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Identification of the sex genes in an early diverged fungus

Abstract

Sex determination in fungi is controlled by a small, specialized region of the genome in contrast to the large sex-specific chromosomes of animals and some plants. Different gene combinations reside at these mating-type (MAT) loci and confer sexual identity; invariably they encode homeodomain, α-box, or high mobility group (HMG)-domain transcription factors1. So far, MAT loci have been characterized from a single monophyletic clade of fungi, the Dikarya (the ascomycetes and basidiomycetes)2, and the ancestral state and evolutionary history of these loci have remained a mystery. Mating in the basal members of the kingdom has been less well studied, and even their precise taxonomic inter-relationships are still obscure3,4. Here we apply bioinformatic and genetic mapping to identify the sex-determining (sex) region in Phycomyces blakesleeanus (Zygomycota), which represents an early branch within the fungi. Each sex allele contains a single gene that encodes an HMG-domain protein, implicating the HMG-domain proteins as an earlier form of fungal MAT loci. Additionally, one allele also contains a copy of a unique, chromosome-specific repetitive element, suggesting a generalized mechanism for the earliest steps in the evolution of sex determination and sex chromosome structure in eukaryotes.

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Figure 1: Structure of the sex locus of Phycomyces blakesleeanus.
Figure 2: Heterozygosity at the sex locus promotes a partially self-fertile phenotype.
Figure 3: Sex co-segregates with sexM and sexP genes encoding HMG-domain proteins.
Figure 4: Recombination around the sex locus and presence of chromosome-specific repetitive elements.

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Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

DNA sequences for the reported genes have been deposited at GenBank under accessions EU009461 and EU009462.

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Acknowledgements

We acknowledge access to the Phycomyces genome project: these sequence data were produced by the US Department of Energy Joint Genome Institute. We thank L. Corrochano and A. Eslava for encouragement and providing Phycomyces strains, and L. Corrochano and X. Lin for comments on the manuscript. This research was supported by National Institutes of Health grants to J.H.

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Correspondence to Joseph Heitman.

Supplementary information

Supplementary Information

This file contains Supplementary Discussion; Supplementary Figures S1-S5 with Legends; Supplementary Tables S1-S2; Supplementary Methods and additional references. This file includes additional discussion on the identification of sex in a zygomycete fungus and its implications to the evolution of mating type in other fungi, five figures expanding on data mentioned in the main text and a model, two tables describing strains and oligonucleotide primers used, and the Methods section. (PDF 4106 kb)

Supplementary Data

This file contains Supplementary Data including allele designations of molecular markers scored from progeny of three genetic crosses of Phycomyces. (PDF 79 kb)

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Idnurm, A., Walton, F., Floyd, A. et al. Identification of the sex genes in an early diverged fungus. Nature 451, 193–196 (2008). https://doi.org/10.1038/nature06453

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