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Levert, E.

Publications and source records attributed to Levert, E..

3 recordsLinked to original sources

Stepwise recombination suppression around the mating-type locus associated with a diploid-like life cycle in Schizothecium fungi

Recombination suppression often evolves around sex-determining loci and extends stepwise, resulting in adjacent regions with different levels of divergence between sex chromosomes, called evolutionary strata. In Ascomycota fungi, evolutionary strata have been found around the mating-type (MAT) locus only in pseudo-homothallic species, i.e., with a diploid-like lifecycle and mycelia carrying nuclei of both mating types. In contrast, no recombination suppression has been observed in fungi with a haploid-like lifecycle, such as heterothallic fungi (with mycelial colonies of a single mating type each). Here, we investigated the evolution of recombination suppression in a clade of dung fungi encompassing 16 pseudo-homothallic and three heterothallic sibling species from the Schizothecium genus (Ascomycota, Sordariales). The analysis of genetic divergence based on genome sequencing indicated recombination suppression around the MAT locus in all investigated 13 pseudo-homothallic species. The non-recombining region ranged from 600 kb to 1.6 Mb and harbored multiple evolutionary strata, varying in size and number among species. The separation of alleles associated with alternative mating types in gene genealogies across strains within species, the high linkage disequilibrium and an inversion in one species supported the lack of recombination in the MAT-proximal region in pseudo-homothallic species. The overall lack of trans-specific polymorphism suggested multiple independent events of recombination suppression or the occurrence of rare events of recombination or genic conversion. Progeny analyses showed the occurrence of recombination close to the MAT locus in heterothallic strains. We thus revealed here multiple and likely independent evolutionary strata, associated with an extended diploid-like stage in Schizothecium fungi, which provides a good model for research on sex-related chromosome evolution.

evolutionary biology↗

Huge genetic diversity of Schizothecium tetrasporum (Wint.). N. Lundq.: delimitation of 18 species distributed into three complexes through genome sequencing

Analyses of the genetic diversity of well-studied fungi of the Sordariales order, such as Neurospora spp. and Podospora anserina (syn. Triangularia anserina), have shown that the species classically defined by morphology are often complexes of cryptic species. Here, we report on the species delimitation among 76 strains producing mycelium and sexual reproductive structures identical to those of the pseudo-homothallic Sordariales species Schizothecium tetrasporum (syn. Neoschizothecium tetrasporum). Their whole genomes were sequenced as well as those of six strains closely related to Schizothecium tetrasporum but producing eight-spored asci instead of four-spored ones. The clustering based on the Average Nucleotide Identity (ANI) between the genomes identified eighteen species grouped into three clades, which were further supported by a phylogenetic tree constructed with whole genome Single Nucleotide Polymorphisms (SNPs). Based on their contrasting breeding systems and their large evolutionary distances, we considered the three clades as distinct species complexes. Indeed, two of them, the Schizothecium tetrasporum and Schizothecium pseudotetrasporum complexes, contains pseudo-homothallic species producing four-spored asci, while the third one, which we named Schizothecium octosporum, contains heterothallic species producing eight-spored asci. Surprisingly it was nestled between the two complexes of pseudo-homothallic species. Our data reveals thus a huge genetic diversity of the Schizothecium tetrasporum morpho-species and a convergent evolution of pseudo-homothallism or reversion to heterothallism within the complexes. An epitype for Schizothecium tetrasporum sensus stricto is defined and the seventeen new Schizothecium species are formally described.

microbiology↗

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

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. AUTHOR SUMMARYRecombination allows faster adaptation and the purging of deleterious mutation but is often paradoxically lacking in sex chromosomes. It has been recently recognized that recombination can also be suppressed on fungal mating-type chromosomes, but the evolutionary explanation and the proximal mechanism of this phenomenon remain unclear. By studying here the sexual biology of a poorly studied mold living in rabbit dung, we reveal a striking convergence in three distant fungal lineages of an independently evolved association between the production of self-fertile sexual spores (carrying two nuclei with opposite mating types), a particular segregation of the mating-type locus and the lack of recombination on mating-type chromosomes, having evolved stepwise. Such a convergent association suggests causal relationships and will contribute to unveil the evolutionary causes of recombination suppression. Graphical summary O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=174 SRC="FIGDIR/small/500756v2_ufig1.gif" ALT="Figure 1"> View larger version (40K): org.highwire.dtl.DTLVardef@1cea706org.highwire.dtl.DTLVardef@378c41org.highwire.dtl.DTLVardef@d90297org.highwire.dtl.DTLVardef@1391c74_HPS_FORMAT_FIGEXP M_FIG C_FIG

evolutionary biology↗