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Arbuscular cell invasion coincides with extracellular vesicles and membrane tubules.

Identifieur interne : 000662 ( Main/Exploration ); précédent : 000661; suivant : 000663

Arbuscular cell invasion coincides with extracellular vesicles and membrane tubules.

Auteurs : Ronelle Roth [Royaume-Uni] ; Stefan Hillmer [Allemagne] ; Charlotta Funaya [Allemagne] ; Marco Chiapello [Royaume-Uni] ; Karin Schumacher [Allemagne] ; Libera Lo Presti [Allemagne] ; Regine Kahmann [Allemagne] ; Uta Paszkowski [Royaume-Uni]

Source :

RBID : pubmed:30737514

Descripteurs français

English descriptors

Abstract

During establishment of arbuscular mycorrhizal symbioses, fungal hyphae invade root cells producing transient tree-like structures, the arbuscules, where exchange of photosynthates for soil minerals occurs. Arbuscule formation and collapse lead to rapid production and degradation of plant and fungal membranes, their spatiotemporal dynamics directly influencing nutrient exchange. We determined the ultra-structural details of both membrane surfaces and the interstitial apoplastic matrix by transmission electron microscopy tomography during growth and senescence of Rhizophagus irregularis arbuscules in rice. Invasive growth of arbuscular hyphae was associated with abundant fungal membrane tubules (memtubs) and plant peri-arbuscular membrane evaginations. Similarly, the phylogenetically distant arbuscular mycorrhizal fungus, Gigaspora rosea, and the fungal maize pathogen, Ustilago maydis, developed memtubs while invading host cells, revealing structural commonalities independent of the mutualistic or parasitic outcome of the interaction. Additionally, extracellular vesicles formed continuously in the peri-arbuscular interface from arbuscule biogenesis to senescence, suggesting an involvement in inter-organismic signal and nutrient exchange throughout the arbuscule lifespan.

DOI: 10.1038/s41477-019-0365-4
PubMed: 30737514


Affiliations:


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Le document en format XML

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<term>Electron Microscope Tomography (MeSH)</term>
<term>Extracellular Vesicles (metabolism)</term>
<term>Glomeromycota (physiology)</term>
<term>Hyphae (physiology)</term>
<term>Mycorrhizae (cytology)</term>
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<term>Plant Cells</term>
<term>Plant Leaves</term>
<term>Plant Roots</term>
<term>Zea mays</term>
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<term>Ustilago</term>
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<div type="abstract" xml:lang="en">During establishment of arbuscular mycorrhizal symbioses, fungal hyphae invade root cells producing transient tree-like structures, the arbuscules, where exchange of photosynthates for soil minerals occurs. Arbuscule formation and collapse lead to rapid production and degradation of plant and fungal membranes, their spatiotemporal dynamics directly influencing nutrient exchange. We determined the ultra-structural details of both membrane surfaces and the interstitial apoplastic matrix by transmission electron microscopy tomography during growth and senescence of Rhizophagus irregularis arbuscules in rice. Invasive growth of arbuscular hyphae was associated with abundant fungal membrane tubules (memtubs) and plant peri-arbuscular membrane evaginations. Similarly, the phylogenetically distant arbuscular mycorrhizal fungus, Gigaspora rosea, and the fungal maize pathogen, Ustilago maydis, developed memtubs while invading host cells, revealing structural commonalities independent of the mutualistic or parasitic outcome of the interaction. Additionally, extracellular vesicles formed continuously in the peri-arbuscular interface from arbuscule biogenesis to senescence, suggesting an involvement in inter-organismic signal and nutrient exchange throughout the arbuscule lifespan.</div>
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<ForeName>Regine</ForeName>
<Initials>R</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-7779-7837</Identifier>
<AffiliationInfo>
<Affiliation>Max-Planck Institute for Terrestrial Microbiology, Marburg, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Paszkowski</LastName>
<ForeName>Uta</ForeName>
<Initials>U</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-7279-7632</Identifier>
<AffiliationInfo>
<Affiliation>Department of Plant Sciences, University of Cambridge, Cambridge, UK. up220@cam.ac.uk.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<GrantList CompleteYN="Y">
<Grant>
<GrantID>BB/N008723/1</GrantID>
<Acronym>BB_</Acronym>
<Agency>Biotechnology and Biological Sciences Research Council</Agency>
<Country>United Kingdom</Country>
</Grant>
</GrantList>
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<PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
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<ArticleDate DateType="Electronic">
<Year>2019</Year>
<Month>02</Month>
<Day>08</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>England</Country>
<MedlineTA>Nat Plants</MedlineTA>
<NlmUniqueID>101651677</NlmUniqueID>
<ISSNLinking>2055-0278</ISSNLinking>
</MedlineJournalInfo>
<CitationSubset>IM</CitationSubset>
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<CommentsCorrections RefType="CommentIn">
<RefSource>Nat Plants. 2019 Feb;5(2):131-132</RefSource>
<PMID Version="1">30737510</PMID>
</CommentsCorrections>
</CommentsCorrectionsList>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D002462" MajorTopicYN="N">Cell Membrane</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
<QualifierName UI="Q000648" MajorTopicYN="Y">ultrastructure</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D055032" MajorTopicYN="N">Electron Microscope Tomography</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D000067128" MajorTopicYN="N">Extracellular Vesicles</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D055137" MajorTopicYN="N">Glomeromycota</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D025301" MajorTopicYN="N">Hyphae</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName>
<QualifierName UI="Q000166" MajorTopicYN="N">cytology</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D012275" MajorTopicYN="N">Oryza</DescriptorName>
<QualifierName UI="Q000166" MajorTopicYN="N">cytology</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D059828" MajorTopicYN="N">Plant Cells</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018515" MajorTopicYN="N">Plant Leaves</DescriptorName>
<QualifierName UI="Q000166" MajorTopicYN="N">cytology</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
<QualifierName UI="Q000648" MajorTopicYN="N">ultrastructure</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018517" MajorTopicYN="N">Plant Roots</DescriptorName>
<QualifierName UI="Q000166" MajorTopicYN="N">cytology</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
<QualifierName UI="Q000648" MajorTopicYN="N">ultrastructure</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D030821" MajorTopicYN="N">Plants, Genetically Modified</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013559" MajorTopicYN="N">Symbiosis</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D014588" MajorTopicYN="N">Ustilago</DescriptorName>
<QualifierName UI="Q000472" MajorTopicYN="N">pathogenicity</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D003313" MajorTopicYN="N">Zea mays</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
</MeshHeadingList>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="received">
<Year>2018</Year>
<Month>08</Month>
<Day>15</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2019</Year>
<Month>01</Month>
<Day>08</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2019</Year>
<Month>2</Month>
<Day>10</Day>
<Hour>6</Hour>
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<Year>2019</Year>
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<Day>10</Day>
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<Minute>0</Minute>
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<PubMedPubDate PubStatus="medline">
<Year>2019</Year>
<Month>7</Month>
<Day>2</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
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<ArticleId IdType="pubmed">30737514</ArticleId>
<ArticleId IdType="doi">10.1038/s41477-019-0365-4</ArticleId>
<ArticleId IdType="pii">10.1038/s41477-019-0365-4</ArticleId>
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</PubmedData>
</pubmed>
<affiliations>
<list>
<country>
<li>Allemagne</li>
<li>Royaume-Uni</li>
</country>
<region>
<li>Angleterre</li>
<li>Angleterre de l'Est</li>
<li>Bade-Wurtemberg</li>
<li>Berlin</li>
<li>District de Giessen</li>
<li>District de Karlsruhe</li>
<li>Hesse (Land)</li>
</region>
<settlement>
<li>Berlin</li>
<li>Cambridge</li>
<li>Heidelberg</li>
<li>Marbourg</li>
</settlement>
<orgName>
<li>Université de Cambridge</li>
</orgName>
</list>
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<country name="Royaume-Uni">
<region name="Angleterre">
<name sortKey="Roth, Ronelle" sort="Roth, Ronelle" uniqKey="Roth R" first="Ronelle" last="Roth">Ronelle Roth</name>
</region>
<name sortKey="Chiapello, Marco" sort="Chiapello, Marco" uniqKey="Chiapello M" first="Marco" last="Chiapello">Marco Chiapello</name>
<name sortKey="Paszkowski, Uta" sort="Paszkowski, Uta" uniqKey="Paszkowski U" first="Uta" last="Paszkowski">Uta Paszkowski</name>
</country>
<country name="Allemagne">
<region name="Bade-Wurtemberg">
<name sortKey="Hillmer, Stefan" sort="Hillmer, Stefan" uniqKey="Hillmer S" first="Stefan" last="Hillmer">Stefan Hillmer</name>
</region>
<name sortKey="Funaya, Charlotta" sort="Funaya, Charlotta" uniqKey="Funaya C" first="Charlotta" last="Funaya">Charlotta Funaya</name>
<name sortKey="Kahmann, Regine" sort="Kahmann, Regine" uniqKey="Kahmann R" first="Regine" last="Kahmann">Regine Kahmann</name>
<name sortKey="Lo Presti, Libera" sort="Lo Presti, Libera" uniqKey="Lo Presti L" first="Libera" last="Lo Presti">Libera Lo Presti</name>
<name sortKey="Lo Presti, Libera" sort="Lo Presti, Libera" uniqKey="Lo Presti L" first="Libera" last="Lo Presti">Libera Lo Presti</name>
<name sortKey="Schumacher, Karin" sort="Schumacher, Karin" uniqKey="Schumacher K" first="Karin" last="Schumacher">Karin Schumacher</name>
</country>
</tree>
</affiliations>
</record>

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