Symbiotic mycorrhizal fungi play an important role in terrestrial ecosystems by facilitating the acquisition of nutrients by plants. But how did these mushrooms become symbiotic? Thanks to the analysis of the genome of 135 species of forest fungi, the largest to date, an international consortium of researchers, coordinated by INRAE ​​and the Joint Genome Institute (US Department of Energy) and involving the University of Lorena and the CNRS, explains how these fungi went from being organisms that feed on decaying matter to symbionts allied to plants during evolution. Their results were published Oct. 12 in Nature Communications.

There are several types of fungi defined by their mode of nutrition: pathogens that parasitize living organisms for food, saprotrophs that feed on decaying organic matter, and mycorrhizae that are in symbiosis with plants. Symbiosis is a beneficial relationship for the plant and the fungus. The fungus helps plants absorb essential minerals, such as nitrogen and phosphorus, and plants provide simple sugars for associated fungi and a favorable environment for their development. This mutualistic symbiosis would have allowed the colonization of terrestrial environments by plants. To understand how symbiotic traits appeared in forest fungi, the consortium compared the functions encoded by the genome of 135 species, including 62 species of mycorrhiza. The originality of this new study lies in the sequencing and analysis of 29 new genomes of species of symbiotic fungi belonging to families that play a key role in forest ecosystems, such as Russulas and Chanterelles, very common in temperate forests.

Their results show that multiple transitions from a saprotrophic to symbiotic lifestyle are accompanied by the loss of genes that encode enzymes that degrade the plant cell wall (eg, cellulases and ligninases), the reorientation of genes present in plants. saprotrophic ancestors to perform new symbiotic functions (for example, membrane transporters of sugars or amino acids) and the appearance of new genes involved in communication with the plant. These mechanisms are observed in all the families of basidiomycetes and ectomycorrhizal ascomycetes (20,000 species), illustrating a remarkable evolutionary convergence spanning more than 100 million years of evolutionary history. For the first time, researchers have also identified some species of "hybrid" fungi, still capable of breaking down organic matter, while establishing a symbiosis with the roots of their host plant. In these fungi, the genes encoding the plant wall degradation enzymes are still present, but repressed during symbiosis. These may be the first steps towards a strict symbiosis.

This new study significantly increases the genomic resources available to study the mechanisms that govern the development and function of mycorrhizal symbioses. In addition to a better understanding of the evolutionary history of forest mushrooms, these resources are now used to study the functioning of mushroom communities in forest ecosystems subject to the vagaries of environmental change.