4.8 Article

Size Variation of the Nonrecombining Region on the Mating-Type Chromosomes in the Fungal Podospora anserina Species Complex

Journal

MOLECULAR BIOLOGY AND EVOLUTION
Volume 38, Issue 6, Pages 2475-2492

Publisher

OXFORD UNIV PRESS
DOI: 10.1093/molbev/msab040

Keywords

convergence; mating-type chromosomes; fungi; fungal chromosomes; sex chromosomes; automixis; pseudohomothallism; evolutionary strata; transposable elements

Funding

  1. European Research Council (ERC) [832352]
  2. Marie Curie European grant [PRESTIGE-2016-4-0013]
  3. Fondation des Treilles
  4. ERC SpoKiGen (ERC-2014-CoG) grant
  5. Swedish Research Council (VR)
  6. Lars Hierta Memorial Foundation
  7. Nilsson-Ehle Endowments of the Royal Physiographic Society of Lund
  8. Universiwte de Paris Diderot
  9. European Research Council (ERC) [832352] Funding Source: European Research Council (ERC)

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The study reveals the presence of nonrecombining regions around the mating-type locus in the fungus Podospora anserina and related species, leading to occasional recombination due to the labile and polymorphic nature of these regions. The size and location of the nonrecombining region vary between strains and species, resulting in differences in heterozygosity levels. Low levels of heterozygosity suggest low but nonnull outcrossing rates in nature for these pseudohomothallic fungi, contributing to our understanding of mating-type chromosome evolution and mating systems.
Sex chromosomes often carry large nonrecombining regions that can extend progressively over time, generating evolutionary strata of sequence divergence. However, some sex chromosomes display an incomplete suppression of recombination. Large genomic regions without recombination and evolutionary strata have also been documented around fungal mating-type loci, but have been studied in only a few fungal systems. In the model fungus Podospora anserina (Ascomycota, Sordariomycetes), the reference S strain lacks recombination across a 0.8-Mb region around the mating-type locus. The lack of recombination in this region ensures that nuclei of opposite mating types are packaged into a single ascospore (pseudohomothallic lifecycle). We found evidence for a lack of recombination around the mating-type locus in the genomes of ten P. anserina strains and six closely related pseudohomothallic Podospora species. Importantly, the size of the nonrecombining region differed between strains and species, as indicated by the heterozygosity levels around the mating-type locus and experimental selfing. The nonrecombining region is probably labile and polymorphic, differing in size and precise location within and between species, resulting in occasional, but infrequent, recombination at a given base pair. This view is also supported by the low divergence between mating types, and the lack of strong linkage disequilibrium, chromosomal rearrangements, transspecific polymorphism and genomic degeneration. We found a pattern suggestive of evolutionary strata in P. pseudocomata. The observed heterozygosity levels indicate low but nonnull outcrossing rates in nature in these pseudohomothallic fungi. This study adds to our understanding of mating-type chromosome evolution and its relationship to mating systems.

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