Recombination suppression and evolutionary strata around mating-type loci in fungi: documenting patterns and understanding evolutionary and mechanistic causes.

Fanny E Hartmann,Pierre Grognet,Marie Foulongne‐Oriol,Philippe Silar,Fantin Carpentier,Marine Duhamel,Fabienne Malagnac,Tatiana Giraud,Michael E Hood

doi:10.1111/nph.17039

Abstract

SummaryGenomic regions determining sexual compatibility often display recombination suppression, as occurs in sex chromosomes, plant self‐incompatibility loci and fungal mating‐type loci. Regions lacking recombination can extend beyond the genes determining sexes or mating types, by several successive steps of recombination suppression. Here we review the evidence for recombination suppression around mating‐type loci in fungi, sometimes encompassing vast regions of the mating‐type chromosomes. The suppression of recombination at mating‐type loci in fungi has long been recognized and maintains the multiallelic combinations required for correct compatibility determination. We review more recent evidence for expansions of recombination suppression beyond mating‐type genes in fungi (‘evolutionary strata’), which have been little studied and may be more pervasive than commonly thought. We discuss testable hypotheses for the ultimate (evolutionary) and proximate (mechanistic) causes for such expansions of recombination suppression, including (1) antagonistic selection, (2) association of additional functions to mating‐type, such as uniparental mitochondria inheritance, (3) accumulation in the margin of nonrecombining regions of various factors, including deleterious mutations or transposable elements resulting from relaxed selection, or neutral rearrangements resulting from genetic drift. The study of recombination suppression in fungi could thus contribute to our understanding of recombination suppression expansion across a broader range of organisms.

Highlights

Recombination suppression around genes controlling mating compatibility in various organismsAs a fundamental feature of sexual reproduction, recombination between different genotypes can generate beneficial allelic combinations and purge deleterious mutations (Otto, 2009)
Matingtype loci are incompatibility loci not associated with gamete size determinism; successful mating is possible only between gametes or cells carrying different alleles at the mating-type loci based on molecular nonselfrecognition, regardless of gamete or cell size
Even in fungi producing small and large gametes or undergoing sex by mating between a spore* and a hypha* as a form of anisogamy*, gamete size is not determined by the mating-type locus*; all haploid genotypes are hermaphrodites*, being able to produce male* and female* gametes, whereas compatibility is most often still determined by molecular mechanisms controlled by the mating-type loci (Butler, 2007; Fraser et al, 2007; Billiard et al, 2011, 2012)

Summary

Introduction

Recombination suppression around genes controlling mating compatibility in various organisms. Even in fungi producing small and large gametes or undergoing sex by mating between a spore* and a hypha* as a form of anisogamy*, gamete size is not determined by the mating-type locus*; all haploid genotypes are hermaphrodites*, being able to produce male* and female* gametes, whereas compatibility is most often still determined by molecular mechanisms controlled by the mating-type loci (Butler, 2007; Fraser et al, 2007; Billiard et al, 2011, 2012). Multiple evolutionary strata extended the region without recombination, in several steps, beyond matingtype genes and centromeres, into regions devoid of genes involved in mating-type determination This expansion has occurred independently in several Microbotryum lineages (Branco et al, 2018) (Fig. 4; Box 3). This approach utilizes the principle that, as soon as recombination cessation links a gene to the mating-type locus*, the alleles at this gene will accumulate differentiating mutations in the (a) Neurospora tetrasperma

Post-meiotic mitosis mat-A mat-a mat-A mat-a mat-a mat-A mat-a

Consequences of recombination suppression: genomic degeneration

Findings

VIII. Conclusion and future directions