Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential.
Identifieur interne : 000F69 ( Main/Exploration ); précédent : 000F68; suivant : 000F70Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential.
Auteurs : Alessandra Salvioli [Italie] ; Stefano Ghignone [Italie] ; Mara Novero [Italie] ; Lorella Navazio [Italie] ; Francesco Venice [Italie] ; Paolo Bagnaresi [Italie] ; Paola Bonfante [Italie]Source :
- The ISME journal [ 1751-7370 ] ; 2016.
Descripteurs français
- KwdFr :
- MESH :
- génétique : Burkholderiaceae, Glomeromycota, Mycorhizes.
- physiologie : Burkholderiaceae, Glomeromycota, Mycorhizes.
- Métabolisme énergétique, Symbiose, Voies et réseaux métaboliques.
English descriptors
- KwdEn :
- MESH :
- genetics : Burkholderiaceae, Glomeromycota, Mycorrhizae.
- physiology : Burkholderiaceae, Glomeromycota, Mycorrhizae.
- Energy Metabolism, Metabolic Networks and Pathways, Symbiosis.
Abstract
Arbuscular mycorrhizal fungi (AMF) occur in the rhizosphere and in plant tissues as obligate symbionts, having key roles in plant evolution and nutrition. AMF possess endobacteria, and genome sequencing of the endobacterium Candidatus Glomeribacter gigasporarum revealed a reduced genome and a dependence on the fungal host. To understand the effect of bacteria on fungal fitness, we used next-generation sequencing to analyse the transcriptional profile of Gigaspora margarita in the presence and in the absence of its endobacterium. Genomic data on AMF are limited; therefore, we first generated a gene catalogue for G. margarita. Transcriptome analysis revealed that the endobacterium has a stronger effect on the pre-symbiotic phase of the fungus. Coupling transcriptomics with cell biology and physiological approaches, we demonstrate that the bacterium increases the fungal sporulation success, raises the fungal bioenergetic capacity, increasing ATP production, and eliciting mechanisms to detoxify reactive oxygen species. By using TAT peptide to translocate the bioluminescent calcium reporter aequorin, we demonstrated that the line with endobacteria had a lower basal intracellular calcium concentration than the cured line. Lastly, the bacteria seem to enhance the fungal responsiveness to strigolactones, the plant molecules that AMF perceive as branching factors. Although the endobacterium exacts a nutritional cost on the AMF, endobacterial symbiosis improves the fungal ecological fitness by priming mitochondrial metabolic pathways and giving the AMF more tools to face environmental stresses. Thus, we hypothesise that, as described for the human microbiota, endobacteria may increase AMF innate immunity.
DOI: 10.1038/ismej.2015.91
PubMed: 26046255
PubMed Central: PMC4681866
Affiliations:
Links toward previous steps (curation, corpus...)
Le document en format XML
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type="published">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Burkholderiaceae (genetics)</term><term>Burkholderiaceae (physiology)</term><term>Energy Metabolism (MeSH)</term><term>Glomeromycota (genetics)</term><term>Glomeromycota (physiology)</term><term>Metabolic Networks and Pathways (MeSH)</term><term>Mycorrhizae (genetics)</term><term>Mycorrhizae (physiology)</term><term>Symbiosis (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Burkholderiaceae (génétique)</term><term>Burkholderiaceae (physiologie)</term><term>Glomeromycota (génétique)</term><term>Glomeromycota (physiologie)</term><term>Mycorhizes (génétique)</term><term>Mycorhizes (physiologie)</term><term>Métabolisme énergétique (MeSH)</term><term>Symbiose (MeSH)</term><term>Voies et réseaux métaboliques (MeSH)</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Burkholderiaceae</term><term>Glomeromycota</term><term>Mycorrhizae</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Burkholderiaceae</term><term>Glomeromycota</term><term>Mycorhizes</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Burkholderiaceae</term><term>Glomeromycota</term><term>Mycorhizes</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Burkholderiaceae</term><term>Glomeromycota</term><term>Mycorrhizae</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Energy Metabolism</term><term>Metabolic Networks and Pathways</term><term>Symbiosis</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Métabolisme énergétique</term><term>Symbiose</term><term>Voies et réseaux métaboliques</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Arbuscular mycorrhizal fungi (AMF) occur in the rhizosphere and in plant tissues as obligate symbionts, having key roles in plant evolution and nutrition. AMF possess endobacteria, and genome sequencing of the endobacterium Candidatus Glomeribacter gigasporarum revealed a reduced genome and a dependence on the fungal host. To understand the effect of bacteria on fungal fitness, we used next-generation sequencing to analyse the transcriptional profile of Gigaspora margarita in the presence and in the absence of its endobacterium. Genomic data on AMF are limited; therefore, we first generated a gene catalogue for G. margarita. Transcriptome analysis revealed that the endobacterium has a stronger effect on the pre-symbiotic phase of the fungus. Coupling transcriptomics with cell biology and physiological approaches, we demonstrate that the bacterium increases the fungal sporulation success, raises the fungal bioenergetic capacity, increasing ATP production, and eliciting mechanisms to detoxify reactive oxygen species. By using TAT peptide to translocate the bioluminescent calcium reporter aequorin, we demonstrated that the line with endobacteria had a lower basal intracellular calcium concentration than the cured line. Lastly, the bacteria seem to enhance the fungal responsiveness to strigolactones, the plant molecules that AMF perceive as branching factors. Although the endobacterium exacts a nutritional cost on the AMF, endobacterial symbiosis improves the fungal ecological fitness by priming mitochondrial metabolic pathways and giving the AMF more tools to face environmental stresses. Thus, we hypothesise that, as described for the human microbiota, endobacteria may increase AMF innate immunity. </div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" IndexingMethod="Curated" Owner="NLM"><PMID Version="1">26046255</PMID><DateCompleted><Year>2016</Year><Month>08</Month><Day>15</Day></DateCompleted><DateRevised><Year>2018</Year><Month>12</Month><Day>02</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1751-7370</ISSN><JournalIssue CitedMedium="Internet"><Volume>10</Volume><Issue>1</Issue><PubDate><Year>2016</Year><Month>Jan</Month></PubDate></JournalIssue><Title>The ISME journal</Title><ISOAbbreviation>ISME J</ISOAbbreviation></Journal><ArticleTitle>Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential.</ArticleTitle><Pagination><MedlinePgn>130-44</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1038/ismej.2015.91</ELocationID><Abstract><AbstractText>Arbuscular mycorrhizal fungi (AMF) occur in the rhizosphere and in plant tissues as obligate symbionts, having key roles in plant evolution and nutrition. AMF possess endobacteria, and genome sequencing of the endobacterium Candidatus Glomeribacter gigasporarum revealed a reduced genome and a dependence on the fungal host. To understand the effect of bacteria on fungal fitness, we used next-generation sequencing to analyse the transcriptional profile of Gigaspora margarita in the presence and in the absence of its endobacterium. Genomic data on AMF are limited; therefore, we first generated a gene catalogue for G. margarita. Transcriptome analysis revealed that the endobacterium has a stronger effect on the pre-symbiotic phase of the fungus. Coupling transcriptomics with cell biology and physiological approaches, we demonstrate that the bacterium increases the fungal sporulation success, raises the fungal bioenergetic capacity, increasing ATP production, and eliciting mechanisms to detoxify reactive oxygen species. By using TAT peptide to translocate the bioluminescent calcium reporter aequorin, we demonstrated that the line with endobacteria had a lower basal intracellular calcium concentration than the cured line. Lastly, the bacteria seem to enhance the fungal responsiveness to strigolactones, the plant molecules that AMF perceive as branching factors. Although the endobacterium exacts a nutritional cost on the AMF, endobacterial symbiosis improves the fungal ecological fitness by priming mitochondrial metabolic pathways and giving the AMF more tools to face environmental stresses. Thus, we hypothesise that, as described for the human microbiota, endobacteria may increase AMF innate immunity. </AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Salvioli</LastName><ForeName>Alessandra</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Life Science and Systems Biology, University of Torino, Torino, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ghignone</LastName><ForeName>Stefano</ForeName><Initials>S</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-2033-2286</Identifier><AffiliationInfo><Affiliation>Institute for Sustainable Plant Protection (IPSP) - CNR, Torino, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Novero</LastName><ForeName>Mara</ForeName><Initials>M</Initials><Identifier Source="ORCID">http://orcid.org/0000-0001-7412-8750</Identifier><AffiliationInfo><Affiliation>Department of Life Science and Systems Biology, University of Torino, Torino, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Navazio</LastName><ForeName>Lorella</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Department of Biology, University of Padova, Padova, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Venice</LastName><ForeName>Francesco</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Department of Life Science and Systems Biology, University of Torino, Torino, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bagnaresi</LastName><ForeName>Paolo</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Research Center for Genomics and Postgenomics, CRA-Fiorenzuola d'Arda, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bonfante</LastName><ForeName>Paola</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Department of Life Science and Systems Biology, University of Torino, Torino, Italy.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><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>06</Month><Day>05</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>ISME J</MedlineTA><NlmUniqueID>101301086</NlmUniqueID><ISSNLinking>1751-7362</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D042521" MajorTopicYN="N">Burkholderiaceae</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D004734" MajorTopicYN="N">Energy Metabolism</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D055137" MajorTopicYN="N">Glomeromycota</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D053858" MajorTopicYN="N">Metabolic Networks and Pathways</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D013559" MajorTopicYN="N">Symbiosis</DescriptorName></MeshHeading></MeshHeadingList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2014</Year><Month>12</Month><Day>19</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2015</Year><Month>03</Month><Day>27</Day></PubMedPubDate><PubMedPubDate 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sortKey="Salvioli, Alessandra" sort="Salvioli, Alessandra" uniqKey="Salvioli A" first="Alessandra" last="Salvioli">Alessandra Salvioli</name></region><name sortKey="Bagnaresi, Paolo" sort="Bagnaresi, Paolo" uniqKey="Bagnaresi P" first="Paolo" last="Bagnaresi">Paolo Bagnaresi</name><name sortKey="Bonfante, Paola" sort="Bonfante, Paola" uniqKey="Bonfante P" first="Paola" last="Bonfante">Paola Bonfante</name><name sortKey="Ghignone, Stefano" sort="Ghignone, Stefano" uniqKey="Ghignone S" first="Stefano" last="Ghignone">Stefano Ghignone</name><name sortKey="Navazio, Lorella" sort="Navazio, Lorella" uniqKey="Navazio L" first="Lorella" last="Navazio">Lorella Navazio</name><name sortKey="Novero, Mara" sort="Novero, Mara" uniqKey="Novero M" first="Mara" last="Novero">Mara Novero</name><name sortKey="Venice, Francesco" sort="Venice, Francesco" uniqKey="Venice F" first="Francesco" last="Venice">Francesco Venice</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix 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