Membrane lipid unsaturation modulates processing of the photosystem II reaction-center protein D1 at low temperatures

The role of membrane lipid unsaturation in the restoration of photosystem II (PSII) function and in the synthesis of the D1 protein at different temperatures after photoinhibition was studied in wild-type cells and a mutant of Synechocystis sp. PCC 6803 with genetically inactivated desaturase genes....

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Veröffentlicht in:Plant physiology (Bethesda) 1997-07, Vol.114 (3), p.841-849
Hauptverfasser: Kanervo, E, Tasaka, Y, Murata, N, Aro, E.M
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creator Kanervo, E
Tasaka, Y
Murata, N
Aro, E.M
description The role of membrane lipid unsaturation in the restoration of photosystem II (PSII) function and in the synthesis of the D1 protein at different temperatures after photoinhibition was studied in wild-type cells and a mutant of Synechocystis sp. PCC 6803 with genetically inactivated desaturase genes. We show that posttranslational carboxyl-terminal processing of the precursor form of the D1 protein is an extremely sensitive reaction in the PSII repair cycle and is readily affected by low temperature. Furthermore, the threshold temperature at which perturbations in D1-protein processing start to emerge is specifically dependent on the extent of thylakoid membrane lipid unsaturation, as indicated by comparison of wild-type cells with the mutant defective in desaturation of 18:1 fatty acids of thylakoid membranes. When the temperature was decreased from 33 degrees C (growth temperature) to 18 degrees C, the inability of the fatty acid mutant to recover from photoinhibition was accompanied by a failure to process the newly synthesized D1 protein, which accumulated in considerable amounts as an unprocessed precursor D1 protein. Precursor D1 integrated into PSII monomer and dimer complexes even at low temperatures, but no activation of oxygen evolution occurred in these complexes in mutant cells defective in fatty acid unsaturation
doi_str_mv 10.1104/pp.114.3.841
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PCC 6803 with genetically inactivated desaturase genes. We show that posttranslational carboxyl-terminal processing of the precursor form of the D1 protein is an extremely sensitive reaction in the PSII repair cycle and is readily affected by low temperature. Furthermore, the threshold temperature at which perturbations in D1-protein processing start to emerge is specifically dependent on the extent of thylakoid membrane lipid unsaturation, as indicated by comparison of wild-type cells with the mutant defective in desaturation of 18:1 fatty acids of thylakoid membranes. When the temperature was decreased from 33 degrees C (growth temperature) to 18 degrees C, the inability of the fatty acid mutant to recover from photoinhibition was accompanied by a failure to process the newly synthesized D1 protein, which accumulated in considerable amounts as an unprocessed precursor D1 protein. Precursor D1 integrated into PSII monomer and dimer complexes even at low temperatures, but no activation of oxygen evolution occurred in these complexes in mutant cells defective in fatty acid unsaturation</description><identifier>ISSN: 0032-0889</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.114.3.841</identifier><identifier>PMID: 9232871</identifier><identifier>CODEN: PPHYA5</identifier><language>eng</language><publisher>Rockville, MD: American Society of Plant Physiologists</publisher><subject>ACIDE GRAS SATURE ; ACIDOS GRASOS SATURADOS ; Bacteriology ; Biological and medical sciences ; biosynthesis ; CHEMICAL COMPOSITION ; chemical constituents of plants ; chemistry ; COMPOSICION QUIMICA ; COMPOSITION CHIMIQUE ; CYANOBACTERIA ; Cyanobacteria - drug effects ; Cyanobacteria - genetics ; Cyanobacteria - metabolism ; CYANOPHYTA ; Darkness ; drug effects ; Fatty Acid Desaturases ; Fatty Acid Desaturases - genetics ; Fatty acids ; FOTOINHIBICION ; FOTOSISTEMAS ; Fundamental and applied biological sciences. Psychology ; Genes, Plant ; genetics ; isolation &amp; purification ; Light ; Lincomycin ; Lincomycin - pharmacology ; Low temperature ; Membrane Lipids ; Membrane Lipids - chemistry ; Membrane Lipids - physiology ; metabolism ; Metabolism. Enzymes ; Microbiology ; Oxygen ; Oxygen - metabolism ; pharmacology ; PHOTOINHIBITION ; Photons ; Photosynthetic Reaction Center Complex Proteins ; Photosynthetic Reaction Center Complex Proteins - biosynthesis ; Photosynthetic Reaction Center Complex Proteins - isolation &amp; purification ; Photosynthetic Reaction Center Complex Proteins - metabolism ; Photosystem II ; Photosystem II Protein Complex ; PHOTOSYSTEME ; PHOTOSYSTEMS ; physiology ; Plants ; PRECURSORS ; Protein Processing, Post-Translational ; PROTEIN SYNTHESIS ; Proteins ; SATURATED FATTY ACIDS ; SINTESIS DE PROTEINAS ; STRESS RESPONSE ; SYNTHESE PROTEIQUE ; TEMPERATURA ; TEMPERATURE ; THYLAKOIDE ; THYLAKOIDS ; TILACOIDES ; Unsaturation ; Whole Plant, Environmental, and Stress Physiology</subject><ispartof>Plant physiology (Bethesda), 1997-07, Vol.114 (3), p.841-849</ispartof><rights>Copyright 1997 American Society of Plant Physiologists</rights><rights>1997 INIST-CNRS</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c583t-d42386aa04d0f53d120afcab0659cec29983a9f1f0c27c3b8a2726e98faa7db63</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/4277775$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/4277775$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,799,881,27903,27904,57996,58229</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&amp;idt=2749758$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/9232871$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kanervo, E</creatorcontrib><creatorcontrib>Tasaka, Y</creatorcontrib><creatorcontrib>Murata, N</creatorcontrib><creatorcontrib>Aro, E.M</creatorcontrib><title>Membrane lipid unsaturation modulates processing of the photosystem II reaction-center protein D1 at low temperatures</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>The role of membrane lipid unsaturation in the restoration of photosystem II (PSII) function and in the synthesis of the D1 protein at different temperatures after photoinhibition was studied in wild-type cells and a mutant of Synechocystis sp. PCC 6803 with genetically inactivated desaturase genes. We show that posttranslational carboxyl-terminal processing of the precursor form of the D1 protein is an extremely sensitive reaction in the PSII repair cycle and is readily affected by low temperature. Furthermore, the threshold temperature at which perturbations in D1-protein processing start to emerge is specifically dependent on the extent of thylakoid membrane lipid unsaturation, as indicated by comparison of wild-type cells with the mutant defective in desaturation of 18:1 fatty acids of thylakoid membranes. When the temperature was decreased from 33 degrees C (growth temperature) to 18 degrees C, the inability of the fatty acid mutant to recover from photoinhibition was accompanied by a failure to process the newly synthesized D1 protein, which accumulated in considerable amounts as an unprocessed precursor D1 protein. Precursor D1 integrated into PSII monomer and dimer complexes even at low temperatures, but no activation of oxygen evolution occurred in these complexes in mutant cells defective in fatty acid unsaturation</description><subject>ACIDE GRAS SATURE</subject><subject>ACIDOS GRASOS SATURADOS</subject><subject>Bacteriology</subject><subject>Biological and medical sciences</subject><subject>biosynthesis</subject><subject>CHEMICAL COMPOSITION</subject><subject>chemical constituents of plants</subject><subject>chemistry</subject><subject>COMPOSICION QUIMICA</subject><subject>COMPOSITION CHIMIQUE</subject><subject>CYANOBACTERIA</subject><subject>Cyanobacteria - drug effects</subject><subject>Cyanobacteria - genetics</subject><subject>Cyanobacteria - metabolism</subject><subject>CYANOPHYTA</subject><subject>Darkness</subject><subject>drug effects</subject><subject>Fatty Acid Desaturases</subject><subject>Fatty Acid Desaturases - genetics</subject><subject>Fatty acids</subject><subject>FOTOINHIBICION</subject><subject>FOTOSISTEMAS</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Genes, Plant</subject><subject>genetics</subject><subject>isolation &amp; purification</subject><subject>Light</subject><subject>Lincomycin</subject><subject>Lincomycin - pharmacology</subject><subject>Low temperature</subject><subject>Membrane Lipids</subject><subject>Membrane Lipids - chemistry</subject><subject>Membrane Lipids - physiology</subject><subject>metabolism</subject><subject>Metabolism. Enzymes</subject><subject>Microbiology</subject><subject>Oxygen</subject><subject>Oxygen - metabolism</subject><subject>pharmacology</subject><subject>PHOTOINHIBITION</subject><subject>Photons</subject><subject>Photosynthetic Reaction Center Complex Proteins</subject><subject>Photosynthetic Reaction Center Complex Proteins - biosynthesis</subject><subject>Photosynthetic Reaction Center Complex Proteins - isolation &amp; purification</subject><subject>Photosynthetic Reaction Center Complex Proteins - metabolism</subject><subject>Photosystem II</subject><subject>Photosystem II Protein Complex</subject><subject>PHOTOSYSTEME</subject><subject>PHOTOSYSTEMS</subject><subject>physiology</subject><subject>Plants</subject><subject>PRECURSORS</subject><subject>Protein Processing, Post-Translational</subject><subject>PROTEIN SYNTHESIS</subject><subject>Proteins</subject><subject>SATURATED FATTY ACIDS</subject><subject>SINTESIS DE PROTEINAS</subject><subject>STRESS RESPONSE</subject><subject>SYNTHESE PROTEIQUE</subject><subject>TEMPERATURA</subject><subject>TEMPERATURE</subject><subject>THYLAKOIDE</subject><subject>THYLAKOIDS</subject><subject>TILACOIDES</subject><subject>Unsaturation</subject><subject>Whole Plant, Environmental, and Stress Physiology</subject><issn>0032-0889</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1997</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkb2P1DAQxS0EOpaFjhIkF-gqdvFXYru4At3xsdIhCrjamjjObk5JbGwHdP89jna1QIVTjKX3ezMTP4ReUrKllIh3IZQqtnyrBH2EVrTibMMqoR6jFSHlTpTST9GzlO4JIZRTcYEuNONMSbpC8xc3NhEmh4c-9C2epwR5jpB7P-HRt_MA2SUcorcupX7aY9_hfHA4HHz26SFlN-LdDkcHdvFsrJuyi4shu37CNxRDxoP_hQsYXFyau_QcPelgSO7Fqa7R3ccP368_b26_ftpdv7_d2ErxvGkF46oGIKIlXcVbygh0FhpSV9o6y7RWHHRHO2KZtLxRwCSrnVYdgGybmq_R1bFvmJvRtctuEQYTYj9CfDAeevOvMvUHs_c_DS3zJSn-y5M_-h-zS9mMfbJuGMqD-TkZqWlVk7r-LyjU8pV11-jtEbTRpxRdd16GErPEaUIoVRhuSpwFf_33D5zhU35Ff3PSIVkYupKk7dMZY1JoWS1TXx2x-5R9PMuCyXKqP1M68Ab2sXS4-0a1lqSmTHP-G5tVvfc</recordid><startdate>19970701</startdate><enddate>19970701</enddate><creator>Kanervo, E</creator><creator>Tasaka, Y</creator><creator>Murata, N</creator><creator>Aro, E.M</creator><general>American Society of Plant Physiologists</general><scope>FBQ</scope><scope>IQODW</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>7S9</scope><scope>L.6</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>19970701</creationdate><title>Membrane lipid unsaturation modulates processing of the photosystem II reaction-center protein D1 at low temperatures</title><author>Kanervo, E ; Tasaka, Y ; Murata, N ; Aro, E.M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c583t-d42386aa04d0f53d120afcab0659cec29983a9f1f0c27c3b8a2726e98faa7db63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1997</creationdate><topic>ACIDE GRAS SATURE</topic><topic>ACIDOS GRASOS SATURADOS</topic><topic>Bacteriology</topic><topic>Biological and medical sciences</topic><topic>biosynthesis</topic><topic>CHEMICAL COMPOSITION</topic><topic>chemical constituents of plants</topic><topic>chemistry</topic><topic>COMPOSICION QUIMICA</topic><topic>COMPOSITION CHIMIQUE</topic><topic>CYANOBACTERIA</topic><topic>Cyanobacteria - drug effects</topic><topic>Cyanobacteria - genetics</topic><topic>Cyanobacteria - metabolism</topic><topic>CYANOPHYTA</topic><topic>Darkness</topic><topic>drug effects</topic><topic>Fatty Acid Desaturases</topic><topic>Fatty Acid Desaturases - genetics</topic><topic>Fatty acids</topic><topic>FOTOINHIBICION</topic><topic>FOTOSISTEMAS</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Genes, Plant</topic><topic>genetics</topic><topic>isolation &amp; purification</topic><topic>Light</topic><topic>Lincomycin</topic><topic>Lincomycin - pharmacology</topic><topic>Low temperature</topic><topic>Membrane Lipids</topic><topic>Membrane Lipids - chemistry</topic><topic>Membrane Lipids - physiology</topic><topic>metabolism</topic><topic>Metabolism. Enzymes</topic><topic>Microbiology</topic><topic>Oxygen</topic><topic>Oxygen - metabolism</topic><topic>pharmacology</topic><topic>PHOTOINHIBITION</topic><topic>Photons</topic><topic>Photosynthetic Reaction Center Complex Proteins</topic><topic>Photosynthetic Reaction Center Complex Proteins - biosynthesis</topic><topic>Photosynthetic Reaction Center Complex Proteins - isolation &amp; purification</topic><topic>Photosynthetic Reaction Center Complex Proteins - metabolism</topic><topic>Photosystem II</topic><topic>Photosystem II Protein Complex</topic><topic>PHOTOSYSTEME</topic><topic>PHOTOSYSTEMS</topic><topic>physiology</topic><topic>Plants</topic><topic>PRECURSORS</topic><topic>Protein Processing, Post-Translational</topic><topic>PROTEIN SYNTHESIS</topic><topic>Proteins</topic><topic>SATURATED FATTY ACIDS</topic><topic>SINTESIS DE PROTEINAS</topic><topic>STRESS RESPONSE</topic><topic>SYNTHESE PROTEIQUE</topic><topic>TEMPERATURA</topic><topic>TEMPERATURE</topic><topic>THYLAKOIDE</topic><topic>THYLAKOIDS</topic><topic>TILACOIDES</topic><topic>Unsaturation</topic><topic>Whole Plant, Environmental, and Stress Physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kanervo, E</creatorcontrib><creatorcontrib>Tasaka, Y</creatorcontrib><creatorcontrib>Murata, N</creatorcontrib><creatorcontrib>Aro, E.M</creatorcontrib><collection>AGRIS</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kanervo, E</au><au>Tasaka, Y</au><au>Murata, N</au><au>Aro, E.M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Membrane lipid unsaturation modulates processing of the photosystem II reaction-center protein D1 at low temperatures</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>1997-07-01</date><risdate>1997</risdate><volume>114</volume><issue>3</issue><spage>841</spage><epage>849</epage><pages>841-849</pages><issn>0032-0889</issn><eissn>1532-2548</eissn><coden>PPHYA5</coden><abstract>The role of membrane lipid unsaturation in the restoration of photosystem II (PSII) function and in the synthesis of the D1 protein at different temperatures after photoinhibition was studied in wild-type cells and a mutant of Synechocystis sp. PCC 6803 with genetically inactivated desaturase genes. We show that posttranslational carboxyl-terminal processing of the precursor form of the D1 protein is an extremely sensitive reaction in the PSII repair cycle and is readily affected by low temperature. Furthermore, the threshold temperature at which perturbations in D1-protein processing start to emerge is specifically dependent on the extent of thylakoid membrane lipid unsaturation, as indicated by comparison of wild-type cells with the mutant defective in desaturation of 18:1 fatty acids of thylakoid membranes. When the temperature was decreased from 33 degrees C (growth temperature) to 18 degrees C, the inability of the fatty acid mutant to recover from photoinhibition was accompanied by a failure to process the newly synthesized D1 protein, which accumulated in considerable amounts as an unprocessed precursor D1 protein. Precursor D1 integrated into PSII monomer and dimer complexes even at low temperatures, but no activation of oxygen evolution occurred in these complexes in mutant cells defective in fatty acid unsaturation</abstract><cop>Rockville, MD</cop><pub>American Society of Plant Physiologists</pub><pmid>9232871</pmid><doi>10.1104/pp.114.3.841</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record>
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source MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; JSTOR Archive Collection A-Z Listing; Oxford University Press Journals All Titles (1996-Current)
subjects ACIDE GRAS SATURE
ACIDOS GRASOS SATURADOS
Bacteriology
Biological and medical sciences
biosynthesis
CHEMICAL COMPOSITION
chemical constituents of plants
chemistry
COMPOSICION QUIMICA
COMPOSITION CHIMIQUE
CYANOBACTERIA
Cyanobacteria - drug effects
Cyanobacteria - genetics
Cyanobacteria - metabolism
CYANOPHYTA
Darkness
drug effects
Fatty Acid Desaturases
Fatty Acid Desaturases - genetics
Fatty acids
FOTOINHIBICION
FOTOSISTEMAS
Fundamental and applied biological sciences. Psychology
Genes, Plant
genetics
isolation & purification
Light
Lincomycin
Lincomycin - pharmacology
Low temperature
Membrane Lipids
Membrane Lipids - chemistry
Membrane Lipids - physiology
metabolism
Metabolism. Enzymes
Microbiology
Oxygen
Oxygen - metabolism
pharmacology
PHOTOINHIBITION
Photons
Photosynthetic Reaction Center Complex Proteins
Photosynthetic Reaction Center Complex Proteins - biosynthesis
Photosynthetic Reaction Center Complex Proteins - isolation & purification
Photosynthetic Reaction Center Complex Proteins - metabolism
Photosystem II
Photosystem II Protein Complex
PHOTOSYSTEME
PHOTOSYSTEMS
physiology
Plants
PRECURSORS
Protein Processing, Post-Translational
PROTEIN SYNTHESIS
Proteins
SATURATED FATTY ACIDS
SINTESIS DE PROTEINAS
STRESS RESPONSE
SYNTHESE PROTEIQUE
TEMPERATURA
TEMPERATURE
THYLAKOIDE
THYLAKOIDS
TILACOIDES
Unsaturation
Whole Plant, Environmental, and Stress Physiology
title Membrane lipid unsaturation modulates processing of the photosystem II reaction-center protein D1 at low temperatures
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