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
Hauptverfasser: 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
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container_issue 6
container_start_page 675
container_title The Plant journal : for cell and molecular biology
container_volume 35
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
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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</creator><creatorcontrib>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</creatorcontrib><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><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 &amp; 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. 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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. 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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. 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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 &amp; 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. 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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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