Contrasted patterns in mating-type chromosomes in fungi: hotspots versus coldspots of recombination

Abstract

It is striking that, while central to sexual reproduction, the genomic regions determining sex or mating-types are often characterized by suppressed recombination that leads to a decrease in the efficiency of selection, shelters genetic load, and inevitably contributes to their genic degeneration. Research on model and lesser-explored fungi has revealed similarities in recombination suppression of the genomic regions involved in mating compatibility across eukaryotes, but fungi also provide opposite examples of enhanced recombination in the genomic regions that determine their mating types. These contrasted patterns of genetic recombination (sensu lato, including gene conversion and ectopic recombination) in regions of the genome involved in mating compatibility point to important yet complex processes occurring in their evolution. A number of pieces in this puzzle remain to be solved, in particular on the unclear selective forces that may cause the patterns of recombination, prompting theoretical developments and experimental studies. This review thus points to fungi as a fascinating group for studying the various evolutionary forces at play in the genomic regions involved in mating compatibility.

Keywords: Cryptococcus neoformans; MAT; Microbotryum violaceum; Muller’s ratchet; Neurospora tetrasperma; Podospora anserina; bipolar; heterothallism; homothallism; tetrapolar.

Fig 1

(A) Illustration of recombination as a mechanism for purging deleterious mutations. A crossing-over event between two chromosomes carrying different deleterious mutations (a and b) produces a chromosome free of deleterious mutations (A and B). (B) Illustration of the concept of Muller’s ratchet. Without recombination, the number of deleterious mutations per chromosome increases over time in the population, and the chromosomes free of deleterious mutations will be lost by chance. The dark blue shading shows a theoretical original state, with a given mean and variance for the number of deleterious alleles per chromosome in a population. The light blue shading shows the resultant state after many generations without recombination, illustrating the Muller’s ratchet effect of an increase in the mean number of deleterious mutations.

Fig 2

Different breeding systems in the fungi. Homothallism means that each haploid is compatible with all other haploids and heterothallism is when only cells of different mating types can mate. Bipolarity qualifies heterothallism where the mating type is determined by a single locus while under tetrapolarity mating can only occur when the two mating-type loci carry different alleles. Letters A and B indicate mating-type loci and numbered subscripts indicate alternate alleles, where they occur.

Fig 3

Patterns of recombination suppression or enhancement associated with mating-type loci (MAT) of fungi. Recombination may be enhanced in association with the mating-type loci of fungi, through non-allelic mating-type switching or by allelic recombination hotspots. A “silent” MAT indicates a potentially coding region placed within a transcriptionally quiescent part of the genome. If these regions are recombined into the active parts they are functional. Recombination may be suppressed, in examples in the basidiomycetes in which the two sex-determination regions are linked and/or by linkage to the centromere.