Identification of Features Regulating OST1 Kinase Activity and OST1 Function in Guard Cells
The phytohormone abscisic acid (ABA) mediates drought responses in plants and, in particular, triggers stomatal closure. Snf1-related kinase 2 (SnRK2) proteins from several plant species have been implicated in ABA-signaling pathways. In Arabidopsis (Arabidopsis thaliana) guard cells, OPEN STOMATA 1...
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| Veröffentlicht in: | Plant physiology (Bethesda) 2006-08, Vol.141 (4), p.1316-1327 |
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| creator | Belin, Christophe Franco, Pierre-Olivier de Bourbousse, Clara Chaignepain, Stéphane Schmitter, Jean-Marie Vavasseur, Alain Giraudat, Jérôme Barbier-Brygoo, Hélène Thomine, Sébastien |
| description | The phytohormone abscisic acid (ABA) mediates drought responses in plants and, in particular, triggers stomatal closure. Snf1-related kinase 2 (SnRK2) proteins from several plant species have been implicated in ABA-signaling pathways. In Arabidopsis (Arabidopsis thaliana) guard cells, OPEN STOMATA 1 (OST1)/SRK2E/SnRK2-6 is a critical positive regulator of ABA signal transduction. A better understanding of the mechanisms responsible for SnRK2 protein kinase activation is thus a major goal toward understanding ABA signal transduction. Here, we report successful purification of OST1 produced in Escherichia coli: The protein is active and autophosphorylates. Using mass spectrometry, we identified five target residues of autophosphorylation in recombinant OST1. Sequence analysis delineates two conserved boxes located in the carboxy-terminal moiety of OST1 after the catalytic domain: the SnRK2-specific box (glutamine-303 to proline-318) and the ABA-specific box (leucine-333 to methionine-362). Site-directed mutagenesis and serial deletions reveal that serine (Ser)-175 in the activation loop and the SnRK2-specific box are critical for the activity of recombinant OST1 kinase. Targeted expression of variants of OST1 kinase in guard cells uncovered additional features that are critical for OST1 function in ABA signaling, although not required for OST1 kinase activity: Ser-7, Ser-18, and Ser-29 and the ABA-specific box. Ser-7, Ser-18, Ser-29, and Ser-43 represent putative targets for regulatory phosphorylation and the ABA-specific box may be a target for the binding of signaling partners in guard cells. |
| doi_str_mv | 10.1104/pp.106.079327 |
| format | Article |
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Snf1-related kinase 2 (SnRK2) proteins from several plant species have been implicated in ABA-signaling pathways. In Arabidopsis (Arabidopsis thaliana) guard cells, OPEN STOMATA 1 (OST1)/SRK2E/SnRK2-6 is a critical positive regulator of ABA signal transduction. A better understanding of the mechanisms responsible for SnRK2 protein kinase activation is thus a major goal toward understanding ABA signal transduction. Here, we report successful purification of OST1 produced in Escherichia coli: The protein is active and autophosphorylates. Using mass spectrometry, we identified five target residues of autophosphorylation in recombinant OST1. Sequence analysis delineates two conserved boxes located in the carboxy-terminal moiety of OST1 after the catalytic domain: the SnRK2-specific box (glutamine-303 to proline-318) and the ABA-specific box (leucine-333 to methionine-362). Site-directed mutagenesis and serial deletions reveal that serine (Ser)-175 in the activation loop and the SnRK2-specific box are critical for the activity of recombinant OST1 kinase. Targeted expression of variants of OST1 kinase in guard cells uncovered additional features that are critical for OST1 function in ABA signaling, although not required for OST1 kinase activity: Ser-7, Ser-18, and Ser-29 and the ABA-specific box. Ser-7, Ser-18, Ser-29, and Ser-43 represent putative targets for regulatory phosphorylation and the ABA-specific box may be a target for the binding of signaling partners in guard cells.</description><identifier>ISSN: 0032-0889</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.106.079327</identifier><identifier>PMID: 16766677</identifier><identifier>CODEN: PPHYA5</identifier><language>eng</language><publisher>Rockville, MD: American Society of Plant Biologists</publisher><subject>Abscisic Acid ; Abscisic Acid - metabolism ; Amino Acid Motifs ; Amino Acid Sequence ; Arabidopsis ; Arabidopsis - cytology ; Arabidopsis - enzymology ; Arabidopsis Proteins ; Arabidopsis Proteins - chemistry ; Arabidopsis Proteins - isolation & purification ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; Biological and medical sciences ; Cell Biology and Signal Transduction ; Cell physiology ; Conserved Sequence ; Escherichia coli ; Escherichia coli - genetics ; Fundamental and applied biological sciences. Psychology ; Guard cells ; Histones ; Leaves ; Life Sciences ; Mass Spectrometry ; Molecular and cellular biology ; Molecular Sequence Data ; Mutagenesis, Site-Directed ; Phosphatases ; Phosphorylation ; Physiological regulation ; Protein Kinases ; Protein Kinases - chemistry ; Protein Kinases - isolation & purification ; Protein Kinases - metabolism ; Protein Structure, Tertiary ; Proteins ; Recombinant Fusion Proteins ; Recombinant Fusion Proteins - metabolism ; Recombinant proteins ; Rice ; Sequence Alignment ; Sequence Analysis, Protein ; Serine ; Serine - physiology ; Signal Transduction ; Vegetal Biology</subject><ispartof>Plant physiology (Bethesda), 2006-08, Vol.141 (4), p.1316-1327</ispartof><rights>Copyright 2006 American Society of Plant Biologists</rights><rights>2006 INIST-CNRS</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>Copyright © 2006, American Society of Plant Biologists 2006</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c629t-35c0d01ca4f132dae823e7d92644ecc2ea2cd560d03458217c94a124ab7257a03</citedby><cites>FETCH-LOGICAL-c629t-35c0d01ca4f132dae823e7d92644ecc2ea2cd560d03458217c94a124ab7257a03</cites><orcidid>0000-0001-6464-6124 ; 0000-0003-0045-1701 ; 0000-0003-2129-5349</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/20205858$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/20205858$$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=18026977$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/16766677$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-00119901$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Belin, Christophe</creatorcontrib><creatorcontrib>Franco, Pierre-Olivier de</creatorcontrib><creatorcontrib>Bourbousse, Clara</creatorcontrib><creatorcontrib>Chaignepain, Stéphane</creatorcontrib><creatorcontrib>Schmitter, Jean-Marie</creatorcontrib><creatorcontrib>Vavasseur, Alain</creatorcontrib><creatorcontrib>Giraudat, Jérôme</creatorcontrib><creatorcontrib>Barbier-Brygoo, Hélène</creatorcontrib><creatorcontrib>Thomine, Sébastien</creatorcontrib><title>Identification of Features Regulating OST1 Kinase Activity and OST1 Function in Guard Cells</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>The phytohormone abscisic acid (ABA) mediates drought responses in plants and, in particular, triggers stomatal closure. Snf1-related kinase 2 (SnRK2) proteins from several plant species have been implicated in ABA-signaling pathways. In Arabidopsis (Arabidopsis thaliana) guard cells, OPEN STOMATA 1 (OST1)/SRK2E/SnRK2-6 is a critical positive regulator of ABA signal transduction. A better understanding of the mechanisms responsible for SnRK2 protein kinase activation is thus a major goal toward understanding ABA signal transduction. Here, we report successful purification of OST1 produced in Escherichia coli: The protein is active and autophosphorylates. Using mass spectrometry, we identified five target residues of autophosphorylation in recombinant OST1. Sequence analysis delineates two conserved boxes located in the carboxy-terminal moiety of OST1 after the catalytic domain: the SnRK2-specific box (glutamine-303 to proline-318) and the ABA-specific box (leucine-333 to methionine-362). Site-directed mutagenesis and serial deletions reveal that serine (Ser)-175 in the activation loop and the SnRK2-specific box are critical for the activity of recombinant OST1 kinase. Targeted expression of variants of OST1 kinase in guard cells uncovered additional features that are critical for OST1 function in ABA signaling, although not required for OST1 kinase activity: Ser-7, Ser-18, and Ser-29 and the ABA-specific box. Ser-7, Ser-18, Ser-29, and Ser-43 represent putative targets for regulatory phosphorylation and the ABA-specific box may be a target for the binding of signaling partners in guard cells.</description><subject>Abscisic Acid</subject><subject>Abscisic Acid - metabolism</subject><subject>Amino Acid Motifs</subject><subject>Amino Acid Sequence</subject><subject>Arabidopsis</subject><subject>Arabidopsis - cytology</subject><subject>Arabidopsis - enzymology</subject><subject>Arabidopsis Proteins</subject><subject>Arabidopsis Proteins - chemistry</subject><subject>Arabidopsis Proteins - isolation & purification</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>Biological and medical sciences</subject><subject>Cell Biology and Signal Transduction</subject><subject>Cell physiology</subject><subject>Conserved Sequence</subject><subject>Escherichia coli</subject><subject>Escherichia coli - genetics</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Guard cells</subject><subject>Histones</subject><subject>Leaves</subject><subject>Life Sciences</subject><subject>Mass Spectrometry</subject><subject>Molecular and cellular biology</subject><subject>Molecular Sequence Data</subject><subject>Mutagenesis, Site-Directed</subject><subject>Phosphatases</subject><subject>Phosphorylation</subject><subject>Physiological regulation</subject><subject>Protein Kinases</subject><subject>Protein Kinases - chemistry</subject><subject>Protein Kinases - isolation & purification</subject><subject>Protein Kinases - metabolism</subject><subject>Protein Structure, Tertiary</subject><subject>Proteins</subject><subject>Recombinant Fusion Proteins</subject><subject>Recombinant Fusion Proteins - metabolism</subject><subject>Recombinant proteins</subject><subject>Rice</subject><subject>Sequence Alignment</subject><subject>Sequence Analysis, Protein</subject><subject>Serine</subject><subject>Serine - physiology</subject><subject>Signal Transduction</subject><subject>Vegetal Biology</subject><issn>0032-0889</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2006</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkk1v1DAQhi0EosvCkSOQC5U4ZPFX_HFBWq26bcVKlWh74mBNHWfrKuukdrJS_z1us2oB-eDRvM-81swYoY8ELwjB_HvfLwgWCyw1o_IVmpGK0ZJWXL1GM4xzjJXSR-hdSncYY8IIf4uOiJBCCCln6Pd57cLgG29h8F0ouqZYOxjG6FLxy23HNqfDtri4vCLFTx8guWJpB7_3w0MBoZ6E9RjsU7UPxekIsS5Wrm3Te_SmgTa5D4d7jq7XJ1ers3JzcXq-Wm5KK6geSlZZXGNigTeE0RqcoszJWlPBubOWOqC2rkRmGK8UJdJqDoRyuJG0koDZHP2YfPvxZudqmxuK0Jo--h3EB9OBN_8qwd-abbc3eVZM5zNH3yaD2__KzpYb85jLgyNaY7InmT0-PBa7-9Glwex8srldCK4bkyFaSlVRkcFyAm3sUoqueXYm2DyuzvR9DoWZVpf5z3938UIfdpWBrwcAkoW2iRCsTy-cwlToJ-7TxN2loYvPOsUUV6pSWf8y6Q10BrYxe1xf0vw1MMGaEyXYH6n2svk</recordid><startdate>20060801</startdate><enddate>20060801</enddate><creator>Belin, Christophe</creator><creator>Franco, Pierre-Olivier de</creator><creator>Bourbousse, Clara</creator><creator>Chaignepain, Stéphane</creator><creator>Schmitter, Jean-Marie</creator><creator>Vavasseur, Alain</creator><creator>Giraudat, Jérôme</creator><creator>Barbier-Brygoo, Hélène</creator><creator>Thomine, Sébastien</creator><general>American Society of Plant Biologists</general><general>American Society of Plant Physiologists</general><general>Oxford University Press ; American Society of Plant Biologists</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>7QL</scope><scope>C1K</scope><scope>1XC</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-6464-6124</orcidid><orcidid>https://orcid.org/0000-0003-0045-1701</orcidid><orcidid>https://orcid.org/0000-0003-2129-5349</orcidid></search><sort><creationdate>20060801</creationdate><title>Identification of Features Regulating OST1 Kinase Activity and OST1 Function in Guard Cells</title><author>Belin, Christophe ; Franco, Pierre-Olivier de ; Bourbousse, Clara ; Chaignepain, Stéphane ; Schmitter, Jean-Marie ; Vavasseur, Alain ; Giraudat, Jérôme ; Barbier-Brygoo, Hélène ; Thomine, Sébastien</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c629t-35c0d01ca4f132dae823e7d92644ecc2ea2cd560d03458217c94a124ab7257a03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2006</creationdate><topic>Abscisic Acid</topic><topic>Abscisic Acid - metabolism</topic><topic>Amino Acid Motifs</topic><topic>Amino Acid Sequence</topic><topic>Arabidopsis</topic><topic>Arabidopsis - cytology</topic><topic>Arabidopsis - enzymology</topic><topic>Arabidopsis Proteins</topic><topic>Arabidopsis Proteins - chemistry</topic><topic>Arabidopsis Proteins - isolation & purification</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Arabidopsis thaliana</topic><topic>Biological and medical sciences</topic><topic>Cell Biology and Signal Transduction</topic><topic>Cell physiology</topic><topic>Conserved Sequence</topic><topic>Escherichia coli</topic><topic>Escherichia coli - genetics</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Guard cells</topic><topic>Histones</topic><topic>Leaves</topic><topic>Life Sciences</topic><topic>Mass Spectrometry</topic><topic>Molecular and cellular biology</topic><topic>Molecular Sequence Data</topic><topic>Mutagenesis, Site-Directed</topic><topic>Phosphatases</topic><topic>Phosphorylation</topic><topic>Physiological regulation</topic><topic>Protein Kinases</topic><topic>Protein Kinases - chemistry</topic><topic>Protein Kinases - isolation & purification</topic><topic>Protein Kinases - metabolism</topic><topic>Protein Structure, Tertiary</topic><topic>Proteins</topic><topic>Recombinant Fusion Proteins</topic><topic>Recombinant Fusion Proteins - metabolism</topic><topic>Recombinant proteins</topic><topic>Rice</topic><topic>Sequence Alignment</topic><topic>Sequence Analysis, Protein</topic><topic>Serine</topic><topic>Serine - physiology</topic><topic>Signal Transduction</topic><topic>Vegetal Biology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Belin, Christophe</creatorcontrib><creatorcontrib>Franco, Pierre-Olivier de</creatorcontrib><creatorcontrib>Bourbousse, Clara</creatorcontrib><creatorcontrib>Chaignepain, Stéphane</creatorcontrib><creatorcontrib>Schmitter, Jean-Marie</creatorcontrib><creatorcontrib>Vavasseur, Alain</creatorcontrib><creatorcontrib>Giraudat, Jérôme</creatorcontrib><creatorcontrib>Barbier-Brygoo, Hélène</creatorcontrib><creatorcontrib>Thomine, Sébastien</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>Bacteriology Abstracts (Microbiology B)</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Hyper Article en Ligne (HAL)</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>Belin, Christophe</au><au>Franco, Pierre-Olivier de</au><au>Bourbousse, Clara</au><au>Chaignepain, Stéphane</au><au>Schmitter, Jean-Marie</au><au>Vavasseur, Alain</au><au>Giraudat, Jérôme</au><au>Barbier-Brygoo, Hélène</au><au>Thomine, Sébastien</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Identification of Features Regulating OST1 Kinase Activity and OST1 Function in Guard Cells</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2006-08-01</date><risdate>2006</risdate><volume>141</volume><issue>4</issue><spage>1316</spage><epage>1327</epage><pages>1316-1327</pages><issn>0032-0889</issn><eissn>1532-2548</eissn><coden>PPHYA5</coden><abstract>The phytohormone abscisic acid (ABA) mediates drought responses in plants and, in particular, triggers stomatal closure. Snf1-related kinase 2 (SnRK2) proteins from several plant species have been implicated in ABA-signaling pathways. In Arabidopsis (Arabidopsis thaliana) guard cells, OPEN STOMATA 1 (OST1)/SRK2E/SnRK2-6 is a critical positive regulator of ABA signal transduction. A better understanding of the mechanisms responsible for SnRK2 protein kinase activation is thus a major goal toward understanding ABA signal transduction. Here, we report successful purification of OST1 produced in Escherichia coli: The protein is active and autophosphorylates. Using mass spectrometry, we identified five target residues of autophosphorylation in recombinant OST1. Sequence analysis delineates two conserved boxes located in the carboxy-terminal moiety of OST1 after the catalytic domain: the SnRK2-specific box (glutamine-303 to proline-318) and the ABA-specific box (leucine-333 to methionine-362). Site-directed mutagenesis and serial deletions reveal that serine (Ser)-175 in the activation loop and the SnRK2-specific box are critical for the activity of recombinant OST1 kinase. Targeted expression of variants of OST1 kinase in guard cells uncovered additional features that are critical for OST1 function in ABA signaling, although not required for OST1 kinase activity: Ser-7, Ser-18, and Ser-29 and the ABA-specific box. Ser-7, Ser-18, Ser-29, and Ser-43 represent putative targets for regulatory phosphorylation and the ABA-specific box may be a target for the binding of signaling partners in guard cells.</abstract><cop>Rockville, MD</cop><pub>American Society of Plant Biologists</pub><pmid>16766677</pmid><doi>10.1104/pp.106.079327</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-6464-6124</orcidid><orcidid>https://orcid.org/0000-0003-0045-1701</orcidid><orcidid>https://orcid.org/0000-0003-2129-5349</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | Plant physiology (Bethesda), 2006-08, Vol.141 (4), p.1316-1327 |
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| source | MEDLINE; JSTOR Archive Collection A-Z Listing; Oxford University Press Journals All Titles (1996-Current); EZB-FREE-00999 freely available EZB journals |
| subjects | Abscisic Acid Abscisic Acid - metabolism Amino Acid Motifs Amino Acid Sequence Arabidopsis Arabidopsis - cytology Arabidopsis - enzymology Arabidopsis Proteins Arabidopsis Proteins - chemistry Arabidopsis Proteins - isolation & purification Arabidopsis Proteins - metabolism Arabidopsis thaliana Biological and medical sciences Cell Biology and Signal Transduction Cell physiology Conserved Sequence Escherichia coli Escherichia coli - genetics Fundamental and applied biological sciences. Psychology Guard cells Histones Leaves Life Sciences Mass Spectrometry Molecular and cellular biology Molecular Sequence Data Mutagenesis, Site-Directed Phosphatases Phosphorylation Physiological regulation Protein Kinases Protein Kinases - chemistry Protein Kinases - isolation & purification Protein Kinases - metabolism Protein Structure, Tertiary Proteins Recombinant Fusion Proteins Recombinant Fusion Proteins - metabolism Recombinant proteins Rice Sequence Alignment Sequence Analysis, Protein Serine Serine - physiology Signal Transduction Vegetal Biology |
| title | Identification of Features Regulating OST1 Kinase Activity and OST1 Function in Guard Cells |
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