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 J. 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

352 Scopus citations

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

    Fingerprint

Keywords

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

ASJC Scopus subject areas

  • General

Cite this

Tisserant, E., Malbreil, M., Kuo, A., Kohler, A., Symeonidi, A., Balestrini, R., Charron, P., Duensing, N., Frei Dit Frey, N., Gianinazzi-Pearson, V., Gilbert, L. B., Handa, Y., Herr, J. R., Hijri, M., Koul, R., Kawaguchi, M., Krajinski, F., Lammers, P. J., Masclaux, F. G., ... 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, 110(50), 20117-20122. https://doi.org/10.1073/pnas.1313452110