Pre-announcement of symbiotic guests: transcriptional reprogramming by mycorrhizal lipochitooligosaccharides shows a strict co-dependency on the GRAS transcription factors NSP1 and RAM1.
Identifieur interne : 001270 ( Main/Corpus ); précédent : 001269; suivant : 001271Pre-announcement of symbiotic guests: transcriptional reprogramming by mycorrhizal lipochitooligosaccharides shows a strict co-dependency on the GRAS transcription factors NSP1 and RAM1.
Auteurs : Natalija Hohnjec ; Lisa F. Czaja-Hasse ; Claudia Hogekamp ; Helge KüsterSource :
- BMC genomics [ 1471-2164 ] ; 2015.
English descriptors
- KwdEn :
- Gene Expression Profiling (MeSH), Gene Expression Regulation, Plant (drug effects), Genome, Plant (MeSH), Glomeromycota (physiology), Host-Pathogen Interactions (MeSH), Lipopolysaccharides (metabolism), Lipopolysaccharides (pharmacology), Medicago truncatula (genetics), Mycorrhizae (physiology), Plant Proteins (genetics), Symbiosis (MeSH), Transcription Factors (genetics).
- MESH :
- chemical , genetics : Plant Proteins, Transcription Factors.
- chemical , metabolism : Lipopolysaccharides.
- drug effects : Gene Expression Regulation, Plant.
- genetics : Medicago truncatula.
- chemical , pharmacology : Lipopolysaccharides.
- physiology : Glomeromycota, Mycorrhizae.
- Gene Expression Profiling, Genome, Plant, Host-Pathogen Interactions, Symbiosis.
Abstract
BACKGROUND
More than 80 % of all terrestrial plant species establish an arbuscular mycorrhiza (AM) symbiosis with Glomeromycota fungi. This plant-microbe interaction primarily improves phosphate uptake, but also supports nitrogen, mineral, and water aquisition. During the pre-contact stage, the AM symbiosis is controled by an exchange of diffusible factors from either partner. Amongst others, fungal signals were identified as a mix of sulfated and non-sulfated lipochitooligosaccharides (LCOs), being structurally related to rhizobial nodulation (Nod)-factor LCOs that in legumes induce the formation of nitrogen-fixing root nodules. LCO signals are transduced via a common symbiotic signaling pathway (CSSP) that activates a group of GRAS transcription factors (TFs). Using complex gene expression fingerprints as molecular phenotypes, this study primarily intended to shed light on the importance of the GRAS TFs NSP1 and RAM1 for LCO-activated gene expression during pre-symbiotic signaling.
RESULTS
We investigated the genome-wide transcriptional responses in 5 days old primary roots of the Medicago truncatula wild type and four symbiotic mutants to a 6 h challenge with LCO signals supplied at 10(-7/-8) M. We were able to show that during the pre-symbiotic stage, sulfated Myc-, non-sulfated Myc-, and Nod-LCO-activated gene expression almost exclusively depends on the LysM receptor kinase NFP and is largely controled by the CSSP, although responses independent of this pathway exist. Our results show that downstream of the CSSP, gene expression activation by Myc-LCOs supplied at 10(-7/-8) M strictly required both the GRAS transcription factors RAM1 and NSP1, whereas those genes either co- or specifically activated by Nod-LCOs displayed a preferential NSP1-dependency. RAM1, a central regulator of root colonization by AM fungi, controled genes activated by non-sulfated Myc-LCOs during the pre-symbiotic stage that are also up-regulated in areas with early physical contact, e.g. hyphopodia and infecting hyphae; linking responses to externally applied LCOs with early root colonization.
CONCLUSIONS
Since both RAM1 and NSP1 were essential for the pre-symbiotic transcriptional reprogramming by Myc-LCOs, we propose that downstream of the CSSP, these GRAS transcription factors act synergistically in the transduction of those diffusible signals that pre-announce the presence of symbiotic fungi.
DOI: 10.1186/s12864-015-2224-7
PubMed: 26597293
PubMed Central: PMC4657205
Links to Exploration step
pubmed:26597293Le document en format XML
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IV - Pflanzengenomforschung, Leibniz Universität Hannover, Herrenhäuser Str. 2, D-30419, Hannover, Germany. czaja@mpipz.mpg.de.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Present address: Max Planck Genome Centre Cologne, Carl-von-Linné-Weg 10, D-50829, Köln, Germany. czaja@mpipz.mpg.de.</nlm:affiliation></affiliation></author><author><name sortKey="Hogekamp, Claudia" sort="Hogekamp, Claudia" uniqKey="Hogekamp C" first="Claudia" last="Hogekamp">Claudia Hogekamp</name><affiliation><nlm:affiliation>Institut für Pflanzengenetik, Abt. IV - Pflanzengenomforschung, Leibniz Universität Hannover, Herrenhäuser Str. 2, D-30419, Hannover, Germany. claudia.hogekamp@genetik.uni-hannover.de.</nlm:affiliation></affiliation></author><author><name sortKey="Kuster, Helge" sort="Kuster, Helge" uniqKey="Kuster H" first="Helge" last="Küster">Helge Küster</name><affiliation><nlm:affiliation>Institut für Pflanzengenetik, Abt. IV - Pflanzengenomforschung, Leibniz Universität Hannover, Herrenhäuser Str. 2, D-30419, Hannover, Germany. helge.kuester@genetik.uni-hannover.de.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2015">2015</date><idno type="RBID">pubmed:26597293</idno><idno type="pmid">26597293</idno><idno type="doi">10.1186/s12864-015-2224-7</idno><idno type="pmc">PMC4657205</idno><idno type="wicri:Area/Main/Corpus">001270</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">001270</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Pre-announcement of symbiotic guests: transcriptional reprogramming by mycorrhizal lipochitooligosaccharides shows a strict co-dependency on the GRAS transcription factors NSP1 and RAM1.</title><author><name sortKey="Hohnjec, Natalija" sort="Hohnjec, Natalija" uniqKey="Hohnjec N" first="Natalija" last="Hohnjec">Natalija Hohnjec</name><affiliation><nlm:affiliation>Institut für Pflanzengenetik, Abt. IV - Pflanzengenomforschung, Leibniz Universität Hannover, Herrenhäuser Str. 2, D-30419, Hannover, Germany. natalija.hohnjec@genetik.uni-hannover.de.</nlm:affiliation></affiliation></author><author><name sortKey="Czaja Hasse, Lisa F" sort="Czaja Hasse, Lisa F" uniqKey="Czaja Hasse L" first="Lisa F" last="Czaja-Hasse">Lisa F. Czaja-Hasse</name><affiliation><nlm:affiliation>Institut für Pflanzengenetik, Abt. IV - Pflanzengenomforschung, Leibniz Universität Hannover, Herrenhäuser Str. 2, D-30419, Hannover, Germany. czaja@mpipz.mpg.de.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Present address: Max Planck Genome Centre Cologne, Carl-von-Linné-Weg 10, D-50829, Köln, Germany. czaja@mpipz.mpg.de.</nlm:affiliation></affiliation></author><author><name sortKey="Hogekamp, Claudia" sort="Hogekamp, Claudia" uniqKey="Hogekamp C" first="Claudia" last="Hogekamp">Claudia Hogekamp</name><affiliation><nlm:affiliation>Institut für Pflanzengenetik, Abt. IV - Pflanzengenomforschung, Leibniz Universität Hannover, Herrenhäuser Str. 2, D-30419, Hannover, Germany. claudia.hogekamp@genetik.uni-hannover.de.</nlm:affiliation></affiliation></author><author><name sortKey="Kuster, Helge" sort="Kuster, Helge" uniqKey="Kuster H" first="Helge" last="Küster">Helge Küster</name><affiliation><nlm:affiliation>Institut für Pflanzengenetik, Abt. IV - Pflanzengenomforschung, Leibniz Universität Hannover, Herrenhäuser Str. 2, D-30419, Hannover, Germany. helge.kuester@genetik.uni-hannover.de.</nlm:affiliation></affiliation></author></analytic><series><title level="j">BMC genomics</title><idno type="eISSN">1471-2164</idno><imprint><date when="2015" type="published">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Gene Expression Profiling (MeSH)</term><term>Gene Expression Regulation, Plant (drug effects)</term><term>Genome, Plant (MeSH)</term><term>Glomeromycota (physiology)</term><term>Host-Pathogen Interactions (MeSH)</term><term>Lipopolysaccharides (metabolism)</term><term>Lipopolysaccharides (pharmacology)</term><term>Medicago truncatula (genetics)</term><term>Mycorrhizae (physiology)</term><term>Plant Proteins (genetics)</term><term>Symbiosis (MeSH)</term><term>Transcription Factors (genetics)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Plant Proteins</term><term>Transcription Factors</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Lipopolysaccharides</term></keywords><keywords scheme="MESH" qualifier="drug effects" xml:lang="en"><term>Gene Expression Regulation, Plant</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Medicago truncatula</term></keywords><keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en"><term>Lipopolysaccharides</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Glomeromycota</term><term>Mycorrhizae</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Gene Expression Profiling</term><term>Genome, Plant</term><term>Host-Pathogen Interactions</term><term>Symbiosis</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p><b>BACKGROUND</b></p><p>More than 80 % of all terrestrial plant species establish an arbuscular mycorrhiza (AM) symbiosis with Glomeromycota fungi. This plant-microbe interaction primarily improves phosphate uptake, but also supports nitrogen, mineral, and water aquisition. During the pre-contact stage, the AM symbiosis is controled by an exchange of diffusible factors from either partner. Amongst others, fungal signals were identified as a mix of sulfated and non-sulfated lipochitooligosaccharides (LCOs), being structurally related to rhizobial nodulation (Nod)-factor LCOs that in legumes induce the formation of nitrogen-fixing root nodules. LCO signals are transduced via a common symbiotic signaling pathway (CSSP) that activates a group of GRAS transcription factors (TFs). Using complex gene expression fingerprints as molecular phenotypes, this study primarily intended to shed light on the importance of the GRAS TFs NSP1 and RAM1 for LCO-activated gene expression during pre-symbiotic signaling.</p></div><div type="abstract" xml:lang="en"><p><b>RESULTS</b></p><p>We investigated the genome-wide transcriptional responses in 5 days old primary roots of the Medicago truncatula wild type and four symbiotic mutants to a 6 h challenge with LCO signals supplied at 10(-7/-8) M. We were able to show that during the pre-symbiotic stage, sulfated Myc-, non-sulfated Myc-, and Nod-LCO-activated gene expression almost exclusively depends on the LysM receptor kinase NFP and is largely controled by the CSSP, although responses independent of this pathway exist. Our results show that downstream of the CSSP, gene expression activation by Myc-LCOs supplied at 10(-7/-8) M strictly required both the GRAS transcription factors RAM1 and NSP1, whereas those genes either co- or specifically activated by Nod-LCOs displayed a preferential NSP1-dependency. RAM1, a central regulator of root colonization by AM fungi, controled genes activated by non-sulfated Myc-LCOs during the pre-symbiotic stage that are also up-regulated in areas with early physical contact, e.g. hyphopodia and infecting hyphae; linking responses to externally applied LCOs with early root colonization.</p></div><div type="abstract" xml:lang="en"><p><b>CONCLUSIONS</b></p><p>Since both RAM1 and NSP1 were essential for the pre-symbiotic transcriptional reprogramming by Myc-LCOs, we propose that downstream of the CSSP, these GRAS transcription factors act synergistically in the transduction of those diffusible signals that pre-announce the presence of symbiotic fungi.</p></div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">26597293</PMID><DateCompleted><Year>2016</Year><Month>09</Month><Day>23</Day></DateCompleted><DateRevised><Year>2018</Year><Month>11</Month><Day>13</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">1471-2164</ISSN><JournalIssue CitedMedium="Internet"><Volume>16</Volume><PubDate><Year>2015</Year><Month>Nov</Month><Day>23</Day></PubDate></JournalIssue><Title>BMC genomics</Title><ISOAbbreviation>BMC Genomics</ISOAbbreviation></Journal><ArticleTitle>Pre-announcement of symbiotic guests: transcriptional reprogramming by mycorrhizal lipochitooligosaccharides shows a strict co-dependency on the GRAS transcription factors NSP1 and RAM1.</ArticleTitle><Pagination><MedlinePgn>994</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1186/s12864-015-2224-7</ELocationID><Abstract><AbstractText Label="BACKGROUND" NlmCategory="BACKGROUND">More than 80 % of all terrestrial plant species establish an arbuscular mycorrhiza (AM) symbiosis with Glomeromycota fungi. This plant-microbe interaction primarily improves phosphate uptake, but also supports nitrogen, mineral, and water aquisition. During the pre-contact stage, the AM symbiosis is controled by an exchange of diffusible factors from either partner. Amongst others, fungal signals were identified as a mix of sulfated and non-sulfated lipochitooligosaccharides (LCOs), being structurally related to rhizobial nodulation (Nod)-factor LCOs that in legumes induce the formation of nitrogen-fixing root nodules. LCO signals are transduced via a common symbiotic signaling pathway (CSSP) that activates a group of GRAS transcription factors (TFs). Using complex gene expression fingerprints as molecular phenotypes, this study primarily intended to shed light on the importance of the GRAS TFs NSP1 and RAM1 for LCO-activated gene expression during pre-symbiotic signaling.</AbstractText><AbstractText Label="RESULTS" NlmCategory="RESULTS">We investigated the genome-wide transcriptional responses in 5 days old primary roots of the Medicago truncatula wild type and four symbiotic mutants to a 6 h challenge with LCO signals supplied at 10(-7/-8) M. We were able to show that during the pre-symbiotic stage, sulfated Myc-, non-sulfated Myc-, and Nod-LCO-activated gene expression almost exclusively depends on the LysM receptor kinase NFP and is largely controled by the CSSP, although responses independent of this pathway exist. Our results show that downstream of the CSSP, gene expression activation by Myc-LCOs supplied at 10(-7/-8) M strictly required both the GRAS transcription factors RAM1 and NSP1, whereas those genes either co- or specifically activated by Nod-LCOs displayed a preferential NSP1-dependency. RAM1, a central regulator of root colonization by AM fungi, controled genes activated by non-sulfated Myc-LCOs during the pre-symbiotic stage that are also up-regulated in areas with early physical contact, e.g. hyphopodia and infecting hyphae; linking responses to externally applied LCOs with early root colonization.</AbstractText><AbstractText Label="CONCLUSIONS" NlmCategory="CONCLUSIONS">Since both RAM1 and NSP1 were essential for the pre-symbiotic transcriptional reprogramming by Myc-LCOs, we propose that downstream of the CSSP, these GRAS transcription factors act synergistically in the transduction of those diffusible signals that pre-announce the presence of symbiotic fungi.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Hohnjec</LastName><ForeName>Natalija</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Institut für Pflanzengenetik, Abt. IV - Pflanzengenomforschung, Leibniz Universität Hannover, Herrenhäuser Str. 2, D-30419, Hannover, Germany. natalija.hohnjec@genetik.uni-hannover.de.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Czaja-Hasse</LastName><ForeName>Lisa F</ForeName><Initials>LF</Initials><AffiliationInfo><Affiliation>Institut für Pflanzengenetik, Abt. IV - Pflanzengenomforschung, Leibniz Universität Hannover, Herrenhäuser Str. 2, D-30419, Hannover, Germany. czaja@mpipz.mpg.de.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Present address: Max Planck Genome Centre Cologne, Carl-von-Linné-Weg 10, D-50829, Köln, Germany. czaja@mpipz.mpg.de.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hogekamp</LastName><ForeName>Claudia</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Institut für Pflanzengenetik, Abt. IV - Pflanzengenomforschung, Leibniz Universität Hannover, Herrenhäuser Str. 2, D-30419, Hannover, Germany. claudia.hogekamp@genetik.uni-hannover.de.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Küster</LastName><ForeName>Helge</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Institut für Pflanzengenetik, Abt. IV - Pflanzengenomforschung, Leibniz Universität Hannover, Herrenhäuser Str. 2, D-30419, Hannover, Germany. helge.kuester@genetik.uni-hannover.de.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><DataBankList CompleteYN="Y"><DataBank><DataBankName>GEO</DataBankName><AccessionNumberList><AccessionNumber>GSE67167</AccessionNumber></AccessionNumberList></DataBank></DataBankList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2015</Year><Month>11</Month><Day>23</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>BMC Genomics</MedlineTA><NlmUniqueID>100965258</NlmUniqueID><ISSNLinking>1471-2164</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance 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MajorTopicYN="N">Glomeromycota</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D054884" MajorTopicYN="N">Host-Pathogen Interactions</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008070" MajorTopicYN="N">Lipopolysaccharides</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName><QualifierName UI="Q000494" MajorTopicYN="Y">pharmacology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D046913" MajorTopicYN="N">Medicago truncatula</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName><QualifierName UI="Q000235" 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