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

Abstract

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.

Authors:

Bennett, Doran I. G.;

; Amarnath, Kapil

Publication Date:: Thu Sep 20 00:00:00 EDT 2018

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

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

OSTI Identifier:: 1471771

Alternate Identifier(s):: OSTI ID: 1490703

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

Resource Type:: Published Article

Journal Name:: Proceedings of the National Academy of Sciences of the United States of America

Additional Journal Information:: Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 115 Journal Issue: 41; Journal ID: ISSN 0027-8424

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

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; photosynthesis; photosystem II; nonphotochemical quenching; excitation energy transport; multiscale model

Citation Formats


                    Bennett, Doran I. G., Fleming, Graham R., and Amarnath, Kapil. Energy-dependent quenching adjusts the excitation diffusion length to regulate photosynthetic light harvesting.  United States: N. p., 2018. 
Web.  doi:10.1073/pnas.1806597115.

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                    Bennett, Doran I. G., Fleming, Graham R., & Amarnath, Kapil. Energy-dependent quenching adjusts the excitation diffusion length to regulate photosynthetic light harvesting.  United States.  https://doi.org/10.1073/pnas.1806597115

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                    Bennett, Doran I. G., Fleming, Graham R., and Amarnath, Kapil. Thu .  
"Energy-dependent quenching adjusts the excitation diffusion length to regulate photosynthetic light harvesting".  United States.  https://doi.org/10.1073/pnas.1806597115.

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@article{osti_1471771,

  title        = {Energy-dependent quenching adjusts the excitation diffusion length to regulate photosynthetic light harvesting},

  author       = {Bennett, Doran I. G. and Fleming, Graham R. and Amarnath, Kapil},

  abstractNote = {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.},

  doi          = {10.1073/pnas.1806597115},

  journal      = {Proceedings of the National Academy of Sciences of the United States of America},

  number       = 41,

  volume       = 115,

  place        = {United States},

  year         = {Thu Sep 20 00:00:00 EDT 2018},

  month        = {Thu Sep 20 00:00:00 EDT 2018}

}

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

Abstract

Citation Formats

In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase journal, August 2002

Dynamic quenching in single photosystem II supercomplexes journal, January 2016

Intra- and inter-monomeric transfers in the light harvesting LHCII complex: the Redfield–Förster picture journal, January 2011

New Fluorescence Parameters for the Determination of Q A Redox State and Excitation Energy Fluxes journal, January 2004

Long-range energy transport in photosystem II journal, June 2016

Enhanced thylakoid photoprotection can increase yield and canopy radiation use efficiency in rice journal, March 2018

Characterizing non-photochemical quenching in leaves through fluorescence lifetime snapshots journal, March 2015

Use of a Pulse-Amplitude Modulated Chlorophyll Fluorometer to Study the Efficiency of Photosynthesis in Arabidopsis Plants book, January 2011

Coexistence of Fluid and Crystalline Phases of Proteins in Photosynthetic Membranes journal, September 2013

Cooperative singlet and triplet exciton transport in tetracene crystals visualized by ultrafast microscopy journal, September 2015

Controlled Disorder in Plant Light-Harvesting Complex II Explains Its Photoprotective Role journal, June 2012

Excitonic connectivity between photosystem II units: what is it, and how to measure it? journal, June 2013

Symmetry-Breaking Charge Transfer in Boron Dipyridylmethene (DIPYR) Dimers 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 journal, January 1999

PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition journal, November 2002

Primary Production of the Biosphere: Integrating Terrestrial and Oceanic Components journal, July 1998

Identification of a mechanism of photoprotective energy dissipation in higher plants journal, November 2007

Single-Molecule Identification of Quenched and Unquenched States of LHCII journal, February 2015

On the Mechanism of Light Harvesting in Photosynthetic Purple Bacteria: B800 to B850 Energy Transfer journal, March 2000

Effect of Antenna-Depletion in Photosystem II on Excitation Energy Transfer in Arabidopsis thaliana journal, March 2010

Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis journal, February 2001

Sunflecks in trees and forests: from photosynthetic physiology to global change biology journal, August 2012

Resolving ultrafast exciton migration in organic solids at the nanoscale journal, September 2017

A Structure-Based Model of Energy Transfer Reveals the Principles of Light Harvesting in Photosystem II Supercomplexes journal, June 2013

Manipulating Triplet Yield through Control of Symmetry-Breaking Charge Transfer journal, May 2018

Rapid Regulation of Light Harvesting and Plant Fitness in the Field journal, July 2002

Lutein Can Act as a Switchable Charge Transfer Quencher in the CP26 Light-harvesting Complex journal, November 2008

Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria book, January 2014

Far-red fluorescence: A direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching journal, October 2008

Meeting the Global Food Demand of the Future by Engineering Crop Photosynthesis and Yield Potential journal, March 2015

Models and measurements of energy-dependent quenching journal, June 2013

Multiscale model of light harvesting by photosystem II in plants journal, January 2016

Excitation migration in fluctuating light-harvesting antenna systems journal, January 2015

Carotenoid Cation Formation and the Regulation of Photosynthetic Light Harvesting journal, January 2005

Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo journal, June 2008

Dissipative pathways in the photosystem-II antenna in plants journal, November 2015

Modeling of Fluorescence Quenching by Lutein in the Plant Light-Harvesting Complex LHCII journal, December 2012

Improving photosynthesis and crop productivity by accelerating recovery from photoprotection journal, November 2016

Functional architecture of higher plant photosystem II supercomplexes journal, August 2009

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Scalable High-Performance Algorithm for the Simulation of Exciton Dynamics. Application to the Light-Harvesting Complex II in the Presence of Resonant Vibrational Modes 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 journal, April 2010

The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence journal, January 1989

Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution journal, March 2004

Architecture of a Charge-Transfer State Regulating Light Harvesting in a Plant Antenna Protein journal, May 2008

In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase
journal, August 2002

Dynamic quenching in single photosystem II supercomplexes
journal, January 2016

Intra- and inter-monomeric transfers in the light harvesting LHCII complex: the Redfield–Förster picture
journal, January 2011

New Fluorescence Parameters for the Determination of Q _A Redox State and Excitation Energy Fluxes
journal, January 2004

Long-range energy transport in photosystem II
journal, June 2016

Enhanced thylakoid photoprotection can increase yield and canopy radiation use efficiency in rice
journal, March 2018

Characterizing non-photochemical quenching in leaves through fluorescence lifetime snapshots
journal, March 2015

Use of a Pulse-Amplitude Modulated Chlorophyll Fluorometer to Study the Efficiency of Photosynthesis in Arabidopsis Plants
book, January 2011

Coexistence of Fluid and Crystalline Phases of Proteins in Photosynthetic Membranes
journal, September 2013

Cooperative singlet and triplet exciton transport in tetracene crystals visualized by ultrafast microscopy
journal, September 2015

Controlled Disorder in Plant Light-Harvesting Complex II Explains Its Photoprotective Role
journal, June 2012

Excitonic connectivity between photosystem II units: what is it, and how to measure it?
journal, June 2013

Symmetry-Breaking Charge Transfer in Boron Dipyridylmethene (DIPYR) Dimers
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
journal, January 1999

PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition
journal, November 2002

Primary Production of the Biosphere: Integrating Terrestrial and Oceanic Components
journal, July 1998

Identification of a mechanism of photoprotective energy dissipation in higher plants
journal, November 2007

Single-Molecule Identification of Quenched and Unquenched States of LHCII
journal, February 2015

On the Mechanism of Light Harvesting in Photosynthetic Purple Bacteria: B800 to B850 Energy Transfer
journal, March 2000

Effect of Antenna-Depletion in Photosystem II on Excitation Energy Transfer in Arabidopsis thaliana
journal, March 2010

Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis
journal, February 2001

Sunflecks in trees and forests: from photosynthetic physiology to global change biology
journal, August 2012

Resolving ultrafast exciton migration in organic solids at the nanoscale
journal, September 2017

A Structure-Based Model of Energy Transfer Reveals the Principles of Light Harvesting in Photosystem II Supercomplexes
journal, June 2013

Manipulating Triplet Yield through Control of Symmetry-Breaking Charge Transfer
journal, May 2018

Rapid Regulation of Light Harvesting and Plant Fitness in the Field
journal, July 2002

Lutein Can Act as a Switchable Charge Transfer Quencher in the CP26 Light-harvesting Complex
journal, November 2008

Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria
book, January 2014

Far-red fluorescence: A direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching
journal, October 2008

Meeting the Global Food Demand of the Future by Engineering Crop Photosynthesis and Yield Potential
journal, March 2015

Models and measurements of energy-dependent quenching
journal, June 2013

Multiscale model of light harvesting by photosystem II in plants
journal, January 2016

Excitation migration in fluctuating light-harvesting antenna systems
journal, January 2015

Carotenoid Cation Formation and the Regulation of Photosynthetic Light Harvesting
journal, January 2005

Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo
journal, June 2008

Dissipative pathways in the photosystem-II antenna in plants
journal, November 2015

Modeling of Fluorescence Quenching by Lutein in the Plant Light-Harvesting Complex LHCII
journal, December 2012

Improving photosynthesis and crop productivity by accelerating recovery from photoprotection
journal, November 2016

Functional architecture of higher plant photosystem II supercomplexes
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?
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
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
journal, April 2010

The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence
journal, January 1989

Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution
journal, March 2004

Architecture of a Charge-Transfer State Regulating Light Harvesting in a Plant Antenna Protein
journal, May 2008