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Identification of Cytokinin-Responsive Genes Using Microarray Meta-Analysis and RNA-Seq in Arabidopsis
Cytokinins are N⁶-substituted adenine derivatives that play diverse roles in plant growth and development. We sought to define a robust set of genes regulated by cytokinin as well as to query the response of genes not represented on microarrays. To this end, we performed a meta-analysis of microarra...
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| Published in: | Plant physiology (Bethesda) 2013-05, Vol.162 (1), p.272-294 |
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| container_end_page | 294 |
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| container_title | Plant physiology (Bethesda) |
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| creator | Bhargava, Apurva Clabaugh, Ivory To, Jenn P. Maxwell, Bridey B. Chiang, Yi-Hsuan Schaller, G. Eric Loraine, Ann Kieber, Joseph J. |
| description | Cytokinins are N⁶-substituted adenine derivatives that play diverse roles in plant growth and development. We sought to define a robust set of genes regulated by cytokinin as well as to query the response of genes not represented on microarrays. To this end, we performed a meta-analysis of microarray data from a variety of cytokinin-treated samples and used RNA-seq to examine cytokininregulated gene expression in Arabidopsis (Arabidopsis thaliana). Microarray meta-analysis using 13 microarray experiments combined with empirically defined filtering criteria identified a set of 226 genes differentially regulated by cytokinin, a subset of which has previously been validated by other methods. RNA-seq validated about 73% of the up-regulated genes identified by this meta-analysis. In silico promoter analysis indicated an overrepresentation of type-B Arabidopsis response regulator binding elements, consistent with the role of type-B Arabidopsis response regulators as primary mediators of cytokinin-responsive gene expression. RNA-seq analysis identified 73 cytokinin-regulated genes that were not represented on the ATH1 microarray. Representative genes were verified using quantitative reverse transcription-polymerase chain reaction and NanoString analysis. Analysis of the genes identified reveals a substantial effect of cytokinin on genes encoding proteins involved in secondary metabolism, particularly those acting in flavonoid and phenylpropanoid biosynthesis, as well as in the regulation of redox state of the cell, particularly a set of glutaredoxin genes. Novel splicing events were found in members of some gene families that are known to play a role in cytokinin signaling or metabolism. The genes identified in this analysis represent a robust set of cytokininresponsive genes that are useful in the analysis of cytokinin function in plants. |
| doi_str_mv | 10.1104/pp.113.217026 |
| format | article |
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RNA-seq validated about 73% of the up-regulated genes identified by this meta-analysis. In silico promoter analysis indicated an overrepresentation of type-B Arabidopsis response regulator binding elements, consistent with the role of type-B Arabidopsis response regulators as primary mediators of cytokinin-responsive gene expression. RNA-seq analysis identified 73 cytokinin-regulated genes that were not represented on the ATH1 microarray. Representative genes were verified using quantitative reverse transcription-polymerase chain reaction and NanoString analysis. Analysis of the genes identified reveals a substantial effect of cytokinin on genes encoding proteins involved in secondary metabolism, particularly those acting in flavonoid and phenylpropanoid biosynthesis, as well as in the regulation of redox state of the cell, particularly a set of glutaredoxin genes. Novel splicing events were found in members of some gene families that are known to play a role in cytokinin signaling or metabolism. The genes identified in this analysis represent a robust set of cytokininresponsive genes that are useful in the analysis of cytokinin function in plants.</description><identifier>ISSN: 0032-0889</identifier><identifier>ISSN: 1532-2548</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.113.217026</identifier><identifier>PMID: 23524861</identifier><identifier>CODEN: PPHYA5</identifier><language>eng</language><publisher>Rockville, MD: American Society of Plant Biologists</publisher><subject>Amino Acid Motifs ; Arabidopsis - drug effects ; Arabidopsis - genetics ; Arabidopsis Proteins - genetics ; Biological and medical sciences ; Cluster Analysis ; Computational Biology ; Cytokinins ; Cytokinins - pharmacology ; Down-Regulation ; Fundamental and applied biological sciences. Psychology ; Gene Expression Profiling ; Gene expression regulation ; Gene Expression Regulation, Plant ; Gene Library ; Genes ; Genomes ; High-Throughput Nucleotide Sequencing ; Molecular Sequence Annotation ; Oligonucleotide Array Sequence Analysis ; Plant cells ; Plant growth regulators ; Plant physiology and development ; Plant Roots - drug effects ; Plant Roots - genetics ; Plant Shoots - drug effects ; Plant Shoots - genetics ; Plants ; Promoter Regions, Genetic - genetics ; RNA Splicing ; RNA, Messenger - genetics ; RNA, Plant - genetics ; Seedlings ; Seedlings - drug effects ; Seedlings - genetics ; Sequence Analysis, RNA ; Signal Transduction ; SIGNALING AND RESPONSE ; Transcription factors ; Up regulation</subject><ispartof>Plant physiology (Bethesda), 2013-05, Vol.162 (1), p.272-294</ispartof><rights>2013 American Society of Plant Biologists</rights><rights>2014 INIST-CNRS</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c406t-c92dd28ee5d8b9acd5233059cc196424a1aad92f02961fffe15b1ce741f73f2a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/41942863$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/41942863$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>315,783,787,27936,27937,58566,58799</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=27321760$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23524861$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bhargava, Apurva</creatorcontrib><creatorcontrib>Clabaugh, Ivory</creatorcontrib><creatorcontrib>To, Jenn P.</creatorcontrib><creatorcontrib>Maxwell, Bridey B.</creatorcontrib><creatorcontrib>Chiang, Yi-Hsuan</creatorcontrib><creatorcontrib>Schaller, G. Eric</creatorcontrib><creatorcontrib>Loraine, Ann</creatorcontrib><creatorcontrib>Kieber, Joseph J.</creatorcontrib><title>Identification of Cytokinin-Responsive Genes Using Microarray Meta-Analysis and RNA-Seq in Arabidopsis</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>Cytokinins are N⁶-substituted adenine derivatives that play diverse roles in plant growth and development. We sought to define a robust set of genes regulated by cytokinin as well as to query the response of genes not represented on microarrays. To this end, we performed a meta-analysis of microarray data from a variety of cytokinin-treated samples and used RNA-seq to examine cytokininregulated gene expression in Arabidopsis (Arabidopsis thaliana). Microarray meta-analysis using 13 microarray experiments combined with empirically defined filtering criteria identified a set of 226 genes differentially regulated by cytokinin, a subset of which has previously been validated by other methods. RNA-seq validated about 73% of the up-regulated genes identified by this meta-analysis. In silico promoter analysis indicated an overrepresentation of type-B Arabidopsis response regulator binding elements, consistent with the role of type-B Arabidopsis response regulators as primary mediators of cytokinin-responsive gene expression. RNA-seq analysis identified 73 cytokinin-regulated genes that were not represented on the ATH1 microarray. Representative genes were verified using quantitative reverse transcription-polymerase chain reaction and NanoString analysis. Analysis of the genes identified reveals a substantial effect of cytokinin on genes encoding proteins involved in secondary metabolism, particularly those acting in flavonoid and phenylpropanoid biosynthesis, as well as in the regulation of redox state of the cell, particularly a set of glutaredoxin genes. Novel splicing events were found in members of some gene families that are known to play a role in cytokinin signaling or metabolism. The genes identified in this analysis represent a robust set of cytokininresponsive genes that are useful in the analysis of cytokinin function in plants.</description><subject>Amino Acid Motifs</subject><subject>Arabidopsis - drug effects</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Biological and medical sciences</subject><subject>Cluster Analysis</subject><subject>Computational Biology</subject><subject>Cytokinins</subject><subject>Cytokinins - pharmacology</subject><subject>Down-Regulation</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Expression Profiling</subject><subject>Gene expression regulation</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene Library</subject><subject>Genes</subject><subject>Genomes</subject><subject>High-Throughput Nucleotide Sequencing</subject><subject>Molecular Sequence Annotation</subject><subject>Oligonucleotide Array Sequence Analysis</subject><subject>Plant cells</subject><subject>Plant growth regulators</subject><subject>Plant physiology and development</subject><subject>Plant Roots - drug effects</subject><subject>Plant Roots - genetics</subject><subject>Plant Shoots - drug effects</subject><subject>Plant Shoots - genetics</subject><subject>Plants</subject><subject>Promoter Regions, Genetic - genetics</subject><subject>RNA Splicing</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Plant - genetics</subject><subject>Seedlings</subject><subject>Seedlings - drug effects</subject><subject>Seedlings - genetics</subject><subject>Sequence Analysis, RNA</subject><subject>Signal Transduction</subject><subject>SIGNALING AND RESPONSE</subject><subject>Transcription factors</subject><subject>Up regulation</subject><issn>0032-0889</issn><issn>1532-2548</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><recordid>eNpFkEFPGzEQRq2qqIS0R45UvlTqZanH9m52j1HUAhK0Ei3n1cQeI8PGXuwNUv59jRLg9I00T99oHmOnIM4BhP4xjiXVuYSFkM0HNoNayUrWuv3IZkKUWbRtd8xOcn4QQoAC_YkdS1VL3TYwY-7KUpi88wYnHwOPjq92U3z0wYfqlvIYQ_bPxC8oUOZ32Yd7fuNNipgS7vgNTVgtAw677DPHYPnt72X1l564D3yZcO1tHMvqMztyOGT6csg5u_v189_qsrr-c3G1Wl5XRotmqkwnrZUtUW3bdYfG1lIpUXfGQNdoqREQbSedkF0DzjmCeg2GFhrcQjmJas6-73vHFJ-2lKd-47OhYcBAcZt7ULqthYZiZs6qPVqeyTmR68fkN5h2PYj-RW0_jiVVv1db-K-H6u16Q_aNfnVZgG8HALPBwSUMxud3bqFKU_Ny-GzPPeQppre9hk7LtlHqP95Fixk</recordid><startdate>20130501</startdate><enddate>20130501</enddate><creator>Bhargava, Apurva</creator><creator>Clabaugh, Ivory</creator><creator>To, Jenn P.</creator><creator>Maxwell, Bridey B.</creator><creator>Chiang, Yi-Hsuan</creator><creator>Schaller, G. Eric</creator><creator>Loraine, Ann</creator><creator>Kieber, Joseph J.</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></search><sort><creationdate>20130501</creationdate><title>Identification of Cytokinin-Responsive Genes Using Microarray Meta-Analysis and RNA-Seq in Arabidopsis</title><author>Bhargava, Apurva ; Clabaugh, Ivory ; To, Jenn P. ; Maxwell, Bridey B. ; Chiang, Yi-Hsuan ; Schaller, G. Eric ; Loraine, Ann ; Kieber, Joseph J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c406t-c92dd28ee5d8b9acd5233059cc196424a1aad92f02961fffe15b1ce741f73f2a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Amino Acid Motifs</topic><topic>Arabidopsis - drug effects</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Biological and medical sciences</topic><topic>Cluster Analysis</topic><topic>Computational Biology</topic><topic>Cytokinins</topic><topic>Cytokinins - pharmacology</topic><topic>Down-Regulation</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Expression Profiling</topic><topic>Gene expression regulation</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene Library</topic><topic>Genes</topic><topic>Genomes</topic><topic>High-Throughput Nucleotide Sequencing</topic><topic>Molecular Sequence Annotation</topic><topic>Oligonucleotide Array Sequence Analysis</topic><topic>Plant cells</topic><topic>Plant growth regulators</topic><topic>Plant physiology and development</topic><topic>Plant Roots - drug effects</topic><topic>Plant Roots - genetics</topic><topic>Plant Shoots - drug effects</topic><topic>Plant Shoots - genetics</topic><topic>Plants</topic><topic>Promoter Regions, Genetic - genetics</topic><topic>RNA Splicing</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Plant - genetics</topic><topic>Seedlings</topic><topic>Seedlings - drug effects</topic><topic>Seedlings - genetics</topic><topic>Sequence Analysis, RNA</topic><topic>Signal Transduction</topic><topic>SIGNALING AND RESPONSE</topic><topic>Transcription factors</topic><topic>Up regulation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bhargava, Apurva</creatorcontrib><creatorcontrib>Clabaugh, Ivory</creatorcontrib><creatorcontrib>To, Jenn P.</creatorcontrib><creatorcontrib>Maxwell, Bridey B.</creatorcontrib><creatorcontrib>Chiang, Yi-Hsuan</creatorcontrib><creatorcontrib>Schaller, G. 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Eric</au><au>Loraine, Ann</au><au>Kieber, Joseph J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Identification of Cytokinin-Responsive Genes Using Microarray Meta-Analysis and RNA-Seq in Arabidopsis</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2013-05-01</date><risdate>2013</risdate><volume>162</volume><issue>1</issue><spage>272</spage><epage>294</epage><pages>272-294</pages><issn>0032-0889</issn><issn>1532-2548</issn><eissn>1532-2548</eissn><coden>PPHYA5</coden><abstract>Cytokinins are N⁶-substituted adenine derivatives that play diverse roles in plant growth and development. We sought to define a robust set of genes regulated by cytokinin as well as to query the response of genes not represented on microarrays. To this end, we performed a meta-analysis of microarray data from a variety of cytokinin-treated samples and used RNA-seq to examine cytokininregulated gene expression in Arabidopsis (Arabidopsis thaliana). Microarray meta-analysis using 13 microarray experiments combined with empirically defined filtering criteria identified a set of 226 genes differentially regulated by cytokinin, a subset of which has previously been validated by other methods. RNA-seq validated about 73% of the up-regulated genes identified by this meta-analysis. In silico promoter analysis indicated an overrepresentation of type-B Arabidopsis response regulator binding elements, consistent with the role of type-B Arabidopsis response regulators as primary mediators of cytokinin-responsive gene expression. RNA-seq analysis identified 73 cytokinin-regulated genes that were not represented on the ATH1 microarray. Representative genes were verified using quantitative reverse transcription-polymerase chain reaction and NanoString analysis. Analysis of the genes identified reveals a substantial effect of cytokinin on genes encoding proteins involved in secondary metabolism, particularly those acting in flavonoid and phenylpropanoid biosynthesis, as well as in the regulation of redox state of the cell, particularly a set of glutaredoxin genes. Novel splicing events were found in members of some gene families that are known to play a role in cytokinin signaling or metabolism. The genes identified in this analysis represent a robust set of cytokininresponsive genes that are useful in the analysis of cytokinin function in plants.</abstract><cop>Rockville, MD</cop><pub>American Society of Plant Biologists</pub><pmid>23524861</pmid><doi>10.1104/pp.113.217026</doi><tpages>23</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Amino Acid Motifs Arabidopsis - drug effects Arabidopsis - genetics Arabidopsis Proteins - genetics Biological and medical sciences Cluster Analysis Computational Biology Cytokinins Cytokinins - pharmacology Down-Regulation Fundamental and applied biological sciences. Psychology Gene Expression Profiling Gene expression regulation Gene Expression Regulation, Plant Gene Library Genes Genomes High-Throughput Nucleotide Sequencing Molecular Sequence Annotation Oligonucleotide Array Sequence Analysis Plant cells Plant growth regulators Plant physiology and development Plant Roots - drug effects Plant Roots - genetics Plant Shoots - drug effects Plant Shoots - genetics Plants Promoter Regions, Genetic - genetics RNA Splicing RNA, Messenger - genetics RNA, Plant - genetics Seedlings Seedlings - drug effects Seedlings - genetics Sequence Analysis, RNA Signal Transduction SIGNALING AND RESPONSE Transcription factors Up regulation |
| title | Identification of Cytokinin-Responsive Genes Using Microarray Meta-Analysis and RNA-Seq in Arabidopsis |
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