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Analysis of Arabidopsis glucose insensitive growth Mutants Reveals the Involvement of the Plastidial Copper Transporter PAA1 in Glucose-Induced Intracellular Signaling
Sugars play important roles in many aspects of plant growth and development, acting as both energy sources and signaling molecules. With the successful use of genetic approaches, the molecular components involved in sugar signaling have been identified and their regulatory roles in the pathways have...
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Published in: | Plant physiology (Bethesda) 2012-07, Vol.159 (3), p.1001-1012 |
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description | Sugars play important roles in many aspects of plant growth and development, acting as both energy sources and signaling molecules. With the successful use of genetic approaches, the molecular components involved in sugar signaling have been identified and their regulatory roles in the pathways have been elucidated. Here, we describe novel mutants of Arabidopsis (Arabidopsis thaliana), named glucose insensitive growth (gig), identified by their insensitivity to high-glucose (Glc)-induced growth inhibition. The gig mutant displayed retarded growth under normal growth conditions and also showed alterations in the expression of Glc-responsive genes under high-Glc conditions. Our molecular identification reveals that GIG encodes the plastidial copper (Cu) transporter PAA1 (for P₁
B
-type ATPase 1). Interestingly, double mutant analysis indicated that in high Glc, gig is epistatic to both hexokinasel (hxk1) and aba insensitive4 (abi4), major regulators in sugar and retrograde signaling. Under high-Glc conditions, the addition of Cu had no effect on the recovery of gig/paa1 to the wild type, whereas exogenous Cu feeding could suppress its phenotype under normal growth conditions. The expression of GIG/PAA1 was also altered by mutations in the nuclear factors HXK1, ABI3, and ABI4 in high Glc. Furthermore, a transient expression assay revealed the interaction between ABI4 and the GIG/PAA1 promoter, suggesting that ABI4 actively regulates the transcription of GIG/PAA1, likely binding to the CCAC/ACGT core element of the GIG/PAA1 promoter. Our findings indicate that the plastidial Cu transporter PAA1, which is essential for plastid function and/or activity, plays an important role in bidirectional communication between the plastid and the nucleus in high Glc. |
doi_str_mv | 10.1104/pp.111.191726 |
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B
-type ATPase 1). Interestingly, double mutant analysis indicated that in high Glc, gig is epistatic to both hexokinasel (hxk1) and aba insensitive4 (abi4), major regulators in sugar and retrograde signaling. Under high-Glc conditions, the addition of Cu had no effect on the recovery of gig/paa1 to the wild type, whereas exogenous Cu feeding could suppress its phenotype under normal growth conditions. The expression of GIG/PAA1 was also altered by mutations in the nuclear factors HXK1, ABI3, and ABI4 in high Glc. Furthermore, a transient expression assay revealed the interaction between ABI4 and the GIG/PAA1 promoter, suggesting that ABI4 actively regulates the transcription of GIG/PAA1, likely binding to the CCAC/ACGT core element of the GIG/PAA1 promoter. Our findings indicate that the plastidial Cu transporter PAA1, which is essential for plastid function and/or activity, plays an important role in bidirectional communication between the plastid and the nucleus in high Glc.</description><identifier>ISSN: 0032-0889</identifier><identifier>ISSN: 1532-2548</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.111.191726</identifier><identifier>PMID: 22582133</identifier><identifier>CODEN: PPHYA5</identifier><language>eng</language><publisher>Rockville, MD: American Society of Plant Biologists</publisher><subject>Arabidopsis - drug effects ; Arabidopsis - genetics ; Arabidopsis - growth & development ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Biological and medical sciences ; CELL BIOLOGY AND SIGNAL TRANSDUCTION ; Chloroplast Proton-Translocating ATPases - genetics ; Chloroplast Proton-Translocating ATPases - metabolism ; Copper - metabolism ; Epistasis, Genetic - drug effects ; Fundamental and applied biological sciences. Psychology ; Gene Expression Regulation, Plant - drug effects ; Genes ; Genes, Plant - genetics ; Genetic Complementation Test ; Genetic loci ; Genetic Loci - genetics ; Glucose - pharmacology ; Intracellular Space - drug effects ; Intracellular Space - metabolism ; Membrane Transport Proteins - genetics ; Membrane Transport Proteins - metabolism ; Models, Biological ; Mutation - genetics ; Phenotypes ; Plant physiology and development ; Plant roots ; Plants ; Plasmids ; Plastids ; Plastids - drug effects ; Plastids - metabolism ; Root growth ; Seedlings ; Signal Transduction - drug effects ; Sugars ; Transcription Factors - metabolism</subject><ispartof>Plant physiology (Bethesda), 2012-07, Vol.159 (3), p.1001-1012</ispartof><rights>2012 American Society of Plant Biologists</rights><rights>2015 INIST-CNRS</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c345t-8260872573293138b0de93ea1fa0f06af5520a9de9ada8566bb3c40101c12dcd3</citedby><cites>FETCH-LOGICAL-c345t-8260872573293138b0de93ea1fa0f06af5520a9de9ada8566bb3c40101c12dcd3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/41549918$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/41549918$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,780,784,27924,27925,58238,58471</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=26144803$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22582133$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lee, Shin Ae</creatorcontrib><creatorcontrib>Yoon, Eun Kyung</creatorcontrib><creatorcontrib>Heo, Jung-Ok</creatorcontrib><creatorcontrib>Lee, Mi-Hyun</creatorcontrib><creatorcontrib>Hwang, Indeok</creatorcontrib><creatorcontrib>Cheong, Hyeonsook</creatorcontrib><creatorcontrib>Lee, Woo Sung</creatorcontrib><creatorcontrib>Hwang, Yong-sic</creatorcontrib><creatorcontrib>Lim, Jun</creatorcontrib><title>Analysis of Arabidopsis glucose insensitive growth Mutants Reveals the Involvement of the Plastidial Copper Transporter PAA1 in Glucose-Induced Intracellular Signaling</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>Sugars play important roles in many aspects of plant growth and development, acting as both energy sources and signaling molecules. With the successful use of genetic approaches, the molecular components involved in sugar signaling have been identified and their regulatory roles in the pathways have been elucidated. Here, we describe novel mutants of Arabidopsis (Arabidopsis thaliana), named glucose insensitive growth (gig), identified by their insensitivity to high-glucose (Glc)-induced growth inhibition. The gig mutant displayed retarded growth under normal growth conditions and also showed alterations in the expression of Glc-responsive genes under high-Glc conditions. Our molecular identification reveals that GIG encodes the plastidial copper (Cu) transporter PAA1 (for P₁
B
-type ATPase 1). Interestingly, double mutant analysis indicated that in high Glc, gig is epistatic to both hexokinasel (hxk1) and aba insensitive4 (abi4), major regulators in sugar and retrograde signaling. Under high-Glc conditions, the addition of Cu had no effect on the recovery of gig/paa1 to the wild type, whereas exogenous Cu feeding could suppress its phenotype under normal growth conditions. The expression of GIG/PAA1 was also altered by mutations in the nuclear factors HXK1, ABI3, and ABI4 in high Glc. Furthermore, a transient expression assay revealed the interaction between ABI4 and the GIG/PAA1 promoter, suggesting that ABI4 actively regulates the transcription of GIG/PAA1, likely binding to the CCAC/ACGT core element of the GIG/PAA1 promoter. Our findings indicate that the plastidial Cu transporter PAA1, which is essential for plastid function and/or activity, plays an important role in bidirectional communication between the plastid and the nucleus in high Glc.</description><subject>Arabidopsis - drug effects</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Biological and medical sciences</subject><subject>CELL BIOLOGY AND SIGNAL TRANSDUCTION</subject><subject>Chloroplast Proton-Translocating ATPases - genetics</subject><subject>Chloroplast Proton-Translocating ATPases - metabolism</subject><subject>Copper - metabolism</subject><subject>Epistasis, Genetic - drug effects</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Expression Regulation, Plant - drug effects</subject><subject>Genes</subject><subject>Genes, Plant - genetics</subject><subject>Genetic Complementation Test</subject><subject>Genetic loci</subject><subject>Genetic Loci - genetics</subject><subject>Glucose - pharmacology</subject><subject>Intracellular Space - drug effects</subject><subject>Intracellular Space - metabolism</subject><subject>Membrane Transport Proteins - genetics</subject><subject>Membrane Transport Proteins - metabolism</subject><subject>Models, Biological</subject><subject>Mutation - genetics</subject><subject>Phenotypes</subject><subject>Plant physiology and development</subject><subject>Plant roots</subject><subject>Plants</subject><subject>Plasmids</subject><subject>Plastids</subject><subject>Plastids - drug effects</subject><subject>Plastids - metabolism</subject><subject>Root growth</subject><subject>Seedlings</subject><subject>Signal Transduction - drug effects</subject><subject>Sugars</subject><subject>Transcription Factors - metabolism</subject><issn>0032-0889</issn><issn>1532-2548</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><recordid>eNpFkEtv1DAUhS0EokNhyRLkDcsUXz8yzjIalXakIioo68hxnKkrT2zZzqD-Iv5mHaWU1bmPT-deHYQ-ArkAIPxrCEXhAhrY0voV2oBgtKKCy9doQ0ipiZTNGXqX0gMhBBjwt-iMUiEpMLZBf9tJucdkE_YjbqPq7eDD0h7crH0y2E7JTMlmezL4EP2ffI-_z1lNOeGf5mSUSzjfG7yfTt6dzNFMeXFaRrdOpWwHqxze-RBMxHdRTSn4mEt927ZQzPHVeqfaT8OszVCMclTaODc7FfEveyj_2enwHr0Zyy3z4VnP0e9vl3e76-rmx9V-195UmnGRK0lrIrdUbBltGDDZk8E0zCgYFRlJrUYhKFFNGapBSVHXfc80J0BAAx30wM5Rtfrq6FOKZuxCtEcVHzsg3RJ4F0JR6NbAC_955cPcH83wQv9LuABfngGVtHJjiUDb9J-rgXNJFu7Tyj2k7OPLnoPgTQOSPQE15ZW9</recordid><startdate>20120701</startdate><enddate>20120701</enddate><creator>Lee, Shin Ae</creator><creator>Yoon, Eun Kyung</creator><creator>Heo, Jung-Ok</creator><creator>Lee, Mi-Hyun</creator><creator>Hwang, Indeok</creator><creator>Cheong, Hyeonsook</creator><creator>Lee, Woo Sung</creator><creator>Hwang, Yong-sic</creator><creator>Lim, Jun</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></search><sort><creationdate>20120701</creationdate><title>Analysis of Arabidopsis glucose insensitive growth Mutants Reveals the Involvement of the Plastidial Copper Transporter PAA1 in Glucose-Induced Intracellular Signaling</title><author>Lee, Shin Ae ; Yoon, Eun Kyung ; Heo, Jung-Ok ; Lee, Mi-Hyun ; Hwang, Indeok ; Cheong, Hyeonsook ; Lee, Woo Sung ; Hwang, Yong-sic ; Lim, Jun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c345t-8260872573293138b0de93ea1fa0f06af5520a9de9ada8566bb3c40101c12dcd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Arabidopsis - drug effects</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - growth & development</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Biological and medical sciences</topic><topic>CELL BIOLOGY AND SIGNAL TRANSDUCTION</topic><topic>Chloroplast Proton-Translocating ATPases - genetics</topic><topic>Chloroplast Proton-Translocating ATPases - metabolism</topic><topic>Copper - metabolism</topic><topic>Epistasis, Genetic - drug effects</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Expression Regulation, Plant - drug effects</topic><topic>Genes</topic><topic>Genes, Plant - genetics</topic><topic>Genetic Complementation Test</topic><topic>Genetic loci</topic><topic>Genetic Loci - genetics</topic><topic>Glucose - pharmacology</topic><topic>Intracellular Space - drug effects</topic><topic>Intracellular Space - metabolism</topic><topic>Membrane Transport Proteins - genetics</topic><topic>Membrane Transport Proteins - metabolism</topic><topic>Models, Biological</topic><topic>Mutation - genetics</topic><topic>Phenotypes</topic><topic>Plant physiology and development</topic><topic>Plant roots</topic><topic>Plants</topic><topic>Plasmids</topic><topic>Plastids</topic><topic>Plastids - drug effects</topic><topic>Plastids - metabolism</topic><topic>Root growth</topic><topic>Seedlings</topic><topic>Signal Transduction - drug effects</topic><topic>Sugars</topic><topic>Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lee, Shin Ae</creatorcontrib><creatorcontrib>Yoon, Eun Kyung</creatorcontrib><creatorcontrib>Heo, Jung-Ok</creatorcontrib><creatorcontrib>Lee, Mi-Hyun</creatorcontrib><creatorcontrib>Hwang, Indeok</creatorcontrib><creatorcontrib>Cheong, Hyeonsook</creatorcontrib><creatorcontrib>Lee, Woo Sung</creatorcontrib><creatorcontrib>Hwang, Yong-sic</creatorcontrib><creatorcontrib>Lim, Jun</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><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lee, Shin Ae</au><au>Yoon, Eun Kyung</au><au>Heo, Jung-Ok</au><au>Lee, Mi-Hyun</au><au>Hwang, Indeok</au><au>Cheong, Hyeonsook</au><au>Lee, Woo Sung</au><au>Hwang, Yong-sic</au><au>Lim, Jun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Analysis of Arabidopsis glucose insensitive growth Mutants Reveals the Involvement of the Plastidial Copper Transporter PAA1 in Glucose-Induced Intracellular Signaling</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2012-07-01</date><risdate>2012</risdate><volume>159</volume><issue>3</issue><spage>1001</spage><epage>1012</epage><pages>1001-1012</pages><issn>0032-0889</issn><issn>1532-2548</issn><eissn>1532-2548</eissn><coden>PPHYA5</coden><abstract>Sugars play important roles in many aspects of plant growth and development, acting as both energy sources and signaling molecules. With the successful use of genetic approaches, the molecular components involved in sugar signaling have been identified and their regulatory roles in the pathways have been elucidated. Here, we describe novel mutants of Arabidopsis (Arabidopsis thaliana), named glucose insensitive growth (gig), identified by their insensitivity to high-glucose (Glc)-induced growth inhibition. The gig mutant displayed retarded growth under normal growth conditions and also showed alterations in the expression of Glc-responsive genes under high-Glc conditions. Our molecular identification reveals that GIG encodes the plastidial copper (Cu) transporter PAA1 (for P₁
B
-type ATPase 1). Interestingly, double mutant analysis indicated that in high Glc, gig is epistatic to both hexokinasel (hxk1) and aba insensitive4 (abi4), major regulators in sugar and retrograde signaling. Under high-Glc conditions, the addition of Cu had no effect on the recovery of gig/paa1 to the wild type, whereas exogenous Cu feeding could suppress its phenotype under normal growth conditions. The expression of GIG/PAA1 was also altered by mutations in the nuclear factors HXK1, ABI3, and ABI4 in high Glc. Furthermore, a transient expression assay revealed the interaction between ABI4 and the GIG/PAA1 promoter, suggesting that ABI4 actively regulates the transcription of GIG/PAA1, likely binding to the CCAC/ACGT core element of the GIG/PAA1 promoter. Our findings indicate that the plastidial Cu transporter PAA1, which is essential for plastid function and/or activity, plays an important role in bidirectional communication between the plastid and the nucleus in high Glc.</abstract><cop>Rockville, MD</cop><pub>American Society of Plant Biologists</pub><pmid>22582133</pmid><doi>10.1104/pp.111.191726</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis - drug effects Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Biological and medical sciences CELL BIOLOGY AND SIGNAL TRANSDUCTION Chloroplast Proton-Translocating ATPases - genetics Chloroplast Proton-Translocating ATPases - metabolism Copper - metabolism Epistasis, Genetic - drug effects Fundamental and applied biological sciences. Psychology Gene Expression Regulation, Plant - drug effects Genes Genes, Plant - genetics Genetic Complementation Test Genetic loci Genetic Loci - genetics Glucose - pharmacology Intracellular Space - drug effects Intracellular Space - metabolism Membrane Transport Proteins - genetics Membrane Transport Proteins - metabolism Models, Biological Mutation - genetics Phenotypes Plant physiology and development Plant roots Plants Plasmids Plastids Plastids - drug effects Plastids - metabolism Root growth Seedlings Signal Transduction - drug effects Sugars Transcription Factors - metabolism |
title | Analysis of Arabidopsis glucose insensitive growth Mutants Reveals the Involvement of the Plastidial Copper Transporter PAA1 in Glucose-Induced Intracellular Signaling |
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