Regulation of Light Harvesting in the Green Alga <i>Chlamydomonas reinhardtii</i>: The C-Terminus of LHCSR Is the Knob of a Dimmer Switch

Liguori, Nicoletta; Roy, Laura M.; Opacic, Milena; Durand, Grégory; Croce, Roberta

doi:10.1021/ja4107463

Cited by 124 publications

(167 citation statements)

References 32 publications

Supporting

Mentioning

147

Contrasting

Unclassified

Order By: Relevance

“…We have recently shown that this is not the case for isolated LHCII in the absence of aggregation from both plants and C. reinhardtii (18,26). Our results here show that LHCII in the membrane is not quenched in response to pH changes, and that the quenching can also not be induced by the interaction of zeaxanthin with LHCBM1.…”

Section: Discussionmentioning

confidence: 40%

“…The data clearly show that the membrane only acquires the ability to switch states in response to pH when LHCSR1 is present. Very little information is available about LHCSR1 of C. reinhardti;, however, this protein has a very high homology with LHCSR3 that was previously shown to assume a Q conformation at low pH by in vitro experiments, with a reduction in its fluorescence yield of ∼30% (17,18). LHCRS1 also retains the C-terminal tail that was shown to be essential in LHCSR3 for sensing the pH (18).…”

Section: Discussionmentioning

confidence: 99%

“…LHCSR3 is considered the protein mainly responsible for NPQ in C. reinhardtii, as a mutant lacking this protein shows a strong reduction of NPQ (11). LHCSR3 is a pigment-binding protein able to switch in vitro to a Q conformation at low pH (17) because of the protonation of its C terminus (18). No information is available regarding LHCSR1, which has not been purified or reconstituted in vitro.…”

mentioning

confidence: 99%

See 2 more Smart Citations

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.

Self Cite

View full text Add to dashboard Cite

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)....

show abstract

Section: Discussionmentioning

confidence: 40%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

See 1 more Smart Citation

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.

Self Cite

View full text Add to dashboard Cite

show abstract

“…So far, three proteins have been shown to have a major role in detecting and transducing the low pH signal: the low pH activated violaxanthin de-epoxidase enzyme (VDE; Arnoux et al, 2009) that catalyses the conversion of the xanthophyll violaxanthin into zeaxanthin, a pigment involved in NPQ and other photoprotection mechanisms (Demmig-Adams, 1990;Havaux and Niyogi, 1999); the pigment-binding LhcSR proteins that belong to the Lhc family and are very likely the active site of quenching after protonation of C-terminal residues (Peers et al, 2009;Bonente et al, 2011;Liguori et al, 2013); and the PsbS protein that is protonated on two luminal Glu residues (Li et al, 2000;Li et al, 2004) and is proposed to subsequently promote the reorganization of the photosynthetic apparatus in order to create quenching sites elsewhere (Bassi and Caffarri, 2000;Bonente et al, 2008a;Johnson et al, 2011). It should be noted that efficient energy quenching also requires the presence of Lhc proteins, but this does not require a specific Lhc isoform (Andersson et al, 2001(Andersson et al, , 2003de Bianchi et al, 2008de Bianchi et al, , 2011.…”

mentioning

confidence: 99%

“…LhcSR3 is homologous to the Lhc proteins: it has a similar structure with three transmembrane helices and it is also able to bind Chls and Cars (Bonente et al, 2011). It has been suggested that LhcSR3 itself is the energy quencher due to its pigment binding ability, the unusual fluorescence properties that show very short lifetime components, and its pH sensitivity (Bonente et al, 2011;Liguori et al, 2013;Tokutsu and Minagawa, 2013). A recent investigation suggests the LhcSR is localized both in grana membranes and stroma lamellae in the moss Physcomitrella patens (Pinnola et al, 2015), and investigations on Chlamydomonas suggest that LhcSR3 can bind both to PSI or PSII depending on illumination conditions (Allorent et al, 2013;Bergner et al, 2015).…”

mentioning

confidence: 99%

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

et al. 2016

View full text Add to dashboard Cite

Photosynthetic organisms must respond to excess light in order to avoid photo-oxidative stress. In plants and green algae the fastest response to high light is non-photochemical quenching (NPQ), a process that allows the safe dissipation of the excess energy as heat. This phenomenon is triggered by the low luminal pH generated by photosynthetic electron transport. In vascular plants the main sensor of the low pH is the PsbS protein, while in the green alga Chlamydomonas reinhardtii LhcSR proteins appear to be exclusively responsible for this role. Interestingly, Chlamydomonas also possesses two PsbS genes, but so far the PsbS protein has not been detected and its biological function is unknown. Here, we reinvestigated the kinetics of gene expression and PsbS and LhcSR3 accumulation in Chlamydomonas during high light stress. We found that, unlike LhcSR3, PsbS accumulates very rapidly but only transiently. In order to determine the role of PsbS in NPQ and photoprotection in Chlamydomonas, we generated transplastomic strains expressing the algal or the Arabidopsis psbS gene optimized for plastid expression. Both PsbS proteins showed the ability to increase NPQ in Chlamydomonas wild-type and npq4 (lacking LhcSR3) backgrounds, but no clear photoprotection activity was observed. Quantification of PsbS and LhcSR3 in vivo indicates that PsbS is much less abundant than LhcSR3 during high light stress. Moreover, LhcSR3, unlike PsbS, also accumulates during other stress conditions. The possible role of PsbS in photoprotection is discussed.

show abstract

Amphipol‐assisted purification method for the highly active and stable photosystem II supercomplex of Chlamydomonas reinhardtii

et al. 2019

View full text Add to dashboard Cite

Photosystem II (PSII) splits water and drives electron transfer to plastoquinone via photochemical reactions using light energy. It is surrounded by light‐harvesting complex II (LHCII) to form the PSII–LHCII supercomplex. Complete characterization of its structure and function has, however, been hampered due to instability of the complex in the presence of detergent. To overcome this problem, we developed a new procedure for purifying the PSII–LHCII supercomplexes of Chlamydomonas reinhardtii employing amphipol A8‐35. The obtained supercomplexes showed little LHCII dissociation even 4 days after purification. Oxygen‐evolving activity was retained within amphipol if the extrinsic polypeptides were kept associated by betaine. Electron microscopy revealed that this method also improved structural uniformity and that the major organization was C2S2M2L2.

show abstract

Regulation of Light Harvesting in the Green Alga Chlamydomonas reinhardtii: The C-Terminus of LHCSR Is the Knob of a Dimmer Switch

Cited by 124 publications

References 32 publications

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

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

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

Amphipol‐assisted purification method for the highly active and stable photosystem II supercomplex of Chlamydomonas reinhardtii

Contact Info

Product

Resources

About