Asymmetry in Sexual Pheromones Is Not Required for Ascomycete Mating

Gonçalves-Sá, Joana; Murray, Andrew W.

doi:10.1016/j.cub.2011.06.054

Cited by 35 publications

(37 citation statements)

References 40 publications

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“…In either case, when both partners secreted a-factor-like or ␣-factor-like pheromones, mating was observed. Although mating occurred with significantly reduced efficiency, this study suggests that the expression of two physically distinct pheromone types is not an absolute requirement for mating in Ascomycetes (103,269).…”

Section: Lipophilic Pheromones Are Common Among Fungimentioning

confidence: 93%

“…The issue of why Ascomycetes of opposite mating types produce two distinct types of pheromones, one lipid soluble like a-factor and the other water soluble like ␣-factor, is not understood (38,51,103,269). This comes at some cost, as cells must express unique and complex processing machinery for the production of each pheromone.…”

Section: Lipophilic Pheromones Are Common Among Fungimentioning

confidence: 99%

“…It is of interest that in a recent study, S. cerevisiae was "reprogrammed" to generate exclusively lipid-modified pheromones or hydrophilic pheromones and their cognate receptors, rather than one of each (103). In either case, when both partners secreted a-factor-like or ␣-factor-like pheromones, mating was observed.…”

Section: Lipophilic Pheromones Are Common Among Fungimentioning

confidence: 99%

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Biogenesis of the Saccharomyces cerevisiae Pheromone a -Factor, from Yeast Mating to Human Disease

Michaelis¹,

Barrowman²

2012

Microbiol Mol Biol Rev

101

106

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SUMMARY The mating pheromone a -factor secreted by Saccharomyces cerevisiae is a farnesylated and carboxylmethylated peptide and is unusually hydrophobic compared to other extracellular signaling molecules. Mature a -factor is derived from a precursor with a C-terminal CAAX motif that directs a series of posttranslational reactions, including prenylation, endoproteolysis, and carboxylmethylation. Historically, a -factor has served as a valuable model for the discovery and functional analysis of CAAX-processing enzymes. In this review, we discuss the three modules comprising the a -factor biogenesis pathway: (i) the C-terminal CAAX-processing steps carried out by Ram1/Ram2, Ste24 or Rce1, and Ste14; (ii) two sequential N-terminal cleavage steps, mediated by Ste24 and Axl1; and (iii) export by a nonclassical mechanism, mediated by the ATP binding cassette (ABC) transporter Ste6. The small size and hydrophobicity of a -factor present both challenges and advantages for biochemical analysis, as discussed here. The enzymes involved in a -factor biogenesis are conserved from yeasts to mammals. Notably, studies of the zinc metalloprotease Ste24 in S. cerevisiae led to the discovery of its mammalian homolog ZMPSTE24, which cleaves the prenylated C-terminal tail of the nuclear scaffold protein lamin A. Mutations that alter ZMPSTE24 processing of lamin A in humans cause the premature-aging disease progeria and related progeroid disorders. Intriguingly, recent evidence suggests that the entire a -factor pathway, including all three biogenesis modules, may be used to produce a prenylated, secreted signaling molecule involved in germ cell migration in Drosophila . Thus, additional prenylated signaling molecules resembling a -factor, with as-yet-unknown roles in metazoan biology, may await discovery.

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Section: Lipophilic Pheromones Are Common Among Fungimentioning

confidence: 93%

Section: Lipophilic Pheromones Are Common Among Fungimentioning

confidence: 99%

Section: Lipophilic Pheromones Are Common Among Fungimentioning

confidence: 99%

See 1 more Smart Citation

Biogenesis of the Saccharomyces cerevisiae Pheromone a -Factor, from Yeast Mating to Human Disease

Michaelis¹,

Barrowman²

2012

Microbiol Mol Biol Rev

101

106

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“…The Basidiomycete bifactorial mating-type system, with PR and HD loci, shows remarkable similarities with some species of the Saccharomycotina and Taphrinomycotina, two basal groups of the Ascomycota, which have homeodomain genes at one of the mating-type idiomorphs (Idnurm et al, 2008) and one pheromone/receptor system comparable to the Basidiomycete PR system (Coppin et al, 1997;Fowler et al, 1999;Gonc¸alves-Sá and Murray, 2011). The alternative idiomorph present in these Ascomycotina and basal Mucoromycotina (of the HMG type; Dyer, 2008;Idnurm et al, 2008) was most likely lost early in the Basidiomycete lineage (Dyer, 2008;Kües et al, 2011).…”

Section: Genomic Changesmentioning

confidence: 99%

Evolution of uni- and bifactorial sexual compatibility systems in fungi

Nieuwenhuis¹,

Billiard²,

Vuilleumier³

et al. 2013

Heredity

129

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Mating systems, that is, whether organisms give rise to progeny by selfing, inbreeding or outcrossing, strongly affect important ecological and evolutionary processes. Large variations in mating systems exist in fungi, allowing the study of their origin and consequences. In fungi, sexual incompatibility is determined by molecular recognition mechanisms, controlled by a single mating-type locus in most unifactorial fungi. In Basidiomycete fungi, however, which include rusts, smuts and mushrooms, a system has evolved in which incompatibility is controlled by two unlinked loci. This bifactorial system probably evolved from a unifactorial system. Multiple independent transitions back to a unifactorial system occurred. It is still unclear what force drove evolution and maintenance of these contrasting inheritance patterns that determine mating compatibility. Here, we give an overview of the evolutionary factors that might have driven the evolution of bifactoriality from a unifactorial system and the transitions back to unifactoriality. Bifactoriality most likely evolved for selfing avoidance. Subsequently, multiallelism at matingtype loci evolved through negative frequency-dependent selection by increasing the chance to find a compatible mate. Unifactoriality then evolved back in some species, possibly because either selfing was favoured or for increasing the chance to find a compatible mate in species with few alleles. Owing to the existence of closely related unifactorial and bifactorial species and the increasing knowledge of the genetic systems of the different mechanisms, Basidiomycetes provide an excellent model for studying the different forces that shape breeding systems.

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“…The bioassay for a-factor production was modified from Gonçalves-Sá and Murray (2011). For details see File S1.…”

Section: Bioassay For A-factor Productionmentioning

confidence: 99%

Genetically Engineered Transvestites Reveal Novel Mating Genes in Budding Yeast

Huberman

Murray

2013

Genetics

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Haploid budding yeast has two mating types, defined by the alleles of the MAT locus, MATa and MATa. Two haploid cells of opposite mating types mate by signaling to each other using reciprocal pheromones and receptors, polarizing and growing toward each other, and eventually fusing to form a single diploid cell. The pheromones and receptors are necessary and sufficient to define a mating type, but other mating-type-specific proteins make mating more efficient. We examined the role of these proteins by genetically engineering "transvestite" cells that swap the pheromone, pheromone receptor, and pheromone processing factors of one mating type for another. These cells mate with each other, but their mating is inefficient. By characterizing their mating defects and examining their transcriptomes, we found Afb1 (a-factor barrier), a novel MATa-specific protein that interferes with a-factor, the pheromone secreted by MATa cells. Strong pheromone secretion is essential for efficient mating, and the weak mating of transvestites can be improved by boosting their pheromone production. Synthetic biology can characterize the factors that control efficiency in biological processes. In yeast, selection for increased mating efficiency is likely to have continually boosted pheromone levels and the ability to discriminate between partners who make more and less pheromone. This discrimination comes at a cost: weak mating in situations where all potential partners make less pheromone. BIOLOGICAL processes are typically defined by the genes that are necessary and sufficient for function. However, in many cases, this minimal gene set does not encompass all the proteins involved in a process, and additional proteins promote biological efficiency. Finding these additional proteins may require the detection of subtle phenotypes, making it hard to know if all the genes involved in a process have been identified. One way to answer this question is to reengineer a pathway and ask whether the synthetic version fully mimics the natural function. Here, we show that this form of synthetic biology illuminates how cells of the budding yeast Saccharomyces cerevisiae mate efficiently.Budding yeast can be stably maintained as haploids or diploids. Haploids mate when two cells of opposite mating types signal to each other using reciprocal pheromones and receptors, polarize and grow toward each other, and eventually fuse to form a single diploid. Yeast has two mating types, a and a ( Figure 1A), determined by two alternative alleles at the MAT locus, MATa and MATa, which encode different transcription factors (Herskowitz 1988). These factors regulate the expression of mating-type-specific genes, many of which are involved with the production and detection of the pheromones that yeast cells use to signal to one another. The pheromones (a-and a-factor) are detected by G-proteincoupled receptors. MATa cells express a-factor (Betz and Duntze 1979), which is secreted through an ATP binding cassette transporter (Ste6) (McGrath and Varshavsky 1989)...

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Asymmetry in Sexual Pheromones Is Not Required for Ascomycete Mating

Cited by 35 publications

References 40 publications

Biogenesis of the Saccharomyces cerevisiae Pheromone a -Factor, from Yeast Mating to Human Disease

Biogenesis of the Saccharomyces cerevisiae Pheromone a -Factor, from Yeast Mating to Human Disease

Evolution of uni- and bifactorial sexual compatibility systems in fungi

Genetically Engineered Transvestites Reveal Novel Mating Genes in Budding Yeast

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