Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Opinion
  • Published:

Signal processing and transduction in plant cells: the end of the beginning?

Nature Reviews Molecular Cell Biology volume 2, pages 307–314 (2001)Cite this article

Abstract

Plants have a very different lifestyle to animals, and one might expect that unique molecules and processes would underpin plant-cell signal transduction. But, with a few notable exceptions, the list is remarkably familiar and could have been constructed from animal studies. Wherein, then, does lifestyle specificity emerge?

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: A wide range of disparate external and internal signals is monitored by plants and used to compute appropriate developmental responses.
Figure 2: Plant cell signalling systems show characteristics of cell-to-cell individuality, threshold phenomena and environmental entrainment.
Figure 3: The domain structures of several known plant receptor proteins, putative receptors or components of putative perception complexes, and their respective ligands.
Figure 4: Plants show extensive cross-talk and interactions between signalling systems.

Similar content being viewed by others

References

  1. Trewavas, A. J. in Plasticity in Plants (eds Jennings, D. & Trewavas, A. J.) Symp. Soc. Expt. Biol. Med. 40, 31– 77 (1986).

    Google Scholar 

  2. Trewavas, A. J., Sexton, R. & Kelly, P. Polarity calcium and abscission: molecular bases for developmental plasticity in plants. J. Embryol. Exp. Morphol. 83, S179–S195 (1984).

    Google Scholar 

  3. Smith, H. & Whitlam, G. C. The shade avoidance syndrome: multiple responses mediated by multiple phytochromes. Plant Cell Environ. 20, 840–844 ( 1997).

    Google Scholar 

  4. Wijensinghe, D. K. & Hutchings, M. J. The effects of environmental heterogeneity on the performance of Glechoma: the interactions between patch scale and patch contrast. J. Ecol. 87, 860–872 (1999).

  5. Trewavas, A. J. in Biochemistry and Molecular Biology of Plants (eds Buchanan, R. B., Gruissem, W. & Jones, R. L.) 930–988 (Am. Soc. of Plant Physiologists, Rockville Maryland, 2000).

    Google Scholar 

  6. Jenkins, G. I. Signal transduction networks and the integration of responses to environmental stimuli. Adv. Bot. Res. 29, 54– 74 (1999).

    Google Scholar 

  7. Novoplansky, A. Developmental responses of Portulaca seedlings to conflicting spectral signals. Oecologia 88, 138– 140 (1991).

    PubMed  Google Scholar 

  8. Novoplansky, A., Cohen, D. & Sachs, T. Ecological implications of correlative inhibition between plant shoots. Oecologia 82, 490– 493 (1990).

    PubMed  Google Scholar 

  9. Kelly, C. E. Resource choice in Cuscuta europea. Proc. Natl Acad. Sci. USA 89, 12194–12197 ( 1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Kelly, C. K. Plant foraging: a marginal value model and coiling response in Cuscuta subinclusa. Ecology 71, 1916– 1925 (1990).

    Google Scholar 

  11. Gilroy, S. & Trewavas, A. J. in The Plant Plasma Membrane (eds Larsson, C. & Moller, I. M.) 203–233 (Springer, Berlin, 1990).

    Google Scholar 

  12. Trewavas, A. J. & Knight, M. R. Calcium, mechanical signalling and plant form. Plant Mol. Biol. 26, 1329–1341 (1994).

    CAS  PubMed  Google Scholar 

  13. Green, P. B. Expression of pattern in plants: combining molecular and calculus-based biophysical paradigms. Am. J. Bot. 86, 1059– 1076 (1999).

    CAS  PubMed  Google Scholar 

  14. Fleming, A. J., Caderas, D., Wehrli, E., McQueen-Mason, S. & Kuhlemeier, C. Analysis of expansin-induced morphogenesis on the apical meristem of tomato. Planta 208, 166– 174 (1999).

    CAS  Google Scholar 

  15. Cosgrove, D. J. New genes and new biological roles for expansins. Curr. Opin. Plant Biol. 3, 73–78 ( 2000).

    CAS  PubMed  Google Scholar 

  16. Knight, M. R., Knight, H. & Watkins, N. J. Calcium and the generation of plant form. Phil. Trans. R. Soc. Lond. B 350, 83– 86 (1995).

    Google Scholar 

  17. Firn, R. & Digby, J. Solving the puzzle of gravitropism — has a lost piece been found? Planta 203, S159–S163 (1997).

    CAS  PubMed  Google Scholar 

  18. Sultan, S. E. Phenotypic plasticity for plant development, function and life history. Trends Plant Sci. 5, 537–542 (2000).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  20. School, H. et al. The stem cell population of Arabidopsis shoot meristem is maintained by a regulatory loop between the clavata and wuschel genes. Cell 100, 635–644 ( 2000).

    Google Scholar 

  21. Trewavas, A. J. in Plant Responses to Environmental Stresses (ed. Lerner, H. R.) 27–42 (Marcel Dekker, New York, 1999 ).

    Google Scholar 

  22. Trewavas, A. J. How do plant growth substances work? (II). Plant Cell Environ. 14, 1–12 (1991 ).

    CAS  Google Scholar 

  23. Mott, K. A. & Buckley, T. N. Patchy stomatal conductance emergent collective behaviour. Trends Plant Sci. 5, 258–262 (2000).

    CAS  PubMed  Google Scholar 

  24. Hillmer, S., Gilroy, S. & Jones, R. L. Visualising enzyme secretion from individual barley protoplasts. Plant Physiol. 102, 279– 286 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Ritchie, S., McCubbin, A., Ambrose, G., Kao, T.-H. & Gilroy, S. The sensitivity of barley aleurone tissue to gibberellin is heterogeneous and may be spatially determined. Plant Physiol. 120, 361–370 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Bradford, K. J. & Trewavas, A. J. Sensitivity thresholds and variable time scales in plant hormone action. Plant Physiol. 105, 1029–1036 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Blakeley, L. M., Rodaway, S. J., Hollen, L. B. & Croker, S. G. Control and kinetics of branch root formation in cultured root segments of Haplopappus ravenii. Plant Physiol. 50, 35–42 (1972).

    Google Scholar 

  28. Novick, A. & Weiner, M. Enzyme induction as an all or none phenomenon. Proc. Natl Acad. Sci. USA 43, 553–566 (1957).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. McAdams, H. H. & Arkin, A. Genetic regulation at the nanomolar scale. Trends Genet. 15, 65–69 (1999).

    CAS  PubMed  Google Scholar 

  30. Gilroy, S., Fricker, M., Read, N. & Trewavas, A. J. Role of calcium in signal transduction of Commelina guard cells. Plant Cell 3, 333–344 ( 1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Blancaflor, E. B. & Gilroy, S. Plant cell biology in the new millennium: new tools and new insights. Am. J. Bot. 87, 1547–1560 ( 2000).

    CAS  PubMed  Google Scholar 

  32. Trewavas, A. J. & Malho, R. Perception and transduction: the origin of the phenotype. Plant Cell 9, 1181–1195 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Trewavas, A. J. Le calcium c'est la vie. Calcium makes waves. Plant Physiol. 120, 1–6 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Trewavas, A. J. How plants learn. Proc. Natl Acad. Sci. USA 96, 4216–4218 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Meskienne, I. & Hirt, H. MAP kinase pathways: molecular plug and play chips for the cell. Plant Mol. Biol. 42, 791–806 (2000).

    Google Scholar 

  36. McCarty, D. R. & Chory, J. Conservation and innovation in plant signalling pathways. Cell 103, 201–209 (2000).

    CAS  PubMed  Google Scholar 

  37. He, Z. et al. Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 288, 2360– 2361 (2000).

    CAS  PubMed  Google Scholar 

  38. Genick, U. K. & Chory, J. Red light sensing in plants. Curr. Biol. 10, R651–R654 (2000).

    CAS  PubMed  Google Scholar 

  39. Smeekens, S. Sugar-induced signal transduction in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 49–81 (2000).

    CAS  PubMed  Google Scholar 

  40. Torii, K. U. Receptor kinase activation and signal transduction in plants: an emerging picture. Curr. Opin. Plant Biol. 3, 361– 367 (2000).

    CAS  PubMed  Google Scholar 

  41. Schopfer, C., Nasrallah, M. & Nasrallah, J. The male determinant of self incompatability in Brassica. Science 286, 1697– 1700 (1999).

    CAS  PubMed  Google Scholar 

  42. Cashmore, A. R., Jarillo, J. A., Wu, Y.-J. & Liu, D. Cryptochromes: blue light receptors for plants and animals. Science 284, 760–765 (1999).

    CAS  PubMed  Google Scholar 

  43. Christie, J. M., Salomon, I., Nozue, K., Wada, M. & Briggs, W. R. LOV (light, oxygen, or voltage) domains of the blue-light photoreceptor phototropin (nph1): binding sites for the chromophore flavin mononucleotide. Proc. Natl Acad. Sci. USA 96, 8779–8783 (2000).

    Google Scholar 

  44. Stepanova, A. N. & Ecker, J. R. Ethylene signalling from mutants to molecules. Curr. Opin. Plant Biol. 3, 353–360 (2000).

    CAS  PubMed  Google Scholar 

  45. Inoue, T. et al. Identification of CRE1 as a cytokinin receptor from Arabidopsis . Nature 409, 1060– 1063 (2001).

    CAS  PubMed  Google Scholar 

  46. Galwieler, L. et al. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226– 2230 (1998).

    Google Scholar 

  47. Jones, A. M. et al. ABP1: auxin-dependent cell expansion mediated by overexpressed auxin-binding protein 1. Science 282, 1114 –1117 (1999).

    Google Scholar 

  48. Salisbury, F. B. & Ross, C. W. Plant Physiology 4th edn (Wadsworth, California, 1992).

    Google Scholar 

  49. Baum, G., Long, J., Jenkins, G. & Trewavas, A. J. Stimulation of the blue light receptor NPH1 causes a transient increase in cytosolic calcium . Proc. Natl Acad. Sci. USA 98, 13554– 13559 (1999).

    Google Scholar 

  50. Taiz, L. & Zeiger, E. Plant Physiology 2nd edn (Sinauer Associates, Massachusetts, 1998).

    Google Scholar 

  51. Kaul, B. et al. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796– 815 (2000).

    CAS  Google Scholar 

  52. Staehelin, L. A. & Newcomb, E. H. in Biochemistry and Molecular Biology of Plants (eds Buchannan, R. B., Gruissem, W. & Jones, R. L.) 2–50 (Am. Soc. of Plant Physiologists, Rockville, Maryland, 2000).

    Google Scholar 

  53. Harmon, A., Gribskov, M. & Harper, J. F. CDPK's, a kinase for every signal. Trends Plant Sci. 5, 154–159 ( 2000).

    CAS  PubMed  Google Scholar 

  54. Satterlee, J. S. & Sussman, M. R. Unusual membrane-associated protein kinases in higher plants. J. Memb. Biol. 164 , 205–213 (1998).

    CAS  Google Scholar 

  55. Hirsch, R. E., Lewis, B. D., Spalding, E. P. & Sussman, M. R. A role for the AKT1 potassium channel in plant nutrition. Science 280, 918–921 ( 1998).

    CAS  PubMed  Google Scholar 

  56. Volkmann, D. The plasma membrane of growing root hairs is composed of zones of local differentiation . Planta 162, 392–403 (1984).

    CAS  PubMed  Google Scholar 

  57. Malho, R., Moutinho, A., Van der Luit, A. & Trewavas, A. J. Spatial characteristics of calcium signalling: the calcium wave as a basic unit in plant cell signaling. Phil. Trans. R. Soc. Lond. B 353, 1463–1473 (1998).

    Google Scholar 

  58. Takahashi, K., Isobe, M., Knight, M. R., Trewavas, A. J. & Muto, S. Hypoosmotic shock induces increases in cytosolic Ca2+ in tobacco suspension culture cells. Plant Physiol. 113, 587–594 ( 1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Alberts, B. et al. Molecular Biology of the Cell (Garland, New York, 1989).

  60. Bose, J. C. Plant Response as Means of Physiological Investigation (Longmans and Co., London, 1906).

  61. Sanders, D. & Bethke, P. in Biochemistry and Molecular Biology of Plants (eds Buchanan, B. B., Gruissem, W. & Jones, R. L.) 110–160 (Am. Soc. of Plant Physiologists, Rockville, Maryland, 2000).

    Google Scholar 

  62. Zhang, H. & Forde, B. G. An Arabidopsis MADS box gene that controls nitrate induced changes in root architecture. Science 279, 407–409 ( 1998).

    CAS  PubMed  Google Scholar 

  63. Trewavas, A. J. Growth substances in context: a decade of sensitivity. Biochem. Soc. Trans 20, 102–108 ( 1991).

    Google Scholar 

  64. Trewavas, A. J. in The Molecular Biology of Plant Development (eds Smith, H. & Grierson, D.) 8–28 (Blackwell Scientific, Oxford, 1982).

    Google Scholar 

  65. Hodgkin, A. L. & Keynes, R. D. Movements of labelled calcium in giant squid axons. J. Physiol. 138, 253–281 (1957).

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Zielinski, R. E. Calmodulin and calmodulin binding proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 697– 725 (1998).

    CAS  PubMed  Google Scholar 

  67. Rodriguez-Concepcion, M., Yalovsky, S., Zik, M., Fromm, H. & Gruissem, W. The prenylation status of a novel plant calmodulin directs plasma membrane or nuclear localisation of the protein. EMBO J. 18, 1996–2007 ( 1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Viner, N., Whitlam, G. & Smith, H. Calcium and phytochrome control of leaf unrolling in dark grown barley seedings. Planta 175, 209–213 (1988).

    CAS  PubMed  Google Scholar 

  69. Jaffe, L. F. Localization in the developing Fucus egg and the general role of localizing currents. Adv. Morphogen. 7, 295– 328 (1968).

    CAS  Google Scholar 

  70. Kropf, D. L. Induction of polarity in fucoid zygotes. Plant Cell 9, 1011–1020 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Hader, D.-P. & Hemmersbacj, R. Graviperception and graviorientation in flagellates. Planta 203, S7– S10 (1997).

    CAS  PubMed  Google Scholar 

  72. Zhang, H., Jennings, A., Barlow, P. W. & Forde, B. G. Dual pathways for regulation of root branching by nitrate. Proc. Natl Acad. Sci. USA 96, 6529–6534 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Addicott, F. T. Abscission (Univ. California Press, London, 1982).

    Google Scholar 

  74. Karban, R. & Baldwin, I. T. Induced Responses to Herbivory (Univ. Chicago Press, Chicago, 1997).

    Google Scholar 

  75. Brown, D. A. & London, E. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14, 111–136 (1998).

    CAS  PubMed  Google Scholar 

  76. Anderson, R. G. W. The caveolae membrane system. Annu. Rev. Biochem. 67 , 199–225 (1998).

    CAS  PubMed  Google Scholar 

  77. Munnik, T. et al. Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate . Plant J. 22, 147–154 (2000).

    CAS  PubMed  Google Scholar 

  78. Stevenson, J. M., Perera, I. Y., Heilmann, I., Persson, S. & Boss, W. F. Inositol signalling and plant growth . Trends Plant Sci. 5, 252– 258 (2000).

    CAS  PubMed  Google Scholar 

  79. Karniol, B. & Chamovitz, D. A. The COP9 signalosome: from the light signalling to general developmental regulation and back. Curr. Opin. Plant Biol. 3, 387–393 (2000).

    CAS  PubMed  Google Scholar 

  80. Blomberg, N., Baraldi, E., Nilges, M. & Saraste, M. The PH superfold: a structural scaffold for multiple functions. Trends Biochem. Sci. 24, 441–445 ( 1999).

    CAS  PubMed  Google Scholar 

  81. Deak, M., Casamayor, A., Currie, R. A., Downes, P. & Alessi, D. R. Characterisation of a plant phosphoinositide-dependent protein kinase-1 homologue which contains a pleckstrin homology domain. FEBS Lett. 451, 220–226 (1999).

    CAS  PubMed  Google Scholar 

  82. Roberts, M. R. Regulatory 14-3-3-protein/protein interactions in plant cells. Curr. Opin. Plant Biol. 3, 400–405 (2000).

    CAS  PubMed  Google Scholar 

  83. Allan, A. C., Fricker, M. D., Ward, J. L., Beale, M. H. & Trewavas, A. J. Two transduction pathways mediate rapid effects of abscisic acid in Commelina guard cells. Plant Cell 6, 1319–1328 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Zuhua, H. et al. Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 288, 2360 –2363 (2000).

    Google Scholar 

  85. Estelle, M. Cytokinin action: two receptors better than one? Curr. Biol. 8, R539–R541 (1998).

    CAS  PubMed  Google Scholar 

  86. Trotochaud, A. E., Jeong, S. & Clark, S. E. CLAVATA3, a multimeric ligand for the CLAVATA1 receptor-kinase . Science 289, 613–617 (2000).

    CAS  PubMed  Google Scholar 

  87. Alonso, J. M., Hirayama, T., Roman, G., Nourizadeh, S. & Ecker, J. R. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284, 2148–2152 (1999).

    CAS  PubMed  Google Scholar 

  88. Beaudoin, N., Serizet, C., Gosti, F. & Giraudat, J. Interactions between abscisic acid and ethylene signaling cascades. Plant Cell 12, 1103–1116 ( 2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Ghassemian, M. et al. Regulation of abscisic acid signalling by the ethylene response pathway in Arabidopsis. Plant Cell 12, 1117–1126 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Sian Ritchie for critical reading of the manuscript at a late stage in its construction. We also gratefully acknowledge the support of the USDA, NSF and NASA (S.G.) and BBSRC and Human Frontier Science Programme Organisation (A.T.).

Author information

Authors and Affiliations

  1. Biology Department, Penn State University, University Park, Pennsylvania, 16802, USA

    Simon Gilroy & Anthony Trewavas

  2. Institute of Cell and Molecular Biology, Kings Buildings, University of Edinburgh, Edinburgh, EH9 3JH, Scotland

    Simon Gilroy & Anthony Trewavas

Authors
  1. Simon Gilroy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anthony Trewavas
    View author publications

    You can also search for this author in PubMed Google Scholar

Related links

Related links

FURTHER INFORMATION

Trewavas lab home page

Gilroy lab home page

ENCYCLOPEDIA OF LIFE SCIENCES

Plant growth factors and receptors

Plant plasma membrane

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gilroy, S., Trewavas, A. Signal processing and transduction in plant cells: the end of the beginning?. Nat Rev Mol Cell Biol 2, 307–314 (2001). https://doi.org/10.1038/35067109

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/35067109

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing