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PMID: 9135999 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Genetic analysis of default mating behavior in Saccharomyces cerevisiae.

Genetics ·Vol. 146 ·No. 1 ·1997-05-00 ·Pages 39-55

Dorer R, Boone C, Kimbrough T, Kim J, Hartwell LH

Abstract

Haploid Saccharomyces cerevisiae cells find each other during conjugation by orienting their growth toward each other along pheromone gradients (chemotropism). However, when their receptors are saturated for pheromone binding, yeast cells must select a mate by executing a default pathway in which they choose a mating partner at random. We previously demonstrated that this default pathway requires the SPA2 gene. In this report we show that the default mating pathway also requires the AXL1, FUS1, FUS2, FUS3, PEA2, RVS161, and BNI1 genes. These genes, including SPA2, are also important for efficient cell fusion during chemotropic mating. Cells containing null mutations in these genes display defects in cell fusion that subtly affect mating efficiency. In addition, we found that the defect in default mating caused by mutations in SPA2 is partially suppressed by multiple copies of two genes, FUS2 and MFA2. These findings uncover a molecular relationship between default mating and cell fusion. Moreover, because axl1 mutants secrete reduced levels of a-factor and are defective at both cell fusion and default mating, these results reveal an important role for a-factor in cell fusion and default mating. We suggest that default mating places a more stringent requirement on some aspects of cell fusion than does chemotropic mating.

MeSH Terms
DNA-Binding Proteins Genes, Fungal Mutation Repressor Proteins Saccharomyces cerevisiae/cytology,genetics,physiology Saccharomyces cerevisiae Proteins Transcription Factors/metabolism
Chemicals
ASH1 protein, S cerevisiae DNA-Binding Proteins Repressor Proteins Saccharomyces cerevisiae Proteins Transcription Factors
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Dorer R
Fred Hutchinson Cancer Research Center, Seattle, Washington 98104, USA.
Boone C
Kimbrough T
Kim J
Hartwell L H
References (66)
66 references, click to expand
  1. Bud10p directs axial cell polarization in budding yeast and resembles a transmembrane receptor.
    Curr Biol. 1996 May 1;6(5):570-9 PMID: 8805277
  2. MAP kinase pathways in yeast: for mating and more.
    Cell. 1995 Jan 27;80(2):187-97 PMID: 7834739
  3. The a-factor transporter (STE6 gene product) and cell polarity in the yeast Saccharomyces cerevisiae.
    J Cell Biol. 1993 Mar;120(5):1203-15 PMID: 7679674
  4. Patterns of bud-site selection in the yeast Saccharomyces cerevisiae.
    J Cell Biol. 1995 May;129(3):751-65 PMID: 7730409
  5. Comparison of dose-response curves for alpha factor-induced cell division arrest, agglutination, and projection formation of yeast cells. Implication for the mechanism of alpha factor action.
    J Biol Chem. 1983 Nov 25;258(22):13849-56 PMID: 6358212
  6. Cell polarity and morphogenesis in Saccharomyces cerevisiae.
    Trends Cell Biol. 1992 Jan;2(1):22-9 PMID: 14731634
  7. Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene.
    Development. 1994 Dec;120(12):3367-77 PMID: 7821209
  8. Courtship in S. cerevisiae: both cell types choose mating partners by responding to the strongest pheromone signal.
    Cell. 1990 Nov 30;63(5):1039-51 PMID: 2257622
  9. A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli.
    Gene. 1987;57(2-3):267-72 PMID: 3319781
  10. Studies concerning the temporal and genetic control of cell polarity in Saccharomyces cerevisiae.
    J Cell Biol. 1991 Aug;114(3):515-32 PMID: 1860883
  11. Regulation of mating in the cell cycle of Saccharomyces cerevisiae.
    J Cell Biol. 1977 Nov;75(2 Pt 1):355-65 PMID: 400872
  12. Two genes required for cell fusion during yeast conjugation: evidence for a pheromone-induced surface protein.
    Mol Cell Biol. 1987 Jul;7(7):2316-28 PMID: 3302672
  13. Defining protein interactions with yeast actin in vivo.
    Nat Struct Biol. 1995 Jan;2(1):28-35 PMID: 7719850
  14. AFR1 acts in conjunction with the alpha-factor receptor to promote morphogenesis and adaptation.
    Mol Cell Biol. 1993 Nov;13(11):6876-88 PMID: 8413281
  15. Interactions between the ankyrin repeat-containing protein Akr1p and the pheromone response pathway in Saccharomyces cerevisiae.
    Mol Cell Biol. 1996 Jan;16(1):168-78 PMID: 8524293
  16. The SPA2 gene of Saccharomyces cerevisiae is important for pheromone-induced morphogenesis and efficient mating.
    J Cell Biol. 1990 Oct;111(4):1451-64 PMID: 2211820
  17. Saccharomyces cerevisiae MATa mutant cells defective in pointed projection formation in response to alpha-factor at high concentrations.
    Yeast. 1994 May;10(5):579-94 PMID: 7941743
  18. Pea2 protein of yeast is localized to sites of polarized growth and is required for efficient mating and bipolar budding.
    J Cell Biol. 1996 Nov;135(3):725-39 PMID: 8909546
  19. Septin scaffolds and cleavage planes in Saccharomyces.
    Cell. 1996 Jan 26;84(2):187-90 PMID: 8565063
  20. Asymmetric accumulation of Ash1p in postanaphase nuclei depends on a myosin and restricts yeast mating-type switching to mother cells.
    Cell. 1996 Mar 8;84(5):699-709 PMID: 8625408
  21. Role for the Rho-family GTPase Cdc42 in yeast mating-pheromone signal pathway.
    Nature. 1995 Aug 24;376(6542):702-5 PMID: 7651520
  22. Sexual conjugation in yeast. Cell surface changes in response to the action of mating hormones.
    J Cell Biol. 1979 Feb;80(2):326-33 PMID: 379012
  23. Applications of high efficiency lithium acetate transformation of intact yeast cells using single-stranded nucleic acids as carrier.
    Yeast. 1991 Apr;7(3):253-63 PMID: 1882550
  24. FUS3 encodes a cdc2+/CDC28-related kinase required for the transition from mitosis into conjugation.
    Cell. 1990 Feb 23;60(4):649-64 PMID: 2406028
  25. Ste20-like protein kinases are required for normal localization of cell growth and for cytokinesis in budding yeast.
    Genes Dev. 1995 Aug 1;9(15):1817-30 PMID: 7649470
  26. Three-dimensional analysis of morphogenesis induced by mating pheromone alpha factor in Saccharomyces cerevisiae.
    J Cell Sci. 1989 Oct;94 ( Pt 2):207-16 PMID: 2695529
  27. FUS3 phosphorylates multiple components of the mating signal transduction cascade: evidence for STE12 and FAR1.
    Mol Biol Cell. 1993 May;4(5):495-510 PMID: 8334305
  28. Multicopy suppression of the cdc24 budding defect in yeast by CDC42 and three newly identified genes including the ras-related gene RSR1.
    Proc Natl Acad Sci U S A. 1989 Dec;86(24):9976-80 PMID: 2690082
  29. Evidence for a branched pathway in the polarized cell division of Saccharomyces cerevisiae.
    Curr Genet. 1995 Feb;27(3):213-6 PMID: 7736604
  30. The SPA2 protein of yeast localizes to sites of cell growth.
    J Cell Biol. 1989 Apr;108(4):1419-29 PMID: 2647769
  31. S. cerevisiae alpha pheromone receptors activate a novel signal transduction pathway for mating partner discrimination.
    Cell. 1991 Oct 18;67(2):389-402 PMID: 1655282
  32. Cell polarization directed by extracellular cues in yeast.
    Mol Biol Cell. 1994 Nov;5(11):1169-75 PMID: 7865882
  33. Developmental mechanisms that generate precise patterns of neuronal connectivity.
    Cell. 1993 Jan;72 Suppl:77-98 PMID: 8428376
  34. Role of yeast insulin-degrading enzyme homologs in propheromone processing and bud site selection.
    Science. 1995 Oct 20;270(5235):464-7 PMID: 7569998
  35. Saccharomyces cerevisiae cells execute a default pathway to select a mate in the absence of pheromone gradients.
    J Cell Biol. 1995 Nov;131(4):845-61 PMID: 7490289
  36. Signal propagation and regulation in the mating pheromone response pathway of the yeast Saccharomyces cerevisiae.
    Dev Biol. 1994 Dec;166(2):363-79 PMID: 7813763
  37. Two differentially regulated mRNAs with different 5' ends encode secreted with intracellular forms of yeast invertase.
    Cell. 1982 Jan;28(1):145-54 PMID: 7039847
  38. Identification of asymmetrically localized determinant, Ash1p, required for lineage-specific transcription of the yeast HO gene.
    Cell. 1996 Mar 8;84(5):711-22 PMID: 8625409
  39. Mother cell-specific HO expression in budding yeast depends on the unconventional myosin myo4p and other cytoplasmic proteins.
    Cell. 1996 Mar 8;84(5):687-97 PMID: 8625407
  40. Molecular basis of cell integrity and morphogenesis in Saccharomyces cerevisiae.
    Microbiol Rev. 1995 Sep;59(3):345-86 PMID: 7565410
  41. Selection of axial growth sites in yeast requires Axl2p, a novel plasma membrane glycoprotein.
    Genes Dev. 1996 Apr 1;10(7):777-93 PMID: 8846915
  42. end5, end6, and end7: mutations that cause actin delocalization and block the internalization step of endocytosis in Saccharomyces cerevisiae.
    Mol Biol Cell. 1995 Dec;6(12):1721-42 PMID: 8590801
  43. Autoimmunity in stiff-Man syndrome with breast cancer is targeted to the C-terminal region of human amphiphysin, a protein similar to the yeast proteins, Rvs167 and Rvs161.
    FEBS Lett. 1994 Aug 29;351(1):73-9 PMID: 8076697
  44. A yeast gene necessary for bud-site selection encodes a protein similar to insulin-degrading enzymes.
    Nature. 1994 Dec 8;372(6506):567-70 PMID: 7990931
  45. Binding of alpha-factor pheromone to yeast a cells: chemical and genetic evidence for an alpha-factor receptor.
    Cell. 1983 Dec;35(2 Pt 1):521-9 PMID: 6360378
  46. Genetic control of bud site selection in yeast by a set of gene products that constitute a morphogenetic pathway.
    Cell. 1991 Jun 28;65(7):1203-12 PMID: 2065354
  47. FAR1 is required for oriented polarization of yeast cells in response to mating pheromones.
    J Cell Biol. 1995 Nov;131(4):863-73 PMID: 7490290
  48. A highly ordered ring of membrane-associated filaments in budding yeast.
    J Cell Biol. 1976 Jun;69(3):717-21 PMID: 773946
  49. Alteration of a yeast SH3 protein leads to conditional viability with defects in cytoskeletal and budding patterns.
    Mol Cell Biol. 1993 Aug;13(8):5070-84 PMID: 8336735
  50. The septins: roles in cytokinesis and other processes.
    Curr Opin Cell Biol. 1996 Feb;8(1):106-19 PMID: 8791410
  51. Pheromonal regulation and sequence of the Saccharomyces cerevisiae SST2 gene: a model for desensitization to pheromone.
    Mol Cell Biol. 1987 Dec;7(12):4169-77 PMID: 2830483
  52. Inhibition of G-protein signaling by dominant gain-of-function mutations in Sst2p, a pheromone desensitization factor in Saccharomyces cerevisiae.
    Mol Cell Biol. 1995 Jul;15(7):3635-43 PMID: 7791771
  53. Specification of sites for polarized growth in Saccharomyces cerevisiae and the influence of external factors on site selection.
    Mol Biol Cell. 1992 Sep;3(9):1025-35 PMID: 1421575
  54. Genetic analysis of the bipolar pattern of bud site selection in the yeast Saccharomyces cerevisiae.
    Mol Cell Biol. 1996 Apr;16(4):1857-70 PMID: 8657162
  55. Role of Bud3p in producing the axial budding pattern of yeast.
    J Cell Biol. 1995 May;129(3):767-78 PMID: 7730410
  56. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm.
    Cell. 1994 Jan 28;76(2):301-14 PMID: 7507411
  57. AFR1 promotes polarized apical morphogenesis in Saccharomyces cerevisiae.
    Mol Cell Biol. 1995 Feb;15(2):723-30 PMID: 7823940
  58. Physiological characterization of Saccharomyces cerevisiae mutants supersensitive to G1 arrest by a factor and alpha factor pheromones.
    Mol Cell Biol. 1982 Jan;2(1):21-9 PMID: 7050666
  59. The likeness of being: phylogenetically conserved molecular mechanisms of growth cone guidance.
    Cell. 1994 Aug 12;78(3):353-6 PMID: 8062381
  60. Development of cell polarity in budding yeast.
    Cell. 1991 Jun 28;65(7):1093-6 PMID: 1905977
  61. Polarization of yeast cells in spatial gradients of alpha mating factor.
    Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8332-6 PMID: 8397402
  62. Actin cytoskeleton and budding pattern are altered in the yeast rvs161 mutant: the Rvs161 protein shares common domains with the brain protein amphiphysin.
    Mol Gen Genet. 1995 Feb 20;246(4):485-95 PMID: 7891662
  63. The C-terminus of the S. cerevisiae alpha-pheromone receptor mediates an adaptive response to pheromone.
    Cell. 1988 Aug 26;54(5):609-20 PMID: 2842059
  64. Yeast mutant affected for viability upon nutrient starvation: characterization and cloning of the RVS161 gene.
    Yeast. 1991 Oct;7(7):727-43 PMID: 1776363
  65. Components required for cytokinesis are important for bud site selection in yeast.
    J Cell Biol. 1993 Jul;122(2):373-86 PMID: 8320260
  66. Cappuccino, a Drosophila maternal effect gene required for polarity of the egg and embryo, is related to the vertebrate limb deformity locus.
    Genes Dev. 1995 Oct 15;9(20):2482-94 PMID: 7590229
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
1997-05-00
Pages
39-55
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1207953
Subset
IM
Grants
NIGMS NIH HHS · GM-07266 · United States
NIGMS NIH HHS · GM-17709 · United States
NIGMS NIH HHS · T32 GM07735 · United States
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