Plant Molecular Biology

, Volume 26, Issue 5, pp 1329–1341

Mechanical signalling, calcium and plant form

  • Anthony Trewavas
  • Marc Knight


Calcium is a dynamic signalling molecule which acts to transduce numerous signals in plant tissues. The basis of calcium signalling is outlined and the necessity for measuring and imaging of calcium indicated. Using plants genetically transformed with a cDNA for the calcium-sensitive luminescent protein, aequorin, we have shown touch and wind signals to immediately increase cytosol calcium. Touch and wind signal plant cells mechanically, through tension and compression of appropiate cells. Many plant tissues and cells are very sensitive to mechanical stimulation and the obvious examples of climbing plants, insectivorous species as well as other less well-known examples are described. Touch sensing in these plants may be a simple evolutionary modification of sensitive mechanosensing system present in every plant. The possibility that gravitropism may be a specific adaptation of touch sensing is discussed. There is a growing appreciation that plant form may have a mechanical basis. A simple mechanical mechanism specifying spherical, cylindrical and flat-bladed structures is suggested. The limited morphological variety of plant tissues may also reflect mechanical specification. The article concludes with a discussion of the mechanisms of mechanical sensing, identifying integrin-like molecules as one important component, and considers the specific role of calcium.

Key words

aequorin cytosol calcium mechanosensing morphogenesis touch wind 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Allan AC, Fricker MD, Ward J, Beale M, Trewavas AJ: Caged ABA induced calcium transients in guard cells of Commelina communis are dependant on previous growth temperature Plant Cell 6 1319–1328.Google Scholar
  2. 2.
    Bachs O, Carafoli E: Calmodulin and calmodulin-binding proteins in liver cell nuclei. J Biol Chem 262: 10786–10790 (1987).PubMedGoogle Scholar
  3. 3.
    Barritt GJ: Communication Within Animal Cells. Oxford University Press Oxford (1992).Google Scholar
  4. 4.
    Bentrup FW: Reception and transduction of electrical and mechanical stimuli. In: Haupt WB, Feinlieb ME (eds) Physiology of Movements. Encyclopedia of Plant Physiology, New Series, vol. 7, pp. 42–70 (1979).Google Scholar
  5. 5.
    Braam J, Davies RW: Rain-, wind- and touch-induced expression of calmodulin and calmodulin related genes in Arabidopsis. Cell 60: 357–364 (1990).CrossRefPubMedGoogle Scholar
  6. 6.
    Bunning E: Über die Verhinderung des Etiolements. Ber Deut Bot Ges 59: 2–9 (1941).Google Scholar
  7. 7.
    Bunning E, Lempnau C: Über die Wirkung mechnischer und photischer Reize auf die Gewebe und Organbildung von Mimosa pudica. Ber Deut Bot Ges 67: 10–18 (1954).Google Scholar
  8. 8.
    Burridge K, Fath K, Kelly T, Nuckolls G, Turner C: Focal adhesions. Annu Rev Cell Biol 4: 487–525 (1988).PubMedGoogle Scholar
  9. 9.
    Caspar T, Pickard BG: Gravitropism by a starchless mutant of Arabidopsis; implications for the starch statolith theory. Planta 177: 185–197 (1989).PubMedGoogle Scholar
  10. 10.
    Clifford PE, Fensom DS, Munt BJ, McDowell WE: Lateral stress initiates bending responses in dandelion peduncles; a clue to geotropism? Can J Bot 60: 2671–2673 (1982).Google Scholar
  11. 11.
    Damsky CH, Werb Z: Signal transduction by integrin receptors for extracellular matrix: cooperative processing of extracellular information. Curr Opin Cell Biol 4: 772–781 (1992).CrossRefPubMedGoogle Scholar
  12. 12.
    Darwin C: The Power of Movement in Plants, John Murray, London (1880).Google Scholar
  13. 13.
    Darwin C: The Movements and Habits of Climbing Plants. John Murray, London (1891).Google Scholar
  14. 14.
    Denton RM, McCormack JG, Edyell NJ: Role of calcium ions in the regulation of intramitochondrial metabolism. Biochem J 190: 107–117 (1980).PubMedGoogle Scholar
  15. 15.
    Ding JP, Pickard BG: Mechanosensory calcium selective cation channels in epidermal cells. Plant J 3: 83–110 (1993).CrossRefGoogle Scholar
  16. 16.
    Evans DE, Briars SA, Williams LE: Active calcium transport by plant cell membranes. J Exp Bot 42: 285–303 (1991).Google Scholar
  17. 17.
    Franklin-Tong VE, Ryde JP, Read ND, Trewavas AJ, Franklin C: The self incompatability response in Papaver rhoeas is mediated by free cytosolic calcium. Plant J 4: 163–177 (1993).CrossRefGoogle Scholar
  18. 18.
    Gilroy S, Bethke PC, Jones RL: Calcium homeostasis in plants. J Cell Sci 106: 453–462 (1993).PubMedGoogle Scholar
  19. 19.
    Gilroy S, Read ND, Trewavas AJ: Elevation of cytosol calcium using caged calcium and caged inostiol phosphate initiates stomatal closure. Nature 346: 769–771 (1990).CrossRefPubMedGoogle Scholar
  20. 20.
    Gilroy S, Trewavas AJ: Signal sensing and signal transduction across the plasma membrane. In: Larsson C, Moller IM (eds) The Plant Plasma Membrane, pp. 203–233. Springer-Verlag, Heidelberg (1990).Google Scholar
  21. 21.
    Ginsburg MH, Xiaoping D, Plow EF: Inside-out integrin signalling. Curr Opin Cell Biol 4: 766–771 (1992).CrossRefPubMedGoogle Scholar
  22. 22.
    Goodner R, Quatrano RS: Fucus embryogenesis: a model to study the establishment of polarity. Plant Cell 5: 1471–1481 (1993).CrossRefPubMedGoogle Scholar
  23. 23.
    Goodwin BC, Briere C, O'Shea POP: Mechanisms underlying the formation of spatial structure in cells. Soc Gen Microbiol Symp 23: 1–9 (1987).Google Scholar
  24. 24.
    Goodwin BC, Trainor LEH: Tip and whorl morphogensis in Acetabularia by calcium regulated strain fields. J Theor Biol 117: 79–106 (1985).Google Scholar
  25. 25.
    Grace J: Plant Response to Wind. Academic Press, London (1977).Google Scholar
  26. 26.
    Hanson JB, Trewavas AJ: Regulation of plant cell cell growth: the changing perspective. New Phytol 90: 1–18 (1982).Google Scholar
  27. 27.
    Hirouchi T, Suda S: Thigmotropism in the growth of pollen tubes of Lilium longiflorum. Plant Cell Physiol 16: 377–381 (1975).Google Scholar
  28. 28.
    Hoch HC, Staples RC, Whitehead B, Comeau J, Wolf ED: Signalling for growth orientation and cell differentiation by surface topography in Uromyces. Science 235: 1659–1662 (1987).Google Scholar
  29. 29.
    Hynes RO: Integrins: A family of cell surface receptors. Cell 48: 549–554 (1987).CrossRefPubMedGoogle Scholar
  30. 30.
    Ingber D: Integrins as mechanochemical transducers. Curr Opin Cell Biol 3: 841–848 (1991).CrossRefPubMedGoogle Scholar
  31. 31.
    Jaffe MJ: Classes and mechanisms of calcium waves. Cell Calcium 14: 736–745 (1993).CrossRefPubMedGoogle Scholar
  32. 32.
    Jaffe MJ: Thigmomorphogenesis; the response of plant growth and development to mechanical perturbation. Planta 114: 143–157 (1973).Google Scholar
  33. 33.
    Jones RS, Mitchell CA: Calcium ion involvment in growth inhibition of mechanically-stressed soybean seedlings. Physiol Plant 76: 598–602 (1989).PubMedGoogle Scholar
  34. 34.
    Kirchhofer D, Grzesiak J, Pierschbascher MD: Calcium as a potential physiological regulator of integrin mediated cell adhesion J Biol Chem 266: 4471–4477 (1991).PubMedGoogle Scholar
  35. 35.
    Kiss JZ, Sack FD: Severely-reduced gravitropism in dark grown hypocotyls of a starch deficient mutant of Nicotiania sylvestris. Planta 180: 123–130 (1989).PubMedGoogle Scholar
  36. 36.
    Knight MR, Campbell AK, Smith SM, Trewavas AJ: Transgenic plant aequorin reports the effects of touch and cold shock and fungal elicitors on cytosolic calcium. Nature 352: 524–526 (1991).CrossRefPubMedGoogle Scholar
  37. 37.
    Knight MR, Smith SM, Trewavas AJ: Wind-induced plant motion immediately increases cytosolic calcium. Proc Natl Acad Sci USA 89: 4967–4972 (1992).PubMedGoogle Scholar
  38. 38.
    Knight MR, Read ND, Campbell AK, Trewavas AJ: Imaging calcium dynamics in living plants using semisynthetic recombinant aequorins. J Cell Biol 121: 83–90 (1993).CrossRefPubMedGoogle Scholar
  39. 39.
    Kutschera U: The role of the epidermis in the control of elongation growth in stems and coleoptiles. Bot Acta 105: 246–253 (1992).Google Scholar
  40. 40.
    Lang A: Progressiveness and contagiousness in plant differentiation and development. Encyclopedia of Plant Physiology vol 15 (1), pp. 409–424 (1964).Google Scholar
  41. 41.
    Linthilac PM, Vesecky TB: Stress-induced alignment of division plane in plant tissues grown in vitro. Nature 307: 363–364 (1984).Google Scholar
  42. 42.
    Liu Y, Storm DR: Dephosphorylation of neuromodulin by calcineurin. J Biol Chem 264: 12800–12804 (1989). Trends Pharmacol 11: 107–111 (1990).PubMedGoogle Scholar
  43. 43.
    Malho R, Read ND, Pais MS, Trewavas AJ: Role of cytosolic free calcium in the reorientation of pollen tube growth. Plant J 5: 331–341 (1994).Google Scholar
  44. 44.
    McCormack JG, Halestrap AP, Denton RM: Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol Rev 70: 391–425 (1990).PubMedGoogle Scholar
  45. 45.
    Melkonian B, Burchet M, Kreimer G, Latzko E: Binding and possible function of calcium in the chloroplast. Curr Topics Plant Biochem Physiol 9: 38–46 (1990).Google Scholar
  46. 46.
    Miller DB, Callahan DA, Gross DJ, Hepler PK: Free Ca2+ gradient in growing pollen tubes of Lilium. J Cell Sci 101: 7–12 (1992).Google Scholar
  47. 47.
    Neel PL, Harris RW: Motion-induced inhibition of elongation and induction of dormancy in Liquidamber. Science 173: 58–59 (1971).Google Scholar
  48. 48.
    Neel PL, Harris RW: Growth inhibition by mechanical stress. Science 174: 961–962 (1972).Google Scholar
  49. 49.
    Neel PL, Harris RW: Tree seedling growth: effect of shaking. Science 175: 918–919 (1972).Google Scholar
  50. 50.
    Obermeyer G, Weisenseel MH: Calcium channel blocker and calmodulin antagonists affect the gradient of free calcium ions in lily pollen tubes. Eur J Cell Biol 56: 319–327 (1991).PubMedGoogle Scholar
  51. 51.
    Odell GM, Oster G, Alberch P, Burnside B: The mechanical basis of morphogenesis. Devel Biol 85: 446–462 (1981).Google Scholar
  52. 52.
    Oster GF, Murray JD, Harris AK: Mechanical aspects of mesenchymal morphogenesis. J Embryol Exp Morphol 78: 83–125 (1983).PubMedGoogle Scholar
  53. 53.
    Pfeffer W: The Physiology of Plants, vol 3 (translated by A.J. Ewart). Clarendon Press, Oxford (1906).Google Scholar
  54. 54.
    Pickard BD, Ding JP: Gravity sensing by higher plants. Adv Comp Envir Physiol 10: 81–110 (1992).Google Scholar
  55. 55.
    Poovaiah BW, Reddy ASN: Calcium and signal transduction in plants. Crit Rev Plant Sci 12: 185–211 (1993).PubMedGoogle Scholar
  56. 56.
    Rathore KS, Cork RJ, Robinson KR: A cytoplasmic gradient of Ca2+ is correlated with the growth of lily pollen tubes. Devel Biol 148: 612–619 (1991).Google Scholar
  57. 57.
    Sanders LC, Wang CS, Walling LL, Lord EM: A homolog of the substrate adhesion factor vitronectin occurs in four species of flowering plants. Plant Cell 3: 629–635 (1991).PubMedGoogle Scholar
  58. 58.
    Schindler M, Meiners S, Cheresh DA: RGD-dependent linkage between plant cell wall and plasma membrane; consequences for growth. J Cell Biol 108: 1955–1965 (1989).PubMedGoogle Scholar
  59. 59.
    Selker JML, Steucek GL, Green PB: Biophysical mechanisms for morphogenetic progressions at the shoot apex. Devel Biol 153: 29–43 (1992).Google Scholar
  60. 60.
    Shacklock P, Read ND, Trewavas AJ: Cytosolic free calcium mediates red light induced photomorphogeneis. Nature 358: 753–755 (1992).Google Scholar
  61. 61.
    Shankar G, Davison I, Helfrich MP, Mason WT, Horton MA. Integrin receptor mediated mobilisation of intranuclear calcium in rat osteoclasts. J Cell Sci 105: 61–68 (1993).PubMedGoogle Scholar
  62. 62.
    Sinclair W, Oliver I, Maher P, Trewvas AJ: Effect of gravistimulation on calmodulin mRNA in wild type and mutant Arabidopsis plants. Plant Physiol, submitted (1994).Google Scholar
  63. 63.
    Stark P: Weitere Untersuchungen über das Restantengesetz beim Haptotropismus. Jahrb Wiss Bot 61: 126–167 (1921).Google Scholar
  64. 64.
    Stinemetz CL, Kuzmanoff KM, Evans ML, Jarret HW: Correlations between calmodulin activity and gravitropic sensitivity in primary roots of maize. Plant Physiol 84: 1337–1342 (1987).PubMedGoogle Scholar
  65. 65.
    Thompson DA: On Growth and Form. Cambridge University Press, Cambridge, UK (1942).Google Scholar
  66. 66.
    Trewavas AJ: How do plant growth substances work? Plant Cell Envir 4: 203–228 (1981).Google Scholar
  67. 67.
    Trewavas AJ: How do plant growth substances work? II. Plant Cell Envir 14: 1–12 (1991).Google Scholar
  68. 68.
    Trewavas AJ, Knight MR: The regulation of shape and form by cytosolic calcium. In: Ingram D, Hudson A (eds) Shape and Form in Plant and Fungal Cells, pp. 221–233. Academic Press, London (1992).Google Scholar
  69. 69.
    Wagner VT, Brian L, Quatrano RS: Role of a vitronectinlike molecule in embryo adhesion of the brown alga Fucus. Proc Natl Acad Sci USA 89: 3644–3648 (1992).PubMedGoogle Scholar
  70. 70.
    Wang N, Butler JP, Ingber D: Mechanotransduction across the cell surface and through the cytoskeleton. Science 260: 1124–1127 (1993).PubMedGoogle Scholar
  71. 71.
    Wayne R, Staves MP, Leopold AC: Gravity dependent polarity of cytoplasmic streaming in Nitellopsis. Protoplasma 155: 43–57 (1990).PubMedGoogle Scholar
  72. 72.
    Wyatt SE, Carpita NC: The plant cytoskelton-cell wall continuum Trends Cell Biol 3: 413–417 (1993).CrossRefPubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • Anthony Trewavas
    • 1
  • Marc Knight
    • 2
  1. 1.Molecular Signalling Group, Institute of Cell and Molecular BiologyUniversity of EdinburghEdinburghUK
  2. 2.Plant SciencesUniversity of OxfordOxfordUK

Personalised recommendations