Publication

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

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 Murat, Emmanuelle 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. Shach ar-Hill,Gerald A. Tuskan,Peter W. Young,Ian R. Sanders,Bernard Henrissat,Stefan A. Rensing,Igor V. Grigoriev,Nicolas Corradi,Christophe Roux,Francis Martin 2013 November 25 PNAS 2013, doi: 10.1073/pnas.1313452110

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.

Highlights

Significance
The arbuscular mycorrhizal symbiosis between fungi of the Glomeromycota phylum and plants involves more than two thirds of all known plant species, including important crop species.
This mutualistic symbiosis, involving one of the oldest fungal lineages, is arguably the most ecologically and agriculturally important symbiosis in terrestrial ecosystems. The Glomeromycota
are unique in that their spores and coenocytic hyphae contain hundreds of nuclei in a common cytoplasm, which raises important questions about the natural selection, population genetics,
and gene expression of these highly unusual organisms. Study of the genome of Rhizophagus irregularis provides insight into genes involved in obligate biotrophy and mycorrhizal symbioses
and the evolution of an ancient asexual organism, and thus is of fundamental importance to the field of genome evolution.

Citation

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 Murat, Emmanuelle 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, and Francis Martin Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis PNAS 2013 : 1313452110v1-201313452.


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