Evolution of the gene encoding mitochondrial intermediate peptidase and its cosegregation with the A mating-type locus of mushroom fungi

James, Timothy Y.; Kües, Ursula; Rehner, Stephen A.; Vilgalys, Rytas

doi:10.1016/j.fgb.2003.11.008

Cited by 52 publications

(58 citation statements)

References 38 publications

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“…We have previously used PCR to amplify and genotype a small fragment of MIP from C. disseminatus, and we demonstrated that the MIP gene fragment cosegregates with the mating-type locus of C. disseminatus, using a small progeny array ( James et al 2004a). PCR primers specific to the four STE3-like sequences were designed to test whether these putative pheromone receptors also cosegregated with the mating-type locus.…”

Section: Resultsmentioning

confidence: 99%

“…To study homologs of the putative B mating-type genes, we used degenerate PCR primers to amplify STE3-like pheromone receptors from homokaryotic strains following standard PCR protocols ( James et al 2004a). Primers br1-F and br1-1R were used to amplify two receptors each from C345.1 and TJ01/19.2; in addition, we used primers br2-F and br2-2R to amplify a small STE3-like fragment from strain TJ01/19.2 (see James et al 2004b for primer sequences).…”

Section: Methodsmentioning

confidence: 99%

“…Cosegregation analyses: We previously studied the cosegregation of MIP and mating type among 13 single-spore progeny of field collection TJ00/38 ( James et al 2004a). This same progeny array was used to determine whether the STE3-like pheromone receptors (CDSTE3.1, CDSTE3.2, and CDSTE3.3) also cosegregate with mating type.…”

Section: Methodsmentioning

confidence: 99%

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Evolution of the Bipolar Mating System of the Mushroom Coprinellus disseminatus From Its Tetrapolar Ancestors Involves Loss of Mating-Type-Specific Pheromone Receptor Function

et al. 2006

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Mating incompatibility in mushroom fungi is controlled by the mating-type loci. In tetrapolar species, two unlinked mating-type loci exist (A and B), whereas in bipolar species there is only one locus. The A and B mating-type loci encode homeodomain transcription factors and pheromones and pheromone receptors, respectively. Most mushroom species have a tetrapolar mating system, but numerous transitions to bipolar mating systems have occurred. Here we determined the genes controlling mating type in the bipolar mushroom Coprinellus disseminatus. Through positional cloning and degenerate PCR, we sequenced both the transcription factor and pheromone receptor mating-type gene homologs from C. disseminatus. Only the transcription factor genes segregate with mating type, discounting the hypothesis of genetic linkage between the A and B mating-type loci as the causal origin of bipolar mating behavior. The mating-type locus of C. disseminatus is similar to the A mating-type locus of the model species Coprinopsis cinerea and encodes two tightly linked pairs of homeodomain transcription factor genes. When transformed into C. cinerea, the C. disseminatus A and B homologs elicited sexual reactions like native matingtype genes. Although mating type in C. disseminatus is controlled by only the transcription factor genes, cellular functions appear to be conserved for both groups of genes. M ATING in fungi is controlled by the loci that determine the mating type of an individual, and only individuals with differing mating types can mate. Basidiomycete fungi have evolved a unique mating system, termed tetrapolar or bifactorial incompatibility, in which mating type is determined by two unlinked loci; compatibility at both loci is required for mating to occur. The origin of the tetrapolar mating system in the basidiomycetes is likely to be ancient since it is observed in at least two of the three major lineages, the Ustilaginomycetes, or smut fungi, and the Hymenomycetes, primarily the mushroom fungi (Burnett 1975). Also unique to the basidiomycetes is the presence of multiple alleles at the mating-type loci that allows most individuals within a population to be mating compatible with one another. Only the mushroom-forming homobasidiomycetes possess large allelic series at both loci, typically termed the A and B mating-type loci (Whitehouse 1949;Raper 1966).The multiallelic tetrapolar mating system is considered to be a novel innovation that could have only evolved once (Raper 1966;Raper and Flexer 1971). For this reason, the ancestor of the homobasidiomycetes is accepted as having a tetrapolar mating system. Although most (65%) of the homobasidiomycetes possess a tetrapolar mating system, many species (25%) instead have a bipolar system controlled by a single locus with multiple alleles (Raper 1966). The distribution of bipolar species is scattered throughout the homobasidiomycete phylogeny, and bipolar species appear to have multiple independent origins from tetrapolar mating systems (Hibbett and Donoghue 2001). The popul...

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Evolution of the Bipolar Mating System of the Mushroom Coprinellus disseminatus From Its Tetrapolar Ancestors Involves Loss of Mating-Type-Specific Pheromone Receptor Function

et al. 2006

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“…Characterization of the A mating locus in M. roreri shows that both A mating genes (HD1 and HD2) are tightly linked and oppositely transcribed (Figure 1a), an orientation typical in other Agaricales (James, 2007). The annotation of the surrounding areas of the A locus revealed the syntenic genes MIP and βFG, which are largely known to directly flank the A mating locus in most Agaricales (James et al, 2004a;James, 2007;Niculita-Hirzel et al, 2008). However, in M. roreri, MIP and βFG are much more distant from the A locus, being~40 and 60 Kb upstream of HD1 and HD2, respectively ( Figure 1a).…”

Section: Microsatellite Analysismentioning

confidence: 99%

The cacao pathogen Moniliophthora roreri (Marasmiaceae) possesses biallelic A and B mating loci but reproduces clonally

Díaz-Valderrama

Aime

2016

Heredity

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The cacao pathogen Moniliophthora roreri belongs to the mushroom-forming family Marasmiaceae, but it has never been observed to produce a fruiting body, which calls to question its capacity for sexual reproduction. In this study, we identified potential A (HD1 and HD2) and B (pheromone precursors and pheromone receptors) mating genes in M. roreri. A PCR-based method was subsequently devised to determine the mating type for a set of 47 isolates from across the geographic range of the fungus. We developed and generated an 11-marker microsatellite set and conducted association and linkage disequilibrium (standardized index of association, I A s ) analyses. We also performed an ancestral reconstruction analysis to show that the ancestor of M. roreri is predicted to be heterothallic and tetrapolar, which together with sliding window analyses support that the A and B mating loci are likely unlinked and follow a tetrapolar organization within the genome. The A locus is composed of a pair of HD1 and HD2 genes, whereas the B locus consists of a paired pheromone precursor, Mr_Ph4, and receptor, STE3_Mr4. Two A and B alleles but only two mating types were identified. Association analyses divided isolates into two well-defined genetically distinct groups that correlate with their mating type; I A s values show high linkage disequilibrium as is expected in clonal reproduction. Interestingly, both mating types were found in South American isolates but only one mating type was found in Central American isolates, supporting a prior hypothesis of clonal dissemination throughout Central America after a single or very few introductions of the fungus from South America.

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“…This makes cloning based on sequence similarity of the few reported sexM and sexP homologs a challenge. The MAT loci of both basidiomycetes and ascomycetes have conserved genes on either side of the idiomorphic regions, and those flanks can be used as the primary targets for identifying full mating-type loci (6,22,23). Alignments of the predicted amino acids encoded by the tptA and rnhA genes of the three available Mucoromycotina species were made, and degenerate oligonucleotides were designed.…”

Section: Resultsmentioning

confidence: 99%

Sex Determination in the First-Described Sexual Fungus

Idnurm

2011

Eukaryot Cell

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The original report of sex in fungi dates 2 centuries ago to the species Syzygites megalocarpus (Mucoromycotina). The organism was subsequently used in 1904 to represent self-fertile homothallic species when the concepts of heterothallism and homothallism were developed for the fungal kingdom. In this study, two putative sex/MAT loci were identified in individual strains of S. megalocarpus, accounting for its homothallic behavior. The strains encode both of the high-mobility-group domain-containing proteins, SexM and SexP, flanked by RNA helicase and glutathione oxidoreductase genes that are found adjacent to the mating-type loci in other Mucoromycotina species. The presence of pseudogenes and the arrangement of genes suggest that the origin of homothallism in this species is from a heterothallic relative, obtained via a chromosomal rearrangement to switch two alleles into two separated loci within a single genetic background. Similar events have given rise to homothallic species from heterothallic species in ascomycete fungi, demonstrating that conserved forces shape the evolution of sex determination and speciation in highly diverged fungi.In research on mating and the mechanisms of sex determination in the fungi, one species stands out for its contributions in this eukaryotic kingdom. Syzygites megalocarpus played two key roles (1). First, it was the species for which sex was first reported, in 1820 (10). Second, it was the main representative of the homothallic (or self-compatible, self-fertile) fungi used in the 1904 research that differentiated fungal species into those with the heterothallic (or self-incompatible, outcrossing) and those with the homothallic mode of reproduction (4).S. megalocarpus is a Mucoromycotina species (a zygomycete) found in the Northern Hemisphere growing as a parasite on mushrooms. As the first fungus in which sex was reported and probably due in part to the personal interactions between 19th century mycologists, S. megalocarpus was a commonly studied species for investigating sex in fungi. For instance, the name "zygospore" was coined by de Bary for those sexual structures of S. megalocarpus (9). Having been isolated and described on a number of independent occasions, the species and representative strains were also reassessed in the mid-1950s to clarify that this name had priority over an alternative name, Sporodinia grandis, that was in use (18).The fungi are a kingdom of eukaryotes closely related to the animal kingdom. They are one of the most species-rich groups on earth, with 90,000 described species and an estimated 1.5 million species in total (17). The kingdom is split into multiple lineages, with the ascomycetes and basidiomycetes (collectively, the monophyletic Dikarya) making up about 95% of species and being the best-studied members. The success of the fungi in generating such diversity and inhabiting a wide range of environments can be attributed to many aspects of their physiology, including the production of spores by either sexual or asexual processes. Both spor...

show abstract

Evolution of the gene encoding mitochondrial intermediate peptidase and its cosegregation with the A mating-type locus of mushroom fungi

Cited by 52 publications

References 38 publications

Evolution of the Bipolar Mating System of the Mushroom Coprinellus disseminatus From Its Tetrapolar Ancestors Involves Loss of Mating-Type-Specific Pheromone Receptor Function

Evolution of the Bipolar Mating System of the Mushroom Coprinellus disseminatus From Its Tetrapolar Ancestors Involves Loss of Mating-Type-Specific Pheromone Receptor Function

The cacao pathogen Moniliophthora roreri (Marasmiaceae) possesses biallelic A and B mating loci but reproduces clonally

Sex Determination in the First-Described Sexual Fungus

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