Elsevier

Fungal Biology Reviews

Volume 29, Issues 3–4, December 2015, Pages 220-229
Fungal Biology Reviews

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

https://doi.org/10.1016/j.fbr.2015.06.001Get rights and content

Highlights

  • Mating type loci and sex chromosomes are associated with suppressed recombination.

  • Exceptions to recombination suppression are known in the fungi.

  • Some fungal mating systems rely on or include increased recombination frequencies.

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.

Introduction

A decade ago an alarming hypothesis captured public imagination: men were going to become extinct within the next 5–10 million years (Marshall Graves, 2002). Behind this prediction was the degeneration of the male-specific Y chromosome. The Y chromosome, which was once an autosome carrying a sex-determining gene, has indeed experienced repeated and expanding stages in its accumulation of mutations relative to its homologous X chromosome. Degeneration of gene content and mutation accumulation are consequences of the lack of crossing-over during meiosis, because it is through such recombination that chromosomes with fewer deleterious mutations than the minimum number in the population can be produced (Graves, 2006, Bergero and Charlesworth, 2009) (Fig. 1a). It was thus first reasoned by Hermann Muller that, in the absence of recombination, chromosomes containing the fewest deleterious mutations would be regularly lost from the population by chance, which would lead to an irreversible and increasing loss in coding capability over time (Muller, 1964, Bergero and Charlesworth, 2009) (Fig. 1b). Although extensions of this model, known as “Muller's ratchet,” have been formulated [e.g., (Kondrashov, 1982)], they all predict a connection between the suppression of recombination and the accumulation of mutations. Furthermore, large regions united by recombination suppression prevent selection from acting independently upon variation in separate loci, causing hitchhiking of deleterious mutations together with positive selection of a beneficial allele [i.e., Hill-Robertson interference (Gillespie, 2000)].

Suppression of recombination and the consequent molecular degeneration around genes controlling sexual compatibility is not unique to humans as it is found in other animals, plants, and in the fungi (Hood, 2002, Fraser and Heitman, 2004a, Fraser and Heitman, 2004b, Whittle et al., 2011, Hood et al., 2013, Fontanillas et al., 2015). An apparent irony is found in that the very elements regulating genetic exchange between individuals are themselves largely excluded from the benefits of this recombination (Idnurm, 2011), especially because sex does not have to be determined genetically but can be through, as examples, environmental sex determination or sequential hermaphroditism (Bachtrog et al., 2014, Beukeboom and Perrin, 2014).

There may be processes that counter the trend toward degeneration and the recombinationally-inert nature of mating-type or sex chromosome regions. In one view, the nonreciprocal transfer of DNA sequence achieved through gene conversion may counter-act some of the deleterious effects of suppressed recombination (Marais et al., 2010, Trombetta et al., 2010), but this phenomenon remains rare in the regions where crossing-over frequencies are low (Bachtrog, 2013). A process of cyclical renewal of sex-determining regions has also been suggested, where new regions evolve to control the process of mating when old sex chromosomes become too degraded (Mank and Avise, 2009, Blaser et al., 2014). However, as recent studies expand both the diversity of species and the genetic tools for documenting recombination, there are some rare exceptions in which presumed dead spots of genetic exchange permit recombination.

Regions controlling mating compatibility are in some cases associated with suppressed recombination while in other cases they harbor crossing-over hotspots (Burgoyne, 1982, Yi and Li, 2005, Hsueh et al., 2006, Brick et al., 2012, Sarbajna et al., 2012, Jakočiūnas et al., 2013, Bolton et al., 2014). The evolutionary drivers for these contrasted relationships between recombination and mating-type determination are still unclear. That is, the regions controlling sex determination or mating compatibility take a broad range of values in their association with either recombination suppression or enhancement.

This article outlines three contrasted situations regarding recombination associated with regions that control mating compatibility; suppressed recombination, enhanced recombination, and non-homologous or non-reciprocal exchange that may counteract molecular degeneration. We outline some of the puzzles about these relationships between mating-type determination and recombination, and we suggest possible explanations. Recent discoveries in fungi provide valuable insights into the evolutionary genomics of sexual compatibility. While previous articles have highlighted the similarities between fungal mating-type chromosomes and the sex chromosomes in other eukaryotes (Fraser and Heitman, 2004a, Fraser and Heitman, 2004b, Menkis et al., 2008, Whittle and Johannesson, 2011), here we focus on the evolutionary causes for these similarities, point out the evolutionary differences, and highlight questions that remain to be answered.

Section snippets

Fungi are key model organisms for understanding the evolutionary genomics of sexual compatibility systems

The fungi are a large group of eukaryotes, with estimates of the total number of species in the millions (Blackwell, 2011). Mating has long been studied in fungi because they are tractable model organisms (Kniep, 1919, Gäumann, 1952), and the spores produced from sexual processes in the pathogen fungal species can be infectious propagules. Mating compatibility is determined by chromosomal regions that are referred to as the mating-type loci. Many species have a single mating-type locus that

Recombination suppressed around mating-type loci – driving forces and evolutionary consequences

In plants and animals, suppression of recombination on sex chromosomes is considered to have evolved due to the benefit of linking together multiple genes involved in sex determination, with the further suppression of recombination linking genes that display antagonistic effects in the opposite sex (Bergero and Charlesworth, 2009). The linking of sexually-antagonistic genes is often viewed as occurring in successive steps, creating “evolutionary strata” of ages of linkage and thus degrees of

Concluding remarks and future directions

The genes involved with mating compatibility are structurally arranged in a diversity of ways in fungi, which has resulted in a range of effects on recombination. There may be highly localized regions of meiotic recombination or conversely a great expansion of linkage that incorporates the majority of the chromosome. Fungi thus represent a fascinating group to study the evolutionary causes and consequences of recombination suppression and enhancement, being tractable systems, with their

Acknowledgments

Our research has been supported by the US National Science Foundation grants DEB-1115765 and DEB-0747222, National Institutes of Health grant R21 AI094364, the Australian Research Council, the Swedish Research Council, the FungiSex ANR-09-0064-01 grant, and the ERC starting grant GenomeFun 309403.

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