The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis

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Abstract

Photosynthesis in plants involves two photosystems responsible for converting light energy into redox processes. The photosystems, PSI and PSII, operate largely in series, and therefore their excitation must be balanced in order to optimize photosynthetic performance1. When plants are exposed to illumination favouring either PSII or PSI they can redistribute excitation towards the light-limited photosystem. Long-term changes in illumination lead to changes in photosystem stoichiometry2,3. In contrast, state transition is a dynamic mechanism that enables plants to respond rapidly to changes in illumination. When PSII is favoured (state 2), the redox conditions in the thylakoids change and result in activation of a protein kinase4,5,6. The kinase phosphorylates the main light-harvesting complex (LHCII) and the mobile antenna complex is detached from PSII. It has not been clear if attachment of LHCII to PSI in state 2 is important in state transitions. Here we show that in the absence of a specific PSI subunit, PSI-H, LHCII cannot transfer energy to PSI, and state transitions are impaired.

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Figure 1: Measurements of transitions between state 1 and state 2.
Figure 2: In vitro phosphorylation of LHCII.
Figure 3: Reversible phosphorylation of LHCII in vivo.
Figure 4: Light saturation curve for P700 oxidation in intact leaves.

References

  1. 1

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

  2. 2

    Pfannschmidt, T., Nilsson, A. & Allen, J. F. Photosynthetic control of chloroplast gene expression. Nature 397, 625–628 (1999).

  3. 3

    Walters, R. G. & Horton, P. Acclimation of Arabidopsis thaliana to the light environment: changes in photosynthetic apparatus. Planta 195, 248–256 (1994).

  4. 4

    Allen, J. F. & Nilsson, A. Redox signalling and the structural basis of regulation of photosynthesis by protein phosphorylation. Physiol. Plant. 100, 863–868 (1997).

  5. 5

    Gal, A., Zer, H. & Ohad, I. Redox-controlled thylakoid protein phosphorylation. News and views. Physiol. Plant. 100, 869–885 (1997).

  6. 6

    Zito, F. et al. The Qo site of cytochrome b6 f complexes controls the activation of the LHCII kinase. EMBO J. 18, 2961–2969 (1999).

  7. 7

    Scheller, H. V., Naver, H. & Møller, B. L. Molecular aspects of photosystem I. Physiol. Plant. 100, 842–851 (1997).

  8. 8

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

  9. 9

    Horton, P. Are grana necessary for regulation of light harvesting? Aust. J. Plant Physiol. 26, 659–669 (1999).

  10. 10

    Naver, H., Haldrup, A. & Scheller, H. V. Cosuppression of photosystem I subunit PSI-H in Arabidopsis thaliana. J. Biol. Chem. 274, 10784–10789 (1999).

  11. 11

    Haldrup, A., Naver, H. & Scheller, H. V. The interaction between plastocyanin and photosystem I is inefficient in transgenic Arabidopsis plants lacking the PSI-N subunit of photosystem I. Plant J. 17, 689–698 (1999).

  12. 12

    Jensen, P. E., Gilpin, M., Knoetzel, J. & Scheller, H. V. The PSI-K subunit of photosystem I is involved in the interaction between light harvesting complex I-680 and the photosystem I reaction center core. J. Biol. Chem. 275, 24701–24708 (2000).

  13. 13

    Allen, J. F., Bennett, J., Steinback, K. E. & Arntzen, C. J. Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature 291, 25–29 (1981).

  14. 14

    Bassi, R. Spectral properties and polypeptide composition of the chlorophyll-proteins from thylakoids of granal and agranal chloroplasts of maize (Zea mays L.). Carlsberg Res. Commun. 50, 127–143 (1985).

  15. 15

    Bassi, R., Machold, O. & Simpson, D. Chlorophyll-proteins of two photosystem I preparations from maize. Carlsberg Res. Commun. 50, 145–162 (1985).

  16. 16

    Knoetzel, J. & Simpson, D. Expression and organisation of antenna proteins in the light- and temperature-sensitive barley mutant chlorina-104. Planta 185, 111–123 (1991).

  17. 17

    Boekema, E. J. et al. Green plant photosystem I binds light-harvesting complex I on one side of the complex. Biochemistry (in the press).

  18. 18

    Fromme, P. Structure and function of photosystem I. Curr. Opin. Struct. Biol. 6, 473–484 (1996).

  19. 19

    Jansson, S., Andersen, B. & Scheller, H. V. Nearest-neighbor analysis of higher-plant photosystem I holocomplex. Plant Physiol. 112, 409–420 (1996).

  20. 20

    Samson, G. & Bruce, D. Complementary changes in absorption cross-sections of photosystems I and photosystems II due to phosphorylation and Mg2+-depletion in spinach thylakoids. Biochim. Biophys. Acta 1232, 21–26 (1995).

  21. 21

    Kruse, O., Nixon, P. J., Schmid, G. H. & Mullineaux, C. W. Isolation of state transition mutants of Chlamydomonas reinhardtii by fluorescence video imaging. Photosynth. Res. 61, 43–51 (1999).

  22. 22

    Fleischmann, M. M. et al. Isolation and characterization of photoautotrophic mutants of Chlamydomonas reinhardtii deficient in state transition. J. Biol. Chem. 274, 30987–30994 (1999).

  23. 23

    Kjær, B. & Scheller, H. V. An isolated reaction center complex from the green sulfur bacterium Chlorobium vibrioforme can photoreduce ferredoxin at high rates. Photosynth. Res. 47, 33–39 (1996).

  24. 24

    Steinback, K. E., Bose, S. & Kyle, D. J. Phosphorylation of the light-harvesting chlorophyll-protein regulates excitation energy distribution between photosystem II and photosystem I. Arch. Biochem. Biophys. 216, 356–361 (1982).

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Acknowledgements

We thank M. Jensen for technical assistance, B.L. Møller for discussions, and The Danish National Research Foundation for financial support.

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Correspondence to Henrik Vibe Scheller.

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