Energy-dependent quenching adjusts the excitation diffusion length to regulate photosynthetic light harvesting

Bennett, Doran I. G.; Fleming, Graham R.; Amarnath, Kapil

doi:10.1073/pnas.1806597115

Title: Energy-dependent quenching adjusts the excitation diffusion length to regulate photosynthetic light harvesting

Journal Article · Thu Sep 20 00:00:00 EDT 2018 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1806597115· OSTI ID:1471771

Bennett, Doran I. G.;

; Amarnath, Kapil

An important determinant of crop yields is the regulation of photosystem II (PSII) light harvesting by energy-dependent quenching (qE). However, the molecular details of excitation quenching have not been quantitatively connected to the fraction of excitations converted to chemical energy by PSII reaction centers (PSII yield), which determines flux to downstream metabolism. Here, we incorporate excitation dissipation by qE into a pigment-scale model of excitation transfer and trapping for a 200 × 200-nm patch of the grana membrane. We show that excitation transport can be rigorously coarse grained to a 2D random walk with an excitation diffusion length determined by the extent of quenching. We present an alternative method for analyzing pulse amplitude-modulated chlorophyll fluorescence measurements that incorporates the effects of a variable excitation diffusion length during qE activation.

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Research Organization:: Energy Frontier Research Centers (EFRC) (United States). Center for Excitonics (CE); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-05CH11231; SC0001088

OSTI ID:: 1471771

Alternate ID(s):: OSTI ID: 1490703

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 115 Journal Issue: 41; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 30 works

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References (45)

In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase Kanazawa, A.; Kramer, D. M. Proceedings of the National Academy of Sciences, Vol. 99, Issue 20 https://doi.org/10.1073/pnas.182427499	journal	August 2002
Dynamic quenching in single photosystem II supercomplexes Gruber, J. Michael; Xu, Pengqi; Chmeliov, Jevgenij Physical Chemistry Chemical Physics, Vol. 18, Issue 37 https://doi.org/10.1039/C6CP05493E	journal	January 2016
Intra- and inter-monomeric transfers in the light harvesting LHCII complex: the Redfield–Förster picture Novoderezhkin, Vladimir; Marin, Alessandro; van Grondelle, Rienk Physical Chemistry Chemical Physics, Vol. 13, Issue 38 https://doi.org/10.1039/c1cp21079c	journal	January 2011
New Fluorescence Parameters for the Determination of Q _A Redox State and Excitation Energy Fluxes Kramer, David M.; Johnson, Giles; Kiirats, Olavi Photosynthesis Research, Vol. 79, Issue 2 https://doi.org/10.1023/B:PRES.0000015391.99477.0d	journal	January 2004
Long-range energy transport in photosystem II Roden, Jan J. J.; Bennett, Doran I. G.; Whaley, K. Birgitta The Journal of Chemical Physics, Vol. 144, Issue 24 https://doi.org/10.1063/1.4953243	journal	June 2016
Enhanced thylakoid photoprotection can increase yield and canopy radiation use efficiency in rice Hubbart, Stella; Smillie, Ian R. A.; Heatley, Matthew Communications Biology, Vol. 1, Issue 1 https://doi.org/10.1038/s42003-018-0026-6	journal	March 2018
Characterizing non-photochemical quenching in leaves through fluorescence lifetime snapshots Sylak-Glassman, Emily J.; Zaks, Julia; Amarnath, Kapil Photosynthesis Research, Vol. 127, Issue 1 https://doi.org/10.1007/s11120-015-0104-2	journal	March 2015
Use of a Pulse-Amplitude Modulated Chlorophyll Fluorometer to Study the Efficiency of Photosynthesis in Arabidopsis Plants Brooks, Matthew D.; Niyogi, Krishna K. Chloroplast Research in Arabidopsis https://doi.org/10.1007/978-1-61779-237-3_16	book	January 2011
Coexistence of Fluid and Crystalline Phases of Proteins in Photosynthetic Membranes Schneider, Anna R.; Geissler, Phillip L. Biophysical Journal, Vol. 105, Issue 5 https://doi.org/10.1016/j.bpj.2013.06.052	journal	September 2013
Cooperative singlet and triplet exciton transport in tetracene crystals visualized by ultrafast microscopy Wan, Yan; Guo, Zhi; Zhu, Tong Nature Chemistry, Vol. 7, Issue 10 https://doi.org/10.1038/nchem.2348	journal	September 2015
Controlled Disorder in Plant Light-Harvesting Complex II Explains Its Photoprotective Role Krüger, Tjaart P. J.; Ilioaia, Cristian; Johnson, Matthew P. Biophysical Journal, Vol. 102, Issue 11 https://doi.org/10.1016/j.bpj.2012.04.044	journal	June 2012
Excitonic connectivity between photosystem II units: what is it, and how to measure it? Stirbet, Alexandrina Photosynthesis Research, Vol. 116, Issue 2-3 https://doi.org/10.1007/s11120-013-9863-9	journal	June 2013
Symmetry-Breaking Charge Transfer in Boron Dipyridylmethene (DIPYR) Dimers Golden, Jessica H.; Estergreen, Laura; Porter, Tyler ACS Applied Energy Materials, Vol. 1, Issue 3 https://doi.org/10.1021/acsaem.7b00214	journal	February 2018
Theory on Rates of Excitation-Energy Transfer between Molecular Aggregates through Distributed Transition Dipoles with Application to the Antenna System in Bacterial Photosynthesis Sumi, Hitoshi The Journal of Physical Chemistry B, Vol. 103, Issue 1 https://doi.org/10.1021/jp983477u	journal	January 1999
PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition Li, X. -P.; Muller-Moule, P.; Gilmore, A. M. Proceedings of the National Academy of Sciences, Vol. 99, Issue 23 https://doi.org/10.1073/pnas.232447699	journal	November 2002
Primary Production of the Biosphere: Integrating Terrestrial and Oceanic Components Field, C. B. Science, Vol. 281, Issue 5374 https://doi.org/10.1126/science.281.5374.237	journal	July 1998
Identification of a mechanism of photoprotective energy dissipation in higher plants Ruban, Alexander V.; Berera, Rudi; Ilioaia, Cristian Nature, Vol. 450, Issue 7169 https://doi.org/10.1038/nature06262	journal	November 2007
Single-Molecule Identification of Quenched and Unquenched States of LHCII Schlau-Cohen, Gabriela S.; Yang, Hsiang-Yu; Krüger, Tjaart P. J. The Journal of Physical Chemistry Letters, Vol. 6, Issue 5 https://doi.org/10.1021/acs.jpclett.5b00034	journal	February 2015
On the Mechanism of Light Harvesting in Photosynthetic Purple Bacteria: B800 to B850 Energy Transfer Scholes, Gregory D.; Fleming, Graham R. The Journal of Physical Chemistry B, Vol. 104, Issue 8 https://doi.org/10.1021/jp993435l	journal	March 2000
Effect of Antenna-Depletion in Photosystem II on Excitation Energy Transfer in Arabidopsis thaliana van Oort, Bart; Alberts, Marieke; de Bianchi, Silvia Biophysical Journal, Vol. 98, Issue 5 https://doi.org/10.1016/j.bpj.2009.11.012	journal	March 2010
Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis Niyogi, Krishna K.; Shih, Connie; Soon Chow, Wah Photosynthesis Research, Vol. 67, Issue 1/2, p. 139-145 https://doi.org/10.1023/A:1010661102365	journal	February 2001
Sunflecks in trees and forests: from photosynthetic physiology to global change biology Way, D. A.; Pearcy, R. W. Tree Physiology, Vol. 32, Issue 9 https://doi.org/10.1093/treephys/tps064	journal	August 2012
Resolving ultrafast exciton migration in organic solids at the nanoscale Penwell, Samuel B.; Ginsberg, Lucas D. S.; Noriega, Rodrigo Nature Materials, Vol. 16, Issue 11 https://doi.org/10.1038/nmat4975	journal	September 2017
A Structure-Based Model of Energy Transfer Reveals the Principles of Light Harvesting in Photosystem II Supercomplexes Bennett, Doran I. G.; Amarnath, Kapil; Fleming, Graham R. Journal of the American Chemical Society, Vol. 135, Issue 24 https://doi.org/10.1021/ja403685a	journal	June 2013
Manipulating Triplet Yield through Control of Symmetry-Breaking Charge Transfer Das, Saptaparna; Thornbury, William G.; Bartynski, Andrew N. The Journal of Physical Chemistry Letters, Vol. 9, Issue 12 https://doi.org/10.1021/acs.jpclett.8b01237	journal	May 2018
Rapid Regulation of Light Harvesting and Plant Fitness in the Field Kulheim, C. Science, Vol. 297, Issue 5578 https://doi.org/10.1126/science.1072359	journal	July 2002
Lutein Can Act as a Switchable Charge Transfer Quencher in the CP26 Light-harvesting Complex Avenson, Thomas J.; Ahn, Tae Kyu; Niyogi, Krishna K. Journal of Biological Chemistry, Vol. 284, Issue 5 https://doi.org/10.1074/jbc.M807192200	journal	November 2008
Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria Demmig-Adams, Barbara; Garab, Gyozo; Adams III, William Advances in Photosynthesis and Respiration https://doi.org/10.1007/978-94-017-9032-1	book	January 2014
Far-red fluorescence: A direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching Miloslavina, Yuliya; Wehner, Antje; Lambrev, Petar H. FEBS Letters, Vol. 582, Issue 25-26 https://doi.org/10.1016/j.febslet.2008.09.044	journal	October 2008
Meeting the Global Food Demand of the Future by Engineering Crop Photosynthesis and Yield Potential Long, Stephen P.; Marshall-Colon, Amy; Zhu, Xin-Guang Cell, Vol. 161, Issue 1 https://doi.org/10.1016/j.cell.2015.03.019	journal	March 2015
Models and measurements of energy-dependent quenching Zaks, Julia; Amarnath, Kapil; Sylak-Glassman, Emily J. Photosynthesis Research, Vol. 116, Issue 2-3 https://doi.org/10.1007/s11120-013-9857-7	journal	June 2013
Multiscale model of light harvesting by photosystem II in plants Amarnath, Kapil; Bennett, Doran I. G.; Schneider, Anna R. Proceedings of the National Academy of Sciences, Vol. 113, Issue 5 https://doi.org/10.1073/pnas.1524999113	journal	January 2016
Excitation migration in fluctuating light-harvesting antenna systems Chmeliov, Jevgenij; Trinkunas, Gediminas; van Amerongen, Herbert Photosynthesis Research, Vol. 127, Issue 1 https://doi.org/10.1007/s11120-015-0083-3	journal	January 2015
Carotenoid Cation Formation and the Regulation of Photosynthetic Light Harvesting Holt, N. E. Science, Vol. 307, Issue 5708 https://doi.org/10.1126/science.1105833	journal	January 2005
Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo Baker, Neil R. Annual Review of Plant Biology, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.arplant.59.032607.092759	journal	June 2008
Dissipative pathways in the photosystem-II antenna in plants Duffy, Christopher D. P.; Ruban, Alexander V. Journal of Photochemistry and Photobiology B: Biology, Vol. 152 https://doi.org/10.1016/j.jphotobiol.2015.09.011	journal	November 2015
Modeling of Fluorescence Quenching by Lutein in the Plant Light-Harvesting Complex LHCII Duffy, C. D. P.; Chmeliov, J.; Macernis, M. The Journal of Physical Chemistry B, Vol. 117, Issue 38 https://doi.org/10.1021/jp3110997	journal	December 2012
Improving photosynthesis and crop productivity by accelerating recovery from photoprotection Kromdijk, Johannes; Głowacka, Katarzyna; Leonelli, Lauriebeth Science, Vol. 354, Issue 6314 https://doi.org/10.1126/science.aai8878	journal	November 2016
Functional architecture of higher plant photosystem II supercomplexes Caffarri, Stefano; Kouřil, Roman; Kereïche, Sami The EMBO Journal, Vol. 28, Issue 19 https://doi.org/10.1038/emboj.2009.232	journal	August 2009
Light Harvesting in Photosystem II Core Complexes Is Limited by the Transfer to the Trap: Can the Core Complex Turn into a Photoprotective Mode? Raszewski, Grzegorz; Renger, Thomas Journal of the American Chemical Society, Vol. 130, Issue 13 https://doi.org/10.1021/ja7099826	journal	April 2008
Scalable High-Performance Algorithm for the Simulation of Exciton Dynamics. Application to the Light-Harvesting Complex II in the Presence of Resonant Vibrational Modes Kreisbeck, Christoph; Kramer, Tobias; Aspuru-Guzik, Alán Journal of Chemical Theory and Computation, Vol. 10, Issue 9 https://doi.org/10.1021/ct500629s	journal	August 2014
Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis Nilkens, Manuela; Kress, Eugen; Lambrev, Petar Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 4 https://doi.org/10.1016/j.bbabio.2010.01.001	journal	April 2010
The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence Genty, Bernard; Briantais, Jean-Marie; Baker, Neil R. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 990, Issue 1 https://doi.org/10.1016/S0304-4165(89)80016-9	journal	January 1989
Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution Liu, Zhenfeng; Yan, Hanchi; Wang, Kebin Nature, Vol. 428, Issue 6980 https://doi.org/10.1038/nature02373	journal	March 2004
Architecture of a Charge-Transfer State Regulating Light Harvesting in a Plant Antenna Protein Ahn, T. K.; Avenson, T. J.; Ballottari, M. Science, Vol. 320, Issue 5877 https://doi.org/10.1126/science.1154800	journal	May 2008

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