Abstract

Sexual identity is governed by sex chromosomes in plants and animals, and by mating type (MAT) loci in fungi. Comparative analysis of the MAT locus from a species cluster of the human fungal pathogen Cryptococcus revealed sequential evolutionary events that fashioned this large, highly unusual region. We hypothesize that MAT evolved via four main steps, beginning with acquisition of genes into two unlinked sex-determining regions, forming independent gene clusters that then fused via chromosomal translocation. A transitional tripolar intermediate state then converted to a bipolar system via gene conversion or recombination between the linked and unlinked sex-determining regions. MAT was subsequently subjected to intra- and interallelic gene conversion and inversions that suppress recombination. These events resemble those that shaped mammalian sex chromosomes, illustrating convergent evolution in sex-determining structures in the animal and fungal kingdoms.

Highlights

  • Elucidating mechanisms by which sex chromosomes evolved from autosomes has been accelerated by the revolution in genomic sciences

  • Our studies reveal that the mating type (MAT) locus of C. neoformans is strikingly divergent from that of the model budding yeast S. cerevisiae, other ascomyctes, and even related basidiomycetes

  • The similarity between the MAT locus of S. cerevisiae and that of C. neoformans is restricted to the presence of related homeodomain proteins, suggesting that these may represent the most ancient components of the ancestral MAT locus that was shared between the ascomycete and basidiomycete lineages

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Summary

Introduction

Elucidating mechanisms by which sex chromosomes evolved from autosomes has been accelerated by the revolution in genomic sciences. The male-specific approximately 50–60 Mb Y chromosome evolved via chromosomal rearrangement, gene conversion, duplication, and degeneration over approximately 300 million years to give rise to four distinct evolutionary temporal groupings, or strata (Lahn and Page 1999; Skaletsky et al 2003). In contrast to mammals and other obligate diploid organisms, fungi are viable as both haploids (the equivalent of gametes in other systems) and diploids. This has influenced the evolution of genes in the sex-determining regions in the two systems, as it enables those in obligate diploids to degenerate to nonfunctional alleles in one of two sexdetermining chromosomes

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