Successful Fertilization Requires the Presence of at Least One Major O-Acetylserine(thiol)lyase for Cysteine Synthesis in Pollen of Arabidopsis
The synthesis of cysteine (Cys) is a master control switch of plant primary metabolism that coordinates the flux of sulfur with carbon and nitrogen metabolism. In Arabidopsis (Arabidopsis thaliana), nine genes encode for O-acetylserine(thiol)lyase (OAS-TL)-like proteins, of which the major isoforms,...
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description | The synthesis of cysteine (Cys) is a master control switch of plant primary metabolism that coordinates the flux of sulfur with carbon and nitrogen metabolism. In Arabidopsis (Arabidopsis thaliana), nine genes encode for O-acetylserine(thiol)lyase (OAS-TL)-like proteins, of which the major isoforms, OAS-TL A, OAS-TL B, and OAS-TL C, catalyze the formation of Cys by combining O-acetylserine and sulfide in the cytosol, the plastids, and the mitochondria, respectively. So far, the significance of individual OAS-TL-like enzymes is unresolved. Generation of all major OAS-TL double loss-of-function mutants in combination with radiolabeled tracer studies revealed that subcellular localization of OAS-TL proteins is more important for efficient Cys synthesis than total cellular OAS-TL activity in leaves. The absence of oastl triple embryos after targeted crosses indicated the exclusiveness of Cys synthesis by the three major OAS-TLs and ruled out alternative sulfur fixation by other OAS-TL-like proteins. Analyses of oastlABC pollen demonstrated that the presence of at least one functional OAS-TL isoform is essential for the proper function of the male gametophyte, although the synthesis of histidine, lysine, and tryptophan is dispensable in pollen. Comparisons of oastlABC pollen derived from genetically different parent plant combinations allowed us to separate distinct functions of Cys and glutathione in pollen and revealed an additional role of glutathione for pollen germination. In contrast, female gametogenesis was not affected by the absence of major OAS-TLs, indicating significant transport of Cys into the developing ovule from the mother plant. |
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In Arabidopsis (Arabidopsis thaliana), nine genes encode for O-acetylserine(thiol)lyase (OAS-TL)-like proteins, of which the major isoforms, OAS-TL A, OAS-TL B, and OAS-TL C, catalyze the formation of Cys by combining O-acetylserine and sulfide in the cytosol, the plastids, and the mitochondria, respectively. So far, the significance of individual OAS-TL-like enzymes is unresolved. Generation of all major OAS-TL double loss-of-function mutants in combination with radiolabeled tracer studies revealed that subcellular localization of OAS-TL proteins is more important for efficient Cys synthesis than total cellular OAS-TL activity in leaves. The absence of oastl triple embryos after targeted crosses indicated the exclusiveness of Cys synthesis by the three major OAS-TLs and ruled out alternative sulfur fixation by other OAS-TL-like proteins. Analyses of oastlABC pollen demonstrated that the presence of at least one functional OAS-TL isoform is essential for the proper function of the male gametophyte, although the synthesis of histidine, lysine, and tryptophan is dispensable in pollen. Comparisons of oastlABC pollen derived from genetically different parent plant combinations allowed us to separate distinct functions of Cys and glutathione in pollen and revealed an additional role of glutathione for pollen germination. In contrast, female gametogenesis was not affected by the absence of major OAS-TLs, indicating significant transport of Cys into the developing ovule from the mother plant.</description><identifier>ISSN: 0032-0889</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.113.221200</identifier><identifier>PMID: 24001608</identifier><identifier>CODEN: PPHYA5</identifier><language>eng</language><publisher>Rockville, MD: American Society of Plant Biologists</publisher><subject>Arabidopsis - enzymology ; Arabidopsis - genetics ; Arabidopsis - physiology ; BIOCHEMISTRY AND METABOLISM ; Biological and medical sciences ; Carbon-Oxygen Lyases - metabolism ; Chromosome Segregation ; Crosses, Genetic ; Cysteine - biosynthesis ; Fertilization - physiology ; Fundamental and applied biological sciences. Psychology ; Gametophytes ; Gene Dosage - genetics ; Germination ; Germination - physiology ; Mutation - genetics ; Phenotype ; Phenotypes ; Plant physiology and development ; Plants ; Pollen ; Pollen - enzymology ; Pollen - physiology ; Protein isoforms ; Seeds ; Sulfhydryl Compounds - metabolism ; Sulfides ; Sulfur ; Sulfur - metabolism ; Thiols ; Tissue Survival ; Tritium - metabolism</subject><ispartof>Plant physiology (Bethesda), 2013-10, Vol.163 (2), p.959-972</ispartof><rights>2013 American Society of Plant Biologists</rights><rights>2014 INIST-CNRS</rights><rights>2013 American Society of Plant Biologists. All Rights Reserved. 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c505t-c0964313d5b099c398e0f34539887fb5e794dc6daaf062c5b7680653e41b2b203</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/23598716$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/23598716$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,803,885,27923,27924,58016,58249</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=27805764$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24001608$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Birke, Hannah</creatorcontrib><creatorcontrib>Heeg, Corinna</creatorcontrib><creatorcontrib>Wirtz, Markus</creatorcontrib><creatorcontrib>Hell, Rüdiger</creatorcontrib><title>Successful Fertilization Requires the Presence of at Least One Major O-Acetylserine(thiol)lyase for Cysteine Synthesis in Pollen of Arabidopsis</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>The synthesis of cysteine (Cys) is a master control switch of plant primary metabolism that coordinates the flux of sulfur with carbon and nitrogen metabolism. In Arabidopsis (Arabidopsis thaliana), nine genes encode for O-acetylserine(thiol)lyase (OAS-TL)-like proteins, of which the major isoforms, OAS-TL A, OAS-TL B, and OAS-TL C, catalyze the formation of Cys by combining O-acetylserine and sulfide in the cytosol, the plastids, and the mitochondria, respectively. So far, the significance of individual OAS-TL-like enzymes is unresolved. Generation of all major OAS-TL double loss-of-function mutants in combination with radiolabeled tracer studies revealed that subcellular localization of OAS-TL proteins is more important for efficient Cys synthesis than total cellular OAS-TL activity in leaves. The absence of oastl triple embryos after targeted crosses indicated the exclusiveness of Cys synthesis by the three major OAS-TLs and ruled out alternative sulfur fixation by other OAS-TL-like proteins. Analyses of oastlABC pollen demonstrated that the presence of at least one functional OAS-TL isoform is essential for the proper function of the male gametophyte, although the synthesis of histidine, lysine, and tryptophan is dispensable in pollen. Comparisons of oastlABC pollen derived from genetically different parent plant combinations allowed us to separate distinct functions of Cys and glutathione in pollen and revealed an additional role of glutathione for pollen germination. In contrast, female gametogenesis was not affected by the absence of major OAS-TLs, indicating significant transport of Cys into the developing ovule from the mother plant.</description><subject>Arabidopsis - enzymology</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - physiology</subject><subject>BIOCHEMISTRY AND METABOLISM</subject><subject>Biological and medical sciences</subject><subject>Carbon-Oxygen Lyases - metabolism</subject><subject>Chromosome Segregation</subject><subject>Crosses, Genetic</subject><subject>Cysteine - biosynthesis</subject><subject>Fertilization - physiology</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gametophytes</subject><subject>Gene Dosage - genetics</subject><subject>Germination</subject><subject>Germination - physiology</subject><subject>Mutation - genetics</subject><subject>Phenotype</subject><subject>Phenotypes</subject><subject>Plant physiology and development</subject><subject>Plants</subject><subject>Pollen</subject><subject>Pollen - enzymology</subject><subject>Pollen - physiology</subject><subject>Protein isoforms</subject><subject>Seeds</subject><subject>Sulfhydryl Compounds - metabolism</subject><subject>Sulfides</subject><subject>Sulfur</subject><subject>Sulfur - metabolism</subject><subject>Thiols</subject><subject>Tissue Survival</subject><subject>Tritium - metabolism</subject><issn>0032-0889</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkV-LEzEUxYMobq0--qjkRVgfZr2ZJPPnRSjFVaHSxdXnIZPesSlpMptkhPol_MqmtO7q0zlwfpwbcgh5yeCKMRDvxjErvypLVgI8IjMmeVmUUjSPyQwge2ia9oI8i3EHAIwz8ZRclCLbCpoZ-X07aY0xDpOl1xiSseaXSsY7-hXvJhMw0rRFepMNOo3UD1QlukIVE107pF_Uzge6LhYa08FGDMbhZdoab9_ag4pIhxwvDzFhDujtweW2aCI1jt54a9EdGxdB9Wbjxxw8J08GlXtenHVOvl9_-Lb8VKzWHz8vF6tCS5Cp0NBWgjO-kT20reZtgzBwIbNp6qGXWLdio6uNUgNUpZZ9XTVQSY6C9WVfAp-T96fecer3uNHoUlC2G4PZq3DovDLd_4kz2-6H_9nxuuVQs1xweS4I_m7CmLq9iRqtVQ79FDsmBBfAeXO8VZxQHXyMAYf7Mwy644jdOGbl3WnEzL_-92339N_VMvDmDKiolR2CctrEB65uQNb5f-bk1YnbxeTDQ85l29Ss4n8AxIWwpA</recordid><startdate>20131001</startdate><enddate>20131001</enddate><creator>Birke, Hannah</creator><creator>Heeg, Corinna</creator><creator>Wirtz, Markus</creator><creator>Hell, Rüdiger</creator><general>American Society of Plant Biologists</general><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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20131001</creationdate><title>Successful Fertilization Requires the Presence of at Least One Major O-Acetylserine(thiol)lyase for Cysteine Synthesis in Pollen of Arabidopsis</title><author>Birke, Hannah ; Heeg, Corinna ; Wirtz, Markus ; Hell, Rüdiger</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c505t-c0964313d5b099c398e0f34539887fb5e794dc6daaf062c5b7680653e41b2b203</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Arabidopsis - enzymology</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - physiology</topic><topic>BIOCHEMISTRY AND METABOLISM</topic><topic>Biological and medical sciences</topic><topic>Carbon-Oxygen Lyases - metabolism</topic><topic>Chromosome Segregation</topic><topic>Crosses, Genetic</topic><topic>Cysteine - biosynthesis</topic><topic>Fertilization - physiology</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gametophytes</topic><topic>Gene Dosage - genetics</topic><topic>Germination</topic><topic>Germination - physiology</topic><topic>Mutation - genetics</topic><topic>Phenotype</topic><topic>Phenotypes</topic><topic>Plant physiology and development</topic><topic>Plants</topic><topic>Pollen</topic><topic>Pollen - enzymology</topic><topic>Pollen - physiology</topic><topic>Protein isoforms</topic><topic>Seeds</topic><topic>Sulfhydryl Compounds - metabolism</topic><topic>Sulfides</topic><topic>Sulfur</topic><topic>Sulfur - metabolism</topic><topic>Thiols</topic><topic>Tissue Survival</topic><topic>Tritium - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Birke, Hannah</creatorcontrib><creatorcontrib>Heeg, Corinna</creatorcontrib><creatorcontrib>Wirtz, Markus</creatorcontrib><creatorcontrib>Hell, Rüdiger</creatorcontrib><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>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>Birke, Hannah</au><au>Heeg, Corinna</au><au>Wirtz, Markus</au><au>Hell, Rüdiger</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Successful Fertilization Requires the Presence of at Least One Major O-Acetylserine(thiol)lyase for Cysteine Synthesis in Pollen of Arabidopsis</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2013-10-01</date><risdate>2013</risdate><volume>163</volume><issue>2</issue><spage>959</spage><epage>972</epage><pages>959-972</pages><issn>0032-0889</issn><eissn>1532-2548</eissn><coden>PPHYA5</coden><abstract>The synthesis of cysteine (Cys) is a master control switch of plant primary metabolism that coordinates the flux of sulfur with carbon and nitrogen metabolism. In Arabidopsis (Arabidopsis thaliana), nine genes encode for O-acetylserine(thiol)lyase (OAS-TL)-like proteins, of which the major isoforms, OAS-TL A, OAS-TL B, and OAS-TL C, catalyze the formation of Cys by combining O-acetylserine and sulfide in the cytosol, the plastids, and the mitochondria, respectively. So far, the significance of individual OAS-TL-like enzymes is unresolved. Generation of all major OAS-TL double loss-of-function mutants in combination with radiolabeled tracer studies revealed that subcellular localization of OAS-TL proteins is more important for efficient Cys synthesis than total cellular OAS-TL activity in leaves. The absence of oastl triple embryos after targeted crosses indicated the exclusiveness of Cys synthesis by the three major OAS-TLs and ruled out alternative sulfur fixation by other OAS-TL-like proteins. Analyses of oastlABC pollen demonstrated that the presence of at least one functional OAS-TL isoform is essential for the proper function of the male gametophyte, although the synthesis of histidine, lysine, and tryptophan is dispensable in pollen. Comparisons of oastlABC pollen derived from genetically different parent plant combinations allowed us to separate distinct functions of Cys and glutathione in pollen and revealed an additional role of glutathione for pollen germination. In contrast, female gametogenesis was not affected by the absence of major OAS-TLs, indicating significant transport of Cys into the developing ovule from the mother plant.</abstract><cop>Rockville, MD</cop><pub>American Society of Plant Biologists</pub><pmid>24001608</pmid><doi>10.1104/pp.113.221200</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis - enzymology Arabidopsis - genetics Arabidopsis - physiology BIOCHEMISTRY AND METABOLISM Biological and medical sciences Carbon-Oxygen Lyases - metabolism Chromosome Segregation Crosses, Genetic Cysteine - biosynthesis Fertilization - physiology Fundamental and applied biological sciences. Psychology Gametophytes Gene Dosage - genetics Germination Germination - physiology Mutation - genetics Phenotype Phenotypes Plant physiology and development Plants Pollen Pollen - enzymology Pollen - physiology Protein isoforms Seeds Sulfhydryl Compounds - metabolism Sulfides Sulfur Sulfur - metabolism Thiols Tissue Survival Tritium - metabolism |
title | Successful Fertilization Requires the Presence of at Least One Major O-Acetylserine(thiol)lyase for Cysteine Synthesis in Pollen of Arabidopsis |
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