On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls

Abstract

Arabidopsis ͉ LHCII ͉ NPQ ͉ two-photon excitation P lants are exposed to sunlight intensities varying over several orders of magnitude during a typical day (1). Under low light conditions, almost all absorbed sunlight photons are used for the primary photosynthetic reaction steps. However, under high light conditions the photosynthetic apparatus must be protected from excess excitation energy, because it may lead to deleterious side-effects. Balancing between efficient utilization of solar energy under restrictive light conditions and dissipation of excess energy when the absorbed light exceeds the photosynthetic capacity is therefore essential for the survival and fitness of plants (2). It is known that light-induced increase of the pH gradient across the thylakoid membrane (3, 4) and the presence of the protein PsbS (5) are necessary for the down-regulation of the photosynthetic activity under excess light and that Zea is simultaneously formed from violaxanthin (Vio) through the enzymatic xanthophyll cycle (6). However, although many different studies have been undertaken to elucidate the details of this important regulation, a complete picture of its mechanisms is still missing. Several different regulation models have been proposed and indeed it cannot be excluded that different mechanisms contribute more or less to plants adaptation to varying light conditions. However, at present even the regulation site and photophysical mechanisms are unresolved, because the models are at least partly contradicting each other (5, 7-15).The most important measurable signature of plants regulation activity is its varying residual Chl fluorescence intensity (16), which is proportional to the regulated amount of excitation energy in the photosynthetic apparatus. The actual extent of adaptation-dependent quenching of Chl singlet excited state energy, known as nonphotochemical quenching (NPQ), is typically quantified by the parameterwhich reflects the reduction in the residual Chl fluorescence of plants, FЈ m , brought about by the unknown excitation energy dissipation mechanisms, in comparison to the residual Chl fluorescence observable from the completely dark adapted plant, F m , in which no photoprotective energy dissipation is operating. FЈ m and F m are usually measured using short, intense light flashes that saturate the photosynthetic reaction center chemistry. This guarantees that the observed differences in FЈ m and F m reflect only the extent of energy dissipation through photoprotective channels, without affecting the adaptation status of the plant (16). It is long known that carotenoids play an important role in the regulation mechanisms and several different types of electronic interactions between carotenoids and Chls have been proposed to play a key role as dissipation valves for excess excitation energy (9, 10, 12). However, so far it was difficult to quantify the extent of these interactions and to investigate directly their involvement in the flow of excitation energy and its regulation, especially in living...

Direct interaction of the major light-harvesting complex II and PsbS in nonphotochemical quenching

“…The opaque proteoliposome fraction was harvested, and protein incorporation was confirmed by freeze-fracture EM ( Coupling , which is closely related to electronic Car S 1 -Chl coupling, increases directly with NPQ. This is observed both in vitro with isolated LHC-II under conditions that promote Chl fluorescence quenching and in A. thaliana plants exposed to high light (19). Φ CarS 1 −Chl Coupling can be determined directly by comparing the Chl fluorescence observed on selective two-photon excitation (TPE) of carotenoids (Car S 1 ) and that observed after direct Chl one-photon excitation (OPE) (19) (details are provided in Eq.…”

“…Coupling on PsbS, Zea, and lutein (Lut) (19). To investigate the correlation with Chl fluorescence quenching in a reconstituted in vitro system, we performed TPE and OPE measurements ( Fig.…”

“…Several models have been proposed to explain the mechanism of excess energy dissipation. These include simple pigment exchange of Vio for Zea (13), aggregation (14) or an internal conformational change of LHC-II (15,16), charge transfer quenching in minor LHCs (17,18), and quenching by carotenoid (Car) S 1 -Chl interactions (19). On the basis of an earlier suggestion (20), a model for qE was put forward, which defines a role for PsbS as a transient pigment-binding protein on pH-induced monomerization (21).…”

Energy transfer dynamics in trimers and aggregates of light-harvesting complex II probed by 2D electronic spectroscopy

“…The molecular mechanism behind NPQ has so far not been unequivocally established 19 and there may, in fact, be several mechanisms acting in parallel, such as decay via the S 1 state of lutein 3,20 and via a Chl-Chl charge transfer state; 17,18,21 other mechanisms have been proposed as well. [22][23][24] While a great amount of effort has been centered on explaining the precise mechanism of quenching the excess excitation energy of Chls, in-depth analyses on examining the Chl energy transfer process in the quenched state of LHCII are scarce. Femtosecond transient absorption spectroscopy studies on LHCII aggregates previously using Chl a excitation have led to proposals of models and dynamics of energy flow to the intermediate quencher state, be it either a carotenoid S 1 state 20 or a Chl-Chl charge transfer state.…”

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

“…NPQ is a complex and multifactorial process that has been deeply investigated in recent years. Although the molecular mechanisms are only partially understood and still debated (Holt et al, 2005;Ruban et al, 2007;Bode et al, 2009;Holzwarth et al, 2009;Kruger et al, 2014), several key actors involved in NPQ have been discovered in plants and green algae (see Duffy and Ruban [2015] and Goss and Lepetit [2015] for recent reviews).…”