Chapter 8 : Fungal Sex: The Mucoromycota

A tree of the fungal kingdom. The previous phylum Zygomycota is polyphyletic and further classified into two phyla, according to Spatafora et al. ( 1 ). The phylum Mucoromycota includes the classes Mucoromycotina, Mortierellomycotina, and Glomeromycotina, and the phylum Zoopagomycota includes the classes Entomophthoromycotina, Zoopagomycotina, and Kickxellomycotina.

Images of the sexual zygospores produced by species in the order Mucorales. (A) Three remnants of zygospores of P. blakesleeanus isolated from an environmental sample from Florida, 2014. The long ribbon structures are desiccated asexual sporangiophores. When two mating types of M. circinelloides are cocultured in dark conditions, zygospores are formed. (B) Light microscopy of two zygospores of M. circinelloides and (C) scanning electron micrograph of an M. circinelloides zygospore.

Alignments of genes within or adjacent to the MAT/sex loci in species of Mucorales, arbuscular mycorrhizal fungi, and microsporidia. Genes encoding allelic or idiomorphic HMG transcription factors, SexP and SexM in (+) and (–) mating types, are flanked by genes encoding a putative triose phosphate transporter (TptA) and RNA helicase (RnhA). This gene cluster is commonly found in the sex locus of Mucorales. Although the gene synteny for TptA-SexP/M-RnhA is conserved, notable differences exist. Examples include differences in the direction of the sexP and/or tptA genes and in the integration of an additional open reading frame or repetitive element, and a level of expansion of the idiomorphic region, which implies expansion of the sex locus. Interestingly, microsporidian genomes contain a similar gene cluster for TptA/HMG/RnhA, which might be involved in sexual reproduction of these obligate intracellular eukaryotic pathogens. In the AMF R. irregularis, the homologous genes encoding TptA, HMG, and RNA helicase are found, although they are less likely to be linked as is seen in the sex locus of Mucorales. In addition, an HD1-like/HD2 gene cluster is encoded in the R. irregularis genome, and the two genes are divergently transcribed, which may represent a basidiomycete MAT locus-like sex locus, with divergently transcribed HD1/HD2 gene pairs.

Diagram comparing pheromone processing steps in the Mucorales and the Oomycetes. Synthesis of β-carotene is an important step for production of trisporic acid, and two enzymes, CarB and CarRA, are among the enzymes known to be involved in this process. Synthesis of trisporic acid is initiated by enzymatic cleavage of β-carotene, which involves enzymes such as CarS, Tsp3, and AcaA. Remarkably, the intermediate products after β-carotene cleavage must be exchanged between cells of the two mating types to complete trisporic acid synthesis. For example, the 4-dihydromethyl trisporate in (+) mating type cells is delivered into (–) mating type cells and is converted by Tsp1 into methyl trisporate, and this is then further converted into trisporic acid. Two intermediate compounds, trisporin and trisporol in (–) mating type cells, are transferred into (+) mating cells and are finally converted into trisporic acid. Sex hormone synthesis in the Oomycete Phytophthora species is analogous to the inter-mating type collaboration to produce sexual pheromone trisporic acid in Mucorales. The α2 hormone is a sex hormone in the A2 mating type, and it is produced from phytol provided by plants. The α2 hormone, then, must be delivered into A1 mating type cells, where it serves as a precursor of α1 hormone synthesis.