Sex in the Mucoralean fungi

Abstract

Sexual development is extant in virtually all eukaryotic species, including throughout the kingdom Fungi. Positioned within the opisthokonts along with metazoans, fungi serve as model systems to elucidate the genetics and impact of sexual development. Basal fungal lineages such as the Mucoralean fungi provide a unique basis to study sexual reproduction, in which common ancestral traits found in both animal and fungal lineages may be conserved. This review discusses the sexual development, sex loci, and evolution of the sex locus in the Mucoralean fungi, which sheds light on our understanding of the evolution and functions of sex.

Keywords: HMG; evolution of sex; evolution of sex chromosome; sex locus; sexual development; trisporic acid.

Figure 1

Scanning electron microscopic image of a zygospore of Mucor circinelloides. A zygospore was formed when the strains NRRL3631(+) and CBS277.49(-) were co-cultured on YPD media for 2 weeks at room temperature in the dark. Scale= 10 μm.

Figure 2

sex loci of Mucorales fungi. The sex loci from four different Mucorales fungi are depicted. The (+) sex loci encode sexP gene; (-) sex loci encode the sexM gene, both of which are flanked by conserved tptA and rnhA genes. Noteworthy features are 1) the direction of transcription of the sexP and sexM genes differs in each species; 2) the presence of a repetitive element in the P. blakesleeanus (+) sex locus; 3) the presence of an additional ORF (arbA, encoding an ankyrin-RCC1-BTB-POZ domain protein) in the R. oryzae (+) and S. megalocarpus (-) sex loci; and 4) a partial gene inversion in the rnhA gene of S. megalocarpus. The tptA gene in S. megalocarpus has yet to be sequenced (indicated by dotted outline). Grey boxes indicate the sex locus and gene sizes are not to scale. (B) The sex locus of M. circinelloides f. griseocyanus (Mcg) includes the promoters of the tptA and rnhA genes but the sex loci of M. circinelloides f. circinelloides (Mcc) and M. circinelloides f. lusitanicus (Mcl) include the promoter of the tptA gene but not of the rnhA gene. Grey boxes indicate the sex locus.

Figure 3

Early steps in sex chromosome evolution. The Mucorales sex locus supports the hypothesis posited by Ohno [34]: a key transcription factor for sex arises on an autosome and one allele undergoes gene inversion followed by gene divergence resulting in divergent alleles (P. blakesleeanus sex locus) (upper). A repetitive element is integrated at the sex locus and elsewhere on the same chromosome (P. blakesleeanus sex locus). The multiple copies of the repetitive element sequence provide templates for recombination and inversion and thereby facilitate the expansion of the sex locus to form a proto-sex chromosome (sex loci of P. blakesleeanus, R. oryzae, and S. megalocarpus). However, allelic sex genes in the same orientation could be an ancestral form, and therefore gene inversion might follow gene divergence (M. circinelloides sex locus) (lower).