• This record comes from PubMed

LHCII - a protein like a 'Swiss Army knife' with many mechanisms and functions

. 2023 ; 61 (4) : 405-416. [epub] 20230713

Status PubMed-not-MEDLINE Language English Country Czech Republic Media electronic-ecollection

Document type Journal Article, Review

The review highlights the relationship between the molecular organization of the light-harvesting complex of photosystem II (LHCII) and sunlight utilization by higher plants. The molecular form of LHCII switches rapidly and reversibly during diurnal changes of light intensity, from low (ca. 10) to high [ca. 1,000 μmol(photon) m-2 s-1], so the sensitivity of LHCII to light may control the balance between light harvesting and photoprotection state. Our understanding and concept of this mechanism are based on the knowledge of the structure and photophysics of different LHCII molecular forms: monomer, dimer, trimer, and aggregate. It is proposed that LHCII monomers, dimers, and lateral aggregates are fundamental blocks of excess light-dissipation machinery. Trimer is exceptionally well suited to play a physiological role of an antenna complex. A correlation between the LHCII molecular form and the presence of xanthophyll cycle pigment violaxanthin and zeaxanthin in the complex structure is also shown. Moreover, the role of LHCII protein phosphorylation in thylakoid membrane architecture is also discussed. The dual function of LHCII has been studied in the natural thylakoid membranes of chloroplasts, in the artificial lipid-LHCII model membranes, and by suspension of LHCII in a detergent solution.

See more in PubMed

Albanese P., Tamara S., Saracco G. et al.: How paired PSII–LHCII supercomplexes mediate the stacking of plant thylakoid membranes unveiled by structural mass-spectrometry. – Nat. Commun. 11: 1361, 2020. 10.1038/s41467-020-15184-1 PubMed DOI PMC

Barzda V., Istokovics A., Simidjiev I., Garab G.: Structural flexibility of chiral macroaggregates of light-harvesting chlorophyll a/b pigment–protein complexes. Light-induced reversible structural changes associated with energy dissipation. – Biochemistry 35: 8981-8985, 1996. 10.1021/bi960114g PubMed DOI

Battersby A.R.: Tetrapyrroles: the pigments of life. – Nat. Prod. Rep. 17: 507-526, 2000. 10.1039/b002635m PubMed DOI

Bellafiore S., Barneche F., Peltier G., Rochaix J.-D.: State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. – Nature 433: 892-895, 2005. 10.1038/nature03286 PubMed DOI

Bethmann S., Melzer M., Schwarz N., Jahns P.: The zeaxanthin epoxidase is degraded along with the D1 protein during photoinhibition of photosystem II. – Plant Direct 3: e00185, 2019. 10.1002/pld3.185 PubMed DOI PMC

Borisova-Mubarakshina M.M., Naydov I.A., Vetoshkina D.V. et al.: Photosynthetic antenna size regulation as an essential mechanism of higher plants acclimation to biotic and abiotic factors: The role of the chloroplast plastoquinone pool and hydrogen peroxide. – In: Carmona E.C., Ortiz A.C., Canas R.Q., Musarella C.M. (ed.): Vegetation Index and Dynamics. IntechOpen, Rijeka: 2022. 10.5772/intechopen.97664 DOI

Brugnoli E., Björkman O.: Growth of cotton under continuous salinity stress: influence on allocation pattern, stomatal and non-stomatal components of photosynthesis and dissipation of excess light energy. – Planta 187: 335-347, 1992. 10.1007/BF00195657 PubMed DOI

Chow W.S., Anderson J.M., Hope A.B.: Variable stoichiometries of photosystem II to photosystem I reaction centers. – Photosynth. Res. 17: 277-281, 1988. 10.1007/Bf00035454 PubMed DOI

Crepin A., Cunill-Semanat E., Kuthanová Trsková E. et al.: Antenna protein clustering in vitro unveiled by fluorescence correlation spectroscopy. – Int. J. Mol. Sci. 22: 2969, 2021. 10.3390/ijms22062969 PubMed DOI PMC

Dall'Osto L., Holt N.E., Kaligotla S. et al.: Zeaxanthin protects plant photosynthesis by modulating chlorophyll triplet yield in specific light-harvesting antenna subunits. – J. Biol. Chem. 287: 41820-41834, 2012. 10.1074/jbc.M112.405498 PubMed DOI PMC

Dekker J.P., Boekema E.J.: Supramolecular organization of thylakoid membrane proteins in green plants. – BBA-Bioenergetics 1706: 12-39, 2005. 10.1016/j.bbabio.2004.09.009 PubMed DOI

Dekker J.P., van Roon H., Boekema E.J.: Heptameric association of light-harvesting complex II trimers in partially solubilized photosystem II membranes. – FEBS Lett. 449: 211-214, 1999. 10.1016/s0014-5793(99)00442-1 PubMed DOI

Demmig-Adams B., Stewart J.J., López-Pozo M. et al.: Zeaxanthin, a molecule for photoprotection in many different environments. – Molecules 25: 5825, 2020. 10.3390/molecules25245825 PubMed DOI PMC

Dogutan D.K., Nocera D.G.: Artificial photosynthesis at efficiencies greatly exceeding that of natural photosynthesis. – Acc. Chem. Res. 52: 3143-3148, 2019. 10.1021/acs.accounts.9b00380 PubMed DOI

Duffy C.D.P., Ruban A.V., Barford W.: Theoretical investigation of the role of strongly coupled chlorophyll dimers in photoprotection of LHCII. – J. Phys. Chem. B 112: 12508-12515, 2008. 10.1021/jp804571k PubMed DOI

Garab G., Cseh Z., Kovács L. et al.: Light-induced trimer to monomer transition in the main light-harvesting antenna complex of plants: Thermo-optic mechanism. – Biochemistry 41: 15121-15129, 2002. 10.1021/bi026157g PubMed DOI

Gotoh E., Suetsugu N., Higa T et al.: Palisade cell shape affects the light-induced chloroplast movements and leaf photosynthesis. – Sci. Rep.-UK 8: 1472, 2018. 10.1038/s41598-018-19896-9 PubMed DOI PMC

Grinzato A., Albanese P., Marotta R. et al.: High-light versus low-light: effects on paired photosystem II supercomplex structural rearrangement in pea plants. – Int. J. Mol. Sci. 21: 8643, 2020. 10.3390/ijms21228643 PubMed DOI PMC

Gruszecki W.I.: Carotenoid orientation: role in membrane stabilization. – In: Krinsky N.I., Mayne S.T., Sies H. (ed.): Carotenoids in Health and Disease. Pp. 151-163. CRC Press, New York: 2004.

Gruszecki W.I., Gospodarek M., Grudzinski W. et al.: Light-induced change of configuration of the LHCII-bound xanthophyll (tentatively assigned to violaxanthin): a resonance Raman study. – J. Phys. Chem. B 113: 2506-2512, 2009b. 10.1021/jp8101755 PubMed DOI

Gruszecki W.I., Grudzinski W., Banaszek-Glos A. et al.: Xanthophyll pigments in light-harvesting complex II in monomolecular layers: localisation, energy transfer and orientation. – BBA-Bioenergetics 1412: 173-183, 1999a. 10.1016/S0005-2728(99)00055-9 PubMed DOI

Gruszecki W.I., Grudzinski W., Gospodarek M. et al.: Xanthophyll-induced aggregation of LHCII as a switch between light-harvesting and energy dissipation systems. – BBA-Bioenergetics 1757: 1504-1511, 2006. 10.1016/j.bbabio.2006.08.002 PubMed DOI

Gruszecki W.I., Grudzinski W., Matula M. et al.: Light-induced excitation quenching and structural transition in light-harvesting complex II. – Photosynth. Res. 59: 175-185, 1999b. 10.1023/A:1006113630174 DOI

Gruszecki W.I., Janik E., Luchowski R. et al.: Supramolecular organization of the main photosynthetic antenna complex LHCII: a monomolecular layer study. – Langmuir 25: 9384-9391, 2009a. 10.1021/la900630a PubMed DOI

Gruszecki W.I., Kernen P., Krupa Z., Strasser R.J.: Involvement of xanthophyll pigments in regulation of light-driven excitation quenching in light-harvesting complex of Photosystem II. – BBA-Bioenergetics 1188: 235-242, 1994. 10.1016/0005-2728(94)90041-8 DOI

Gruszecki W.I., Matula M., Ko-chi N. et al.: Cis-trans-isomerization of violaxanthin in LHC II: violaxanthin isomerization cycle within the violaxanthin cycle. – BBA-Bioenergetics 1319: 267-274, 1997b. 10.1016/S0005-2728(96)00167-3 DOI

Gruszecki W.I., Matula M., Mysliwa-Kurdziel B. et al.: Effect of xanthophyll pigments on fluorescence of chlorophyll a in LHC II embedded to liposomes. – J. Photoch. Photobio. B 37: 84-90, 1997a. 10.1016/S1011-1344(96)07328-9 DOI

Gruszecki W.I., Strzalka K.: Does the xanthophyll cycle take part in the regulation of fluidity of the thylakoid membrane? – BBA-Bioenergetics 1060: 310-314, 1991. 10.1016/S0005-2728(05)80322-6 DOI

Gruszecki W.I., Zelent B., Tajmir-Riahi H.-A. et al.: Chlorophyll a–violaxanthin interactions in monolayers at air–water interface and in Langmuir-Blodgett films. – Colloid. Surface. B 19: 117-125, 2000. 10.1016/S0927-7765(00)00132-6 DOI

Gruszecki W.I., Zubik M., Luchowski R. et al.: Photoprotective role of the xanthophyll cycle studied by means of modeling of xanthophyll–LHCII interactions. – Chem. Phys. 373: 122-128, 2010. 10.1016/j.chemphys.2010.03.025 DOI

Hancock A.M., Son M.J., Nairat M. et al.: Ultrafast energy transfer between lipid-linked chromophores and plant light-harvesting complex II. – Phys. Chem. Chem. Phys. 23: 19511-19524, 2021. 10.1039/d1cp01628h PubMed DOI PMC

Holm J.K., Várkonyi Z., Kovács L. et al.: Thermo-optically induced reorganizations in the main light harvesting antenna of plants. II. Indications for the role of LHCII-only macrodomains in thylakoids. – Photosynth. Res. 86: 275-282, 2005. 10.1007/s11120-005-5302-x PubMed DOI

Horton P., Ruban A.: Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection. – J. Exp. Bot. 56: 365-373, 2005. 10.1093/jxb/eri023 PubMed DOI

Janik E., Bednarska J., Sowinski K. et al.: Light-induced formation of dimeric LHCII. – Photosynth. Res. 132: 265-276, 2017a. 10.1007/s11120-017-0387-6 PubMed DOI PMC

Janik E., Bednarska J., Zubik M. et al.: Molecular architecture of plant thylakoids under physiological and light stress conditions: a study of lipid-light-harvesting complex II model membranes. – Plant Cell 25: 2155-2170, 2013. PubMed PMC

Janik E., Bednarska J., Zubik M. et al.: Is it beneficial for the major photosynthetic antenna complex of plants to form trimers? – J. Phys. Chem. B 119: 8501-8508, 2015. 10.1021/acs.jpcb.5b04005 PubMed DOI

Janik E., Bednarska J., Zubik M. et al.: The xanthophyll cycle pigments, violaxanthin and zeaxanthin, modulate molecular organization of the photosynthetic antenna complex LHCII. – Arch. Biochem. Biophys. 592: 1-9, 2016. 10.1016/j.abb.2016.01.003 PubMed DOI

Janik E., Bednarska J., Zubik M. et al.: A chloroplast “wake up” mechanism: Illumination with weak light activates the photosynthetic antenna function in dark-adapted plants. – J. Plant Physiol. 210: 1-8, 2017b. 10.1016/j.jplph.2016.12.006 PubMed DOI

Jennings R.C., Garlaschi F.M., Zucchelli G.: Light-induced fluorescence quenching in the light-harvesting chlorophyll a/b protein complex. – Photosynth. Res. 27: 57-64, 1991. 10.1007/BF00029976 PubMed DOI

Johnson M.P., Goral T.K., Duffy C.D.P. et al.: Photoprotective energy dissipation involves the reorganization of photosystem II light-harvesting complexes in the grana membranes of spinach chloroplasts. – Plant Cell 23: 1468-1479, 2011. 10.1105/tpc.110.081646 PubMed DOI PMC

Kaiser E., Galvis V.C., Armbruster U.: Efficient photosynthesis in dynamic light environments: a chloroplast's perspective. – Biochem. J. 476: 2725-2741, 2019. 10.1042/Bcj20190134 PubMed DOI PMC

Kasahara M., Kagawa T., Oikawa K. et al.: Chloroplast avoidance movement reduces photodamage in plants. – Nature 420: 829-832, 2002. 10.1038/nature01213 PubMed DOI

Kim E., Watanabe A., Duffy C.D.P. et al.: Multimeric and monomeric photosystem II supercomplexes represent structural adaptations to low- and high-light conditions. – J. Biol. Chem. 295: 14537-14545, 2020. 10.1074/jbc.RA120.014198 PubMed DOI PMC

Kirchoff H.: Molecular crowding and order in photosynthetic membranes. – Trends Plant Sci. 13: 201-207, 2008. 10.1016/j.tplants.2008.03.001 PubMed DOI

Koller D.: Light-driven leaf movements. – Plant Cell Environ. 13: 615-632, 1990. 10.1111/j.1365-3040.1990.tb01079.x DOI

Kromdijk J., Glowacka K., Leonelli L. et al.: Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. – Science 354: 857-861, 2016. 10.1126/science.aai8878 PubMed DOI

Latowski D., Kruk J., Burda K. et al.: Kinetics of violaxanthin de-epoxidation by violaxanthin de-epoxidase, a xanthophyll cycle enzyme, is regulated by membrane fluidity in model lipid bilayers. – Eur. J. Biochem. 269: 4656-4665, 2002. 10.1046/j.1432-1033.2002.03166.x PubMed DOI

Liu Z.F., Yan H.C., Wang K.B. et al.: Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. – Nature 428: 287-292, 2004. 10.1038/nature02373 PubMed DOI

Marshall H.L., Geider R.J., Flynn K.J.: A mechanistic model of photoinhibition. – New Phytol. 145: 347-359, 2000. 10.1046/j.1469-8137.2000.00575.x DOI

Miloslavina Y., Wehner A., Lambrev P.H. et al.: Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching. – FEBS Lett. 582: 3625-3631, 2008. 10.1016/j.febslet.2008.09.044 PubMed DOI

Nan G.-N., Zhou X.-Q., Zhang X.-M. et al.: Xanthophyll cycle-related non-photochemical quenching protects Sargassum thunbergii from high light-induced photoinhibition. – Front. Mar. Sci. 9: 1067596, 2022. 10.3389/fmars.2022.1067596 DOI

Natali A., Gruber J.M., Dietzel L. et al.: Light-harvesting complexes (LHCs) cluster spontaneously in membrane environment leading to shortening of their excited state lifetimes. – J. Biol. Chem. 291: 16730-16739, 2016. 10.1074/jbc.M116.730101 PubMed DOI PMC

Owens T.: Excitation energy transfer between chlorophylls and carotenoids. A proposed molecular mechanism for non-photochemical quenching. – In: Baker N.R., Bowyer J.R. (ed.): Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field. Pp. 95-110. BIOS Scientific Publishers, Oxford: 1994.

Pagliano C., Nield J., Marsano F. et al.: Proteomic characterization and three-dimensional electron microscopy study of PSII-LHCII supercomplexes from higher plants. – BBA-Bioenergetics 1837: 1454-1462, 2014. 10.1016/j.bbabio.2013.11.004 PubMed DOI

Perico C., Sparkes I.: Plant organelle dynamics: cytoskeletal control and membrane contact sites. – New Phytol. 220: 381-394, 2018. 10.1111/nph.15365 PubMed DOI

Rintamäki E., Salonen M., Suoranta U.M. et al.: Phosphorylation of light-harvesting complex II and photosystem II core proteins shows different irradiance-dependent regulation in vivo. Application of phosphothreonine antibodies to analysis of thylakoid phosphoproteins. – J. Biol. Chem. 272: 30476-30482, 1997. 10.1074/jbc.272.48.30476 PubMed DOI

Ruban A.V.: Plants in light. – Commun. Integr. Biol. 2: 50-55, 2009. 10.4161/cib.2.1.7504 PubMed DOI PMC

Ruban A.V.: Crops on the fast track for light. – Nature 541: 36-37, 2017. 10.1038/541036a PubMed DOI

Ruban A.V., Calkoen F., Kwa S.L.S. et al.: Characterisation of LHC II in aggregated state by linear and circular dichroism spectroscopy. – BBA-Bioenergetics 1321: 61-70, 1997. 10.1016/S0005-2728(97)00047-9 DOI

Ruban A.V., Horton P.: The xanthophyll cycle modulates the kinetics of nonphotochemical energy dissipation in isolated light-harvesting complexes, intact chloroplasts, and leaves of spinach. – Plant Physiol. 119: 531-542, 1999. 10.1104/pp.119.2.531 PubMed DOI PMC

Ruban A.V., Horton P., Robert B.: Resonance Raman spectroscopy of the photosystem II light-harvesting complex of green plants: a comparison of trimeric and aggregated states. – Biochemistry 34: 2333-2337, 1995. 10.1021/bi00007a029 PubMed DOI

Ruban A.V., Johnson M.P., Duffy C.D.P.: The photoprotective molecular switch in the photosystem II antenna. – BBA-Bioenergetics 1817: 167-181, 2012. 10.1016/j.bbabio.2011.04.007 PubMed DOI

Ruban A.V., Pascal A., Lee P.J. et al.: Molecular configuration of xanthophyll cycle carotenoids in photosystem II antenna complexes. – J. Biol. Chem. 277: 42937-42942, 2002. 10.1074/jbc.M207823200 PubMed DOI

Sapozhnikov D.I.T., Kransovskaya T.A., Maevskaya A.N.: [Change in the interrelationship of the basic carotenoids of the plastids of green leaves under the action of light.] – Dokl. Akad. Nauk SSSR 113: 465-467, 1957. [In Russian: ]

Son M., Moya R., Pinnola A. et al.: Protein–protein interactions induce pH-dependent and zeaxanthin-independent photoprotection in the plant light-harvesting complex, LHCII. – J. Am. Chem. Soc. 143: 17577-17586, 2021. 10.1021/jacs.1c07385 PubMed DOI

Standfuss R., Terwisscha van Scheltinga A.C., Lamborghini M., Kühlbrandt W.: Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 Å resolution. – EMBO J. 24: 919-928, 2005. 10.1038/sj.emboj.7600585 PubMed DOI PMC

Su X.D., Ma J., Wei X.P. et al.: Structure and assembly mechanism of plant C2S2M2-type PSII-LHCII supercomplex. – Science 357: 815-820, 2017. 10.1126/science.aan0327 PubMed DOI

Tikkanen M., Aro E.-M.: Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants. – BBA-Bioenergetics 1817: 232-238, 2012. 10.1016/j.bbabio.2011.05.005 PubMed DOI

Trauner D.: Richard Willstatter and the 1915 Nobel Prize in Chemistry. – Angew. Chem. Int. Ed. 54: 11910-11916, 2015. 10.1002/anie.201505507 PubMed DOI

Wada M., Kong S.-G.: Actin-mediated movement of chloroplasts. – J. Cell Sci. 131: jcs210310, 2018. 10.1242/jcs.210310 PubMed DOI

Welc R., Luchowski R., Grudzinski W. et al.: A key role of xanthophylls that are not embedded in proteins in regulation of the photosynthetic antenna function in plants, revealed by monomolecular layer studies. – J. Phys. Chem. B 120: 13056-13064, 2016. 10.1021/acs.jpcb.6b10393 PubMed DOI

Welc R., Luchowski R., Kluczyk D. et al.: Mechanisms shaping the synergism of zeaxanthin and PsbS in photoprotective energy dissipation in the photosynthetic apparatus of plants. – Plant J. 107: 418-433, 2021. 10.1111/tpj.15297 PubMed DOI

Willstätter R., Stoll A.: Untersuchungen über Chlorophyll: Methoden und Ergebnisse. Pp. 424. Springer, Berlin-Heidelberg: 1913. [In German] 10.1007/978-3-642-49665-3 DOI

Wood W.H.J., Johnson M.P.: Modeling the role of LHCII-LHCII, PSII-LHCII, and PSI-LHCII interactions in state transitions. – Biophys. J. 119: 287-299, 2020. 10.1016/j.bpj.2020.05.034 PubMed DOI PMC

Woodward R.B., Ayer W.A., Beaton J.M. et al.: The total synthesis of chlorophyll. – J. Am. Chem. Soc. 82: 3800-3802, 1960. 10.1021/ja01499a093 DOI

Wu G.X., Ma L., Sayre R.T., Lee C.-H.: Identification of the optimal light harvesting antenna size for high-light stress mitigation in plants. – Front. Plant Sci. 11: 505, 2020. 10.3389/fpls.2020.00505 PubMed DOI PMC

Xu P.Q., Tian L.J., Kloz M., Croce R.: Molecular insights into zeaxanthin-dependent quenching in higher plants. – Sci. Rep.-UK 5: 13679, 2015. 10.1038/srep13679 PubMed DOI PMC

Yamamoto H.Y., Nakayama T.O.M., Chichester C.O.: Studies on the light and dark interconversion of leaf xanthophylls. – Arch. Biochem. Biophys. 97: 168-173, 1962. 10.1016/0003-9861(62)90060-7 PubMed DOI

Zhou J.T., Sekatskii S., Welc R. et al.: The role of xanthophylls in the supramolecular organization of the photosynthetic complex LHCII in lipid membranes studied by high-resolution imaging and nanospectroscopy. – BBA-Bioenergetics 1861: 148117, 2020. 10.1016/j.bbabio.2019.148117 PubMed DOI

Zubik M., Luchowski R., Kluczyk D. et al.: Recycling of energy dissipated as heat accounts for high activity of photosystem II. – J. Phys. Chem. Lett. 11: 3242-3248, 2020. PubMed PMC

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...