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LHCII can substitute for LHCI as an antenna for photosystem I but with reduced light-harvesting capacity

Abstract

Light-harvesting complexes (LHCs) are major constituents of the antenna systems in higher plant photosystems. Four Lhca subunits are tightly bound to the photosystem I (PSI) core complex, forming its outer antenna moiety called LHCI. The Arabidopsis thaliana mutant ΔLhca lacks all Lhca1–4 subunits and compensates for its decreased antenna size by binding LHCII trimers, the main constituent of the photosystem II antenna system, to PSI. In this work we have investigated the effect of LHCI/LHCII substitution by comparing the light harvesting and excitation energy transfer efficiency properties of PSI complexes isolated from ΔLhca mutants and from the wild type, as well as the consequences for plant growth. We show that the excitation energy transfer efficiency was not compromised by the substitution of LHCI with LHCII but a significant reduction in the absorption cross-section was observed. The absence of LHCI subunits in PSI thus significantly limits light harvesting, even on LHCII binding, inducing, as a consequence, a strong reduction in growth.

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Figure 1: Genetic and biochemical characterization of the ΔLhca mutant.
Figure 2: Biochemical characterization of pigment–protein complexes.
Figure 3: Absorption spectra of PSI complexes.
Figure 4: Role of red-shifted absorption forms under canopy conditions.
Figure 5: Time-resolved fluorescence maps of different supercomplexes.
Figure 6: Decay-associated spectra of PSI supercomplexes.
Figure 7: Trapping time and quantum yield of PSI supercomplexes.

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References

  1. Qin, X., Suga, M., Kuang, T. & Shen, J. R. Photosynthesis. Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex. Science 348, 989–995 (2015).

    Article  CAS  Google Scholar 

  2. Mazor, Y., Borovikova, A. & Nelson, N. The structure of plant photosystem I super-complex at 2.8 Å resolution. Elife 4, e07433 (2015).

    Article  Google Scholar 

  3. Croce, R. & van Amerongen, H. Light-harvesting in photosystem I. Photosynth. Res. 116, 153–166 (2013).

    Article  CAS  Google Scholar 

  4. van Amerongen, H. & Croce, R. Light harvesting in photosystem II. Photosynth. Res. 116, 251–263 (2013).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  6. Ballottari, M., Girardon, J., Dall'Osto, L. & Bassi, R. Evolution and functional properties of Photosystem II light harvesting complexes in eukaryotes. Biochim. Biophys. Acta 1817, 143–157 (2012).

    Article  CAS  Google Scholar 

  7. Ballottari, M., Govoni, C., Caffarri, S. & Morosinotto, T. Stoichiometry of LHCI antenna polypeptides and characterization of gap and linker pigments in higher plants photosystem I. Eur. J. Biochem. 271, 4659–4665 (2004).

    Article  CAS  Google Scholar 

  8. Ben-Shem, A., Frolow, F. & Nelson, N. Crystal structure of plant photosystem I. Nature 426, 630–635 (2003).

    Article  CAS  Google Scholar 

  9. Amunts, A., Toporik, H., Borovikova, A. & Nelson, N. Structure determination and improved model of plant photosystem I. J. Biol. Chem. 285, 3478–3486 (2010).

    Article  CAS  Google Scholar 

  10. Ballottari, M., Dall'Osto, L., Morosinotto, T. & Bassi, R. Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation. J. Biol. Chem. 282, 8947–8958 (2007).

    Article  CAS  Google Scholar 

  11. Williams, W. P. & Salamon, Z. Enhancement studies on algae and isolated chloroplasts. Part I.: Variability of photosynthetic enhancement in Chlorella pyrenoidosa. Biochim. Biophys. Acta. 430, 282–299 (1976).

    Article  CAS  Google Scholar 

  12. Hodges, M. & Barber, J. State 1-state 2 transitions in a unicellular green algae: analysis of in vivo chlorophyll fluorescence induction curves in the presence of 3-(3,4-dichlorophenyl)-1, 1-dimethylurea (DCMU). Plant Physiol. 72, 1119–1122 (1983).

    Article  CAS  Google Scholar 

  13. Wollman, F. A. State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J. 20, 3623–3630 (2001).

    Article  CAS  Google Scholar 

  14. Allen, J. F. Botany. State transitions--a question of balance. Science 299, 1530–1532 (2003).

    Article  CAS  Google Scholar 

  15. Grieco, M., Suorsa, M., Jajoo, A., Tikkanen, M. & Aro, E. M. Light-harvesting II antenna trimers connect energetically the entire photosynthetic machinery – including both photosystems II and I. Biochim. Biophys. Acta 1847, 607–619 (2015).

    Article  CAS  Google Scholar 

  16. Goldschmidt-Clermont, M. & Bassi, R. Sharing light between two photosystems: mechanism of state transitions. Curr. Opin. Plant Biol. 25, 71–78 (2015).

    Article  CAS  Google Scholar 

  17. Wientjes, E., Drop, B., Kouřil, R., Boekema, E. J. & Croce, R. During state 1 to state 2 transition in Arabidopsis thaliana, the photosystem II supercomplex gets phosphorylated but does not disassemble. J. Biol. Chem. 288, 32821–6 (2013).

    Article  CAS  Google Scholar 

  18. Bellafiore, S., Barneche, F., Peltier, G. & Rochaix, J. D. State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433, 892–895 (2005).

    Article  CAS  Google Scholar 

  19. Depège, N., Bellafiore, S. & Rochaix, J. D. Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299, 1572–1575 (2003).

    Article  Google Scholar 

  20. Pesaresi, P. et al. Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell 21, 2402–2423 (2009).

    Article  CAS  Google Scholar 

  21. Pesaresi, P. et al. Optimizing photosynthesis under fluctuating light: the role of the Arabidopsis STN7 kinase. Plant Signal. Behav. 5, 21–25 (2010).

    Article  CAS  Google Scholar 

  22. Rochaix, J. D. et al. Protein kinases and phosphatases involved in the acclimation of the photosynthetic apparatus to a changing light environment. Philos. Trans. R. Soc. Lond. B 367, 3466–3474 (2012).

    Article  CAS  Google Scholar 

  23. Pribil, M., Pesaresi, P., Hertle, A., Barbato, R. & Leister, D. Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow. PLoS Biol. 8, e1000288 (2010).

    Article  Google Scholar 

  24. Shapiguzov, A. et al. The PPH1 phosphatase is specifically involved in LHCII dephosphorylation and state transitions in Arabidopsis. Proc. Natl Acad. Sci. USA 107, 4782–4787 (2010).

    Article  CAS  Google Scholar 

  25. Wientjes, E., van Amerongen, H. & Croce, R. LHCII is an antenna of both photosystems after long-term acclimation. Biochim. Biophys. Acta 1827, 420–426 (2013).

    Article  CAS  Google Scholar 

  26. Galka, P. et al. Functional analyses of the plant photosystem I-light-harvesting complex II supercomplex reveal that light-harvesting complex II loosely bound to photosystem II is a very efficient antenna for photosystem I in state II. Plant Cell 24, 2963–2978 (2012).

    Article  CAS  Google Scholar 

  27. Akhtar, P. et al. Excitation energy transfer between light-harvesting complex II and photosystem I in reconstituted membranes. Biochim. Biophys. Acta 1857, 462–472 (2016).

    Article  CAS  Google Scholar 

  28. Wientjes, E., Oostergetel, G. T., Jansson, S., Boekema, E. J. & Croce, R. The role of Lhca complexes in the supramolecular organization of higher plant photosystem I. J. Biol. Chem. 284, 7803–7810 (2009).

    Article  CAS  Google Scholar 

  29. Morosinotto, T., Ballottari, M., Klimmek, F., Jansson, S. & Bassi, R. The association of the antenna system to photosystem I in higher plants. Cooperative interactions stabilize the supramolecular complex and enhance red-shifted spectral forms. J. Biol. Chem. 280, 31050–31058 (2005).

    Article  CAS  Google Scholar 

  30. Malkin, S., Armond, P. A., Mooney, H. A. & Fork, D. C. Photosystem II photosynthetic unit sizes from fluorescence induction in leaves: correlation to photosynthetic capacity. Plant Physiol. 67, 570–579 (1981).

    Article  CAS  Google Scholar 

  31. Järvi, S., Suorsa, M., Paakkarinen, V. & Aro, E. M. Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes. Biochem. J. 439, 207–214 (2011).

    Article  Google Scholar 

  32. Allen, J. F. Plastoquinone redox control of chloroplast thylakoid protein phosphorylation and distribution of excitation energy between photosystems: discovery, background, implications. Photosynth. Res. 73, 139–148 (2002).

    Article  CAS  Google Scholar 

  33. Liu, Z. et al. Crystal structure of spinach major light-harvesting complex at 2.72 A resolution. Nature 428, 287–292 (2004).

    Article  CAS  Google Scholar 

  34. Standfuss, J., Terwisscha van Scheltinga, A. C., Lamborghini, M. & Kühlbrandt, W. Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 A resolution. EMBO J. 24, 919–928 (2005).

    Article  CAS  Google Scholar 

  35. Bassi, R., Croce, R., Cugini, D. & Sandonà, D. Mutational analysis of a higher plant antenna protein provides identification of chromophores bound into multiple sites. Proc. Natl Acad. Sci. USA 96, 10056–10061 (1999).

    Article  CAS  Google Scholar 

  36. Kouril, R. et al. Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana. Biochemistry 44, 10935–10940 (2005).

    Article  CAS  Google Scholar 

  37. Morosinotto, T., Breton, J., Bassi, R. & Croce, R. The nature of a chlorophyll ligand in Lhca proteins determines the far red fluorescence emission typical of photosystem I. J. Biol. Chem. 278, 49223–49229 (2003).

    Article  CAS  Google Scholar 

  38. Rivadossi, A., Zucchelli, G., Garlaschi, F. M. & Jennings, R. C. The importance of PSI chlorophyll red forms in light-harvesting by leaves. Photosynt. Res. 60, 209–215 (1999).

    Article  CAS  Google Scholar 

  39. Laisk, A., Oja, V., Eichelmann, H. & Dall'Osto, L. Action spectra of photosystems II and I and quantum yield of photosynthesis in leaves in state 1. Biochim. Biophys. Acta 1837, 315–325 (2014).

    Article  CAS  Google Scholar 

  40. Ballottari, M. et al. Regulation of photosystem I light harvesting by zeaxanthin. Proc. Natl Acad. Sci. USA 111, E2431–E2438 (2014).

    Article  CAS  Google Scholar 

  41. Gobets, B. et al. Time-resolved fluorescence emission measurements of photosystem I particles of various cyanobacteria: a unified compartmental model. Biophys. J. 81, 407–424 (2001).

    Article  CAS  Google Scholar 

  42. Wientjes, E., van Stokkum, I. H., van Amerongen, H. & Croce, R. The role of the individual Lhcas in photosystem I excitation energy trapping. Biophys. J. 101, 745–754 (2011).

    Article  CAS  Google Scholar 

  43. Slavov, C., Ballottari, M., Morosinotto, T., Bassi, R. & Holzwarth, A. R. Trap-limited charge separation kinetics in higher plant photosystem I complexes. Biophys. J. 94, 3601–3612 (2008).

    Article  CAS  Google Scholar 

  44. Jennings, R. C., Zucchelli, G., Croce, R. & Garlaschi, F. M. The photochemical trapping rate from red spectral states in PSI-LHCI is determined by thermal activation of energy transfer to bulk chlorophylls. Biochim. Biophys. Acta 1557, 91–98 (2003).

    Article  CAS  Google Scholar 

  45. Benson, S. et al. An intact light harvesting complex I antenna system is required for complete state transitions in Arabidopsis. Nat. Plants 1, 15176 (2015).

    Article  CAS  Google Scholar 

  46. Ganeteg, U., Külheim, C., Andersson, J. & Jansson, S. Is each light-harvesting complex protein important for plant fitness? Plant Physiol. 134, 502–509 (2004).

    Article  CAS  Google Scholar 

  47. Ballottari, M., Mozzo, M., Croce, R., Morosinotto, T. & Bassi, R. Occupancy and functional architecture of the pigment binding sites of photosystem II antenna complex Lhcb5. J. Biol. Chem. 284, 8103–8113 (2009).

    Article  CAS  Google Scholar 

  48. Cesaratto, A. et al. Analysis of cadmium-based pigments with time-resolved photoluminescence. Anal. Methods 6, 130–138 (2014).

    Article  CAS  Google Scholar 

  49. van Stokkum, I. H., Larsen, D. S. & van Grondelle, R. Global and target analysis of time-resolved spectra. Biochim. Biophys. Acta 1657, 82–104 (2004).

    Article  CAS  Google Scholar 

  50. Bonente, G., Pippa, S., Castellano, S., Bassi, R. & Ballottari, M. Acclimation of Chlamydomonas reinhardtii to different growth irradiances. J. Biol. Chem. 287, 5833–5847 (2012).

    Article  CAS  Google Scholar 

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Acknowledgements

The work was financed by the Italian Ministry of Agriculture, Food and Forestry (MIPAAF) project HYDROBIO and by the Marie Curie Actions Initial Training Networks ACCLIPHOT (PITN-GA-2012-316427) and S2B (675006–SE2B) to R.B. G.C. acknowledges support from the European Research Council Advanced Grant STRATUS (ERC-2011-AdG No. 291198).

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Contributions

M.Ba., L.D. and R.B. conceived the work and designed the experiments. M.Br. and L.D. performed all the experiments for the isolation of the ΔLhca mutant, its physiological and biochemical characterization and purification of PSI complexes. M.Ba. performed all the experiments for the spectroscopic characterization of PSI complexes. C.D. and G.C. coordinated the time-resolved fluorescence analysis experiments. I.B., M.J.P.A. and C.D. contributed to the time-resolved fluorescence analysis experiments. I.B., M.J.P.A., D.V., G.C., M.Ba. and C.D. analysed the fluorescence decay results by global analysis. All of the authors contributed to writing the manuscript. All of the authors discussed the results and commented on the manuscript.

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Correspondence to Roberto Bassi.

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The authors declare no competing financial interests.

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Supplementary Tables 1–5, Supplementary Figs 1–11 and Supplementary References. (PDF 1849 kb)

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Bressan, M., Dall'Osto, L., Bargigia, I. et al. LHCII can substitute for LHCI as an antenna for photosystem I but with reduced light-harvesting capacity. Nature Plants 2, 16131 (2016). https://doi.org/10.1038/nplants.2016.131

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