Structure, Function, and Phylogeny of the Mating Locus in the Rhizopus oryzae Complex

Department of Biology, Duke University, Durham, North Carolina, United States of America.
PLoS ONE (Impact Factor: 3.23). 12/2010; 5(12):e15273. DOI: 10.1371/journal.pone.0015273
Source: PubMed


The Rhizopus oryzae species complex is a group of zygomycete fungi that are common, cosmopolitan saprotrophs. Some strains are used beneficially for production of Asian fermented foods but they can also act as opportunistic human pathogens. Although R. oryzae reportedly has a heterothallic (+/-) mating system, most strains have not been observed to undergo sexual reproduction and the genetic structure of its mating locus has not been characterized. Here we report on the mating behavior and genetic structure of the mating locus for 54 isolates of the R. oryzae complex. All 54 strains have a mating locus similar in overall organization to Phycomyces blakesleeanus and Mucor circinelloides (Mucoromycotina, Zygomycota). In all of these fungi, the minus (-) allele features the SexM high mobility group (HMG) gene flanked by an RNA helicase gene and a TP transporter gene (TPT). Within the R. oryzae complex, the plus (+) mating allele includes an inserted region that codes for a BTB/POZ domain gene and the SexP HMG gene. Phylogenetic analyses of multiple genes, including the mating loci (HMG, TPT, RNA helicase), ITS1-5.8S-ITS2 rDNA, RPB2, and LDH genes, identified two distinct groups of strains. These correspond to previously described sibling species R. oryzae sensu stricto and R. delemar. Within each species, discordant gene phylogenies among multiple loci suggest an outcrossing population structure. The hypothesis of random-mating is also supported by a 50:50 ratio of plus and minus mating types in both cryptic species. When crossed with tester strains of the opposite mating type, most isolates of R. delemar failed to produce zygospores, while isolates of R. oryzae produced sterile zygospores. In spite of the reluctance of most strains to mate in vitro, the conserved sex locus structure and evidence for outcrossing suggest that a normal sexual cycle occurs in both species.

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Available from: Andrii Gryganskyi
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    • "This includes a myriad of species throughout the Ascomycota including S. cerevisiae (a and a), Schizosaccharomyces pombe (P and M), Candida albicans (a/a and a/a), Neurospora crassa (A and a), and Aspergillus fumigatus (MAT1-1 and MAT1-2) just to name a few (Glass et al., 1988; Hull et al., 2000; Magee and Magee, 2000; O'Gorman et al., 2009). In the Mucorales, we again find just two mating types, typically called P and M for plus (þ) and minus (À), in Phycomyces blakesleeanus , Mucor circinelloides, and Rhizopus oryzae (Gryganskyi et al., 2010; Idnurm et al., 2008; Lee et al., 2008). This is in marked contrast to the Basidiomycota branch of the dikarya in which a majority of species have the tetrapolar mating system configuration. "
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    ABSTRACT: Sexual reproduction is conserved throughout each supergroup within the eukaryotic tree of life, and therefore thought to have evolved once and to have been present in the last eukaryotic common ancestor (LECA). Given the antiquity of sex, there are features of sexual reproduction that are ancient and ancestral, and thus shared in diverse extant organisms. On the other hand, the vast evolutionary distance that separates any given extant species from the LECA necessarily implies that other features of sex will be derived. While most types of sex we are familiar with involve two opposite sexes or mating types, recent studies in the fungal kingdom have revealed novel and unusual patterns of sexual reproduction, including unisexual reproduction. In this mode of reproduction a single mating type can on its own undergo self-fertile/homothallic reproduction, either with itself or with other members of the population of the same mating type. Unisexual reproduction has arisen independently as a derived feature in several different lineages. That a myriad of different types of sex determination and sex determinants abound in animals, plants, protists, and fungi suggests that sex specification itself may not be ancestral and instead may be a derived trait. If so, then the original form of sexual reproduction may have been unisexual, onto which sexes were superimposed as a later feature. In this model, unisexual reproduction is both an ancestral and a derived trait. In this review, we consider what is new and what is old about sexual reproduction from the unique vantage point of the fungal kingdom.
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    • "The two sexes of P. blakesleeanus depend on specific allelomorphs , DNA sequences with little homology to each other that occupy the same place in linkage group V of the genome and behave in crosses as single allelic markers (Idnurm et al. 2008). The (þ) and (À) allelomorphs contain a gene, sexP and sexM, respectively, similar to those found in other Mucorales: Mucor circinelloides (Lee et al. 2008), Rhizopus oryzae (Gryganskyi et al. 2010), Syzygites megalocarpus (Idnurm 2011a), and Mucor mucedo (Wetzel et al. 2012). Gene sexM is necessary for mating, but not for vegetative growth in M. circinelloides (Li et al. 2011). "
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    • "It is worth mentioning that an ANK-containing gene has been also identified in the MAT idiomorph of Rhizopus oryzae, a species belonging to a basal group of fungi, the Mucorales [63]. However, this R. oryzae gene contains two additional domains (BTB and RCC1) that are not present in T. indicum Ti_orf3, suggesting that these two ANK-containing genes are not orthologs. "
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