scholarly journals The asymmetric chemical structures of two mating pheromones reflect their differential roles in conjugation of Schizosaccharomyces pombe

2019 ◽  
Author(s):  
Taisuke Seike ◽  
Hiromi Maekawa ◽  
Taro Nakamura ◽  
Chikashi Shimoda

AbstractIn the fission yeast Schizosaccharomyces pombe, the mating reaction is controlled by two mating pheromones, M-factor and P-factor, secreted by M- and P-type cells, respectively. M-factor is a C-terminally farnesylated lipid peptide, whereas P-factor is a simple peptide. To examine whether this chemical asymmetry in the two pheromones is essential for conjugation, we constructed a mating system in which either pheromone can stimulate both M- and P-cells, and examined whether the resulting autocrine strains can mate. Autocrine M-cells responding to M-factor successfully mated with P-factor-less P-cells, indicating that P-factor is not essential for conjugation; by contrast, autocrine P-cells responding to P-factor were unable to mate with M-factor-less M-cells. The sterility of the autocrine P-cells was completely recovered by expressing the M-factor receptor. These observations indicate that the different chemical characteristics of the two types of pheromone, a lipid and a simple peptide, are not essential; however, a lipid peptide is absolutely required for successful mating. Our findings allow us to propose a model of the differential roles of M-factor and P-factor in conjugation of S. pombe.Summary statementLipid pheromone peptides secreted locally from one cell may be concentrated at the fusion site with an opposite mating-type cell, which then polarizes to enable successful conjugation in S. pombe.

1995 ◽  
Vol 15 (9) ◽  
pp. 4964-4970 ◽  
Author(s):  
M Willer ◽  
L Hoffmann ◽  
U Styrkársdóttir ◽  
R Egel ◽  
J Davey ◽  
...  

The mat1 locus is a key regulator of both conjugation and meiosis in the fission yeast Schizosaccharomyces pombe. Two alternative DNA segments of this locus, mat1-P and mat1-M, specify the haploid cell types (Plus and Minus). Each segment includes two genes: mat1-P includes mat1-Pc and mat1-Pm, while mat1-M includes mat1-Mc and mat1-Mm. The mat1-Pc and mat1-Mc genes are responsible for establishing the pheromone communication system that mediates conjugation between P and M cells, while all four mat1 genes are required for meiosis in diploid P/M cells. Our understanding of the initiation of meiosis is based largely on indirect observations, and a more precise investigation of these events was required to define the interaction between the mat1 genes. Here we resolve this issue using synthetic pheromones and P/M strains with mutations in either mat1-Pc or mat1-Mc. Our results suggest a model in which the mat1 locus plays two roles in controlling meiosis. In the first instance, the mat1-Pc and mat1-Mc functions are required to produce the mating pheromones and receptors that allow the generation of a pheromone signal. This signal is required to induce the expression of mat1-Pm and mat1-Mm. This appears to be the major pheromone-dependent step in controlling meiosis since ectopic expression of these genes allows meiosis in the absence of mat1-Pc and mat1-Mc. The mat1-Pm and mat1-Mm products complete the initiation of meiosis by activating transcription of the mei3 gene.


1993 ◽  
Vol 13 (1) ◽  
pp. 80-88 ◽  
Author(s):  
K Tanaka ◽  
J Davey ◽  
Y Imai ◽  
M Yamamoto

A defect in the map3 gene of the fission yeast Schizosaccharomyces pombe causes h+ mating-type-specific sterility. This gene was cloned by complementation. Nucleotide sequence analysis showed that it has a coding capacity of 365 amino acids. The deduced map3 gene product is a putative seven-transmembrane protein and has 20.0% amino acid identity with the a-factor receptor of Saccharomyces cerevisiae, encoded by STE3. It is also homologous with the Ustilago maydis mating pheromone receptors. The map3 gene is expressed in h+ cells but not in h- cells, and the transcripts are induced in response to nitrogen starvation. h+ cells defective in map3 do not respond to purified M-factor. When map3 is expressed ectopically in h- cells, they apparently acquire the ability to respond to the M-factor produced by themselves. The gpa1 gene, which encodes the alpha-subunit of a G-protein presumed to couple with the mating pheromone receptors, is essential for this function of map3. These observations strongly suggest that map3 encodes the M-factor receptor. Furthermore, this study provides strong support for the notion that pheromone signaling is essential for initiation of meiosis in S. pombe and that either M-factor signaling or P-factor signaling alone is sufficient.


1994 ◽  
Vol 14 (6) ◽  
pp. 3895-3905
Author(s):  
S Kjaerulff ◽  
J Davey ◽  
O Nielsen

We previously identified two genes, mfm1 and mfm2, with the potential to encode the M-factor mating pheromone of the fission yeast Schizosaccharomyces pombe (J. Davey, EMBO J. 11:951-960, 1992), but further analysis revealed that a mutant strain lacking both genes still produced active M-factor. Here we describe the isolation and characterization of a third M-factor gene, mfm3. A mutant lacking all three genes fails to produce M-factor, indicating that all functional M-factor genes now have been identified. The triple mutant exhibits an absolute mating defect in M cells, a defect that is not rescued by addition of exogenous M-factor. A mutational analysis reveals that all three mfm genes contribute to the production of M-factor. Their transcription is limited to M cells and requires the mat1-Mc and ste11 gene products. Each gene is induced when the cells are starved of nitrogen and further induced by a pheromone signal. Additionally, the signal transduction machinery associated with the pheromone response is required for transcription of the mfm genes in both stimulated and unstimulated cells.


2003 ◽  
Vol 43 (4) ◽  
pp. 273-280 ◽  
Author(s):  
Anna L. Okorokova-Fa�anha ◽  
Lev A. Okorokov ◽  
Karl Ekwall

1989 ◽  
Vol 54 (1) ◽  
pp. 13-22 ◽  
Author(s):  
Stéphane Ronsseray ◽  
Monique Lehmann ◽  
Georges Periquet

SummaryM and M′ strains of Drosophila melanogaster in the P-M system of hybrid dysgenesis were compared in two series of tests, with the following results. (1) The singed-weak hypermutability regulation test showed that M′ strains had lower P excision rates than M strains, suggesting that P-elements repression must occur in M′ strains although it is not detectable by gonadal dysgenesis assays. (2) The evolution of mixed P + M and mixed P + M′ populations was compared, using a strong P strain. The P + M cultures invariably evolved in a few generations into strong P cultures, while the P + M′ cultures evolved into P-type cultures with reduced P-factor potentials. However, after 30 generations of culture, both these types of mixed cultures had similar P copy numbers, suggesting that regulation of copy number had occurred in them.


1994 ◽  
Vol 14 (1) ◽  
pp. 50-58
Author(s):  
H P Xu ◽  
M White ◽  
S Marcus ◽  
M Wigler

We have shown that the expression of mam2, the gene encoding the Schizosaccharomyces pombe P-factor pheromone receptor, is dependent upon components of the pheromone signal transduction pathway, including Ras1, Gpa1, Byr1 and Byr2, each of which is required for both conjugation and sporulation. Studies of the expression of mam2 in mutant S. pombe cells confirm previous conclusions, based on the ability of cells to sporulate, that the Byr1 protein kinase acts downstream of the Byr2 protein kinase and that both act downstream of Ras1, the S. pombe RAS homolog, and Gpa1, the G alpha component that mediates the occupancy of the mam2 receptor. In addition, our present studies show that Ras1 and Gpa1 each act downstream from the other and hence act in concert. The Spk1 kinase, which is required for conjugation and sporulation and which is a structural and functional homolog of the vertebrate MAP kinases, is not required for mam2 expression.


2021 ◽  
Author(s):  
Olivia Muriel ◽  
Laetitia Michon ◽  
Wanda Kukulski ◽  
Sophie G Martin

Cell-cell fusion is central to the process of fertilization for sexual reproduction. This necessitates the remodeling of peri-cellular matrix or cell wall material and the merging of plasma membranes. In walled fission yeast S. pombe, the fusion of P and M cells during sexual reproduction relies on the fusion focus, an actin structure that concentrates glucanase-containing secretory vesicles for local cell wall digestion necessary for membrane fusion. Here, we present a correlative light and electron microscopy (CLEM) quantitative study of a large dataset of 3D tomograms of the fusion site, which revealed the ultrastructure of the fusion focus as an actin-containing, vesicle-dense structure excluding other organelles. Unexpectedly, the data revealed asymmetries between the two gametes: M-cells exhibit a taut and convex plasma membrane that progressively protrudes into P-cells, which exhibit a more slack, wavy plasma membrane. These asymmetries are relaxed upon plasma membrane fusion, with observations of ramified pores that may result from multiple initiations or inhomogeneous expansion. We show that P-cells have a higher exo- to endocytosis ratio than M-cells, and that local reduction in exocytosis abrogates membrane waviness and compromises cell fusion significantly more in P- than M-cells. Reciprocally, reduction of turgor pressure specifically in M-cells prevents their protrusions into P-cells and delays cell fusion. Thus, asymmetric membrane conformations, which result from differential turgor pressure and exocytosis/endocytosis ratios between mating types, favor cell-cell fusion.


1993 ◽  
Vol 13 (1) ◽  
pp. 80-88
Author(s):  
K Tanaka ◽  
J Davey ◽  
Y Imai ◽  
M Yamamoto

A defect in the map3 gene of the fission yeast Schizosaccharomyces pombe causes h+ mating-type-specific sterility. This gene was cloned by complementation. Nucleotide sequence analysis showed that it has a coding capacity of 365 amino acids. The deduced map3 gene product is a putative seven-transmembrane protein and has 20.0% amino acid identity with the a-factor receptor of Saccharomyces cerevisiae, encoded by STE3. It is also homologous with the Ustilago maydis mating pheromone receptors. The map3 gene is expressed in h+ cells but not in h- cells, and the transcripts are induced in response to nitrogen starvation. h+ cells defective in map3 do not respond to purified M-factor. When map3 is expressed ectopically in h- cells, they apparently acquire the ability to respond to the M-factor produced by themselves. The gpa1 gene, which encodes the alpha-subunit of a G-protein presumed to couple with the mating pheromone receptors, is essential for this function of map3. These observations strongly suggest that map3 encodes the M-factor receptor. Furthermore, this study provides strong support for the notion that pheromone signaling is essential for initiation of meiosis in S. pombe and that either M-factor signaling or P-factor signaling alone is sufficient.


Genetics ◽  
2021 ◽  
Author(s):  
Taisuke Seike ◽  
Natsue Sakata ◽  
Chikashi Shimoda ◽  
Hironori Niki ◽  
Chikara Furusawa

Abstract Most sexually reproducing organisms have the ability to recognize individuals of the same species. In ascomycete fungi including yeasts, mating between cells of opposite mating type depends on the molecular recognition of two peptidyl mating pheromones by their corresponding G-protein coupled receptors (GPCRs). Although such pheromone/receptor systems are likely to function in both mate choice and prezygotic isolation, very few studies have focused on the stringency of pheromone receptors. The fission yeast Schizosaccharomyces pombe has two mating types, Plus (P) and Minus (M). Here we investigated the stringency of the two GPCRs, Mam2 and Map3, for their respective pheromones, P-factor and M-factor, in fission yeast. First, we switched GPCRs between S. pombe and the closely related species Schizosaccharomyces octosporus, which showed that SoMam2 (Mam2 of S. octosporus) is partially functional in S. pombe, whereas SoMap3 (Map3 of S. octosporus) is not interchangeable. Next, we swapped individual domains of Mam2 and Map3 with the respective domains in SoMam2 and SoMap3, which revealed differences between the receptors both in the intracellular regions that regulate the downstream signaling of pheromones and in the activation by the pheromone. In particular, we demonstrated that two amino acid residues of Map3, F214 and F215, are key residues important for discrimination of closely related M-factors. Thus, the differences in these two GPCRs might reflect the significantly distinct stringency/flexibility of their respective pheromone/receptor systems; nevertheless, species-specific pheromone recognition remains incomplete.


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