Dynamic feedback of the photosystem II reaction centre on photoprotection in plants

Abstract

Photosystem II of higher plants is protected against light damage by thermal dissipation of excess excitation energy, a process that can be monitored through non-photochemical quenching of chlorophyll fluorescence. When the light intensity is lowered, non-photochemical quenching largely disappears on a time scale ranging from tens of seconds to many minutes. With the use of picosecond fluorescence spectroscopy, we demonstrate that one of the underlying mechanisms is only functional when the reaction centre of photosystem II is closed, that is when electron transfer is blocked and the risk of photodamage is high. This is accompanied by the appearance of a long-wavelength fluorescence band. As soon as the reaction centre reopens, this quenching, together with the long-wavelength fluorescence, disappears instantaneously. This allows plants to maintain a high level of photosynthetic efficiency even in dangerous high-light conditions.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Time-resolved fluorescence spectra of the thylakoid membrane.
Fig. 2: Steady-state PSII fluorescence spectra.
Fig. 3: Results of the spectral decomposition.

References

  1. 1.

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

    CAS  Article  Google Scholar 

  2. 2.

    Demmig-Adams, B. & Adams, W. W. The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci. 1, 21–26 (1996).

    Article  Google Scholar 

  3. 3.

    de Bianchi, S., Ballottari, M., Dall’Osto, L. & Bassi, R. Regulation of plant light harvesting by thermal dissipation of excess energy. Biochem. Soc. Trans. 38, 651–660 (2010).

    Article  PubMed  Google Scholar 

  4. 4.

    Ruban, A. V., Johnson, M. P. & Duffy, C. D. The photoprotective molecular switch in the photosystem II antenna. Biochim. Biophys. Acta 1817, 167–181 (2012).

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Li, X. P., Muller-Moule, P., Gilmore, A. M. & Niyogi, K. K. PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc. Natl Acad. Sci. USA 99, 15222–15227 (2002).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. 6.

    Belgio, E. et al. Economic photoprotection in photosystem II that retains a complete light-harvesting system with slow energy traps. Nat. Commun. 5, 4433 (2014).

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Müller, P., Li, X.-P. & Niyogi, K. K. Non-photochemical quenching. A response to excess light energy. Plant Physiol. 125, 1558–1566 (2001).

    Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

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

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Li, X. P. et al. Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J. Biol. Chem. 279, 22866–22874 (2004).

    CAS  Article  PubMed  Google Scholar 

  10. 10.

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

    CAS  Article  Google Scholar 

  11. 11.

    Niyogi, K. K., Grossman, A. R. & Bjorkman, 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  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Belgio, E., Johnson, M. P., Juric, S. & Ruban, A. V. Higher plant photosystem II light-harvesting antenna, not the reaction center, determines the excited-state lifetime-both the maximum and the nonphotochemically quenched. Biophys. J. 102, 2761–2771 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Ruban, A. V. & Horton, P. Spectroscopy of non-photochemical and photochemical quenching of chlorophyll fluorescence in leaves; evidence for a role of the light harvesting complex of photosystem II in the regulation of energy dissipation. Photosynth. Res. 40, 181–190 (1994).

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Horton, P., Johnson, M. P., Perez-Bueno, M. L., Kiss, A. Z. & Ruban, A. V. Photosynthetic acclimation: does the dynamic structure and macro-organisation of photosystem II in higher plant grana membranes regulate light harvesting states? FEBS J. 275, 1069–1079 (2008).

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Niyogi, K. K., Li, X.-P., Rosenberg, V. & Jung, H.-S. Is PsbS the site of non-photochemical quenching in photosynthesis? J. Exp. Bot. 56, 375–382 (2005).

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Avenson, T. J. et al. Zeaxanthin radical cation formation in minor light-harvesting complexes of higher plant antenna. J. Biol. Chem. 283, 3550–3558 (2008).

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    Holt, N. E. et al. Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307, 433–436 (2005).

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Miloslavina, Y. et al. Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching. FEBS Lett. 582, 3625–3631 (2008).

    CAS  Article  PubMed  Google Scholar 

  19. 19.

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

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    Bode, S. et al. On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls. Proc. Natl Acad. Sci. USA 106, 12311–12316 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. 21.

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

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Pascal, A. A. et al. Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nature 436, 134–137 (2005).

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Johnson, M. P. et al. Photoprotective energy dissipation involves the reorganization of photosystem II light-harvesting complexes in the grana membranes of spinach chloroplasts. Plant Cell 23, 1468–1479 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. 24.

    Xu, P., Tian, L., Kloz, M. & Croce, R. Molecular insights into zeaxanthin-dependent quenching in higher plants. Sci. Rep. 5, 13679 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Lambrev, P. H., Miloslavina, Y., Jahns, P. & Holzwarth, A. R. On the relationship between non-photochemical quenching and photoprotection of photosystem II. Biochim. Biophys. Acta 1817, 760–769 (2012).

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Lambrev, P. H., Nilkens, M., Miloslavina, Y., Jahns, P. & Holzwarth, A. R. Kinetic and spectral resolution of multiple nonphotochemical quenching components in Arabidopsis leaves. Plant Physiol. 152, 1611–1624 (2010).

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Kromdijk, J. et al. Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354, 857–861 (2016).

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    Zhu, X. G., Ort, D. R., Whitmarsh, J. & Long, S. P. The slow reversibility of photosystem II thermal energy dissipation on transfer from high to low light may cause large losses in carbon gain by crop canopies: a theoretical analysis. J. Exp. Bot. 55, 1167–1175 (2004).

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Holzwarth, A. R. & Jahns, P. in Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria (eds Barbara Demmig-Adams, Gyozo Garab, William Adams III, & Govindjee) 129–156 (Springer, Dordrecht, the Netherlands, 2014).

  30. 30.

    Sylak-Glassman, E. J., Zaks, J., Amarnath, K., Leuenberger, M. & Fleming, G. R. Characterizing non-photochemical quenching in leaves through fluorescence lifetime snapshots. Photosynth. Res. 127, 69–76 (2016).

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Holzwarth, A. R., Miloslavina, Y., Nilkens, M. & Jahns, P. Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studied by time-resolved fluorescence. Chem. Phys. Lett. 483, 262–267 (2009).

    CAS  Article  Google Scholar 

  32. 32.

    Miloslavina, Y. et al. Ultrafast fluorescence study on the location and mechanism of non-photochemical quenching in diatoms. Biochim. Biophys. Acta Bioenerg. 1787, 1189–1197 (2009).

    CAS  Article  Google Scholar 

  33. 33.

    Wientjes, E., van Amerongen, H. & Croce, R. Quantum yield of charge separation in photosystem II: functional effect of changes in the antenna size upon light acclimation. J. Phys. Chem. B 117, 11200–11208 (2013).

    CAS  Article  PubMed  Google Scholar 

  34. 34.

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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. 35.

    Ruban, A. V., Dekker, J. P., Horton, P. & Grondelle, R. V. Temperature dependence of chlorophyll fluorescence from the light harvesting complex II of higher plants. Photochem. Photobiol. 61, 216–221 (1995).

    CAS  Article  Google Scholar 

  36. 36.

    Magdaong, N. M., Enriquez, M. M., LaFountain, A. M., Rafka, L. & Frank, H. A. Effect of protein aggregation on the spectroscopic properties and excited state kinetics of the LHCII pigment–protein complex from green plants. Photosynth. Res. 118, 259–276 (2013).

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Chmeliov, J. et al. The nature of self-regulation in photosynthetic light-harvesting antenna. Nat. Plants 2, 16045 (2016).

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Natali, A. et al. Light-harvesting complexes (LHCs) cluster spontaneously in membrane environment leading to shortening of their excited state lifetimes. J. Biol. Chem. 291, 16730–16739 (2016).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Lawton, W. H. & Sylvestre, E. A. Self modeling curve resolution. Technometrics 13, 617–633 (1971).

    Article  Google Scholar 

  40. 40.

    Trinkunas, G. et al. Exciton band structure in bacterial peripheral light-harvesting complexes. J. Phys. Chem. B 116, 5192–5198 (2012).

    CAS  Article  PubMed  Google Scholar 

  41. 41.

    Chmeliov, J. et al. Excitons in the LH3 complexes from purple bacteria. J. Phys. Chem. B 117, 11058–11068 (2013).

    CAS  Article  PubMed  Google Scholar 

  42. 42.

    van Oort, B. et al. Picosecond fluorescence of intact and dissolved PSI-LHCI crystals. Biophys. J. 95, 5851–5861 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Tian, L., Xu, P., Chukhutsina, V. U., Holzwarth, A. R. & Croce, R. Zeaxanthin-dependent nonphotochemical quenching does not occur in photosystem I in the higher plant Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 114, 4828–4832 (2017).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Savikhin, S., Xu, W., Chitnis, P. R. & Struve, W. S. Ultrafast primary processes in PS I from Synechocystis sp. PCC 6803: roles of P700 and A(0). Biophys. J. 79, 1573–1586 (2000).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Wientjes, E. & Croce, R. PMS: photosystem I electron donor or fluorescence quencher. Photosynth. Res. 111, 185–191 (2012).

    CAS  Article  PubMed  Google Scholar 

  46. 46.

    Wientjes, E., Philippi, J., Borst, J. W. & van Amerongen, H. Imaging the photosystem I/photosystem II chlorophyll ratio inside the leaf. Biochim. Biophys. Acta 1858, 259–265 (2017).

    CAS  Article  PubMed  Google Scholar 

  47. 47.

    Croce, R., Zucchelli, G., Garlaschi, F. M., Bassi, R. & Jennings, R. C. Excited state equilibration in the photosystem I−light-harvesting I complex: P700 is almost isoenergetic with its antenna. Biochemistry 35, 8572–8579 (1996).

    CAS  Article  PubMed  Google Scholar 

  48. 48.

    Bos, I. et al. Multiple LHCII antennae can transfer energy efficiently to a single photosystem I. Biochim. Biophys. Acta 1858, 371–378 (2017).

    CAS  Article  PubMed  Google Scholar 

  49. 49.

    Chmeliov, J., Trinkunas, G., van Amerongen, H. & Valkunas, L. Light harvesting in a fluctuating antenna. J. Am. Chem. Soc. 136, 8963–8972 (2014).

    CAS  Article  PubMed  Google Scholar 

  50. 50.

    Chmeliov, J., Trinkunas, G., van Amerongen, H. & Valkunas, L. Excitation migration in fluctuating light-harvesting antenna systems. Photosynth. Res. 127, 49–60 (2016).

    CAS  Article  PubMed  Google Scholar 

  51. 51.

    Farooq, S., Chmeliov, J., Trinkunas, G., Valkunas, L. & van Amerongen, H. Is there excitation energy transfer between different layers of stacked photosystem-II-containing thylakoid membranes? J. Phys. Chem. Lett. 7, 1406–1410 (2016).

    CAS  Article  PubMed  Google Scholar 

  52. 52.

    Mller, P. The internal conversion rate of the primary donor in reaction centers of Rhodobacter sphaeroides. Ber. Bunsen. Phys. Chem. 100, 1967–1973 (1996).

    Article  Google Scholar 

  53. 53.

    Vass, I. Role of charge recombination processes in photodamage and photoprotection of the photosystem II complex. Physiol. Plant. 142, 6–16 (2011).

    CAS  Article  PubMed  Google Scholar 

  54. 54.

    Mozzo, M., Dall’Osto, L., Hienerwadel, R., Bassi, R. & Croce, R. Photoprotection in the antenna complexes of photosystem II: role of individual xanthophylls in chlorophyll triplet quenching. J. Biol. Chem. 283, 6184–6192 (2008).

    CAS  Article  PubMed  Google Scholar 

  55. 55.

    Peterman, E. J., Dukker, F. M., van Grondelle, R. & van Amerongen, H. Chlorophyll a and carotenoid triplet states in light-harvesting complex II of higher plants. Biophys. J. 69, 2670–2678 (1995).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Peterman, E. J. G. et al. Xanthophylls in light-harvesting complex II of higher plants: light harvesting and triplet quenching. Biochemistry 36, 12208–12215 (1997).

    CAS  Article  PubMed  Google Scholar 

  57. 57.

    Gruber, J. M., Chmeliov, J., Krger, T. P., Valkunas, L. & van Grondelle, R. Singlet-triplet annihilation in single LHCII complexes. Phys. Chem. Chem. Phys. 17, 19844–19853 (2015).

    Article  PubMed  Google Scholar 

  58. 58.

    Su, X. et al. Structure and assembly mechanism of plant C2S2M2-type PSII-LHCII supercomplex. Science 357, 815–820 (2017).

    CAS  Article  PubMed  Google Scholar 

  59. 59.

    van Oort, B. et al. Ultrafast resonance energy transfer from a site-specifically attached fluorescent chromophore reveals the folding of the N-terminal domain of CP29. Chem. Phys. 357, 113–119 (2009).

    Article  Google Scholar 

  60. 60.

    van Stokkum, I. H. M. et al. (Sub)-picosecond spectral evolution of fluorescence in photoactive proteins studied with a synchroscan streak camera system. Photochem. Photobiol. 82, 380–388 (2006).

    Article  PubMed  Google Scholar 

  61. 61.

    Barzda, V. et al. Singlet-singlet annihilation kinetics in aggregates and trimers of LHCII. Biophys. J. 80, 2409–2421 (2001).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  62. 62.

    Krüger, T. P. J., Novoderezhkin, V. I., Ilioaia, C. & van Grondelle, R. Fluorescence spectral dynamics of single LHCII trimers. Biophys. J. 98, 3093–3101 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  63. 63.

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

    Article  PubMed  Google Scholar 

  64. 64.

    Berry, M. W., Murray, B., Langville, A. N., Pauca, V. P. & Robert, J. P. Algorithms and applications for approximate nonnegative matrix factorization. Comput. Stat. Data Anal. 52, 155–173 (2006).

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank J. Philippi for the design and construction of the moving cuvette and actinic lighting system and R. Croce for critically reading the manuscript. H.v.A. and S.F. received financial support from the Foundation for Fundamental Research on Matter (FOM), which is part of the Netherlands Organization for Scientific Research (NWO). E.W. acknowledges funding from a Marie Sklodowska-Curie fellowship (655542; E.W.) and a Veni grant (016.161.038; E.W.) from the NWO, Earth and Life Sciences (ALW). J.C. and L.V. were supported by the Research Council of Lithuania (LMT grant no. MIP-080/2015).

Author information

Affiliations

Authors

Contributions

H.v.A. devised the project. S.F. (with assistance of R.K., E.W. and A.B.) performed the measurements. J.C., H.v.A., S.F. and E.W. analysed the data (with significant input from L.V., G.T. and R.K.). H.v.A., S.F. and J.C. wrote the manuscript. All authors discussed the results and commented on the manuscript.

Corresponding author

Correspondence to Herbert van Amerongen.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Table 1 and 2, and Supplementary Figures 1–4

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Farooq, S., Chmeliov, J., Wientjes, E. et al. Dynamic feedback of the photosystem II reaction centre on photoprotection in plants. Nature Plants 4, 225–231 (2018). https://doi.org/10.1038/s41477-018-0127-8

Download citation

Further reading

Search

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing