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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). Art. No. e1002528. ISSN 1553-7404. PMCID PMC3280970. https://resolver.caltech.edu/CaltechAUTHORS:20200218-151248653

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[img] Image (TIFF) (Figure S1. Fosmid map of the HD and P/R assembly in T. wingfieldii) - Supplemental Material
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[img] Image (TIFF) (Figure S2. Fosmid map of the HD and P/R assembly in C. amylolentus. One fosmid (4E01) constitutes the HD locus while three fosmids (3N14, 4E22, and 3H19) span the P/R locus) - Supplemental Material
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[img] Image (TIFF) (Figure S3. Estimations of the sizes of the gaps within the PR locus assembly based on Southern blotting) - Supplemental Material
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[img] Image (TIFF) (Figure S4. Results of PCR assay indicating similarity and divergence between CBS6039 and CBS6273 within the P/R locus assembly) - Supplemental Material
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[img] Image (TIFF) (Figure S5. Extensive chromosomal rearrangements are present throughout MAT in the sibling species and C. neoformans strain JEC21) - Supplemental Material
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[img] Image (TIFF) (Figure S6. Phylogenetic analysis of additional C. amylolentus genes) - Supplemental Material
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[img] Image (TIFF) (Figure S7. Phylogenetic analysis of the homeodomain transcription factor genes, SXI1 and SXI2 in C. amylolentus) - Supplemental Material
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[img] Image (TIFF) (Figure S8. Fluorescence microscopy of C. amylolentus mating structures) - Supplemental Material
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[img] Image (TIFF) (Figure S9. Evidence for one meiotic event in each basidium) - Supplemental Material
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[img] Image (TIFF) (Figure S10. The SXI1 and SXI2 dimorphic region is similar in CBS6039 and F1 set 2 progeny #4) - Supplemental Material
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[img] Image (TIFF) (Figure S11. F1 Set 2 progeny #16 is recombinant and types as CBS6039 at SXI1 and as CBS6273 at SXI2) - Supplemental Material
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[img] Image (TIFF) (Figure S12. The SXI1-SXI2 dimorphic region differs between CBS6273 and progeny set 2 F1 progeny #16) - Supplemental Material
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[img] Image (TIFF) (Figure S13. Mating assays between MAT recombinant progeny and the bi-mater set 1 F1 #4 crossed to the parental strains) - Supplemental Material
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[img] MS Word (Table S1. Random spore dissection of set 1 F1 progeny and molecular analysis of the nuclear markers) - Supplemental Material
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[img] MS Word (Table S2. RAPD analysis of F1 set 1 progeny) - Supplemental Material
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[img] MS Word (Table S3. List of primers, RAPD markers, and mitochondrial markers used in the study) - Supplemental Material
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[img] MS Word (Table S4. Filamentous phenotype and mitochondrial DNA (mtDNA) inheritance identified in all 65 progeny) - Supplemental Material
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[img] MS Word (Text S1. Additional discussions on strains, filamentous phenotype, RPL22 duplication, and analyses of HD dimorphic region in key progeny) - Supplemental Material
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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.


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https://doi.org/10.1371/journal.pgen.1002528DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3280970/PubMed CentralArticle
https://doi.org/10.1371/journal.pgen.1002528.s001DOIFigure S1
https://doi.org/10.1371/journal.pgen.1002528.s002DOIFigure S2
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https://doi.org/10.1371/journal.pgen.1002528.s007DOIFigure S7
https://doi.org/10.1371/journal.pgen.1002528.s008DOIFigure S8
https://doi.org/10.1371/journal.pgen.1002528.s009DOIFigure S9
https://doi.org/10.1371/journal.pgen.1002528.s010DOIFigure S10
https://doi.org/10.1371/journal.pgen.1002528.s011DOIFigure S11
https://doi.org/10.1371/journal.pgen.1002528.s012DOIFigure S12
https://doi.org/10.1371/journal.pgen.1002528.s013DOIFigure S13
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https://doi.org/10.1371/journal.pgen.1002528.s018DOIText S1
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. 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. 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. The authors have declared that no competing interests exist.
Funders:
Funding AgencyGrant Number
NIHR37 AI39115-14
NIHR01 AI50113-08
NIH5R01-AI063443-04 S1 Sub # 1-P30
Issue or Number:2
PubMed Central ID:PMC3280970
Record Number:CaltechAUTHORS:20200218-151248653
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200218-151248653
Official Citation:Findley K, Sun S, Fraser JA, Hsueh Y-P, Averette AF, Li W, 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. https://doi.org/10.1371/journal.pgen.1002528
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:101339
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:19 Feb 2020 19:45
Last Modified:19 Feb 2020 19:45

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