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.
Your institute does not have access to this article
Open Access articles citing this article.
Photosynthesis Research Open Access 18 March 2022
Submergence of the filamentous Zygnematophyceae Mougeotia induces differential gene expression patterns associated with core metabolism and photosynthesis
Protoplasma Open Access 22 December 2021
Nature Communications Open Access 16 April 2021
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
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).
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).
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).
Niyogi, K. K. Photoprotection revisited: Genetic and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 333– 359 (1999).
Demmig-Adams, B. Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochim. Biophys. Acta 1020, 1– 24 (1990).
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).
Gilmore, A. M. Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves. Physiol. Plant. 99, 197–209 (1997).
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).
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).
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).
Bassi, R., Pineau, B., Dainese, P. & Marquardt, J. Carotenoid-binding proteins of photosystem II. Eur. J. Biochem. 212, 297–303 (1993).
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).
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).
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).
Horton, P. & Ruban, A. V. Regulation of Photosystem II. Photosynth. Res. 34, 375–385 (1992).
Crofts, A. R. & Yerkes, C. T. A molecular mechanism for q E-quenching. FEBS Lett. 352, 265– 270 (1994).
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).
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).
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).
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).
Jansson, S. A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci. 4, 236–240 (1999).
Funk, C. et al. The PSII-S protein of higher plants: A new type of pigment-binding protein. Biochemistry 34, 11133– 11141 (1995).
Kim, S. et al. Characterization of a spinach psbS cDNA encoding the 22 kDa protein of photosystem II. FEBS Lett. 314, 67–71 (1992).
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).
Ghanotakis, D. F. et al. Comparative structural and catalytic properties of oxygen-evolving photosystem II preparations. Photosynth. Res. 14, 191–199 (1987).
Kim, S., Pichersky, E. & Yocum, C. F. Topological studies of spinach 22 kDa protein of Photosystem II. Biochim. Biophys. Acta 1188, 339–348 (1994).
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).
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).
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).
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).
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).
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).
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).
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).
Demmig-Adams, B. Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant Cell Physiol. 39, 474– 482 (1998).
Ottander, C., Campbell, D. & Öquist, G. Seasonal changes in photosystem II organisation and pigment composition in Pinus sylvestris. Planta 197, 176–183 (1995).
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).
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).
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).
Douglas, S. E. Plastid evolution: Origins, diversity, trends. Curr. Op. Genet. Dev. 8, 655–661 ( 1998).
Niyogi, K. K., Björkman, O. & Grossman, A. R. The roles of specific xanthophylls in photoprotection. Proc. Natl Acad. Sci. USA 94, 14162– 14167 (1997).
Bell, C. J. & Ecker, J. R. Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics 19 , 137–144 (1994).
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).
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).
Clough, S. J. & Bent, A. F. Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998).
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).
Kühlbrandt, W., Wang, D. N. & Fujiyoshi, Y. Atomic model of plant light-harvesting complex by electron crystallography. Nature 367, 614– 621 (1994).
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.
About this article
Cite this article
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
Functional division of f-type and m-type thioredoxins to regulate the Calvin cycle and cyclic electron transport around photosystem I
Journal of Plant Research (2022)
Photosynthesis Research (2022)
Nature Communications (2021)
Nature Communications (2021)
The PsbS protein and low pH are necessary and sufficient to induce quenching in the light-harvesting complex of plants LHCII
Scientific Reports (2021)