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Sexual reproduction is critical for successful evolution of eukaryotic organisms in adaptation to changing environments. In the opportunistic human fungal pathogens, the  Cryptococcus  pathogenic species complex,  C .  neoformans  primarily undergoes bisexual reproduction, while  C .  deneoformans  undergoes both unisexual and bisexual reproduction. During both unisexual and bisexual cycles, a common set of genetic circuits regulates a yeast-to-hyphal morphological transition, that produces either monokaryotic or dikaryotic hyphae. As such, both the unisexual and bisexual cycles can generate genotypic and phenotypic diversity  de novo . Despite the similarities between these two cycles, genetic and morphological differences exist, such as the absence of an opposite mating-type partner and monokaryotic instead of dikaryotic hyphae during  C .  deneoformans  unisexual cycle. To better understand the similarities and differences between these modes of sexual reproduction, we focused on two cellular processes involved in sexual reproduction: cell-cell fusion and karyogamy. We identified orthologs of the plasma membrane fusion protein Prm1 and the nuclear membrane fusion protein Kar5 in both  Cryptococcus  species, and demonstrated their conserved roles in cell fusion and karyogamy during  C .  deneoformans  α-α unisexual reproduction and  C .  deneoformans  and  C .  neoformans   a -α bisexual reproduction. Notably, karyogamy occurs inside the basidum during bisexual reproduction in  C .  neoformans , but often occurs earlier following cell fusion during bisexual reproduction in  C .  deneoformans . Characterization of these two genes also showed that cell fusion is dispensable for solo unisexual reproduction in  C .  deneoformans . The blastospores produced along hyphae during  C .  deneoformans  unisexual reproduction are diploid, suggesting that diploidization occurs early during hyphal development, possibly through either an endoreplication pathway or cell fusion-independent karyogamy events. Taken together, our findings suggest distinct mating mechanisms for unisexual and bisexual reproduction in  Cryptococcus , exemplifying distinct evolutionary trajectories within this pathogenic species complex.

plos genetics

PRM1 and KAR5 function in cell-cell fusion and karyogamy to drive distinct bisexual and unisexual cycles in the Cryptococcus pathogenic species complex