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Amanite tue-mouches (Amanita muscaria) est rès commune. Elle est fortement toxique (troubles digestifs et effets hallucinatoires) mais non mortelle.. © INRA, BOSSENNEC Jean-Marie

Unearthing the Roots of Fungal Symbioses

To understand the bases of mutualistic symbiosis between soil mycorrhizal fungi and plants, an international consortium of researchers conducted the first broad, comparative phylogenomic analysis of mycorrhizal fungi. Scientists describe how the comparative analyses of 18 new fungal genomes allowed them to track the evolution of symbiotic fungi interacting with trees, heath plants and orchids. The results help understand how plants and fungi developed symbiotic relationships, and how the mutualistic association provides host plants with beneficial traits for environmental adaptation. These resources will facilitate field studies aiming to predict responses of mycorrhizal communities to environmental shifts, such as altered forest-management practices and climate change. The consortium, led by INRA and involving the U.S. Department of Energy Joint Genome Institute (JGI), Clark University, University of Lorraine, CNRS, University of Aix-Marseilles and other collaborators, published these results in Nature Genetics on 23 February 2015.

Updated on 02/26/2015
Published on 02/23/2015

Almost all land plants form symbiotic associations with mycorrhizal fungi. These below-ground fungi play a key role in terrestrial ecosystems as they regulate nutrient and carbon cycles, and influence soil structure and ecosystem multifunctionality. “The mycorrhizal symbiosis is of key interest to biologists and ecologists because mycorrhizal fungi influence plant productivity and plant diversity, and mycorrhizal fungi connect plants below ground via a hyphal network allowing the movement of resources among coexisting plants”, explains Francis Martin, one of the leading INRA scientists of the study.

Recent studies indicate that mycorrhizal fungi also play a significant role in below-ground carbon sequestration, which may mitigate the effects of anthropogenic CO2 emissions. Mycorrhizal fungi include some of the most conspicuous forest mushrooms, including the iconic Fly Agaric, Amanita muscaria, the Black Truffle of Périgord, Tuber melanosporum, and the King Bolete, Boletus edulis. The fungal lineages containing mycorrhizal species are separated by tens or hundreds of millions of years, but they share remarkable morphological and metabolic similarities.

To identify the genetic innovations that led to convergent evolution of the mycorrhizal lifestyle from ancestral saprotrophic species, a large-scale comparative genomics project has been implemented by the Mycorrhizal Genomics Initiative consortium, led by INRA. These teams, together with longtime collaborators at the JGI, Clark University, University of Lorraine, University of Aix-Marseilles and other collaborators worldwide conducted the first broad, comparative phylogenomic analysis of mycorrhizal fungi, drawing on 49 fungal genomes, 18 of which were sequenced for this study. The 18 new fungal sequences included 13 mycorrhizal genomes, from ectomycorrhizal fungi that colonize tree roots, and including species that commingle with orchids and heathland plant roots. “Thanks to the comparative analyses of these genomes we identified the major innovations driving the evolution of symbiotic fungi in the past 200 million years. Scientists now understand how plants and fungi developed symbiotic relationships, and how the mutualistic association provides host plants with beneficial traits for environmental adaptation” says Martin.

The analyses of the fungal genomes and fossils suggested that in comparison to wood decayers, such as brown rot fungi and white rot fungi, that evolved over 300 million years ago, ectomycorrhizal fungi emerged more recently from several species of wood and litter decayers, and then spread out across lineages less than 200 million years ago during the expansion of forest ecosystems. It appears that mushroom-forming fungi evolved a complex mechanism for breakdown of plant cell walls in ‘white rot’ and then cast it aside following the evolution of ectomycorrhizal associations.

“The other major part of the story is that in mycorrhizal lineages there is a huge turnover in genes that are involved in the symbiosis”, comments Martin. Many of these have no homologs in even closely related species, suggesting that the evolution of the symbiosis is associated with massive genetic innovation. A subset of these genes is likely used to control plant immunity during the massive colonization of root tissues by the fungus. This study suggests that the genes required for mutualism were reinvented each time it developed in evolutionary history, although similar functional categories (e.g. nutrient transporters, secreted effector proteins) appear to be expressed in a similar manner.

After the genome sequencing of the first two sequenced ectomycorrhizal fungi, Laccaria bicolor and Tuber melanosporum, and the first sequenced arbuscular mycorrhizal fungus, Rhizophagus irregularis, this large-scale study of mycorrhizal genomics is also the first step in both broader and deeper exploration of mycorrhizal diversity, their interactions with host plans, and roles in forest ecosystems using genomics tools.

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Forest, Grassland and Freshwater Ecology
Associated Centre(s):
Nancy-Lorraine

Reference

Annegret Kohler, Alan Kuo, Laszlo G Nagy, Emmanuelle Morin, Kerrie W Barry, Francois Buscot, Björn Canbäck, Cindy Choi, Nicolas Cichocki, Alicia Clum, Jan Colpaert, Alex Copeland, Mauricio D Costa, Jeanne Doré, Dimitrios Floudas, Gilles Gay, Mariangela Girlanda, Bernard Henrissat, Sylvie Herrmann, Jaqueline Hess, Nils Högberg, Tomas Johansson, Hassine-Radhouane Khouja, Kurt LaButti, Urs Lahrmann, Anthony Levasseur, Erika A Lindquist, Anna Lipzen, Roland Marmeisse, Elena Martino, Claude Murat, Chew Y Ngan, Uwe Nehls, Jonathan M Plett, Anne Pringle, Robin A Ohm, Silvia Perotto, Robert Riley, Francois Rineau, Joske Ruytinx, Asaf Salamov, Firoz Shah, Hui Sun, Mika Tarkka, Andrew Tritt, Claire Veneault-Fourrey, Alga Zuccaro, Mycorrhizal Genomics Initiative Consortium, Anders Tunlid, Igor V Grigoriev, David S Hibbett & Francis Martin. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nature Genetics, Advance online publication on 23 February 2015. doi:10.1038/ng.3223