Transitions in sexuality: recapitulation of an ancestral tri- and tetrapolar mating system in Cryptococcus neoformans

Hsueh, Yen-Ping, Fraser, James A. and Heitman, Joseph (2008) Transitions in sexuality: recapitulation of an ancestral tri- and tetrapolar mating system in Cryptococcus neoformans. Eukaryotic Cell, 7 10: 1847-1855. doi:10.1128/EC.00271-08


Author Hsueh, Yen-Ping
Fraser, James A.
Heitman, Joseph
Title Transitions in sexuality: recapitulation of an ancestral tri- and tetrapolar mating system in Cryptococcus neoformans
Formatted title
Transitions in sexuality: recapitulation of an ancestral tri- and tetrapolar mating system in Cryptococcus neoformans
Journal name Eukaryotic Cell   Check publisher's open access policy
ISSN 1535-9778
1535-9786
Publication date 2008-10-01
Year available 2008
Sub-type Article (original research)
DOI 10.1128/EC.00271-08
Open Access Status Not Open Access
Volume 7
Issue 10
Start page 1847
End page 1855
Total pages 9
Place of publication Washington, DC, United States
Publisher American Society for Microbiology
Language eng
Formatted abstract
Sex is orchestrated by the mating-type locus (MAT) in fungi and by sex chromosomes in plants and animals. In fungi, two patterns of sexuality occur: bipolar with a single, typically biallelic sex determinant that promotes inbreeding, and tetrapolar with two unlinked, often multiallelic sex determinants that restrict inbreeding. Multiallelism in either bipolar or tetrapolar mating systems promotes outcrossing. Cryptococcus neoformans is a pathogenic bipolar yeast with two unusually large MAT alleles (a/α) spanning >100 kb, ∼100-fold larger than many other fungal MAT loci. Based on comparative genomic analysis, this unusual MAT locus is hypothesized to have evolved from an ancestral tetrapolar system. In this model, the unlinked homeodomain (HD) transcription factor and pheromone/receptor tetrapolar loci acquired additional sex-related genes and then fused via chromosomal translocation, forming an intermediate transitional mating system (which we term tripolar), which then underwent recombination and gene conversion to fashion the extant bipolar MAT alleles. To experimentally validate this model, C. neoformans was engineered to have a tetrapolar mating system by relocating the MAT SXI1α and SXI2a HD genes to an unlinked genomic locale. Genetic and molecular analyses revealed that this modified organism could complete a tetrapolar sexual cycle. Analysis of progeny generated from bipolar, tripolar, and tetrapolar crosses provides direct experimental evidence that the tripolar state confers decreased fertility and therefore may represent an unstable evolutionary intermediate. These findings illustrate how transitions between outcrossing and inbreeding preference occur by involving sex determinant linkage and collapse from multiallelic to biallelic sex determination, providing insights into both fungal sex evolution and early steps in sex chromosome evolution.
Keyword Microbiology
Mycology
Microbiology
Mycology
MICROBIOLOGY
Q-Index Code C1
Q-Index Status Provisional Code
Grant ID AI50113
Institutional Status UQ

Document type: Journal Article
Sub-type: Article (original research)
Collection: School of Chemistry and Molecular Biosciences
 
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