Evidence for chloroplast control of external Ca²⁺-induced cytosolic Ca²⁺ transients and stomatal closure
The role of guard cell chloroplasts in stomatal function is controversial. It is usually assumed that stomatal closure is preceded by a transient increase in cytosolic free Ca²⁺ concentration ([Ca²⁺]cyt) in the guard cells. Here, we provide the evidence that chloroplasts play a critical role in the...
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description | The role of guard cell chloroplasts in stomatal function is controversial. It is usually assumed that stomatal closure is preceded by a transient increase in cytosolic free Ca²⁺ concentration ([Ca²⁺]cyt) in the guard cells. Here, we provide the evidence that chloroplasts play a critical role in the generation of extracellular Ca²⁺ ([Ca²⁺]ext)-induced [Ca²⁺]cyt transients and stomatal closure in Arabidopsis. CAS (Ca²⁺ sensing receptor) is a plant-specific putative Ca²⁺-binding protein that was originally proposed to be a plasma membrane-localized external Ca²⁺ sensor. In the present study, we characterized the intracellular localization of CAS in Arabidopsis with a combination of techniques, including (i) in vivo localization of green fluorescent protein (GFP) fused gene expression, (ii) subcellular fractionation and fractional analysis of CAS with Western blots, and (iii) database analysis of thylakoid membrane proteomes. Each technique produced consistent results. CAS was localized mainly to chloroplasts. It is an integral thylakoid membrane protein, and the N-terminus acidic Ca²⁺-binding region is likely exposed to the stromal side of the membrane. The phenotype of T-DNA insertion CAS knockout mutants and cDNA mutant-complemented plants revealed that CAS is essential for stomatal closure induced by external Ca²⁺. In contrast, overexpression of CAS promoted stomatal closure in the absence of externally applied Ca²⁺. Furthermore, using the transgenic aequorin system, we showed that [Ca²⁺]ext-induced [Ca²⁺]cyt transients were significantly reduced in CAS knockout mutants. Our results suggest that thylakoid membrane-localized CAS is essential for [Ca²⁺]ext-induced [Ca²⁺]cyt transients and stomatal closure. |
doi_str_mv | 10.1111/j.1365-313X.2007.03390.x |
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It is usually assumed that stomatal closure is preceded by a transient increase in cytosolic free Ca²⁺ concentration ([Ca²⁺]cyt) in the guard cells. Here, we provide the evidence that chloroplasts play a critical role in the generation of extracellular Ca²⁺ ([Ca²⁺]ext)-induced [Ca²⁺]cyt transients and stomatal closure in Arabidopsis. CAS (Ca²⁺ sensing receptor) is a plant-specific putative Ca²⁺-binding protein that was originally proposed to be a plasma membrane-localized external Ca²⁺ sensor. In the present study, we characterized the intracellular localization of CAS in Arabidopsis with a combination of techniques, including (i) in vivo localization of green fluorescent protein (GFP) fused gene expression, (ii) subcellular fractionation and fractional analysis of CAS with Western blots, and (iii) database analysis of thylakoid membrane proteomes. Each technique produced consistent results. CAS was localized mainly to chloroplasts. It is an integral thylakoid membrane protein, and the N-terminus acidic Ca²⁺-binding region is likely exposed to the stromal side of the membrane. The phenotype of T-DNA insertion CAS knockout mutants and cDNA mutant-complemented plants revealed that CAS is essential for stomatal closure induced by external Ca²⁺. In contrast, overexpression of CAS promoted stomatal closure in the absence of externally applied Ca²⁺. Furthermore, using the transgenic aequorin system, we showed that [Ca²⁺]ext-induced [Ca²⁺]cyt transients were significantly reduced in CAS knockout mutants. Our results suggest that thylakoid membrane-localized CAS is essential for [Ca²⁺]ext-induced [Ca²⁺]cyt transients and stomatal closure.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/j.1365-313X.2007.03390.x</identifier><identifier>PMID: 18088326</identifier><language>eng</language><publisher>Oxford, UK: Oxford, UK : Blackwell Publishing Ltd</publisher><subject>Arabidopsis ; Arabidopsis - genetics ; Arabidopsis - metabolism ; Binding sites ; Biological and medical sciences ; Botany ; Calcium - metabolism ; Calcium - pharmacology ; calcium signaling ; Calcium Signaling - physiology ; CAS ; Cell structures and functions ; Cellular biology ; Chlorophyll - metabolism ; Chloroplast, photosynthetic membrane and photosynthesis ; chloroplasts ; Chloroplasts - metabolism ; Cytosol - drug effects ; Cytosol - metabolism ; extracellular Ca ; extracellular Ca2 ; Fundamental and applied biological sciences. Psychology ; Gene expression ; Gene Expression Regulation, Plant - physiology ; Molecular and cellular biology ; Plant Stomata - drug effects ; Plant Stomata - metabolism ; Plants, Genetically Modified ; Proteins ; Receptors, Calcium-Sensing - metabolism ; Seedlings - genetics ; Seedlings - metabolism ; stomatal movement</subject><ispartof>The Plant journal : for cell and molecular biology, 2008-03, Vol.53 (6), p.988-998</ispartof><rights>2008 The Authors</rights><rights>2008 INIST-CNRS</rights><rights>Journal compilation © 2008 Blackwell Publishing Ltd and the Society for Experimental Biology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4760-cee5fd8d422e4137123f5949ae3dcaee19a770e75ca7ab64763d436cdd77425c3</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fj.1365-313X.2007.03390.x$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fj.1365-313X.2007.03390.x$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=20206890$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18088326$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Nomura, Hironari</creatorcontrib><creatorcontrib>Komori, Teiko</creatorcontrib><creatorcontrib>Kobori, Maki</creatorcontrib><creatorcontrib>Nakahira, Yoichi</creatorcontrib><creatorcontrib>Shiina, Takashi</creatorcontrib><title>Evidence for chloroplast control of external Ca²⁺-induced cytosolic Ca²⁺ transients and stomatal closure</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>The role of guard cell chloroplasts in stomatal function is controversial. It is usually assumed that stomatal closure is preceded by a transient increase in cytosolic free Ca²⁺ concentration ([Ca²⁺]cyt) in the guard cells. Here, we provide the evidence that chloroplasts play a critical role in the generation of extracellular Ca²⁺ ([Ca²⁺]ext)-induced [Ca²⁺]cyt transients and stomatal closure in Arabidopsis. CAS (Ca²⁺ sensing receptor) is a plant-specific putative Ca²⁺-binding protein that was originally proposed to be a plasma membrane-localized external Ca²⁺ sensor. In the present study, we characterized the intracellular localization of CAS in Arabidopsis with a combination of techniques, including (i) in vivo localization of green fluorescent protein (GFP) fused gene expression, (ii) subcellular fractionation and fractional analysis of CAS with Western blots, and (iii) database analysis of thylakoid membrane proteomes. Each technique produced consistent results. CAS was localized mainly to chloroplasts. It is an integral thylakoid membrane protein, and the N-terminus acidic Ca²⁺-binding region is likely exposed to the stromal side of the membrane. The phenotype of T-DNA insertion CAS knockout mutants and cDNA mutant-complemented plants revealed that CAS is essential for stomatal closure induced by external Ca²⁺. In contrast, overexpression of CAS promoted stomatal closure in the absence of externally applied Ca²⁺. Furthermore, using the transgenic aequorin system, we showed that [Ca²⁺]ext-induced [Ca²⁺]cyt transients were significantly reduced in CAS knockout mutants. Our results suggest that thylakoid membrane-localized CAS is essential for [Ca²⁺]ext-induced [Ca²⁺]cyt transients and stomatal closure.</description><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Binding sites</subject><subject>Biological and medical sciences</subject><subject>Botany</subject><subject>Calcium - metabolism</subject><subject>Calcium - pharmacology</subject><subject>calcium signaling</subject><subject>Calcium Signaling - physiology</subject><subject>CAS</subject><subject>Cell structures and functions</subject><subject>Cellular biology</subject><subject>Chlorophyll - metabolism</subject><subject>Chloroplast, photosynthetic membrane and photosynthesis</subject><subject>chloroplasts</subject><subject>Chloroplasts - metabolism</subject><subject>Cytosol - drug effects</subject><subject>Cytosol - metabolism</subject><subject>extracellular Ca</subject><subject>extracellular Ca2</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant - physiology</subject><subject>Molecular and cellular biology</subject><subject>Plant Stomata - drug effects</subject><subject>Plant Stomata - metabolism</subject><subject>Plants, Genetically Modified</subject><subject>Proteins</subject><subject>Receptors, Calcium-Sensing - metabolism</subject><subject>Seedlings - genetics</subject><subject>Seedlings - metabolism</subject><subject>stomatal movement</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2008</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc1u1DAUhS0EotPCK4CFRHcJ13ZiJwsW1aj8qRJItBI7y7VvICNPPNgJzCx5JZYseRSeBIeZFokN3tjS_c7x1TmEUAYly-fZqmRC1oVg4kPJAVQJQrRQbu-Qxe3gLllAK6FQFeNH5DilFQBTQlb3yRFroGkElwsynH_pHQ4WaRcitZ98iGHjTRqpDcMYg6eho7gdMQ7G06X5-f3Xtx9FP7jJoqN2N4YUfG9vJnSMZkg9DmOiZnA0jWFtxqy0PqQp4gNyrzM-4cPDfUKuXpxfLl8VF29fvl6eXRS2Unlni1h3rnEV51gxoRgXXd1WrUHhrEFkrVEKUNXWKHMts0a4SkjrnFIVr604Iad7300MnydMo173yaL3ZsAwJa1AtKzNqf0P5FA1QkiVwSf_gKswzaFkhom8JBeQoUcHaLpeo9Ob2K9N3OmbvDPw9ACYZI3vclq2T7ccBw6yaWej53vua-9x99cH9Ny_Xum5Zj3XrOf-9Z_-9VZfvnszv7L-8V7fmaDNx5j_uHrPgQmARjacSfEbQ4uwYA</recordid><startdate>200803</startdate><enddate>200803</enddate><creator>Nomura, Hironari</creator><creator>Komori, Teiko</creator><creator>Kobori, Maki</creator><creator>Nakahira, Yoichi</creator><creator>Shiina, Takashi</creator><general>Oxford, UK : Blackwell Publishing Ltd</general><general>Blackwell Publishing Ltd</general><general>Blackwell Science</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>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>200803</creationdate><title>Evidence for chloroplast control of external Ca²⁺-induced cytosolic Ca²⁺ transients and stomatal closure</title><author>Nomura, Hironari ; Komori, Teiko ; Kobori, Maki ; Nakahira, Yoichi ; Shiina, Takashi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4760-cee5fd8d422e4137123f5949ae3dcaee19a770e75ca7ab64763d436cdd77425c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2008</creationdate><topic>Arabidopsis</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Binding sites</topic><topic>Biological and medical sciences</topic><topic>Botany</topic><topic>Calcium - metabolism</topic><topic>Calcium - pharmacology</topic><topic>calcium signaling</topic><topic>Calcium Signaling - physiology</topic><topic>CAS</topic><topic>Cell structures and functions</topic><topic>Cellular biology</topic><topic>Chlorophyll - metabolism</topic><topic>Chloroplast, photosynthetic membrane and photosynthesis</topic><topic>chloroplasts</topic><topic>Chloroplasts - metabolism</topic><topic>Cytosol - drug effects</topic><topic>Cytosol - metabolism</topic><topic>extracellular Ca</topic><topic>extracellular Ca2</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant - physiology</topic><topic>Molecular and cellular biology</topic><topic>Plant Stomata - drug effects</topic><topic>Plant Stomata - metabolism</topic><topic>Plants, Genetically Modified</topic><topic>Proteins</topic><topic>Receptors, Calcium-Sensing - metabolism</topic><topic>Seedlings - genetics</topic><topic>Seedlings - metabolism</topic><topic>stomatal movement</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nomura, Hironari</creatorcontrib><creatorcontrib>Komori, Teiko</creatorcontrib><creatorcontrib>Kobori, Maki</creatorcontrib><creatorcontrib>Nakahira, Yoichi</creatorcontrib><creatorcontrib>Shiina, Takashi</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>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nomura, Hironari</au><au>Komori, Teiko</au><au>Kobori, Maki</au><au>Nakahira, Yoichi</au><au>Shiina, Takashi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Evidence for chloroplast control of external Ca²⁺-induced cytosolic Ca²⁺ transients and stomatal closure</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2008-03</date><risdate>2008</risdate><volume>53</volume><issue>6</issue><spage>988</spage><epage>998</epage><pages>988-998</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>The role of guard cell chloroplasts in stomatal function is controversial. It is usually assumed that stomatal closure is preceded by a transient increase in cytosolic free Ca²⁺ concentration ([Ca²⁺]cyt) in the guard cells. Here, we provide the evidence that chloroplasts play a critical role in the generation of extracellular Ca²⁺ ([Ca²⁺]ext)-induced [Ca²⁺]cyt transients and stomatal closure in Arabidopsis. CAS (Ca²⁺ sensing receptor) is a plant-specific putative Ca²⁺-binding protein that was originally proposed to be a plasma membrane-localized external Ca²⁺ sensor. In the present study, we characterized the intracellular localization of CAS in Arabidopsis with a combination of techniques, including (i) in vivo localization of green fluorescent protein (GFP) fused gene expression, (ii) subcellular fractionation and fractional analysis of CAS with Western blots, and (iii) database analysis of thylakoid membrane proteomes. Each technique produced consistent results. CAS was localized mainly to chloroplasts. It is an integral thylakoid membrane protein, and the N-terminus acidic Ca²⁺-binding region is likely exposed to the stromal side of the membrane. The phenotype of T-DNA insertion CAS knockout mutants and cDNA mutant-complemented plants revealed that CAS is essential for stomatal closure induced by external Ca²⁺. In contrast, overexpression of CAS promoted stomatal closure in the absence of externally applied Ca²⁺. Furthermore, using the transgenic aequorin system, we showed that [Ca²⁺]ext-induced [Ca²⁺]cyt transients were significantly reduced in CAS knockout mutants. Our results suggest that thylakoid membrane-localized CAS is essential for [Ca²⁺]ext-induced [Ca²⁺]cyt transients and stomatal closure.</abstract><cop>Oxford, UK</cop><pub>Oxford, UK : Blackwell Publishing Ltd</pub><pmid>18088326</pmid><doi>10.1111/j.1365-313X.2007.03390.x</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis Arabidopsis - genetics Arabidopsis - metabolism Binding sites Biological and medical sciences Botany Calcium - metabolism Calcium - pharmacology calcium signaling Calcium Signaling - physiology CAS Cell structures and functions Cellular biology Chlorophyll - metabolism Chloroplast, photosynthetic membrane and photosynthesis chloroplasts Chloroplasts - metabolism Cytosol - drug effects Cytosol - metabolism extracellular Ca extracellular Ca2 Fundamental and applied biological sciences. Psychology Gene expression Gene Expression Regulation, Plant - physiology Molecular and cellular biology Plant Stomata - drug effects Plant Stomata - metabolism Plants, Genetically Modified Proteins Receptors, Calcium-Sensing - metabolism Seedlings - genetics Seedlings - metabolism stomatal movement |
title | Evidence for chloroplast control of external Ca²⁺-induced cytosolic Ca²⁺ transients and stomatal closure |
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