The complex evolution and genomic dynamics of mating-type loci in Cryptococcus and Kwoniella
Research highlight
Most fungi do not have males and females. Many have mating types instead, set by special stretches of DNA. Two cells can only mate if their types are compatible. In this group of fungi the mating genes sit in two regions, and how those regions are arranged shapes the way each species reproduces.
Cryptococcus, which includes yeasts that cause a dangerous form of meningitis in people with weakened immune systems, and its sister group Kwoniella show a wide range of these arrangements. The researchers produced new, high-quality genome assemblies and compared them.
They found that one of the two mating regions grew larger several separate times in Cryptococcus, probably as pheromone genes were copied. They also found three new cases where the two regions ended up together, each time because a piece of chromosome moved. In one species the regions share a chromosome but are still inherited separately. In the other two they fused into a single block that is passed on intact. Lab tests also confirmed that Cryptococcus decagattii can mate and produce spores.
Why it matters: fusing the two mating regions has happened independently in several groups of fungi. Understanding how it happens helps explain how these yeasts, including those that cause disease, reproduce and evolve, and shows the value of studying many different species.
Abstract
Sexual reproduction in basidiomycete fungi is governed by MAT loci (P/R and HD), which exhibit remarkable evolutionary plasticity, characterized by expansions, rearrangements, and gene losses often associated with mating system transitions. The sister genera Cryptococcus and Kwoniella provide a powerful framework for studying MAT loci evolution owing to their diverse reproductive strategies and distinct architectures, spanning bipolar and tetrapolar systems with either linked or unlinked MAT loci. Building on recent comparative genomic analyses, we generated additional chromosome-level assemblies, uncovering distinct trajectories shaping MAT loci organization. Contrasting with the small-scale expansions and gene acquisitions observed in Kwoniella, our analyses revealed independent expansions of the P/R locus in tetrapolar Cryptococcus, possibly driven by pheromone gene duplications. Notably, these expansions coincided with a pronounced GC-content reduction best explained by reduced GC-biased gene conversion following recombination suppression, rather than relaxed codon usage selection. Diverse modes of MAT locus linkage were also identified, including three previously unrecognized transitions: one resulting in a pseudobipolar arrangement and two leading to bipolarity. All three transitions involved translocations. In the pseudobipolar configuration, the P/R and HD loci remained on the same chromosome but genetically unlinked, whereas the bipolar transitions additionally featured rearrangements that fused the two loci into a nonrecombining region. Mating assays confirmed a sexual cycle in Cryptococcus decagattii, demonstrating its ability to undergo mating and sporulation. Progeny analysis in Kwoniella mangrovensis revealed substantial ploidy variation and aneuploidy, likely stemming from haploid–diploid mating, yet evidence of recombination and loss of heterozygosity indicates that meiotic exchange occurs despite irregular chromosome segregation. Our findings underscore the importance of continued diversity sampling and provide further evidence for convergent evolution of fused MAT loci in basidiomycetes, offering new insights into the genetic and chromosomal changes driving reproductive transitions.