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Fungal Sex: The Mucoromycota

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  • Authors: Soo Chan Lee1, Alexander Idnurm2
  • Editors: Joseph Heitman3, Neil A. R. Gow4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: South Texas Center for Emerging Infectious Diseases (STCEID), Department of Biology, University of Texas at San Antonio, San Antonio, TX 78249; 2: School of BioSciences, University of Melbourne, Parkville 3010 VIC, Australia; 3: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 4: School of Medical Sciences, University of Aberdeen, Fosterhill, Aberdeen, AB25 2ZD, United Kingdom
  • Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0041-2017
  • Received 04 January 2017 Accepted 06 January 2017 Published 23 March 2017
  • Alexander Idnurm, alexander.idnurm@unimelb.edu.au
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  • Abstract:

    Although at the level of resolution of genes and molecules most information about mating in fungi is from a single lineage, the Dikarya, many fundamental discoveries about mating in fungi have been made in the earlier branches of the fungi. These are nonmonophyletic groups that were once classified into the chytrids and zygomycetes. Few species in these lineages offer the potential of genetic tractability, thereby hampering the ability to identify the genes that underlie those fundamental insights. Research performed during the past decade has now established the genes required for mating type determination and pheromone synthesis in some species in the phylum Mucoromycota, especially in the order Mucorales. These findings provide striking parallels with the evolution of mating systems in the Dikarya fungi. Other discoveries in the Mucorales provide the first examples of sex-cell type identity being driven directly by a gene that confers mating type, a trait considered more of relevance to animal sex determination but difficult to investigate in animals. Despite these discoveries, there remains much to be gleaned about mating systems from these fungi.

  • Citation: Lee S, Idnurm A. 2017. Fungal Sex: The Mucoromycota. Microbiol Spectrum 5(2):FUNK-0041-2017. doi:10.1128/microbiolspec.FUNK-0041-2017.

Key Concept Ranking

Restriction Fragment Length Polymorphism
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/content/journal/microbiolspec/10.1128/microbiolspec.FUNK-0041-2017
2017-03-23
2017-09-24

Abstract:

Although at the level of resolution of genes and molecules most information about mating in fungi is from a single lineage, the Dikarya, many fundamental discoveries about mating in fungi have been made in the earlier branches of the fungi. These are nonmonophyletic groups that were once classified into the chytrids and zygomycetes. Few species in these lineages offer the potential of genetic tractability, thereby hampering the ability to identify the genes that underlie those fundamental insights. Research performed during the past decade has now established the genes required for mating type determination and pheromone synthesis in some species in the phylum Mucoromycota, especially in the order Mucorales. These findings provide striking parallels with the evolution of mating systems in the Dikarya fungi. Other discoveries in the Mucorales provide the first examples of sex-cell type identity being driven directly by a gene that confers mating type, a trait considered more of relevance to animal sex determination but difficult to investigate in animals. Despite these discoveries, there remains much to be gleaned about mating systems from these fungi.

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Image of FIGURE 1
FIGURE 1

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.

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0041-2017
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Image of FIGURE 2
FIGURE 2

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

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0041-2017
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Image of FIGURE 3
FIGURE 3

Alignments of genes within or adjacent to the / 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 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 and/or 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 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 , the homologous genes encoding TptA, HMG, and RNA helicase are found, although they are less likely to be linked as is seen in the locus of Mucorales. In addition, an HD1-like/HD2 gene cluster is encoded in the genome, and the two genes are divergently transcribed, which may represent a basidiomycete locus-like locus, with divergently transcribed HD1/HD2 gene pairs.

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0041-2017
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Image of FIGURE 4
FIGURE 4

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 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.

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0041-2017
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