PsbS‐dependent and ‐independent mechanisms regulate carotenoid‐chlorophyll energy coupling in grana thylakoids
Abstract
In higher plants, PsbS is known to play a key role in the regulation of photosynthetic light harvesting. However, the molecular mechanism and role of electronic carotenoid–chlorophyll (Chl) interactions for the downregulation of excess excitation (nonphotochemical energy quenching, NPQ) are still poorly understood. Here, we explored carotenoid → Chl energy transfer in isolated grana thylakoid membranes from mutants either deficient in or overexpressing PsbS. Since it was suggested that PsbS regulates the supramolecular protein network to control NPQ, we varied this network by diluting the grana protein densities. Our results indicate that different electronic quenching mechanisms are operative in grana thylakoids: a PsbS-dependent mechanism and a membrane protein density-dependent mechanism that is also operative in the absence of PsbS.
- Authors:
-
[1];
[2];
- Department of Biophysical Chemistry Institute for Physical and Theoretical Chemistry Technische Universität Braunschweig Germany
- Institute of Biological Chemistry Washington State University Pullman WA USA, DOE Plant Research Laboratory Michigan State University East Lansing MI USA
- Institute of Biological Chemistry Washington State University Pullman WA USA
- Publication Date:
- Research Org.:
- Washington State Univ., Pullman, WA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); USDA
- OSTI Identifier:
- 1560742
- Alternate Identifier(s):
- OSTI ID: 1560744; OSTI ID: 1735371; OSTI ID: 1735372
- Grant/Contract Number:
- SC0017160
- Resource Type:
- Published Article
- Journal Name:
- FEBS Letters
- Additional Journal Information:
- Journal Name: FEBS Letters Journal Volume: 593 Journal Issue: 22; Journal ID: ISSN 0014-5793
- Publisher:
- Federation of European Biochemical Societies
- Country of Publication:
- Netherlands
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; carotenoid–chlorophyll interactions; electronic coupling; grana thylakoid; photosynthetic regulation; PsbS
Citation Formats
Gacek, Daniel A., Holleboom, Christoph‐Peter, Tietz, Stefanie, Kirchhoff, Helmut, and Walla, Peter Jomo. PsbS‐dependent and ‐independent mechanisms regulate carotenoid‐chlorophyll energy coupling in grana thylakoids. Netherlands: N. p., 2019.
Web. doi:10.1002/1873-3468.13586.
Gacek, Daniel A., Holleboom, Christoph‐Peter, Tietz, Stefanie, Kirchhoff, Helmut, & Walla, Peter Jomo. PsbS‐dependent and ‐independent mechanisms regulate carotenoid‐chlorophyll energy coupling in grana thylakoids. Netherlands. https://doi.org/10.1002/1873-3468.13586
Gacek, Daniel A., Holleboom, Christoph‐Peter, Tietz, Stefanie, Kirchhoff, Helmut, and Walla, Peter Jomo. Sun .
"PsbS‐dependent and ‐independent mechanisms regulate carotenoid‐chlorophyll energy coupling in grana thylakoids". Netherlands. https://doi.org/10.1002/1873-3468.13586.
@article{osti_1560742,
title = {PsbS‐dependent and ‐independent mechanisms regulate carotenoid‐chlorophyll energy coupling in grana thylakoids},
author = {Gacek, Daniel A. and Holleboom, Christoph‐Peter and Tietz, Stefanie and Kirchhoff, Helmut and Walla, Peter Jomo},
abstractNote = {In higher plants, PsbS is known to play a key role in the regulation of photosynthetic light harvesting. However, the molecular mechanism and role of electronic carotenoid–chlorophyll (Chl) interactions for the downregulation of excess excitation (nonphotochemical energy quenching, NPQ) are still poorly understood. Here, we explored carotenoid → Chl energy transfer in isolated grana thylakoid membranes from mutants either deficient in or overexpressing PsbS. Since it was suggested that PsbS regulates the supramolecular protein network to control NPQ, we varied this network by diluting the grana protein densities. Our results indicate that different electronic quenching mechanisms are operative in grana thylakoids: a PsbS-dependent mechanism and a membrane protein density-dependent mechanism that is also operative in the absence of PsbS.},
doi = {10.1002/1873-3468.13586},
journal = {FEBS Letters},
number = 22,
volume = 593,
place = {Netherlands},
year = {Sun Sep 08 00:00:00 EDT 2019},
month = {Sun Sep 08 00:00:00 EDT 2019}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1002/1873-3468.13586
https://doi.org/10.1002/1873-3468.13586
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 3 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
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
Light‐harvesting antenna composition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis
journal, October 2011
- Goral, Tomasz K.; Johnson, Matthew P.; Duffy, Christopher D. P.
- The Plant Journal, Vol. 69, Issue 2
Composition, architecture and dynamics of the photosynthetic apparatus in higher plants: The photosynthetic apparatus in higher plants
journal, March 2012
- Nevo, Reinat; Charuvi, Dana; Tsabari, Onie
- The Plant Journal, Vol. 70, Issue 1
Toward an Understanding of the Mechanism of Nonphotochemical Quenching in Green Plants †
journal, July 2004
- Holt, Nancy E.; Fleming, Graham R.; Niyogi, Krishna K.
- Biochemistry, Vol. 43, Issue 26
A Hidden State in Light-Harvesting Complex II Revealed By Multipulse Spectroscopy
journal, April 2015
- van Oort, Bart; van Grondelle, Rienk; van Stokkum, Ivo H. M.
- The Journal of Physical Chemistry B, Vol. 119, Issue 16
Photosystem II Subunit PsbS Is Involved in the Induction of LHCSR Protein-dependent Energy Dissipation in Chlamydomonas reinhardtii
journal, June 2016
- Correa-Galvis, Viviana; Redekop, Petra; Guan, Katharine
- Journal of Biological Chemistry, Vol. 291, Issue 33
The PsbS Protein Controls the Organization of the Photosystem II Antenna in Higher Plant Thylakoid Membranes
journal, November 2007
- Kiss, Anett Z.; Ruban, Alexander V.; Horton, Peter
- Journal of Biological Chemistry, Vol. 283, Issue 7
Kinetic Modeling of Charge-Transfer Quenching in the CP29 Minor Complex
journal, October 2008
- Cheng, Yuan-Chung; Ahn, Tae Kyu; Avenson, Thomas J.
- The Journal of Physical Chemistry B, Vol. 112, Issue 42
Supermolecular structure of photosystem II and location of the PsbS protein
journal, October 2000
- Nield, Jon; Funk, Christiane; Barber, James
- Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 355, Issue 1402
Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis
journal, September 1994
- Frank, Harry A.; Cua, Agnes; Chynwat, Veeradej
- Photosynthesis Research, Vol. 41, Issue 3
Light harvesting control in plants
journal, June 2018
- Ruban, Alexander V.
- FEBS Letters, Vol. 592, Issue 18
Understanding the Energy Transfer Function of LHCII, the Major Light-Harvesting Complex of Green Plants †
journal, January 2001
- van Amerongen, Herbert; van Grondelle, Rienk
- The Journal of Physical Chemistry B, Vol. 105, Issue 3
PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition
journal, November 2002
- Li, X. -P.; Muller-Moule, P.; Gilmore, A. M.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 23
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
Chlorophyll Fluorescence and Photosynthesis: The Basics
journal, June 1991
- Krause, G. H.; Weis, E.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 42, Issue 1
Two-Photon Study on the Electronic Interactions between the First Excited Singlet States in Carotenoid−Tetrapyrrole Dyads
journal, April 2011
- Liao, Pen-Nan; Pillai, Smitha; Gust, Devens
- The Journal of Physical Chemistry A, Vol. 115, Issue 16
A quantitative model of the domain structure of the photosynthetic membrane
journal, August 2001
- Albertsson, Per-Åke
- Trends in Plant Science, Vol. 6, Issue 8
Aggregation and fluorescence quenching of chlorophyll a of the light-harvesting complex II from spinach in vitro
journal, September 2003
- Kirchhoff, Helmut; Hinz, Hans-Jürgen; Rösgen, Jörg
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1606, Issue 1-3
Correlation of Car S 1 → Chl with Chl → Car S 1 Energy Transfer Supports the Excitonic Model in Quenched Light Harvesting Complex II
journal, December 2010
- Liao, Pen-Nan; Holleboom, Christoph-Peter; Wilk, Laura
- The Journal of Physical Chemistry B, Vol. 114, Issue 47
Two mechanisms for dissipation of excess light in monomeric and trimeric light-harvesting complexes
journal, April 2017
- Dall'Osto, Luca; Cazzaniga, Stefano; Bressan, Mauro
- Nature Plants, Vol. 3, Issue 5
On the role of excitonic interactions in carotenoid–phthalocyanine dyads and implications for photosynthetic regulation
journal, September 2011
- Liao, Pen-Nan; Pillai, Smitha; Kloz, Miroslav
- Photosynthesis Research, Vol. 111, Issue 1-2
Two-Photon Spectra of Chlorophylls and Carotenoid–Tetrapyrrole Dyads
journal, October 2017
- Gacek, Daniel A.; Moore, Ana L.; Moore, Thomas A.
- The Journal of Physical Chemistry B, Vol. 121, Issue 43
Efficient Light Harvesting by Photosystem II Requires an Optimized Protein Packing Density in Grana Thylakoids
journal, April 2010
- Haferkamp, Silvia; Haase, Winfried; Pascal, Andrew A.
- Journal of Biological Chemistry, Vol. 285, Issue 22
Carotenoid–chlorophyll coupling and fluorescence quenching in aggregated minor PSII proteins CP24 and CP29
journal, March 2015
- Holleboom, Christoph-Peter; Gacek, Daniel Alexander; Liao, Pen-Nan
- Photosynthesis Research, Vol. 124, Issue 2
Photoprotection in Plants Involves a Change in Lutein 1 Binding Domain in the Major Light-harvesting Complex of Photosystem II
journal, June 2011
- Ilioaia, Cristian; Johnson, Matthew P.; Liao, Pen-Nan
- Journal of Biological Chemistry, Vol. 286, Issue 31
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
The back and forth of energy transfer between carotenoids and chlorophylls and its role in the regulation of light harvesting
journal, April 2013
- Holleboom, Christoph-Peter; Walla, Peter J.
- Photosynthesis Research, Vol. 119, Issue 1-2
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–Chlorophyll Coupling and Fluorescence Quenching Correlate with Protein Packing Density in Grana-Thylakoids
journal, March 2013
- Holleboom, Christoph-Peter; Yoo, Sunny; Liao, Pen-Nan
- The Journal of Physical Chemistry B, Vol. 117, Issue 38
Carotenoid Cation Formation and the Regulation of Photosynthetic Light Harvesting
journal, January 2005
- Holt, N. E.
- Science, Vol. 307, Issue 5708
A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes: EPR and electron-transport properties
journal, November 1981
- Berthold, Deborah A.; Babcock, Gerald T.; Yocum, Charles F.
- FEBS Letters, Vol. 134, Issue 2
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
Chloroplast structure: from chlorophyll granules to supra-molecular architecture of thylakoid membranes
journal, January 2003
- Staehelin, L. Andrew
- Photosynthesis Research, Vol. 76, Issue 1/3, p. 185-196
The PsbS protein controls the macro-organisation of photosystem II complexes in the grana membranes of higher plant chloroplasts
journal, December 2009
- Kereïche, Sami; Kiss, Anett Z.; Kouřil, Roman
- FEBS Letters, Vol. 584, Issue 4
Sensing and Responding to Excess Light
journal, June 2009
- Li, Zhirong; Wakao, Setsuko; Fischer, Beat B.
- Annual Review of Plant Biology, Vol. 60, Issue 1
Nonphotochemical Chlorophyll Fluorescence Quenching: Mechanism and Effectiveness in Protecting Plants from Photodamage
journal, February 2016
- Ruban, Alexander V.
- Plant Physiology, Vol. 170, Issue 4
Modeling of Fluorescence Quenching by Lutein in the Plant Light-Harvesting Complex LHCII
journal, December 2012
- Duffy, C. D. P.; Chmeliov, J.; Macernis, M.
- The Journal of Physical Chemistry B, Vol. 117, Issue 38
Time-resolved two-photon spectroscopy of carotenoids
journal, June 2019
- Šebelík, Václav; Fuciman, Marcel; West, Robert G.
- Chemical Physics, Vol. 522
Antioxidants in Photosynthesis and Human Nutrition
journal, December 2002
- Demmig-Adams, B.
- Science, Vol. 298, Issue 5601
The role of xanthophyll cycle carotenoids in the protection of photosynthesis
journal, January 1996
- Demmig-Adams, Barbara; Adams, William W.
- Trends in Plant Science, Vol. 1, Issue 1
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