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Genetic variation and evolutionary history of a mycorrhizal fungus regulate the currency of exchange in symbiosis with the food security crop cassava.

Identifieur interne : 000153 ( Main/Exploration ); précédent : 000152; suivant : 000154

Genetic variation and evolutionary history of a mycorrhizal fungus regulate the currency of exchange in symbiosis with the food security crop cassava.

Auteurs : Romain Savary [Suisse] ; Cindy Dupuis [Suisse] ; Frédéric G. Masclaux [Suisse] ; Ivan D. Mateus [Suisse] ; Edward C. Rojas [Suisse, Danemark] ; Ian R. Sanders [Suisse]

Source :

RBID : pubmed:32066875

Descripteurs français

English descriptors

Abstract

Most land plants form symbioses with arbuscular mycorrhizal fungi (AMF). Diversity of AMF increases plant community productivity and plant diversity. For decades, it was known that plants trade carbohydrates for phosphate with their fungal symbionts. However, recent studies show that plant-derived lipids probably represent the most essential currency of exchange. Understanding the regulation of plant genes involved in the currency of exchange is crucial to understanding stability of this mutualism. Plants encounter many different AMF genotypes that vary greatly in the benefit they confer to plants. Yet the role that fungal genetic variation plays in the regulation of this currency has not received much attention. We used a high-resolution phylogeny of one AMF species (Rhizophagus irregularis) to show that fungal genetic variation drives the regulation of the plant fatty acid pathway in cassava (Manihot esculenta); a pathway regulating one of the essential currencies of trade in the symbiosis. The regulation of this pathway was explained by clearly defined patterns of fungal genome-wide variation representing the precise fungal evolutionary history. This represents the first demonstrated link between the genetics of AMF and reprogramming of an essential plant pathway regulating the currency of exchange in the symbiosis. The transcription factor RAM1 was also revealed as the dominant gene in the fatty acid plant gene co-expression network. Our study highlights the crucial role of variation in fungal genomes in the trade of resources in this important symbiosis and also opens the door to discovering characteristics of AMF genomes responsible for interactions between AMF and cassava that will lead to optimal cassava growth.

DOI: 10.1038/s41396-020-0606-6
PubMed: 32066875
PubMed Central: PMC7242447


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Le document en format XML

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<term>Fungi (genetics)</term>
<term>Fungi (isolation & purification)</term>
<term>Fungi (physiology)</term>
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<term>Genome, Fungal (MeSH)</term>
<term>Manihot (microbiology)</term>
<term>Manihot (physiology)</term>
<term>Mycorrhizae (classification)</term>
<term>Mycorrhizae (genetics)</term>
<term>Mycorrhizae (isolation & purification)</term>
<term>Mycorrhizae (physiology)</term>
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<term>Plant Roots (physiology)</term>
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<term>Champignons (génétique)</term>
<term>Champignons (isolement et purification)</term>
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<term>Mycorhizes (génétique)</term>
<term>Mycorhizes (isolement et purification)</term>
<term>Mycorhizes (physiologie)</term>
<term>Phylogenèse (MeSH)</term>
<term>Racines de plante (microbiologie)</term>
<term>Racines de plante (physiologie)</term>
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<term>Variation génétique (MeSH)</term>
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<term>Mycorrhizae</term>
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<term>Fungi</term>
<term>Mycorrhizae</term>
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<term>Mycorhizes</term>
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<term>Racines de plante</term>
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<term>Mycorhizes</term>
<term>Racines de plante</term>
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<div type="abstract" xml:lang="en">Most land plants form symbioses with arbuscular mycorrhizal fungi (AMF). Diversity of AMF increases plant community productivity and plant diversity. For decades, it was known that plants trade carbohydrates for phosphate with their fungal symbionts. However, recent studies show that plant-derived lipids probably represent the most essential currency of exchange. Understanding the regulation of plant genes involved in the currency of exchange is crucial to understanding stability of this mutualism. Plants encounter many different AMF genotypes that vary greatly in the benefit they confer to plants. Yet the role that fungal genetic variation plays in the regulation of this currency has not received much attention. We used a high-resolution phylogeny of one AMF species (Rhizophagus irregularis) to show that fungal genetic variation drives the regulation of the plant fatty acid pathway in cassava (Manihot esculenta); a pathway regulating one of the essential currencies of trade in the symbiosis. The regulation of this pathway was explained by clearly defined patterns of fungal genome-wide variation representing the precise fungal evolutionary history. This represents the first demonstrated link between the genetics of AMF and reprogramming of an essential plant pathway regulating the currency of exchange in the symbiosis. The transcription factor RAM1 was also revealed as the dominant gene in the fatty acid plant gene co-expression network. Our study highlights the crucial role of variation in fungal genomes in the trade of resources in this important symbiosis and also opens the door to discovering characteristics of AMF genomes responsible for interactions between AMF and cassava that will lead to optimal cassava growth.</div>
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<MeshHeading>
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</MeshHeading>
<MeshHeading>
<DescriptorName UI="D005658" MajorTopicYN="N">Fungi</DescriptorName>
<QualifierName UI="Q000145" MajorTopicYN="N">classification</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
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</MeshHeading>
<MeshHeading>
<DescriptorName UI="D014644" MajorTopicYN="Y">Genetic Variation</DescriptorName>
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<DescriptorName UI="D016681" MajorTopicYN="N">Genome, Fungal</DescriptorName>
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<DescriptorName UI="D002365" MajorTopicYN="N">Manihot</DescriptorName>
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</MeshHeading>
<MeshHeading>
<DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName>
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<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000302" MajorTopicYN="N">isolation & purification</QualifierName>
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<DescriptorName UI="D018517" MajorTopicYN="N">Plant Roots</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D013559" MajorTopicYN="Y">Symbiosis</DescriptorName>
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<PubMedPubDate PubStatus="accepted">
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<Month>01</Month>
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<Month>01</Month>
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<PubMedPubDate PubStatus="entrez">
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<ArticleId IdType="doi">10.1038/s41396-020-0606-6</ArticleId>
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<country>
<li>Danemark</li>
<li>Suisse</li>
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<li>Canton de Vaud</li>
<li>Hovedstaden</li>
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<name sortKey="Savary, Romain" sort="Savary, Romain" uniqKey="Savary R" first="Romain" last="Savary">Romain Savary</name>
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<name sortKey="Dupuis, Cindy" sort="Dupuis, Cindy" uniqKey="Dupuis C" first="Cindy" last="Dupuis">Cindy Dupuis</name>
<name sortKey="Masclaux, Frederic G" sort="Masclaux, Frederic G" uniqKey="Masclaux F" first="Frédéric G" last="Masclaux">Frédéric G. Masclaux</name>
<name sortKey="Masclaux, Frederic G" sort="Masclaux, Frederic G" uniqKey="Masclaux F" first="Frédéric G" last="Masclaux">Frédéric G. Masclaux</name>
<name sortKey="Mateus, Ivan D" sort="Mateus, Ivan D" uniqKey="Mateus I" first="Ivan D" last="Mateus">Ivan D. Mateus</name>
<name sortKey="Rojas, Edward C" sort="Rojas, Edward C" uniqKey="Rojas E" first="Edward C" last="Rojas">Edward C. Rojas</name>
<name sortKey="Sanders, Ian R" sort="Sanders, Ian R" uniqKey="Sanders I" first="Ian R" last="Sanders">Ian R. Sanders</name>
<name sortKey="Savary, Romain" sort="Savary, Romain" uniqKey="Savary R" first="Romain" last="Savary">Romain Savary</name>
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<country name="Danemark">
<region name="Hovedstaden">
<name sortKey="Rojas, Edward C" sort="Rojas, Edward C" uniqKey="Rojas E" first="Edward C" last="Rojas">Edward C. Rojas</name>
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</record>

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