Stepwise recombination suppression around the mating-type locus in an ascomycete fungus with self-fertile spores

Author:

Vittorelli Nina,Rodríguez de la Vega Ricardo C.,Snirc Alodie,Levert Emilie,Gautier Valérie,Lalanne Christophe,De Filippo Elsa,Gladieux PierreORCID,Guillou Sonia,Zhang YuORCID,Tejomurthula Sravanthi,Grigoriev Igor V.,Debuchy RobertORCID,Silar Philippe,Giraud Tatiana,Hartmann Fanny E.ORCID

Abstract

Recombination is often suppressed at sex-determining loci in plants and animals, and at self-incompatibility or mating-type loci in plants and fungi. In fungal ascomycetes, recombination suppression around the mating-type locus is associated with pseudo-homothallism,i.e. the production of self-fertile dikaryotic sexual spores carrying the two opposite mating types. This has been well studied in two species complexes from different families ofSordariales:Podospora anserinaandNeurospora tetrasperma. However, it is unclear whether this intriguing association holds in other species. We show here thatSchizothecium tetrasporum, a fungus from a third family in the orderSordariales, also produces mostly self-fertile dikaryotic spores carrying the two opposite mating types. This was due to a high frequency of second meiotic division segregation at the mating-type locus, indicating the occurrence of a single and systematic crossing-over event between the mating-type locus and the centromere, as inP.anserina. The mating-type locus has the typicalSordarialesorganization, plus aMAT1-1-1pseudogene in theMAT1-2haplotype. High-quality genome assemblies of opposite mating types and segregation analyses revealed a suppression of recombination in a region of 1.47 Mb around the mating-type locus. We detected three evolutionary strata, indicating a stepwise extension of recombination suppression. The three strata displayed no rearrangement or transposable element accumulation but gene losses and gene disruptions were present, and precisely at the strata margins. Our findings indicate a convergent evolution of self-fertile dikaryotic sexual spores across multiple ascomycete fungi. The particular pattern of meiotic segregation at the mating-type locus was associated with recombination suppression around this locus, that had extended stepwise. This association between pseudo-homothallism and recombination suppression across lineages and the presence of gene disruption at the strata limits are consistent with a recently proposed mechanism of sheltering deleterious alleles to explain stepwise recombination suppression.

Funder

H2020 European Research Council

ANR

Joint Genome Institute

DOE Office of Science User Facility

Office of Science of the US Department of Energy

Publisher

Public Library of Science (PLoS)

Subject

Cancer Research,Genetics (clinical),Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics

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