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

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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, SXI2 a) 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.

          Author Summary

          Fungal gene clusters mediate sex determination, natural product synthesis, and metabolic functions. Eukaryotic organisms share features of gene cluster formation including translocations, inversions, gene conversion, and suppressed recombination. The C. neoformans/ C. gattii mating-type ( MAT) locus spans a single >100 kb gene cluster encoding >20 genes, many involved in sex. We examined MAT gene cluster evolution in model and pathogenic Cryptococcus species. MAT was characterized from two closely related species, T. wingfieldii and C. amylolentus, and is organized into two unlinked gene clusters on different chromosomes. MAT organization in these species provides insight into evolutionary transitions from tetrapolar to bipolar mating systems involving fusion of physically unlinked sex-determinants into one contiguous region. These sex determination transitions occurred concomitantly with the origin of the pathogenic species complex from the last common ancestor shared with tetrapolar non-pathogenic species. We discovered a tetrapolar sexual cycle in C. amylolentus that generates recombinant meiotic progeny, many of which are infertile. Fertile progeny are biased towards one parental mating-type (A1B1) and may be an evolutionary precursor to unisexual mating of the closely related pathogenic species. This study reveals factors orchestrating gene cluster formation and sex chromosome evolution in fungi, including features shared with animals and plants.

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          Most cited references 58

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          Consed: a graphical tool for sequence finishing.

          Sequencing of large clones or small genomes is generally done by the shotgun approach (Anderson et al. 1982). This has two phases: (1) a shotgun phase in which a number of reads are generated from random subclones and assembled into contigs, followed by (2) a directed, or finishing phase in which the assembly is inspected for correctness and for various kinds of data anomalies (such as contaminant reads, unremoved vector sequence, and chimeric or deleted reads), additional data are collected to close gaps and resolve low quality regions, and editing is performed to correct assembly or base-calling errors. Finishing is currently a bottleneck in large-scale sequencing efforts, and throughput gains will depend both on reducing the need for human intervention and making it as efficient as possible. We have developed a finishing tool, consed, which attempts to implement these principles. A distinguishing feature relative to other programs is the use of error probabilities from our programs phred and phrap as an objective criterion to guide the entire finishing process. More information is available at http:// www.genome.washington.edu/consed/consed. html.
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            Sex Chromosomes and Sex-Linked Genes

             Susumu Ohno (1967)
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              Sexual reproduction between partners of the same mating type in Cryptococcus neoformans.

              Cryptococcus neoformans is a globally distributed human fungal pathogen that causes life-threatening meningoencephalitis in immunocompromised patients. It has a defined sexual cycle involving haploid cells of alpha and a mating types, yet the vast majority of environmental and clinical isolates are alpha (ref. 3). Sexual recombination is normally expected to occur between isolates of opposite mating type in organisms with two mating types (or sexes). How sexual reproductive potential can be maintained in an organism with a largely unisexual, nearly clonal population genetic structure is unknown. One clue, however, is that alpha strains undergo fruiting, a process that resembles sexual mating but is thought to be strictly mitotic and asexual. We report here that hallmarks of mating occur during fruiting, including diploidization and meiosis. Pheromone response pathway elements and the key meiotic regulator Dmc1 are required for efficient fruiting. Furthermore, fusion and meiosis can occur between non-isogenic alpha strains, enabling genetic exchange. These studies reveal how sexual reproduction can occur between partners of the same mating type. These findings have implications for the evolution of microbial pathogens, as well as for parthenogenesis, cell fusion events and transitions between self-fertilizing and outcrossing modes of reproduction observed in both fungi and other kingdoms.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, USA )
                1553-7390
                1553-7404
                February 2012
                February 2012
                16 February 2012
                : 8
                : 2
                Affiliations
                [1 ]Genetics and Molecular Biology Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland, United States of America
                [2 ]Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, United States of America
                [3 ]School of Molecular and Microbial Sciences, University of Queensland, Brisbane, Australia
                [4 ]Division of Biology, California Institute of Technology, Pasadena, California, United States of America
                University of California San Francisco, United States of America
                Author notes

                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.

                Article
                PGENETICS-D-11-01918
                10.1371/journal.pgen.1002528
                3280970
                22359516
                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.
                Page count
                Pages: 19
                Categories
                Research Article
                Biology
                Evolutionary Biology
                Microbiology
                Mycology

                Genetics

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