Structural Requirements for Activity of the Pheromones of Ustilago hordei

Kosted, Paula J.; Gerhardt, Shirley A.; Anderson, Cynthia M.; Stierle, Andrea A.; Sherwood, John E.

doi:10.1006/fgbi.2000.1191

Cited by 19 publications

(17 citation statements)

References 50 publications

(48 reference statements)

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“…For R. toruloides, the precursor gene encodes multiple copies of the pheromone, and an initial processing step is required to reveal C-terminal CAAX motifs for each (3,63). Other Basidiomycetes for which pheromones are known are Usitlago maydis (32,144,244,252), Usitlago hordei (6,145), Cryptococcus neoformans (72,177,189,243), Schizophyllum commune (92,267), Coprinus cinereus (38,52,197), and Sporisorium reilianium (235). For S. reilianium, at least 8 pheromone precursor genes have been identified, ranging in size from 10 to 74 residues, all encoding CAAX motifs.…”

Section: The Basidiomycetes Secrete Exclusively Hydrophobic (Prenylatmentioning

confidence: 99%

“…Notably, S. commune pheromone-receptor gene pairs have been expressed in S. cerevisiae and can substitute for the endogenous S. cerevisiae receptors and pheromones (92). Genetic and biochemical evidence supports the importance of prenylation for several Basidiomycete pheromones (145), and a few of these pheromones have been purified and/or synthesized to demonstrate their activity (6,144,197).…”

Section: The Basidiomycetes Secrete Exclusively Hydrophobic (Prenylatmentioning

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

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: The Basidiomycetes Secrete Exclusively Hydrophobic (Prenylatmentioning

confidence: 99%

Section: The Basidiomycetes Secrete Exclusively Hydrophobic (Prenylatmentioning

confidence: 99%

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

Michaelis¹,

Barrowman²

2012

Microbiol Mol Biol Rev

106

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“…Notably, no mutations C terminal to Y22 were found that block processing, suggesting that recognition is directed to the cut site itself and the N-terminal regions. It is notable that the lipophilic pheromones from several other fungi (Schizosaccharomyces pombe, Ustilago hordeii, and Cryptococcus neoformans) also have an Asn residue that immediately precedes the predicted mature pheromone sequence (23,26,36), suggesting that Asn may form part of a consensus sequence for fungal pheromone processing.…”

Section: Vol 5 2006 Biogenesis Of Yeast A-factor Mutants 1567mentioning

confidence: 99%

“…In Saccharomyces cerevisiae and other ascomycetes, the mating pheromones produced by the two mating types differ, in that one is an unmodified peptide, while the other is a prenylated and carboxymethylated peptide (i.e., ␣-factor and a-factor, respectively) (3,7,21,24,25,41,49,59,61,70). Basidomycetes, which can have two or even more mating types, encode exclusively the latter class of modified peptide pheromones (8,13,18,26,27,36,47,56,60). These pheromones are synthesized as precursors terminating in a C-terminal CAAX motif (where C is cysteine, A is usually aliphatic, and X is any residue).…”

mentioning

confidence: 99%

Saccharomyces cerevisiae a -Factor Mutants Reveal Residues Critical for Processing, Activity, and Export

et al. 2006

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The Saccharomyces cerevisiae mating pheromone a-factor provides a paradigm for understanding the biogenesis of prenylated fungal pheromones. The biogenesis of a-factor involves multiple steps: (i) C-terminal CAAX modification (where C is cysteine, A is aliphatic, and X is any residue) which includes prenylation, proteolysis, and carboxymethylation (by Ram1p/Ram2p, Ste24p or Rce1p, and Ste14p, respectively); (ii) N-terminal processing, involving two sequential proteolytic cleavages (by Ste24p and Axl1p); and (iii) nonclassical export (by Ste6p). Once exported, mature a-factor interacts with the Ste3p receptor on MAT␣ cells to stimulate mating. The a-factor biogenesis machinery is well defined, as is the CAAX motif that directs C-terminal modification; however, very little is known about the sequence determinants within a-factor required for N-terminal processing, activity, and export. Here we generated a large collection of a-factor mutants and identified residues critical for the N-terminal processing steps mediated by Ste24p and Axl1p. We also identified mutants that fail to support mating but do not affect biogenesis or export, suggesting a defective interaction with the Ste3p receptor. Mutants significantly impaired in export were also found, providing evidence that the Ste6p transporter recognizes sequence determinants as well as CAAX modifications. We also performed a phenotypic analysis of the entire set of isogenic a-factor biogenesis machinery mutants, which revealed information about the dependency of biogenesis steps upon one another, and demonstrated that export by Ste6p requires the completion of all processing events. Overall, this comprehensive analysis will provide a useful framework for the study of other fungal pheromones, as well as prenylated metazoan proteins involved in development and aging.Most fungi secrete pheromones that play important signaling roles in mating to stimulate cell and/or nuclear fusion. In Saccharomyces cerevisiae and other ascomycetes, the mating pheromones produced by the two mating types differ, in that one is an unmodified peptide, while the other is a prenylated and carboxymethylated peptide (i.e., ␣-factor and a-factor, respectively) (3,7,21,24,25,41,49,59,61,70). Basidomycetes, which can have two or even more mating types, encode exclusively the latter class of modified peptide pheromones (8,13,18,26,27,36,47,56,60). These pheromones are synthesized as precursors terminating in a C-terminal CAAX motif (where C is cysteine, A is usually aliphatic, and X is any residue). The S. cerevisiae pheromone a-factor is the best-characterized example of this class of fungal pheromones and provides a paradigm for understanding their biogenesis and secretion (14,20). Studies of a-factor have also yielded critical insights into the processing and properties of eukaryotic CAAX proteins in general, which include Ras and other small GTP-binding proteins, the ␥-subunits of heterotrimeric G proteins, and the nuclear lamins A and B (30,68,69).Components of the machinery required for th...

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“…The pheromone precursors of S. reilianum (Sr) were aligned to the respective pheromone precursors of U. maydis (Um) and U. hordei (Uh). The potential mature pheromone peptide sequences are in boldface (33,56). The processing sites of the S. reilianum pheromone precursors have not been verified.…”

Section: Vol 4 2005 Mating Type Loci Of S Reilianummentioning

confidence: 99%

Mating Type Loci of Sporisorium reilianum : Novel Pattern with Three a and Multiple b Specificities

et al. 2005

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Sporisorium reilianum and Ustilago maydis are two closely related smut fungi, which both infect maize but differ fundamentally in their mode of plant invasion and site of symptom development. As a prelude to studying the molecular basis of these differences, we have characterized the mating type loci of S. reilianum. S. reilianum has two unlinked mating type loci, a and b. Genes in both loci and adjacent regions show a high degree of synteny to the corresponding genes of U. maydis. The b locus occurs in at least five alleles and encodes two subunits of a heterodimeric homeodomain transcription factor, while the a locus encodes a pheromone/ receptor system. However, in contrast to that of U. maydis, the a locus of S. reilianum exists in three alleles containing two active pheromone genes each. The alleles of the a locus appear to have arisen through recent recombination events within the locus itself. This has created a situation where each pheromone is specific for recognition by only one mating partner.Sporisorium reilianum causes head smut in maize and sorghum (41,42). This soilborne pathogen infects the host plant at the seedling stage (25), supposedly through the roots (37). The infection is systemic, and disease symptoms become apparent only after the onset of flower development when the fungal sori replace male or female inflorescences. In its mode of colonizing the host, S. reilianum is fundamentally different from the well-studied close relative Ustilago maydis, which can infect maize plants via the leaves, stems, or flowers and rapidly causes the formation of prominent tumor-like structures on all green parts of the plant (18). For U. maydis the route of infection has been studied in detail. When haploid, yeast-like sporidia of different mating types recognize each other, they form conjugation hyphae that grow towards each other and fuse at their tips. The resulting dikaryon is filamentous and shows tip growth, leaving empty sections devoid of cytoplasm behind. On the plant surface the dikaryon differentiates into infection structures, so-called appressoria, which are characteristic swellings of the hyphal tips at the site of entry (9, 55). For S. reilianum a detailed molecular investigation of the infection process is lacking. However, it was demonstrated that haploid sporidia as well as germinated teliospores grow filamentously in the vicinity of the root (39). In an in vitro root infection system using germinated teliospores (37), roots were shown to be invaded by hyphae without the apparent formation of appressoria (37).In U. maydis the initial stages of the infection process are regulated by two unlinked mating type loci (23). The a locus exists in two alleles and encodes a pheromone/receptor system responsible for recognition of haploid sporidia. The lipopeptide pheromones Mfa1 and Mfa2 are secreted by sporidia of the opposite a mating type and are reciprocally detected through specific seven-transmembrane pheromone receptors (Pra2 and Pra1). After detection of the pheromone signal, the cells resp...

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Structural Requirements for Activity of the Pheromones of Ustilago hordei

Cited by 19 publications

References 50 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

Saccharomyces cerevisiae a -Factor Mutants Reveal Residues Critical for Processing, Activity, and Export

Mating Type Loci of Sporisorium reilianum : Novel Pattern with Three a and Multiple b Specificities

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