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.

  • Letter
  • Published:

Chloroplast avoidance movement reduces photodamage in plants

Abstract

When plants are exposed to light levels higher than those required for photosynthesis, reactive oxygen species are generated in the chloroplasts and cause photodamage. This can occur even under natural growth conditions. To mitigate photodamage, plants have developed several protective mechanisms1,2,3. One is chloroplast avoidance movement4,5,6, in which chloroplasts move from the cell surface to the side walls of cells under high light conditions, although experimental support is still awaited7,8. Here, using different classes of mutant defective in chloroplast avoidance movement, we show that these mutants are more susceptible to damage in high light than wild-type plants. Damage of the photosynthetic apparatus and subsequent bleaching of leaf colour and necrosis occur faster under high light conditions in the mutants than in wild-type plants. We conclude that chloroplast avoidance movement actually decreases the amount of light absorption by chloroplasts, and might therefore be important to the survival of plants under natural growth conditions.

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

Access options

Buy this article

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

Figure 1: Chloroplast movement in Arabidopsis mutant cells.
Figure 2: Phenotypes of plants exposed to continuous strong light.
Figure 3: Inhibition and recovery kinetics of PSII photochemistry.

Similar content being viewed by others

References

  1. Asada, K. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 601–639 (1999)

    Article  CAS  Google Scholar 

  2. Niyogi, K. K. Photoprotection revisited: genetic and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 333–359 (1999)

    Article  CAS  Google Scholar 

  3. Demmig-Adams, B. & Adams, W. W. III Photoprotection and other responses of plants to high light stress. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43, 599–626 (1992)

    Article  CAS  Google Scholar 

  4. Wada, M. & Kagawa, T. Photomovement (eds Häder, D.-P. & Lebert, M.) 897–924 (Elsevier, Amsterdam, 2001)

    Book  Google Scholar 

  5. Haupt, W. & Scheuerlein, R. Chloroplast movement. Plant Cell Environ. 13, 595–614 (1990)

    Article  Google Scholar 

  6. Zurzycki, J. The Blue Light Syndrome (ed. Senger, H.) 50–68 (Springer, Berlin, 1980)

    Book  Google Scholar 

  7. Brugnoli, E. & Björkman, O. Chloroplast movements in leaves: influence on chlorophyll fluorescence and measurements of light-induced absorbance changes related to ΔpH and zeaxanthin formation. Photosynth. Res. 32, 23–35 (1992)

    Article  CAS  Google Scholar 

  8. Park, Y.-I., Chow, W. S. & Anderson, J. M. Chloroplast movement in the shade plant Tradescantia albiflora helps protect photosystem II against light stress. Plant Physiol. 111, 867–875 (1996)

    Article  CAS  Google Scholar 

  9. Trojan, A. & Gabrys, H. Chloroplast distribution in Arabidopsis thaliana (L.) depends on light conditions during growth. Plant Physiol. 111, 419–425 (1996)

    Article  CAS  Google Scholar 

  10. 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 

  11. 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 

  12. 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 

  13. Kadota, A. & Wada, M. Photoorientation of chloroplasts in protonemal cells of the fern Adiantum as analyzed by use of a video-tracking system. Bot. Mag. Tokyo 105, 265–279 (1992)

    Article  Google Scholar 

  14. Tlalka, M. & Gabrys, H. Influence of calcium on blue-light-induced chloroplast movement in Lemna trisulca L. Planta 189, 491–498 (1993)

    Article  CAS  Google Scholar 

  15. Powles, S. B. Photoinhibition of photosynthesis induced by visible light. Annu. Rev. Plant Physiol. 35, 15–44 (1984)

    Article  CAS  Google Scholar 

  16. Barber, J. & Andersson, B. Too much of a good thing: light can be bad for photosynthesis. Trends Biochem. Sci. 17, 61–66 (1992)

    Article  CAS  Google Scholar 

  17. Björkman, O. & Demmig, B. Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170, 489–504 (1987)

    Article  Google Scholar 

  18. Miyagawa, Y., Tamoi, M. & Shigeoka, S. Evaluation of the defense system in chloroplasts to photooxidative stress caused by paraquat using transgenic tobacco plants expressing catalase from Escherichia coli. Plant Cell Physiol. 41, 311–320 (2000)

    Article  CAS  Google Scholar 

  19. Kinoshita, T. et al. phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414, 656–660 (2001)

    Article  ADS  CAS  Google Scholar 

  20. Escoubas, J. M., Lomas, M., LaRoche, J. & Falkowski, P. G. Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc. Natl Acad. Sci. USA 92, 10237–10241 (1995)

    Article  ADS  CAS  Google Scholar 

  21. Sukenik, A., Wyman, K. D., Bennett, J. & Falkowski, P. G. A novel mechanism for regulating the excitation of photosystem II in a green alga. Nature 327, 704–707 (1987)

    Article  ADS  CAS  Google Scholar 

  22. Haughn, G. W. & Somerville, C. Sulfonylurea-resistant mutants of Arabidopsis thaliana. Mol. Gen. Genet. 204, 430–434 (1986)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank J. Silverthorne (University of California, Santa Cruz) and S. Christensen (Tokyo Metropolitan University) for critical reading of the manuscript, and N. Murata (National Institute for Basic Biology, Japan) for use of the PAM-2000 system. This work was partly supported by BRAIN (Program for Promotion of Basic Research Activities for Innovative Biosciences) and a Grant-in-Aid for Scientific Research from the Ministry of Education, Sports, Science and Technology (MEXT) of Japan to M.W., and by PRESTO, Japan Science and Technology Corporation, Japan, to T.K.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masamitsu Wada.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kasahara, M., Kagawa, T., Oikawa, K. et al. Chloroplast avoidance movement reduces photodamage in plants. Nature 420, 829–832 (2002). https://doi.org/10.1038/nature01213

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01213

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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