The Cell Wall-Associated Kinases, WAKs, Regulate Cell Expansion and the Stress Response

  • Bruce D. KohornEmail author
  • Susan L. Kohorn
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 13)


The plant cell wall is secreted and assembled by cells to provide structure and shape, and thereby helps to determine the form of a plant organ. Control of the synthesis and directional enlargement of the wall is therefore crucial for plant development, but the wall also serves as a first defense against common plant stresses such as pathogens and physical wounding. There is now substantial evidence to suggest that the Cell Wall Associated Kinases, WAK s, are pectin receptors required for both normal cell elongation and for an induced stress response.


Pollen Tube Cell Wall Biosynthesis Cellulose Synthesis Vacuolar Invertase Wall Associate Kinase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Abrash EB, Bergmann DC (2010) Regional specification of stomatal production by the putative ligand CHALLAH. Development 137:447–455PubMedCrossRefGoogle Scholar
  2. Anderson CM, Wagner TA, Perret M, He ZH, He D, Kohorn BD (2001) WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrix. Plant Mol Biol 47:197–206PubMedCrossRefGoogle Scholar
  3. Andreasson E, Ellis B (2010) Convergence and specificity in the Arabidopsis MAPK nexus. Trends Plant Sci 15:106–113PubMedCrossRefGoogle Scholar
  4. Arioli T, Peng L, Betzner AS, Burn J, Wittke W, Herth W, Camilleri C, Hofte H, Plazinski J, Birch R et al (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279:717–720PubMedCrossRefGoogle Scholar
  5. Bai L, Zhang G, Zhou Y, Zhang Z, Wang W, Du Y, Wu Z, Song CP (2009) Plasma membrane-associated proline-rich extensin-like receptor kinase 4, a novel regulator of Ca signalling, is required for abscisic acid responses in Arabidopsis thaliana. Plant J 60:314–327PubMedCrossRefGoogle Scholar
  6. Boisson-Dernier A, Roy S, Kritsas K, Grobei MA, Jaciubek M, Schroeder JI, Grossniklaus U (2009) Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge. Development 136:3279–3288PubMedCrossRefGoogle Scholar
  7. Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742–744PubMedCrossRefGoogle Scholar
  8. Bosch M, Hepler PK (2005) Pectin methylesterases and pectin dynamics in pollen tubes. Plant Cell 17:3219–3226PubMedCrossRefGoogle Scholar
  9. Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G (2010) A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci USA 107:9452–9457PubMedCrossRefGoogle Scholar
  10. Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344:1879–1900PubMedCrossRefGoogle Scholar
  11. Cao X, Rogers SW, Butler J, Beevers L, Rogers JC (2000) Structural requirements for ligand binding by a probable plant vacuolar sorting receptor. Plant Cell 12:493–506PubMedCrossRefGoogle Scholar
  12. Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18:465–476PubMedCrossRefGoogle Scholar
  13. Colcombet J, Hirt H (2008) Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem J 413:217–226PubMedCrossRefGoogle Scholar
  14. Crowell EF, Gonneau M, Vernhettes S, Hofte H (2010) Regulation of anisotropic cell expansion in higher plants. C R Biol 333:320–324PubMedCrossRefGoogle Scholar
  15. Decreux A, Messiaen J (2005) Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol 46:268–278PubMedCrossRefGoogle Scholar
  16. Decreux A, Thomas A, Spies B, Brasseur R, Van Cutsem P, Messiaen J (2006) In vitro characterization of the homogalacturonan-binding domain of the wall-associated kinase WAK1 using site-directed mutagenesis. Phytochemistry 67:1068–1079PubMedCrossRefGoogle Scholar
  17. Diener AC, Ausubel FM (2005) RESISTANCE TO FUSARIUM OXYSPORUM 1, a dominant Arabidopsis disease-resistance gene, is not race specific. Genetics 171:305–321PubMedCrossRefGoogle Scholar
  18. Escobar-Restrepo JM, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang WC, Grossniklaus U (2007) The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317:656–660PubMedCrossRefGoogle Scholar
  19. Guo H, Li L, Ye H, Yu X, Algreen A, Yin Y (2009a) Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc Natl Acad Sci USA 106:7648–7653PubMedCrossRefGoogle Scholar
  20. Guo H, Ye H, Li L, Yin Y (2009b) A family of receptor-like kinases are regulated by BES1 and involved in plant growth in Arabidopsis thaliana. Plant Signal Behav 4:784–786PubMedCrossRefGoogle Scholar
  21. Haffani YZ, Silva-Gagliardi NF, Sewter SK, Grace Aldea M, Zhao Z, Nakhamchik A, Cameron RK, Goring DR (2006) Altered expression of PERK receptor kinases in Arabidopsis leads to changes in growth and floral organ formation. Plant Signal Behav 1:251–260PubMedCrossRefGoogle Scholar
  22. Hara K, Yokoo T, Kajita R, Onishi T, Yahata S, Peterson KM, Torii KU, Kakimoto T (2009) Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant Cell Physiol 50:1019–1031PubMedCrossRefGoogle Scholar
  23. Harholt J, Suttangkakul A, Vibe Scheller H (2010) Biosynthesis of pectin. Plant Physiol 153:384–395PubMedCrossRefGoogle Scholar
  24. He ZH, Fujiki M, Kohorn BD (1996) A cell wall-associated, receptor-like protein kinase. J Biol Chem 271:19789–19793PubMedCrossRefGoogle Scholar
  25. He ZH, He D, Kohorn BD (1998) Requirement for the induced expression of a cell wall associated receptor kinase for survival during the pathogen response. Plant J 14:55–63PubMedCrossRefGoogle Scholar
  26. He ZH, Cheeseman I, He D, Kohorn BD (1999) A cluster of five cell wall-associated receptor kinase genes, Wak1-5, are expressed in specific organs of Arabidopsis. Plant Mol Biol 39:1189–1196PubMedCrossRefGoogle Scholar
  27. Hematy K, Hofte H (2008) Novel receptor kinases involved in growth regulation. Curr Opin Plant Biol 11:321–328PubMedCrossRefGoogle Scholar
  28. Hematy K, Sado PE, Van Tuinen A, Rochange S, Desnos T, Balzergue S, Pelletier S, Renou JP, Hofte H (2007) A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr Biol 17:922–931PubMedCrossRefGoogle Scholar
  29. Hematy K, Cherk C, Somerville S (2009) Host-pathogen warfare at the plant cell wall. Curr Opin Plant Biol 12:406–413PubMedCrossRefGoogle Scholar
  30. Hou X, Tong H, Selby J, Dewitt J, Peng X, He ZH (2005) Involvement of a cell wall-associated kinase, WAKL4, in Arabidopsis mineral responses. Plant Physiol 139:1704–1716PubMedCrossRefGoogle Scholar
  31. Keegstra K (2010) Plant cell walls. Plant Physiol 154:483–486PubMedCrossRefGoogle Scholar
  32. Kohorn BD (2000) Plasma membrane-cell wall contacts. Plant Physiol 124:31–38PubMedCrossRefGoogle Scholar
  33. Kohorn BD (2001) WAKs; cell wall associated kinases. Curr Opin Cell Biol 13:529–533PubMedCrossRefGoogle Scholar
  34. Kohorn BD, Lane S, Smith TA (1992) An Arabidopsis serine/threonine kinase homologue with an epidermal growth factor repeat selected in yeast for its specificity for a thylakoid membrane protein. Proc Natl Acad Sci USA 89:10989–10992PubMedCrossRefGoogle Scholar
  35. Kohorn BD, Kobayashi M, Johansen S, Friedman HP, Fischer A, Byers N (2006a) Wall-associated kinase 1 (WAK1) is crosslinked in endomembranes, and transport to the cell surface requires correct cell-wall synthesis. J Cell Sci 119:2282–2290PubMedCrossRefGoogle Scholar
  36. Kohorn BD, Kobayashi M, Johansen S, Riese J, Huang LF, Koch K, Fu S, Dotson A, Byers N (2006b) An Arabidopsis cell wall-associated kinase required for invertase activity and cell growth. Plant J 46:307–316PubMedCrossRefGoogle Scholar
  37. Kohorn BD, Johansen S, Shishido A, Todorova T, Martinez R, Defeo E, Obregon P (2009) Pectin activation of MAP kinase and gene expression is WAK2 dependent. Plant J 60:974–982PubMedCrossRefGoogle Scholar
  38. Krichevsky A, Kozlovsky SV, Tian GW, Chen MH, Zaltsman A, Citovsky V (2007) How pollen tubes grow. Dev Biol 303:405–420PubMedCrossRefGoogle Scholar
  39. Lally D, Ingmire P, Tong HY, He ZH (2001) Antisense expression of a cell wall-associated protein kinase, WAK4, inhibits cell elongation and alters morphology. Plant Cell 13:1317–1331PubMedCrossRefGoogle Scholar
  40. Li YC, Montelione GT (1995) Human type-alpha transforming growth factor undergoes slow conformational exchange between multiple backbone conformations as characterized by nitrogen-15 relaxation measurements. Biochemistry 34:2408–2423PubMedCrossRefGoogle Scholar
  41. Li H, Zhou SY, Zhao WS, Su SC, Peng YL (2009) A novel wall-associated receptor-like protein kinase gene, OsWAK1, plays important roles in rice blast disease resistance. Plant Mol Biol 69:337–346PubMedCrossRefGoogle Scholar
  42. Mangeon A, Junqueira RM, Sachetto-Martins G (2010) Functional diversity of the plant glycine-rich proteins superfamily. Plant Signal Behav 5:99–104PubMedCrossRefGoogle Scholar
  43. Miyazaki S, Murata T, Sakurai-Ozato N, Kubo M, Demura T, Fukuda H, Hasebe M (2009) ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr Biol 19:1327–1331PubMedCrossRefGoogle Scholar
  44. Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11:266–277PubMedCrossRefGoogle Scholar
  45. Moscatiello R, Mariani P, Sanders D, Maathuis FJ (2006) Transcriptional analysis of calcium-dependent and calcium-independent signalling pathways induced by oligogalacturonides. J Exp Bot 57:2847–2865PubMedCrossRefGoogle Scholar
  46. Mousavi A, Hotta Y (2005) Glycine-rich proteins: a class of novel proteins. Appl Biochem Biotechnol 120:169–174PubMedCrossRefGoogle Scholar
  47. Mutwil M, Debolt S, Persson S (2008) Cellulose synthesis: a complex complex. Curr Opin Plant Biol 11:252–257PubMedCrossRefGoogle Scholar
  48. Naithani S, Chookajorn T, Ripoll DR, Nasrallah JB (2007) Structural modules for receptor dimerization in the S-locus receptor kinase extracellular domain. Proc Natl Acad Sci USA 104:12211–12216PubMedCrossRefGoogle Scholar
  49. Nakhamchik A, Zhao Z, Provart NJ, Shiu SH, Keatley SK, Cameron RK, Goring DR (2004) A comprehensive expression analysis of the Arabidopsis proline-rich extensin-like receptor kinase gene family using bioinformatic and experimental approaches. Plant Cell Physiol 45:1875–1881PubMedCrossRefGoogle Scholar
  50. Park AR, Cho SK, Yun UJ, Jin MY, Lee SH, Sachetto-Martins G, Park OK (2001) Interaction of the Arabidopsis receptor protein kinase Wak1 with a glycine-rich protein, AtGRP-3. J Biol Chem 276:26688–26693PubMedCrossRefGoogle Scholar
  51. Rae PM, Kohorn BD, Wade RP (1980) The 10 kb Drosophila virilis 28S rDNA intervening sequence is flanked by a direct repeat of 14 base pairs of coding sequence. Nucleic Acids Res 8:3491–3504PubMedCrossRefGoogle Scholar
  52. Ringli C, Keller B, Ryser U (2001) Glycine-rich proteins as structural components of plant cell walls. Cell Mol Life Sci 58:1430–1441PubMedCrossRefGoogle Scholar
  53. Sampoli Benitez BA, Komives EA (2000) Disulfide bond plasticity in epidermal growth factor. Proteins 40:168–174PubMedCrossRefGoogle Scholar
  54. Sanchez-Rodriguez C, Estevez JM, Llorente F, Hernandez-Blanco C, Jorda L, Pagan I, Berrocal M, Marco Y, Somerville S, Molina A (2009) The ERECTA receptor-like kinase regulates cell wall-mediated resistance to pathogens in Arabidopsis thaliana. Mol Plant Microbe Interact 22:953–963PubMedCrossRefGoogle Scholar
  55. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289PubMedCrossRefGoogle Scholar
  56. Seifert GJ (2004) Nucleotide sugar interconversions and cell wall biosynthesis: how to bring the inside to the outside. Curr Opin Plant Biol 7:277–284PubMedCrossRefGoogle Scholar
  57. Seifert GJ, Blaukopf C (2010) Irritable walls: the plant extracellular matrix and signaling. Plant Physiol 153:467–478PubMedCrossRefGoogle Scholar
  58. Shpak ED, Berthiaume CT, Hill EJ, Torii KU (2004) Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation. Development 131:1491–1501PubMedCrossRefGoogle Scholar
  59. Sivaguru M, Ezaki B, He ZH, Tong H, Osawa H, Baluska F, Volkmann D, Matsumoto H (2003) Aluminum-induced gene expression and protein localization of a cell wall-associated receptor kinase in Arabidopsis. Plant Physiol 132:2256–2266PubMedCrossRefGoogle Scholar
  60. Smith TA, Kohorn BD (1991) Direct selection for sequences encoding proteases of known specificity. Proc Natl Acad Sci USA 88:5159–5162PubMedCrossRefGoogle Scholar
  61. Snyders S, Kohorn BD (1999) TAKs, thylakoid membrane protein kinases associated with energy transduction. J Biol Chem 274:9137–9140PubMedCrossRefGoogle Scholar
  62. Snyders S, Kohorn BD (2001) Disruption of thylakoid-associated kinase 1 leads to alteration of light harvesting in Arabidopsis. J Biol Chem 276:32169–32176PubMedCrossRefGoogle Scholar
  63. Szymanski DB (2009) Plant cells taking shape: new insights into cytoplasmic control. Curr Opin Plant Biol 12:735–744PubMedCrossRefGoogle Scholar
  64. Taylor NG (2008) Cellulose biosynthesis and deposition in higher plants. New Phytol 178:239–252PubMedCrossRefGoogle Scholar
  65. van Zanten M, Snoek LB, Proveniers MC, Peeters AJ (2009) The many functions of ERECTA. Trends Plant Sci 14:214–218PubMedCrossRefGoogle Scholar
  66. Verica JA, He ZH (2002) The cell wall-associated kinase (WAK) and WAK-like kinase gene family. Plant Physiol 129:455–459PubMedCrossRefGoogle Scholar
  67. Verica JA, Chae L, Tong H, Ingmire P, He ZH (2003) Tissue-specific and developmentally regulated expression of a cluster of tandemly arrayed cell wall-associated kinase-like kinase genes in Arabidopsis. Plant Physiol 133:1732–1746PubMedCrossRefGoogle Scholar
  68. Wagner TA, Kohorn BD (2001) Wall-associated kinases are expressed throughout plant development and are required for cell expansion. Plant Cell 13:303–318PubMedCrossRefGoogle Scholar
  69. Willats WG, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47:9–27PubMedCrossRefGoogle Scholar
  70. Winship LJ, Obermeyer G, Geitmann A, Hepler PK (2010) Under pressure, cell walls set the pace. Trends Plant Sci 15:363–369PubMedCrossRefGoogle Scholar
  71. Winter H, Huber SC (2000) Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Crit Rev Biochem Mol Biol 35:253–289PubMedCrossRefGoogle Scholar
  72. Wolf S, Mouille G, Pelloux J (2009) Homogalacturonan methyl-esterification and plant development. Mol Plant 2:851–860PubMedCrossRefGoogle Scholar
  73. Xu SL, Rahman A, Baskin TI, Kieber JJ (2008) Two leucine-rich repeat receptor kinases mediate signaling, linking cell wall biosynthesis and ACC synthase in Arabidopsis. Plant Cell 20:3065–3079PubMedCrossRefGoogle Scholar
  74. Yamazaki N, Fry SC, Darvill AG, Albersheim P (1983) HopPathogen interactions: XXIV. Fragments isolated from suspension-cultured sycamore cell walls inhibit the ability of the cells to incorporate [C]leucine into proteins. Plant Physiol 72:864–869PubMedCrossRefGoogle Scholar
  75. Zhang S, Chen C, Li L, Meng L, Singh J, Jiang N, Deng XW, He ZH, Lemaux PG (2005) Evolutionary expansion, gene structure, and expression of the rice wall-associated kinase gene family. Plant Physiol 139:1107–1124PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Biology DepartmentBowdoin CollegeBrunswickUSA

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