phot1 and phot2 mediate blue light regulation of stomatal opening (original) (raw)

Nature volume 414, pages 656–660 (2001) Cite this article

Abstract

The stomatal pores of higher plants allow for gaseous exchange into and out of leaves. Situated in the epidermis, they are surrounded by a pair of guard cells which control their opening in response to many environmental stimuli, including blue light1,2. Opening of the pores is mediated by K+ accumulation in guard cells through a K+ channel and driven by an inside-negative electrical potential3. Blue light causes phosphorylation and activation of the plasma membrane H+-ATPase that creates this potential1,2,4,5,6. Thus far, no blue light receptor mediating stomatal opening has been identified7, although the carotenoid, zeaxanthin, has been proposed2,8. Arabidopsis mutants deficient in specific blue-light-mediated responses have identified7,9,10,11,12,13,14 four blue light receptors, cryptochrome 1 (cry1), cryptochrome 2 (cry2), phot1 and phot2. Here we show that in a double mutant of phot1 and phot2 stomata do not respond to blue light although single mutants are phenotypically normal. These results demonstrate that phot1 and phot2 act redundantly as blue light receptors mediating stomatal opening.

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

Access options

Subscribe to this journal

Receive 52 print issues and online access

$199.00 per year

only $3.83 per issue

Buy this article

USD 39.95

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

Additional access options:

Figure 1: Analyses of Arabidopsis blue-light photoreceptor mutants.

The alternative text for this image may have been generated using AI.

Figure 2: Stomatal opening under blue light.

The alternative text for this image may have been generated using AI.

Figure 3: Amount of plasma membrane H+-ATPase, fusicoccin-induced stomatal opening, and blue light-dependent H+ extrusion in Arabidopsis blue light photoreceptor mutants.

The alternative text for this image may have been generated using AI.

Similar content being viewed by others

References

  1. Assmann, S. M. Signal transduction in guard cells. Annu. Rev. Cell Biol. 9, 345–375 (1993).
    Article CAS Google Scholar
  2. Schroeder, J. I., Allen, G. J., Hugouvieux, V., Kwak, J. M. & Waner, D. Guard cell signal transduction. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 627–658 (2001).
    Article CAS Google Scholar
  3. Schroeder, J. I., Raschke, K. & Neher, E. Voltage dependence of K+ channels in guard cell protoplasts. Proc. Natl Acad. Sci. USA 84, 4108–4112 (1987).
    Article ADS CAS Google Scholar
  4. Assmann, S. M., Simoncini, L. & Schroeder, J. I. Blue light activates electrogenic ion pumping in guard cell protoplasts of Vicia faba L. Nature 318, 285–287 (1985).
    Article ADS CAS Google Scholar
  5. Shimazaki, K., Iino, M. & Zeiger, E. Blue light-dependent proton extrusion by guard-cell protoplasts of Vicia faba. Nature 319, 324–326 (1986).
    Article ADS CAS Google Scholar
  6. Kinoshita, T. & Shimazaki, K. Blue light activates the plasma membrane H+-ATPase by phosphorylation of the C-terminus in stomatal guard cells. EMBO J. 18, 5548–5558 (1999).
    Article CAS Google Scholar
  7. Briggs, W. R. & Huala, E. Blue-light photoreceptors in higher plants. Annu. Rev. Cell Dev. 15, 33–62 (1999).
    Article CAS Google Scholar
  8. Zeiger, E. & Zhu, J. Role of zeaxanthin in blue light photoreception and modulation of light-CO2 interactions in guard cells. J. Exp. Bot. 49, 433–442 (1998).
    Article Google Scholar
  9. Ahmad, M. & Cashmore, A. R. HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature 366, 162–166 (1993).
    Article ADS CAS Google Scholar
  10. Briggs, W. R. et al. The phototropin family of photoreceptors. Plant Cell 13, 993–997 (2001).
    Article CAS Google Scholar
  11. Huala, E. et al. Arabidopsis NPH1: A protein kinase with a putative redox-sensing domain. Science 278, 2121–2123 (1997).
    Article ADS Google Scholar
  12. Sakai, T. et al. Arabidopsis nph1 and npl1: Blue light receptors that mediate both phototropism and chloroplast relocation. Proc. Natl Acad. Sci. USA 98, 6969–6974 (2001).
    Article ADS CAS Google Scholar
  13. Kagawa, T. et al. Arabidopsis NPL1: A phototropin homolog controlling the chloroplast high-light avoidance response. Science 291, 2138–2141 (2001).
    Article ADS CAS Google Scholar
  14. Jarillo, J. A. et al. Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature 410, 952–954 (2001).
    Article ADS CAS Google Scholar
  15. Baum, G., Long, J. C., Jenkins, G. I. & Trewavas, A. J. Stimulation of the blue light phototropic receptor NPH1 causes a transient increase in cytosolic Ca2+. Proc. Natl Acad. Sci. USA 96, 13554–13559 (1999).
    Article ADS CAS Google Scholar
  16. Shimazaki, K., Goh, C. H. & Kinoshita, T. Involvement of intracellular Ca2+ in blue light-dependent proton pumping in guard cell protoplasts from Vicia faba. Physiol. Plant. 105, 554–561 (1999).
    Article CAS Google Scholar
  17. Christie, J. M., Salomon, M., 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 (1999).
    Article ADS CAS Google Scholar
  18. Karlsson, P. E. Blue light regulation of stomata in wheat seedlings. II. Action spectrum and search for action dichroism. Physiol. Plant. 66, 207–210 (1986).
    Article Google Scholar
  19. Eisinger, W., Swartz, T. E., Bogomolni, R. A. & Taiz, L. The ultraviolet action spectrum for stomatal opening in broad bean. Plant Physiol. 122, 99–105 (2000).
    Article CAS Google Scholar
  20. Lasceve, G. et al. Arabidopsis contains at least four independent blue-light-activated signal transduction pathways. Plant Physiol. 120, 605–614 (1999).
    Article CAS Google Scholar
  21. Niyogi, K. K., Grossman, A. R. & Bjorkman, O. Arabidopsis mutants define a central role for the xanthrophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10, 1121–1134 (1998).
    Article CAS Google Scholar
  22. Schwartz, A. & Zeiger, E. Metabolic energy for stomatal opening. Role of photophosphorylation and oxidative phosphorylation. Planta 161, 129–136 (1984).
    Article CAS Google Scholar
  23. Eckert, M. & Kaldenhoff, R. Light-induced stomatal movement of selected Arabidopsis thaliana mutants. J. Exp. Bot. 51, 1435–1442 (2000).
    Article CAS Google Scholar
  24. Ballio, A. et al. Fusicoccin: A new wilting toxin produced by Fusicoccum amygdali Del. Nature 203, 297 (1964).
    Article ADS CAS Google Scholar
  25. Willmer, C. & Fricker, M. D. Stomata 2nd edn (Chapman & Hall, London, 1996).
    Book Google Scholar
  26. Iino, M., Ogawa, T. & Zeiger, E. Kinetic properties of blue light response of stomata. Proc. Natl Acad. Sci. USA 82, 8019–8023 (1985).
    Article ADS CAS Google Scholar
  27. Chomczynski, P. & Sacchi, N. Single step-method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156–159 (1987).
    Article CAS Google Scholar
  28. Merlot, S., Gosti, F., Guerrier, D., Vavasseur, A. & Giraudat, J. The ABI1 and ABI2 protein phosphatase 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J. 25, 295–303 (2001).
    Article CAS Google Scholar
  29. Kondo, N. & Sugahara, K. Changes in transpiration rate of SO2-resistant and -sensitive plants with SO2 fumigation and the participation of abscisic acid. Plant Cell Physiol. 19, 365–373 (1978).
    Article CAS Google Scholar
  30. Bradford, M. M. A rapid sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976).
    Article CAS Google Scholar

Download references

Acknowledgements

We thank J. Silverthorne for a critical reading of the manuscript. This work was supported in part by a grant from the research fellowships of the Japan Society for the Promotion of Science for Young Scientists to T. Kinoshita and N.S., a Grant-in-Aid for Scientific Research on Priority Areas from the Ministry of Education, Science, Sports and Culture of Japan to K.S. and M.W., and Kyushu University Interdisciplinary Programmes in Education and Projects in Research Development to K.S. This work was also supported partly by the PROBRAIN and NOVARTIS to M.W. and partly by a grant from PRESTO, Japan Science and Technology Corporation (T. Kagawa).

Author information

Author notes

  1. Toshinori Kinoshita, Michio Doi and Takatoshi Kagawa: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Biology, Faculty of Science, Kyushu University, Ropponmatsu, 810-8560, Fukuoka, Japan
    Toshinori Kinoshita, Michio Doi & Ken-ichiro Shimazaki
  2. Division of Biological Regulation and Photobiology, National Institute for Basic Biology, Okazaki, 444-8585, Japan
    Noriyuki Suetsugu, Takatoshi Kagawa & Masamitsu Wada
  3. Department of Biological Sciences, Graduate School of Science, Tokyo Metropolitan University, Tokyo, 192-0397, Japan
    Noriyuki Suetsugu & Masamitsu Wada
  4. Unit Process and Combined Circuit, PRESTO, Japan Science and Technology Corporation, 1-8, Honcho 4-chome, Kawaguchi, 332-0012, Saitama, Japan
    Takatoshi Kagawa

Authors

  1. Toshinori Kinoshita
  2. Michio Doi
  3. Noriyuki Suetsugu
  4. Takatoshi Kagawa
  5. Masamitsu Wada
  6. Ken-ichiro Shimazaki

Corresponding author

Correspondence toKen-ichiro Shimazaki.

Rights and permissions

About this article

Cite this article

Kinoshita, T., Doi, M., Suetsugu, N. et al. phot1 and phot2 mediate blue light regulation of stomatal opening.Nature 414, 656–660 (2001). https://doi.org/10.1038/414656a

Download citation

This article is cited by