A LuxR Homolog in a Cottonwood Tree Endophyte That Activates Gene Expression in Response to a Plant Signal or Specific Peptides.
Identifieur interne : 001681 ( Main/Corpus ); précédent : 001680; suivant : 001682A LuxR Homolog in a Cottonwood Tree Endophyte That Activates Gene Expression in Response to a Plant Signal or Specific Peptides.
Auteurs : Amy L. Schaefer ; Yasuhiro Oda ; Bruna Goncalves Coutinho ; Dale A. Pelletier ; Justin Weiburg ; Vittorio Venturi ; E Peter Greenberg ; Caroline S. HarwoodSource :
- mBio [ 2150-7511 ] ; 2016.
English descriptors
- KwdEn :
- ATP-Binding Cassette Transporters (genetics), ATP-Binding Cassette Transporters (metabolism), Endophytes (genetics), Gene Expression Regulation (MeSH), Peptide Hydrolases (metabolism), Peptides (genetics), Peptides (metabolism), Populus (microbiology), Pseudomonas (genetics), Transcription Factors (genetics), Transcription Factors (metabolism), Transcriptional Activation (drug effects).
- MESH :
- chemical , genetics : ATP-Binding Cassette Transporters, Peptides, Transcription Factors.
- chemical , metabolism : ATP-Binding Cassette Transporters, Peptide Hydrolases, Peptides, Transcription Factors.
- drug effects : Transcriptional Activation.
- genetics : Endophytes, Pseudomonas.
- microbiology : Populus.
- Gene Expression Regulation.
Abstract
UNLABELLED
Homologs of the LuxR acyl-homoserine lactone (AHL) quorum-sensing signal receptor are prevalent in Proteobacteria isolated from roots of the Eastern cottonwood tree, Populus deltoides Many of these isolates possess an orphan LuxR homolog, closely related to OryR from the rice pathogen Xanthomonas oryzae OryR does not respond to AHL signals but, instead, responds to an unknown plant compound. We discovered an OryR homolog, PipR, in the cottonwood endophyte Pseudomonas sp. strain GM79. The genes adjacent to pipR encode a predicted ATP-binding cassette (ABC) peptide transporter and peptidases. We purified the putative peptidases, PipA and AapA, and confirmed their predicted activities. A transcriptional pipA-gfp reporter was responsive to PipR in the presence of plant leaf macerates, but it was not influenced by AHLs, similar to findings with OryR. We found that PipR also responded to protein hydrolysates to activate pipA-gfp expression. Among many peptides tested, the tripeptide Ser-His-Ser showed inducer activity but at relatively high concentrations. An ABC peptide transporter mutant failed to respond to leaf macerates, peptone, or Ser-His-Ser, while peptidase mutants expressed higher-than-wild-type levels of pipA-gfp in response to any of these signals. Our studies are consistent with a model where active transport of a peptidelike signal is required for the signal to interact with PipR, which then activates peptidase gene expression. The identification of a peptide ligand for PipR sets the stage to identify plant-derived signals for the OryR family of orphan LuxR proteins.
IMPORTANCE
We describe the transcription factor PipR from a Pseudomonas strain isolated as a cottonwood tree endophyte. PipR is a member of the LuxR family of transcriptional factors. LuxR family members are generally thought of as quorum-sensing signal receptors, but PipR is one of an emerging subfamily of LuxR family members that respond to compounds produced by plants. We found that PipR responds to a peptidelike compound, and we present a model for Pip system signal transduction. A better understanding of plant-responsive LuxR homologs and the compounds to which they respond is of general importance, as they occur in dozens of bacterial species that are associated with economically important plants and, as we report here, they also occur in members of certain root endophyte communities.
DOI: 10.1128/mBio.01101-16
PubMed: 27486195
PubMed Central: PMC4981722
Links to Exploration step
pubmed:27486195Le document en format XML
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Pelletier</name><affiliation><nlm:affiliation>Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Weiburg, Justin" sort="Weiburg, Justin" uniqKey="Weiburg J" first="Justin" last="Weiburg">Justin Weiburg</name><affiliation><nlm:affiliation>University of Washington, Seattle, Washington, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Venturi, Vittorio" sort="Venturi, Vittorio" uniqKey="Venturi V" first="Vittorio" last="Venturi">Vittorio Venturi</name><affiliation><nlm:affiliation>International Centre for Genetic Engineering and Biotechnology, Trieste, Italy.</nlm:affiliation></affiliation></author><author><name sortKey="Greenberg, E Peter" sort="Greenberg, E Peter" uniqKey="Greenberg E" first="E Peter" last="Greenberg">E Peter Greenberg</name><affiliation><nlm:affiliation>University of Washington, Seattle, Washington, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Harwood, Caroline S" sort="Harwood, Caroline S" uniqKey="Harwood C" first="Caroline S" last="Harwood">Caroline S. Harwood</name><affiliation><nlm:affiliation>University of Washington, Seattle, Washington, USA csh5@uw.edu.</nlm:affiliation></affiliation></author></analytic><series><title level="j">mBio</title><idno type="eISSN">2150-7511</idno><imprint><date when="2016" type="published">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>ATP-Binding Cassette Transporters (genetics)</term><term>ATP-Binding Cassette Transporters (metabolism)</term><term>Endophytes (genetics)</term><term>Gene Expression Regulation (MeSH)</term><term>Peptide Hydrolases (metabolism)</term><term>Peptides (genetics)</term><term>Peptides (metabolism)</term><term>Populus (microbiology)</term><term>Pseudomonas (genetics)</term><term>Transcription Factors (genetics)</term><term>Transcription Factors (metabolism)</term><term>Transcriptional Activation (drug effects)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>ATP-Binding Cassette Transporters</term><term>Peptides</term><term>Transcription Factors</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>ATP-Binding Cassette Transporters</term><term>Peptide Hydrolases</term><term>Peptides</term><term>Transcription Factors</term></keywords><keywords scheme="MESH" qualifier="drug effects" xml:lang="en"><term>Transcriptional Activation</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Endophytes</term><term>Pseudomonas</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Populus</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Gene Expression Regulation</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p><b>UNLABELLED</b></p><p>Homologs of the LuxR acyl-homoserine lactone (AHL) quorum-sensing signal receptor are prevalent in Proteobacteria isolated from roots of the Eastern cottonwood tree, Populus deltoides Many of these isolates possess an orphan LuxR homolog, closely related to OryR from the rice pathogen Xanthomonas oryzae OryR does not respond to AHL signals but, instead, responds to an unknown plant compound. We discovered an OryR homolog, PipR, in the cottonwood endophyte Pseudomonas sp. strain GM79. The genes adjacent to pipR encode a predicted ATP-binding cassette (ABC) peptide transporter and peptidases. We purified the putative peptidases, PipA and AapA, and confirmed their predicted activities. A transcriptional pipA-gfp reporter was responsive to PipR in the presence of plant leaf macerates, but it was not influenced by AHLs, similar to findings with OryR. We found that PipR also responded to protein hydrolysates to activate pipA-gfp expression. Among many peptides tested, the tripeptide Ser-His-Ser showed inducer activity but at relatively high concentrations. An ABC peptide transporter mutant failed to respond to leaf macerates, peptone, or Ser-His-Ser, while peptidase mutants expressed higher-than-wild-type levels of pipA-gfp in response to any of these signals. Our studies are consistent with a model where active transport of a peptidelike signal is required for the signal to interact with PipR, which then activates peptidase gene expression. The identification of a peptide ligand for PipR sets the stage to identify plant-derived signals for the OryR family of orphan LuxR proteins.</p></div><div type="abstract" xml:lang="en"><p><b>IMPORTANCE</b></p><p>We describe the transcription factor PipR from a Pseudomonas strain isolated as a cottonwood tree endophyte. PipR is a member of the LuxR family of transcriptional factors. LuxR family members are generally thought of as quorum-sensing signal receptors, but PipR is one of an emerging subfamily of LuxR family members that respond to compounds produced by plants. We found that PipR responds to a peptidelike compound, and we present a model for Pip system signal transduction. A better understanding of plant-responsive LuxR homologs and the compounds to which they respond is of general importance, as they occur in dozens of bacterial species that are associated with economically important plants and, as we report here, they also occur in members of certain root endophyte communities.</p></div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">27486195</PMID><DateCompleted><Year>2017</Year><Month>06</Month><Day>20</Day></DateCompleted><DateRevised><Year>2019</Year><Month>12</Month><Day>27</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2150-7511</ISSN><JournalIssue CitedMedium="Internet"><Volume>7</Volume><Issue>4</Issue><PubDate><Year>2016</Year><Month>08</Month><Day>02</Day></PubDate></JournalIssue><Title>mBio</Title><ISOAbbreviation>mBio</ISOAbbreviation></Journal><ArticleTitle>A LuxR Homolog in a Cottonwood Tree Endophyte That Activates Gene Expression in Response to a Plant Signal or Specific Peptides.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1128/mBio.01101-16</ELocationID><ELocationID EIdType="pii" ValidYN="Y">e01101-16</ELocationID><Abstract><AbstractText Label="UNLABELLED">Homologs of the LuxR acyl-homoserine lactone (AHL) quorum-sensing signal receptor are prevalent in Proteobacteria isolated from roots of the Eastern cottonwood tree, Populus deltoides Many of these isolates possess an orphan LuxR homolog, closely related to OryR from the rice pathogen Xanthomonas oryzae OryR does not respond to AHL signals but, instead, responds to an unknown plant compound. We discovered an OryR homolog, PipR, in the cottonwood endophyte Pseudomonas sp. strain GM79. The genes adjacent to pipR encode a predicted ATP-binding cassette (ABC) peptide transporter and peptidases. We purified the putative peptidases, PipA and AapA, and confirmed their predicted activities. A transcriptional pipA-gfp reporter was responsive to PipR in the presence of plant leaf macerates, but it was not influenced by AHLs, similar to findings with OryR. We found that PipR also responded to protein hydrolysates to activate pipA-gfp expression. Among many peptides tested, the tripeptide Ser-His-Ser showed inducer activity but at relatively high concentrations. An ABC peptide transporter mutant failed to respond to leaf macerates, peptone, or Ser-His-Ser, while peptidase mutants expressed higher-than-wild-type levels of pipA-gfp in response to any of these signals. Our studies are consistent with a model where active transport of a peptidelike signal is required for the signal to interact with PipR, which then activates peptidase gene expression. The identification of a peptide ligand for PipR sets the stage to identify plant-derived signals for the OryR family of orphan LuxR proteins.</AbstractText><AbstractText Label="IMPORTANCE">We describe the transcription factor PipR from a Pseudomonas strain isolated as a cottonwood tree endophyte. PipR is a member of the LuxR family of transcriptional factors. LuxR family members are generally thought of as quorum-sensing signal receptors, but PipR is one of an emerging subfamily of LuxR family members that respond to compounds produced by plants. We found that PipR responds to a peptidelike compound, and we present a model for Pip system signal transduction. A better understanding of plant-responsive LuxR homologs and the compounds to which they respond is of general importance, as they occur in dozens of bacterial species that are associated with economically important plants and, as we report here, they also occur in members of certain root endophyte communities.</AbstractText><CopyrightInformation>Copyright © 2016 Schaefer et al.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Schaefer</LastName><ForeName>Amy L</ForeName><Initials>AL</Initials><AffiliationInfo><Affiliation>University of Washington, Seattle, Washington, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Oda</LastName><ForeName>Yasuhiro</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>University of Washington, Seattle, Washington, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Coutinho</LastName><ForeName>Bruna Goncalves</ForeName><Initials>BG</Initials><AffiliationInfo><Affiliation>University of Washington, Seattle, Washington, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pelletier</LastName><ForeName>Dale A</ForeName><Initials>DA</Initials><AffiliationInfo><Affiliation>Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Weiburg</LastName><ForeName>Justin</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>University of Washington, Seattle, Washington, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Venturi</LastName><ForeName>Vittorio</ForeName><Initials>V</Initials><AffiliationInfo><Affiliation>International Centre for Genetic Engineering and Biotechnology, Trieste, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Greenberg</LastName><ForeName>E Peter</ForeName><Initials>EP</Initials><AffiliationInfo><Affiliation>University of Washington, Seattle, Washington, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Harwood</LastName><ForeName>Caroline S</ForeName><Initials>CS</Initials><Identifier Source="ORCID">0000-0003-4450-5177</Identifier><AffiliationInfo><Affiliation>University of Washington, Seattle, Washington, USA csh5@uw.edu.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2016</Year><Month>08</Month><Day>02</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>mBio</MedlineTA><NlmUniqueID>101519231</NlmUniqueID></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D018528">ATP-Binding Cassette Transporters</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010455">Peptides</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D014157">Transcription Factors</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 3.4.-</RegistryNumber><NameOfSubstance UI="D010447">Peptide Hydrolases</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D018528" MajorTopicYN="N">ATP-Binding Cassette Transporters</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D060026" MajorTopicYN="N">Endophytes</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D005786" MajorTopicYN="Y">Gene Expression Regulation</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010447" MajorTopicYN="N">Peptide Hydrolases</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010455" MajorTopicYN="N">Peptides</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName><QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D011549" MajorTopicYN="N">Pseudomonas</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D014157" MajorTopicYN="N">Transcription Factors</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D015533" MajorTopicYN="N">Transcriptional Activation</DescriptorName><QualifierName UI="Q000187" MajorTopicYN="Y">drug effects</QualifierName></MeshHeading></MeshHeadingList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="entrez"><Year>2016</Year><Month>8</Month><Day>4</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2016</Year><Month>8</Month><Day>4</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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