Two mechanisms for dissipation of excess light in monomeric and trimeric light-harvesting complexes
Abstract
Oxygenic photoautotrophs require mechanisms for rapidly matching the level of chlorophyll excited states from light harvesting with the rate of electron transport from water to carbon dioxide. These photoprotective reactions prevent formation of reactive excited states and photoinhibition. The fastest response to excess illumination is the so-called non-photochemical quenching which, in higher plants, requires the luminal pH sensor PsbS and other yet unidentified components of the photosystem II antenna. Both trimeric light-harvesting complex II (LHCII) and monomeric LHC proteins have been indicated as site(s) of the heat-dissipative reactions. Different mechanisms have been proposed: Energy transfer to a lutein quencher in trimers, formation of a zeaxanthin radical cation in monomers. Here, we report on the construction of a mutant lacking all monomeric LHC proteins but retaining LHCII trimers. Its non-photochemical quenching induction rate was substantially slower with respect to the wild type. A carotenoid radical cation signal was detected in the wild type, although it was lost in the mutant. Here, we conclude that non-photochemical quenching is catalysed by two independent mechanisms, with the fastest activated response catalysed within monomeric LHC proteins depending on both zeaxanthin and lutein and on the formation of a radical cation. Trimeric LHCII was responsible formore »
- Authors:
-
- Univ. di Verona, Verona (Italy). Dipartimento di Biotecnologie
- Lund Univ. (Sweden). Dept. of Chemical Physics
- Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Inst., Dept. of Plant and Microbial Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division; Univ. of California, Berkeley, CA (United States). Dept. of Chemistry, Graduate Group in Applied Science and Technology
- Univ. di Verona, Verona (Italy). Dipartimento di Biotecnologie; Consiglio Nazionale delle Ricerche (CNR), Firenze (Italy). Istituto per la Protezione delle Piante (IPP)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
- OSTI Identifier:
- 1393220
- DOE Contract Number:
- AC02-05CH11231
- Resource Type:
- Journal Article
- Journal Name:
- Nature Plants
- Additional Journal Information:
- Journal Volume: 3; Journal Issue: 5; Journal ID: ISSN 2055-0278
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- Antenna complex; Non-photochemical quenching
Citation Formats
Dall'Osto, Luca, Cazzaniga, Stefano, Bressan, Mauro, Paleček, David, Židek, Karel, Niyogi, Krishna K., Fleming, Graham R., Zigmantas, Donatas, and Bassi, Roberto. Two mechanisms for dissipation of excess light in monomeric and trimeric light-harvesting complexes. United States: N. p., 2017.
Web. doi:10.1038/nplants.2017.33.
Dall'Osto, Luca, Cazzaniga, Stefano, Bressan, Mauro, Paleček, David, Židek, Karel, Niyogi, Krishna K., Fleming, Graham R., Zigmantas, Donatas, & Bassi, Roberto. Two mechanisms for dissipation of excess light in monomeric and trimeric light-harvesting complexes. United States. doi:10.1038/nplants.2017.33.
Dall'Osto, Luca, Cazzaniga, Stefano, Bressan, Mauro, Paleček, David, Židek, Karel, Niyogi, Krishna K., Fleming, Graham R., Zigmantas, Donatas, and Bassi, Roberto. Mon .
"Two mechanisms for dissipation of excess light in monomeric and trimeric light-harvesting complexes". United States. doi:10.1038/nplants.2017.33.
@article{osti_1393220,
title = {Two mechanisms for dissipation of excess light in monomeric and trimeric light-harvesting complexes},
author = {Dall'Osto, Luca and Cazzaniga, Stefano and Bressan, Mauro and Paleček, David and Židek, Karel and Niyogi, Krishna K. and Fleming, Graham R. and Zigmantas, Donatas and Bassi, Roberto},
abstractNote = {Oxygenic photoautotrophs require mechanisms for rapidly matching the level of chlorophyll excited states from light harvesting with the rate of electron transport from water to carbon dioxide. These photoprotective reactions prevent formation of reactive excited states and photoinhibition. The fastest response to excess illumination is the so-called non-photochemical quenching which, in higher plants, requires the luminal pH sensor PsbS and other yet unidentified components of the photosystem II antenna. Both trimeric light-harvesting complex II (LHCII) and monomeric LHC proteins have been indicated as site(s) of the heat-dissipative reactions. Different mechanisms have been proposed: Energy transfer to a lutein quencher in trimers, formation of a zeaxanthin radical cation in monomers. Here, we report on the construction of a mutant lacking all monomeric LHC proteins but retaining LHCII trimers. Its non-photochemical quenching induction rate was substantially slower with respect to the wild type. A carotenoid radical cation signal was detected in the wild type, although it was lost in the mutant. Here, we conclude that non-photochemical quenching is catalysed by two independent mechanisms, with the fastest activated response catalysed within monomeric LHC proteins depending on both zeaxanthin and lutein and on the formation of a radical cation. Trimeric LHCII was responsible for the slowly activated quenching component whereas inclusion in supercomplexes was not required. Finally, this latter activity does not depend on lutein nor on charge transfer events, whereas zeaxanthin was essential.},
doi = {10.1038/nplants.2017.33},
journal = {Nature Plants},
issn = {2055-0278},
number = 5,
volume = 3,
place = {United States},
year = {2017},
month = {4}
}
Works referenced in this record:
Light-induced Dissociation of an Antenna Hetero-oligomer Is Needed for Non-photochemical Quenching Induction
journal, March 2009
- Betterle, Nico; Ballottari, Matteo; Zorzan, Simone
- Journal of Biological Chemistry, Vol. 284, Issue 22
Structure of spinach photosystem II–LHCII supercomplex at 3.2 Å resolution
journal, May 2016
- Wei, Xuepeng; Su, Xiaodong; Cao, Peng
- Nature, Vol. 534, Issue 7605
Biochemical Properties of the PsbS Subunit of Photosystem II Either Purified from Chloroplast or Recombinant
journal, April 2002
- Dominici, Paola; Caffarri, Stefano; Armenante, Franca
- Journal of Biological Chemistry, Vol. 277, Issue 25
Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa
journal, November 1987
- Schägger, Hermann; von Jagow, Gebhard
- Analytical Biochemistry, Vol. 166, Issue 2
Higher Plant Photosystem II Light-Harvesting Antenna, Not the Reaction Center, Determines the Excited-State Lifetime—Both the Maximum and the Nonphotochemically Quenched
journal, June 2012
- Belgio, Erica; Johnson, Matthew P.; Jurić, Snježana
- Biophysical Journal, Vol. 102, Issue 12
Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants
journal, October 1998
- Pogson, B. J.; Niyogi, K. K.; Bjorkman, O.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 22
Regulation of Photosynthetic Light Harvesting Involves Intrathylakoid Lumen pH Sensing by the PsbS Protein
journal, March 2004
- Li, Xiao-Ping; Gilmore, Adam M.; Caffarri, Stefano
- Journal of Biological Chemistry, Vol. 279, Issue 22
High-light vs. low-light: Effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana
journal, March 2013
- Kouřil, Roman; Wientjes, Emilie; Bultema, Jelle B.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 3
Far-red fluorescence: A direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching
journal, October 2008
- Miloslavina, Yuliya; Wehner, Antje; Lambrev, Petar H.
- FEBS Letters, Vol. 582, Issue 25-26
Crystal structures of the PsbS protein essential for photoprotection in plants
journal, August 2015
- Fan, Minrui; Li, Mei; Liu, Zhenfeng
- Nature Structural & Molecular Biology, Vol. 22, Issue 9
Regulation of plant light harvesting by thermal dissipation of excess energy
journal, March 2010
- de Bianchi, Silvia; Ballottari, Matteo; Dall’Osto, Luca
- Biochemical Society Transactions, Vol. 38, Issue 2
Regulation of Light Harvesting in Green Plants
journal, June 1996
- Horton, P.; Ruban, A. V.; Walters, R. G.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 47, Issue 1
Carotenoid Cation Formation and the Regulation of Photosynthetic Light Harvesting
journal, January 2005
- Holt, N. E.
- Science, Vol. 307, Issue 5708
A pigment-binding protein essential for regulation of photosynthetic light harvesting
journal, January 2000
- Li, Xiao-Ping; Björkman, Olle; Shih, Connie
- Nature, Vol. 403, Issue 6768
Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution
journal, March 2004
- Liu, Zhenfeng; Yan, Hanchi; Wang, Kebin
- Nature, Vol. 428, Issue 6980
Architecture of a Charge-Transfer State Regulating Light Harvesting in a Plant Antenna Protein
journal, May 2008
- Ahn, T. K.; Avenson, T. J.; Ballottari, M.
- Science, Vol. 320, Issue 5877
Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studied by time-resolved fluorescence
journal, December 2009
- Holzwarth, Alfred R.; Miloslavina, Yuliya; Nilkens, Manuela
- Chemical Physics Letters, Vol. 483, Issue 4-6
Direct interaction of the major light-harvesting complex II and PsbS in nonphotochemical quenching
journal, March 2013
- Wilk, L.; Grunwald, M.; Liao, P. -N.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 14
On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls
journal, July 2009
- Bode, S.; Quentmeier, C. C.; Liao, P. -N.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 30
Isolation of monomeric photosystem II that retains the subunit PsbS
journal, August 2013
- Haniewicz, Patrycja; De Sanctis, Daniele; Büchel, Claudia
- Photosynthesis Research, Vol. 118, Issue 3
Two-dimensional electronic spectroscopy with double modulation lock-in detection: enhancement of sensitivity and noise resistance
journal, January 2011
- Augulis, Ramūnas; Zigmantas, Donatas
- Optics Express, Vol. 19, Issue 14
Crystal structure of plant light-harvesting complex shows the active, energy-transmitting state
journal, January 2009
- Barros, Tiago; Royant, Antoine; Standfuss, Jörg
- The EMBO Journal, Vol. 28, Issue 3
Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses
journal, November 2014
- Suga, Michihiro; Akita, Fusamichi; Hirata, Kunio
- Nature, Vol. 517, Issue 7532
Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis
journal, June 2013
- Niyogi, Krishna K.; Truong, Thuy B.
- Current Opinion in Plant Biology, Vol. 16, Issue 3
Identification of a mechanism of photoprotective energy dissipation in higher plants
journal, November 2007
- Ruban, Alexander V.; Berera, Rudi; Ilioaia, Cristian
- Nature, Vol. 450, Issue 7169
Arabidopsis Mutants Define a Central Role for the Xanthophyll Cycle in the Regulation of Photosynthetic Energy Conversion
journal, July 1998
- Niyogi, Krishna K.; Grossman, Arthur R.; Björkman, Olle
- The Plant Cell, Vol. 10, Issue 7
Interaction between avoidance of photon absorption, excess energy dissipation and zeaxanthin synthesis against photooxidative stress in Arabidopsis
journal, October 2013
- Cazzaniga, Stefano; Dall' Osto, Luca; Kong, Sam-Geun
- The Plant Journal, Vol. 76, Issue 4
A guide to the Lhc genes and their relatives in Arabidopsis
journal, June 1999
- Jansson, S.
- Trends in Plant Science, Vol. 4, Issue 6
Reversible and irreversible intermediates during photoinhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation.
journal, February 1992
- Vass, I.; Styring, S.; Hundal, T.
- Proceedings of the National Academy of Sciences, Vol. 89, Issue 4
The Light-Harvesting Chlorophyll a/b Binding Proteins Lhcb1 and Lhcb2 Play Complementary Roles during State Transitions in Arabidopsis
journal, September 2014
- Pietrzykowska, M.; Suorsa, M.; Semchonok, D. A.
- The Plant Cell, Vol. 26, Issue 9
The Major Antenna Complex of Photosystem II Has a Xanthophyll Binding Site Not Involved in Light Harvesting
journal, July 2001
- Caffarri, Stefano; Croce, Roberta; Breton, Jacques
- Journal of Biological Chemistry, Vol. 276, Issue 38
Singlet Energy Dissipation in the Photosystem II Light-Harvesting Complex Does Not Involve Energy Transfer to Carotenoids
journal, April 2010
- Müller, Marc G.; Lambrev, Petar; Reus, Michael
- ChemPhysChem, Vol. 11, Issue 6
Lutein Can Act as a Switchable Charge Transfer Quencher in the CP26 Light-harvesting Complex
journal, November 2008
- Avenson, Thomas J.; Ahn, Tae Kyu; Niyogi, Krishna K.
- Journal of Biological Chemistry, Vol. 284, Issue 5
The molecular mechanism of the control of excitation energy dissipation in chloroplast membranes Inhibition of ΔpH-dependent quenching of chlorophyll fluorescence by dicyclohexylcarbodiimide
journal, September 1992
- Ruban, A. V.; Walters, R. G.; Horton, P.
- FEBS Letters, Vol. 309, Issue 2
Zeaxanthin Radical Cation Formation in Minor Light-harvesting Complexes of Higher Plant Antenna
journal, November 2007
- Avenson, Thomas J.; Ahn, Tae Kyu; Zigmantas, Donatas
- Journal of Biological Chemistry, Vol. 283, Issue 6
Kinetic and Spectral Resolution of Multiple Nonphotochemical Quenching Components in Arabidopsis Leaves
journal, December 2009
- Lambrev, Petar H.; Nilkens, Manuela; Miloslavina, Yuliya
- Plant Physiology, Vol. 152, Issue 3
Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo
journal, June 2008
- Baker, Neil R.
- Annual Review of Plant Biology, Vol. 59, Issue 1
Identification of proton-active residues in a higher plant light-harvesting complex
journal, November 1996
- Walters, R. G.; Ruban, A. V.; Horton, P.
- Proceedings of the National Academy of Sciences, Vol. 93, Issue 24
Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis
journal, April 2010
- Nilkens, Manuela; Kress, Eugen; Lambrev, Petar
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 4
Lutein Accumulation in the Absence of Zeaxanthin Restores Nonphotochemical Quenching in the Arabidopsis thaliana npq1 Mutant
journal, June 2009
- Li, Zhirong; Ahn, Tae Kyu; Avenson, Thomas J.
- The Plant Cell, Vol. 21, Issue 6