A Dual Strategy to Cope with High Light in <i>Chlamydomonas reinhardtii</i>

Allorent, Guillaume; Tokutsu, Ryutaro; Roach, Thomas; Peers, Graham; Cardol, Pierre; Girard‐Bascou, Jacqueline; Seigneurin-Berny, Daphné; Petroutsos, Dimitris; Kuntz, Marcel; Breyton, Cécile; Franck, Fabrice; Wollman, Françis-André; Niyogi, Krishna; Krieger‐Liszkay, Anja; Minagawa, Jun; Finazzi, Guido

doi:10.1105/tpc.112.108274

Cited by 219 publications

(238 citation statements)

References 67 publications

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“…6A). Moreover, LHCSR3 comigrated with both PSII and PSI, in agreement with a recent report (Allorent et al, 2013), while PSBR peaked with PSBA, in accordance with being a PSII complex subunit.…”

Section: Diminishment Of Psbr Expression Destabilizes the Binding Of supporting

confidence: 79%

PHOTOSYSTEM II SUBUNIT R Is Required for Efficient Binding of LIGHT-HARVESTING COMPLEX STRESS-RELATED PROTEIN3 to Photosystem II-Light-Harvesting Supercomplexes in Chlamydomonas reinhardtii

et al. 2015

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Okazaki 444-8585, Japan (R.T., J.M.)In Chlamydomonas reinhardtii, the LIGHT-HARVESTING COMPLEX STRESS-RELATED PROTEIN3 (LHCSR3) protein is crucial for efficient energy-dependent thermal dissipation of excess absorbed light energy and functionally associates with photosystem II-lightharvesting complex II (PSII-LHCII) supercomplexes. Currently, it is unknown how LHCSR3 binds to the PSII-LHCII supercomplex. In this study, we investigated the role of PHOTOSYSTEM II SUBUNIT R (PSBR) an intrinsic membrane-spanning PSII subunit, in the binding of LHCSR3 to PSII-LHCII supercomplexes. Down-regulation of PSBR expression diminished the efficiency of oxygen evolution and the extent of nonphotochemical quenching and had an impact on the stability of the oxygen-evolving complex as well as on PSII-LHCII-LHCSR3 supercomplex formation. Its down-regulation destabilized the PSII-LHCII supercomplex and strongly reduced the binding of LHCSR3 to PSII-LHCII supercomplexes, as revealed by quantitative proteomics. PHOTOSYSTEM II SUBUNIT P deletion, on the contrary, destabilized PHOTOSYSTEM II SUBUNIT Q binding but did not affect PSBR and LHCSR3 association with PSII-LHCII. In summary, these data provide clear evidence that PSBR is required for the stable binding of LHCSR3 to PSII-LHCII supercomplexes and is essential for efficient energy-dependent quenching and the integrity of the PSII-LHCII-LHCSR3 supercomplex under continuous high light.

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Section: Diminishment Of Psbr Expression Destabilizes the Binding Of supporting

confidence: 79%

PHOTOSYSTEM II SUBUNIT R Is Required for Efficient Binding of LIGHT-HARVESTING COMPLEX STRESS-RELATED PROTEIN3 to Photosystem II-Light-Harvesting Supercomplexes in Chlamydomonas reinhardtii

et al. 2015

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“…2A). To ensure that the result is not a result of the absence of a rapid equilibration of the proton concentration between the medium and the cells and between the stroma and the lumen of the thylakoids, we added the protonophore nigericin (27)(28)(29). The presence of nigericin did not affect the results, indicating that the absence of equilibration of the proton concentration is not the reason for the absence of quenching ( Fig.…”

Section: Resultsmentioning

confidence: 99%

LHCSR1 induces a fast and reversible pH-dependent fluorescence quenching in LHCII in Chlamydomonas reinhardtii cells

Dinc¹,

Tian²,

Roy³

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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To avoid photodamage, photosynthetic organisms are able to thermally dissipate the energy absorbed in excess in a process known as nonphotochemical quenching (NPQ). Although NPQ has been studied extensively, the major players and the mechanism of quenching remain debated. This is a result of the difficulty in extracting molecular information from in vivo experiments and the absence of a validation system for in vitro experiments. Here, we have created a minimal cell of the green alga Chlamydomonas reinhardtii that is able to undergo NPQ. We show that LHCII, the main light harvesting complex of algae, cannot switch to a quenched conformation in response to pH changes by itself. Instead, a small amount of the protein LHCSR1 (light-harvesting complex stress related 1) is able to induce a large, fast, and reversible pH-dependent quenching in an LHCII-containing membrane. These results strongly suggest that LHCSR1 acts as pH sensor and that it modulates the excited state lifetimes of a large array of LHCII, also explaining the NPQ observed in the LHCSR3-less mutant. The possible quenching mechanisms are discussed.photosynthesis | light-harvesting | nonphotochemical quenching | green algae | thylakoid membranes P hotosynthetic organisms get their energy from light and have developed a series of mechanisms to respond to the changes in light intensity that occur in their natural environment (1, 2). This is particularly important in high-light conditions, as the energy absorbed in excess can induce photodamage, eventually leading to the death of the organism. Photosynthetic organisms are equipped with many pigment-protein complexes, most of which in plants and green algae are members of the light-harvesting complex (Lhc) multigenic family (3). These complexes maximize light absorption in low light, but can easily become overexcited in high light (4), when a large part of the absorbed light cannot be used for charge separation in the reaction centers of the photosystems. Especially when the changes in light intensity are very fast, and thus protein degradation is not an option, photoprotective mechanisms need to be switched on to avoid the formation of singlet oxygen. The most rapid response to high light intensity is the dissipation of a large part of the absorbed energy as heat in a series of processes known as nonphotochemical quenching (NPQ) (1,5,6).The general idea is that the LHCs can switch between a lightharvesting conformation, characterized by a long excited-state lifetime, and a quenched (Q) conformation that shows a shorter lifetime because of the presence of competing de-excitation processes (7). How this switch is induced and the nature of these de-excitation processes is a matter of debate. It is known that NPQ is triggered by low luminal pH, which is a signal for the overexcitation of the membrane; this activates the quenching processes (5, 8), which involves the proteins PsbS (in plants and mosses) (9, 10) and/or lightharvesting complex stress related (LHCSR) (in green algae, mosses, and diatoms) (10-12)....

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“…These theoretical predictions lead us to hypothesize that the intrinsic dynamic properties of the electron transport chain demand the ability to adjust antenna cross sections, but that this requirement is weaker for high light conditions. Indeed, the phosphorylation of the LHCII antenna, which is largely mediated by the STN7/Stt7 kinase in low light, is inhibited at high light intensities [48,62]. This has been ascribed to the negative regulation of the kinase through the thioredoxin pathway in high light [36,63] or to a conformational change in the PSII antenna [64].…”

Section: Resultsmentioning

confidence: 99%

“…Moreover, our model can bring essential information concerning the physiology of light acclimation by simulating the relative weight of qE and qT under changing light conditions, and therefore allows an exploration of the interplay between the two processes (e.g. [48]) under a wide range of simulated environmental conditions. Eventually, the model opens the possibility of investigating evolutionary issues.…”

Section: Discussionmentioning

confidence: 99%

“…For example, mutation of PGR5/PGRL1 in Arabidopsis, two proteins required for the 'antimycin A-sensitive' CEF pathway [46], also suppresses qE [47], most probably because of the diminished capacity of lumen acidification in the light. In Chlamydomonas, the analysis of npq4 stt7 double mutants indicates that qE and qT are functionally linked during high light stress [48]. The qT component has also been linked to the regulation of CEF by the analysis of stt7 mutants [49,50] and the enrichment of CEF supercomplexes in conditions favouring the association of mobile LHCII antennae with PSI [51,52].…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Short-term acclimation of the photosynthetic electron transfer chain to changing light: a mathematical model

Ebenhöh

Fucile

Finazzi

et al. 2014

Phil. Trans. R. Soc. B

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One contribution of 20 to a Theme Issue 'Changing the light environment: chloroplast signalling and response mechanisms'. Photosynthetic eukaryotes house two photosystems with distinct light absorption spectra. Natural fluctuations in light quality and quantity can lead to unbalanced or excess excitation, compromising photosynthetic efficiency and causing photodamage. Consequently, these organisms have acquired several distinct adaptive mechanisms, collectively referred to as non-photochemical quenching (NPQ) of chlorophyll fluorescence, which modulates the organization and function of the photosynthetic apparatus. The ability to monitor NPQ processes fluorometrically has led to substantial progress in elucidating the underlying molecular mechanisms. However, the relative contribution of distinct NPQ mechanisms to variable light conditions in different photosynthetic eukaryotes remains unclear. Here, we present a mathematical model of the dynamic regulation of eukaryotic photosynthesis using ordinary differential equations. We demonstrate that, for Chlamydomonas, our model recapitulates the basic fluorescence features of short-term light acclimation known as state transitions and discuss how the model can be iteratively refined by comparison with physiological experiments to further our understanding of light acclimation in different species.

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A Dual Strategy to Cope with High Light in Chlamydomonas reinhardtii

Cited by 219 publications

References 67 publications

PHOTOSYSTEM II SUBUNIT R Is Required for Efficient Binding of LIGHT-HARVESTING COMPLEX STRESS-RELATED PROTEIN3 to Photosystem II-Light-Harvesting Supercomplexes in Chlamydomonas reinhardtii

PHOTOSYSTEM II SUBUNIT R Is Required for Efficient Binding of LIGHT-HARVESTING COMPLEX STRESS-RELATED PROTEIN3 to Photosystem II-Light-Harvesting Supercomplexes in Chlamydomonas reinhardtii

LHCSR1 induces a fast and reversible pH-dependent fluorescence quenching in LHCII in Chlamydomonas reinhardtii cells

Short-term acclimation of the photosynthetic electron transfer chain to changing light: a mathematical model

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