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A pigment-binding protein essential for regulation of photosynthetic light harvesting

Abstract

Photosynthetic light harvesting in plants is regulated in response to changes in incident light intensity. Absorption of light that exceeds a plant's capacity for fixation of CO2 results in thermal dissipation of excitation energy in the pigment antenna of photosystem II by a poorly understood mechanism. This regulatory process, termed nonphotochemical quenching, maintains the balance between dissipation and utilization of light energy to minimize generation of oxidizing molecules, thereby protecting the plant against photo-oxidative damage. To identify specific proteins that are involved in nonphotochemical quenching, we have isolated mutants of Arabidopsis thaliana that cannot dissipate excess absorbed light energy. Here we show that the gene encoding PsbS, an intrinsic chlorophyll-binding protein of photosystem II, is necessary for nonphotochemical quenching but not for efficient light harvesting and photosynthesis. These results indicate that PsbS may be the site for nonphotochemical quenching, a finding that has implications for the functional evolution of pigment-binding proteins.

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Figure 1: Nonphotochemical quenching phenotypes.
Figure 2: Light-induced spectral absorbance changes in leaves.
Figure 3: Cloning of NPQ4.
Figure 4: LHC protein levels in wild type and npq4-1.

References

  1. 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).

    CAS  Article  Google Scholar 

  2. Dau, H. Short-term adaptation of plants to changing light intensities and its relation to photosystem II photochemistry and fluorescence emission. J. Photochem. Photobiol. B: Biol. 26, 3–27 ( 1994).

    CAS  Article  Google Scholar 

  3. Horton, P., Ruban, A. V. & Walters, R. G. Regulation of light harvesting in green plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 655– 684 (1996).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  5. Demmig-Adams, B. Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochim. Biophys. Acta 1020, 1– 24 (1990).

    CAS  Article  Google Scholar 

  6. Horton, P. et al. Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll–protein complex. FEBS Lett. 292, 1–4 ( 1991).

    CAS  Article  Google Scholar 

  7. Gilmore, A. M. Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves. Physiol. Plant. 99, 197–209 (1997).

    CAS  Article  Google Scholar 

  8. Niyogi, K. K., Grossman, A. R. & Björkman, O. Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10, 1121–1134 ( 1998).

    CAS  Article  Google Scholar 

  9. Tardy, F. & Havaux, M. Photosynthesis, chlorophyll fluorescence, light-harvesting system and photoinhibition resistance of a zeaxanthin-accumulating mutant of Arabidopsis thaliana. J. Photochem. Photobiol. B: Biol. 34, 87–94 ( 1996).

    CAS  Article  Google Scholar 

  10. Hurry, V., Anderson, J. M., Chow, W. S. & Osmond, C. B. Accumulation of zeaxanthin in abscisic acid-deficient mutants of Arabidopsis does not affect chlorophyll fluorescence quenching or sensitivity to photoinhibition in vivo. Plant Physiol. 113, 639–648 (1997).

    CAS  Article  Google Scholar 

  11. Bassi, R., Pineau, B., Dainese, P. & Marquardt, J. Carotenoid-binding proteins of photosystem II. Eur. J. Biochem. 212, 297–303 (1993).

    CAS  Article  Google Scholar 

  12. Walters, R. G., Ruban, A. V. & Horton, P. Higher plant light-harvesting complexes LHCIIa and LHCIIc are bound by dicyclohexylcarbodiimide during inhibition of energy dissipation. Eur. J. Biochem. 226, 1063– 1069 (1994).

    CAS  Article  Google Scholar 

  13. Jahns, P. & Krause, G. H. Xanthophyll cycle and energy-dependent fluorescence quenching in leaves from pea plants grown under intermittent light. Planta 192, 176– 182 (1994).

    CAS  Article  Google Scholar 

  14. Gilmore, A. M., Hazlett, T. L., Debrunner, P. G. & Govindjee. Photosystem II chlorophyll a fluorescence lifetimes and intensity are independent of the antenna size differences between barley wild-type and chlorina mutants: Photochemical quenching and xanthophyll cycle-dependent nonphotochemical quenching of fluorescence. Photosynth. Res. 48, 171–187 (1996).

    CAS  Article  Google Scholar 

  15. Horton, P. & Ruban, A. V. Regulation of Photosystem II. Photosynth. Res. 34, 375–385 (1992).

    CAS  Article  Google Scholar 

  16. Crofts, A. R. & Yerkes, C. T. A molecular mechanism for q E-quenching. FEBS Lett. 352, 265– 270 (1994).

    CAS  Article  Google Scholar 

  17. Ruban, A. V., Young, A. J. & Horton, P. Induction of nonphotochemical energy dissipation and absorbance changes in leaves. Evidence for changes in state of the light-harvesting system of photosystem II in vivo. Plant Physiol. 102 , 741–750 (1993).

    CAS  Article  Google Scholar 

  18. Bilger, W. & Björkman, O. Relationships among violaxanthin deepoxidation, thylakoid membrane conformation, and nonphotochemical chlorophyll fluorescence quenching in leaves of cotton (Gossypium hirsutum L.). Planta 193, 238–246 (1994).

    CAS  Article  Google Scholar 

  19. Yamamoto, H. Y. & Kamite, L. The effects of dithiothreitol on violaxanthin de-epoxidation and absorbance changes in the 500-nm region. Biochim. Biophys. Acta 267, 538– 543 (1972).

    CAS  Article  Google Scholar 

  20. Espineda, C. E., Linford, A. S., Devine, D. & Brusslan, J. A. The AtCAO gene, encoding chlorophyll a oxygenase, is required for chlorophyll b synthesis in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 96, 10507–10511 (1999).

    ADS  CAS  Article  Google Scholar 

  21. Jansson, S. A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci. 4, 236–240 (1999).

    CAS  Article  Google Scholar 

  22. Funk, C. et al. The PSII-S protein of higher plants: A new type of pigment-binding protein. Biochemistry 34, 11133– 11141 (1995).

    CAS  Article  Google Scholar 

  23. Kim, S. et al. Characterization of a spinach psbS cDNA encoding the 22 kDa protein of photosystem II. FEBS Lett. 314, 67–71 (1992).

    CAS  Article  Google Scholar 

  24. Wedel, N., Klein, R., Ljungberg, U., Andersson, B. & Herrmann, R. G. The single-copy gene psbS codes for a phylogenetically intriguing 22 kDa polypeptide of photosystem II. FEBS Lett. 314, 61–66 (1992).

    CAS  Article  Google Scholar 

  25. Ghanotakis, D. F. et al. Comparative structural and catalytic properties of oxygen-evolving photosystem II preparations. Photosynth. Res. 14, 191–199 (1987).

    CAS  Article  Google Scholar 

  26. Kim, S., Pichersky, E. & Yocum, C. F. Topological studies of spinach 22 kDa protein of Photosystem II. Biochim. Biophys. Acta 1188, 339–348 (1994).

    Article  Google Scholar 

  27. Funk, C., Adamska, I., Green, B. R., Andersson, B. & Renger, G. The nuclear-encoded chlorophyll-binding photosystem II-S protein is stable in the absence of pigments. J. Biol. Chem. 270, 30141–30147 ( 1995).

    CAS  Article  Google Scholar 

  28. Bossmann, B., Knoetzel, J. & Jansson, S. Screening of chlorina mutants of barley ( Hordeum vulgare L.) with antibodies against light-harvesting proteins of PS I and PS II: Absence of specific antenna proteins. Photosynth. Res. 52, 127–136 ( 1997).

    CAS  Article  Google Scholar 

  29. Owens, T. G. in Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field (eds Baker, N. R. & Bowyer, J. R.) 95–109 (BIOS Scientific, Oxford, 1994).

    Google Scholar 

  30. Phillip, D., Ruban, A. V., Horton, P., Asato, A. & Young, A. J. Quenching of chlorophyll fluorescence in the major light-harvesting complex of photosystem II: a systematic study of the effect of carotenoid structure. Proc. Natl Acad. Sci. USA 93, 1492–1497 (1996).

    ADS  CAS  Article  Google Scholar 

  31. Ruban, A. V., Young, A. J. & Horton, P. Dynamic properties of the minor chlorophyll a/ b binding proteins of photosystem II, an in vitro model for photoprotective energy dissipation in the photosynthetic membrane of green plants. Biochemistry 35, 674–678 (1996).

    CAS  Article  Google Scholar 

  32. Ruban, A. V. & Horton, P. The xanthophyll cycle modulates the kinetics of nonphotochemical energy dissipation in isolated light-harvesting complexes, intact chloroplasts, and leaves of spinach. Plant Physiol. 119, 531–542 ( 1999).

    CAS  Article  Google Scholar 

  33. Johnson, G. N., Young, A. J., Scholes, J. D. & Horton, P. The dissipation of excess excitation energy in British plant species. Plant Cell Environ. 16, 673–679 (1993).

    CAS  Article  Google Scholar 

  34. Demmig-Adams, B. & Adams, W. W., III. Capacity for energy dissipation in the pigment bed in leaves with different xanthophyll cycle pools. Aust. J. Plant Physiol. 21 , 575–588 (1994).

    CAS  Google Scholar 

  35. Demmig-Adams, B. Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant Cell Physiol. 39, 474– 482 (1998).

    CAS  Article  Google Scholar 

  36. Ottander, C., Campbell, D. & Öquist, G. Seasonal changes in photosystem II organisation and pigment composition in Pinus sylvestris. Planta 197, 176–183 (1995).

    CAS  Article  Google Scholar 

  37. Green, B. R. & Pichersky, E. Hypothesis for the evolution of three-helix Chl a/b and Chl a/c light-harvesting proteins from two-helix and four-helix ancestors. Photosynth. Res. 39, 149–162 (1994).

    CAS  Article  Google Scholar 

  38. Dolganov, N. A. M., Bhaya, D. & Grossman, A. R. Cyanobacterial protein with similarity to the chlorophyll a/b binding proteins of higher plants: Evolution and regulation. Proc. Natl Acad. Sci. USA 92, 636– 640 (1995).

    ADS  CAS  Article  Google Scholar 

  39. Green, B. R. & Kühlbrandt, W. Sequence conservation of light-harvesting and stress-response proteins in relation to the three-dimensional molecular structure of LHCII. Photosynth. Res. 44, 139–148 (1995).

    CAS  Article  Google Scholar 

  40. Douglas, S. E. Plastid evolution: Origins, diversity, trends. Curr. Op. Genet. Dev. 8, 655–661 ( 1998).

    CAS  Article  Google Scholar 

  41. Niyogi, K. K., Björkman, O. & Grossman, A. R. The roles of specific xanthophylls in photoprotection. Proc. Natl Acad. Sci. USA 94, 14162– 14167 (1997).

    ADS  CAS  Article  Google Scholar 

  42. Bell, C. J. & Ecker, J. R. Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics 19 , 137–144 (1994).

    CAS  Article  Google Scholar 

  43. Konieczny, A. & Ausubel, F. M. A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J. 4, 403–410 ( 1993).

    CAS  Article  Google Scholar 

  44. Hajdukiewicz, P., Svab, Z. & Maliga, P. The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25, 989 –994 (1994).

    CAS  Article  Google Scholar 

  45. Clough, S. J. & Bent, A. F. Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998).

    CAS  Article  Google Scholar 

  46. Jansson, S., Stefánsson, H., Nyström, U., Gustafsson, P. & Albertsson, P.-A. Antenna protein composition of PS I and PS II in thylakoid sub-domains. Biochim. Biophys. Acta 1320, 297–309 ( 1997).

    CAS  Article  Google Scholar 

  47. Kühlbrandt, W., Wang, D. N. & Fujiyoshi, Y. Atomic model of plant light-harvesting complex by electron crystallography. Nature 367, 614– 621 (1994).

    ADS  Article  Google Scholar 

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Acknowledgements

We thank A. K. Tran and V. Canale for technical assistance; J. Brusslan for unpublished data on CH1; T. Shikanai for the npq4-4 allele; C. Funk, J. Knötzel and A. Staehelin for antibodies; R. Malkin for comments on the manuscript; and the Arabidopsis Biological Resource Center for strains and DNA clones. This work was supported by grants from the U.S. Department of Agriculture–National Research Initiative Competitive Grants Program and the Searle Scholars Program/The Chicago Community Trust to K.K.N., a grant from the National Science Foundation to A.G. and O.B., and grants from the Swedish Forestry and Agricultural Research Council and the Foundation for Strategic Research to S.J. When this work was initiated, K.K.N. was supported as a Department of Energy Biosciences Fellow of the Life Sciences Research Foundation.

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Correspondence to Krishna K. Niyogi.

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Li, XP., Björkman, O., Shih, C. et al. A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403, 391–395 (2000). https://doi.org/10.1038/35000131

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