Role of Zeaxanthin & PsbS in Photoprotection: Non-Photochemical Quenching, Study notes of Chemistry

Download Role of Zeaxanthin & PsbS in Photoprotection: Non-Photochemical Quenching and more Study notes Chemistry in PDF only on Docsity! review ©2005 EUROPEAN MOLECULAR BIOLOGY ORGANIZATION EMBO reports VOL 6 | NO 7 | 2005 revie Light and oxygenic photosynthesis: energy dissipation as a protection mechanism against photo-oxidation Ildikó Szabó+, Elisabetta Bergantino & Giorgio Mario Giacometti University of Padova, Padova, Italy Efficient photosynthesis is of fundamental importance for plant survival and fitness. However, in oxygenic photosynthesis, the complex apparatus responsible for the conversion of light into chemical energy is susceptible to photodamage. Oxygenic photo- synthetic organisms have therefore evolved several protective mechanisms to deal with light energy. Rapidly inducible non- photochemical quenching (NPQ) is a short-term response by which plants and eukaryotic algae dissipate excitation energy as heat. This review focuses on recent advances in the elucidation of the molecular mechanisms underlying this protective quenching pathway in higher plants. Keywords: photosynthesis; non-photochemical quenching; PsbS; zeaxanthin; light-harvesting complex EMBO reports (2005) 6, 629–634. doi:10.1038/sj.embor.7400460 Introduction During photosynthesis, photons are absorbed by antenna pig- ments, such as protein-bound chlorophylls (Chl) and carotenoids. The excitation energy is transferred from the site of absorption, primarily the light-harvesting complexes (LHCs), to the reaction centres (RCs; Nield et al, 2000). Here, excitation is converted into charge separation, which drives the electron flow between photo- system II (PSII) and photosystem I (PSI) through the cytochrome b6f complex. The net result of this process is the oxidation of water molecules, the production of molecular oxygen, the reduction of NADP+ and the generation of a proton gradient (∆pH). The energy stored as ∆pH is exploited for ATP synthesis. The interplay between light and oxygenic photosynthesis is an enterprise of complex reg- ulation. This short review focuses on the molecular mechanisms that allow sophisticated regulation of the amount of excitation energy transferred to the RC of PSII. The photosynthetic apparatus is highly dynamic and able to respond to several environmental stimuli, including changes in the quality and quantity of incident light and the availability of carbon dioxide. A short-term response is ensured by non-photochemical quenching (NPQ), a process in which absorbed light energy is dissipated as heat and does not take part in photochemistry. The phenomenon involves quenching of chlorophyll a (Chla) fluores- cence, which is induced under steady-state illumination and which can be analysed in terms of three components: state transi- tion (qT), ∆pH-dependent quenching (qE) and photoinhibition (qI). The majority of NPQ is believed to occur through qE in the PSII antenna pigments bound to the light-harvesting proteins (LHCII; Demmig-Adams & Adams, 1992). Non-photochemical quenching: state transition Rapid reorganization of the light-harvesting apparatus, termed ‘state transition’, occurs in response to changes in the availability of carbon dioxide and the reduction state of chloroplasts. A kinase system becomes activated and phosphorylates a fraction of LHCII proteins. As a consequence, lateral redistribution of the phosphorylated LHCII proteins and their association with PSI take place (Wollman, 2001; Allen & Forsberg, 2001). Because the fluorescence yield of PSII diminishes during state transition due to antenna size reduction, this process, also called qT, is considered a component of NPQ. A thylakoid-associated Ser–Thr regulatory kinase, STN7, recently identified in Arabidopsis, has been shown to be required for state transition (Bellafiore et al, 2005) and cytochrome b6f has been recognized as a key partner in kinase activation in Chlamydomonas (Wollman & Lemaire, 1988). In previous models, state transition was considered neces- sary to maximize photosynthetic efficiency by balancing the excitation of the two photosystems. A recent reinterpretation, however, indicates a different role: in conditions of limiting CO2 and a high reduction level of the chloroplast, the photosynthetic apparatus is switched from the oxygenic type, with two photo- systems working in series, to an ATP-generator type, with cyclic electron flow around PSI (for comprehensive reviews, see Wollman, 2001; Aro & Ohad, 2003). Non-photochemical quenching: photoinhibition The photosynthetic apparatus must deal with marked changes in light intensity. Directional movements of whole leaves and/or chloroplasts, which may allow the plant to optimize light absorp- tion, are relatively slow processes. Rather than regulating light absorption, a fast response is obtained through the regulation of dissipative de-excitation of absorbed photons. In normal condi- tions, most of the energy in singlet-excited chlorophyll (1Chl*) is 629 Department of Biology, University of Padova, Viale G. Colombo 3, 35121 Padova, Italy +Corresponding author. Tel: +39 (0)49 8276324; Fax: +39 (0)49 8276300; E-mail: ildi@civ.bio.unipd.it Submitted 29 March 2005; accepted 19 May 2005 review EMBO reports VOL 6 | NO 7 | 2005 ©2005 EUROPEAN MOLECULAR BIOLOGY ORGANIZATION Photoprotection in photosynthetic organisms I. Szabó et al 630 used at the RC to drive electron transport; in this case, Chl fluores- cence quenching is correlated to charge separation (photochemi- cal quenching). However, when the rate of formation of 1Chla* exceeds the overall rate of its energy conversion at the RC, inter- system crossing leads to an increasing population of 3Chla* (triplet state) in the antenna moiety, which can activate molecular oxygen to its highly reactive singlet state (1O2). Singlet oxygen molecules, as well as the other forms of reactive oxygen species (ROS), are known to induce oxidative damage to pigments, pro- teins and lipids in the thylakoid membrane, thereby impairing overall photosynthetic efficiency (photoinhibition). The fluores- cence quenching associated with this phenomenon, which is slowly reversible or even partially irreversible, represents the por- tion of NPQ indicated as qI. By scavenging the triplet excited state of Chl and dissipating associated energy by fast thermalization, carotenoids prevent activation of oxygen, thus protecting chloro- phyll–protein complexes from photo-oxidation. Without the pro- tection exerted by carotenoids, rapid and complete destruction of the entire photosystems would occur. Non-photochemical quenching: ∆pH-dependent quenching When the acceptor quinones are reduced at steady state, charge separation at the PSII RC is followed by recombination, with a high probability of the formation of 3P680 and singlet oxygen. The chloro- phylls of the special pair P680 cannot be protected against oxygen activation because the two nearby β-carotene molecules are not close enough (Ferreira et al, 2004). For this reason, regulation of the transmission of excitation to the PSII RC is of the utmost importance. The portion of NPQ named qE has a central role in this con- text and is a ∆pH-dependent, rapidly inducible component. qE is also called feedback de-excitation, because thermal dissipa- tion of antenna 1Chla* is stimulated by ∆pH, which builds up across the thylakoid membrane during photosynthetic electron transport and is therefore brought about by the same excitation that qE contributes to dissipation. qE has been shown to be important for plant fitness in variable light conditions rather than for the induction of tolerance to high-intensity light itself (Kulheim et al, 2002), and may easily be measured as the quickly reversible portion of maximal PSII fluorescence quenching, which is not associated with charge separation (Demmig-Adams & Adams, 2000). During the past decade, our understanding of qE has been greatly advanced, particularly by the selection of NPQ-deficient Arabidopsis mutants by video imaging of Chl fluorescence quenching (Niyogi et al, 1998), the successful application of res- onance Raman spectroscopy (Robert et al, 2004), which yielded structural information about specific pigment molecules in thy- lakoid membrane complexes in vivo and in vitro, and the ability to detect non-fluorescent, optically dark excited states of pig- ments by femtosecond transient absorption kinetics in intact membranes (Ma et al, 2003; Holt et al, 2005). The resolution of the crystal structure of the isolated antenna LHCII complex (Liu et al, 2004; Standfuss et al, 2005), as well as in vitro reconstitu- tion of antenna proteins (Sandonà et al, 1998) has also signifi- cantly contributed to the identification of the key components responsible for qE. They are pigments of the xanthophyll cycle, PsbS Cp43 Fe CP24 CP29CP26 LHCII hv Stroma Lumen QA Phe P680 YZ QB D2 D1 Cp47 2H2O O2 + 4H + to cyt b6ƒ MnMn MnMn PQH2 e– Fig 1 | Organization of photosystem II and light-harvesting complex II in the thylakoid membrane. Cp43, Cp47: internal antenna chlorophyll–protein complexes. D1, D2: main components of reaction centres (RCs) with binding sites for electron acceptor quinones (Q B , Q A ). P 680 : chlorophyll special pair. Other cofactors associated with D1/D2: pheophytin (Phe), non-haem iron (Fe), Mn-cluster. Accessory chlorophylls and β-carotene are not shown. Chl, chlorophyll; PQH 2 , plastoquinone pool; cytb6f, cytochrome b6f complex; Y Z , D1-Tyr161. For a more detailed description, see Ferreira et al (2004). Scheme adapted from J. Nield (Imperial College London, UK) with permission. See downloads section of www.bio.ic.ac.uk/research/nield/. review ©2005 EUROPEAN MOLECULAR BIOLOGY ORGANIZATION EMBO reports VOL 6 | NO 7 | 2005 Photoprotection in photosynthetic organisms I. Szabó et al 633 qI, antenna qE, and RC qE) take place depending on the balance between the dissipation ability of the carbon fixation apparatus and light flux. Concluding remarks With reference to the three ‘hot topics’ mentioned above, some conclusions may be drawn. Zea is certainly deeply involved in determining qE, and its ability to quench chlorophyll excitation directly has been clearly demonstrated. There is good evidence that this occurs in at least two different sites in the PSII–LHCII supercomplex: in the hydrophobic pocket of LHCII monomers, and in connection with the involvement of PsbS in producing qE. On the basis of the literature, various mechanisms can be envisaged for qE. A Zea-dependent qE may occur, together with a conformational change in antenna proteins, either on aggrega- tion of LHCII trimers with each other (Liu et al, 2004) or by aggre- gation of minor antennae CP29 and CP26 with LHCII (Horton & Ruban, 2005). A variant of this mechanism introduces the formation of a quenching site at the level of each LHCII monomer as the result of binding of Zea, which displaces Vio, with no need for confor- mational rearrangement of the LHCII trimers (Standfuss et al, 2005). In this view, conformational rearrangements may still be important in relation to the Zea-dependent contribution to qE of the minor antennae CP29 and CP26, which lie in a strategic loca- tion inside the PSII–LHCII supercomplex, at the interface between the peripheral LHCII and the internal antennae CP43 and CP47. Other qE mechanisms depend on PsbS. Some experimental evidence also positions this protein at the interface between LHCII and the PSII core. The quenching mechanism associated with PsbS is also dependent on Zea, but the detailed mechanism is still hypothetical. In one model, PsbS has a critical role in bringing activated Zea into close proximity with a Chl, thus pro- moting the formation of a Chl–Zea heterodimer that is responsi- ble for the quenching process (Fig 3). Chl may be bound to PsbS itself (Funk et al, 1995) or, more probably, may be located on a neighbouring minor or major antenna protein. PsbS has been proposed to bind Zea on protonation and consequent conforma- tional change (Aspinall O’Dea et al, 2002; Li et al, 2004), which may consist of proton-induced monomerization, followed by its association with an LHCII component (Bergantino et al, 2003). These mechanisms are all well supported by experimental data and their coexistence is highly probable: some qE persists in PsbS-less Arabidopsis (Li et al, 2000), and PsbS-mediated quenching seems to be essential only in rapidly fluctuating light conditions (Kulheim et al, 2002). Instead, inhibition of single antenna protein expression does not significantly affect feedback de-excitation in field conditions, but it does affect overall plant fitness (Ganeteg et al, 2004). In the emerging scenario, the interplay of these proposed mechanisms ensures the best photo- protective performance in each different and variable light condition. ACKNOWLEDGEMENTS The authors thank R. Bassi and D. Carbonera for useful discussions. I.S. is grateful to the EMBO Young Investigator Programme for financial support. Thanks are due to G. Walton and C. Friso for revision of the text and figures, respectively. REFERENCES Allen JF, Forsberg J (2001) Molecular recognition in thylakoid structure and function. 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