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Eukaryotic Cell, October 2008, p. 1847-1855, Vol. 7, No. 10
1535-9778/08/$08.00+0     doi:10.1128/EC.00271-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Transitions in Sexuality: Recapitulation of an Ancestral Tri- and Tetrapolar Mating System in Cryptococcus neoformans{triangledown} ,{dagger}

Yen-Ping Hsueh, James A. Fraser,{ddagger} and Joseph Heitman*

Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina 27710

Received 11 August 2008/ Accepted 12 August 2008

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/{alpha}) 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 SXI1{alpha} 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.

* Corresponding author. Mailing address: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710. Phone: (919) 684-2824. Fax: (919) 681-8984. E-mail: heitm001{at}duke.edu

{triangledown} Published ahead of print on 22 August 2008.

{dagger} Supplemental material for this article may be found at http://ec.asm.org/.

{ddagger} Current address: Molecular and Microbial Sciences, University of Queensland, Brisbane, Australia.

Eukaryotic Cell, October 2008, p. 1847-1855, Vol. 7, No. 10
1535-9778/08/$08.00+0     doi:10.1128/EC.00271-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.





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