Calcium Pumps and Interacting BON1 Protein Modulate Calcium Signature, Stomatal Closure, and Plant Immunity
Calcium signaling is essential for environmental responses including immune responses. Here, we provide evidence that the evolutionarily conserved protein BONZAI1 (BON1) functions together with autoinhibited calcium ATPase10 (ACA10) and ACA8 to regulate calcium signals in Arabidopsis. BON1 is a plas...
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| Veröffentlicht in: | Plant physiology (Bethesda) 2017-09, Vol.175 (1), p.424-437 |
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| creator | Yang, Dong-Lei Shi, Zhenying Bao, Yongmei Yan, Jiapei Yang, Ziyuan Yu, Huiyun Li, Yun Gou, Mingyue Wang, Shu Zou, Baohong Xu, Dachao Ma, Zhiqi Kim, Jitae Hua, Jian |
| description | Calcium signaling is essential for environmental responses including immune responses. Here, we provide evidence that the evolutionarily conserved protein BONZAI1 (BON1) functions together with autoinhibited calcium ATPase10 (ACA10) and ACA8 to regulate calcium signals in Arabidopsis. BON1 is a plasma membrane localized protein that negatively regulates the expression of immune receptor genes and positively regulates stomatal closure. We found that BON1 interacts with the autoinhibitory domains of ACA10 and ACA8, and the aca10 loss-of-function (LOF) mutants have an autoimmune phenotype similar to that of the bon1 LOF mutants. Genetic evidences indicate that BON1 positively regulates the activities of ACA10 and ACA8. Consistent with this idea, the steady level of calcium concentration is increased in both aca10 and bon1 mutants. Most strikingly, cytosolic calcium oscillation imposed by external calcium treatment was altered in aca10, aca8, and bon1 mutants in guard cells. In addition, calcium- and pathogen-induced stomatal closure was compromised in the aca10 and bon1 mutants. Taken together, this study indicates that ACA10/8 and BON1 physically interact on plasma membrane and function in the generation of cytosol calcium signatures that are critical for stomatal movement and impact plant immunity. |
| doi_str_mv | 10.1104/pp.17.00495 |
| format | Article |
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Here, we provide evidence that the evolutionarily conserved protein BONZAI1 (BON1) functions together with autoinhibited calcium ATPase10 (ACA10) and ACA8 to regulate calcium signals in Arabidopsis. BON1 is a plasma membrane localized protein that negatively regulates the expression of immune receptor genes and positively regulates stomatal closure. We found that BON1 interacts with the autoinhibitory domains of ACA10 and ACA8, and the aca10 loss-of-function (LOF) mutants have an autoimmune phenotype similar to that of the bon1 LOF mutants. Genetic evidences indicate that BON1 positively regulates the activities of ACA10 and ACA8. Consistent with this idea, the steady level of calcium concentration is increased in both aca10 and bon1 mutants. Most strikingly, cytosolic calcium oscillation imposed by external calcium treatment was altered in aca10, aca8, and bon1 mutants in guard cells. In addition, calcium- and pathogen-induced stomatal closure was compromised in the aca10 and bon1 mutants. Taken together, this study indicates that ACA10/8 and BON1 physically interact on plasma membrane and function in the generation of cytosol calcium signatures that are critical for stomatal movement and impact plant immunity.</description><identifier>ISSN: 0032-0889</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.17.00495</identifier><identifier>PMID: 28701352</identifier><language>eng</language><publisher>United States: American Society of Plant Biologists</publisher><subject>Arabidopsis - genetics ; Arabidopsis - immunology ; Arabidopsis - physiology ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Calcium - metabolism ; Calcium Signaling ; Calcium-Transporting ATPases - genetics ; Calcium-Transporting ATPases - metabolism ; Carrier Proteins - genetics ; Carrier Proteins - metabolism ; Cell Membrane - metabolism ; Cytosol - metabolism ; Genes, Reporter ; Homeostasis ; Loss of Function Mutation ; Membrane Proteins - genetics ; Membrane Proteins - metabolism ; Plant Immunity ; Plant Stomata - genetics ; Plant Stomata - immunology ; Plant Stomata - physiology ; SIGNALING AND RESPONSE</subject><ispartof>Plant physiology (Bethesda), 2017-09, Vol.175 (1), p.424-437</ispartof><rights>2017 American Society of Plant Biologists</rights><rights>2017 American Society of Plant Biologists. All Rights Reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c414t-37bf67374f457a10ff6ba12afad4a3bb0d0a6a77a47c7c075830109b1a9478f33</citedby><orcidid>0000-0003-2573-2702 ; 0000-0001-8855-6617 ; 0000-0003-0581-6036 ; 0000-0002-8441-2162 ; 0000-0002-3777-3344 ; 0000-0001-5402-7725</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26375403$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26375403$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>315,782,786,805,27933,27934,58026,58259</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28701352$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yang, Dong-Lei</creatorcontrib><creatorcontrib>Shi, Zhenying</creatorcontrib><creatorcontrib>Bao, Yongmei</creatorcontrib><creatorcontrib>Yan, Jiapei</creatorcontrib><creatorcontrib>Yang, Ziyuan</creatorcontrib><creatorcontrib>Yu, Huiyun</creatorcontrib><creatorcontrib>Li, Yun</creatorcontrib><creatorcontrib>Gou, Mingyue</creatorcontrib><creatorcontrib>Wang, Shu</creatorcontrib><creatorcontrib>Zou, Baohong</creatorcontrib><creatorcontrib>Xu, Dachao</creatorcontrib><creatorcontrib>Ma, Zhiqi</creatorcontrib><creatorcontrib>Kim, Jitae</creatorcontrib><creatorcontrib>Hua, Jian</creatorcontrib><title>Calcium Pumps and Interacting BON1 Protein Modulate Calcium Signature, Stomatal Closure, and Plant Immunity</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>Calcium signaling is essential for environmental responses including immune responses. Here, we provide evidence that the evolutionarily conserved protein BONZAI1 (BON1) functions together with autoinhibited calcium ATPase10 (ACA10) and ACA8 to regulate calcium signals in Arabidopsis. BON1 is a plasma membrane localized protein that negatively regulates the expression of immune receptor genes and positively regulates stomatal closure. We found that BON1 interacts with the autoinhibitory domains of ACA10 and ACA8, and the aca10 loss-of-function (LOF) mutants have an autoimmune phenotype similar to that of the bon1 LOF mutants. Genetic evidences indicate that BON1 positively regulates the activities of ACA10 and ACA8. Consistent with this idea, the steady level of calcium concentration is increased in both aca10 and bon1 mutants. Most strikingly, cytosolic calcium oscillation imposed by external calcium treatment was altered in aca10, aca8, and bon1 mutants in guard cells. In addition, calcium- and pathogen-induced stomatal closure was compromised in the aca10 and bon1 mutants. Taken together, this study indicates that ACA10/8 and BON1 physically interact on plasma membrane and function in the generation of cytosol calcium signatures that are critical for stomatal movement and impact plant immunity.</description><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - immunology</subject><subject>Arabidopsis - physiology</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Calcium - metabolism</subject><subject>Calcium Signaling</subject><subject>Calcium-Transporting ATPases - genetics</subject><subject>Calcium-Transporting ATPases - metabolism</subject><subject>Carrier Proteins - genetics</subject><subject>Carrier Proteins - metabolism</subject><subject>Cell Membrane - metabolism</subject><subject>Cytosol - metabolism</subject><subject>Genes, Reporter</subject><subject>Homeostasis</subject><subject>Loss of Function Mutation</subject><subject>Membrane Proteins - genetics</subject><subject>Membrane Proteins - metabolism</subject><subject>Plant Immunity</subject><subject>Plant Stomata - genetics</subject><subject>Plant Stomata - immunology</subject><subject>Plant Stomata - physiology</subject><subject>SIGNALING AND RESPONSE</subject><issn>0032-0889</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpFkEtPwzAQhC0EoqVw4gzyEQladmOnTo5Q8ahUaKXCOdokThXIC9s59N-TvuC0o91vR6Nh7BJhhAjyvmlGqEYAMvSPWB994Q09XwbHrA_QaQiCsMfOrP0CABQoT1nPC1Qnfa_PvidUJHlb8kVbNpZTlfJp5bShxOXVij_O35EvTO10XvG3Om0Lcpoffpb5qiLXGn3Hl64uyVHBJ0Vtt5uN1aKgyvFpWbZV7tbn7CSjwuqL_Rywz-enj8nrcDZ_mU4eZsNEonRDoeJsrISSmfQVIWTZOCb0KKNUkohjSIHGpBRJlagElB8IQAhjpFCqIBNiwG52vo2pf1ptXVTmNtFFF0bXrY0wxCDwPfQ26O0OTUxtrdFZ1Ji8JLOOEKJNu1HTRKiibbsdfb03buNSp3_soc4OuNoBX9bV5v8-FsqXIMQv929-RA</recordid><startdate>20170901</startdate><enddate>20170901</enddate><creator>Yang, Dong-Lei</creator><creator>Shi, Zhenying</creator><creator>Bao, Yongmei</creator><creator>Yan, Jiapei</creator><creator>Yang, Ziyuan</creator><creator>Yu, Huiyun</creator><creator>Li, Yun</creator><creator>Gou, Mingyue</creator><creator>Wang, Shu</creator><creator>Zou, Baohong</creator><creator>Xu, Dachao</creator><creator>Ma, Zhiqi</creator><creator>Kim, Jitae</creator><creator>Hua, Jian</creator><general>American Society of Plant Biologists</general><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><orcidid>https://orcid.org/0000-0003-2573-2702</orcidid><orcidid>https://orcid.org/0000-0001-8855-6617</orcidid><orcidid>https://orcid.org/0000-0003-0581-6036</orcidid><orcidid>https://orcid.org/0000-0002-8441-2162</orcidid><orcidid>https://orcid.org/0000-0002-3777-3344</orcidid><orcidid>https://orcid.org/0000-0001-5402-7725</orcidid></search><sort><creationdate>20170901</creationdate><title>Calcium Pumps and Interacting BON1 Protein Modulate Calcium Signature, Stomatal Closure, and Plant Immunity</title><author>Yang, Dong-Lei ; Shi, Zhenying ; Bao, Yongmei ; Yan, Jiapei ; Yang, Ziyuan ; Yu, Huiyun ; Li, Yun ; Gou, Mingyue ; Wang, Shu ; Zou, Baohong ; Xu, Dachao ; Ma, Zhiqi ; Kim, Jitae ; Hua, Jian</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c414t-37bf67374f457a10ff6ba12afad4a3bb0d0a6a77a47c7c075830109b1a9478f33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - immunology</topic><topic>Arabidopsis - physiology</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Calcium - metabolism</topic><topic>Calcium Signaling</topic><topic>Calcium-Transporting ATPases - genetics</topic><topic>Calcium-Transporting ATPases - metabolism</topic><topic>Carrier Proteins - genetics</topic><topic>Carrier Proteins - metabolism</topic><topic>Cell Membrane - metabolism</topic><topic>Cytosol - metabolism</topic><topic>Genes, Reporter</topic><topic>Homeostasis</topic><topic>Loss of Function Mutation</topic><topic>Membrane Proteins - genetics</topic><topic>Membrane Proteins - metabolism</topic><topic>Plant Immunity</topic><topic>Plant Stomata - genetics</topic><topic>Plant Stomata - immunology</topic><topic>Plant Stomata - physiology</topic><topic>SIGNALING AND RESPONSE</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yang, Dong-Lei</creatorcontrib><creatorcontrib>Shi, Zhenying</creatorcontrib><creatorcontrib>Bao, Yongmei</creatorcontrib><creatorcontrib>Yan, Jiapei</creatorcontrib><creatorcontrib>Yang, Ziyuan</creatorcontrib><creatorcontrib>Yu, Huiyun</creatorcontrib><creatorcontrib>Li, Yun</creatorcontrib><creatorcontrib>Gou, Mingyue</creatorcontrib><creatorcontrib>Wang, Shu</creatorcontrib><creatorcontrib>Zou, Baohong</creatorcontrib><creatorcontrib>Xu, Dachao</creatorcontrib><creatorcontrib>Ma, Zhiqi</creatorcontrib><creatorcontrib>Kim, Jitae</creatorcontrib><creatorcontrib>Hua, Jian</creatorcontrib><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><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yang, Dong-Lei</au><au>Shi, Zhenying</au><au>Bao, Yongmei</au><au>Yan, Jiapei</au><au>Yang, Ziyuan</au><au>Yu, Huiyun</au><au>Li, Yun</au><au>Gou, Mingyue</au><au>Wang, Shu</au><au>Zou, Baohong</au><au>Xu, Dachao</au><au>Ma, Zhiqi</au><au>Kim, Jitae</au><au>Hua, Jian</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Calcium Pumps and Interacting BON1 Protein Modulate Calcium Signature, Stomatal Closure, and Plant Immunity</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2017-09-01</date><risdate>2017</risdate><volume>175</volume><issue>1</issue><spage>424</spage><epage>437</epage><pages>424-437</pages><issn>0032-0889</issn><eissn>1532-2548</eissn><abstract>Calcium signaling is essential for environmental responses including immune responses. Here, we provide evidence that the evolutionarily conserved protein BONZAI1 (BON1) functions together with autoinhibited calcium ATPase10 (ACA10) and ACA8 to regulate calcium signals in Arabidopsis. BON1 is a plasma membrane localized protein that negatively regulates the expression of immune receptor genes and positively regulates stomatal closure. We found that BON1 interacts with the autoinhibitory domains of ACA10 and ACA8, and the aca10 loss-of-function (LOF) mutants have an autoimmune phenotype similar to that of the bon1 LOF mutants. Genetic evidences indicate that BON1 positively regulates the activities of ACA10 and ACA8. Consistent with this idea, the steady level of calcium concentration is increased in both aca10 and bon1 mutants. Most strikingly, cytosolic calcium oscillation imposed by external calcium treatment was altered in aca10, aca8, and bon1 mutants in guard cells. In addition, calcium- and pathogen-induced stomatal closure was compromised in the aca10 and bon1 mutants. Taken together, this study indicates that ACA10/8 and BON1 physically interact on plasma membrane and function in the generation of cytosol calcium signatures that are critical for stomatal movement and impact plant immunity.</abstract><cop>United States</cop><pub>American Society of Plant Biologists</pub><pmid>28701352</pmid><doi>10.1104/pp.17.00495</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0003-2573-2702</orcidid><orcidid>https://orcid.org/0000-0001-8855-6617</orcidid><orcidid>https://orcid.org/0000-0003-0581-6036</orcidid><orcidid>https://orcid.org/0000-0002-8441-2162</orcidid><orcidid>https://orcid.org/0000-0002-3777-3344</orcidid><orcidid>https://orcid.org/0000-0001-5402-7725</orcidid><oa>free_for_read</oa></addata></record> |
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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 | Arabidopsis - genetics Arabidopsis - immunology Arabidopsis - physiology Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Calcium - metabolism Calcium Signaling Calcium-Transporting ATPases - genetics Calcium-Transporting ATPases - metabolism Carrier Proteins - genetics Carrier Proteins - metabolism Cell Membrane - metabolism Cytosol - metabolism Genes, Reporter Homeostasis Loss of Function Mutation Membrane Proteins - genetics Membrane Proteins - metabolism Plant Immunity Plant Stomata - genetics Plant Stomata - immunology Plant Stomata - physiology SIGNALING AND RESPONSE |
| title | Calcium Pumps and Interacting BON1 Protein Modulate Calcium Signature, Stomatal Closure, and Plant Immunity |
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