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

Emilie Tisserant 1 Mathilde Malbreil 2 Alan Kuo 3 Annegret Kohler 1 Aikaterini Symeonidi 4, 5 Raffaella Balestrini 6 Philippe Charron 7 Nina Duensing 8 Nicolas Frei Dit Frey 2 Vivienne Gianinazzi-Pearson 9 Luz B. Gilbert 2 Yoshihiro Handa 10 Joshua R. Herr 1 Mohamed Hijri 11 Raman Koul 12 Masayoshi Kawaguchi 10 Franziska Krajinski 8 Peter J. Lammers 12 Frederic G. Masclaux 13, 14 Claude Murat 1 Emmanuelle Morin 1 Steve Ndikumana 7 Marco Pagni 13 Denis Petitpierre 1 Natalia Requena 15 Pawel Rosikiewicz 13 Rohan Riley 7 Katsuharu Saito 16 Helene San Clemente 2 Harris Shapiro 3 Diederik van Tuinen 9 Guillaume Bécard 2 Paola Bonfante 6 Uta Paszkowski 17 Yair Y. Shachar-Hill 18 Gerald A. Tuskan 19 J. Peter W. Young 20 Ian R. Sanders 13 Bernard Henrissat 21, 22 Stefan A. Rensing 4, 5 Igor V. Grigoriev 3 Nicolas Corradi 7 Christophe Roux 2 Francis Martin 1, *
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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Emilie Tisserant, Mathilde Malbreil, Alan Kuo, Annegret Kohler, Aikaterini Symeonidi, et al.. 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 , National Academy of Sciences, 2013, 110 (50), pp.20117-20122. ⟨10.1073/pnas.1313452110⟩. ⟨hal-01578663⟩



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