Photoprotective Energy Dissipation in Higher Plants Involves Alteration of the Excited State Energy of the Emitting Chlorophyll(s) in the Light Harvesting Antenna II (LHCII)

Overview

Journal J Biol Chem

Specialty Biochemistry

Date 2009 Jul 2

PMID 19567871

Citations 39

Authors

Matthew P Johnson

Alexander V Ruban

Affiliations

Soon will be listed here.

Abstract

Non-photochemical quenching (NPQ), a mechanism of energy dissipation in higher plants protects photosystem II (PSII) reaction centers from damage by excess light. NPQ involves a reduction in the chlorophyll excited state lifetime in the PSII harvesting antenna (LHCII) by a quencher. Yet, little is known about the effect of the quencher on chlorophyll excited state energy and dynamics. Application of picosecond time-resolved fluorescence spectroscopy demonstrated that NPQ involves a red-shift (60 +/- 5 cm(-1)) and slight enhancement of the vibronic satellite of the main PSII lifetime component present in intact chloroplasts. Whereas this fluorescence red-shift was enhanced by the presence of zeaxanthin, it was not dependent upon it. The red-shifted fluorescence of intact chloroplasts in the NPQ state was accompanied by red-shifted chlorophyll a absorption. Nearly identical absorption and fluorescence changes were observed in isolated LHCII complexes quenched in a low detergent media, suggesting that the mechanism of quenching is the same in both systems. In both cases, the extent of the fluorescence red-shift was shown to correlate with the lifetime of a component. The alteration in the energy of the emitting chlorophyll(s) in intact chloroplasts and isolated LHCII was also accompanied by changes in lutein 1 observed in their 77K fluorescence excitation spectra. We suggest that the characteristic red-shifted fluorescence emission reflects an altered environment of the emitting chlorophyll(s) in LHCII brought about by their closer interaction with lutein 1 in the quenching locus.

Citing Articles

Deciphering the Mechanism of Melatonin-Induced Enhancement of Photosystem II Function in Moderate Drought-Stressed Oregano Plants.

Moustaka J, Sperdouli I, Isgoren S, Sas B, Moustakas M Plants (Basel). 2024; 13(18).

PMID: 39339565 PMC: 11434670. DOI: 10.3390/plants13182590.

Impacts of Drought on Photosynthesis in Major Food Crops and the Related Mechanisms of Plant Responses to Drought.

Qiao M, Hong C, Jiao Y, Hou S, Gao H Plants (Basel). 2024; 13(13).

PMID: 38999648 PMC: 11243883. DOI: 10.3390/plants13131808.

Light quality as a driver of photosynthetic apparatus development.

Kochetova G, Avercheva O, Bassarskaya E, Zhigalova T Biophys Rev. 2022; 14(4):779-803.

PMID: 36124269 PMC: 9481803. DOI: 10.1007/s12551-022-00985-z.

The Structural and Spectral Features of Light-Harvesting Complex II Proteoliposomes Mimic Those of Native Thylakoid Membranes.

Wilson S, Li D, Ruban A J Phys Chem Lett. 2022; 13(24):5683-5691.

PMID: 35709359 PMC: 9237827. DOI: 10.1021/acs.jpclett.2c01019.

Oxidative modification of LHC II associated with photosystem II and PS I-LHC I-LHC II membranes.

Kale R, Seep J, Sallans L, Frankel L, Bricker T Photosynth Res. 2022; 152(3):261-274.

PMID: 35179681 DOI: 10.1007/s11120-022-00902-1.

References

Rees D, Noctor G, Ruban A, Crofts J, Young A, Horton P . pH dependent chlorophyll fluorescence quenching in spinach thylakoids from light treated or dark adapted leaves. Photosynth Res. 2014; 31(1):11-9. DOI: 10.1007/BF00049532. View

Schreiber U . Detection of rapid induction kinetics with a new type of high-frequency modulated chlorophyll fluorometer. Photosynth Res. 2014; 9(1-2):261-72. DOI: 10.1007/BF00029749. View

Vasilev S, Bruce D . Nonphotochemical quenching of excitation energy in photosystem II. A picosecond time-resolved study of the low yield of chlorophyll a fluorescence induced by single-turnover flash in isolated spinach thylakoids. Biochemistry. 1998; 37(31):11046-54. DOI: 10.1021/bi9806854. View

Holt N, Fleming G, Niyogi K . Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry. 2004; 43(26):8281-9. DOI: 10.1021/bi0494020. View

Ruban A, Pascal A, Robert B, Horton P . Activation of zeaxanthin is an obligatory event in the regulation of photosynthetic light harvesting. J Biol Chem. 2001; 277(10):7785-9. DOI: 10.1074/jbc.M110693200. View

Ruban A, Berera R, Ilioaia C, van Stokkum I, Kennis J, Pascal A . Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature. 2007; 450(7169):575-8. DOI: 10.1038/nature06262. View

Croce R, Zucchelli G, Garlaschi F, Jennings R . A thermal broadening study of the antenna chlorophylls in PSI-200, LHCI, and PSI core. Biochemistry. 1998; 37(50):17355-60. DOI: 10.1021/bi9813227. View

Gilmore A, Shinkarev V, Hazlett T, Govindjee G . Quantitative analysis of the effects of intrathylakoid pH and xanthophyll cycle pigments on chlorophyll a fluorescence lifetime distributions and intensity in thylakoids. Biochemistry. 1998; 37(39):13582-93. DOI: 10.1021/bi981384x. View

Robert B, Horton P, Pascal A, Ruban A . Insights into the molecular dynamics of plant light-harvesting proteins in vivo. Trends Plant Sci. 2004; 9(8):385-90. DOI: 10.1016/j.tplants.2004.06.006. View

10.

Croce R, Morosinotto T, Castelletti S, Breton J, Bassi R . The Lhca antenna complexes of higher plants photosystem I. Biochim Biophys Acta. 2002; 1556(1):29-40. DOI: 10.1016/s0005-2728(02)00304-3. View

11.

Ahn T, Avenson T, Ballottari M, Cheng Y, Niyogi K, Bassi R . Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science. 2008; 320(5877):794-7. DOI: 10.1126/science.1154800. View

12.

Ruban A, YOUNG A, Pascal A, Horton P . The Effects of Illumination on the Xanthophyll Composition of the Photosystem II Light-Harvesting Complexes of Spinach Thylakoid Membranes. Plant Physiol. 1994; 104(1):227-234. PMC: 159181. DOI: 10.1104/pp.104.1.227. View

13.

Castelletti S, Morosinotto T, Robert B, Caffarri S, Bassi R, Croce R . Recombinant Lhca2 and Lhca3 subunits of the photosystem I antenna system. Biochemistry. 2003; 42(14):4226-34. DOI: 10.1021/bi027398r. View

14.

Ruban A, YOUNG A, Horton P . Induction of Nonphotochemical Energy Dissipation and Absorbance Changes in Leaves (Evidence for Changes in the State of the Light-Harvesting System of Photosystem II in Vivo). Plant Physiol. 1993; 102(3):741-750. PMC: 158843. DOI: 10.1104/pp.102.3.741. View

15.

Bilger W, Bjorkman O . Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res. 2014; 25(3):173-85. DOI: 10.1007/BF00033159. View

16.

van Grondelle R, Novoderezhkin V . Energy transfer in photosynthesis: experimental insights and quantitative models. Phys Chem Chem Phys. 2006; 8(7):793-807. DOI: 10.1039/b514032c. View

17.

Crouchman S, Ruban A, Horton P . PsbS enhances nonphotochemical fluorescence quenching in the absence of zeaxanthin. FEBS Lett. 2006; 580(8):2053-8. DOI: 10.1016/j.febslet.2006.03.005. View

18.

Veerman J, Vasilev S, Paton G, Ramanauskas J, Bruce D . Photoprotection in the lichen Parmelia sulcata: the origins of desiccation-induced fluorescence quenching. Plant Physiol. 2007; 145(3):997-1005. PMC: 2048789. DOI: 10.1104/pp.107.106872. View

19.

Ilioaia C, Johnson M, Horton P, Ruban A . Induction of efficient energy dissipation in the isolated light-harvesting complex of Photosystem II in the absence of protein aggregation. J Biol Chem. 2008; 283(43):29505-12. PMC: 2662029. DOI: 10.1074/jbc.M802438200. View

20.

van Oort B, van Hoek A, Ruban A, van Amerongen H . Aggregation of light-harvesting complex II leads to formation of efficient excitation energy traps in monomeric and trimeric complexes. FEBS Lett. 2007; 581(18):3528-32. DOI: 10.1016/j.febslet.2007.06.070. View