The Extracellular Matrix of the Plant Cell: Location of Signal Perception, Transduction and Response

  • Karl-Josef Dietz
Part of the Progress in Botany book series (BOTANY, volume 62)


The plant protoplast is enclosed by a rigid corset mainly built from carbohydrates that, once formed during cell development, apparently remain invariable. This misleading perception is supported by the static appearance of plant cells in microscopic studies. For instance, a leaf typically will not change its habitus following full expansion. It is a module built for specific physiological functions and will be shed under sub-optimal conditions. However, during recent years, a large body of knowledge proving that the extracellular matrix (ECM) is responsive to a large array of internal and external stimuli (some of which will be discussed below) has accumulated. In the following discussion, “internal signals” are considered to be produced endogenously in the plant, whereas environmental parameters may act as external stimuli.


Guard Cell Anion Channel Extracellular Protease Jerusalem Artichoke Expansin Gene 
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.


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  1. Amtmann A, Jelitto T, Sanders D (1999) K+-selective inward-rectifying channels and apoplastic pH in barley roots. Plant Physiol 120:331–338PubMedCrossRefGoogle Scholar
  2. Baker B, Zambryski P, Staskawicz B, Dinesh-Kumar SP (1997) Signaling in plant-microbe interactions. Science 276:726–373PubMedCrossRefGoogle Scholar
  3. Becraft PW, Stinard PS, McCarty DR (1996) CRINKLY4: a TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273:1406–1409PubMedCrossRefGoogle Scholar
  4. Blinda A, Koch B, Ramanjulu S, Dietz KJ (1997) De novo synthesis and accumulation of apoplast proteins in leaves of heavy metal exposed barley seedlings. Plant Cell Environ 20:969–981CrossRefGoogle Scholar
  5. Braun DM, Walker JC (1996) Plant transmembrane receptors: new pieces in the signaling puzzle. Trends Biochem Sci 21:70–73PubMedGoogle Scholar
  6. Bressan RA, Nelson DE, Iraki NM, LaRosa PC, Singh NK, Hasegawa PM, Carpita NC (1990) Reduced cell expansion and changes in cell walls of plant cells adapted to NaCl. In: Katterman F (ed) Environmental injury to plants. Academic Press, San Diego, pp 137–171Google Scholar
  7. Brummell D, Harpster MH, Dunsmuir P (1999) Differential expression of expansin gene family members during growth and ripening of tomato fruit. Plant Mol Biol 39:161–169PubMedCrossRefGoogle Scholar
  8. Brune A, Urbach W, Dietz KJ (1994) Zinc stress induces changes in apoplasmic protein content and polypeptide composition of barley primary leaves. J Exp Bot 45:1189–1196CrossRefGoogle Scholar
  9. Canny MJ (1995) Apoplastic water and solute movement: new rules for an old space. Annu Rev Plant Physiol Plant Mol Biol 46:215–236CrossRefGoogle Scholar
  10. Canut H, Carrasco A, Galaud JP, Cassan C, Bouyssou H, Vita N, Ferrara P, Pont-Lezica R (1998) High affinity RGD-binding sites at the plasma membrane of Arabidopsis thaliana links the cell wall. Plant J 16:63–71PubMedCrossRefGoogle Scholar
  11. Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physiological properties of the walls during growth. Plant J 3:1–30PubMedCrossRefGoogle Scholar
  12. Clayton H, Knight MR, Knight H, McAinsh MR, Hetherington AM (1999) Dissection of the ozone-induced calcium signature. Plant J 17:575–579PubMedCrossRefGoogle Scholar
  13. Cosgrove D (1999) Enzymes and other agents that enhance cell wall extensibility. Annu Rev Plant Physiol Plant Mol Biol 50:391–417PubMedCrossRefGoogle Scholar
  14. Didier R, Wittwer F, Mandel T, Kuhlemeier C (1998) Localized upregulation of a new expansin gene predicts the site of leaf formation in the tomato meristem. Plant Cell 10:1427–1437Google Scholar
  15. Dietz KJ (1997) Functions and responses of the leaf apoplast under stress. Prog Bot 58:221–254CrossRefGoogle Scholar
  16. Felle HH (1998) The apoplastic pH of the Zea mays root cortex as measured with pH-sensitive microelectrodes: aspects of regulation. J Exp Bot 49:987–995Google Scholar
  17. Fleming AJ, McQueen-Mason S, Mandel T, Kuhlemeier C (1997) Induction of leaf primordia by the cell wall protein expansin. Science 276:1415–1418CrossRefGoogle Scholar
  18. Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911–1914PubMedCrossRefGoogle Scholar
  19. Forsthoefel NR, Cushman MAF, Ostrem JA, Cushman JC (1998) Induction of a cysteine protease cDNA from Mesembryanthemum crystallinum leaves by environmental stress and plant growth regulators. Plant Sci 136:195–206CrossRefGoogle Scholar
  20. Gamble RL, Coonfield ML, Schaller GE (1998) Histidine kinase activity of the ETR1 ethylene receptor from Arabidopsis. Proc Natl Acad Sci USA 95:7825–7829PubMedCrossRefGoogle Scholar
  21. Gao M, Showalter AM (1999) Yariv reagent treatment induces programmed cell death in Arabidopsis cell cultures and implicates arabinogalactan protein involvement. Plant J 19:321–331PubMedCrossRefGoogle Scholar
  22. Gens JS, Reuzeau C, Doolittle KW, McNally JG, Pickard BG (1996) Covisualization by computational optical-sectioning microscopy of integrin and associated proteins at the cell membrane of living onion protoplasts. Protoplasma 194:215–230PubMedCrossRefGoogle Scholar
  23. 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
  24. 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 in Arabidopsis. Plant Mol Biol 39:1189–1196PubMedCrossRefGoogle Scholar
  25. Hedrich R, Marten I (1993) Malate-induced feedback regulation of plasma membrane anion channels could provide a CO2 sensor to guard cells. EMBO J 12:897–901PubMedGoogle Scholar
  26. Hoffmann B, Kosegarten H (1995) FITC-dextran for measuring apoplast pH and apoplastic pH gradients between various cell types in sunflower leaves. Physiol Plant 95:327–335CrossRefGoogle Scholar
  27. Hollenbach B, Schreiber L, Hartung W, Dietz KJ (1997) Cadmium leads to stimulated expression of a lipid transfer protein (ltp) in barley: implications for the involvement of LTP in wax assembly. Planta 203:9–19PubMedGoogle Scholar
  28. Hooley R (1998) Plant hormone perception and action: a role for G-protein signal transduction? Philos Trans R Soc Lond B Biol Sci 353:1425–1430PubMedCrossRefGoogle Scholar
  29. Hoth S, Hedrich R (1999) Distinct molecular bases for pH sensitivity of the guard cell K+ channels KST1 and KATI. J Biol Chem 274:11599–11603PubMedCrossRefGoogle Scholar
  30. Jonak C, Ligterink W, Hirt H (1999) MAP kinases in plant signal transduction. Cell Mol Life Sci 55:204–213PubMedCrossRefGoogle Scholar
  31. Jones JT, Mullet JE (1995) A salt- and dehydration-inducible pea gene, Cyp15a, encodes a cell-wall protein with sequence similarity to cysteine proteases. Plant Mol Biol 28:1055–1065PubMedCrossRefGoogle Scholar
  32. Jorda L, Coego A, Conejero V, Vera P (1999) A genomic cluster containing four differentially regulated subtilisin-like processing protease genes is in tomato plants. J Biol Chem 274, 2360–2365PubMedCrossRefGoogle Scholar
  33. Josefsson LG, Rask L (1997) Cloning of a putative G-protein-coupled receptor from Arabidopsis thaliana. Eur J Biochem 249:415–420PubMedCrossRefGoogle Scholar
  34. Katembe WJ, Swatzell LJ, Makaroff CA, Kiss JZ (1997) Immunolocalization of integrin-like proteins in Arabidopsis and Chara. Physiol Plant 99:7–14PubMedCrossRefGoogle Scholar
  35. Kinoshita T, Fukuzawa H, Shimada T, Saito T, Matsuda Y (1992) Primary structure and expression of a gamete lytic enzyme in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 89:4693–4697PubMedCrossRefGoogle Scholar
  36. Kollmann R, Glockmann C (1991) Studies on graft unions. III. On the mechanism of secondary formation of plasmodesmata at the graft interface. Protoplasma 165:71–85CrossRefGoogle Scholar
  37. Kreuger M, Van Holst GJ (1993) Arabinogalactan proteins are essential in somatic embryogenesis of Daucus carota L. Planta 189:243–248CrossRefGoogle Scholar
  38. Lease K, Ingham E, Walker JC (1998) Challenges in understanding RLK function. Curr Opin Plant Biol 1:388–392PubMedCrossRefGoogle Scholar
  39. Leckie F, Mattei B, Capodicasa C, Hemmings A, Nuss L, Aracri B, De Lorenzo G, 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 leucinerich repeats (LRRs) confers a new recognition capability. EMBO J 18:2352–2363PubMedCrossRefGoogle Scholar
  40. Lee YR, Assmann SM (1999) Arabidopsis thaliana “extra-large GTP-binding protein” (AtXLGl): a new class of G-protein. Plant Mol Biol 40:55–64Google Scholar
  41. Lemtiri-Chlieh F, MacRobbie EA (1994) Role of calcium in the modulation of Vicia guard cell potassium channels by abscisic acid: a patch-clamp study. J Memb Biol 137:99–107CrossRefGoogle Scholar
  42. Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929–938PubMedCrossRefGoogle Scholar
  43. Li Z, Wurtzel ET (1998) The ltk gene family encodes novel receptor like kinases with temporal expression in developing maize endosperm. Plant Mol Biol 37:749–761PubMedCrossRefGoogle Scholar
  44. Longhurst CM, Jennings LK (1998) Integrin-mediated signal transduction. Cell Mol Life Sci 54:514–526PubMedCrossRefGoogle Scholar
  45. Lynch TM, Lintilhac PM, Domozych D (1998) Mechanotransduction molecules in the plant gravisensory response: amyloplast/statolith membranes contain a β1 integrin-like protein. Protoplasma 201:92–100PubMedCrossRefGoogle Scholar
  46. Marcantonio EE, Hynes RO (1988) Antibodies to the conserved cytoplasmic domain of the integrin ßl subunit react with proteins in vertebrates, invertebrates, and fungi. J Cell Biol 106:1765–1772PubMedCrossRefGoogle Scholar
  47. Marten I, Lohse G, Hedrich R (1991) Plant growth hormones control voltage dependent activity of anion channels in plasma membrane of guard cells. Nature 353:758–762CrossRefGoogle Scholar
  48. Marten I, Hoth S, Deeken R, Ache P, Ketchum KA, Hoshi T, Hedrich R (1999) AKT3, a phloem-localized K+-channel, is blocked by protons. Proc Natl Acad Sci USA 96:7581–7586PubMedCrossRefGoogle Scholar
  49. McCabe PF, Valentine TA, Forsberg LS, Pennel RI (1997) Soluble signals from cells identified at the cell wall establish a developmental pathway in carrot. Plant Cell 9:2225–2241PubMedGoogle Scholar
  50. McCubbin AG, Kao TH (1999) The emerging complexity of self-incompatibility (S-) loci. Sexual Plant Reproduction 12:1–5CrossRefGoogle Scholar
  51. McGeehan G, Burkhart W, Anderegg R, Becherer JD, Gillikin JW, Graham JS (1992) Sequencing and characterization of the soybean leaf metalloproteinase. Plant Physiol 99:1179–1183PubMedCrossRefGoogle Scholar
  52. McQueen-Mason S, Cosgrove D (1994) Disruption of hydrogen bonding between plant cell wall polymers by proteins that induce wall extension. Proc Natl Acad Sci USA 91:6574–6578PubMedCrossRefGoogle Scholar
  53. Messdaghi D, Dietz KJ (2000) Characterization of an extrazellular chymostatin-sensitive serine protease preferentially expressed in young plant tissues. Biochim Biophys Acta 1480:107–116PubMedCrossRefGoogle Scholar
  54. Mimura T, Yin ZH, Wirth E, Dietz KJ (1992) Phosphate transport and apoplastic phosphate homeostasis in barley leaves. Plant Cell Physiol 33:563–568Google Scholar
  55. Moorhead G, Douglas P, Cotelle V, Harthill J, Morrice N, Meek S, Deiting U, Stitt M, Scarabel M, Aitken A, MacKintosh C (1999) Phosphorylation-dependent interactions between enzymes of plant metabolism and 14–3–3 proteins. Plant J 18:1–12PubMedCrossRefGoogle Scholar
  56. Miihling KH, Plieth C, Hansen UP, Sattelmacher B (1995) Apoplastic pH of intact leaves of Vicia faba as influenced by light. J Exp Bot 46:377–382CrossRefGoogle Scholar
  57. Murai M, Yoshida S (1998) Evidence for the cell wall involvement in temporal changes in freezing tolerance of Jerusalem artichoke tubers during cold acclimation. Plant Cell Physiol 39:97–105PubMedCrossRefGoogle Scholar
  58. Neumann PM, Azaizeh H, Leon D (1994) Hardening of root cell walls: a growth inhibitor response to salinity stress. Plant Cell Environ 17:303–309CrossRefGoogle Scholar
  59. Neuteboom LW, Ng JMY, Kuyper M, Clijdesdale OR, Hookaas PJJ, Van der Zaal BJ (1999) Isolation and characterization of cDNA clones corresponding with mRNAs that accumulate during auxin-induced lateral root formation. Plant Mol Biol 39:273–287PubMedCrossRefGoogle Scholar
  60. Nothnagel EA (1997) Proteoglycans and related components in plant cells. Int Rev Cytol 174:195–291PubMedCrossRefGoogle Scholar
  61. Ojima A, Shiota H, Higashi K, Kamada H, Shimma Y, Wada M, Satoh S (1997) An extracellular insoluble inhibitor of cysteine proteinases in cell cultures and seeds of carrot. Plant Mol Biol 34:99–109PubMedCrossRefGoogle Scholar
  62. Palme K, Bischoff F, Cvrckova F, Zarsky V (1999) Small G-proteins in Arabidopsis thali-ana. Biochem Soc Trans 25:1001–1005Google Scholar
  63. Plakidou-Dymock S, Dymock D, Hooley R (1998) A plant seven-transmembrane receptor that influences sensitivity to cytokinins. Curr Biol 8:315–324PubMedCrossRefGoogle Scholar
  64. Quatrano RS, Brian L, Aldridge J, Schultz T (1991) Polar axis fixation in Fucus zygotes: components of the cytoskeleton and extracellular matrix. Development 1 [Suppl]:11–16Google Scholar
  65. Ramanjulu S, Kaiser WM, Dietz KJ (1999) Salt and drought stress differentially affect the accumulation of extracellular proteins in barley. Z Nat 54:337–347Google Scholar
  66. Reiter WD (1998) Arabidopsis thaliana as a model system to study synthesis, structure and function of the plant cell wall. Plant Physiol Biochem 36:167–176CrossRefGoogle Scholar
  67. Reuzeau C, Pont-Lezica RF (1995) Comparing plant and animal extracellular matrix-cytoskeleton connections. Are they alike? Protoplasma 186:113–121CrossRefGoogle Scholar
  68. Ribeiro A, Akkermans ADL, Van Kammen A, Bisseling T, Pawlowski K (1995) A nodule-specific gene encoding a subtilisin-like protease is expressed in early stages of actinorhizal nodule development. Plant Cell 7:785–794PubMedGoogle Scholar
  69. Rodrigo I, Vera P, Conejero V (1989) Degradation of tomato pathogenesis-related proteins by an endogenous 37-kDa aspartyl endoproteinase. Eur J Biochem 184:663–669PubMedCrossRefGoogle Scholar
  70. Sakurai N (1998) Dynamic function and regulation of apoplast in the plant body. J Plant Res 111:133–148CrossRefGoogle Scholar
  71. Samaj J, Ensikat HJ, Baluska F, Knox JP, Barthlott W, Volkmann D (1999) Immunogold localization of plant surface arabinogalactan-proteins using glycerol liquid substitution and scanning electron microscopy. J Microsc 193:150–157PubMedCrossRefGoogle Scholar
  72. Satterlee JS, Sussman MR (1998) Unusual membrane-associated protein kinases in higher plants. J Memb Biol 164:205–213CrossRefGoogle Scholar
  73. Scheel D (1998) Resistance response: physiology and signal transduction. Curr Opin Plant Biol 1:305–310PubMedCrossRefGoogle Scholar
  74. Schroeder JI (1995) Anion channels as central mechanisms for signal transduction in guard cells and putative functions in roots for plant-soil interactions. Plant Mol Biol 28:353–361PubMedCrossRefGoogle Scholar
  75. Schultz C, Gilson P, Oxley D, Youl J, Bacic A (1998) GPI achors on arabinogalactan proteins: implications for signalling in plants. Trends Plant Sci 3:426–431CrossRefGoogle Scholar
  76. Schulz-Lessdorf B, Lohse B, Hedrich R (1996) GCACl recognizes the pH gradient across the plasma membrane. Plant J 10:993–1004CrossRefGoogle Scholar
  77. Schwarz M, Schroeder JI (1998) Abscisic acid maintains S-type anion channel activity in ATP depleted Vicia faba guard cells. FEBS Lett 428:177–182PubMedCrossRefGoogle Scholar
  78. Serpe MD, Nothnagel E A (1994) Effects of Yariv phenylglycosides on Rosa cell suspensions: evidence for the involvement of arabinogalactan-proteins in cell-proliferation. Planta 193:542–550CrossRefGoogle Scholar
  79. Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5:9–23PubMedGoogle Scholar
  80. Speer M, Kaiser WM (1994) Replacement of nitrate by ammonium as the nitrogen source increases the salt sensitivity of pea plants. II. Inter- and intracellular solute compart-mentation in leaflets. Plant Cell Environ 17:1223–1231CrossRefGoogle Scholar
  81. Speer M, Brune A, Kaiser WM (1994) Replacement of nitrate by ammonium as the nitrogen source increases the salt sensitivity of pea plants. I. Ion concentrations in roots and leaves. Plant Cell Environ 17:1215–1221CrossRefGoogle Scholar
  82. Stanchev B, Doughty J, Scutt CP, Dickinson H, Croy RRD (1996) Cloning of PCP1, a member of a family of pollen coat protein (PCP) genes from Brassica oleracea encoding novel cysteine-rich proteins involved in pollen-stigma interactions. Plant J 10:303–313PubMedCrossRefGoogle Scholar
  83. Stephenson AG, Doughty J, Dixon S, Elleman C, Hiscock S, Dickinson HG (1997) The male determinant of self-incompatibility in Brassica olerácea is located in the pollen coating. Plant J 12:1351–1359CrossRefGoogle Scholar
  84. Swatzell LJ, Edelmann RE, Makaroff CA, Kiss JZ (1999) Integrin-like proteins are localized to plasma membrane fractions, not plastids, in Arabidopsis. Plant Cell Physiol 40:173–183Google Scholar
  85. Taylor DP, Slattery J, Leopold AC (1996) Apoplastic pH in corn root gravitropism: a laser scanning confocal microscopy measurement. Physiol Plant 97:35–38PubMedCrossRefGoogle Scholar
  86. Thiel G, Brüdern A, Gradmann D (1996) Small inward rectifying K+ channels in coleoptiles: inhibition by external Ca2+ and function in cell elongation. J Membr Biol 149:9–20PubMedCrossRefGoogle Scholar
  87. Thiyagarajah M, Fry SC, Yeo AR (1996) In vitro salt tolerance of cell wall enzymes from halophytes and glycophytes. J Exp Bot 47:1717–1724CrossRefGoogle Scholar
  88. Thompson JE, Smith RC, Fry S (1997) Xyloglucan undergoes interpolymeric transglyco-sylation during binding to the plant cell wall in vivo: evidence from 13C/3H dual labelling and isopycnic centrifugation in caesium trifluoroacetate. Biochem J 327:699–708PubMedGoogle Scholar
  89. Tominaga R, Samejima M, Sakai F, Hayashi T (1999) Occurrence of cell oligosaccharides in the apoplast of auxin-treated pea stems. Plant Physiol 119:249–254PubMedCrossRefGoogle Scholar
  90. Vera P, Conejero V (1988) Pathogenesis-related proteins in tomato: P69 as an alkaline endoproteinase. Plant Physiol 87:58–63PubMedCrossRefGoogle Scholar
  91. Walker JC, Zhang R (1990) Relationship of a putative receptor protein kinase from maize to the S-locus glycoprotein of Brassica. Nature 345:743–746PubMedCrossRefGoogle Scholar
  92. Walker JC, Jinn TL, Stone JM (1999) Remodelling the extracellular matrix during plant development: the role of receptor protein kinases in floral abscission. In: Roberts K, Vera P (eds) Dynamics of the plant extracellular matrix. Instituto Juan March de Estudios e Investigaciones, Madrid, p 15–16Google Scholar
  93. Walton JD (1994) Deconstructing the cell wall. Plant Physiol 104:1113–1118PubMedGoogle Scholar
  94. Wang Y, Kollmann R (1996) Vascular differentiation in the graft union of in-vitro grafts with different compatibility. Structural and functional aspects. J Plant Physiol 147:521–533CrossRefGoogle Scholar
  95. Wayne R, Staves MP, Leopold AC (1992) The contribution of the extracellular matrix to gravisensing in characean cells. J Cell Sci 101:611–623PubMedGoogle Scholar
  96. Weil M, Krausgrill S, Schuster A, Rausch T (1994) A 17-kDa Nicotiana tabacum cell-wall peptide acts as an in vitro inhibitor of the cell wall isoform of acid invertase. Planta 193:438–445PubMedGoogle Scholar
  97. Wojtaszek P, Trethowan J, Bolwell GP (1997) Reconstitution in vitro of the components and conditions required for the oxidative cross-linking of extracellular proteins in French bean (Phaseolus vulgaris L.). FEBS Lett 405:95–98PubMedCrossRefGoogle Scholar
  98. Yamagata H, Masuzawa T, Nagaoka Y, Ohnishi T, Iwasaki T (1994) Cucumisin, a serine protease from melon fruits, shares structural homology with subtilisin and is generated from a large precursor. J Biol Chem 269:32725–32731PubMedGoogle Scholar
  99. Youl JJ, Bacic A, Oxley D. (1998) Arabinogalactan-proteins from Nicotiana alata and Pyrus communis contain glycosylphosphatidylinositol membrane anchors. Proc Natl Acad Sci USA 95:7921–7926PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2001

Authors and Affiliations

  • Karl-Josef Dietz
    • 1
  1. 1.Geobotanisches InstitutETH ZürichZürichSwitzerland

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