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Discovery of a Modified Tetrapolar Sexual Cycle in Cryptococcus amylolentus and the Evolution of MAT in the Cryptococcus Species Complex

Findley, Keisha and Sun, Sheng and Fraser, James A. and Hsueh, Yen-Ping and Averette, Anna Floyd and Li, Wenjun and Dietrich, Fred S. and Heitman, Joseph (2012) Discovery of a Modified Tetrapolar Sexual Cycle in Cryptococcus amylolentus and the Evolution of MAT in the Cryptococcus Species Complex. PLoS Genetics, 8 (2). e1002528. ISSN 1553-7390. PMCID PMC3280970. https://resolver.caltech.edu/CaltechAUTHORS:20120328-120210924

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Abstract

Sexual reproduction in fungi is governed by a specialized genomic region called the mating-type locus (MAT). The human fungal pathogenic and basidiomycetous yeast Cryptococcus neoformans has evolved a bipolar mating system (a, α) in which the MAT locus is unusually large (>100 kb) and encodes >20 genes including homeodomain (HD) and pheromone/receptor (P/R) genes. To understand how this unique bipolar mating system evolved, we investigated MAT in the closely related species Tsuchiyaea wingfieldii and Cryptococcus amylolentus and discovered two physically unlinked loci encoding the HD and P/R genes. Interestingly, the HD (B) locus sex-specific region is restricted (~2 kb) and encodes two linked and divergently oriented homeodomain genes in contrast to the solo HD genes (SXI1α, SXI2a) of C. neoformans and Cryptococcus gattii. The P/R (A) locus contains the pheromone and pheromone receptor genes but has expanded considerably compared to other outgroup species (Cryptococcus heveanensis) and is linked to many of the genes also found in the MAT locus of the pathogenic Cryptococcus species. Our discovery of a heterothallic sexual cycle for C. amylolentus allowed us to establish the biological roles of the sex-determining regions. Matings between two strains of opposite mating-types (A1B1×A2B2) produced dikaryotic hyphae with fused clamp connections, basidia, and basidiospores. Genotyping progeny using markers linked and unlinked to MAT revealed that meiosis and uniparental mitochondrial inheritance occur during the sexual cycle of C. amylolentus. The sexual cycle is tetrapolar and produces fertile progeny of four mating-types (A1B1, A1B2, A2B1, and A2B2), but a high proportion of progeny are infertile, and fertility is biased towards one parental mating-type (A1B1). Our studies reveal insights into the plasticity and transitions in both mechanisms of sex determination (bipolar versus tetrapolar) and sexual reproduction (outcrossing versus inbreeding) with implications for similar evolutionary transitions and processes in fungi, plants, and animals.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1371/journal.pgen.1002528DOIArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc3280970/PubMed CentralArticle
Additional Information:This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Received September 2, 2011; Accepted December 21, 2011; Published February 16, 2012. This work was supported by NIAID R37 grant AI39115-14 and R01 grant AI50113-08 to JH and an NIH Minority Supplement 5R01-AI063443-04 S1 Sub #1-P30 that supported KF. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank Marianela Rodriguez-Carres and Banu Metin for helpful and critical discussions and technical assistance, Valerie Knowlton of NC State University for assistance with SEM, Leslie Eibest of Duke University for assistance with environmental SEM, Lisa Bukovnik of Duke University for assistance with sequencing, Rytas Vilgalys for inspiration, and Alvaro Fonseca for discussions. Author Contributions: Conceived and designed the experiments: KF SS JH. Performed the experiments: KF SS JAF Y-PH AFA WL FSD. Analyzed the data: KF SS JH. Wrote the paper: KF SS JH.
Funders:
Funding AgencyGrant Number
NIHAI39115-14
NIHAI50113-08
NIH5R01-AI063443-04 S1 Sub # 1-P30
Issue or Number:2
PubMed Central ID:PMC3280970
Record Number:CaltechAUTHORS:20120328-120210924
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20120328-120210924
Official Citation:Findley K, Sun S, Fraser JA, Hsueh Y-P, Averette AF, et al. (2012) Discovery of a Modified Tetrapolar Sexual Cycle in Cryptococcus amylolentus and the Evolution of MAT in the Cryptococcus Species Complex. PLoS Genet 8(2): e1002528. doi:10.1371/journal.pgen.1002528
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:29880
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:29 Mar 2012 14:14
Last Modified:06 Jul 2020 23:02

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