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WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrix

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Plant Cell Walls

Abstract

There are only a few proteins identified at the cell surface that could directly regulate plant cell wall functions. The cell wall-associated kinases (WAKs) of angiosperms physically link the plasma membrane to the carbohydrate matrix and are unique in that they have the potential to directly signal cellular events through their cytoplasmic kinase domain. In Arabidopsis there are five WAKs and each has a cytoplasmic serine/threonine protein kinase domain, spans the plasma membrane, and extends a domain into the cell wall. The WAK extracellular domain is variable among the five isoforms, and collectively the family is expressed in most vegetative tissues. WAK1 and WAK2 are the most ubiquitously and abundantly expressed of the five tandemly arrayed genes, and their messages are present in vegetative meristems, junctions of organ types, and areas of cell expansion. They are also induced by pathogen infection and wounding. Recent experiments demonstrate that antisense WAK expression leads to a reduction in WAK protein levels and the loss of cell expansion. A large amount of WAK is covalently linked to pectin, and most WAK that is bound to pectin is also phosphorylated. In addition, one WAK isoform binds to a secreted glycine-rich protein (GRP). The data support a model where WAK is bound to GRP as a phosphorylated kinase, and also binds to pectin. How WAKs are involved in signaling from the pectin extracellular matrix in coordination with GRPs will be key to our understanding of the cell wall’s role in cell growth.

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Abbreviations

ECM:

extracellular matrix

EGF:

epidermal growth factor

GA:

gibberellic acid

GRP:

glycine-rich protein

GST:

glutathione S-transferase

GUS:

β-glucuronidase

INA:

2,2-dichloroisonicotinic acid

KAPP:

protein type 2C phosphatase

SA:

salicylic acid

SAR:

systemic acquired resistance

SRK:

S-locus receptor kinase

WAK:

wall-associated kinase

References

  • Arabidopsis Genome Initiative. 2000. Analysis of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.

    Google Scholar 

  • Baskin, T.I., Meekes, H.T., Liang, B.M. and Sharp, R.E. 1999. Regulation of growtb anisotropy in well-watered and water-stressed maize roots. II. Role of cortical microtubules and cellulose microfibrils. Plant Physiol. 119: 681–692.

    Google Scholar 

  • Blanar, M.A. and Rutter, W.J. 1992. Interaction cloning: isolation of a eDNA encoding FIP, a basic-HLH-zip protein that interacts with cFos. Science 256: 1014–1018.

    Google Scholar 

  • Bleecker, A.B. 1999. Etbylene perception and signaling: an evolutionary perspective. Trends Plant Sci. 4: 269–274.

    Google Scholar 

  • Brand, U., Fletcher, J.C., Hobe, M., Meyerowitz, E.M. and Simon, R. 2000. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289: 617–619.

    Google Scholar 

  • Braun, D.M., Stone, J.M. and Walker, J.C. 1997. Interaction of the maize and Arabidopsis kinase interaction domains with a subset of receptor-like protein kinases: implications for transmembrane signaling in plants. Plant J. 12: 83–95.

    Google Scholar 

  • Caderas, D., Muster, M., Vogler, H., Mandel, T., Rose, J.K.C., McQueen-Mason, S. and Kuhlemeier, C. 2000. Limited correlation between expansin gene expression and elongation growtb rate. Plant Physiol. 123: 1399–1413.

    Google Scholar 

  • Carpita, N. and Gibeaut, D. 1993. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of tbe walls during growth. Plant J. 3: 1–30.

    Google Scholar 

  • Catalá, C., Rose, J.K.C. and Bennett, A.B. 2000. Auxin-regulated genes encoding cell wall-modifying proteins are expressed duro ing early tomato fruit growth. Plant Physiol. 122: 527–534.

    Google Scholar 

  • Chang, C., Kwok, S.F., Bleecker, A.B. and Meyerowitz, E.M. 1993. Arabidopsis etbylene-response gene ETR1: similarity of product to two-component regulators. Science 262: 539–544.

    Google Scholar 

  • Chang, C. and Shockey, J.A. 1999. The ethylene-response pathway: signal perception to gene regulation. Curr. Opin. Plant Biol. 2: 352–358.

    Google Scholar 

  • Chao, Q., Rothenberg, M., Solano, R., Roman, G., Terzaghi, W. and Ecker, J.R. 1997. Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89: 1133–1144.

    Google Scholar 

  • Chen, R., Hilson, P., Sedbrook, J., Rosen, E., Caspar, T. and Masson, P.H. 1998. The Arabidopsis thaliana AGRAVITROPICI gene encodes a component of tbe polar-auxin-transport efflux carrier. Proc. Natl. Acad. Sci. USA 95: 15112–15117.

    Google Scholar 

  • Cheng, S.H., Keller, B. and Condit, C.M. 1996. Common occurrence of homologues of petunia glycine-rich protein-1 among plants. Plant Mol. Biol. 31: 163–168.

    Google Scholar 

  • Cho, H.T. and Cosgrove, D.J. 2000. From the cover: altered expression of expansin modulates leaf growtb and pedicel abscission in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 97: 9783–9788.

    Google Scholar 

  • Cosgrove, D.J. 1997. Assembly and enlargement of the primary cell wall in plants. Annu. Rev. Cell Dev. Biol. 13: 171–201.

    Google Scholar 

  • Fisher, D.D. and Cyr, R.J. 1998. Extending the microtubule/ microfibril paradigm. Cellulose syntbesis is required for normal cortical microtubule alignment in elongating cells. Plant Physiol. 116: 1043–1051.

    Google Scholar 

  • Fowler, T., Bernhardt, C. and Tierney, M. 1999. Characterization and expression of four proline-rich cell wall protein genes in A rabidopsis encoding two distinct subsets of multiple domain proteins. Plant Physiol. 121: 1081–1092.

    Google Scholar 

  • Franklin-Tong, V.E. 1999. Signaling and the modulation of pollen tube growth. Plant Cell 11: 727–738.

    Google Scholar 

  • Galweiler, L., Guan, C.H., Muller, A., Wisman, E., Mendgen, K., Yephremov, A. and Palme, K. 1998. Regulation of polar auxin transport by AtPINI in Arabidopsis vascular tissue. Science 282: 2226–2230.

    Google Scholar 

  • Hammond-Kosack, K.E. and Jones, J.D.G. 1996. Resistance gene-dependent plant defense responses. Plant Cell 8: 1773–1791.

    Google Scholar 

  • He, Z., Wang, Z.Y., Li, J., Zhu, Q., Lamb, C., Ronald, P. and Chory, J. 2000. Perception of brassinosteroids by the extracellular domain of the receptor kinase BRII. Science 288: 2360–2363.

    Google Scholar 

  • He, Z.-H., Fujiki, M. and Kohorn, B.D. 1996. A cell wall-associated, receptor-like kinase. J. Biol. Chem. 271: 19789–19793.

    Google Scholar 

  • He, Z.-H., He, D. and Kohorn, B.D. 1998. Requirement for the induced expression of a cell wall associated receptor kinase for survival during the pathogen response. Plant J. 14: 55–63.

    Google Scholar 

  • He, Z.-H., Cheeseman, I., He, D. and Kohorn, B.D. 1999. A cluster of five cell wall-associated receptor kinase genes, Wak1-5, are expressed in specific organs of Arabidopsis. Plant Mol. Biol. 39: 1189–1196.

    Google Scholar 

  • Holzinger, A., Phillips, K.S. and Weaver, T.E. 1996. Single-step purification/solubilization of recombinant proteins: application to Surface Protein B. Biotechniques 20: 804–808.

    Google Scholar 

  • Jones, A.M. 1998. Auxin transport: down and out and up again. Science 282: 2201–2203.

    Google Scholar 

  • Kieber, J.J., RotJienberg, M., Roman, G., Feldmann, K.A. and Ecker, J.R. 1993. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 72: 427–441.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Kohorn, B.D. 1999. Shuffling the deck: plant signaling plays a club. Trends Cell Biol. 10: 381–383.

    Google Scholar 

  • Kohorn, B.D. 2000. Plasma membrane-cell wall contacts. Plant Physiol. 124: 31–38.

    Google Scholar 

  • Kohorn, B.D., He, Z.-H. and Fujiki, M. 1996. Elusin: a receptorlike kinase with an EGF domain in the cell wall. In: P.R Shewry, N.G. Halford and R. Hooley (Eds.) Protein Phosphorylation in Plants, Clarendon Press, Oxford, UK.

    Google Scholar 

  • Kost, B., Mathur, J. and Chua, N.H. 1999. Cytoskeleton in plant development. Curro Opin. Plant Biol. 2: 462–470.

    Google Scholar 

  • Laval, V., Chabannes, M., Carriere, M., Canul, H., Barre, A., Rouge, P., Pont-Lezica, R and Galaud, J. 1999. A family of Arabidopsis plasma membrane receptors presenting animal β-integrin domains. Biochim. Biophys. Acta 1435: 61–70.

    Google Scholar 

  • Li, J. and Chory, J. 1997. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90: 929–938.

    Google Scholar 

  • Li, H., Lin, Y., Heath, R.M., Shu, M.X. and Yang, Z. 1999. Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell 11: 1731–1742.

    Google Scholar 

  • Luschnig, C., Gaxiola, R.A., Grisafi, P. and Fink, G.R 1998. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 12: 2175–2187.

    Google Scholar 

  • Lynch, T.M. and Lintilhac, P.M. 1997. Mechanical signals in plant development: a new method for single cell studies. Dev. Biol. 181: 246–256.

    Google Scholar 

  • Majewska-Sawka, A. and Nothnagel, E.A. 2000. The multiple roles of arabinogalactan proteins in plant development. Plant Physiol. 122: 3–9.

    Google Scholar 

  • Muller, A., Guan, C., Galweiler, L., Tanzler, P., Huijser, P., Marchant, A., Parry, G., Bennett, M., Wisman, E. and Palme, K. 1998. AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 17: 6903–6911.

    Google Scholar 

  • Mussig, C. and Altmann, T. 1999. Physiology and molecular mode of action of brassinosteroids. Plant Physiol. Biochem. 37: 363–372.

    Google Scholar 

  • Nicol, F., His, I., Jauneau, A., Vernhettes, S., Canut, H. and Höfte, H. 1998. A plasma membrane-bound putative endo-1,4-β-D-glucanse is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J. 17: 5563–5576.

    Google Scholar 

  • Oxley, D. and Bacic, A. 1999. Structure of the glycosylphos-phatidylinositol anchor of an arabinogalactan protein from Pyrus communis suspension-cultured cells. Proc. Natl. Acad. Sci. USA 25: 14246–14251.

    Google Scholar 

  • Pear, J.R, Kawagoe, Y., Schreckengost, W.E., Delmer, D.P. and Stalker, D.M. 1996. Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. Proc. Natl. Acad. Sci. USA 25: 12637–12642.

    Google Scholar 

  • Phillips, A.L. 1998. Gibberellins in Arabidopsis. Plant Physiol. Biochem. 36: 115–124.

    Google Scholar 

  • Reiter, W.-D. 1998. The molecular analysis of cell wall components. Trends Plant Sci. 3: 27–32.

    Google Scholar 

  • Roberts, K. 1994. The plant extracellular matrix: in a new expansive mood. Curr. Opin. Cell Biol. 6: 688–694.

    Google Scholar 

  • Schaller, G.E. and Bleecker, A.B. 1995. Ethylene-binding sites generated in yeast expressing the Arabidopsis ETR1 gene. Science 270: 1809–1811.

    Google Scholar 

  • Schopfer, C.R, Nasrallah, M.E. and Nasrallah, J.B. 1999. The male determinant of self-incompatibility in Brassica. Science 286: 1697–1700.

    Google Scholar 

  • Schumacher, K. and Chory, J. 2000. Brassinosteroid signal transduction: still casting the actors. Curr. Opin. Plant Biol. 3: 79–84.

    Google Scholar 

  • Showalter, A.M. 1993. Structure and function of plant cell wall proteins. Plant Cell 5: 9–23.

    Google Scholar 

  • Silverstone, A.L., Chang, C.-W., Krol, E. and Sun, T.-P. 1997. Developmental regulation of the gibberellin biosynthetic gene GA1 in Arabidopsis thaliana. Plant J. 12: 9–19.

    Google Scholar 

  • Silverstone, A.L. and Sun, T.-P. 2000. Gibberellins and the green revolution. Trends Plant Sci. 5: 1–2.

    Google Scholar 

  • Svetek, J., Yadav, M.P. and Nothnagel, E.A. 1999. Presence of a glycosylphosphatidylinositol lipid anchor on rose arabinogalactan proteins. J. Biol. Chem. 274: 14724–14733.

    Google Scholar 

  • Trotochaud, A.E., Hao, T., Wu, G., Yang, Z. and Clark, S.E. 1999. 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: 393–406.

    Google Scholar 

  • Trotochaud, A.E., Jeong, S. and Clark, S.E. 2000. CLAVATA3, a multimeric ligand for the CLAVATA1 receptor-kinase. Science 289: 613–617.

    Google Scholar 

  • Utsuno, K., Shikartai, T., Yamada, Y. and Hashimoto, T. 1998. Agr, an Agravitropic locus of Arabidopsis thaliana, encodes a novel membrane-protein family member. Plant Cell Physiol. 39: 1111–1118.

    Google Scholar 

  • Vissenberg, K., Martinez-Vilchez, I.M., Verbelen, J.-P., Miller, J.G. and Fry, S.C. 2000. In vivo colocalization of xyloglucan endotransglycosylase activity and its donor substrate in the elongation zone of Arabidopsis roots. Plant Cell 12: 1229–1237.

    Google Scholar 

  • Wagner, T.A. and Kohom, B. 2001. Wall associated kinases, WAKs, are expressed throughout plant development and are required for cell expansion. Plant Cell 13: 303–318.

    Google Scholar 

  • Wyatt, S.E. and Carpita, N.C. 1993. The plant cytoskeleton-cell-wall continuum. Trends Cell Biol. 12: 413–417.

    Google Scholar 

  • Xu, W., Campbell, P., Vargheese, A.K. and Braarn, I. 1996. The Arabidopsis XET-related gene faruily: environmental and hormonal regulation of expression. Plant J. 9: 879–889.

    Google Scholar 

  • Zhang, Y., Brown, R.I. and West, C. 1998. Two proteins of the Dictyostelium spore coat bind to cellulose in vitro. Biochemistry 37: 10766–10779.

    Google Scholar 

  • Zuo, I., Niu, Q.-W., Nishizawa, N., Wu, Y., Kost, B. and Chua, H. 2000. KORRIGAN, an Arabidopsis endo-1,4-β-glucan: localizes to the cell plate by polarized targeting and is esser for cytokinesis. Plant Cell 12: 1137–1152.

    Google Scholar 

  • Zurek, D.M. and Clouse, S.D. 1994. Molecular cloning and cl acterization of a brassinosteroid-regulated gene from elon, ing soybean (Glycine max L.) epicotyls. Plant Physiol. J 161–170.

    Google Scholar 

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Anderson, C.M., Wagner, T.A., Perret, M., He, ZH., He, D., Kohorn, B.D. (2001). WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrix. In: Carpita, N.C., Campbell, M., Tierney, M. (eds) Plant Cell Walls. Springer, Dordrecht. https://doi.org/10.1007/978-94-010-0668-2_12

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  • DOI: https://doi.org/10.1007/978-94-010-0668-2_12

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