<i>Chlamydomonas reinhardtii</i> PsbS Protein Is Functional and Accumulates Rapidly and Transiently under High Light

Tibiletti, Tania; Auroy, Pascaline; Peltier, Gilles; Caffarri, Stefano

doi:10.1104/pp.16.00572

Cited by 114 publications

(100 citation statements)

References 65 publications

(106 reference statements)

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“…S4 H and I). Thus, in agreement with two recent reports (36,37), PSBS is functional in Chlamydomonas and may contribute to qE activity in response to UV-B.…”

Section: Resultssupporting

confidence: 79%

See 1 more Smart Citation

UV-B photoreceptor-mediated protection of the photosynthetic machinery in Chlamydomonas reinhardtii

Allorent

Lefebvre-Legendre

Chappuis

et al. 2016

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

141

138

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Life on earth is dependent on the photosynthetic conversion of light energy into chemical energy. However, absorption of excess sunlight can damage the photosynthetic machinery and limit photosynthetic activity, thereby affecting growth and productivity. Photosynthetic light harvesting can be down-regulated by nonphotochemical quenching (NPQ). A major component of NPQ is qE (energy-dependent nonphotochemical quenching), which allows dissipation of light energy as heat. Photodamage peaks in the UV-B part of the spectrum, but whether and how UV-B induces qE are unknown. Plants are responsive to UV-B via the UVR8 photoreceptor. Here, we report in the green alga Chlamydomonas reinhardtii that UVR8 induces accumulation of specific members of the light-harvesting complex (LHC) superfamily that contribute to qE, in particular LHC Stress-Related 1 (LHCSR1) and Photosystem II Subunit S (PSBS). The capacity for qE is strongly induced by UV-B, although the patterns of qE-related proteins accumulating in response to UV-B or to high light are clearly different. The competence for qE induced by acclimation to UV-B markedly contributes to photoprotection upon subsequent exposure to high light. Our study reveals an anterograde link between photoreceptor-mediated signaling in the nucleocytosolic compartment and the photoprotective regulation of photosynthetic activity in the chloroplast.L ight is essential for photosynthesis, but absorption of excess light energy is detrimental. To avoid photodamage, photosynthetic light harvesting is regulated by nonphotochemical quenching (NPQ), which allows dissipation of harmful excess energy as heat through its qE (energy-dependent nonphotochemical quenching) component (1-6). Specialized members of the light harvesting complex (LHC) protein family, such as Photosystem II Subunit S (PSBS) in higher plants or members of the LHC Stress-Related (LHCSR) family in mosses and algae, are central to qE (7-11). Protonation of key residues in these proteins triggers qE in response to the acidification of the thylakoid lumen, which is coupled to photosynthetic electron transport (7, 9). Furthermore, the deepoxidation of violaxanthin to zeaxanthin, which is also activated by the acidification of the thylakoid lumen, enhances qE (12). In response to high levels of visible light, LHCSR3 protein accumulation is of major importance for qE capacity in Chlamydomonas reinhardtii (11). The induction of LHCSR3 expression under high light is thought to involve retrograde signaling, from the chloroplast to nuclear gene expression (13), and recent data show that the response is also dependent on the phototropin (PHOT) blue light photoreceptor (14).UV-B radiation is intrinsic to sunlight reaching the earth surface and is potentially damaging to living tissues. UV-B stress tolerance is induced through the specific activation of acclimation responses (15)(16)(17)(18)(19)(20). Plants sense UV-B radiation via the homodimeric UV-B photoreceptor UV Resistance Locus 8 (UVR8) (21-23) that is mainly localized in the cytosol ...

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“…S4 H and I). Thus, in agreement with two recent reports (36,37), PSBS is functional in Chlamydomonas and may contribute to qE activity in response to UV-B.…”

Section: Resultssupporting

confidence: 79%

“…At higher light intensity (900 μmol·m −2 ·s −1 ), PSBS expression was detectable (Fig. S1) (36,37), although at lower levels than under UV-B (Fig. S1).…”

Section: Resultsmentioning

confidence: 99%

UV-B photoreceptor-mediated protection of the photosynthetic machinery in Chlamydomonas reinhardtii

Allorent

Lefebvre-Legendre

Chappuis

et al. 2016

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

141

138

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“…Most work on the thermal dissipation of excessive light intensities in green algae has been based on studies in Chlamydomonas reinhardtii . The formation of qE in this chlorophyte appears to depend exclusively on the presence of the proteins PSBS and LHCSR3, but not on the xanthophyll cycle (XC) (Anwaruzzaman et al ., ; Grossman et al ., ; Bonente et al ., ; Correa‐Galvis et al ., ; Tibiletti et al ., ). This has also been shown for several other unicellular green algae (Quaas et al ., ), but our knowledge of the underlying mechanisms is scarce.…”

Section: Introductionmentioning

confidence: 97%

Photoprotection in a monophyletic branch of chlorophyte algae is independent of energy‐dependent quenching (qE)

et al. 2017

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Phototrophic organisms need to ensure high photosynthetic performance whilst suppressing reactive oxygen species (ROS)-induced stress occurring under excess light conditions. The xanthophyll cycle (XC), related to the high-energy quenching component (qE) of the nonphotochemical quenching (NPQ) of excitation energy, is considered to be an obligatory component of photoprotective mechanisms. The pigment composition of at least one representative of each major clade of Ulvophyceae (Chlorophyta) was investigated. We searched for a light-dependent conversion of pigments and investigated the NPQ capacity with regard to the contribution of XC and the qE component when grown under different light conditions. A XC was found to be absent in a monophyletic group of Ulvophyceae, the Bryopsidales, when cultivated under low light, but was triggered in one of the 10 investigated bryopsidalean species, Caulerpa cf. taxifolia, when cultivated under high light. Although Bryopsidales accumulate zeaxanthin (Zea) under high-light (HL) conditions, NPQ formation is independent of a XC and not related to qE. qE- and XC-independent NPQ in the Bryopsidales contradicts the common perception regarding its ubiquitous occurrence in Chloroplastida. Zea accumulation in HL-acclimated Bryopsidales most probably represents a remnant of a functional XC. The existence of a monophyletic algal taxon that lacks qE highlights the need for broad biodiversity studies on photoprotective mechanisms.

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“…In vascular plants, LHCSR is substituted by the PsbS subunit, which, however, does not bind pigments (Li et al, ). PsbS is also present in C. reinhardtii , but it is accumulated only transiently upon high‐light or ultraviolet exposure, and its contribution to NPQ is limited (Allorent et al, ; Correa‐Galvis et al, ; Tibiletti, Auroy, Peltier, & Caffarri, ). Both LHCSR proteins are overexpressed on prolonged high light treatment, but the molecular mechanisms at the base of NPQ and the interaction of LHCSR subunits with PSII supercomplexes are still not clear: LHCSR3 has been suggested to be bound to CP26 and/or to an LHCII trimer (Semchonok et al, ) suggesting a possible key role of monomeric subunits in the energy pathway from PSII to LHCSR subunits during NPQ induction.…”

Section: Introductionmentioning

confidence: 99%

Photosystem II antenna complexes CP26 and CP29 are essential for nonphotochemical quenching in Chlamydomonas reinhardtii

Cazzaniga

Kim

Bellamoli

et al. 2019

Plant Cell & Environment

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Photosystems must balance between light harvesting to fuel the photosynthetic process for CO2 fixation and mitigating the risk of photodamage due to absorption of light energy in excess. Eukaryotic photosynthetic organisms evolved an array of pigment‐binding proteins called light harvesting complexes constituting the external antenna system in the photosystems, where both light harvesting and activation of photoprotective mechanisms occur. In this work, the balancing role of CP29 and CP26 photosystem II antenna subunits was investigated in Chlamydomonas reinhardtii using CRISPR‐Cas9 technology to obtain single and double mutants depleted of monomeric antennas. Absence of CP26 and CP29 impaired both photosynthetic efficiency and photoprotection: Excitation energy transfer from external antenna to reaction centre was reduced, and state transitions were completely impaired. Moreover, differently from higher plants, photosystem II monomeric antenna proteins resulted to be essential for photoprotective thermal dissipation of excitation energy by nonphotochemical quenching.

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Chlamydomonas reinhardtii PsbS Protein Is Functional and Accumulates Rapidly and Transiently under High Light

Cited by 114 publications

References 65 publications

UV-B photoreceptor-mediated protection of the photosynthetic machinery in Chlamydomonas reinhardtii

UV-B photoreceptor-mediated protection of the photosynthetic machinery in Chlamydomonas reinhardtii

Photoprotection in a monophyletic branch of chlorophyte algae is independent of energy‐dependent quenching (qE)

Photosystem II antenna complexes CP26 and CP29 are essential for nonphotochemical quenching in Chlamydomonas reinhardtii

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