Wall Extensibility: Hormones and Wall Extension

  • R. E. Cleland
Part of the Encyclopedia of Plant Physiology book series (PLANT, volume 13 / B)

Abstract

Plant cells can undergo striking amounts of cell elongation. For example, a cell initially 20 to 30 μ in length can end up over 2000 times as long (Bannon 1964). During elongation there must be a proportional increase in wall area. This increase occurs in one of three patterns. In algal rhizoids, fungal hyphae, root hairs, and pollen tubes (Green 1969) the wall increases in area only at the tip (tip growth). In bacteria (Fiedler and Glazer 1973), yeast (Gooday and Trinci 1980) and the red alga Griffithsia pacifica (Waaland et al. 1972) growth is restricted to only a part of the lateral wall (band growth); but in the majority of cells growth occurs throughout the whole lateral surface (Roelofsen 1965, Roland and Vian 1979). In this case (surface growth), growth involves an extension of wall already present as well as synthesis of new wall. As it is primarily surface growth which is controlled by plant hormones, further discussion of cell elongation will be restricted to cells which undergo this type of extension.

Keywords

Permeability Cellulose Hydrolysis Urea Polysaccharide 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adams PA, Montague MJ, Tepfer M, Rayle DL, Ikuma H, Kaufman PB (1975) Effect of gibberellic acid on the plasticity and elasticity of Avena stem segments. Plant Physiol 56:757–760PubMedGoogle Scholar
  2. Albersheim P (1976) The primary cell wall. In : Bonner J, Varner JE (eds) Plant Biochemistry, 3rd edn. Academic Press, New York, pp 225–274Google Scholar
  3. Baker DB, Ray PM (1965) Direct and indirect effects of auxin on cell wall synthesis in oat coleoptile tissue. Plant Physiol 40: 345–352PubMedGoogle Scholar
  4. Bannon MW (1964) Tracheid size and anticlinal division in the cambium of Pseudotsuga. Can J Bot 42: 603–631Google Scholar
  5. Bates GW, Ray PM (1979) pH dependent release of polymers from isolated cell walls. Plant Physiol 63: S20Google Scholar
  6. Bonner J (1933) The action of plant growth hormones. J Gen Physiol 17: 63–76PubMedGoogle Scholar
  7. Burke D, Kaufman P, McNeil M, Albersheim P (1974) The structure of plant cell walls. VI. A survey of the walls of suspension-cultured monocots. Plant Physiol 54: 109–115PubMedGoogle Scholar
  8. Burström H (1964) Calcium, water conditions and growth of pea seedling stems. Physiol Plant 17: 207–219Google Scholar
  9. Burström H (1975) Growth, solute and water fluxes in the etiolated Pisum stem. Z Pflanzen-physiol 76: 339–352Google Scholar
  10. Burström H, Uhrström I, Wurscher R (1967) Growth, turgor, water potential and Young’s modulus in pea internodes. Physiol Plant 20: 213–231Google Scholar
  11. Cleland RE (1959) Effect of osmotic concentration on auxin-action and on irreversible and reversible expansion of the Avena coleoptile. Physiol Plant 12: 809–825Google Scholar
  12. Cleland RE (1960) Effect of auxin on loss of calcium from cell walls. Nature 185: 44Google Scholar
  13. Cleland RE (1967a) Extensibility of isolated cell walls: measurement and changes during cell elongation. Planta 74: 197–209Google Scholar
  14. Cleland RE (1967 b) A dual role of turgor pressure in auxin-induced cell elongation in Avena coleoptiles. Planta 77: 182–191Google Scholar
  15. Cleland RE (1971 a) Cell wall extension. Annu Rev Plant Physiol 22: 197–222Google Scholar
  16. Cleland RE (1971b) Mechanical behaviour of isolated Avena coleoptile walls subjected to constant stress. Plant Physiol 47: 805–811PubMedGoogle Scholar
  17. Cleland RE (1977) The control of cell enlargement. In: Jennings DH (ed) Integration of activity in the higher plant. Soc Exp Biol Symp 31. Cambridge Press, Cambridge pp 101–115Google Scholar
  18. Cleland RE, Haughton PM (1971) The effect of auxin on stress relaxation of isolated Avena coleoptiles. Plant Physiol 47: 812–815PubMedGoogle Scholar
  19. Cleland RE, Rayle DL (1972) Absence of auxin-induced stored growth in Avena coleoptiles and its implications concerning the mechanism of wall extension. Planta 106: 61–71Google Scholar
  20. Cleland RE, Rayle DL (1977) Reevaluation of the effect of calcium ions on auxin-induced elongation. Plant Physiol 60: 709–712PubMedGoogle Scholar
  21. Cleland RE, Rayle DL (1978) Auxin, H+-excretion and cell elongation. Bot Mag Tokyo Spec Issue 1: 125–139Google Scholar
  22. Cleland RE, Thompson M, Rayle DL, Purves WK (1968) Differences in the effects of auxins and gibberellins on wall extensibility of cucumber hypocotyls. Nature 219: 510–511PubMedGoogle Scholar
  23. Cooil B, Bonner J (1957) Effects of calcium and potassium ions on the auxin-induced growth of Avena coleoptile section. Planta 48: 696–723Google Scholar
  24. Courtney JS, Morré DJ (1980 a) Studies on the role of wall extensibility in the control of cell expansion. Bot Gaz 141: 56–62Google Scholar
  25. Courtney JS, Morré DJ (1980b) Studies on the chemical basis of auxin-induced cell wall loosening. Bot Gaz 141: 63–68Google Scholar
  26. Courtney JS, Morré DJ, Key JL (1967) Inhibition of RNA synthesis and auxin-induced cell wall extensibility and growth by actinomycin D. Plant Physiol 42: 434–439Google Scholar
  27. Darvill AG, Smith CJ, Hall MA (1978) Cell wall structure and elongation growth in Zea mays coleoptile tissue. New Phytol 80: 503–516Google Scholar
  28. Datko AH, Maclachlan GA (1968) IAA and synthesis of glucanases and pectic enzymes. Plant Physiol 43: 735–742PubMedGoogle Scholar
  29. Digby J, Firn RD (1977) Some criticisms of the use of nojirimycin as a specific inhibitor of auxin-induced growth. Z Pflanzenphysiol 82: 355–362Google Scholar
  30. Evans ML (1974) Evidence against the involvement of galactosidase and glucosidase in auxin- or acid-stimulated growth. Plant Physiol 54: 213–215PubMedGoogle Scholar
  31. Falk SO, Hertz CH, Virgin HI (1958) On the relation between turgor pressure and tissue rigidity. I. Experiments on resonance frequency and tissue rigidity. Physiol Plant 11: 802–817Google Scholar
  32. Fan DF, Maclachlan GA (1967) Massive synthesis of RNA and cellulase in the pea epicotyl in response to IAA, with or without concurrent cell division. Plant Physiol 42: 1114–1122PubMedGoogle Scholar
  33. Ferry JD (1970) Viscoelastic properties of polymers, 2nd ed. Wiley, New York, p 671Google Scholar
  34. Fiedler F, Glazer L (1973) Assembly of bacterial cell walls. Biochem Biophys Acta 300: 467–485Google Scholar
  35. Fujihara S, Yamamoto R, Masuda Y (1978 a) Viscoelastic properties of plant cell walls. II. Effect of pre-extension rate on stress relaxation. Biorheology 15: 77–85PubMedGoogle Scholar
  36. Fujihara S, Yamamoto R, Masuda Y (1978 b) Viscoelastic properties of plant cell walls. III. Hysteresis loop in the stress-strain curve at constant strain rate. Biorheology 15: 87–97Google Scholar
  37. Goldberg R (1977) On possible connections between auxin induced growth and cell wall glucanase activities. Plant Sci Lett 8: 233–242Google Scholar
  38. Gooday GW, Trinci APJ (1980) Wall structure and biosynthesis in fungi. Symp Soc Gen Microbiol 30: 207–252Google Scholar
  39. Goring H, Bleiss W, Schenk D, Kretschmer H (1978) Dependence of the detectability of stored growth on the elongation rates in IAA- and acid-induced elongation of wheat coleoptile section. Plant Cell Physiol 19:833–838Google Scholar
  40. Green PB (1969) Cell morphogenesis. Annu Rev Plant Physiol 20: 365–394Google Scholar
  41. Hager A, Menzel H, Krauss A (1971) Versuche und Hypothese zur Primärwirkung des Auxins beim Streckungswachstum. Planta 100: 47–75Google Scholar
  42. Haughton PM, Sellen DB (1969) Dynamic mechanical properties of the cell walls of some green algae. J Exp Bot 20: 516–535Google Scholar
  43. Haughton PM, Sellen DB, Preston RD (1968) Dynamic mechanical properties of the cell walls of Nitella opaca. J Exp Bot 19: 1–12Google Scholar
  44. Heyn ANJ (1931) Der Mechanismus der Zellstreckung. Rec Trav Bot Néerl 28: 113–244Google Scholar
  45. Heyn ANJ (1933) Further investigations on the mechanism of cell elongation and the properties of the cell wall in connection with elongation. Protoplasma 19: 78–96Google Scholar
  46. Heyn ANJ (1970) Dextranase activity in coleoptiles of Avena. Science 167: 874–875PubMedGoogle Scholar
  47. Huber DJ, Nevins DJ (1979) Autolysis of cell wall β-d-glucan in corn coleoptile. Plant Cell Physiol 20: 201–212Google Scholar
  48. Iwami S, Masuda Y (1973) Hydrogen-ion induced curvature in cucumber hypocotyls. Plant Cell Physiol 14: 757–762Google Scholar
  49. Jaccard M, Pilet PE (1979) Growth and rheological changes of collenchyma cells: the fusicoccin effect. Plant Cell Physiol 20: 1–7Google Scholar
  50. Jacobs M, Ray PM (1975) Promotion of xyloglucan metabolism by acid pH. Plant Physiol 56: 373–376PubMedGoogle Scholar
  51. Johnson KD, Daniels D, Dowler MJ, Rayle DL (1974) Activiation of Avena coleoptile cell wall glycosidases by hydrogen ions and auxin. Plant Physiol 53: 224–228PubMedGoogle Scholar
  52. Kamisaka S, Sano H, Katsumi M, Masuda Y (1972) Effects of cyclic-AMP and gibberellic acid on lettuce hypocotyl elongation and mechanical properties of its cell wall. Plant Cell Physiol 12: 167–174Google Scholar
  53. Katsumi M, Kazama H (1978) Gibberellin control of cell elongation in cucumber hypocotyl sections. Bot Mag Tokyo Spec Issue 1: 141–158Google Scholar
  54. Katz M, Ordin L (1967) A cell wall polysaccharide-hydrolyzing enzyme system in Avena sativa L coleoptiles. Biochem Biophys Acta 141: 126–134PubMedGoogle Scholar
  55. Kawamura H, Kamisaka S, Masuda Y (1976) Regulation of lettuce hypocotyl elongation by gibberellic acid. Correlation between cell elongation, stress-relaxation properties of the cell walls and wall polysaccharide content. Plant Cell Physiol 17: 23–34Google Scholar
  56. Keegstra K, Talmadge KW, Bauer WD, Albersheim P (1973) The structure of plant cell walls. III. A model of the walls of suspension-cultured sycamore cells based on the interconnections of the macromolecular components. Plant Physiol 51: 188–197PubMedGoogle Scholar
  57. Labovitch JM, Ray PM (1974 a) Turnover of cell wall polysaccharide in elongating pea stem sections. Plant Physiol 53: 669–673Google Scholar
  58. Labovitch JM, Ray PM (1974b) Relationship between promotion of xyloglucan metabolism and induction of elongation by IAA. Plant Physiol 54: 499–502Google Scholar
  59. Lockhart JA (1960) Intracellular mechanisms of growth inhibition by radiant energy. Plant Physiol 35: 129–135PubMedGoogle Scholar
  60. Lockhart JA (1965) An analysis of irreversible plant cell elongation. J Theor Biol 8: 264–275PubMedGoogle Scholar
  61. Lockhart JA (1967) Physical nature of irreversible deformation of plant cells. Plant Physiol 42: 1545–1552PubMedGoogle Scholar
  62. Loescher W, Nevins DJ (1972) Auxin-induced changes in Avena coleoptile cell wall composition. Plant Physiol 50: 556–563PubMedGoogle Scholar
  63. Loescher WH, Nevins DJ (1973) Turgor-dependent changes in Avena coleoptile cell wall composition. Plant Physiol 52: 248–251PubMedGoogle Scholar
  64. Maclachlan GA (1977) Cellulose metabolism and cell growth. In: Pilet PE (ed) Plant growth regulation. Springer, Berlin Heidelberg New York, pp 13–20Google Scholar
  65. McNeil M, Albersheim P, Taiz L, Jones RL (1975) The structure of plant cell walls. VII. Barley aleurone cells. Plant Physiol 55: 64–68PubMedGoogle Scholar
  66. Marré E (1979) Fusicoccin: a tool in plant physiology. Annu Rev Plant Physiol 30: 273–288Google Scholar
  67. Masuda Y (1969) Auxin-induced cell expansion in relation to cell wall extensibility. Plant Cell Physiol 10: 1–9Google Scholar
  68. Masuda Y (1968) Auxin-induced cell wall loosening. Bot Mag Tokyo Spec Issue 1: 103–123Google Scholar
  69. Masuda Y, Yamamoto R (1970) Effect of auxin on β-1,3-glucanase activity in Avena coleoptile. Dev Growth Differ 11: 287–296PubMedGoogle Scholar
  70. Masuda Y, Yamamoto R, Kawamura H, Yamagata Y (1974) Stress relaxation properties of the cell wall of tissue segments under different growth conditions. Plant Cell Physiol 15: 1083–1092Google Scholar
  71. Métraux JP, Taiz L (1977) Cell wall extension in Nitella as influenced by acid and ions. Proc Natl Acad Sci USA 74: 1565–1569PubMedGoogle Scholar
  72. Monro JA, Penny D, Bailey RW (1976) The organization and growth of primary cell walls of lupin hypocotyls. Phytochemistry 15: 1193–1198Google Scholar
  73. Morré DJ, Eisinger WR (1968) Cell wall extensibility; its control by auxin and relationship to cell elongation. In: Wightman F, Setterfield G (eds) Biochemistry and physiology of plant growth substances. Runge Press, Ottawa, pp 625–645Google Scholar
  74. Nakamura T, Sekine S, Arai K, Takahashi N (1975) Effects of gibberellic acid and IAA on stress-relaxation properties of pea hook cell wall. Plant Cell Physiol 16: 127–138Google Scholar
  75. Nevins DJ (1975a) The effect of nojirimycin on plant growth and its implications concerning a role of exo-β-glucanases in auxin-induced cell expansion. Plant Cell Physiol 16: 347–356Google Scholar
  76. Nevins DJ (1975 b) The in vitro simulation of IAA-induced modification of Avena cell wall polysaccharides by an exo-glucanase. Plant Cell Physiol 16: 495–503Google Scholar
  77. Nevins DJ, Huber DJ, Yamamoto R, Loescher W (1977) β-d-glucan of Avena coleoptile cell wall. Plant Physiol 60: 617–620PubMedGoogle Scholar
  78. Nishitani K, Masuda Y (1980) Modifications of cell wall polysaccharides during auxin-induced growth in azuki bean epicotyl segments. Plant Cell Physiol 21: 169–181Google Scholar
  79. Nishitani K, Shibaoka H, Masuda Y (1979) Growth and cell changes in azuki bean epicotyls. II. Changes in wall polysaccharides during auxin-induced growth of excised segments. Plant Cell Physiol 20: 463–472Google Scholar
  80. Noodén LD, Thimann KV (1963) Evidence for a requirement for protein synthesis for auxin-induced cell enlargement. Proc Natl Acad Sci USA 50: 194–200PubMedGoogle Scholar
  81. Olson AC, Bonner J, Morré DJ (1965) Force extension analysis of Avena coleoptile cell walls. Planta 66: 127–133Google Scholar
  82. Osborne DJ (1977) Auxin and ethylene and the control of cell growth. Identification of three classes of target cells. In: Pilet PE (ed) Plant growth regulation. Springer, Berlin Heidelberg New York, pp 161–171Google Scholar
  83. Penny P, Penny D (1978) Rapid responses to phytohormones. In: Letham DS, Goodwin PB, Higgins TJV (eds) Phytohormones and related compounds. Vol II. North Holland, Amsterdam, pp 537–597Google Scholar
  84. Penny P, Penny D, Marshall D, Heyes JK (1972) Early responses of excised stem segments to auxins. J Exp Bot 23: 23–36Google Scholar
  85. Penny D, Penny P, Marshall DC (1974) High resolution measurement of plant growth. Can J Bot 52: 959–969Google Scholar
  86. Pilet PE (1971) Les Parois Cellulaires. Doin, Paris, p 172Google Scholar
  87. Pilet PE, Roland J-C (1974) Growth and extensibility of collenchyma cells. Plant Sci Lett 2: 203–207Google Scholar
  88. Preston RD (1974) The physical biology of plant cell walls. Chapman and Hall, London, p 491Google Scholar
  89. Probine MC, Preston RD (1962) Cell growth and the structure and mechanical properties of the wall in internodal cells of Nitella opaca. II. Mechanical properties of the walls. J Exp Bot 13: 111–127Google Scholar
  90. Ray PM (1962) Cell wall synthesis and cell elongation in oat coleoptile tissues. Am J Bot 49: 928–939Google Scholar
  91. Ray PM (1974) The biochemistry of the action of IAA on plant growth. In: Runeckles VC, Sondheimer E (eds) The chemistry and biochemistry of plant hormones. Academic Press, New York, pp 93–122Google Scholar
  92. Ray PM, Ruesink AW (1962) Kinetic experiments on the nature of the growth mechanism in oat coleoptile cells. Dev Biol 4: 377–397Google Scholar
  93. Ray PM, Green PB, Cleland RE (1972) Role of turgor in plant cell growth. Nature 239: 163–164Google Scholar
  94. Rayle DL (1973) Auxin-induced hydrogen-ion excretion in Avena coleoptiles and its implications. Planta 114: 63–73Google Scholar
  95. Rayle DL, Cleland RE (1970) Enhancement of wall loosening and elongation by acid solutions. Plant Physiol 46: 250–253PubMedGoogle Scholar
  96. Rayle DL, Cleland RE (1972) The in-vitro acid-growth response: relation to in-vivo growth responses and auxin action. Planta 104: 282–296Google Scholar
  97. Rayle DL, Cleland RE (1977) Control of plant cell enlargement by hydrogen ions. Curr Top Dev Biol 11: 187–214PubMedGoogle Scholar
  98. Rayle DL, Haughton PM, Cleland RE (1970) An in vitro system that simulates plant cell extension growth. Proc Natl Acad Sci USA 67: 1814–1817PubMedGoogle Scholar
  99. Roelofsen PA (1965) Ultrastructure of the wall in growing cells and its relation to the direction of growth. Adv Bot Res 2: 69–149Google Scholar
  100. Roland J-C, Vian B (1979) The wall of the growing cell: its three dimensional organization. Int Rev Cytol 61: 129–166Google Scholar
  101. Ruesink AW (1969) Polysaccharidases and the control of cell wall elongation. Planta 89: 95–107Google Scholar
  102. Sakurai N, Masuda Y (1978) Auxin-induced extensibility, cell wall loosening and changes in the wall polysaccharide content of barley coleoptile segments. Plant Cell Physiol 19: 1225–1233Google Scholar
  103. Sakurai N, Masuda Y (1979) Effect of cycloheximide and cordycepin on auxin-induced elongation and β-glucan degredation of non-cellulosic polysaccharides of Avena coleoptile cell walls. Plant Cell Physiol 20: 593–603Google Scholar
  104. Sakurai N, Nevins DJ, Masuda Y (1977) Auxin and hydrogen ion-induced cell wall loosening and cell extension in Avena coleoptile segments. Plant Cell Physiol 18: 371–380Google Scholar
  105. Sakurai N, Nishitani K, Masuda Y (1979) Auxin-induced changes in the molecular weight of hemicellulosic polysaccharides of the Avena coleoptile cell wall. Plant Cell Physiol 20: 1349–1357Google Scholar
  106. Sumiya K, Yamada T (1974) Effect of IAA on stress relaxation of Japanese black pine seedling. Wood Res 56: 13–20Google Scholar
  107. Tagawa T, Bonner J (1957) Mechanical properties of the Avena coleoptile as related to auxin and to ionic interactions. Plant Physiol 32: 207–212PubMedGoogle Scholar
  108. Tanimoto E, Igari M (1976) Correlation between β-galactosidase and auxin-induced elongation growth in etiolated pea stems. Plant Cell Physiol 17: 673–682Google Scholar
  109. Tanimoto E, Masuda Y (1968) Effect of auxin on cell wall degrading enzymes. Physiol Plant 21: 820–826Google Scholar
  110. Tanimoto E, Masuda Y (1971) Role of the epidermis in auxin-induced elongation of light-grown pea stem segments. Plant Cell Physiol 12: 663–673Google Scholar
  111. Tepfer M, Cleland RE (1979) A comparison of acid-induced cell wall loosening in Valonia ventricosa and in oat coleoptiles. Plant Physiol 63: 898–902PubMedGoogle Scholar
  112. Terry M, Rubinstein B, Jones RL (1980) Changes in soluble cell wall polysaccharides and growth. Plant Physiol 65: S23Google Scholar
  113. Uhrström I (1974) The effect of auxin and low pH on Young’s modulus in Pisum stems and on water permeability in potato parenchyma. Physiol Plant 30: 97–102Google Scholar
  114. Valent BS, Albersheim P (1974) The structure of plant cell walls. V. On the binding of xyloglucan to cellulose fibers. Plant Physiol 54: 105–108PubMedGoogle Scholar
  115. Verma DPS, Maclachlan GA, Byrne H, Ewings D (1975) Regulation and in vitro translation of messenger RNA for cellulose from auxin-treated pea epicotyls. J Biol Chem 250: 1019–1026PubMedGoogle Scholar
  116. Waaland SD, Waaland JR, Cleland RE (1972) A new pattern of plant cell elongation: bipolar band growth. J Cell Biol 54: 184–190PubMedGoogle Scholar
  117. Wada S, Ray PM (1978) Matric polysaccharides of oat coleoptile cell walls. Phytochemistry 17: 923–931Google Scholar
  118. Wada S, Tanimoto E, Masuda Y (1968) Cell elongation and metabolic turnover of the cell wall as affected by auxin and cell wall degrading enzymes. Plant Cell Physiol 9: 269–276Google Scholar
  119. Yamagata Y, Masuda Y (1975) Comparative studies on auxin and fusicoccin actions on plant growth. Plant Cell Physiol 16: 41–52Google Scholar
  120. Yamagata Y, Masuda Y (1976) Auxin-induced extension of the isolated epidermis of light-grown pea epicotyls. Plant Cell Physiol 17: 1235–1242Google Scholar
  121. Yamagata Y, Yamamoto R, Masuda Y (1974) Auxin and hydrogen ion actions on light-grown pea epicotyl sections. II. Effect of hydrogen ions on extension of isolated epidermis. Plant Cell Physiol 15: 833–841Google Scholar
  122. Yamamoto R, Masuda Y (1971) Stress-relaxation properties of the Avena coleoptile cell wall. Physiol Plant 25: 330–335Google Scholar
  123. Yamamoto R, Nevins DJ (1979) A transglucosylase from Sclerotinia libertiana. Plant Physiol 64: 193–196PubMedGoogle Scholar
  124. Yamamoto R, Shinozyki K, Masuda Y (1970) Stress-relaxation properties of plant cell walls with special reference to auxin action. Plant Cell Physiol 11: 947–956Google Scholar
  125. Yamamoto R, Makai K, Masuda Y (1974) Auxin and hydrogen ion actions on light-grown pea epicotyl segments. III. Effect of auxin and hydrogen ions on stress-relaxation properties. Plant Cell Physiol 15: 1027–1038Google Scholar
  126. Yoda S, Ashida J (1960) Effect of gibberellin and auxin on the extensibility of the pea stem. Plant Cell Physiol 1: 99–105Google Scholar
  127. Zarra I, Masuda Y (1979) Growth and cell wall changes in rice coleoptiles growing under different conditions. II. Auxin-induced growth in coleoptile segments. Plant Cell Physiol 20: 1125–1133Google Scholar

Copyright information

© Springer-Verlag Berlin · Heidelberg 1981

Authors and Affiliations

  • R. E. Cleland

There are no affiliations available

Personalised recommendations