Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis

Emilie Tisserant, Mathilde Malbreil, Alan Kuo, Annegret Kohler, Aikaterini Symeonidi, Raffaella Balestrini, Philippe Charron, Nina Duensing, Nicolas Frei Dit Frey, Vivienne Gianinazzi-Pearson, Luz B. Gilbert, Yoshihiro Handa, Joshua R. Herr, Mohamed Hijri, Raman Koul, Masayoshi Kawaguchi, Franziska Krajinski, Peter Lammers, Frederic G. Masclaux, Claude MuratEmmanuelle Morin, Steve Ndikumana, Marco Pagni, Denis Petitpierre, Natalia Requena, Pawel Rosikiewicz, Rohan Riley, Katsuharu Saito, Hélène San Clemente, Harris Shapiro, Diederik Van Tuinen, Guillaume Bécard, Paola Bonfante, Uta Paszkowski, Yair Y. Shachar-Hill, Gerald A. Tuskan, Peter W. Young, Ian R. Sanders, Bernard Henrissat, Stefan A. Rensing, Igor V. Grigoriev, Nicolas Corradi, Christophe Roux, Francis Martin

Research output: Contribution to journalArticle

335 Citations (Scopus)

Abstract

The mutualistic symbiosis involving Glomeromycota, a distinctive phylum of early diverging Fungi, is widely hypothesized to have promoted the evolution of land plants during the middle Paleozoic. These arbuscular mycorrhizal fungi (AMF) perform vital functions in the phosphorus cycle that are fundamental to sustainable crop plant productivity. The unusual biological features of AMF have long fascinated evolutionary biologists. The coenocytic hyphae host a community of hundreds of nuclei and reproduce clonally through large multinucleated spores. It has been suggested that the AMF maintain a stable assemblage of several different genomes during the life cycle, but this genomic organization has been questioned. Here we introduce the 153-Mb haploid genome of Rhizophagus irregularis and its repertoire of 28,232 genes. The observed low level of genome polymorphism (0.43 SNP per kb) is not consistent with the occurrence of multiple, highly diverged genomes. The expansion of mating-related genes suggests the existence of cryptic sex-related processes. A comparison of gene categories confirms that R. irregularis is close to the Mucoromycotina. The AMF obligate biotrophy is not explained by genome erosion or any related loss of metabolic complexity in central metabolism, but is marked by a lack of genes encoding plant cell wall-degrading enzymes and of genes involved in toxin and thiamine synthesis. A battery of mycorrhiza-induced secreted proteins is expressed in symbiotic tissues. The present comprehensive repertoire of R. irregularis genes provides a basis for future research on symbiosis-related mechanisms in Glomeromycota.

Original languageEnglish (US)
Pages (from-to)20117-20122
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume110
Issue number50
DOIs
StatePublished - Dec 10 2013
Externally publishedYes

Fingerprint

symbiosis
mycorrhizal fungi
genome
Glomeromycota
genes
Mucoromycotina
embryophytes
thiamin
mycorrhizae
haploidy
hyphae
biologists
life cycle (organisms)
toxins
spores
cell walls
genetic polymorphism
genomics
phosphorus
fungi

Keywords

  • Carbohydrate-active enzymes
  • Effector
  • Fungal evolution
  • Glomales
  • Mutualism

ASJC Scopus subject areas

  • General

Cite this

Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. / Tisserant, Emilie; Malbreil, Mathilde; Kuo, Alan; Kohler, Annegret; Symeonidi, Aikaterini; Balestrini, Raffaella; Charron, Philippe; Duensing, Nina; Frei Dit Frey, Nicolas; Gianinazzi-Pearson, Vivienne; Gilbert, Luz B.; Handa, Yoshihiro; Herr, Joshua R.; Hijri, Mohamed; Koul, Raman; Kawaguchi, Masayoshi; Krajinski, Franziska; Lammers, Peter; Masclaux, Frederic G.; Murat, Claude; Morin, Emmanuelle; Ndikumana, Steve; Pagni, Marco; Petitpierre, Denis; Requena, Natalia; Rosikiewicz, Pawel; Riley, Rohan; Saito, Katsuharu; San Clemente, Hélène; Shapiro, Harris; Van Tuinen, Diederik; Bécard, Guillaume; Bonfante, Paola; Paszkowski, Uta; Shachar-Hill, Yair Y.; Tuskan, Gerald A.; Young, Peter W.; Sanders, Ian R.; Henrissat, Bernard; Rensing, Stefan A.; Grigoriev, Igor V.; Corradi, Nicolas; Roux, Christophe; Martin, Francis.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 110, No. 50, 10.12.2013, p. 20117-20122.

Research output: Contribution to journalArticle

Tisserant, E, Malbreil, M, Kuo, A, Kohler, A, Symeonidi, A, Balestrini, R, Charron, P, Duensing, N, Frei Dit Frey, N, Gianinazzi-Pearson, V, Gilbert, LB, Handa, Y, Herr, JR, Hijri, M, Koul, R, Kawaguchi, M, Krajinski, F, Lammers, P, Masclaux, FG, Murat, C, Morin, E, Ndikumana, S, Pagni, M, Petitpierre, D, Requena, N, Rosikiewicz, P, Riley, R, Saito, K, San Clemente, H, Shapiro, H, Van Tuinen, D, Bécard, G, Bonfante, P, Paszkowski, U, Shachar-Hill, YY, Tuskan, GA, Young, PW, Sanders, IR, Henrissat, B, Rensing, SA, Grigoriev, IV, Corradi, N, Roux, C & Martin, F 2013, 'Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis', Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 50, pp. 20117-20122. https://doi.org/10.1073/pnas.1313452110
Tisserant, Emilie ; Malbreil, Mathilde ; Kuo, Alan ; Kohler, Annegret ; Symeonidi, Aikaterini ; Balestrini, Raffaella ; Charron, Philippe ; Duensing, Nina ; Frei Dit Frey, Nicolas ; Gianinazzi-Pearson, Vivienne ; Gilbert, Luz B. ; Handa, Yoshihiro ; Herr, Joshua R. ; Hijri, Mohamed ; Koul, Raman ; Kawaguchi, Masayoshi ; Krajinski, Franziska ; Lammers, Peter ; Masclaux, Frederic G. ; Murat, Claude ; Morin, Emmanuelle ; Ndikumana, Steve ; Pagni, Marco ; Petitpierre, Denis ; Requena, Natalia ; Rosikiewicz, Pawel ; Riley, Rohan ; Saito, Katsuharu ; San Clemente, Hélène ; Shapiro, Harris ; Van Tuinen, Diederik ; Bécard, Guillaume ; Bonfante, Paola ; Paszkowski, Uta ; Shachar-Hill, Yair Y. ; Tuskan, Gerald A. ; Young, Peter W. ; Sanders, Ian R. ; Henrissat, Bernard ; Rensing, Stefan A. ; Grigoriev, Igor V. ; Corradi, Nicolas ; Roux, Christophe ; Martin, Francis. / Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. In: Proceedings of the National Academy of Sciences of the United States of America. 2013 ; Vol. 110, No. 50. pp. 20117-20122.
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abstract = "The mutualistic symbiosis involving Glomeromycota, a distinctive phylum of early diverging Fungi, is widely hypothesized to have promoted the evolution of land plants during the middle Paleozoic. These arbuscular mycorrhizal fungi (AMF) perform vital functions in the phosphorus cycle that are fundamental to sustainable crop plant productivity. The unusual biological features of AMF have long fascinated evolutionary biologists. The coenocytic hyphae host a community of hundreds of nuclei and reproduce clonally through large multinucleated spores. It has been suggested that the AMF maintain a stable assemblage of several different genomes during the life cycle, but this genomic organization has been questioned. Here we introduce the 153-Mb haploid genome of Rhizophagus irregularis and its repertoire of 28,232 genes. The observed low level of genome polymorphism (0.43 SNP per kb) is not consistent with the occurrence of multiple, highly diverged genomes. The expansion of mating-related genes suggests the existence of cryptic sex-related processes. A comparison of gene categories confirms that R. irregularis is close to the Mucoromycotina. The AMF obligate biotrophy is not explained by genome erosion or any related loss of metabolic complexity in central metabolism, but is marked by a lack of genes encoding plant cell wall-degrading enzymes and of genes involved in toxin and thiamine synthesis. A battery of mycorrhiza-induced secreted proteins is expressed in symbiotic tissues. The present comprehensive repertoire of R. irregularis genes provides a basis for future research on symbiosis-related mechanisms in Glomeromycota.",
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AU - Balestrini, Raffaella

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AU - Duensing, Nina

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AU - Masclaux, Frederic G.

AU - Murat, Claude

AU - Morin, Emmanuelle

AU - Ndikumana, Steve

AU - Pagni, Marco

AU - Petitpierre, Denis

AU - Requena, Natalia

AU - Rosikiewicz, Pawel

AU - Riley, Rohan

AU - Saito, Katsuharu

AU - San Clemente, Hélène

AU - Shapiro, Harris

AU - Van Tuinen, Diederik

AU - Bécard, Guillaume

AU - Bonfante, Paola

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AU - Sanders, Ian R.

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