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Evolution of fungal mating-type chromosomes

Periodic Reporting for period 1 - MatTypeEvol (Evolution of fungal mating-type chromosomes)

Reporting period: 2016-03-01 to 2018-02-28

Sex chromosomes often show extensive areas of suppressed recombination and cytological differentiation, a well-documented phenomenon in animals and plants. Lack of recombination is expected to limit the efficacy of natural selection, leading to degeneration in gene content. Similarly, fungal mating-type chromosomes can display patterns of suppressed recombination, however the mechanisms responsible and the extent of genic degeneration are still unclear. The proposed research investigates the evolution of fungal mating-type chromosomes, more specifically the patterns and mechanisms underlying genomic regions with suppressed recombination linked to mating compatibility genes and how this phenomenon impacts fitness and the genome. I use comparative genomics and a model fungal system with dimorphic mating-type chromosomes of different degrees and ages for understanding the steps involved in the evolution of suppressed recombination and genomic degeneration. This project compiles results that yield unprecedented insights into the evolution of mating-type chromosomes, the dynamics of genome degradation in sexual eukaryotic species, and more generally contribute for a unified view of evolution in dimorphic chromosomes with suppressed recombination.
During the completion of this project a total of 31 fungal genomes were sequenced with Pacific Biosciences technology, assembled and annotated. These high quality genomes were used to compile a phylogeny for the Microbotryum violaceum complex and detect and compare regions of suppressed recombination across species.
One of the main findings of the study were that fungal mating type chromosomes evolve in a very similar way to sex chromosomes in plants and animals. It was previously thought that the typical sex chromosome structure (with strong asymmetry and one highly degenerated chromosome, such as the Y in humans) was caused by the existence of separate sexes and alleles specifically beneficial in one sex or the other. Given that fungi display mating types (with very few loci defining mating compatibility) and do not have separate sexes, finding the exact same chromosome structure in fungi and plants/animals with traditional sex chromosomes implies that separate sexes alone cannot be responsible for sex chromosome architecture.
The project also investigated the evolution of suppressed recombination in Microbotryum and documented for the first time repeated independent events of recombination suppression in closely related species. Recombination suppression leads to higher gamete compatibility in these selfing species and is under strong selection. Comprehensive genomic analyses indicated at least five independent events of recombination suppression, with distinct chromosomal arrangements and different ages.
This project made crucial contributions for the understanding of sexual reproduction in eukaryotes. Finding such striking parallel across plants, animals and fungi will foster discussion and revision of current theories for the evolution of sexual reproduction in eukaryotes beyond sexual antagonism. Furthermore, two graduate students were trained in genomics throughout the course of the project, one of which from an underrepresented background.
Microbotryum violaceum infecting a Silene latifolia flower. Photo by Michale Hood.