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Title: Light potentials of photosynthetic energy storage in the field: what limits the ability to use or dissipate rapidly increased light energy?

Abstract

The responses of plant photosynthesis to rapid fluctuations in environmental conditions are critical for efficient conversion of light energy. These responses are not well-seen laboratory conditions and are difficult to probe in field environments. We demonstrate an open science approach to this problem that combines multifaceted measurements of photosynthesis and environmental conditions, and an unsupervised statistical clustering approach. In a selected set of data on mint ( Mentha sp.), we show that ‘light potentials’ for linear electron flow and non-photochemical quenching (NPQ) upon rapid light increases are strongly suppressed in leaves previously exposed to low ambient photosynthetically active radiation (PAR) or low leaf temperatures, factors that can act both independently and cooperatively. Further analyses allowed us to test specific mechanisms. With decreasing leaf temperature or PAR, limitations to photosynthesis during high light fluctuations shifted from rapidly induced NPQ to photosynthetic control of electron flow at the cytochrome b 6 f complex. At low temperatures, high light induced lumen acidification, but did not induce NPQ, leading to accumulation of reduced electron transfer intermediates, probably inducing photodamage, revealing a potential target for improving the efficiency and robustness of photosynthesis. We discuss the implications of the approach for open science efforts to understandmore » and improve crop productivity.« less

Authors:
ORCiD logo [1];  [1]; ORCiD logo [1];  [1];  [1]; ORCiD logo [1]
  1. Michigan State Univ., East Lansing, MI (United States)
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division
OSTI Identifier:
1836279
Alternate Identifier(s):
OSTI ID: 1842945
Grant/Contract Number:  
FG02-91ER20021; FG02-11ER16220; SC0007101
Resource Type:
Accepted Manuscript
Journal Name:
Royal Society Open Science
Additional Journal Information:
Journal Volume: 8; Journal Issue: 12; Journal ID: ISSN 2054-5703
Publisher:
The Royal Society Publishing
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; non-photochemical quenching; photodamage; proton motive force; qE; photosynthetic control fund; unsupervised learning; Photosynthesis, photoprotection, energy efficiency, environmental conditions,

Citation Formats

Kanazawa, Atsuko, Chattopadhyay, Abhijnan, Kuhlgert, Sebastian, Tuitupou, Hainite, Maiti, Tapabrata, and Kramer, David M. Light potentials of photosynthetic energy storage in the field: what limits the ability to use or dissipate rapidly increased light energy?. United States: N. p., 2021. Web. doi:10.1098/rsos.211102.
Kanazawa, Atsuko, Chattopadhyay, Abhijnan, Kuhlgert, Sebastian, Tuitupou, Hainite, Maiti, Tapabrata, & Kramer, David M. Light potentials of photosynthetic energy storage in the field: what limits the ability to use or dissipate rapidly increased light energy?. United States. https://doi.org/10.1098/rsos.211102
Kanazawa, Atsuko, Chattopadhyay, Abhijnan, Kuhlgert, Sebastian, Tuitupou, Hainite, Maiti, Tapabrata, and Kramer, David M. Wed . "Light potentials of photosynthetic energy storage in the field: what limits the ability to use or dissipate rapidly increased light energy?". United States. https://doi.org/10.1098/rsos.211102. https://www.osti.gov/servlets/purl/1836279.
@article{osti_1836279,
title = {Light potentials of photosynthetic energy storage in the field: what limits the ability to use or dissipate rapidly increased light energy?},
author = {Kanazawa, Atsuko and Chattopadhyay, Abhijnan and Kuhlgert, Sebastian and Tuitupou, Hainite and Maiti, Tapabrata and Kramer, David M.},
abstractNote = {The responses of plant photosynthesis to rapid fluctuations in environmental conditions are critical for efficient conversion of light energy. These responses are not well-seen laboratory conditions and are difficult to probe in field environments. We demonstrate an open science approach to this problem that combines multifaceted measurements of photosynthesis and environmental conditions, and an unsupervised statistical clustering approach. In a selected set of data on mint ( Mentha sp.), we show that ‘light potentials’ for linear electron flow and non-photochemical quenching (NPQ) upon rapid light increases are strongly suppressed in leaves previously exposed to low ambient photosynthetically active radiation (PAR) or low leaf temperatures, factors that can act both independently and cooperatively. Further analyses allowed us to test specific mechanisms. With decreasing leaf temperature or PAR, limitations to photosynthesis during high light fluctuations shifted from rapidly induced NPQ to photosynthetic control of electron flow at the cytochrome b 6 f complex. At low temperatures, high light induced lumen acidification, but did not induce NPQ, leading to accumulation of reduced electron transfer intermediates, probably inducing photodamage, revealing a potential target for improving the efficiency and robustness of photosynthesis. We discuss the implications of the approach for open science efforts to understand and improve crop productivity.},
doi = {10.1098/rsos.211102},
journal = {Royal Society Open Science},
number = 12,
volume = 8,
place = {United States},
year = {Wed Dec 15 00:00:00 EST 2021},
month = {Wed Dec 15 00:00:00 EST 2021}
}

Works referenced in this record:

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

  • Kanazawa, A.; Kramer, D. M.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 20
  • DOI: 10.1073/pnas.182427499

Mechanism of photosystem-I photoinhibition in leaves ofCucumis sativus L.
journal, January 1994


Detecting Features in Spatial Point Processes with Clutter via Model-Based Clustering
journal, March 1998


Dynamic control of protein diffusion within the granal thylakoid lumen
journal, November 2011

  • Kirchhoff, H.; Hall, C.; Wood, M.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 50
  • DOI: 10.1073/pnas.1104141109

The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II
journal, January 2012

  • Jahns, Peter; Holzwarth, Alfred R.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 1
  • DOI: 10.1016/j.bbabio.2011.04.012

Control of the light harvesting function of chloroplast membranes: The LHCII-aggregation model for non-photochemical quenching
journal, July 2005


On the relationship between non-photochemical quenching and photoprotection of Photosystem II
journal, May 2012

  • Lambrev, Petar H.; Miloslavina, Yuliya; Jahns, Peter
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 5
  • DOI: 10.1016/j.bbabio.2012.02.002

Dynamic Environmental Photosynthetic Imaging Reveals Emergent Phenotypes
journal, June 2016


Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions
journal, July 2004


Diversity in Photoprotection and Energy Balancing in Terrestrial and Aquatic Phototrophs
book, June 2020

  • Kanazawa, Atsuko; Neofotis, Peter; Davis, Geoffry A.
  • Photosynthesis in Algae: Biochemical and Physiological Mechanisms
  • DOI: 10.1007/978-3-030-33397-3_12

The mechanisms contributing to photosynthetic control of electron transport by carbon assimilation in leaves
journal, August 1990

  • Foyer, Christine; Furbank, Robert; Harbinson, Jeremy
  • Photosynthesis Research, Vol. 25, Issue 2
  • DOI: 10.1007/BF00035457

Calcium-dependent regulation of photosynthesis
journal, September 2015

  • Hochmal, Ana Karina; Schulze, Stefan; Trompelt, Kerstin
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 9
  • DOI: 10.1016/j.bbabio.2015.02.010

The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced pmf
journal, October 2007

  • Takizawa, Kenji; Cruz, Jeffrey A.; Kanazawa, Atsuko
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1767, Issue 10
  • DOI: 10.1016/j.bbabio.2007.07.006

The Importance of Energy Balance in Improving Photosynthetic Productivity
journal, November 2010


MultispeQ Beta: a tool for large-scale plant phenotyping connected to the open PhotosynQ network
journal, October 2016

  • Kuhlgert, Sebastian; Austic, Greg; Zegarac, Robert
  • Royal Society Open Science, Vol. 3, Issue 10
  • DOI: 10.1098/rsos.160592

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
  • DOI: 10.1074/jbc.M402461200

Plastidic glucose-6-phosphate dehydrogenases are regulated to maintain activity in the light
journal, May 2019

  • Preiser, Alyssa L.; Fisher, Nicholas; Banerjee, Aparajita
  • Biochemical Journal, Vol. 476, Issue 10
  • DOI: 10.1042/BCJ20190234

Role of Thylakoid ATP/ADP Carrier in Photoinhibition and Photoprotection of Photosystem II in Arabidopsis    
journal, March 2010

  • Yin, Lan; Lundin, Björn; Bertrand, Martine
  • Plant Physiology, Vol. 153, Issue 2
  • DOI: 10.1104/pp.110.155804

Hacking the thylakoid proton motive force for improved photosynthesis: modulating ion flux rates that control proton motive force partitioning into Δ ψ and ΔpH
journal, August 2017

  • Davis, Geoffry A.; Rutherford, A. William; Kramer, David M.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1730
  • DOI: 10.1098/rstb.2016.0381

Trapping of the quenched conformation associated with non-photochemical quenching of chlorophyll fluorescence at low temperature
journal, September 2007

  • Lambrev, Petar H.; Tsonev, Tsonko; Velikova, Violeta
  • Photosynthesis Research, Vol. 94, Issue 2-3
  • DOI: 10.1007/s11120-007-9216-7

Model-Based Clustering, Discriminant Analysis, and Density Estimation
journal, June 2002

  • Fraley, Chris; Raftery, Adrian E.
  • Journal of the American Statistical Association, Vol. 97, Issue 458
  • DOI: 10.1198/016214502760047131

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


The water-water cycle is not a major alternative sink in fluctuating light at chilling temperature
journal, April 2021


Improving Photosynthetic Efficiency for Greater Yield
journal, June 2010


Control of Non-Photochemical Exciton Quenching by the Proton Circuit of Photosynthesis
book, October 2014


Regulation and Levels of the Thylakoid K + /H + Antiporter KEA3 Shape the Dynamic Response of Photosynthesis in Fluctuating Light
journal, May 2016

  • Armbruster, Ute; Leonelli, Lauriebeth; Correa Galvis, Viviana
  • Plant and Cell Physiology
  • DOI: 10.1093/pcp/pcw085

Repetitive Short-Pulse Light Mainly Inactivates Photosystem I in Sunflower Leaves
journal, June 2014

  • Sejima, Takehiro; Takagi, Daisuke; Fukayama, Hiroshi
  • Plant and Cell Physiology, Vol. 55, Issue 6
  • DOI: 10.1093/pcp/pcu061

Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis
journal, May 2014

  • Kunz, H. -H.; Gierth, M.; Herdean, A.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 20
  • DOI: 10.1073/pnas.1323899111

The Plastid Lipocalin LCNP Is Required for Sustained Photoprotective Energy Dissipation in Arabidopsis
journal, December 2017

  • Malnoë, Alizée; Schultink, Alex; Shahrasbi, Sanya
  • The Plant Cell, Vol. 30, Issue 1
  • DOI: 10.1105/tpc.17.00536

Balancing the central roles of the thylakoid proton gradient
journal, January 2003


How Many Clusters? Which Clustering Method? Answers Via Model-Based Cluster Analysis
journal, August 1998


Integrating the proton circuit into photosynthesis: progress and challenges
journal, January 2005


Chlorophyll-depleted wheat mutants are disturbed in photosynthetic electron flow regulation but can retain an acclimation ability to a fluctuating light regime
journal, October 2020


Fluctuating Light Takes Crop Photosynthesis on a Rollercoaster Ride
journal, October 2017

  • Kaiser, Elias; Morales, Alejandro; Harbinson, Jeremy
  • Plant Physiology, Vol. 176, Issue 2
  • DOI: 10.1104/pp.17.01250

Chloroplast Redox Regulatory Mechanisms in Plant Adaptation to Light and Darkness
journal, April 2019

  • Cejudo, Francisco Javier; Ojeda, Valle; Delgado-Requerey, Víctor
  • Frontiers in Plant Science, Vol. 10
  • DOI: 10.3389/fpls.2019.00380

Close relationship between the state of the xanthophyll cycle pigments and photosystem II efficiency during recovery from winter stress
journal, April 1996


Photoprotection of photosystems in fluctuating light intensities
journal, December 2014

  • Allahverdiyeva, Yagut; Suorsa, Marjaana; Tikkanen, Mikko
  • Journal of Experimental Botany, Vol. 66, Issue 9
  • DOI: 10.1093/jxb/eru463

Homeostasis of adenylate status during photosynthesis in a fluctuating environment
journal, February 2000


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

  • Kromdijk, Johannes; Głowacka, Katarzyna; Leonelli, Lauriebeth
  • Science, Vol. 354, Issue 6314
  • DOI: 10.1126/science.aai8878

Excitation-energy quenching in aggregates of the LHC II chlorophyll-protein complex: a time-resolved fluorescence study
journal, February 1993

  • Mullineaux, Conrad W.; Pascal, Andrew A.; Horton, Peter
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1141, Issue 1
  • DOI: 10.1016/0005-2728(93)90184-H

Closing in on maximum yield of chlorophyll fluorescence using a single multiphase flash of sub-saturating intensity: Fm using a single multiphase flash
journal, May 2013

  • Loriaux, S. D.; Avenson, T. J.; Welles, J. M.
  • Plant, Cell & Environment, Vol. 36, Issue 10
  • DOI: 10.1111/pce.12115

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
  • DOI: 10.1016/j.cplett.2009.10.085

Thioredoxins Play a Crucial Role in Dynamic Acclimation of Photosynthesis in Fluctuating Light
journal, January 2017


Limitations to photosynthesis by proton motive force-induced photosystem II photodamage
journal, October 2016

  • Davis, Geoffry A.; Kanazawa, Atsuko; Schöttler, Mark Aurel
  • eLife, Vol. 5
  • DOI: 10.7554/eLife.16921

Impact of ion fluxes across thylakoid membranes on photosynthetic electron transport and photoprotection
journal, June 2021


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


The xanthophyll cycle, its regulation and components
journal, August 1997


Flexibility in the Energy Balancing Network of Photosynthesis Enables Safe Operation under Changing Environmental Conditions
journal, March 2020

  • Walker, Berkley J.; Kramer, David M.; Fisher, Nicholas
  • Plants, Vol. 9, Issue 3
  • DOI: 10.3390/plants9030301

Determining the limitations and regulation of photosynthetic energy transduction in leaves
journal, September 2007


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
  • DOI: 10.1073/pnas.232447699

The regulation of the chloroplast proton motive force plays a key role for photosynthesis in fluctuating light
journal, June 2017

  • Armbruster, Ute; Correa Galvis, Viviana; Kunz, Hans-Henning
  • Current Opinion in Plant Biology, Vol. 37
  • DOI: 10.1016/j.pbi.2017.03.012

Photoinhibition and Zeaxanthin Formation in Intact Leaves: A Possible Role of the Xanthophyll Cycle in the Dissipation of Excess Light Energy
journal, June 1987

  • Demmig, Barbara; Winter, Klaus; Krüger, Almuth
  • Plant Physiology, Vol. 84, Issue 2
  • DOI: 10.1104/pp.84.2.218

A Holistic Approach to Study Photosynthetic Acclimation Responses of Plants to Fluctuating Light
journal, April 2021

  • Gjindali, Armida; Herrmann, Helena A.; Schwartz, Jean-Marc
  • Frontiers in Plant Science, Vol. 12
  • DOI: 10.3389/fpls.2021.668512

How Does Cyclic Electron Flow Alleviate Photoinhibition in Arabidopsis?
journal, December 2008

  • Takahashi, Shunichi; Milward, Sara E.; Fan, Da-Yong
  • Plant Physiology, Vol. 149, Issue 3
  • DOI: 10.1104/pp.108.134122

A kinetic model of rapidly reversible nonphotochemical quenching
journal, August 2012

  • Zaks, J.; Amarnath, K.; Kramer, D. M.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 39
  • DOI: 10.1073/pnas.1211017109

Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light
journal, February 2013

  • Allahverdiyeva, Y.; Mustila, H.; Ermakova, M.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 10
  • DOI: 10.1073/pnas.1221194110

The xanthophyll cycle and sustained thermal energy dissipation activity in Vinca minor and Euonymus kiautschovicus in winter
journal, February 1995


Manipulation of Photoprotection to Improve Plant Photosynthesis
journal, November 2010


mclust 5: Clustering, Classification and Density Estimation Using Gaussian Finite Mixture Models
journal, January 2016

  • Scrucca, Luca; Fop, Michael; Murphy, T. ,Brendan
  • The R Journal, Vol. 8, Issue 1
  • DOI: 10.32614/RJ-2016-021

Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin
journal, October 1990


Flavodiiron Proteins Promote Fast and Transient O 2 Photoreduction in Chlamydomonas
journal, May 2017

  • Chaux, Frédéric; Burlacot, Adrien; Mekhalfi, Malika
  • Plant Physiology, Vol. 174, Issue 3
  • DOI: 10.1104/pp.17.00421

Effects of Inorganic Phosphate on the Light Dependent Thylakoid Energization of Intact Spinach Chloroplasts
journal, September 1989

  • Heineke, Dieter; Stitt, Mark; Heldt, Hans W.
  • Plant Physiology, Vol. 91, Issue 1
  • DOI: 10.1104/pp.91.1.221

Reciprocal cybrids reveal how organellar genomes affect plant phenotypes
journal, January 2020

  • Flood, Pádraic J.; Theeuwen, Tom P. J. M.; Schneeberger, Korbinian
  • Nature Plants, Vol. 6, Issue 1
  • DOI: 10.1038/s41477-019-0575-9

Ion antiport accelerates photosynthetic acclimation in fluctuating light environments
journal, November 2014

  • Armbruster, Ute; Carrillo, L. Ruby; Venema, Kees
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms6439

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

  • Genty, Bernard; Briantais, Jean-Marie; Baker, Neil R.
  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 990, Issue 1
  • DOI: 10.1016/S0304-4165(89)80016-9

The roles of specific xanthophylls in photoprotection
journal, December 1997

  • Niyogi, K. K.; Bjorkman, O.; Grossman, A. R.
  • Proceedings of the National Academy of Sciences, Vol. 94, Issue 25
  • DOI: 10.1073/pnas.94.25.14162

pH-Dependent Regulation of Electron and Proton Transport in Chloroplasts In Situ and In Silico
journal, April 2020

  • Vershubskii, A. V.; Tikhonov, A. N.
  • Biochemistry (Moscow), Supplement Series A: Membrane and Cell Biology, Vol. 14, Issue 2
  • DOI: 10.1134/S1990747819030218