions in the Nitella cell wall. J. Exp. Bot. 49: 797–805.
Goubet, F. and Mohnen, D. 1999. Solubilization and partial charac-terization of homogalacturonan-methyltransferase from micro-somal membranes of suspension-cultured tobacco cells. Plant Physiol. 121: 281–290.
Guillon, F. and Thibault, J.-F. 1989. Methylation analysis and mild acid hydrolysis of the ‘hairy’ fragments of sugar beet pectins. Carbohydrate Res. 190: 85–96.
Hadfield, K.A. and Bennett, A.B. 1998. Polygalacturonases: many genes in search of a function. Plant Physiol. 117: 337–343.
Hart, D.A. and Kindel, P.K. 1970. Isolation and partial characterization of apiogalacturonans from the cell wall of Lemna minor. Biochem. J. 116: 569–579.
Herron, S.R., Benen, J.A.E., Scavetta, R.D., Visser, J. and Jurnak, F. 2000. Structure and function of pectic enzymes: virulence factors of plant pathogens. Proc. Natl. Acad. Sci. USA 97: 8762–8769
Ishii, T. 1997. O-Acetylated oligosaccharides from pectins of potato tuber cell walls. Plant Physiol. 113: 1265–1272
Ishii, T., Matsunaga, T., Pellerin, P., O'Neill, M.A., Darvill, A. and Albersheim, P. 1999. The plant cell wall polysaccharide rhamno-galacturonan II self-assembles into a covalently cross-linked dimer. J. Biol. Chem. 274: 13098–13104.
Ishikawa, M., Kuroyama, Y., Takeuchi, Y. and Tsumuraya, Y. 2000. Characterization of pectin methyltransferase from soybean hypocotyls. Planta 210: 782–791.
Jarvis, M.C. 1984. Structure and properties of pectin gels in plant cell walls. Plant Cell Envir. 7: 153–164.
Jarvis, M.C. 1992. Control of thickness of collenchyma cell walls by pectins. Planta187: 218–220.
Jarvis, M.C. and Apperley, D. 1995. Chain conformation in concen-trated pectin gels: evidence from 13 C NMR. Carbohydrate Res. 275: 131–145.
Jarvis, M.C., Forsyth, W. and Duncan, H.J. 1988. A survey of the pectic content of nonlignified monocot cell walls. Plant Physiol. 88: 309–314.
Jauneau, A., Roy, S., Reis, D. and Vian, B. 1998. Probes and microscopical methods for the localization of pectins in plant cells. Int. J. Plant Sci. 159: 1–13.
Jones, L., Seymour, G.B. and Knox, J.P. 1997. Localization of pec-tic galactan in tomato cell walls using a monoclonal antibody specific to (1→4)-β-D-galactan. Plant Physiol. 113: 1405–1412.
Kester, H.C.M., Benen, J.A.E. and Visser, J. 1999. The exopolygalacturonase from Aspergillus tubingensis is also active on xylogalacturonan. Biotechnol. Appl. Biochem. 30: 53–57.
Kester, H.C.M., Benen, J.A.E., Visser, J., Warren, M.E., Orlando, R., Bergmann, C., et al. 2000. Tandem mass spectrometric analysis of Aspergillus niger pectin methylesterase: mode of action on fully methyl-esterified oligogalacturonates. Biochem. J. 346: 469–474.
Kikuchi, A., Edashige, Y., Ishii, T. and Satoh, S. 1996. A xylo-galacturonan whose level is dependent on the size of cell clusters is present in the pectin from cultured carrot cells. Planta 200: 369–372.
Knox, J.P. 1992. Cell adhesion, cell separation and plant morpho-genesis. Plant J. 2: 137–141.
Knox, J.P. 1997. The use of antibodies to study the architecture and developmental regulation of plant cell walls. Int. Rev. Cytol. 171: 79–120.
Knox, J.P., Linstead, P.J., King, J., Cooper, C. and Roberts, K. 1990. Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apices. Planta 181: 512–521.
Kobayashi, M., Matoh, T. and Azuma, J. 1996. Two chains of rhamnogalacturonan II are cross-linked by borate-diol ester bonds in higher plant cell walls. Plant Physiol. 110: 1017–1020.
Kobayashi, M., Nakagawa, H., Asaka, T. and Matoh, T. 1999. Borate-rhamnogalacturonan II bonding re-inforced by Ca2 +retains pectic polysaccharides in higher plant cell walls. Plant Physiol. 119: 199–203.
Leckie, F., Mattei, B., Capodicasa, C., Hemmings, A., Nuss, L., Aracri, B., De Lorenzo, G. and Cervone, F. 1999. The specificity of polygalacturonase-inhibiting protein (PGIP): a single amino acid substitution in the solvent-exposed β-strand/β-turn region of the leucine-rich repeats (LRRs) confers a new recognition capability. EMBO J. 18: 2352–2363.
Le Goff, A., Renard, C.M.G.C., Bonnin, E. and Thibault, J.-F. 2001. Extraction, purification and chemical characterization of xylogalacturonans from pea hulls. Carbohydrate Polymers 45: 325–334.
Lerouge, P., O'Neill, M.A., Darvill, A.G. and Albersheim, P. 1993. Structural characterization of endo-glycanase-generated oligo-glycosyl sie chains of rhamnogalacturonan I. Carbohydrate Res. 243: 359–371.
Liberman, M., Mutaftschiev, S., Jauneau, A., Vian, B., Catesson, A.M. and Goldberg, R. 1999. Mung bean hypocotyl homogalac-turonan: localization, organization and origin. Ann. Bot. 84: 225–233.
Limberg, G., Körner, R., Bucholt, H.C., Christensen, T.M.I.E., Roepstorff, P. and Mikkelsen, J.D. 2000a. Analysis of different de-esterification mechanisms for pectin by enzymatic finger-printing using endopectin lyase and endopolygalacturonase II from A. niger. Carbohydrate Res. 327: 293–307.
Limberg, G., Körner, R., Bucholt, H.C., Christensen, T.M.I.E., Roepstorff, P. and Mikkelsen, J.D. 2000b. Quantification of the amount of galacturonic acid residues in block sequences in pectin homogalacturonan by enzymatic fingerprinting with exo-and endo-polygalacturonase II from Aspergillus niger. Carbohydrate Res. 327: 321–332.
Liners, F., Gaspar, T. and van Cutsem, P. 1994. Acetyl-and methyl-esterification of pectins of friable and compact sugar-beet calli: consequences for intercellular adhesion. Planta 192: 545–556.
Liners, F., Thibault, J.-F. and Van Cutsem, P. 1992. Influence of the degree of polymerization of oligogalacturonates and of esterification pattern on pectin on their recognition by monoclonal antibodies. Plant Physiol. 99: 1099–1104.
Longland, J.M., Fry, S.C. and Trewavas, A.J. 1989. Developmental control of apiogalacturonan biosynthesis and UDP-apiose production in a duckweed. Plant Physiol. 90: 972–976.
McCabe, P.F., Valentine, T.A., Forsberg, L.S. and Pennell, R.I., 1997. Soluble signals from cells identified at the cell wall establish a developmental pathway in carrot. Plant Cell 9: 2225–2241.
McCartney, L., Ormerod, A.P., Gidley, M.J. and Knox, J.P. 2000. Temporal and spatial regulation of pectic (1→4)-β-D-galactan in cell walls of developing pea cotyledons: implications for mechanical properties. Plant J. 22: 105–113.
Marty, P., Jouan, B., Bertheau, Y., Vian, B. and Goldberg, R. 1997. Charge density in stem cell walls of Solanum tuberosum genotypes and susceptibility to blackleg. Phytochemistry 44: 1435–1441.
Matoh, T., Takasaki, M., Takabe, K. and Kobayashi, M. 1998. Immunocytochemistry of rhamnogalacturonan II in cell walls of higher plants. Plant Cell Physiol. 39: 483–491.
Messiaen, J. and Van Cutsem, P. 1999. Polyamines and pectins. II. Modulation of pectic-signal transduction. Planta 208: 247–256.
Messiaen, J., Cambier, P. and Van Cutsem, P. 1997. Polyamines and pectins. I. Ion exchange and selectivity. Plant Physiol. 113: 387–395.
Micheli, F., Holliger, C., Goldberg, R. and Richard, L. 1998. Characterization of the pectin methylesterase-like gene AtPME3:a new member of a gene family comprising at least 12 genes in Arabidopsis thaliana. Gene 220: 13–20.
Moerschbacher, B.M., Mierau, M., Graessner, B., Noll, U. and Mort, A.J. 1999. Small oligomers of galacturonic acid are endogenous suppressors of disease resistance reactions in wheat leaves. J. Exp. Bot. 50: 605–612.
Mohnen, D. 1999. Biosynthesis of pectins and galactomannans. In: D. Barton, K. Nakanishi and O. Meth-Cohn (Eds.) Comprehensive Natural Products Chemistry, vol. 3, Elsevier Science, Amsterdam, pp. 497–527.
Mølgaard, A., Kauppinen, S. and Larsen, S. 2000. Rhamnogalacturonan acetylesterase elucidates the structure and function of a new family of hydrolases. Struct. Fold. Design 8: 373–383.
Mollet, J.-C., Park, S.-Y., Nothnagel, E.A. and Lord, E.M. 2000. A lily stylar pectin is necessary for pollen tube adhesion to an in vitro stylar matrix. Plant Cell 12: 1737–1749.
Morris, E.R., Powell, D.A., Gidley, M.J. and Rees, D.A. 1982. Conformation and interactions of pectins I. Polymorphism between gel and solid states of calcium polygalacturonate. J. Mol. Biol. 155: 507–516.
Mutter, M., Beldman, G., Pitson, S.M., Schols, H.A. and Voragen, A.G.J. 1998a. Rhamnogalacturonan α-D-galactopyranosyluronohydrolase: an enzyme that specifically removes the terminal nonreducing galacturonosyl residue in rhamnogalacturonan regions of pectin. Plant Physiol. 117: 153–163.
Mutter, M., Colquhoun, I.J., Beldman, G., Schols, H,A., Bakx, E.J. and Voragen, A.G.J. 1998b. Characterization of recombinant rhamnogalacturonan α-L-rhamnopyranosyl-(1,4)-α-D-galactopyranosyluronide lyase from Aspergillus aculeatus:an enzyme that fragments rhamnogalacturonan I regions of pectin. Plant Physiol. 117: 141–152.
Mutter, M., Renard, C.M.G.C., Beldman, G., Schols, H.A. and Voragen, A.G.J. 1998c. Mode of action of RG-hydrolase and RG-lyase toward rhamnogalacturonan oligomers. Characterization of degradation products using RG-rhamnohydrolase and RG-galacturonohydrolase. Carbohydrate Res. 311: 155–164.
Nothnagel, E. 1997. Proteoglycans and related components in plant cells. Int. Rev. Cytol. 174: 195–291.
O'Neill, M.A., Albersheim, P. and Darvill, A. 1990. The pectic polysaccharides of primary cell walls. In: P.M. Dey (Ed.) Methods in Plant Biochemistry, vol. 2, Academic Press, London, pp. 415–441.
O'Neill, M.A., Warrenfeltz, D., Kates, K., Pellerin, P., Doci, T., Darvill, A.G. and Albersheim, P. 1996. Rhamnogalacturonan-II, a pectic polysaccharide in the walls of growing plant cell, forms a dimer that is covalently-linked by a borate ester. J. Biol. Chem. 271: 22923–22930.
Orfila, C. and Knox, J.P. 2000. Spatial regulation of pectic polysac-charides in relation to pit fields in cell walls of tomato fruit pericarp. Plant Physiol. 122: 775–781.
Orfila, C., Seymour, G.B., Willats, W.G.T., Huxham, I.M., Jarvis, M.C., Dover, C.J., Thompson, A.J. and Knox, J.P. 2001. Altered middle lamella homogalacturonan and disrupted deposition of (1→5)-α-L-arabinan in the pericarp of Cnr, a ripening mutant of tomato. Plant Physiol. 126: 210–221.
Pauly, M. and Scheller, H.V. 2000. O-Acetylation of plant cell wall polysaccharides: identification and partial characterization of a rhamnogalacturonan O-acetyl-transferase from potato suspension-cultured cells. Planta 210: 659–667.
Petersen, T.N., Kauppinen, S. and Larsen, S. 1997. The crystal structure of rhamnogalacturonase A from Aspergillus aculeatus: a right-handed parallel β helix. Structure 5: 533–544.
Pérez, S., Mazeau, K. and du Penhoat, C.H. 2000. The three-dimensional structures of the pectic polysaccharides. Plant Physiol. Biochem. 38: 37–55.
Pilling, J., Willmitzer, L. and Fisahn, J. 2000. Expression of a Petunia inflata pectin methyl esterase in Solanum tuberosum L. enhances stem elongation and modifies cation distribution. Planta 210: 391–399.
Pitson, S.M., Voragen, A.G.J., Vincken, J.P. and Beldman, G. 1997. Action patterns and mapping of the substrate-binding regions of endo-(1→5)-α-L-arabinanases from Aspergillus niger and Aspergillus aculeatus. Carbohydrate Res. 303: 207–218.
Potgieter, M.J. and van Wyk, A.E. 1992. Intercellular pectic pro-tuberances in plants: their structure and taxonomic significance. Bot. Bull. Acad. Sin. 33: 295–316.
Powell, D.A., Morris, E.R., Gidley, M.J. and Rees, D.A. 1982. Conformation and interactions of pectins II. Influence of residue sequence on chain association in calcium pectate gels. J. Mol. Biol. 155: 517–531.
Prade, R.A., Zhan, D.F., Ayoubi, P. and Mort, A.J. 1999. Pectins, pectinases and plant-microbe interactions. Biotech. Genet. Eng. Rev. 16: 361–391.
Pulmann, J., Bucheli, E., Swain, M.J., Dunning, N., Albersheim, P., Darvill. A.G. and Hahn, M.G. 1994. Generation of monoclonal antibodies against plant cell wall polysaccharides. I. Characterization of a monoclonal antibody to a terminal α-(1→2)-linked fucosyl-containing epitope. Plant Physiol. 104: 699–710.
Qi, X.Y., Behrens, B.X., West, P.R. and Mort, A.J. 1995. Solubilization and partial characterization of extensin fragments from cell-walls of cotton suspension cultures: evidence for a covalent cross-link between extensin and pectin. Plant Physiol. 108: 1691–1701.
Redgwell, R.J. and Selvendran, R.R. 1986. Structural features of the cell wall polysaccharides of onion Allium cepa. Carbohydrate Res. 157: 183–199.
Renard, C.M.G.C., Crépeau, M.-J. and Thibault, J.-F. 1999. Glucuronic acid is directly linked to galacturonic acid in the rhamnogalacturonan backbone of beet pectins. Eur. J. Biochem. 266: 566–574.
Renard, C.C. and Jarvis, M.C. 1999a. Acetylation and methylation of homogalacturonans 1. Optimisation of the reaction and characterization of the products. Carbohydrate Polymers 39: 201–207.
Renard, C.M.G.C. and Jarvis, M.C. 1999b. A cross-polarization, magic-angle-spinning, 13C-NMR study of polysaccharides in sugar beet cell walls. Plant Physiol 119: 1315–1322.
Renard, C.M.G.C., Voragen, A.G.J., Thibault, J.-F. and Pilnik, W. 1991. Studies on apple protopectin V: structural studies on enzymatically extracted pectins. Carbohydr Polym 16: 137–154.
Renard, C.M.G.C., Weightman, R.M. and Thibault, J.F. 1997. The xylose-rich pectins from pea hulls. Int. J. Biol. Macromol. 21: 155–162.
Rhee, S. and Somerville, C. 1998. Tetrad pollen formation in quartet mutants of Arabidopsis thaliana is associated with persistence of pectic polysaccharides of the pollen mother cell wall. Plant J. 15: 79–88.
Roberts, J.A., Whitelaw, C.A., Gonzalez-Carranza, Z.H. and Mc-Manus, M.T. 2000. Cell separation processes in plants: models, mechanisms and manipulation. Ann. Bot. 86: 223–235.
Rogers, L.M., Kim, Y.-K., Guo, W., González-Candelas, L., Li, D. and Kolattukudy, P.E. 2000. Requirement for either a host-or pectin-induced pectate lyase for infection of Pisum sativum by Nectria hematococca. Proc. Natl. Acad. Sci. USA 97: 9813–9818.
Rojo, E., León, J. and Sánchez-Serrano, J.J.1999. Cross-talk between wound signalling pathways determines local versus systemic gene expression in Arabidopsis thaliana. Plant J. 20: 135–142.
Rombouts, F.M. and Thibault, J.F. 1986. Enzymatic and chemical degradation of the fine structure of pectins from sugar beet pulp. Carbohydrate Res. 256: 83–95.
Ros, J.M., Schols, H.A. and Voragen, A.G.J. 1996. Extraction, characterization, and enzymatic degradation of lemon peel pectins. Carbohydrate Res. 282: 271–284.
Rutherford, R. and Masson, P. 1996. Arabidopsis thaliana sku mutant seedlings show exaggerated surface dependent alteration in root growth vector. Plant Physiol. 111: 987–998.
Ryttersgaard, C., Poulsen, J.C.N., Christgau, S., Sandal, T., Dalboge, H. and Larsen, S. 1999. Crystallization and preliminary X-ray studies of β-l,4-galactanase from Aspergillus aculeatus. Acta Crystallogr. D55: 929–930.
Scavetta, R.D., Herron, S.R., Hotchkiss, A.T., Kita, N., Keen, N.T., Benen, J.A.E., et al. 1999. Structure of a plant cell wall fragment complexed to pectate lyase C. Plant Cell 11: 1081–1092.
Scheller, H.V., Doong, R.L., Ridley, B.L. and Mohnen, D. 1999. Pectin biosynthesis: a solubilized α-1,4-galacturonosyltransferase from tobacco catalyzes the transfer of galacturonic acid from UDP-galacturonic acid onto the non-reducing end of homogalacturonan. Planta 207: 512–517.
Schols, H.A., Bakx, E.J., Schipper, D. and Voragen, A.G.J. 1995. A xylogalacturonan subunit present in the modified hairy regions of apple pectin. Carbohydrate Res. 279: 265–279.
Schols, H.A. and Voragen, A.G.J. 1996. Complex pectins: structure elucidation using enzymes. In: J. Visser and A.G.J. Voragen (Eds.) Pectins and Pectinases, Elsevier Science, Amsterdam, pp. 3–19.
Schmohl, N. and Horst, W.J. 2000. Cell wall pectin content modulates aluminium sensitivity of Zea mays (L.) cells grown in suspension culture. Plant Cell Envir. 23: 735–742.
Scott, M., Pickersgill, R.W., Hazlewood, G.P., Gilbert, H.J. and Harris, G.W. 1999. Crystallization and preliminary X-ray analysis of arabinanase A from Pseudomonas fluorescens subspecies cellulosa. Acta Crystallogr. D55: 544–546.
Sedbrook, J., Hung, K., Carroll, K. and Masson, P. 1998. sku5, a mutation in a pectin esterase-like gene, confers an exaggerated right slanting phenotype on agar surfaces. 9th International Conference on Arabidopsis Research, University of Wisconsin-Madison, USA, abstract p109.
Shedletzky, E., Shmuel M., Trainin. T., Kalman, S. and Delmer, D. 1992. Cell wall structure in cells adapted to growth on the cellulose-synthesis inhibitor 2,6-dichlorobenzonitrile. Plant Physiol. 100: 120–130.
Shevchik, V.E. and HugouvieuxCottePattat, N. 1997. Identification of a bacterial pectin acetyl esterase in Erwinia chrysanthemi 3937. Mol. Microbiol. 24: 1285–1301.
Sieber, P., Schorderet, M., Ryser, U., Buchala, A., Kolattukudy, P., Métraux, J.-P. and Nawrath, C. 2000. Transgenic arabidopsis plants expressing a fungal cutinase show alterations in the structure and properties of the cuticle and postgenital organ fusions. Plant Cell 12: 721–737.
Simpson, S.D., Ashford, D.A., Harvey, D.J. and Bowles, D.J. 1998. Short chain oligogalacturonides induce ethylene production and expression of the gene encoding aminocyclopropane 1-carboxylic acid oxidase in tomato plants. Glycobiology 8: 579–583.
Sinha, N. and Lynch, M. 1998. Fused organs in the adherent1 mutation in maize show altered epidermal walls with no perturbations in tissue identities. Planta 206: 184–195.
Smith, B.G. and Harris, P.J. 1999. The polysaccharide composition of Poales cell walls: Poaceae cell walls are not unique. Biochem. System. Ecol. 27:33–53.
Smith, C.J.S, Watson, C.F., Morris, P.C., Bird, C.R., Seymour, G.B., Gray, J.E., et al. 1990. Inheritance and effect on ripening of antisense polygalacturonase genes in transgenic tomatoes. Plant Mol. Biol. 14: 369–379.
Smith, D.L. and Gross, K.C. 2000. A family of at least seven β-galactosidase genes is expressed during tomato fruit development. Plant Physiol. 123: 1173–1183.
Sørensen, S.O., Pauly, M., Bush. M., Skjøt, M., McCann, M.C., Borkhardt, B. and Ulvskov, P. 2000. Pectin engineering: modification of potato pectin by in vivo expression of an endo-1,4-β-D-galactanase. Proc. Natl. Acad. Sci. USA 97: 7639–7644.
Steele-King, C.G., Willats, W.G.T. and Knox, J.P. 2000. Arabinogalactan-proteins and cell development in roots and somatic embryos. In: E.A. Nothnagel, A Bacic and A.E. Clarke (Eds.) Cell and Developmental Biology of Arabinogalactan Proteins, Kluwer Academic Publishers Plenum, pp. 95–108.
Tegeder, M., Wang, X.-D., Frommer, W.B., Offler, C.E. and Patrick, J.W. 1999. Sucrose transport into developing seeds of Pisum sativum L. Plant J. 18: 151–161.
Thibault, J.F., Renard, C.M.G.C., Axelos, M.V., Roger, P. and Crepeau, M.J. 1993. Studies of the length of homogalacturonic regions in pectins by acid-hydrolysis. Carbohydrate Res. 238: 271–286.
Thompson, A.J., Tor, M., Barry, C.S., Vrebalov, J., Orfila, C., Jarvis, M.C., et al. 1999. Molecular and genetic characterization of a novel pleiotropic tomato-ripening mutant. Plant Physiol. 120: 383–389.
Thompson, J.E. and Fry, S.C. 2000. Evidence for covalent linkage between xyloglucan and acidic pectins in suspension-cultured rose cells. Planta 211: 275–286.
Tibbits, C.W., MacDougall, A.J. and Ring, S.G. 1998. Calcium binding and swelling behaviour of a high methoxyl pectin gel. Carbohydrate Res. 310: 101–107.
Tieman, D.M. and Handa, A.K. 1994. Reduction in pectin methylesterase activity modifies tissue integrity and cation levels in ripening tomato (Lycopersicon esculentum Mill.) fruits. Plant Physiol. 106: 429–436.
Torki, M., Mandaron, P., Mache, R. and Falconet, D. 2000. Characterization of a ubiquitous expressed gene family encoding polygalacturonase in Arabidopsis thaliana. Gene 242: 427–436.
van Alebeek, G.J.,W.M., Zabotina, O., Beldman, G., Schols, H.A. and Voragen, A.G.J. 2000.Esterification and glycosidation of oligogalacturonides: examination of the reaction products using MALDI-TOF MS and HPAEC. Carbohydrate Polymers 43: 39–46.
VandenBosch, K.A., Bradley, D.J., Knox, J.P., Perotto, S., Butcher, G.W. and Brewin, N.J. 1989. Common components of the infection thread matrix and the intercellular space identified by immunocytochemical analysis of pea nodules and uninfected roots. EMBO J. 8: 335–342.
van der Vlugt-Bergmans, C.J.B., Meeuwsen, P.J.A., Voragen, A.G.J. and van Ooyen, A.J.J. 2000. Endo-xylogalacturonan hydrolase, a novel pectinolytic enzyme. Appl. Envir. Microbiol. 66: 36–41.
van Santen, Y., Benen, J.A.E., Schröter, K.-H., Kalk, K.H., Armand, S., Visser, J. and Dijkstra, B.W. 1999. 1.68-Å crystal structure of endopolygalacturonase II from Aspergillus niger and identification of active site residues by site-directed mutagenesis. J. Biol. Chem. 274: 30474–30480.
Vicré, M., Jauneau, A., Knox, J. P. and Driouich A. 1998. Immunolocalization of β(1→4)-and β (1→6)-D-galactan epitopes in the cell wall and Golgi stacks of developing flax root tissues. Protoplasma 203: 26–34.
Vidal, S., Salmon, J.M., Williams, P. and Pellerin, P. 1999. Penicillium daleae, a soil fungus able to degrade rhamnogalacturonan II, a complex pectic polysaccharide. Enzyme Microbiol. Technol. 24: 283–290.
Vidal, S., Doco, T., Williams, P., Pellerin, P., York, W.S., O'Neill, M.A., et al. 2000. Structural characterization of the pectic polysaccharide rhamnogalacturonan II: evidence for the back-bone location of the aceric acid-containing oligoglycosyl side chain. Carbohydrate Res. 326: 277–294
Vitali, J., Schick, B., Kester, H.C.M., Visser, J. and Jurnak, F. 1998. The three-dimensional Structure of Aspergillus niger pectin lyase B at 1.7 Å resolution. Plant Physiol. 116: 69–80.
Wallace, G. and Fry, S.C 1994. Phenolic components of the plant cell wall. Int. Rev. Cytol. 151: 229–267.
Walkinshaw, M.D. and Arnott, S. 1981. Conformations and interactions of pectins. II. Models of junction zones in pectinic acid and calcium pectate gels. J. Mol. Biol. 53: 1075–1085.
Wen, F., Zhu, Y. and Hawes, M.C. 1999. Effect of pectin methylesterase gene expression on pea root development. Plant Cell 11: 1129–1140.
Willats, W.G.T., Marcus, S.E. and Knox J.P. 1998. Generation of a monoclonal antibody specific to (1→5)-α-L-arabinan. Carbohydrate Res. 308: 149–152.
Willats, W.G.T., Gilmartin P.M., Mikkelsen, J.D. and Knox, J.P. 1999a. Cell wall antibodies without immunization: Generation and use of de-esterified homogalacturonan block-specific antibodies from a naive phage display library. Plant J. 18: 57–65.
Willats, W.G.T., Steele-King, C.G., Marcus, S.E. and Knox, J.P. 1999b. Side chains of pectic polysaccharides are regulated in relation to cell proliferation and cell differentiation. Plant J. 20: 619–628.
Willats, W.G.T., Limberg, G., Bucholt, H.C., van Alebeek, G.-J., Benen, J., Christensen, T. M.I.E., et al. 2000a. Analysis of pectic epitopes recognised by hybridoma and phage display monoclonal antibodies using defined oligosaccharides, polysaccharides and enzymatic degradation. Carbohydrate Res. 327: 309–320.
Willats, W.G.T., Steele-King, C.G., McCartney, L., Orfila, C., Marcus S.E. and Knox, J.P. 2000b. Making and using antibody probes to study plant cell walls. Plant Physiol. Biochem. 38: 27–36.
Willats, W.G.T., Orfila, C., Limberg, G., Buchholt, H.C., van Ale-beek, G.-J.W.M., Voragen, A.G.J., et al. 2001. 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. J. Biol. Chem. 276: 19404–19413.
Williams, M.N.V., Freshour, G., Darvill, A.G., Albersheim, P. and Hahn, M.G. 1996. An antibody Fab selected from a recombinant phage display library detects deesterified pectic polysaccharide rhamnogalacturonan II in plant cells. Plant Cell 8: 673–685.
Williamson, G. 1991. Purification and characterization of pectin acetylesterase from orange peel. Phytochemistry 30: 445–449.
Yao, C., Conway, W.S., Ren, R., Smith, D., Ross, G.S. and Sams, C.E. 1999. Gene encoding polygalacturonase inhibitor in apple fruit is developmentally regulated and activated by wounding and fungal infection. Plant Mol. Biol. 39: 1231–1241.
Yu, L. and Mort, A.J. 1996. Partial characterization of xylogalacturonans from cell walls of ripe watermelon fruit: inhibition of endopolygalacturonase activity by xylosylation. In: J Visser and A.G.J. Voragen (Eds.) Pectins and Pectinases, Elsevier Science, Amsterdam, pp. 79–88.
Zhan, D., Janssen, P. and Mort, A.J. 1998. Scarcity or complete lack of single rhamnose residues interspersed within the homogalacturonan regions of citrus pectin. Carbohydrate Res. 308: 373–380.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Willats, W.G., McCartney, L., Mackie, W. et al. Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47, 9–27 (2001). https://doi.org/10.1023/A:1010662911148
Issue Date:
DOI: https://doi.org/10.1023/A:1010662911148