TY - JOUR TI - Obligate sexual reproduction of a homothallic fungus closely related to the Cryptococcus pathogenic species complex AU - Passer, Andrew Ryan AU - Clancey, Shelly Applen AU - Shea, Terrance AU - David-Palma, Márcia AU - Averette, Anna Floyd AU - Boekhout, Teun AU - Porcel, Betina M AU - Nowrousian, Minou AU - Cuomo, Christina A AU - Sun, Sheng AU - Heitman, Joseph AU - Coelho, Marco A A2 - Rokas, Antonis A2 - Weigel, Detlef A2 - Dyer, Paul VL - 11 PY - 2022 DA - 2022/06/17 SP - e79114 C1 - eLife 2022;11:e79114 DO - 10.7554/eLife.79114 UR - https://doi.org/10.7554/eLife.79114 AB - Sexual reproduction is a ubiquitous, ancient eukaryotic trait. While most sexual organisms have to find a mating partner, species as diverse as animals, plants, and fungi have evolved the ability to reproduce sexually without requiring another individual. Here, we uncovered the mechanism of self-compatibility (homothallism) in Cryptococcus depauperatus, a fungal species closely related to the human fungal pathogens Cryptococcus neoformans and Cryptococcus gattii. In contrast to C. neoformans or C. gattii, which grow as a yeast asexually, and produce hyphae, basidia, and infectious spores during sexual reproduction, C. depauperatus grows exclusively as hyphae decorated with basidia and abundant spores, thus continuously engaged in sexual reproduction. Through comparative genomics and analyses of mutants defective in key mating/meiosis genes, we demonstrate the C. depauperatus sexual cycle involves meiosis and that self-compatibility is orchestrated by an unlinked mating receptor (Ste3a) and pheromone ligand (MFα) pair derived from opposite mating types of a heterothallic (self-sterile) ancestor. We identified a putative mating-type (MAT) determining region containing genes phylogenetically aligned with MATa alleles of other species, and a few MATα gene alleles scattered throughout the genome, but no homologs of the mating-type homeodomain genes SXI1 (HD1) and SXI2 (HD2). Comparative analyses suggest a dramatic remodeling of the MAT locus possibly owing to reduced selective constraints to maintain mating-type genes in tight linkage, associated with a transition to self-fertility. Our findings support C. depauperatus as an obligately sexual, homothallic fungus and provide insight into repeated transitions between sexual reproduction modes that have occurred throughout the fungal kingdom. KW - sexual reproduction KW - meiosis KW - cryptococcus KW - Cryptococcus depauperatus KW - homothallism in fungi JF - eLife SN - 2050-084X PB - eLife Sciences Publications, Ltd ER -