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Plants cope with fluctuating light by frequency‐dependent nonphotochemical quenching and cyclic electron transport
Summary In natural environments, plants are exposed to rapidly changing light. Maintaining photosynthetic efficiency while avoiding photodamage requires equally rapid regulation of photoprotective mechanisms. We asked what the operation frequency range of regulation is in which plants can efficientl...
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Published in: | The New phytologist 2023-09, Vol.239 (5), p.1869-1886 |
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cites | cdi_FETCH-LOGICAL-c4153-2d2cb401ddaba157e98ac208d636d4e5be0a6bfc7e04c09597dcab45640616a43 |
container_end_page | 1886 |
container_issue | 5 |
container_start_page | 1869 |
container_title | The New phytologist |
container_volume | 239 |
creator | Niu, Yuxi Lazár, Dušan Holzwarth, Alfred R. Kramer, David M. Matsubara, Shizue Fiorani, Fabio Poorter, Hendrik Schrey, Silvia D. Nedbal, Ladislav |
description | Summary
In natural environments, plants are exposed to rapidly changing light. Maintaining photosynthetic efficiency while avoiding photodamage requires equally rapid regulation of photoprotective mechanisms. We asked what the operation frequency range of regulation is in which plants can efficiently respond to varying light.
Chlorophyll fluorescence, P700, plastocyanin, and ferredoxin responses of wild‐types Arabidopsis thaliana were measured in oscillating light of various frequencies. We also investigated the npq1 mutant lacking violaxanthin de‐epoxidase, the npq4 mutant lacking PsbS protein, and the mutants crr2‐2, and pgrl1ab impaired in different pathways of the cyclic electron transport.
The fastest was the PsbS‐regulation responding to oscillation periods longer than 10 s. Processes involving violaxanthin de‐epoxidase dampened changes in chlorophyll fluorescence in oscillation periods of 2 min or longer. Knocking out the PGR5/PGRL1 pathway strongly reduced variations of all monitored parameters, probably due to congestion in the electron transport. Incapacitating the NDH‐like pathway only slightly changed the photosynthetic dynamics.
Our observations are consistent with the hypothesis that nonphotochemical quenching in slow light oscillations involves violaxanthin de‐epoxidase to produce, presumably, a largely stationary level of zeaxanthin. We interpret the observed dynamics of photosystem I components as being formed in slow light oscillations partially by thylakoid remodeling that modulates the redox rates. |
doi_str_mv | 10.1111/nph.19083 |
format | article |
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In natural environments, plants are exposed to rapidly changing light. Maintaining photosynthetic efficiency while avoiding photodamage requires equally rapid regulation of photoprotective mechanisms. We asked what the operation frequency range of regulation is in which plants can efficiently respond to varying light.
Chlorophyll fluorescence, P700, plastocyanin, and ferredoxin responses of wild‐types Arabidopsis thaliana were measured in oscillating light of various frequencies. We also investigated the npq1 mutant lacking violaxanthin de‐epoxidase, the npq4 mutant lacking PsbS protein, and the mutants crr2‐2, and pgrl1ab impaired in different pathways of the cyclic electron transport.
The fastest was the PsbS‐regulation responding to oscillation periods longer than 10 s. Processes involving violaxanthin de‐epoxidase dampened changes in chlorophyll fluorescence in oscillation periods of 2 min or longer. Knocking out the PGR5/PGRL1 pathway strongly reduced variations of all monitored parameters, probably due to congestion in the electron transport. Incapacitating the NDH‐like pathway only slightly changed the photosynthetic dynamics.
Our observations are consistent with the hypothesis that nonphotochemical quenching in slow light oscillations involves violaxanthin de‐epoxidase to produce, presumably, a largely stationary level of zeaxanthin. We interpret the observed dynamics of photosystem I components as being formed in slow light oscillations partially by thylakoid remodeling that modulates the redox rates.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.19083</identifier><identifier>PMID: 37429324</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; BASIC BIOLOGICAL SCIENCES ; Chlorophyll ; Chlorophyll - metabolism ; Chlorophylls ; cyclic electron transport ; Electron Transport ; Ferredoxin ; Fluorescence ; frequency analysis ; Frequency ranges ; Light ; Light-Harvesting Protein Complexes - metabolism ; Membrane Proteins - metabolism ; Mutants ; Mutation - genetics ; Natural environment ; nonphotochemical quenching ; Oscillations ; Photosynthesis ; Photosynthesis - physiology ; photosynthetic oscillation ; Photosynthetic Reaction Center Complex Proteins - genetics ; Photosystem I ; Photosystem II Protein Complex - metabolism ; Plastocyanin ; Quenching ; regulation ; Transport ; Violaxanthin ; Zeaxanthin</subject><ispartof>The New phytologist, 2023-09, Vol.239 (5), p.1869-1886</ispartof><rights>2023 The Authors. © 2023 New Phytologist Foundation</rights><rights>2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.</rights><rights>2023. This article is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4153-2d2cb401ddaba157e98ac208d636d4e5be0a6bfc7e04c09597dcab45640616a43</citedby><cites>FETCH-LOGICAL-c4153-2d2cb401ddaba157e98ac208d636d4e5be0a6bfc7e04c09597dcab45640616a43</cites><orcidid>0000-0001-8775-1541 ; 0000-0002-9627-9864 ; 0000-0002-1440-6496 ; 0000-0001-5821-1968 ; 0000-0001-8035-4017 ; 0000-0001-9900-2433 ; 0000-0003-2181-6888 ; 0000-0002-4282-3406 ; 0000-0002-9562-4873 ; 0000000187751541 ; 0000000295624873 ; 0000000296279864 ; 0000000180354017 ; 0000000214406496 ; 0000000199002433 ; 0000000242823406 ; 0000000321816888 ; 0000000158211968</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37429324$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/biblio/1989057$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Niu, Yuxi</creatorcontrib><creatorcontrib>Lazár, Dušan</creatorcontrib><creatorcontrib>Holzwarth, Alfred R.</creatorcontrib><creatorcontrib>Kramer, David M.</creatorcontrib><creatorcontrib>Matsubara, Shizue</creatorcontrib><creatorcontrib>Fiorani, Fabio</creatorcontrib><creatorcontrib>Poorter, Hendrik</creatorcontrib><creatorcontrib>Schrey, Silvia D.</creatorcontrib><creatorcontrib>Nedbal, Ladislav</creatorcontrib><creatorcontrib>Michigan State Univ., East Lansing, MI (United States)</creatorcontrib><title>Plants cope with fluctuating light by frequency‐dependent nonphotochemical quenching and cyclic electron transport</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary
In natural environments, plants are exposed to rapidly changing light. Maintaining photosynthetic efficiency while avoiding photodamage requires equally rapid regulation of photoprotective mechanisms. We asked what the operation frequency range of regulation is in which plants can efficiently respond to varying light.
Chlorophyll fluorescence, P700, plastocyanin, and ferredoxin responses of wild‐types Arabidopsis thaliana were measured in oscillating light of various frequencies. We also investigated the npq1 mutant lacking violaxanthin de‐epoxidase, the npq4 mutant lacking PsbS protein, and the mutants crr2‐2, and pgrl1ab impaired in different pathways of the cyclic electron transport.
The fastest was the PsbS‐regulation responding to oscillation periods longer than 10 s. Processes involving violaxanthin de‐epoxidase dampened changes in chlorophyll fluorescence in oscillation periods of 2 min or longer. Knocking out the PGR5/PGRL1 pathway strongly reduced variations of all monitored parameters, probably due to congestion in the electron transport. Incapacitating the NDH‐like pathway only slightly changed the photosynthetic dynamics.
Our observations are consistent with the hypothesis that nonphotochemical quenching in slow light oscillations involves violaxanthin de‐epoxidase to produce, presumably, a largely stationary level of zeaxanthin. We interpret the observed dynamics of photosystem I components as being formed in slow light oscillations partially by thylakoid remodeling that modulates the redox rates.</description><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>Chlorophyll</subject><subject>Chlorophyll - metabolism</subject><subject>Chlorophylls</subject><subject>cyclic electron transport</subject><subject>Electron Transport</subject><subject>Ferredoxin</subject><subject>Fluorescence</subject><subject>frequency analysis</subject><subject>Frequency ranges</subject><subject>Light</subject><subject>Light-Harvesting Protein Complexes - metabolism</subject><subject>Membrane Proteins - metabolism</subject><subject>Mutants</subject><subject>Mutation - genetics</subject><subject>Natural environment</subject><subject>nonphotochemical quenching</subject><subject>Oscillations</subject><subject>Photosynthesis</subject><subject>Photosynthesis - physiology</subject><subject>photosynthetic oscillation</subject><subject>Photosynthetic Reaction Center Complex Proteins - genetics</subject><subject>Photosystem I</subject><subject>Photosystem II Protein Complex - metabolism</subject><subject>Plastocyanin</subject><subject>Quenching</subject><subject>regulation</subject><subject>Transport</subject><subject>Violaxanthin</subject><subject>Zeaxanthin</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNp10b1u1TAUB_AIgeilMPACyIIFhrR2YjvxiCqgSBV0AInNco7PbVzl2sF2VGXjEXhGngS3KQxIePHy89_no6qeM3rCyjn183jCFO3bB9WOcanqnrXdw2pHadPXkstvR9WTlK4ppUrI5nF11Ha8UW3Dd1W-nIzPiUCYkdy4PJL9tEBeTHb-ikzuasxkWMk-4vcFPay_fvy0OKO36DPxofwccoARDw7MRO7MePvSeEtghckBwQkhx-BJjsanOcT8tHq0N1PCZ_f3cfX1_bsvZ-f1xecPH8_eXtTAmWjrxjYwcMqsNYNhokPVG2hob2UrLUcxIDVy2EOHlENpTXUWzMCF5FQyaXh7XL3cckPKTidwGWGE4H0pSDPVKyq6gl5vaI6h1J-yPrgEOJW5YFiSbvpWNYL3oi_01T_0OizRlxaK4pwLKpQo6s2mIIaUIu71HN3BxFUzqm_3pcvU9N2-in1xn7gMB7R_5Z8FFXC6gRs34fr_JP3p8nyL_A1Aw6IQ</recordid><startdate>202309</startdate><enddate>202309</enddate><creator>Niu, Yuxi</creator><creator>Lazár, Dušan</creator><creator>Holzwarth, Alfred R.</creator><creator>Kramer, David M.</creator><creator>Matsubara, Shizue</creator><creator>Fiorani, Fabio</creator><creator>Poorter, Hendrik</creator><creator>Schrey, Silvia D.</creator><creator>Nedbal, Ladislav</creator><general>Wiley Subscription Services, Inc</general><general>Wiley</general><scope>24P</scope><scope>WIN</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>7SN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>OTOTI</scope><orcidid>https://orcid.org/0000-0001-8775-1541</orcidid><orcidid>https://orcid.org/0000-0002-9627-9864</orcidid><orcidid>https://orcid.org/0000-0002-1440-6496</orcidid><orcidid>https://orcid.org/0000-0001-5821-1968</orcidid><orcidid>https://orcid.org/0000-0001-8035-4017</orcidid><orcidid>https://orcid.org/0000-0001-9900-2433</orcidid><orcidid>https://orcid.org/0000-0003-2181-6888</orcidid><orcidid>https://orcid.org/0000-0002-4282-3406</orcidid><orcidid>https://orcid.org/0000-0002-9562-4873</orcidid><orcidid>https://orcid.org/0000000187751541</orcidid><orcidid>https://orcid.org/0000000295624873</orcidid><orcidid>https://orcid.org/0000000296279864</orcidid><orcidid>https://orcid.org/0000000180354017</orcidid><orcidid>https://orcid.org/0000000214406496</orcidid><orcidid>https://orcid.org/0000000199002433</orcidid><orcidid>https://orcid.org/0000000242823406</orcidid><orcidid>https://orcid.org/0000000321816888</orcidid><orcidid>https://orcid.org/0000000158211968</orcidid></search><sort><creationdate>202309</creationdate><title>Plants cope with fluctuating light by frequency‐dependent nonphotochemical quenching and cyclic electron transport</title><author>Niu, Yuxi ; Lazár, Dušan ; Holzwarth, Alfred R. ; Kramer, David M. ; Matsubara, Shizue ; Fiorani, Fabio ; Poorter, Hendrik ; Schrey, Silvia D. ; Nedbal, Ladislav</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4153-2d2cb401ddaba157e98ac208d636d4e5be0a6bfc7e04c09597dcab45640616a43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>Chlorophyll</topic><topic>Chlorophyll - metabolism</topic><topic>Chlorophylls</topic><topic>cyclic electron transport</topic><topic>Electron Transport</topic><topic>Ferredoxin</topic><topic>Fluorescence</topic><topic>frequency analysis</topic><topic>Frequency ranges</topic><topic>Light</topic><topic>Light-Harvesting Protein Complexes - metabolism</topic><topic>Membrane Proteins - metabolism</topic><topic>Mutants</topic><topic>Mutation - genetics</topic><topic>Natural environment</topic><topic>nonphotochemical quenching</topic><topic>Oscillations</topic><topic>Photosynthesis</topic><topic>Photosynthesis - physiology</topic><topic>photosynthetic oscillation</topic><topic>Photosynthetic Reaction Center Complex Proteins - genetics</topic><topic>Photosystem I</topic><topic>Photosystem II Protein Complex - metabolism</topic><topic>Plastocyanin</topic><topic>Quenching</topic><topic>regulation</topic><topic>Transport</topic><topic>Violaxanthin</topic><topic>Zeaxanthin</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Niu, Yuxi</creatorcontrib><creatorcontrib>Lazár, Dušan</creatorcontrib><creatorcontrib>Holzwarth, Alfred R.</creatorcontrib><creatorcontrib>Kramer, David M.</creatorcontrib><creatorcontrib>Matsubara, Shizue</creatorcontrib><creatorcontrib>Fiorani, Fabio</creatorcontrib><creatorcontrib>Poorter, Hendrik</creatorcontrib><creatorcontrib>Schrey, Silvia D.</creatorcontrib><creatorcontrib>Nedbal, Ladislav</creatorcontrib><creatorcontrib>Michigan State Univ., East Lansing, MI (United States)</creatorcontrib><collection>Wiley Open Access</collection><collection>Wiley Online Library Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>OSTI.GOV</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Niu, Yuxi</au><au>Lazár, Dušan</au><au>Holzwarth, Alfred R.</au><au>Kramer, David M.</au><au>Matsubara, Shizue</au><au>Fiorani, Fabio</au><au>Poorter, Hendrik</au><au>Schrey, Silvia D.</au><au>Nedbal, Ladislav</au><aucorp>Michigan State Univ., East Lansing, MI (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Plants cope with fluctuating light by frequency‐dependent nonphotochemical quenching and cyclic electron transport</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2023-09</date><risdate>2023</risdate><volume>239</volume><issue>5</issue><spage>1869</spage><epage>1886</epage><pages>1869-1886</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>Summary
In natural environments, plants are exposed to rapidly changing light. Maintaining photosynthetic efficiency while avoiding photodamage requires equally rapid regulation of photoprotective mechanisms. We asked what the operation frequency range of regulation is in which plants can efficiently respond to varying light.
Chlorophyll fluorescence, P700, plastocyanin, and ferredoxin responses of wild‐types Arabidopsis thaliana were measured in oscillating light of various frequencies. We also investigated the npq1 mutant lacking violaxanthin de‐epoxidase, the npq4 mutant lacking PsbS protein, and the mutants crr2‐2, and pgrl1ab impaired in different pathways of the cyclic electron transport.
The fastest was the PsbS‐regulation responding to oscillation periods longer than 10 s. Processes involving violaxanthin de‐epoxidase dampened changes in chlorophyll fluorescence in oscillation periods of 2 min or longer. Knocking out the PGR5/PGRL1 pathway strongly reduced variations of all monitored parameters, probably due to congestion in the electron transport. Incapacitating the NDH‐like pathway only slightly changed the photosynthetic dynamics.
Our observations are consistent with the hypothesis that nonphotochemical quenching in slow light oscillations involves violaxanthin de‐epoxidase to produce, presumably, a largely stationary level of zeaxanthin. We interpret the observed dynamics of photosystem I components as being formed in slow light oscillations partially by thylakoid remodeling that modulates the redox rates.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>37429324</pmid><doi>10.1111/nph.19083</doi><tpages>1886</tpages><orcidid>https://orcid.org/0000-0001-8775-1541</orcidid><orcidid>https://orcid.org/0000-0002-9627-9864</orcidid><orcidid>https://orcid.org/0000-0002-1440-6496</orcidid><orcidid>https://orcid.org/0000-0001-5821-1968</orcidid><orcidid>https://orcid.org/0000-0001-8035-4017</orcidid><orcidid>https://orcid.org/0000-0001-9900-2433</orcidid><orcidid>https://orcid.org/0000-0003-2181-6888</orcidid><orcidid>https://orcid.org/0000-0002-4282-3406</orcidid><orcidid>https://orcid.org/0000-0002-9562-4873</orcidid><orcidid>https://orcid.org/0000000187751541</orcidid><orcidid>https://orcid.org/0000000295624873</orcidid><orcidid>https://orcid.org/0000000296279864</orcidid><orcidid>https://orcid.org/0000000180354017</orcidid><orcidid>https://orcid.org/0000000214406496</orcidid><orcidid>https://orcid.org/0000000199002433</orcidid><orcidid>https://orcid.org/0000000242823406</orcidid><orcidid>https://orcid.org/0000000321816888</orcidid><orcidid>https://orcid.org/0000000158211968</orcidid><oa>free_for_read</oa></addata></record> |
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source | Wiley-Blackwell Read & Publish Collection |
subjects | Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism BASIC BIOLOGICAL SCIENCES Chlorophyll Chlorophyll - metabolism Chlorophylls cyclic electron transport Electron Transport Ferredoxin Fluorescence frequency analysis Frequency ranges Light Light-Harvesting Protein Complexes - metabolism Membrane Proteins - metabolism Mutants Mutation - genetics Natural environment nonphotochemical quenching Oscillations Photosynthesis Photosynthesis - physiology photosynthetic oscillation Photosynthetic Reaction Center Complex Proteins - genetics Photosystem I Photosystem II Protein Complex - metabolism Plastocyanin Quenching regulation Transport Violaxanthin Zeaxanthin |
title | Plants cope with fluctuating light by frequency‐dependent nonphotochemical quenching and cyclic electron transport |
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