Stepwise recombination suppression around the mating-type locus in the fungusSchizothecium tetrasporum(Ascomycota, Sordariales)

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 of Sordariales: Podospora anserina and Neurospora tetrasperma. However, it is unclear whether this intriguing convergent association holds in other species. We show here that Schizothecium tetrasporum, a fungus from a third family in the order Sordariales, 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 in P. anserina. The mating-type locus has the typical Sordariales organization, plus a MAT1-1-1 pseudogene in the MAT1-2 haplotype. High-quality genome assemblies of opposite mating types and segregation analyses revealed a suppression of recombination in a region of 1.3 Mb around the mating-type locus. We detected three evolutionary strata, displaying a stepwise extension of recombination suppression, but no rearrangement or transposable element accumulation in the non-recombining region. 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 is consistent with a recently proposed mechanism of deleterious allele sheltering through recombination suppression around a permanently heterozygous locus.

The fate of recessive deleterious or overdominant mutations near mating-type loci under partial selfing

“…Increasing intra-tetrad selfing also induces more heterozygosity and thus slightly reinforces the sheltering effect of the mating-type locus. This is consistent with the findings that, in fungi, ascomycetes that reproduce via outcrossing and live as haploids do not show evolutionary strata (Skinner et al, 1993, Zhong et al, 2002, Phan et al, 2003, Kuhn et al, 2006, Jin et al, 2007, Malkus et al, 2009) whereas pseudo-homothallic ascomycete fungi, living as dikaryotic and undergoing mostly intra-tetrad selfing, are those with evolutionary strata around their mating-type locus (Menkis et al, 2008, Hartmann, Duhamel, et al, 2021, Hartmann, Ament-Velásquez, et al, 2021, Vittorelli et al, 2022). In basidiomycetes also, the species with evolutionary strata are dikaryotic and automictic, e.g.…”

“…In conclusion, our findings show that a mating-type locus has a sheltering effect on nearby deleterious mutations, especially in case of selfing and automixis, which can then play a role in the evolution of recombination suppression near mating-compatibility loci (Antonovics and Abrams, 2004, Jay et al, 2022). This may contribute to explain why evolutionary strata of recombination suppression near the mating-type locus are found mostly in automictic (pseudo-homothalic) fungi (Menkis et al, 2008, Branco et al, 2017, Branco et al, 2018, Hartmann et al, 2020, Hartmann, Ament-Velásquez, et al, 2021, Foulongne-Oriol et al, 2021, Vittorelli et al, 2022).…”

“…We therefore need to understand whether such mutations can persist in the vicinity of permanently heterozygous alleles (such as those occurring at mating-type loci) and under what conditions. In particular, it is usually considered that selfing purges deleterious mutations (Glémin, 2007, Billiard and Tran, 2012), while most evolutionary strata on fungal mating-type chromosomes have been reported in selfing (automictic) fungi (Branco et al, 2017, Branco et al, 2018, Hartmann, Ament-Velásquez, et al, 2021, Vittorelli et al, 2022). Indeed, bcause mating types are determined at the haploid stage in fungi, mating types do not prevent selfing when considering diploid individuals (Billiard et al, 2012).…”

“…Indeed, in many fungi, two gametes can form a new individual only if they carry different mating types, but there is no sexual antagonism or other form of antagonistic selection between cells of opposite mating types; the cells of different mating types do not show contrasted phenotypes or footprints of diversifying selection (Bazzicalupo et al, 2019). Yet, evolutionary strata have been documented on the mating-type chromosomes of multiple fungi, with recombination suppression extending stepwise beyond mating-type determining genes (Fraser et al, 2004, Menkis et al, 2008, Branco et al, 2017, Branco et al, 2018, Hartmann, Duhamel, et al, 2021, Hartmann, Ament-Velásquez, et al, 2021, Vittorelli et al, 2022). Evolutionary strata have also been reported around other supergenes, i.e ., large genomic regions encompassing multiple genes linked by recombination suppression, such as in ants and butterflies (Yan et al, 2020, Jay et al, 2021).…”

Dynamics of transposable element accumulation in the non-recombining regions of mating-type chromosomes in anther-smut fungi

“…Fungi with evolutionary strata are most often automictic, i.e. undergoing intra-tetrad selfing (Hartmann et al ., 2020; Vittorelli et al ., 2022). Theoretical models have suggested that this may be because automictic fungi are dikaryotic for most of their lifecycle, even in ascomycetes, thus allowing the sheltering of deleterious alleles (Jay et al ., 2022), and because automixis can prevent diploid selfing to purge deleterious mutations near mating-type loci (Antonovics & Abrams, 2004; Tezenas et al ., 2022).…”