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Evolution of the Mating Type Locus: Insights Gained from the Dimorphic Primary Fungal Pathogens Histoplasma capsulatum, Coccidioides immitis, and Coccidioides posadasii ^,

School of Molecular and Microbial Sciences, University of Queensland, Brisbane, QLD 4072, Australia,¹ Department of Plant and Microbial Biology, University of California, Berkeley, California 94720,² Department of Biology, University of Texas at San Antonio, San Antonio, Texas 78249,³ Department of Microbiology and Immunology, University of California, San Francisco, California 94143,⁴ Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina 27710⁵

Received 17 January 2007/ Accepted 14 February 2007

Sexual reproduction of fungi is governed by the mating type (MAT) locus, a specialized region of the genome encoding key transcriptional regulators that direct regulatory networks to specify cell identity and fate. Knowledge of MAT locus structure and evolution has been considerably advanced in recent years as a result of genomic analyses that enable the definition of MAT locus sequences in many species as well as provide an understanding of the evolutionary plasticity of this unique region of the genome. Here, we extend this analysis to define the mating type locus of three dimorphic primary human fungal pathogens, Histoplasma capsulatum, Coccidioides immitis, and Coccidioides posadasii, using genomic analysis, direct sequencing, and bioinformatics. These studies provide evidence that all three species possess heterothallic bipolar mating type systems, with isolates encoding either a high-mobility-group (HMG) domain or an -box transcriptional regulator. These genes are intact in all loci examined and have not been subject to loss or decay, providing evidence that the loss of fertility upon passage in H. capsulatum is not attributable to mutations at the MAT locus. These findings also suggest that an extant sexual cycle remains to be defined in both Coccidioides species, in accord with population genetic evidence. Based on these MAT sequences, a facile PCR test was developed that allows the mating type to be rapidly ascertained. Finally, these studies highlight the evolutionary forces shaping the MAT locus, revealing examples in which flanking genes have been inverted or subsumed and incorporated into an expanding MAT locus, allowing us to propose an expanded model for the evolution of the MAT locus in the phylum Ascomycota.

Published ahead of print on 2 March 2007.

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

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