Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress
Summary Plant nutrition critically depends on the activity of membrane transporters that translocate minerals from the soil into the plant and are responsible for their intra‐ and intercellular distribution. Most plant membrane transporters are encoded by multigene families whose members often exhib...
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Veröffentlicht in: | The Plant journal : for cell and molecular biology 2003-09, Vol.35 (6), p.675-692 |
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creator | Maathuis, Frans J. M. Filatov, Victor Herzyk, Pawel C. Krijger, Gerard B. Axelsen, Kristian Chen, Sixue Green, Brian J. Li, Yi Madagan, Kathryn L. Sánchez‐Fernández, Rocío Forde, Brian G. Palmgren, Michael G. Rea, Philip A. Williams, Lorraine E. Sanders, Dale Amtmann, Anna |
description | Summary
Plant nutrition critically depends on the activity of membrane transporters that translocate minerals from the soil into the plant and are responsible for their intra‐ and intercellular distribution. Most plant membrane transporters are encoded by multigene families whose members often exhibit overlapping expression patterns and a high degree of sequence homology. Furthermore, many inorganic nutrients are transported by more than one transporter family. These considerations, coupled with a large number of so‐far non‐annotated putative transporter genes, hamper our progress in understanding how the activity of specific transporters is integrated into a response to fluctuating conditions. We designed an oligonucleotide microarray representing 1096 Arabidopsis transporter genes and analysed the root transporter transcriptome over a 96‐h period with respect to 80 mm NaCl, K+ starvation and Ca2+ starvation. Our data show that cation stress led to changes in transcript level of many genes across most transporter gene families. Analysis of transcriptionally modulated genes across all functional groups of transporters revealed families such as V‐type ATPases and aquaporins that responded to all treatments, and families – which included putative non‐selective cation channels for the NaCl treatment and metal transporters for Ca2+ starvation conditions – that responded to specific ionic environments. Several gene families including primary pumps, antiporters and aquaporins were analysed in detail with respect to the mRNA levels of different isoforms during ion stress. Cluster analysis allowed identification of distinct expression profiles, and several novel putative regulatory motifs were discovered within sets of co‐expressed genes. |
doi_str_mv | 10.1046/j.1365-313X.2003.01839.x |
format | Article |
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Plant nutrition critically depends on the activity of membrane transporters that translocate minerals from the soil into the plant and are responsible for their intra‐ and intercellular distribution. Most plant membrane transporters are encoded by multigene families whose members often exhibit overlapping expression patterns and a high degree of sequence homology. Furthermore, many inorganic nutrients are transported by more than one transporter family. These considerations, coupled with a large number of so‐far non‐annotated putative transporter genes, hamper our progress in understanding how the activity of specific transporters is integrated into a response to fluctuating conditions. We designed an oligonucleotide microarray representing 1096 Arabidopsis transporter genes and analysed the root transporter transcriptome over a 96‐h period with respect to 80 mm NaCl, K+ starvation and Ca2+ starvation. Our data show that cation stress led to changes in transcript level of many genes across most transporter gene families. Analysis of transcriptionally modulated genes across all functional groups of transporters revealed families such as V‐type ATPases and aquaporins that responded to all treatments, and families – which included putative non‐selective cation channels for the NaCl treatment and metal transporters for Ca2+ starvation conditions – that responded to specific ionic environments. Several gene families including primary pumps, antiporters and aquaporins were analysed in detail with respect to the mRNA levels of different isoforms during ion stress. Cluster analysis allowed identification of distinct expression profiles, and several novel putative regulatory motifs were discovered within sets of co‐expressed genes.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1046/j.1365-313X.2003.01839.x</identifier><identifier>PMID: 12969422</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Science Ltd</publisher><subject>abiotic stress ; Arabidopsis - drug effects ; Arabidopsis - genetics ; Arabidopsis - growth & development ; Arabidopsis - physiology ; Arabidopsis Proteins - genetics ; Arabidopsis thaliana ; Biological and medical sciences ; Biological Transport ; Calcium - pharmacology ; Cations - pharmacokinetics ; Cell physiology ; expression profiling ; Fundamental and applied biological sciences. Psychology ; Genes, Plant ; Ion Pumps - genetics ; Ion Pumps - physiology ; membrane transporter ; microarray ; mineral nutrition ; Multigene Family ; Oligonucleotide Array Sequence Analysis - methods ; Plant physiology and development ; Plant Roots - physiology ; Plasma membrane and permeation ; Potassium - pharmacology ; Reverse Transcriptase Polymerase Chain Reaction ; Sodium Chloride - pharmacology ; Transcription, Genetic - genetics</subject><ispartof>The Plant journal : for cell and molecular biology, 2003-09, Vol.35 (6), p.675-692</ispartof><rights>2003 INIST-CNRS</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5979-ebfda0e367753d46f3709d5539c486f04219a5446d4222859e82811bf19fab283</citedby><cites>FETCH-LOGICAL-c5979-ebfda0e367753d46f3709d5539c486f04219a5446d4222859e82811bf19fab283</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1046%2Fj.1365-313X.2003.01839.x$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1046%2Fj.1365-313X.2003.01839.x$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=15101701$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/12969422$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Maathuis, Frans J. M.</creatorcontrib><creatorcontrib>Filatov, Victor</creatorcontrib><creatorcontrib>Herzyk, Pawel</creatorcontrib><creatorcontrib>C. Krijger, Gerard</creatorcontrib><creatorcontrib>B. Axelsen, Kristian</creatorcontrib><creatorcontrib>Chen, Sixue</creatorcontrib><creatorcontrib>Green, Brian J.</creatorcontrib><creatorcontrib>Li, Yi</creatorcontrib><creatorcontrib>Madagan, Kathryn L.</creatorcontrib><creatorcontrib>Sánchez‐Fernández, Rocío</creatorcontrib><creatorcontrib>Forde, Brian G.</creatorcontrib><creatorcontrib>Palmgren, Michael G.</creatorcontrib><creatorcontrib>Rea, Philip A.</creatorcontrib><creatorcontrib>Williams, Lorraine E.</creatorcontrib><creatorcontrib>Sanders, Dale</creatorcontrib><creatorcontrib>Amtmann, Anna</creatorcontrib><title>Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>Summary
Plant nutrition critically depends on the activity of membrane transporters that translocate minerals from the soil into the plant and are responsible for their intra‐ and intercellular distribution. Most plant membrane transporters are encoded by multigene families whose members often exhibit overlapping expression patterns and a high degree of sequence homology. Furthermore, many inorganic nutrients are transported by more than one transporter family. These considerations, coupled with a large number of so‐far non‐annotated putative transporter genes, hamper our progress in understanding how the activity of specific transporters is integrated into a response to fluctuating conditions. We designed an oligonucleotide microarray representing 1096 Arabidopsis transporter genes and analysed the root transporter transcriptome over a 96‐h period with respect to 80 mm NaCl, K+ starvation and Ca2+ starvation. Our data show that cation stress led to changes in transcript level of many genes across most transporter gene families. Analysis of transcriptionally modulated genes across all functional groups of transporters revealed families such as V‐type ATPases and aquaporins that responded to all treatments, and families – which included putative non‐selective cation channels for the NaCl treatment and metal transporters for Ca2+ starvation conditions – that responded to specific ionic environments. Several gene families including primary pumps, antiporters and aquaporins were analysed in detail with respect to the mRNA levels of different isoforms during ion stress. Cluster analysis allowed identification of distinct expression profiles, and several novel putative regulatory motifs were discovered within sets of co‐expressed genes.</description><subject>abiotic stress</subject><subject>Arabidopsis - drug effects</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis - physiology</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis thaliana</subject><subject>Biological and medical sciences</subject><subject>Biological Transport</subject><subject>Calcium - pharmacology</subject><subject>Cations - pharmacokinetics</subject><subject>Cell physiology</subject><subject>expression profiling</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Genes, Plant</subject><subject>Ion Pumps - genetics</subject><subject>Ion Pumps - physiology</subject><subject>membrane transporter</subject><subject>microarray</subject><subject>mineral nutrition</subject><subject>Multigene Family</subject><subject>Oligonucleotide Array Sequence Analysis - methods</subject><subject>Plant physiology and development</subject><subject>Plant Roots - physiology</subject><subject>Plasma membrane and permeation</subject><subject>Potassium - pharmacology</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>Sodium Chloride - pharmacology</subject><subject>Transcription, Genetic - genetics</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2003</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkc2OFCEURonROO3oKxg2uquSv6Jg4cJMRkcziS7axB2hqYvSqSpKoMfpxIeXsjvO1hWEe7574YAQpqSlRMg3-5Zy2TWc8m8tI4S3hCqu2_tHaPOv8BhtiJak6QVlF-hZzntCaM-leIouKNNSC8Y26Pc22Tm7FJYSJ8B2tuMxh4yjxynGgstaXmIqkDJOcAd2zHixqQQXFltCnFd0OowlLCPg7zAD9nYKY4CMw4zLD6ix2mHOgEvE7pTJpR7m5-iJr_3gxXm9RF_fX2-vbprbzx8-Xr27bVyne93Azg-WAJd93_FBSM97ooeu49oJJT0RjGrbCSGH-iSmOg2KKUp3nmpvd0zxS_T61HdJ8ecBcjFTyA7G0c4QD9lQpRSRegXVCXQp5pzAmyWFyaajocSs5s3erILNKtis5s1f8-a-Rl-eZxx2EwwPwbPqCrw6AzY7O_oq1oX8wHW0fg-hlXt74n6FEY7_fQGz_fJp3fE_ymuhsg</recordid><startdate>200309</startdate><enddate>200309</enddate><creator>Maathuis, Frans J. M.</creator><creator>Filatov, Victor</creator><creator>Herzyk, Pawel</creator><creator>C. Krijger, Gerard</creator><creator>B. Axelsen, Kristian</creator><creator>Chen, Sixue</creator><creator>Green, Brian J.</creator><creator>Li, Yi</creator><creator>Madagan, Kathryn L.</creator><creator>Sánchez‐Fernández, Rocío</creator><creator>Forde, Brian G.</creator><creator>Palmgren, Michael G.</creator><creator>Rea, Philip A.</creator><creator>Williams, Lorraine E.</creator><creator>Sanders, Dale</creator><creator>Amtmann, Anna</creator><general>Blackwell Science Ltd</general><general>Blackwell Science</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>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope></search><sort><creationdate>200309</creationdate><title>Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress</title><author>Maathuis, Frans J. M. ; Filatov, Victor ; Herzyk, Pawel ; C. Krijger, Gerard ; B. Axelsen, Kristian ; Chen, Sixue ; Green, Brian J. ; Li, Yi ; Madagan, Kathryn L. ; Sánchez‐Fernández, Rocío ; Forde, Brian G. ; Palmgren, Michael G. ; Rea, Philip A. ; Williams, Lorraine E. ; Sanders, Dale ; Amtmann, Anna</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5979-ebfda0e367753d46f3709d5539c486f04219a5446d4222859e82811bf19fab283</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2003</creationdate><topic>abiotic stress</topic><topic>Arabidopsis - drug effects</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - growth & development</topic><topic>Arabidopsis - physiology</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis thaliana</topic><topic>Biological and medical sciences</topic><topic>Biological Transport</topic><topic>Calcium - pharmacology</topic><topic>Cations - pharmacokinetics</topic><topic>Cell physiology</topic><topic>expression profiling</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Genes, Plant</topic><topic>Ion Pumps - genetics</topic><topic>Ion Pumps - physiology</topic><topic>membrane transporter</topic><topic>microarray</topic><topic>mineral nutrition</topic><topic>Multigene Family</topic><topic>Oligonucleotide Array Sequence Analysis - methods</topic><topic>Plant physiology and development</topic><topic>Plant Roots - physiology</topic><topic>Plasma membrane and permeation</topic><topic>Potassium - pharmacology</topic><topic>Reverse Transcriptase Polymerase Chain Reaction</topic><topic>Sodium Chloride - pharmacology</topic><topic>Transcription, Genetic - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Maathuis, Frans J. M.</creatorcontrib><creatorcontrib>Filatov, Victor</creatorcontrib><creatorcontrib>Herzyk, Pawel</creatorcontrib><creatorcontrib>C. Krijger, Gerard</creatorcontrib><creatorcontrib>B. Axelsen, Kristian</creatorcontrib><creatorcontrib>Chen, Sixue</creatorcontrib><creatorcontrib>Green, Brian J.</creatorcontrib><creatorcontrib>Li, Yi</creatorcontrib><creatorcontrib>Madagan, Kathryn L.</creatorcontrib><creatorcontrib>Sánchez‐Fernández, Rocío</creatorcontrib><creatorcontrib>Forde, Brian G.</creatorcontrib><creatorcontrib>Palmgren, Michael G.</creatorcontrib><creatorcontrib>Rea, Philip A.</creatorcontrib><creatorcontrib>Williams, Lorraine E.</creatorcontrib><creatorcontrib>Sanders, Dale</creatorcontrib><creatorcontrib>Amtmann, Anna</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><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Maathuis, Frans J. M.</au><au>Filatov, Victor</au><au>Herzyk, Pawel</au><au>C. Krijger, Gerard</au><au>B. Axelsen, Kristian</au><au>Chen, Sixue</au><au>Green, Brian J.</au><au>Li, Yi</au><au>Madagan, Kathryn L.</au><au>Sánchez‐Fernández, Rocío</au><au>Forde, Brian G.</au><au>Palmgren, Michael G.</au><au>Rea, Philip A.</au><au>Williams, Lorraine E.</au><au>Sanders, Dale</au><au>Amtmann, Anna</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2003-09</date><risdate>2003</risdate><volume>35</volume><issue>6</issue><spage>675</spage><epage>692</epage><pages>675-692</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>Summary
Plant nutrition critically depends on the activity of membrane transporters that translocate minerals from the soil into the plant and are responsible for their intra‐ and intercellular distribution. Most plant membrane transporters are encoded by multigene families whose members often exhibit overlapping expression patterns and a high degree of sequence homology. Furthermore, many inorganic nutrients are transported by more than one transporter family. These considerations, coupled with a large number of so‐far non‐annotated putative transporter genes, hamper our progress in understanding how the activity of specific transporters is integrated into a response to fluctuating conditions. We designed an oligonucleotide microarray representing 1096 Arabidopsis transporter genes and analysed the root transporter transcriptome over a 96‐h period with respect to 80 mm NaCl, K+ starvation and Ca2+ starvation. Our data show that cation stress led to changes in transcript level of many genes across most transporter gene families. Analysis of transcriptionally modulated genes across all functional groups of transporters revealed families such as V‐type ATPases and aquaporins that responded to all treatments, and families – which included putative non‐selective cation channels for the NaCl treatment and metal transporters for Ca2+ starvation conditions – that responded to specific ionic environments. Several gene families including primary pumps, antiporters and aquaporins were analysed in detail with respect to the mRNA levels of different isoforms during ion stress. Cluster analysis allowed identification of distinct expression profiles, and several novel putative regulatory motifs were discovered within sets of co‐expressed genes.</abstract><cop>Oxford, UK</cop><pub>Blackwell Science Ltd</pub><pmid>12969422</pmid><doi>10.1046/j.1365-313X.2003.01839.x</doi><tpages>18</tpages><oa>free_for_read</oa></addata></record> |
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subjects | abiotic stress Arabidopsis - drug effects Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis - physiology Arabidopsis Proteins - genetics Arabidopsis thaliana Biological and medical sciences Biological Transport Calcium - pharmacology Cations - pharmacokinetics Cell physiology expression profiling Fundamental and applied biological sciences. Psychology Genes, Plant Ion Pumps - genetics Ion Pumps - physiology membrane transporter microarray mineral nutrition Multigene Family Oligonucleotide Array Sequence Analysis - methods Plant physiology and development Plant Roots - physiology Plasma membrane and permeation Potassium - pharmacology Reverse Transcriptase Polymerase Chain Reaction Sodium Chloride - pharmacology Transcription, Genetic - genetics |
title | Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress |
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