Homogalacturonan synthesis in Arabidopsis thaliana requires a Golgi-localized protein with a putative methyltransferase domain

Plant Journal

Volumn 50, Issue 4, 2007, Pages 605-614

  Mouille, Grégory ^a   Ralet, Marie Christine ^b   Cavelier, Céline ^a   Eland, Cathlene ^c   Effroy, Delphine ^a   Hématy, Kian ^a   McCartney, Lesley ^a   Truong, Hoai Nam ^a   Gaudon, Virginie ^a   Thibault, Jean François ^b   Marchant, Alan ^c   Höfte, Herman ^a  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

^b INRA   (France)

^c SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

Arabidopsis; Homogalacturonan; Methyltransferase; Pectin; Plant cell wall

Indexed keywords

BIOSYNTHESIS; CELL ADHESION; ENZYMES; PLANT CELL CULTURE; POLYSACCHARIDES;

ARABIDOPSIS; HOMOGALACTURONAN; METHYLTRANSFERASE; PLANT CELL WALL;

PLANTS (BOTANY);

ARABIDOPSIS PROTEIN; GREEN FLUORESCENT PROTEIN; METHYLTRANSFERASE; PECTIN; POLYGALACTURONIC ACID;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; CONFOCAL MICROSCOPY; ENZYMOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; GOLGI COMPLEX; INFRARED SPECTROSCOPY; METABOLISM;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; GOLGI APPARATUS; GREEN FLUORESCENT PROTEINS; METHYLTRANSFERASES; MICROSCOPY, CONFOCAL; PECTINS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

BIOSYNTHESIS; CELLS; ENZYMES; PECTINS; PLANTS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 34248383533     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2007.03086.x     Document Type: Article

References (48)

1. Ahmed, A.R. Labavitch, J.M. (1977) A simplified method for accurate determination of cell wall uronide content. J. Food Biochem. 1, 361 365.
2. Blakeney, A.B., Harris, P.J., Henry, R.J. Stone, B.A. (1983) A simple and rapid preparation of alditol acetates for monosaccharide analysis. Carbohydr. Res. 113, 291 299.
3. Bonnin, E., Le Goff, A., Körner, R., van Alebeek, G.J.W.M., Christensen, T.M.I.E., Voragen, A.G.J., Roepstorff, P., Caprari, A. Thibault, J.-F. (2001) Study of the mode of action of endopolygalacturonase from Fusarium moniliforme. Biochim. Biophys. Acta, 1526, 301 309.
4. Bourlard, T., Schaumann-Gaudinet, A., Bruyant-Vannier, M.-P. Morvan, C. (1997) Various pectin methyltransferase activities with affinity for low and highly methylated pectins. Plant Cell Physiol. 38, 259 267.
5. Bouton, S., Leboeuf, E., Mouille, G., Leydecker, M.-T., Talbotec, J., Granier, F., Lahaye, M., Höfte, H. Truong, H.N. (2002) QUASIMODO1 encodes a putative membrane-bound glycosyltransferase required for normal pectin synthesis and cell adhesion in Arabidopsis. Plant Cell, 14, 2577 2590.
6. Brandizzi, F., Snapp, E.A.G.R., Lippincott-Schwartz, J. Hawes, C. (2002) Membrane protein transport between the endoplasmic reticulum and the Golgi in tobacco leaves is energy dependent but cytoskeleton independent: evidence from selective photobleaching. Plant Cell, 14, 1293 1309.
7. Caprari, C., Mattei, B., Basile, M.L., Salvi, G., Crescenzi, V., De Lorenzo, G. Cervone, F. (1996) 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). Mol. Plant Microbe Interact. 9, 617 624.
8. Craigon, D.J., James, N., Okyere, J., Higgins, J., Jotham, J. May, S. (2004) NASCArrays: a repository for microarray data generated by NASC's transcriptomics service. Nucl. Acids Res. 32, 575 577.
9. Doong, R.L. Mohnen, D. (1998) Solubilization and characterization of a galacturonyltransferase that synthesizes the pectic polysaccharide homogalacturonan. Plant J. 13, 363 374.
10. Dunkley, T. P., Hester, S., Shadforth, I. P. et al. (2006) Mapping the Arabidopsis organelle proteome. Proc. Natl Acad. Sci. USA, 103, 6518 6523.
11. Estelle, M.A. Somerville, C.R. (1987) Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology. Mol. Gen. Genet. 206, 200 206.
12. Filisetti-Cozzi, T.M.C.C. Carpita, N.C. (1991) Measurement of uronic acids without interference from neutral sugars. Anal. Biochem. 197, 157 162.
13. Goubet, F. Mohnen, D. (1999a) Solubilization and partial characterization of homogalacturonan-methyltransferase from microsomal membranes of suspension-cultured tobacco cells. Plant Physiol. 121, 281 290.
14. Goubet, F. Mohnen, D. (1999b) Subcellular localization and topology of homogalacturonan methyltransferase in suspension-cultured Nicotiana tabacum cells. Planta, 209, 112 117.
15. Goubet, F., Council, L.N. Mohnen, D. (1998) Identification and partial characterization of the pectin methyltransferase 'homogalacturonan- methyltransferase' from membranes of tobacco cell suspensions. Plant Physiol. 116, 337 347.
16. Guillaumie, F., Sterling, J.D., Jensen, K.J., Thomas, O.R.T. Mohnen, D. (2003) Solid-supported enzymatic synthesis of pectic oligogalacturonides and their analysis by MALDI-TOF mass spectrometry. Carbohydr. Res. 338, 1951 1960.
17. Henrissat, B., Coutinho, P.M. Davies, G.J. (2001) A census of carbohydrate-active enzymes in the genome of Arabidopsis thaliana. Plant Mol. Biol. 47, 55 72.
18. Ishikawa, M., Kuroyama, H., Takeuchi, Y. Tsumuraya, Y. (2000) Characterization of pectin methyltransferase from soybean hypocotyls. Planta, 210, 782 791.
19. Iwai, H., Masaoka, N., Ishii, T. Satoh, S. (2002) A pectin glucuronyltransferase gene is essential for intercellular attachment in the plant meristem. Proc. Natl Acad. Sci. USA, 25, 16319 16324.
20. Kapila, J., de Rycke, R., van Montagu, M. Angenon, G. (1997) An Agrobacterium-mediated transient gene expression system for intact leaves. Plant Sci. 122, 101 108.
21. Kohn, R., Markovic, O. Machova, E. (1983) Deesterification mode of pectin by pectin esterases of Aspergillus foetidus. Collect. Czech Chem. Commun. 48, 790 797.
22. Komalavilas, P. Mort, A.J. (1989) The acetylation at O-3 of GalA in the rhamnose-rich portion of pectins. Carbohydr. Res. 189, 261 272.
23. Kumar, S., Tamura, K. Nei, M. (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5, 150 163.
24. Levigne, S., Thomas, M., Ralet, M.-C., Quéméner, B. Thibault, J.-F. (2002) Determination of the degrees of methylation and acetylation of pectins using a C18 column and internal standards. Food Hydrocolloids, 16, 547 550.
25. Limberg, G., Korner, R., Buchholt, H.C., Christensen, T.M, Roepstorff, P. Mikkelsen, J.D. (2000) 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. Carbohydr. Res. 327, 321 332.
26. Marchler-Bauer, A. Bryant, SH. (2004) cd-search: protein domain annotations on the fly. Nucl. Acids Res. 32, 327 331.
27. Mohnen, D 1999) Biosynthesis of pectins and galactomannans. In Comprehensive Natural Products Chemistry, Vol. 3 (Barton, D., Nakanishi, K., Meth-Cohn, O., eds). Amsterdam : Elsevier, pp. 498 527.
28. Mouille, G., Robin, S., Lecomte, M., Pagant, S. Hofte, H. (2003) Classification and identification of Arabidopsis cell wall mutants using Fourier-transform-infrared (FT-IR) microspectroscopy. Plant J. 35, 393 404.
29. Northcote, D.H. Pickett-Heaps, J.D. (1966) A function of the Golgi apparatus in polysaccharide synthesis and transport in the root-cap cells of wheat. Biochem. J. 98, 159 167.
30. Perrone, P., Hewage, C.M., Thomson, A.R., Bailey, K., Sadler, I.H. Fry, S.C. (2002) Patterns of methyl and O-acetyl esterification in spinach pectins: new complexity. Phytochemistry, 60, 67 77.
31. Ralet, M.-C., Crépeau, M.-J., Buchholt, H.-C. Thibault, J.-F. (2003) Polyelectrolyte behaviour and calcium binding properties of sugar beet pectins differing in their degrees of methylation and acetylation. Biochem. Eng. J. 16, 191 201.
32. Ralet, M.-C., Cabrera, J.C., Bonnin, E., Quéméner, B., Hellìn, P. Thibault, J.-F. (2005) Mapping sugar beet pectin acetylation pattern. Phytochemistry, 66, 1832 1843.
33. Renard, C.M.G.C., Crépeau, M.-J. Thibault, J.-F. (1999) Glucuronic acid directly linked to galacturonic acid in the rhamnogalacturonan backbone of beet pectins. Eur. J. Biochem. 266, 566 574.
34. Robert, S., Bichet, A., Grandjean, O., Kierzkowski, D., Satiat-Jeunemaitre, B., Pelletier, S., Hauser, M.-T., Hofte, H. Vernhettes, S (2005) An Arabidopsis endo-1,4-β-d-glucanase involved in cellulose synthesis undergoes regulated intracellular cycling. Plant Cell, 17, 3378 3389.
35. Robin, S., Lecomte, M., Höfte, H. Mouille, G (2003) A procedure for the clustering of cell wall mutants in the model plant Arabidopsis based on Fourier-transform infrared (FT-IR) spectroscopy. J. Appl. Stat. 30, 669 681.
36. Rosso, M.G., Li, Y., Strizhov, N., Reiss, B., Dekker, K. Weisshaar, B. (2003) An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol. Biol. 53, 247 259.
37. Saeman, J.F., Moore, W.E., Mitchell, R.L. Millet, M.A. (1954) Techniques for the determination of pulp constituents by quantitative paper chromatography. Tappi, 37, 336 343.
38. Sterling, J.D., Atmodjo, M.A., Inwood, S.E., Kumar Kolli, V.S., Quigley, H.F., Hahn, M.G. Mohnen, D. (2006) Functional identification of an Arabidopsis pectin biosynthetic homogalacturonan galacturonosyltransferase. Proc. Natl Acad. Sci. USA, 103, 5236 5241.
39. Thibault, J.-F. (1979) Automated method for the determination of pectic substances. Lebensm. Wiss. Technol. 12, 247 251.
40. Thibault, J.-F. Rinaudo, M. (1985) Interaction of mono- and divalent counterions with alkali- and enzyme-deesterified pectins in salt-free solution. Biopolymers, 24, 2131 2143.
41. Thibault, J.-F., Renard, C.M.G.C., Axelos, M.A.V., Roger, P. Crépeau, M.-J. (1993) Studies of the length of homogalacturonic regions in pectins by acid-hydrolysis. Carbohydr. Res. 238, 271 286.
42. Tollier, M.T. Robin, J.P. (1979) Adaptation de la méthode à l'orcinol sulfurique au dosage automatique des oses neutres et totaux. Ann. Technol. Agric. 28, 1 15.
43. Toufighi, K., Brady, S.M., Austin, R., Ly, E. Provart, N.J. (2005) The Botany Array Resource: e-Northerns, Expression Angling, and promoter analyses. Plant J. 43, 153 163.
44. Wen-jun, S. Forde, B.G. (1989) Efficient transformation of Agrobacterium spp. by high voltage electroporation. Nucl. Acids Res. 17, 8385 8390.
45. Willats, W.G., Gilmartin, P.M., Mikkelsen, J.D. Knox, J.P. (1999) 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.
46. Willats, W.G., McCartney, L., Mackie, W. Knox, J.P. (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol. Biol. 47, 9 27.
47. Zhang, G.F. Staehelin, L.A. (1992) Functional compartmentation of the Golgi apparatus of plant cells: immunocytochemical analysis of high-pressure frozen and freeze-substituted sycamore maple suspension culture cells. Plant Physiol. 99, 1070 1083.
48. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L. Gruissem, W. (2004) genevestigator. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621 2632.