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

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 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 1.47 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.

Genome biology and evolution of mating type loci in four cereal rust fungi

“…Indeed, several fungal species carry extensive non-recombining regions around MAT loci. Recombination suppression can range from hundreds of kbp (kilo base pairs) to several mbp (mega base pairs) and lead to genetic degeneration (5, 9), such as in Neurospora tetrasperma (10), Podospora anserina (11), Schizothecium tetrasporum (12) and several Microbotryum spp. (8, 13).…”

The Sordariomycetes: an expanding resource with Big Data for mining in evolutionary genomics and transcriptomics

“…For example, the genomes of a large number of species of Xylariale have recently been sequenced, and comparative genomics has revealed genetic changes that are probably associated with bioactivities, diverse lifestyles, environmental adaptations, and selective pressure in these “mystical”-looking fungi ( Robinson et al., 2020 ; Wibberg et al., 2020 ; Franco et al., 2022 ; Fricke et al., 2023 ). At the same time, the annotation of classic model genomes, such as those of Neurospora , Podospora , and Sordaria genomes, has undergone continuous improvement, in part on the basis of information obtained from newly sequenced genomes of the same or closely related species ( Teichert et al., 2014 ; Gladieux et al., 2015 ; Blank-Landeshammer et al., 2019 ; Teichert et al., 2020 ; Lelandais et al., 2022 ; Rodriguez et al., 2022 ; Vittorelli et al., 2023 ). These accumulating data continue to contribute to a new era of evolutionary genomics and transcriptomics at further taxonomic levels within the Sordariomycetes class.…”

Repeated loss of function at HD mating-type genes and of recombination suppression without mating-type locus linkage in anther-smut fungi

“…Recombination is typically suppressed at loci determining sexes and mating types, which ensures proper function in these complex phenotypes. Recombination suppression has furthermore often extended stepwise outward from these mating-compatibility loci in plants, animals and fungi 17,18, 19,20,21, 22, 23, 24 , and the reason why is still debated 23, 25 . It has long been accepted that recombination suppression extended on sex chromosomes because it was beneficial to link sexually antagonistic genes (i.e., with an allele being beneficial in only one sex) to the sex-determining locus 26 .…”