Capturing the Quenching Mechanism of Light-Harvesting Complexes of Plants by Zooming in on the Ensemble

Mascoli, Vincenzo; Liguori, Nicoletta; Xu, Pengqi; Roy, Laura M.; Stokkum, Ivo H. M. van; Croce, Roberta

doi:10.1016/j.chempr.2019.08.002

Cited by 59 publications

(106 citation statements)

References 61 publications

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“…The Chl a have the lowest energy levels, which are the emissive states that give rise to each component. The existence of three components indicates multiple Chl a emissive sites within LHCSR3, consistent with previous models of LHCs (Mascoli et al 2019, Mascoli et al 2020, Krüger et al 2010, Krüger et al 2011. The two dynamic components arise from changes in the extent of quenching of the Chl emitters.…”

Section: Roles Of Ph and Zea In Fluorescence Intensity In Vivo And Insupporting

confidence: 88%

Identification of parallel pH- and zeaxanthin-dependent quenching of excess energy in LHCSR3 in Chlamydomonas reinhardtii

Troiano

Perozeni

Moya

et al. 2020

Preprint

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Under high light conditions, oxygenic photosynthetic organisms avoid photodamage by thermally dissipating excess absorbed energy, which is called non-photochemical quenching (NPQ). In green algae, a chlorophyll and carotenoid-binding protein, light-harvesting complex stress-related (LHCSR3), detects excess energy via pH and serves as a quenching site. However, the mechanisms by which LHCSR3 functions have not been determined. Using a combined in vivo and in vitro approach, we identify two parallel yet distinct quenching processes, individually controlled by pH and carotenoid composition, and their likely molecular origin within LHCSR3 from Chlamydomonas reinhardtii. The pH-controlled quenching is removed within a mutant LHCSR3 that lacks the protonable residues responsible for sensing pH. Constitutive quenching in zeaxanthin-enriched systems demonstrates zeaxanthin-controlled quenching, which may be shared with other light-harvesting complexes. We show that both quenching processes prevent the formation of damaging reactive oxygen species, and thus provide distinct timescales and mechanisms of protection in a changing environment.

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Section: Roles Of Ph and Zea In Fluorescence Intensity In Vivo And Insupporting

confidence: 88%

Identification of parallel pH- and zeaxanthin-dependent quenching of excess energy in LHCSR3 in Chlamydomonas reinhardtii

Troiano

Perozeni

Moya

et al. 2020

Preprint

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“…The biexponential decay kinetics of Chl a L imply two subpopulations with different levels of quenching, likely reflecting a quenched conformation and an unquenched one 58,59 . Recent transient absorption studies on CP29, a minor antenna complex homologous to LHCII, found a similar biexponential decay of the terminal Chl a excited state, which was attributed to the coexistence of quenched and unquenched conformations 60 . The coexistence of multiple conformations with distinct photophysics is further supported by single-molecule fluorescence measurements that identified unquenched and quenched conformations of LHCII 61,62 and other homologous complexes 63,64 .…”

Section: Resultsmentioning

confidence: 87%

Observation of dissipative chlorophyll-to-carotenoid energy transfer in light-harvesting complex II in membrane nanodiscs

et al. 2020

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Plants prevent photodamage under high light by dissipating excess energy as heat. Conformational changes of the photosynthetic antenna complexes activate dissipation by leveraging the sensitivity of the photophysics to the protein structure. The mechanisms of dissipation remain debated, largely due to two challenges. First, because of the ultrafast timescales and large energy gaps involved, measurements lacked the temporal or spectral requirements. Second, experiments have been performed in detergent, which can induce nonnative conformations, or in vivo, where contributions from homologous antenna complexes cannot be disentangled. Here, we overcome both challenges by applying ultrabroadband twodimensional electronic spectroscopy to the principal antenna complex, LHCII, in a near-native membrane. Our data provide evidence that the membrane enhances two dissipative pathways, one of which is a previously uncharacterized chlorophyll-to-carotenoid energy transfer. Our results highlight the sensitivity of the photophysics to local environment, which may control the balance between light harvesting and dissipation in vivo.

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“…This switch can be experimentally evidenced though measurements of change in the excited-state lifetime of the complex. For monomeric CP29, lifetimes changing from ∼100 ps to about 4 ns have been recently observed [56], and associated to quenched and lightharvesting states, respectively.…”

Section: Resultsmentioning

confidence: 96%

The energy transfer model of nonphotochemical quenching: Lessons from the minor CP29 antenna complex of plants

Lapillo

Cignoni

Cupellini

et al. 2020

Biochimica et Biophysica Acta (BBA) - Bioenergetics

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Antenna complexes in photosystems of plants and green algae are able to switch between a light-harvesting unquenched conformation and a quenched conformation so to avoid photodamage. When the switch is activated, nonphotochemical quenching (NPQ) mechanisms take place for an efficient deactivation of excess excitation energy. The molecular details of these mechanisms have not been fully clarified but different hypotheses have been proposed. Among them, a popular one involves excitation energy transfer (EET) from the singlet excited Chls to the lowest singlet state (S 1) of carotenoids. In this work, we combine such model with µs-long molecular dynamics simulations of the CP29 minor antenna complex to investigate how conformational fluctuations affect the electronic couplings and the final EET quenching. The computational framework is applied to both CP29 embedding violaxanthin and zeaxantin in its L2 site. Our results demonstrate that the EET model is rather insensitive to physically reasonable variations in single chlorophyll-carotenoid couplings, and that very large conformational changes would be needed to see the large variation of the complex lifetime expected in the switch from light-harvesting to quenched state. We show, however, that a major role in regulating the EET quenching is played by the S 1 energy of the carotenoid, in line with very recent spectroscopy experiments.

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Capturing the Quenching Mechanism of Light-Harvesting Complexes of Plants by Zooming in on the Ensemble

Cited by 59 publications

References 61 publications

Identification of parallel pH- and zeaxanthin-dependent quenching of excess energy in LHCSR3 in Chlamydomonas reinhardtii

Identification of parallel pH- and zeaxanthin-dependent quenching of excess energy in LHCSR3 in Chlamydomonas reinhardtii

Observation of dissipative chlorophyll-to-carotenoid energy transfer in light-harvesting complex II in membrane nanodiscs

The energy transfer model of nonphotochemical quenching: Lessons from the minor CP29 antenna complex of plants

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