[en] Wall-associated kinase 1--WAK1 is a transmembrane protein containing a
cytoplasmic Ser/Thr kinase domain and an extracellular domain in contact with the
pectin fraction of the plant cell wall in Arabidopsis thaliana (L.) HEYNH. In a
previous paper [Decreux, A., Messiaen, J., 2005. Wall-associated kinase WAK1
interacts with cell wall pectins in a calcium-induced conformation. Plant Cell
Physiol. 46, 268-278], we showed that a recombinant peptide expressed in yeast
corresponding to amino acids 67-254 of the extracellular domain of WAK1
specifically interacts with commercial non-methylesterified homogalacturonic
acid, purified homogalacturonans from Arabidopsis and oligogalacturonides in a
calcium-induced conformation. In this report, we used a receptor binding domain
sequence-based prediction method to identify four putative binding sites in the
extracellular domain of WAK1, in which cationic amino acids were selected for
substitution by site-directed mutagenesis. Interaction studies between mutated
forms of WAK1 and homogalacturonans allowed us to identify and confirm at least
five specific amino acids involved in the interaction with homogalacturonan
dimers and multimers. The presence of this homogalacturonan-binding domain within
the extracellular domain of WAK1 is discussed in terms of cell wall architecture
and signal transduction.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Decreux, Annabelle ; Université de Liège - ULiège > Pathologie spéciale et autopsies
Thomas, Annick ; Université de Liège - ULiège > Chimie et bio-industries > Centre de Bio. Fond. - Section de Biologie moléc. et numér.
Spies, B.
Brasseur, Robert ; Université de Liège - ULiège > Gembloux Agro-Bio Tech
Van Cutsem, P.
Messiaen, J.
Language :
English
Title :
In Vitro Characterization Of The Homogalacturonan-Binding Domain Of The Wall-Associated Kinase Wak1 Using Site-Directed Mutagenesis
Anderson C.M., Wagner T.A., Perret M., He Z.H., He D., and Kohorn B.D. WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrix. Plant Mol. Biol. 47 (2001) 197-206
Bellincampi D., Dipierro N., Salvi G., Cervone F., and De Lorenzo G. Extracellular H2O2 induced by oligogalacturonides is not involved in the inhibition of the auxin-regulated rolB gene expression in tobacco leaf explants. Plant Physiol. 122 (2000) 1379-1385
Carpin S., Crevecoeur M., de Meyer M., Simon P., Greppin H., and Penel C. Identification of a Ca(2+)-pectate binding site on an apoplastic peroxidase. Plant Cell 13 (2001) 511-520
Combet C., Blanchet C., Geourjon C., and Deleage G. NPS@: network protein sequence analysis. TIBS 25 (2000) 147-150
Decreux A. Study of the receptor-like kinase WAK1 from Arabidopsis thaliana. Highlighting and Characterization of the Interaction of WAK1 Extracellular Domain with Pectin (2006), Presses Universitaires de Namur, Namur, Belgium
Decreux A., and Messiaen J. Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol. 46 (2005) 268-278
De Loof H., Rosseneu M., Brasseur R., and Ruysschaert J.M. Use of hydrophobicity profiles to predict receptor binding domains on apolipoprotein E and the low density lipoprotein apolipoprotein B-E receptor. Proc. Natl. Acad. Sci. USA 83 (1986) 2295-2299
Eisenberg D., Weiss R.M., and Terwilliger T.C. The helical hydrophobic moment: a measure of the amphiphilicity of a helix. Nature 299 (1982) 371-374
Eisenberg D., Schwarz E., Komaromy M., and Wall R. Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J. Mol. Biol. 179 (1984) 125-142
Ferguson H.A., and Goodrich J.A. Expression and purification of recombinant human c-Fos/c-Jun that is highly active in DNA binding and transcriptional activation in vivo. Nucleic Acid Res. 29 (2001) e98
Fiete D.J., Beranek M.C., and Baenziger J.U. A cysteine-rich domain of the "mannose" receptor mediates GalNAc-4-SO4 binding. Proc. Natl. Acad. Sci. USA 95 (1998) 2089-2093
Gaboriaud C., Bissery V., Benchetrit T., and Mornon J.P. Hydrophobic cluster analysis: an efficient new way to compare and analyse amino acid sequences. FEES Lett. 224 (1987) 149-155
Gallet X., Charloteaux B., Thomas A., and Brasseur R. A fast method to predict protein interaction sites from sequences. J. Mol. Biol. 302 (2000) 917-926
He Z.H., Cheeseman I., He D., and Kohorn B.D. A cluster of five cell wall-associated receptor kinase genes, Wakl-5, are expressed in specific organs of Arabidopsis. Plant Mol. Biol. 39 (1999) 1189-1196
He Z.H., Fujiki M., and Kohorn B.D. A cell wall-associated, receptor-like protein kinase. J. Biol. Chem. 271 (1996) 19789-19793
He Z.H., He D., and Kohorn B.D. Requirement for the induced expression of a cell wall associated receptor kinase for survival during the pathogen response. Plant J. 14 (1998) 55-63
Johansson K., El-Ahmad M., Friemanna R., Jornvall H., Markovic O., and Eklund H. Crystal structure of plant pectin methylesterase. FEES Lett. 514 (2002) 243-249
Lally D., Ingmire P., Tong H.Y., and He Z.H. Antisense expression of a cell wall-associated protein kinase, WAK4, inhibits cell elongation and alters morphology. Plant Cell 13 (2001) 1317-1331
Lemesle-Varloot L., Henrissat B., Gaboriaud C., Bissery V., Morgat A., and Mornon J.P. Hydrophobic cluster analysis: procedures to derive structural and functional information from 2-D-representation of protein sequences. Biochimie 72 (1990) 555-574
Liners F., Letesson J.J., Didembourg C., and Van Cutsem P. Monoclonal antibodies against pectin - recognition of a conformation induced by calcium. Plant Physiol. 91 (1989) 1419-1424
Liners F., Thibault J.F., and Van Cutsem P. Influence of the degree of polymerization of oligogalacturonates and of esterification pattern of pectin on their recognition by monoclonal antibodies. Plant Physiol. 99 (1992) 1099-1104
Liners F., and Van Cutsem P. Distribution of pectic polysaccharides throughout wall of suspension-cultured carrot cells. Protoplasma 170 (1992) 10-21
Manfield I.W., Bernal A.J., Moller I., McCartney L., Riess N.P., Knox J.P., and Willats W.G.T. Re-engineering of the PAM1 phage display monoclonal antibody to produce a soluble, versatile anti-homogalacturonan scFv. Plant Sci. 169 (2005) 1090-1095
Mauro M.L., De Lorenzo G., Costantino P., and Bellincampi D. Oligogalacturonides inhibit the induction of late but not of early auxin-responsive genes in tobacco. Planta 215 (2002) 494-501
Messiaen J., Read N.D., Van Cutsem P., and Trewavas A.J. Cell wall elicitors increase cytosolic free Ca2+ in plant cells. J. Cell Sci. 104 (1993) 365-371
Messiaen J., and Van Cutsem P. Defense gene transcription in carrot cells treated with oligogalacturonides. Plant Cell Physiol. 34 (1993) 1117-1123
Messiaen J., and Van Cutsem P. Pectic signal transduction in carrot cells: membrane, cytosolic and nuclear responses induced by oligogalacturonides. Plant Cell Physiol. 35 (1994) 677-689
Mollet J.C., Park S.Y., Nothnagel E.A., and Lord E.M. A lily stylar pectin is necessary for pollen tube adhesion to an in vitro stylar matrix. Plant Cell 12 (2000) 1737-1749
Morris E.R., Powell D.A., Gidley M.J., and Rees D.A. Conformations and interactions of pectins. I. Polymorphism between gel and solid states of calcium polygalacturonate. J. Mol. Biol. 155 (1982) 507-516
Niture S.K., Pant A., and Kumar A.R. Active site characterization of the single endo- polygalacturonase produced by Fusarium moniliforme NCIM 1276. Eur. J. Biochem. 268 (2001) 832-840
Park A.R., Cho S.K., Yun U.J., Jin M.Y., Lee S.H., Sachetto-Martins G., and Park O.K. Interaction of the Arabidopsis receptor protein kinase Wakl with a glycine-rich protein, AtGRP-3. J. Biol. Chem. 276 (2001) 26688-26693
Peumans W.J., Rouge P., and van Damme E.J.M. The tomato lectin consists of two homologous chitin-binding modules separated by an extensin-like linker. Biochem. J. 376 (2003) 717-724
Powell D.A., Morris E.R., Gidley M.J., and Rees D.A. Conformations and interactions of pectins. II. Influence of residue sequence on chain association in calcium pectate gels. J. Mol. Biol. 155 (1982) 517-531
Ridley B.L., O'Neill M.A., and Mohnen D. Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57 (2001) 929-967
Scavetta R.D., Herron S.R., Hotchkiss A.T., Kita N., Keen N.T., Benen J.A.E., Kester H.C.M., Visser J., and Jurnak F. Structure of a plant cell wall fragment complexed to pectate lyase C. Plant Cell 11 (1999) 1081-1092
Shah K., Penel C., Gagnon J., and Dunand C. Purification and identification of a Ca2+-pectate binding peroxidase from Arabidopsis leaves. Phytochemistry 65 (2004) 307-312
Shiu S.H., and Bleecker A.B. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc. Natl. Acad. Sci. USA 98 (2001) 10763-10768
Trotochaud A.E., Hao T., Wu G., Yang Z., and Clark S.E. The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein. Plant Cell 11 (1999) 393-406
Verica J.A., Chae L., Tong H., Ingmire P., and He Z.H. Tissue-specific and develop-mentally regulated expression of a cluster of tandemly arrayed cell wall-associated kinase-like kinase genes in Arabidopsis. Plant Physiol. 133 (2003) 1732-1746
Verica J.A., and He Z.H. The cell wall-associated kinase (WAK) and WAK-like kinase gene family. Plant Physiol. 129 (2002) 455-459
Wagner T.A., and Kohorn B.D. Wall-associated kinases are expressed throughout plant development and are required for cell expansion. Plant Cell 13 (2001) 303-318
Willats W.G.T., Orfila C., Limberg G., Buchholt H.C., van Alebeek G.J.W.M., Vor-agen A.G.J., Marcus S.E., Christensen T.M.I.E., Mikkelsen J.D., Murray B.S., and Knox J.P. 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. 273 (2001) 19404-19413
Woodcock S., Mornon J.P., and Henrissat B. Detection of secondary structure elements in proteins by hydrophobic cluster analysis. Protein Eng. 5 (1992) 629-635
Yang E.J., Oh Y.A., Lee E.S., Park A.R., Cho S.K., Yoo Y.J., and Park O.K. Oxygen-evolving enhancer protein 2 is phosphorylated by glycine-rich protein 3/wall-associated kinase 1 in Arabidopsis. Biochem. Biophys. Res. Commun. 305 (2003) 862-868
