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GENOMEFUN Report Summary

Project ID: 309403
Funded under: FP7-IDEAS-ERC
Country: France

Final Report Summary - GENOMEFUN (Genomics of adaptive divergence in Fungi)

Identifying the genes underlying adaptation of living organisms to their environment, their distribution in genomes and the evolutionary forces shaping genomic diversity are key challenges in evolutionary biology. The GenomeFun project aimed at elucidating the genomic bases of adaptation using two kinds of fungi as models, domesticated fungi used for cheese making and plant pathogenic fungi.
Domestication is an excellent model for studies of adaptation because it involves recent and strong selection on a few, identified traits. Few studies have focused on the domestication of fungi, despite their importance to bioindustry and to a general understanding of adaptation in eukaryotes. Penicillium fungi are ubiquitous molds among which two distantly related species have been independently selected for cheese making—P. roqueforti for blue cheeses like Roquefort and P. camemberti for soft cheeses like Camembert. By comparing the genomes of ten Penicillium species, we have shown that adaptation to cheese was associated with multiple recent horizontal transfers of large genomic regions carrying crucial metabolic genes involved in milk metabolism. These genomic regions were experimentally associated with faster growth and greater competitiveness on cheese. We also used a population genomics approach to reconstruct the evolutionary history of Penicillium roqueforti, the fungus used for blue cheese production. Four populations were identified, including two containing only cheese strains (one corresponding to the emblematic Roquefort “protected designation of origin” strains), and two non-cheese populations including silage and food-spoiling strains. We showed that the two cheese populations were derived from independent domestication events. The non-Roquefort population had lost most of its genetic diversity and displayed greater fitness for traits related to industrial cheese maturation, such as greater lipolysis, cheese colonization and salt tolerance. It probably originated from the industrial selection of a single strain and is used worldwide for the production of all types of blue cheese other than Roquefort. The Roquefort population has kept some genetic diversity, probably due to the ancient use of different strains across multiple farms and the protected designation of origin imposing to use local fungal strains. The Roquefort population showed differentiated traits, with possible selection for slower growth before the invention of refrigeration and greater spore production on the traditional multiplication medium (bread). This study sheds light on the processes of adaptation to rapid environmental changes, has industrial and food safety implications and raises questions about the conservation of genetic resources.
We also used fungi pathogen of plants as models for elucidating the genomic mechanisms of rapid adaptation. We performed one of the first studies on the abundance and distribution of recent adaptive events in genomes. We showed that footprints of recent and rapid adaptation were abundant and scattered throughout the genome, likely in relation to coevolution with the host plant. We also discovered unexpected and striking patterns on mating-type chromosomes, with independent events of suppressed recombination in multiple fungal linages. Such convergent adaptation provides unique insights into the predictability of evolution and ultimately into processes of adaptation and biological diversification. We found that selection was less efficient in regions without recombination, leading to the accumulation of repetitive elements, deleterious mutations and massive genomic rearrangements. Furthermore, we showed that the fungal mating-type chromosomes displayed successive steps of recombination suppression, as animal and plant sex chromosomes. Yet the currently accepted theory for explaining such successive steps of recombination suppression are linked to differences between males and females which cannot apply to fungal mating-type chromosomes. Our finding thus call for a unified theory of sex-related chromosome evolution and we have proposed alternative hypotheses.
In conclusion, the ERC GenomeFun project brought unique insights into the genomic mechanisms of rapid adaptation, with fundamental and applied implications.

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