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An ancient light-harvesting protein is critical for the regulation of algal photosynthesis

Nature volume 462, pages 518–521 (2009)Cite this article

Abstract

Light is necessary for photosynthesis, but its absorption by pigment molecules such as chlorophyll can cause severe oxidative damage and result in cell death. The excess absorption of light energy by photosynthetic pigments has led to the evolution of protective mechanisms that operate on the timescale of seconds to minutes and involve feedback-regulated de-excitation of chlorophyll molecules in photosystem II (qE). Despite the significant contribution of eukaryotic algae to global primary production1, little is known about their qE mechanism, in contrast to that in flowering plants2,3. Here we show that a qE-deficient mutant of the unicellular green alga Chlamydomonas reinhardtii, npq4, lacks two of the three genes encoding LHCSR (formerly called LI818). This protein is an ancient member of the light-harvesting complex superfamily, and orthologues are found throughout photosynthetic eukaryote taxa4, except in red algae and vascular plants. The qE capacity of Chlamydomonas is dependent on environmental conditions and is inducible by growth under high light conditions. We show that the fitness of the npq4 mutant in a shifting light environment is reduced compared to wild-type cells, demonstrating that LHCSR is required for survival in a dynamic light environment. Thus, these data indicate that plants and algae use different proteins to dissipate harmful excess light energy and protect the photosynthetic apparatus from damage.

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Figure 1: NPQ of chlorophyll fluorescence in Chlamydomonas reinhardtii cells.
Figure 2: Survival of wild type (WT) and npq4 following a shift from a low-light-acclimated state to excess light for four hours.
Figure 3: Analysis of the LHCSR genes, LHCSR mRNA levels, and LHCSR protein accumulation in Chlamydomonas WT and npq4 mutant.

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References

  1. Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240 (1998)

    Article  ADS  CAS  Google Scholar 

  2. Ruban, A. V. et al. Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450, 575–578 (2007)

    Article  ADS  CAS  Google Scholar 

  3. Ahn, T. K. et al. Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320, 794–797 (2008)

    Article  ADS  CAS  Google Scholar 

  4. Koziol, A. G. et al. Tracing the evolution of the light-harvesting antennae in chlorophyll a/b-containing organisms. Plant Physiol. 143, 1802–1816 (2007)

    Article  CAS  Google Scholar 

  5. Schenck, H. On the focusing of sunlight by ocean waves. J. Opt. Soc. Am. 47, 653–657 (1957)

    Article  ADS  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. Külheim, C., Ågren, J. & Jansson, S. Rapid regulation of light harvesting and plant fitness in the field. Science 297, 91–93 (2002)

    Article  ADS  Google Scholar 

  8. Falkowski, P. G. et al. The evolution of modern eukaryotic phytoplankton. Science 305, 354–360 (2004)

    Article  ADS  CAS  Google Scholar 

  9. Niyogi, K. K., Björkman, O. & Grossman, A. R. Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell 9, 1369–1380 (1997)

    Article  CAS  Google Scholar 

  10. Elrad, D., Niyogi, K. K. & Grossman, A. R. A major light-harvesting polypeptide of photosystem II functions in thermal dissipation. Plant Cell 14, 1801–1816 (2002)

    Article  CAS  Google Scholar 

  11. Merchant, S. S. et al. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318, 245–251 (2007)

    Article  ADS  CAS  Google Scholar 

  12. Golan, T., Müller-Moulé, P. & Niyogi, K. K. Photoprotection mutants of Arabidopsis thaliana acclimate to high light by increasing photosynthesis and specific antioxidants. Plant Cell Environ. 29, 879–887 (2006)

    Article  CAS  Google Scholar 

  13. Li, X.-P. et al. A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403, 391–395 (2000)

    Article  ADS  CAS  Google Scholar 

  14. Gagné, G. & Guertin, M. The early genetic response to light in the green unicellular alga Chlamydomonas eugametos grown under light dark cycles involves genes that represent direct responses to light and photosynthesis. Plant Mol. Biol. 18, 429–445 (1992)

    Article  Google Scholar 

  15. Savard, F., Richard, C. & Guertin, M. The Chlamydomonas reinhardtii LI818 gene represents a distant relative of the cabI/II genes that is regulated during the cell cycle and in response to illumination. Plant Mol. Biol. 32, 461–473 (1996)

    Article  CAS  Google Scholar 

  16. Miura, K. et al. Expression profiling-based identification of CO2-responsive genes regulated by CCM1 controlling a carbon-concentrating mechanism in Chlamydomonas reinhardtii . Plant Physiol. 135, 1595–1607 (2004)

    Article  CAS  Google Scholar 

  17. Zhang, Z. et al. Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot. Cell 3, 1331–1348 (2004)

    Article  CAS  Google Scholar 

  18. Naumann, B. et al. Comparative quantitative proteomics to investigate the remodeling of bioenergetic pathways under iron deficiency in Chlamydomonas reinhardtii . Proteomics 7, 3964–3979 (2007)

    Article  CAS  Google Scholar 

  19. Ledford, H. K. et al. Comparative profiling of lipid-soluble antioxidants and transcripts reveals two phases of photo-oxidative stress in a xanthophyll-deficient mutant of Chlamydomonas reinhardtii . Mol. Genet. Genom. 272, 470–479 (2004)

    Article  CAS  Google Scholar 

  20. Yamano, T., Miura, K. & Fukuzawa, H. Expression analysis of genes associated with the induction of the carbon-concentrating mechanism in Chlamydomonas reinhardtii . Plant Physiol. 147, 340–354 (2008)

    Article  CAS  Google Scholar 

  21. Turkina, M. V. et al. Environmentally modulated phosphoproteome of photosynthetic membranes in the green alga Chlamydomonas reinhardtii . Mol. Cell. Proteom. 5, 1412–1425 (2006)

    Article  CAS  Google Scholar 

  22. Allmer, J., Naumann, B., Markert, C., Zhang, M. & Hippler, M. Mass spectrometric genomic data mining: novel insights into bioenergetic pathways in Chlamydomonas reinhardtii . Proteomics 6, 6207–6220 (2006)

    Article  CAS  Google Scholar 

  23. Bonente, G. et al. The occurrence of the psbS gene product in Chlamydomonas reinhardtii and in other photosynthetic organisms and its correlation with energy quenching. Photochem. Photobiol. 84, 1359–1370 (2008)

    Article  CAS  Google Scholar 

  24. Alboresi, A., Caffarri, S., Nogue, F., Bassi, R. & Morosinotto, T. In silico and biochemical analysis of Physcomitrella patens photosynthetic antenna: identification of subunits which evolved upon land adaptation. PLoS One 3 10.1371/journal.pone.0002033 (2008)

  25. Rensing, S. A. et al. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319, 64–69 (2008)

    Article  ADS  CAS  Google Scholar 

  26. Richard, C., Ouellet, H. & Guertin, M. Characterization of the LI818 polypeptide from the green unicellular alga Chlamydomonas reinhardtii . Plant Mol. Biol. 42, 303–316 (2000)

    Article  CAS  Google Scholar 

  27. Wilson, A. et al. A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18, 992–1007 (2006)

    Article  CAS  Google Scholar 

  28. Casper-Lindley, C. & Björkman, O. Fluorescence quenching in four unicellular algae with different light-harvesting and xanthophyll-cycle pigments. Photosynth. Res. 56, 277–289 (1998)

    Article  CAS  Google Scholar 

  29. Moustafa, A. et al. Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324, 1724–1726 (2009)

    Article  ADS  CAS  Google Scholar 

  30. Baroli, I., Do, A. D., Yamane, T. & Niyogi, K. K. Zeaxanthin accumulation in the absence of a functional xanthophyll cycle protects Chlamydomonas reinhardtii from photooxidative stress. Plant Cell 15, 992–1008 (2003)

    Article  CAS  Google Scholar 

  31. Baroli, I., Do, A. D., Yamane, T. & Niyogi, K. K. Zeaxanthin accumulation in the absence of a functional xanthophyll cycle protects Chlamydomonas reinhardtii from photooxidative stress. Plant Cell 15, 992–1008 (2003)

    Article  CAS  Google Scholar 

  32. Earley, K. et al. Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45, 616–629 (2006)

    Article  CAS  Google Scholar 

  33. Niyogi, K. K., Björkman, O. & Grossman, A. R. Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell 9, 1369–1380 (1997)

    Article  CAS  Google Scholar 

  34. Porra, R. J., Thompson, W. A. & Kriedemann, P. E. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975, 384–394 (1989)

    Article  CAS  Google Scholar 

  35. Richard, C., Ouellet, H. & Guertin, M. Characterization of the LI818 polypeptide from the green unicellular alga Chlamydomonas reinhardtii . Plant Mol. Biol. 42, 303–316 (2000)

    Article  CAS  Google Scholar 

  36. Naumann, B. et al. Comparative quantitative proteomics to investigate the remodeling of bioenergetic pathways under iron deficiency in Chlamydomonas reinhardtii . Proteomics 7, 3964–3979 (2007)

    Article  CAS  Google Scholar 

  37. Naumann, B., Stauber, E. J., Busch, A., Sommer, F. & Hippler, M. N-terminal processing of Lhca3 is a key step in remodeling of the photosystem-I light-harvesting complex under iron deficiency in Chlamydomonas reinhardtii . J. Biol. Chem. 280, 20431–20441 (2005)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank M. Guertin for providing the anti-LHCSR (LI818) antibody. This work was supported by grants from the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, Office of Science, US Department of Energy (K.K.N.), the Deutsche Forschungsgemeinschaft (M.H.), and the National Science Foundation (A.R.G.).

Author Contributions G.P., T.B.T., E.O., A.B., D.E. and K.K.N. performed research; G.P., A.R.G., M.H., and K.K.N. designed research; G.P., M.H. and K.K.N. analysed data and wrote the paper; all authors discussed the results and commented on the manuscript.

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Author notes

  1. Graham Peers

    Present address: Present address: Synthetic Genomics, Inc., 11149 North Torrey Pines Road, Suite 100, La Jolla, California 92037, USA.,

  2. Thuy B. Truong and Elisabeth Ostendorf: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Plant and Microbial Biology, University of California, Berkeley, California 94720-3102, USA,

    Graham Peers, Thuy B. Truong & Krishna K. Niyogi

  2. Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA,

    Thuy B. Truong & Krishna K. Niyogi

  3. Institute of Plant Biochemistry and Biotechnology, University of Münster, 48143 Münster, Germany

    Elisabeth Ostendorf, Andreas Busch & Michael Hippler

  4. Department of Plant Biology, Carnegie Institution, Stanford, California 94305, USA,

    Dafna Elrad & Arthur R. Grossman

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Correspondence to Michael Hippler or Krishna K. Niyogi.

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Peers, G., Truong, T., Ostendorf, E. et al. An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462, 518–521 (2009). https://doi.org/10.1038/nature08587

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