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A NAC‐type transcription factor confers aluminium resistance by regulating cell wall‐associated receptor kinase 1 and cell wall pectin

Transcriptional regulation is important for plants to respond to toxic effects of aluminium (Al). However, our current knowledge to these events is confined to a few transcription factors. Here, we functionally characterized a rice bean (Vigna umbellata) NAC‐type transcription factor, VuNAR1, in ter...

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Published in:Plant, cell and environment cell and environment, 2020-02, Vol.43 (2), p.463-478
Main Authors: Lou, He Qiang, Fan, Wei, Jin, Jian Feng, Xu, Jia Meng, Chen, Wei Wei, Yang, Jian Li, Zheng, Shao Jian
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description Transcriptional regulation is important for plants to respond to toxic effects of aluminium (Al). However, our current knowledge to these events is confined to a few transcription factors. Here, we functionally characterized a rice bean (Vigna umbellata) NAC‐type transcription factor, VuNAR1, in terms of Al stress response. We demonstrated that rice bean VuNAR1 is a nuclear‐localized transcriptional activator, whose expression was specifically upregulated by Al in roots but not in shoot. VuNAR1 overexpressing Arabidopsis plants exhibit improved Al resistance via Al exclusion. However, VuNAR1‐mediated Al exclusion is independent of the function of known Al‐resistant genes. Comparative transcriptomic analysis revealed that VuNAR1 specifically regulates the expression of genes associated with protein phosphorylation and cell wall modification in Arabidopsis. Transient expression assay demonstrated the direct transcriptional activation of cell wall‐associated receptor kinase 1 (WAK1) by VuNAR1. Moreover, yeast one‐hybrid assays and MEME motif searches identified a new VuNAR1‐specific binding motif in the promoter of WAK1. Compared with wild‐type Arabidopsis plants, VuNAR1 overexpressing plants have higher WAK1 expression and less pectin content. Taken together, our results suggest that VuNAR1 regulates Al resistance by regulating cell wall pectin metabolism via directly binding to the promoter of WAK1 and induce its expression. A rice bean NAC‐type transcription factor is involved in Al resistance by directly regulating WAK1 expression that is associated with cell wall pectin content.
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However, our current knowledge to these events is confined to a few transcription factors. Here, we functionally characterized a rice bean (Vigna umbellata) NAC‐type transcription factor, VuNAR1, in terms of Al stress response. We demonstrated that rice bean VuNAR1 is a nuclear‐localized transcriptional activator, whose expression was specifically upregulated by Al in roots but not in shoot. VuNAR1 overexpressing Arabidopsis plants exhibit improved Al resistance via Al exclusion. However, VuNAR1‐mediated Al exclusion is independent of the function of known Al‐resistant genes. Comparative transcriptomic analysis revealed that VuNAR1 specifically regulates the expression of genes associated with protein phosphorylation and cell wall modification in Arabidopsis. Transient expression assay demonstrated the direct transcriptional activation of cell wall‐associated receptor kinase 1 (WAK1) by VuNAR1. Moreover, yeast one‐hybrid assays and MEME motif searches identified a new VuNAR1‐specific binding motif in the promoter of WAK1. Compared with wild‐type Arabidopsis plants, VuNAR1 overexpressing plants have higher WAK1 expression and less pectin content. Taken together, our results suggest that VuNAR1 regulates Al resistance by regulating cell wall pectin metabolism via directly binding to the promoter of WAK1 and induce its expression. A rice bean NAC‐type transcription factor is involved in Al resistance by directly regulating WAK1 expression that is associated with cell wall pectin content.</description><identifier>ISSN: 0140-7791</identifier><identifier>EISSN: 1365-3040</identifier><identifier>DOI: 10.1111/pce.13676</identifier><identifier>PMID: 31713247</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>aluminium stress ; Aluminum ; Aluminum - pharmacology ; Arabidopsis ; Arabidopsis - genetics ; Arabidopsis Proteins ; Beans ; Binding ; Cell activation ; Cell Wall - metabolism ; Cell walls ; cell wall‐associated receptor kinase ; Drug Resistance - drug effects ; Drug Resistance - physiology ; Gene expression ; Gene Expression Regulation, Plant - drug effects ; Gene regulation ; Genes ; Iron-Sulfur Proteins - genetics ; Iron-Sulfur Proteins - metabolism ; Kinases ; Membrane Proteins - genetics ; Membrane Proteins - metabolism ; nutrients ; Pectin ; Pectins - metabolism ; Phosphorylation ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plant Roots - drug effects ; Plant Roots - metabolism ; Plants, Genetically Modified ; Protein Kinases - genetics ; Protein Kinases - metabolism ; Resistance factors ; signalling ; Transcription activation ; Transcription factors ; Transcription Factors - metabolism ; transcriptome ; Up-Regulation - drug effects ; Vigna - drug effects ; Vigna - genetics ; Vigna - metabolism ; Vigna umbellata ; Yeasts</subject><ispartof>Plant, cell and environment, 2020-02, Vol.43 (2), p.463-478</ispartof><rights>2019 John Wiley &amp; Sons Ltd</rights><rights>2019 John Wiley &amp; Sons Ltd.</rights><rights>2020 John Wiley &amp; Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3886-5af1581172566813172a53043d2b3da686664aaf42b432b712b15ba66551a4073</citedby><cites>FETCH-LOGICAL-c3886-5af1581172566813172a53043d2b3da686664aaf42b432b712b15ba66551a4073</cites><orcidid>0000-0002-3336-8165 ; 0000-0003-0385-5787 ; 0000-0002-2454-098X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31713247$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lou, He Qiang</creatorcontrib><creatorcontrib>Fan, Wei</creatorcontrib><creatorcontrib>Jin, Jian Feng</creatorcontrib><creatorcontrib>Xu, Jia Meng</creatorcontrib><creatorcontrib>Chen, Wei Wei</creatorcontrib><creatorcontrib>Yang, Jian Li</creatorcontrib><creatorcontrib>Zheng, Shao Jian</creatorcontrib><title>A NAC‐type transcription factor confers aluminium resistance by regulating cell wall‐associated receptor kinase 1 and cell wall pectin</title><title>Plant, cell and environment</title><addtitle>Plant Cell Environ</addtitle><description>Transcriptional regulation is important for plants to respond to toxic effects of aluminium (Al). However, our current knowledge to these events is confined to a few transcription factors. Here, we functionally characterized a rice bean (Vigna umbellata) NAC‐type transcription factor, VuNAR1, in terms of Al stress response. We demonstrated that rice bean VuNAR1 is a nuclear‐localized transcriptional activator, whose expression was specifically upregulated by Al in roots but not in shoot. VuNAR1 overexpressing Arabidopsis plants exhibit improved Al resistance via Al exclusion. However, VuNAR1‐mediated Al exclusion is independent of the function of known Al‐resistant genes. Comparative transcriptomic analysis revealed that VuNAR1 specifically regulates the expression of genes associated with protein phosphorylation and cell wall modification in Arabidopsis. Transient expression assay demonstrated the direct transcriptional activation of cell wall‐associated receptor kinase 1 (WAK1) by VuNAR1. Moreover, yeast one‐hybrid assays and MEME motif searches identified a new VuNAR1‐specific binding motif in the promoter of WAK1. Compared with wild‐type Arabidopsis plants, VuNAR1 overexpressing plants have higher WAK1 expression and less pectin content. Taken together, our results suggest that VuNAR1 regulates Al resistance by regulating cell wall pectin metabolism via directly binding to the promoter of WAK1 and induce its expression. A rice bean NAC‐type transcription factor is involved in Al resistance by directly regulating WAK1 expression that is associated with cell wall pectin content.</description><subject>aluminium stress</subject><subject>Aluminum</subject><subject>Aluminum - pharmacology</subject><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis Proteins</subject><subject>Beans</subject><subject>Binding</subject><subject>Cell activation</subject><subject>Cell Wall - metabolism</subject><subject>Cell walls</subject><subject>cell wall‐associated receptor kinase</subject><subject>Drug Resistance - drug effects</subject><subject>Drug Resistance - physiology</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant - drug effects</subject><subject>Gene regulation</subject><subject>Genes</subject><subject>Iron-Sulfur Proteins - genetics</subject><subject>Iron-Sulfur Proteins - metabolism</subject><subject>Kinases</subject><subject>Membrane Proteins - genetics</subject><subject>Membrane Proteins - metabolism</subject><subject>nutrients</subject><subject>Pectin</subject><subject>Pectins - metabolism</subject><subject>Phosphorylation</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plant Roots - drug effects</subject><subject>Plant Roots - metabolism</subject><subject>Plants, Genetically Modified</subject><subject>Protein Kinases - genetics</subject><subject>Protein Kinases - metabolism</subject><subject>Resistance factors</subject><subject>signalling</subject><subject>Transcription activation</subject><subject>Transcription factors</subject><subject>Transcription Factors - metabolism</subject><subject>transcriptome</subject><subject>Up-Regulation - drug effects</subject><subject>Vigna - drug effects</subject><subject>Vigna - genetics</subject><subject>Vigna - metabolism</subject><subject>Vigna umbellata</subject><subject>Yeasts</subject><issn>0140-7791</issn><issn>1365-3040</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNp1kD1PwzAQhi0EoqUw8AeQJSaGFDuO7XSsqvIhVcAAc3RxnMoldYKdqOrGzMRv5JfgfgATXk4-Pfec7kXonJIhDe-6UXpImZDiAPVD5REjCTlEfUITEkk5oj104v2CkNCQo2PUY1RSFieyjz7G-GE8-Xr_bNeNxq0D65UzTWtqi0tQbe2wqm2pncdQdUtjTbfETnvjW7BK43wdfvOugtbYOVa6qvAKqioIwftaGWh1EQilm43q1VjwGlMMtviDcaNVGD9FRyVUXp_t6wC93EyfJ3fR7PH2fjKeRYqlqYg4lJSnlMqYC5HScEoMPBzMijhnBYhUCJEAlEmcJyzOJY1zynMQgnMKCZFsgC533sbVb532bbaoO2fDyixmYQVPxJa62lHK1d47XWaNM0tw64ySbJN6FlLPtqkH9mJv7PKlLn7Jn5gDcL0DVqbS6_9N2dNkulN-AxiAjck</recordid><startdate>202002</startdate><enddate>202002</enddate><creator>Lou, He Qiang</creator><creator>Fan, Wei</creator><creator>Jin, Jian Feng</creator><creator>Xu, Jia Meng</creator><creator>Chen, Wei Wei</creator><creator>Yang, Jian Li</creator><creator>Zheng, Shao Jian</creator><general>Wiley Subscription Services, Inc</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>7QP</scope><scope>7ST</scope><scope>C1K</scope><scope>SOI</scope><orcidid>https://orcid.org/0000-0002-3336-8165</orcidid><orcidid>https://orcid.org/0000-0003-0385-5787</orcidid><orcidid>https://orcid.org/0000-0002-2454-098X</orcidid></search><sort><creationdate>202002</creationdate><title>A NAC‐type transcription factor confers aluminium resistance by regulating cell wall‐associated receptor kinase 1 and cell wall pectin</title><author>Lou, He Qiang ; 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However, our current knowledge to these events is confined to a few transcription factors. Here, we functionally characterized a rice bean (Vigna umbellata) NAC‐type transcription factor, VuNAR1, in terms of Al stress response. We demonstrated that rice bean VuNAR1 is a nuclear‐localized transcriptional activator, whose expression was specifically upregulated by Al in roots but not in shoot. VuNAR1 overexpressing Arabidopsis plants exhibit improved Al resistance via Al exclusion. However, VuNAR1‐mediated Al exclusion is independent of the function of known Al‐resistant genes. Comparative transcriptomic analysis revealed that VuNAR1 specifically regulates the expression of genes associated with protein phosphorylation and cell wall modification in Arabidopsis. Transient expression assay demonstrated the direct transcriptional activation of cell wall‐associated receptor kinase 1 (WAK1) by VuNAR1. Moreover, yeast one‐hybrid assays and MEME motif searches identified a new VuNAR1‐specific binding motif in the promoter of WAK1. Compared with wild‐type Arabidopsis plants, VuNAR1 overexpressing plants have higher WAK1 expression and less pectin content. Taken together, our results suggest that VuNAR1 regulates Al resistance by regulating cell wall pectin metabolism via directly binding to the promoter of WAK1 and induce its expression. A rice bean NAC‐type transcription factor is involved in Al resistance by directly regulating WAK1 expression that is associated with cell wall pectin content.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>31713247</pmid><doi>10.1111/pce.13676</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-3336-8165</orcidid><orcidid>https://orcid.org/0000-0003-0385-5787</orcidid><orcidid>https://orcid.org/0000-0002-2454-098X</orcidid><oa>free_for_read</oa></addata></record>
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subjects aluminium stress
Aluminum
Aluminum - pharmacology
Arabidopsis
Arabidopsis - genetics
Arabidopsis Proteins
Beans
Binding
Cell activation
Cell Wall - metabolism
Cell walls
cell wall‐associated receptor kinase
Drug Resistance - drug effects
Drug Resistance - physiology
Gene expression
Gene Expression Regulation, Plant - drug effects
Gene regulation
Genes
Iron-Sulfur Proteins - genetics
Iron-Sulfur Proteins - metabolism
Kinases
Membrane Proteins - genetics
Membrane Proteins - metabolism
nutrients
Pectin
Pectins - metabolism
Phosphorylation
Plant Proteins - genetics
Plant Proteins - metabolism
Plant Roots - drug effects
Plant Roots - metabolism
Plants, Genetically Modified
Protein Kinases - genetics
Protein Kinases - metabolism
Resistance factors
signalling
Transcription activation
Transcription factors
Transcription Factors - metabolism
transcriptome
Up-Regulation - drug effects
Vigna - drug effects
Vigna - genetics
Vigna - metabolism
Vigna umbellata
Yeasts
title A NAC‐type transcription factor confers aluminium resistance by regulating cell wall‐associated receptor kinase 1 and cell wall pectin
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