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Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion

A conserved regulatory mechanism protects plants against the potentially damaging effects of excessive light. Nearly all photosynthetic eukaryotes are able to dissipate excess absorbed light energy in a process that involves xanthophyll pigments. To dissect the role of xanthophylls in photoprotectiv...

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Published in:The Plant cell 1998-07, Vol.10 (7), p.1121-1134
Main Authors: Niyogi, K.K. (University of California, Berkeley.), Grossman, A.R, Bjorkman, O
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Grossman, A.R
Bjorkman, O
description A conserved regulatory mechanism protects plants against the potentially damaging effects of excessive light. Nearly all photosynthetic eukaryotes are able to dissipate excess absorbed light energy in a process that involves xanthophyll pigments. To dissect the role of xanthophylls in photoprotective energy dissipation in vivo, we isolated Arabidopsis xanthophyll cycle mutants by screening for altered nonphotochemical quenching of chlorophyll fluorescence. The npq1 mutants are unable to convert violaxanthin to zeaxanthin in excessive light, whereas the npq2 mutants accumulate zeaxanthin constitutively. The npq2 mutants are new alleles of aba1, the zeaxanthin epoxidase gene. The high levels of zeaxanthin in npq2 affected the kinetics of induction and relaxation but not the extent of nonphotochemical quenching. Genetic mapping, DNA sequencing, and complementation of npq1 demonstrated that this mutation affects the structural gene encoding violaxanthin deepoxidase. The npq1 mutant exhibited greatly reduced nonphotochemical quenching, demonstrating that violaxanthin deepoxidation is required for the bulk of rapidly reversible nonphotochemical quenching in Arabidopsis. Altered regulation of photosynthetic energy conversion in npq1 was associated with increased sensitivity to photoinhibition. These results, in conjunction with the analysis of npq mutants of Chlamydomonas, suggest that the role of the xanthophyll cycle in nonphotochemical quenching has been conserved, although different photosynthetic eukaryotes rely on the xanthophyll cycle to different extents for the dissipation of excess absorbed light energy
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(University of California, Berkeley.) ; Grossman, A.R ; Bjorkman, O</creator><creatorcontrib>Niyogi, K.K. (University of California, Berkeley.) ; Grossman, A.R ; Bjorkman, O</creatorcontrib><description>A conserved regulatory mechanism protects plants against the potentially damaging effects of excessive light. Nearly all photosynthetic eukaryotes are able to dissipate excess absorbed light energy in a process that involves xanthophyll pigments. To dissect the role of xanthophylls in photoprotective energy dissipation in vivo, we isolated Arabidopsis xanthophyll cycle mutants by screening for altered nonphotochemical quenching of chlorophyll fluorescence. The npq1 mutants are unable to convert violaxanthin to zeaxanthin in excessive light, whereas the npq2 mutants accumulate zeaxanthin constitutively. The npq2 mutants are new alleles of aba1, the zeaxanthin epoxidase gene. The high levels of zeaxanthin in npq2 affected the kinetics of induction and relaxation but not the extent of nonphotochemical quenching. Genetic mapping, DNA sequencing, and complementation of npq1 demonstrated that this mutation affects the structural gene encoding violaxanthin deepoxidase. The npq1 mutant exhibited greatly reduced nonphotochemical quenching, demonstrating that violaxanthin deepoxidation is required for the bulk of rapidly reversible nonphotochemical quenching in Arabidopsis. Altered regulation of photosynthetic energy conversion in npq1 was associated with increased sensitivity to photoinhibition. These results, in conjunction with the analysis of npq mutants of Chlamydomonas, suggest that the role of the xanthophyll cycle in nonphotochemical quenching has been conserved, although different photosynthetic eukaryotes rely on the xanthophyll cycle to different extents for the dissipation of excess absorbed light energy</description><identifier>ISSN: 1040-4651</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1105/tpc.10.7.1121</identifier><identifier>PMID: 9668132</identifier><language>eng</language><publisher>United States: American Society of Plant Physiologists</publisher><subject>ABSORBANCE ; ABSORBANCIA ; ACTIVIDAD ENZIMATICA ; ACTIVITE ENZYMATIQUE ; ALLELES ; Amino Acid Sequence ; Arabidopsis - enzymology ; Arabidopsis - genetics ; ARABIDOPSIS THALIANA ; Base Sequence ; beta Carotene - analogs &amp; derivatives ; beta Carotene - metabolism ; CARTE GENETIQUE ; CHEMICAL COMPOSITION ; CHLOROPHYLLE ; CHLOROPHYLLS ; Chromosome Mapping ; CHROMOSOME MAPS ; CLOROFILAS ; COMPLEMENTATION ; COMPOSICION QUIMICA ; COMPOSITION CHIMIQUE ; Energy Metabolism ; ENZYMIC ACTIVITY ; ESPECTROMETRIA ; Ethyl Methanesulfonate ; Fast Neutrons ; FEUILLE ; FLUORESCENCE ; FLUORESCENCIA ; GENE ; GENES ; Genes, Plant ; GENETIC MAPPING ; GENETIC MAPS ; GENETIC MARKERS ; Genetic mutation ; GENETIC TRANSFORMATION ; GENETICA ; GENETICS ; GENETIQUE ; HOJAS ; INDUCED MUTATION ; Kinetics ; LEAVES ; LIGHT ; LIGHT INTENSITY ; LINKAGE ; LUMIERE ; Lutein - metabolism ; LUZ ; MAPAS GENETICOS ; MARCADORES GENETICOS ; MARQUEUR GENETIQUE ; MUTACION INDUCIDA ; Mutagenesis ; MUTANT ; MUTANTES ; MUTANTS ; MUTATION PROVOQUEE ; OXIDOREDUCTASES ; Oxidoreductases - chemistry ; Oxidoreductases - genetics ; OXIDORREDUCTASAS ; OXYDOREDUCTASE ; Photoinhibition ; Photons ; Photosynthesis ; Plant cells ; Plants ; Point Mutation ; Polymorphism, Genetic ; SIMPLE SEQUENCE LENGTH POLYMORPHISM ; SPECTRAL DATA ; SPECTROMETRIE ; SPECTROMETRY ; STRUCTURAL GENES ; TRANSFORMACION GENETICA ; TRANSFORMATION GENETIQUE ; VIOLAXANTHIN ; VIOLAXANTHIN DEEPOXIDASE ; XANTHOPHYLLE ; XANTHOPHYLLS ; XANTOFILAS ; ZEAXANTHIN ; ZEAXANTHIN EPOXIDASE ; Zeaxanthins</subject><ispartof>The Plant cell, 1998-07, Vol.10 (7), p.1121-1134</ispartof><rights>Copyright 1998 American Society of Plant Physiologists</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4461-fb0d2f6d4c343e35a1efdef83e2c51e27a19801ec14fffba8f7f7d045e04d9393</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/3870716$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/3870716$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,881,27903,27904,58217,58450</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/9668132$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Niyogi, K.K. (University of California, Berkeley.)</creatorcontrib><creatorcontrib>Grossman, A.R</creatorcontrib><creatorcontrib>Bjorkman, O</creatorcontrib><title>Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>A conserved regulatory mechanism protects plants against the potentially damaging effects of excessive light. Nearly all photosynthetic eukaryotes are able to dissipate excess absorbed light energy in a process that involves xanthophyll pigments. To dissect the role of xanthophylls in photoprotective energy dissipation in vivo, we isolated Arabidopsis xanthophyll cycle mutants by screening for altered nonphotochemical quenching of chlorophyll fluorescence. The npq1 mutants are unable to convert violaxanthin to zeaxanthin in excessive light, whereas the npq2 mutants accumulate zeaxanthin constitutively. The npq2 mutants are new alleles of aba1, the zeaxanthin epoxidase gene. The high levels of zeaxanthin in npq2 affected the kinetics of induction and relaxation but not the extent of nonphotochemical quenching. Genetic mapping, DNA sequencing, and complementation of npq1 demonstrated that this mutation affects the structural gene encoding violaxanthin deepoxidase. The npq1 mutant exhibited greatly reduced nonphotochemical quenching, demonstrating that violaxanthin deepoxidation is required for the bulk of rapidly reversible nonphotochemical quenching in Arabidopsis. Altered regulation of photosynthetic energy conversion in npq1 was associated with increased sensitivity to photoinhibition. These results, in conjunction with the analysis of npq mutants of Chlamydomonas, suggest that the role of the xanthophyll cycle in nonphotochemical quenching has been conserved, although different photosynthetic eukaryotes rely on the xanthophyll cycle to different extents for the dissipation of excess absorbed light energy</description><subject>ABSORBANCE</subject><subject>ABSORBANCIA</subject><subject>ACTIVIDAD ENZIMATICA</subject><subject>ACTIVITE ENZYMATIQUE</subject><subject>ALLELES</subject><subject>Amino Acid Sequence</subject><subject>Arabidopsis - enzymology</subject><subject>Arabidopsis - genetics</subject><subject>ARABIDOPSIS THALIANA</subject><subject>Base Sequence</subject><subject>beta Carotene - analogs &amp; derivatives</subject><subject>beta Carotene - metabolism</subject><subject>CARTE GENETIQUE</subject><subject>CHEMICAL COMPOSITION</subject><subject>CHLOROPHYLLE</subject><subject>CHLOROPHYLLS</subject><subject>Chromosome Mapping</subject><subject>CHROMOSOME MAPS</subject><subject>CLOROFILAS</subject><subject>COMPLEMENTATION</subject><subject>COMPOSICION QUIMICA</subject><subject>COMPOSITION CHIMIQUE</subject><subject>Energy Metabolism</subject><subject>ENZYMIC ACTIVITY</subject><subject>ESPECTROMETRIA</subject><subject>Ethyl Methanesulfonate</subject><subject>Fast Neutrons</subject><subject>FEUILLE</subject><subject>FLUORESCENCE</subject><subject>FLUORESCENCIA</subject><subject>GENE</subject><subject>GENES</subject><subject>Genes, Plant</subject><subject>GENETIC MAPPING</subject><subject>GENETIC MAPS</subject><subject>GENETIC MARKERS</subject><subject>Genetic mutation</subject><subject>GENETIC TRANSFORMATION</subject><subject>GENETICA</subject><subject>GENETICS</subject><subject>GENETIQUE</subject><subject>HOJAS</subject><subject>INDUCED MUTATION</subject><subject>Kinetics</subject><subject>LEAVES</subject><subject>LIGHT</subject><subject>LIGHT INTENSITY</subject><subject>LINKAGE</subject><subject>LUMIERE</subject><subject>Lutein - metabolism</subject><subject>LUZ</subject><subject>MAPAS GENETICOS</subject><subject>MARCADORES GENETICOS</subject><subject>MARQUEUR GENETIQUE</subject><subject>MUTACION INDUCIDA</subject><subject>Mutagenesis</subject><subject>MUTANT</subject><subject>MUTANTES</subject><subject>MUTANTS</subject><subject>MUTATION PROVOQUEE</subject><subject>OXIDOREDUCTASES</subject><subject>Oxidoreductases - chemistry</subject><subject>Oxidoreductases - genetics</subject><subject>OXIDORREDUCTASAS</subject><subject>OXYDOREDUCTASE</subject><subject>Photoinhibition</subject><subject>Photons</subject><subject>Photosynthesis</subject><subject>Plant cells</subject><subject>Plants</subject><subject>Point Mutation</subject><subject>Polymorphism, Genetic</subject><subject>SIMPLE SEQUENCE LENGTH POLYMORPHISM</subject><subject>SPECTRAL DATA</subject><subject>SPECTROMETRIE</subject><subject>SPECTROMETRY</subject><subject>STRUCTURAL GENES</subject><subject>TRANSFORMACION GENETICA</subject><subject>TRANSFORMATION GENETIQUE</subject><subject>VIOLAXANTHIN</subject><subject>VIOLAXANTHIN DEEPOXIDASE</subject><subject>XANTHOPHYLLE</subject><subject>XANTHOPHYLLS</subject><subject>XANTOFILAS</subject><subject>ZEAXANTHIN</subject><subject>ZEAXANTHIN EPOXIDASE</subject><subject>Zeaxanthins</subject><issn>1040-4651</issn><issn>1532-298X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1998</creationdate><recordtype>article</recordtype><recordid>eNpVUc9vFCEUJkZT2-rRowkHr1N5wAzDwUPT-KNJEw_axBthmccOzewwAbZx_ntZd1PriY98P-C9j5B3wK4AWPuxLO6qYlVvHF6Qc2gFb7juf72smEnWyK6F1-Qi5wfGGCjQZ-RMd10Pgp-T9TrZTRjikkOmu32xc8l0QB9mpJY6nEuyE01xQupjomVE-rtqxriM6zRRt7rKhPkvkXC7n2wJcabR02WMJea1arEER3HGtF2pi_Mjplw1b8grb6eMb0_nJbn_8vnnzbfm7vvX25vru8ZJ2UHjN2zgvhukE1KgaC2gr__rBXLXAnJlQfcM0IH03m9s75VXA5MtMjloocUl-XTMXfabHQ6nkcySws6m1UQbzP_MHEazjY8GpGQtr_7m6Hcp5pzQP1mBmUMDpjZwwMocGqj698_fe1KfVl75D0f-IZeYnodxwZQRvWIKun8x3kZjtylkc_8DtNa1Q9G34g_43Jtx</recordid><startdate>19980701</startdate><enddate>19980701</enddate><creator>Niyogi, K.K. 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(University of California, Berkeley.) ; Grossman, A.R ; Bjorkman, O</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4461-fb0d2f6d4c343e35a1efdef83e2c51e27a19801ec14fffba8f7f7d045e04d9393</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1998</creationdate><topic>ABSORBANCE</topic><topic>ABSORBANCIA</topic><topic>ACTIVIDAD ENZIMATICA</topic><topic>ACTIVITE ENZYMATIQUE</topic><topic>ALLELES</topic><topic>Amino Acid Sequence</topic><topic>Arabidopsis - enzymology</topic><topic>Arabidopsis - genetics</topic><topic>ARABIDOPSIS THALIANA</topic><topic>Base Sequence</topic><topic>beta Carotene - analogs &amp; derivatives</topic><topic>beta Carotene - metabolism</topic><topic>CARTE GENETIQUE</topic><topic>CHEMICAL COMPOSITION</topic><topic>CHLOROPHYLLE</topic><topic>CHLOROPHYLLS</topic><topic>Chromosome Mapping</topic><topic>CHROMOSOME MAPS</topic><topic>CLOROFILAS</topic><topic>COMPLEMENTATION</topic><topic>COMPOSICION QUIMICA</topic><topic>COMPOSITION CHIMIQUE</topic><topic>Energy Metabolism</topic><topic>ENZYMIC ACTIVITY</topic><topic>ESPECTROMETRIA</topic><topic>Ethyl Methanesulfonate</topic><topic>Fast Neutrons</topic><topic>FEUILLE</topic><topic>FLUORESCENCE</topic><topic>FLUORESCENCIA</topic><topic>GENE</topic><topic>GENES</topic><topic>Genes, Plant</topic><topic>GENETIC MAPPING</topic><topic>GENETIC MAPS</topic><topic>GENETIC MARKERS</topic><topic>Genetic mutation</topic><topic>GENETIC TRANSFORMATION</topic><topic>GENETICA</topic><topic>GENETICS</topic><topic>GENETIQUE</topic><topic>HOJAS</topic><topic>INDUCED MUTATION</topic><topic>Kinetics</topic><topic>LEAVES</topic><topic>LIGHT</topic><topic>LIGHT INTENSITY</topic><topic>LINKAGE</topic><topic>LUMIERE</topic><topic>Lutein - metabolism</topic><topic>LUZ</topic><topic>MAPAS GENETICOS</topic><topic>MARCADORES GENETICOS</topic><topic>MARQUEUR GENETIQUE</topic><topic>MUTACION INDUCIDA</topic><topic>Mutagenesis</topic><topic>MUTANT</topic><topic>MUTANTES</topic><topic>MUTANTS</topic><topic>MUTATION PROVOQUEE</topic><topic>OXIDOREDUCTASES</topic><topic>Oxidoreductases - chemistry</topic><topic>Oxidoreductases - genetics</topic><topic>OXIDORREDUCTASAS</topic><topic>OXYDOREDUCTASE</topic><topic>Photoinhibition</topic><topic>Photons</topic><topic>Photosynthesis</topic><topic>Plant cells</topic><topic>Plants</topic><topic>Point Mutation</topic><topic>Polymorphism, Genetic</topic><topic>SIMPLE SEQUENCE LENGTH POLYMORPHISM</topic><topic>SPECTRAL DATA</topic><topic>SPECTROMETRIE</topic><topic>SPECTROMETRY</topic><topic>STRUCTURAL GENES</topic><topic>TRANSFORMACION GENETICA</topic><topic>TRANSFORMATION GENETIQUE</topic><topic>VIOLAXANTHIN</topic><topic>VIOLAXANTHIN DEEPOXIDASE</topic><topic>XANTHOPHYLLE</topic><topic>XANTHOPHYLLS</topic><topic>XANTOFILAS</topic><topic>ZEAXANTHIN</topic><topic>ZEAXANTHIN EPOXIDASE</topic><topic>Zeaxanthins</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Niyogi, K.K. (University of California, Berkeley.)</creatorcontrib><creatorcontrib>Grossman, A.R</creatorcontrib><creatorcontrib>Bjorkman, O</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Plant cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Niyogi, K.K. (University of California, Berkeley.)</au><au>Grossman, A.R</au><au>Bjorkman, O</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion</atitle><jtitle>The Plant cell</jtitle><addtitle>Plant Cell</addtitle><date>1998-07-01</date><risdate>1998</risdate><volume>10</volume><issue>7</issue><spage>1121</spage><epage>1134</epage><pages>1121-1134</pages><issn>1040-4651</issn><eissn>1532-298X</eissn><abstract>A conserved regulatory mechanism protects plants against the potentially damaging effects of excessive light. Nearly all photosynthetic eukaryotes are able to dissipate excess absorbed light energy in a process that involves xanthophyll pigments. To dissect the role of xanthophylls in photoprotective energy dissipation in vivo, we isolated Arabidopsis xanthophyll cycle mutants by screening for altered nonphotochemical quenching of chlorophyll fluorescence. The npq1 mutants are unable to convert violaxanthin to zeaxanthin in excessive light, whereas the npq2 mutants accumulate zeaxanthin constitutively. The npq2 mutants are new alleles of aba1, the zeaxanthin epoxidase gene. The high levels of zeaxanthin in npq2 affected the kinetics of induction and relaxation but not the extent of nonphotochemical quenching. Genetic mapping, DNA sequencing, and complementation of npq1 demonstrated that this mutation affects the structural gene encoding violaxanthin deepoxidase. The npq1 mutant exhibited greatly reduced nonphotochemical quenching, demonstrating that violaxanthin deepoxidation is required for the bulk of rapidly reversible nonphotochemical quenching in Arabidopsis. Altered regulation of photosynthetic energy conversion in npq1 was associated with increased sensitivity to photoinhibition. These results, in conjunction with the analysis of npq mutants of Chlamydomonas, suggest that the role of the xanthophyll cycle in nonphotochemical quenching has been conserved, although different photosynthetic eukaryotes rely on the xanthophyll cycle to different extents for the dissipation of excess absorbed light energy</abstract><cop>United States</cop><pub>American Society of Plant Physiologists</pub><pmid>9668132</pmid><doi>10.1105/tpc.10.7.1121</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record>
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subjects ABSORBANCE
ABSORBANCIA
ACTIVIDAD ENZIMATICA
ACTIVITE ENZYMATIQUE
ALLELES
Amino Acid Sequence
Arabidopsis - enzymology
Arabidopsis - genetics
ARABIDOPSIS THALIANA
Base Sequence
beta Carotene - analogs & derivatives
beta Carotene - metabolism
CARTE GENETIQUE
CHEMICAL COMPOSITION
CHLOROPHYLLE
CHLOROPHYLLS
Chromosome Mapping
CHROMOSOME MAPS
CLOROFILAS
COMPLEMENTATION
COMPOSICION QUIMICA
COMPOSITION CHIMIQUE
Energy Metabolism
ENZYMIC ACTIVITY
ESPECTROMETRIA
Ethyl Methanesulfonate
Fast Neutrons
FEUILLE
FLUORESCENCE
FLUORESCENCIA
GENE
GENES
Genes, Plant
GENETIC MAPPING
GENETIC MAPS
GENETIC MARKERS
Genetic mutation
GENETIC TRANSFORMATION
GENETICA
GENETICS
GENETIQUE
HOJAS
INDUCED MUTATION
Kinetics
LEAVES
LIGHT
LIGHT INTENSITY
LINKAGE
LUMIERE
Lutein - metabolism
LUZ
MAPAS GENETICOS
MARCADORES GENETICOS
MARQUEUR GENETIQUE
MUTACION INDUCIDA
Mutagenesis
MUTANT
MUTANTES
MUTANTS
MUTATION PROVOQUEE
OXIDOREDUCTASES
Oxidoreductases - chemistry
Oxidoreductases - genetics
OXIDORREDUCTASAS
OXYDOREDUCTASE
Photoinhibition
Photons
Photosynthesis
Plant cells
Plants
Point Mutation
Polymorphism, Genetic
SIMPLE SEQUENCE LENGTH POLYMORPHISM
SPECTRAL DATA
SPECTROMETRIE
SPECTROMETRY
STRUCTURAL GENES
TRANSFORMACION GENETICA
TRANSFORMATION GENETIQUE
VIOLAXANTHIN
VIOLAXANTHIN DEEPOXIDASE
XANTHOPHYLLE
XANTHOPHYLLS
XANTOFILAS
ZEAXANTHIN
ZEAXANTHIN EPOXIDASE
Zeaxanthins
title Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion
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