Violaxanthin and Zeaxanthin May Replace Lutein at the L1 Site of LHCII, Conserving the Interactions with Surrounding Chlorophylls and the Capability of Triplet-Triplet Energy Transfer
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
P-DiSC-2019
University of Padua
NExUS
MIUR Dipartimenti di Eccellenza
RIBA 2017
201795SBA3_004, HARVEST
Progetti di Ricerca d'Interesse Nazionale PRIN
CZ.02.2.69/0. 0/0.0/18_053/0016982.
European Union
60077344
RVO
CEP - Centrální evidence projektů
PubMed
35563202
PubMed Central
PMC9105099
DOI
10.3390/ijms23094812
PII: ijms23094812
Knihovny.cz E-zdroje
- Klíčová slova
- LHCII, ODMR, TR-EPR, TTET, carotenoid, light-harvesting complex II, triplet state,
- MeSH
- Arabidopsis * metabolismus MeSH
- chlorofyl metabolismus MeSH
- fotosystém II (proteinový komplex) metabolismus MeSH
- karotenoidy metabolismus MeSH
- lutein * MeSH
- přenos energie MeSH
- světlosběrné proteinové komplexy metabolismus MeSH
- xanthofyly chemie MeSH
- zeaxanthiny metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- chlorofyl MeSH
- fotosystém II (proteinový komplex) MeSH
- karotenoidy MeSH
- lutein * MeSH
- světlosběrné proteinové komplexy MeSH
- violaxanthin MeSH Prohlížeč
- xanthofyly MeSH
- zeaxanthiny MeSH
Carotenoids represent the first line of defence of photosystems against singlet oxygen (1O2) toxicity, because of their capacity to quench the chlorophyll triplet state (3Chl) through a physical mechanism based on the transfer of triplet excitation (triplet-triplet energy transfer, TTET). In previous works, we showed that the antenna LHCII is characterised by a robust photoprotective mechanism, able to adapt to the removal of individual chlorophylls while maintaining a remarkable capacity for 3Chl quenching. In this work, we investigated the effects on this quenching induced in LHCII by the replacement of the lutein bound at the L1 site with violaxanthin and zeaxanthin. We studied LHCII isolated from the Arabidopsis thaliana mutants lut2-in which lutein is replaced by violaxanthin-and lut2 npq2, in which all xanthophylls are replaced constitutively by zeaxanthin. We characterised the photophysics of these systems via optically detected magnetic resonance (ODMR) and time-resolved electron paramagnetic resonance (TR-EPR). We concluded that, in LHCII, lutein-binding sites have conserved characteristics, and ensure efficient TTET regardless of the identity of the carotenoid accommodated.
Department of Biotechnology University of Verona Strada Le Grazie 37134 Verona Italy
Department of Chemical Sciences University of Padova via Marzolo 1 35131 Padova Italy
Zobrazit více v PubMed
Caffarri S., Croce R., Breton J., Bassi R. The Major Antenna Complex of Photosystem II Has a Xanthophyll Binding Site Not Involved in Light Harvesting. J. Biol. Chem. 2001;276:35924–35933. doi: 10.1074/jbc.M105199200. PubMed DOI
Liu Z., Yan H., Wang K., Kuang T., Zhang J., Gui L., An X., Chang W. Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature. 2004;428:287–292. doi: 10.1038/nature02373. PubMed DOI
Rochaix J.-D. Regulation and Dynamics of the Light-Harvesting System. Annu. Rev. Plant Biol. 2014;65:287–309. doi: 10.1146/annurev-arplant-050213-040226. PubMed DOI
Croce R., van Amerongen H. Light harvesting in oxygenic photosynthesis: Structural biology meets spectroscopy. Science. 2020;369:eaay2058. doi: 10.1126/science.aay2058. PubMed DOI
Krieger-Liszkay A. Singlet oxygen production in photosynthesis. J. Exp. Bot. 2004;56:337–346. doi: 10.1093/jxb/erh237. PubMed DOI
Pinnola A., Bassi R. Molecular mechanisms involved in plant photoprotection. Biochem. Soc. Trans. 2018;46:467–482. doi: 10.1042/BST20170307. PubMed DOI
Murchie E.H., Ruban A.V. Dynamic non-photochemical quenching in plants: From molecular mechanism to productivity. Plant J. 2020;101:885–896. doi: 10.1111/tpj.14601. PubMed DOI
Ruban A.V. Nonphotochemical Chlorophyll Fluorescence Quenching: Mechanism and Effectiveness in Protecting Plants from Photodamage. Plant Physiol. 2016;170:1903–1916. doi: 10.1104/pp.15.01935. PubMed DOI PMC
Carbonera D., Di Valentin M., Agostini G., Giacometti G., Liddell P.A., Gust D., Moore A.L., Moore T.A. Energy transfer and spin polarization of the carotenoid triplet state in synthetic carotenoporphyrin dyads and in natural antenna complexes. Appl. Magn. Reson. 1997;13:487–504. doi: 10.1007/BF03162222. DOI
Remelli R., Varotto C., Sandonà D., Croce R., Bassi R. Chlorophyll Binding to Monomeric Light-harvesting Complex. J. Biol. Chem. 1999;274:33510–33521. doi: 10.1074/jbc.274.47.33510. PubMed DOI
Agostini A., Nicol L., Da Roit N., Bortolus M., Croce R., Carbonera D. Altering the exciton landscape by removal of specific chlorophylls in monomeric LHCII provides information on the sites of triplet formation and quenching by means of ODMR and EPR spectroscopies. Biochim. Biophys. Acta-Bioenerg. 2021;1862:148481. doi: 10.1016/j.bbabio.2021.148481. PubMed DOI
Formaggio E., Cinque G., Bassi R. Functional architecture of the major light-harvesting complex from higher plants. J. Mol. Biol. 2001;314:1157–1166. doi: 10.1006/jmbi.2000.5179. PubMed DOI
Mascoli V., Liguori N., Cupellini L., Elias E., Mennucci B., Croce R. Uncovering the interactions driving carotenoid binding in light-harvesting complexes. Chem. Sci. 2021;12:5113–5122. doi: 10.1039/D1SC00071C. PubMed DOI PMC
Saccon F., Durchan M., Polívka T., Ruban A.V. The robustness of the terminal emitter site in major LHCII complexes controls xanthophyll function during photoprotection. Photochem. Photobiol. Sci. 2020;19:1308–1318. doi: 10.1039/D0PP00174K. PubMed DOI
Saccon F., Durchan M., Kaňa R., Prášil O., Ruban A.V., Polívka T. Spectroscopic Properties of Violaxanthin and Lutein Triplet States in LHCII are Independent of Carotenoid Composition. J. Phys. Chem. B. 2019;123:9312–9320. doi: 10.1021/acs.jpcb.9b06293. PubMed DOI
Dall’Osto L., Lico C., Alric J., Giuliano G., Havaux M., Bassi R. Lutein is needed for efficient chlorophyll triplet quenching in the major LHCII antenna complex of higher plants and effective photoprotection in vivounder strong light. BMC Plant Biol. 2006;6:32. doi: 10.1186/1471-2229-6-32. PubMed DOI PMC
Dall’Osto L., Holt N.E., Kaligotla S., Fuciman M., Cazzaniga S., Carbonera D., Frank H.A., Alric J., Bassi R. Zeaxanthin Protects Plant Photosynthesis by Modulating Chlorophyll Triplet Yield in Specific Light-harvesting Antenna Subunits. J. Biol. Chem. 2012;287:41820–41834. doi: 10.1074/jbc.M112.405498. PubMed DOI PMC
Havaux M., Dall’Osto L., Cuiné S., Giuliano G., Bassi R. The Effect of Zeaxanthin as the Only Xanthophyll on the Structure and Function of the Photosynthetic Apparatus in Arabidopsis thaliana. J. Biol. Chem. 2004;279:13878–13888. doi: 10.1074/jbc.M311154200. PubMed DOI
Carbonera D. Optically detected magnetic resonance (ODMR) of photoexcited triplet states. Photosynth. Res. 2009;102:403–414. doi: 10.1007/s11120-009-9407-5. PubMed DOI
Di Valentin M., Biasibetti F., Ceola S., Carbonera D. Identification of the Sites of Chlorophyll Triplet Quenching in Relation to the Structure of LHC-II from Higher Plants. Evidence from EPR Spectroscopy. J. Phys. Chem. B. 2009;113:13071–13078. doi: 10.1021/jp904012j. PubMed DOI
Agostini A., Palm D.M., Paulsen H., Carbonera D. Optically Detected Magnetic Resonance of Chlorophyll Triplet States in Water-Soluble Chlorophyll Proteins from Lepidium virginicum: Evidence for Excitonic Interaction among the Four Pigments. J. Phys. Chem. B. 2018;122:6156–6163. doi: 10.1021/acs.jpcb.8b01906. PubMed DOI
Carbonera D., Agostini A., Di Valentin M., Gerotto C., Basso S., Giacometti G.M., Morosinotto T. Photoprotective sites in the violaxanthin–chlorophyll a binding Protein (VCP) from Nannochloropsis gaditana. Biochim. Biophys. Acta-Bioenerg. 2014;1837:1235–1246. doi: 10.1016/j.bbabio.2014.03.014. PubMed DOI
Di Valentin M., Carbonera D. The fine tuning of carotenoid–chlorophyll interactions in light-harvesting complexes: An important requisite to guarantee efficient photoprotection via triplet–triplet energy transfer in the complex balance of the energy transfer processes. J. Phys. B At. Mol. Opt. Phys. 2017;50:162001. doi: 10.1088/1361-6455/aa7dd4. DOI
Ruban A.V., Berera R., Ilioaia C., van Stokkum I.H.M., Kennis J.T.M., Pascal A.A., van Amerongen H., Robert B., Horton P., van Grondelle R. Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature. 2007;450:575–578. doi: 10.1038/nature06262. PubMed DOI
Di Valentin M., Büchel C., Giacometti G.M., Carbonera D. Chlorophyll triplet quenching by fucoxanthin in the fucoxanthin–chlorophyll protein from the diatom Cyclotella meneghiniana. Biochem. Biophys. Res. Commun. 2012;427:637–641. doi: 10.1016/j.bbrc.2012.09.113. PubMed DOI
Carbonera D., Giacometti G., Agostini G., Angerhofer A., Aust V. ODMR of carotenoid and chlorophyll triplets in CP43 and CP47 complexes of spinach. Chem. Phys. Lett. 1992;194:275–281. doi: 10.1016/0009-2614(92)86051-I. DOI
Peterman E.J., Dukker F.M., van Grondelle R., van Amerongen H. Chlorophyll a and carotenoid triplet states in light-harvesting complex II of higher plants. Biophys. J. 1995;69:2670–2678. doi: 10.1016/S0006-3495(95)80138-4. PubMed DOI PMC
Carbonera D., Giacometti G., Agostini G. FDMR of Carotenoid and Chlorophyll triplets in light-harvesting complex LHCII of spinach. Appl. Magn. Reson. 1992;3:859–872. doi: 10.1007/BF03260117. DOI
van der Vos R., Carbonera D., Hoff A.J. Microwave and optical spectroscopy of carotenoid triplets in light-harvesting complex LHC II of spinach by absorbance-detected magnetic resonance. Appl. Magn. Reson. 1991;2:179–202. doi: 10.1007/BF03166035. DOI
Ho J., Kish E., Méndez-Hernández D.D., WongCarter K., Pillai S., Kodis G., Niklas J., Poluektov O.G., Gust D., Moore T.A., et al. Triplet–triplet energy transfer in artificial and natural photosynthetic antennas. Proc. Natl. Acad. Sci. USA. 2017;114:E5513–E5521. doi: 10.1073/pnas.1614857114. PubMed DOI PMC
Aust V., Angerhofer A., Ullrich J., von Schütz J.U., Wolf H.C., Cogdell R.J. ADMR of carotenoid triplet states in bacterial photosynthetic antenna and reaction center complexes. Chem. Phys. Lett. 1991;181:213–221. doi: 10.1016/0009-2614(91)90357-F. DOI
Agostini A., Niklas J., Schulte T., Di Valentin M., Bortolus M., Hofmann E., Lubitz W., Carbonera D. Changing the site energy of per-614 in the Peridinin-chlorophyll a-protein does not alter its capability of chlorophyll triplet quenching. Biochim. Biophys. Acta-Bioenerg. 2018;1859:612–618. doi: 10.1016/j.bbabio.2018.05.008. PubMed DOI
Galinato M.G.I., Niedzwiedzki D., Deal C., Birge R.R., Frank H.A. Cation radicals of xanthophylls. Photosynth. Res. 2007;94:67–78. doi: 10.1007/s11120-007-9218-5. PubMed DOI
Spezia R., Aschi M., Di Nola A., Di Valentin M., Carbonera D., Amadei A. The Effect of Protein Conformational Flexibility on the Electronic Properties of a Chromophore. Biophys. J. 2003;84:2805–2813. doi: 10.1016/S0006-3495(03)70010-1. PubMed DOI PMC
Müller P., Li X.-P., Niyogi K.K. Non-Photochemical Quenching. A Response to Excess Light Energy. Plant Physiol. 2001;125:1558–1566. doi: 10.1104/pp.125.4.1558. PubMed DOI PMC
Ruban A.V., Johnson M.P., Duffy C.D.P. The photoprotective molecular switch in the photosystem II antenna. Biochim. Biophys. Acta-Bioenerg. 2012;1817:167–181. doi: 10.1016/j.bbabio.2011.04.007. PubMed DOI
Holt N.E., Fleming G.R., Niyogi K.K. Toward an Understanding of the Mechanism of Nonphotochemical Quenching in Green Plants. Biochemistry. 2004;43:8281–8289. doi: 10.1021/bi0494020. PubMed DOI
Dreuw A., Fleming G.R., Head-Gordon M. Chlorophyll fluorescence quenching by xanthophylls. Phys. Chem. Chem. Phys. 2003;5:3247. doi: 10.1039/b304944b. DOI
Dreuw A., Fleming G.R., Head-Gordon M. Charge-Transfer State as a Possible Signature of a Zeaxanthin−Chlorophyll Dimer in the Non-photochemical Quenching Process in Green Plants. J. Phys. Chem. B. 2003;107:6500–6503. doi: 10.1021/jp034562r. DOI
Cupellini L., Calvani D., Jacquemin D., Mennucci B. Charge transfer from the carotenoid can quench chlorophyll excitation in antenna complexes of plants. Nat. Commun. 2020;11:662. doi: 10.1038/s41467-020-14488-6. PubMed DOI PMC
Sláma V., Cupellini L., Mennucci B. Exciton properties and optical spectra of light harvesting complex II from a fully atomistic description. Phys. Chem. Chem. Phys. 2020;22:16783–16795. doi: 10.1039/D0CP02492A. PubMed DOI
Novoderezhkin V.I., Palacios M.A., van Amerongen H., van Grondelle R. Excitation Dynamics in the LHCII Complex of Higher Plants: Modeling Based on the 2.72 Å Crystal Structure. J. Phys. Chem. B. 2005;109:10493–10504. doi: 10.1021/jp044082f. PubMed DOI
Bassi R., Rigoni F., Barbato R., Giacometti G.M. Light-harvesting chlorophyll a/b proteins (LHCII) populations in phosphorylated membranes. Biochim. Biophys. Acta-Bioenerg. 1988;936:29–38. doi: 10.1016/0005-2728(88)90248-4. DOI
Dall’Osto L., Caffarri S., Bassi R. A Mechanism of Nonphotochemical Energy Dissipation, Independent from PsbS, Revealed by a Conformational Change in the Antenna Protein CP26. Plant Cell. 2005;17:1217–1232. doi: 10.1105/tpc.104.030601. PubMed DOI PMC
Dainese P., Hoyer-Hansen G., Bassi R. The resolution of chlorophyll a/b binding proteins by a preparative method based on flat bed isoelectric focusing. Photochem. Photobiol. 1990;51:693–703. doi: 10.1111/php.1990.51.6.693. PubMed DOI
Lampoura S.S., Barzda V., Owen G.M., Hoff A.J., van Amerongen H. Aggregation of LHCII Leads to a Redistribution of the Triplets over the Central Xanthophylls in LHCII. Biochemistry. 2002;41:9139–9144. doi: 10.1021/bi025724x. PubMed DOI
Santabarbara S., Agostini G., Casazza A.P., Syme C.D., Heathcote P., Böhles F., Evans M.C.W., Jennings R.C., Carbonera D. Chlorophyll triplet states associated with Photosystem I and Photosystem II in thylakoids of the green alga Chlamydomonas reinhardtii. Biochim. Biophys. Acta-Bioenerg. 2007;1767:88–105. doi: 10.1016/j.bbabio.2006.10.007. PubMed DOI
Carbonera D., Collareta P., Giacometti G. The P700 triplet state in an intact environment detected by ODMR. A well resolved triplet minus singlet spectrum. Biochim. Biophys. Acta-Bioenerg. 1997;1322:115–128. doi: 10.1016/S0005-2728(97)00068-6. DOI
Santabarbara S., Bordignon E., Jennings R.C., Carbonera D. Chlorophyll Triplet States Associated with Photosystem II of Thylakoids. Biochemistry. 2002;41:8184–8194. doi: 10.1021/bi0201163. PubMed DOI
Stoll S., Schweiger A. EasySpin, a comprehensive software package for spectral simulation and analysis in EPR. J. Magn. Reson. 2006;178:42–55. doi: 10.1016/j.jmr.2005.08.013. PubMed DOI
Carbonera D., di Valentin M., Corvaja C., Giacometti G., Agostini G., Liddell P.A., Moore A.L., Moore T.A., Gust D. Carotenoid triplet detection by time-resolved EPR spectroscopy in carotenopyropheophorbide dyads. J. Photochem. Photobiol. A Chem. 1997;105:329–335. doi: 10.1016/S1010-6030(96)04571-6. DOI
Di Valentin M., Meneghin E., Orian L., Polimeno A., Büchel C., Salvadori E., Kay C.W.M., Carbonera D. Triplet–triplet energy transfer in fucoxanthin-chlorophyll protein from diatom Cyclotella meneghiniana: Insights into the structure of the complex. Biochim. Biophys. Acta-Bioenerg. 2013;1827:1226–1234. doi: 10.1016/j.bbabio.2013.07.003. PubMed DOI
Di Valentin M., Agostini G., Salvadori E., Ceola S., Giacometti G.M., Hiller R.G., Carbonera D. Triplet–triplet energy transfer in Peridinin-Chlorophyll a-protein reconstituted with Chl a and Chl d as revealed by optically detected magnetic resonance and pulse EPR: Comparison with the native PCP complex from Amphidinium carterae. Biochim. Biophys. Acta-Bioenerg. 2009;1787:168–175. doi: 10.1016/j.bbabio.2008.12.004. PubMed DOI
Mozzo M., Dall’Osto L., Hienerwadel R., Bassi R., Croce R. Photoprotection in the Antenna Complexes of Photosystem II. J. Biol. Chem. 2008;283:6184–6192. doi: 10.1074/jbc.M708961200. PubMed DOI
Johnson M.P., Havaux M., Triantaphylides C., Ksas B., Pascal A.A., Robert B., Davison P.A., Ruban A.V., Horton P. Elevated Zeaxanthin Bound to Oligomeric LHCII Enhances the Resistance of Arabidopsis to Photooxidative Stress by a Lipid-protective, Antioxidant Mechanism. J. Biol. Chem. 2007;282:22605–22618. doi: 10.1074/jbc.M702831200. PubMed DOI
Morosinotto T., Caffarri S., Dall’Osto L., Bassi R. Mechanistic aspects of the xanthophyll dynamics in higher plant thylakoids. Physiol. Plant. 2003;119:347–354. doi: 10.1034/j.1399-3054.2003.00213.x. DOI
Cazzaniga S., Bressan M., Carbonera D., Agostini A., Dall’Osto L. Differential Roles of Carotenes and Xanthophylls in Photosystem I Photoprotection. Biochemistry. 2016;55:3636–3649. doi: 10.1021/acs.biochem.6b00425. PubMed DOI