Home LiteratureArticle Details
PMID: 8636217 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Identification of a developmentally regulated septin and involvement of the septins in spore formation in Saccharomyces cerevisiae.

The Journal of cell biology ·Vol. 132 ·No. 3 ·1996-02-00 ·Pages 399-411

Fares H, Goetsch L, Pringle JR

Abstract

The Saccharomyces cerevisiae CDC3, CDC10, CDC11, and CDC12 genes encode a family of related proteins, the septins, which are involved in cell division and the organization of the cell surface during vegetative growth. A search for additional S. cerevisiae septin genes using the polymerase chain reaction identified SPR3, a gene that had been identified previously on the basis of its sporulation-specific expression. The predicted SPR3 product shows 25-40% identity in amino acid sequence to the previously known septins from S. cerevisiae and other organisms. Immunoblots confirmed the sporulation-specific expression of Spr3p and showed that other septins are also present at substantial levels in sporulating cells. Consistent with the expression data, deletion of SPR3 in either of two genetic backgrounds had no detectable effect on exponentially growing cells. In one genetic background, deletion of SPR3 produced a threefold reduction in sporulation efficiency, although meiosis appeared to be completed normally. In this background, deletion of CDC10 had no detectable effect on sporulation. In the other genetic background tested, the consequences of the two deletions were reversed. Immunofluorescence observations suggest that Spr3p, Cdc3p, and Cdc11p are localized to the leading edges of the membrane sacs that form near the spindle-pole bodies and gradually extend to engulf the nuclear lobes that contain the haploid chromosome sets, thus forming the spores. Deletion of SPR3 does not prevent the localization of Cdc3p and Cdc11p, but these proteins appear to be less well organized, and the intensity of their staining is reduced. Taken together, the results suggest that the septins play important but partially redundant roles during the process of spore formation.

MeSH Terms
Amino Acid Sequence Base Sequence Cell Cycle Proteins/analysis,biosynthesis,isolation & purification Cell Division Cytoskeletal Proteins DNA Primers Fungal Proteins/biosynthesis GTP Phosphohydrolases Gene Expression Regulation, Fungal Genes, Fungal Genotype Membrane Proteins Molecular Sequence Data Multigene Family Mutagenesis Polymerase Chain Reaction Profilins Recombinant Proteins/biosynthesis Restriction Mapping Saccharomyces cerevisiae/genetics,growth & development,physiology Saccharomyces cerevisiae Proteins Schizosaccharomyces pombe Proteins Sequence Deletion Sequence Homology, Amino Acid Spores, Fungal Transcription Factors
Chemicals
CDC11 protein, S cerevisiae CDC12 protein, S cerevisiae CDC3 protein, S cerevisiae Cell Cycle Proteins Cytoskeletal Proteins DNA Primers Fungal Proteins Membrane Proteins Profilins Recombinant Proteins SPR3 protein, S cerevisiae Saccharomyces cerevisiae Proteins Schizosaccharomyces pombe Proteins Transcription Factors cdc10 protein, S pombe CDC10 protein, S cerevisiae GTP Phosphohydrolases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Fares H
Department of Biology, University of North Carolina, Chapel Hill 27599, USA.
Goetsch L
Pringle J R
References (77)
77 references, click to expand
  1. Cellular morphogenesis in the Saccharomyces cerevisiae cell cycle: localization of the CDC3 gene product and the timing of events at the budding site.
    J Cell Biol. 1991 Feb;112(4):535-44 PMID: 1993729
  2. Formation of septum-like structures at locations remote from the budding sites in cytokinesis-defective mutants of Saccharomyces cerevisiae.
    J Bacteriol. 1985 May;162(2):763-7 PMID: 3886632
  3. Control of meiotic gene expression in Saccharomyces cerevisiae.
    Microbiol Rev. 1994 Mar;58(1):56-70 PMID: 8177171
  4. Genetics and molecular biology of chitin synthesis in fungi.
    Annu Rev Microbiol. 1993;47:505-34 PMID: 8257107
  5. SSG1, a gene encoding a sporulation-specific 1,3-beta-glucanase in Saccharomyces cerevisiae.
    J Bacteriol. 1993 Jun;175(12):3823-37 PMID: 8509335
  6. Dependence of inessential late gene expression on early meiotic events in Saccharomyces cerevisiae.
    Mol Gen Genet. 1989 Feb;215(3):490-500 PMID: 2651894
  7. Fine structure of ascospore development in the yeast Saccharomyces cerevisiae.
    Can J Microbiol. 1971 Apr;17(4):507-10 PMID: 4101740
  8. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  9. Localization and possible functions of Drosophila septins.
    Mol Biol Cell. 1995 Dec;6(12):1843-59 PMID: 8590810
  10. Characterization of a DL-dityrosine-containing macromolecule from yeast ascospore walls.
    J Biol Chem. 1990 Sep 5;265(25):15118-23 PMID: 2203769
  11. Physical maps of the six smallest chromosomes of Saccharomyces cerevisiae at a resolution of 2.6 kilobase pairs.
    Genetics. 1993 May;134(1):81-150 PMID: 8514151
  12. Ascospore wall development in Saccharomyces cerevisiae.
    J Bacteriol. 1973 Feb;113(2):1054-7 PMID: 4570590
  13. Developmental changes in translatable RNA species associated with meiosis and spore formation in Saccharomyces cerevisiae.
    Mol Cell Biol. 1984 Apr;4(4):695-702 PMID: 6371495
  14. Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis.
    Exp Cell Res. 1971 Dec;69(2):265-76 PMID: 4950437
  15. Identification of a set of genes with developmentally down-regulated expression in the mouse brain.
    Biochem Biophys Res Commun. 1992 Jun 30;185(3):1155-61 PMID: 1378265
  16. The Drosophila peanut gene is required for cytokinesis and encodes a protein similar to yeast putative bud neck filament proteins.
    Cell. 1994 May 6;77(3):371-9 PMID: 8181057
  17. Are mitotic functions required in meiosis?
    Genetics. 1974 Apr;76(4):745-53 PMID: 4599956
  18. Characterization and mutational analysis of a cluster of three genes expressed preferentially during sporulation of Saccharomyces cerevisiae.
    Mol Cell Biol. 1986 Jul;6(7):2443-51 PMID: 3023934
  19. Isolation of genes expressed preferentially during sporulation in the yeast Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1983 May;80(10):3000-4 PMID: 6304689
  20. An Escherichia coli vector to express and purify foreign proteins by fusion to and separation from maltose-binding protein.
    Gene. 1988 Dec 30;74(2):365-73 PMID: 3073105
  21. Rat monoclonal antitubulin antibodies derived by using a new nonsecreting rat cell line.
    J Cell Biol. 1982 Jun;93(3):576-82 PMID: 6811596
  22. Functional analysis of the sporulation-specific SPR6 gene of Saccharomyces cerevisiae.
    Curr Genet. 1990 Nov;18(4):293-301 PMID: 2253272
  23. Genetic Control of the Cell Division Cycle in Yeast: V. Genetic Analysis of cdc Mutants.
    Genetics. 1973 Jun;74(2):267-86 PMID: 17248617
  24. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
    Genetics. 1989 May;122(1):19-27 PMID: 2659436
  25. Cellular morphogenesis in the Saccharomyces cerevisiae cell cycle: localization of the CDC11 gene product and the timing of events at the budding site.
    Dev Genet. 1991;12(4):281-92 PMID: 1934633
  26. A chromosomal gene required for killer plasmid expression, mating, and spore maturation in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1976 Jun;73(6):2061-5 PMID: 778853
  27. Isolation of DNA sequences preferentially expressed during sporulation in Saccharomyces cerevisiae.
    Mol Cell Biol. 1984 Jan;4(1):142-50 PMID: 6366508
  28. Lymphocyte HEV adhesion variants differ in the expression of multiple gene sequences.
    Gene. 1990 Nov 15;95(2):279-84 PMID: 2174398
  29. Isolation of two developmentally regulated genes involved in spore wall maturation in Saccharomyces cerevisiae.
    Genes Dev. 1990 Oct;4(10):1775-89 PMID: 2249774
  30. Use of the DNA polymerase chain reaction for homology probing: isolation of partial cDNA or genomic clones encoding the iron-sulfur protein of succinate dehydrogenase from several species.
    Proc Natl Acad Sci U S A. 1989 Mar;86(6):1934-8 PMID: 2494655
  31. Isolation and functional analysis of sporulation-induced transcribed sequences from Saccharomyces cerevisiae.
    Mol Cell Biol. 1986 Jun;6(6):2185-97 PMID: 3537714
  32. Transient G1 arrest of S. cerevisiae cells of mating type alpha by a factor produced by cells of mating type a.
    Exp Cell Res. 1974 Nov;89(1):175-87 PMID: 4611778
  33. Homologs of the yeast neck filament associated genes: isolation and sequence analysis of Candida albicans CDC3 and CDC10.
    Mol Gen Genet. 1994 Mar;242(6):689-98 PMID: 8152419
  34. Transcriptional regulation of sporulation genes in yeast.
    Mol Gen Genet. 1987 Dec;210(3):449-59 PMID: 3323843
  35. Overproduction of FtsZ suppresses sensitivity of lon mutants to division inhibition.
    J Bacteriol. 1986 Jun;166(3):756-62 PMID: 3011743
  36. A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae.
    Cell. 1990 Jun 15;61(6):1089-101 PMID: 2190690
  37. Saccharomyces cerevisiae exhibits a sporulation-specific temporal pattern of transcript accumulation.
    Mol Cell Biol. 1985 Apr;5(4):751-61 PMID: 3887135
  38. Isolation of the centromere-linked CDC10 gene by complementation in yeast.
    Proc Natl Acad Sci U S A. 1980 Apr;77(4):2173-7 PMID: 6990421
  39. GTP-binding domain: three consensus sequence elements with distinct spacing.
    Proc Natl Acad Sci U S A. 1987 Apr;84(7):1814-8 PMID: 3104905
  40. Large-scale analysis of gene expression, protein localization, and gene disruption in Saccharomyces cerevisiae.
    Genes Dev. 1994 May 1;8(9):1087-105 PMID: 7926789
  41. Changing patterns of gene expression during sporulation in yeast.
    Proc Natl Acad Sci U S A. 1984 Dec;81(23):7323-7 PMID: 6390434
  42. CSD2, CSD3, and CSD4, genes required for chitin synthesis in Saccharomyces cerevisiae: the CSD2 gene product is related to chitin synthases and to developmentally regulated proteins in Rhizobium species and Xenopus laevis.
    Mol Cell Biol. 1992 Apr;12(4):1764-76 PMID: 1532231
  43. Subcellular differentiation in sporulating yeast cells.
    Cell. 1986 Jun 6;45(5):771-9 PMID: 3518948
  44. A Collection of cDNA Clones with Specific Expression Patterns in Mouse Brain.
    Eur J Neurosci. 1990;2(8):704-711 PMID: 12106288
  45. The sporulation-specific enzymes encoded by the DIT1 and DIT2 genes catalyze a two-step reaction leading to a soluble LL-dityrosine-containing precursor of the yeast spore wall.
    Proc Natl Acad Sci U S A. 1994 May 10;91(10):4524-8 PMID: 8183942
  46. Cell membrane formation during the cellularization of the syncytial blastoderm of Drosophila.
    Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):2199-203 PMID: 7892247
  47. 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
  48. Isolation and characterization of a mammalian gene encoding a high-affinity cAMP phosphodiesterase.
    Proc Natl Acad Sci U S A. 1989 May;86(10):3599-603 PMID: 2542941
  49. Pheromones and pheromone receptors are the primary determinants of mating specificity in the yeast Saccharomyces cerevisiae.
    Genetics. 1989 Mar;121(3):463-76 PMID: 2653961
  50. Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae.
    J Cell Biol. 1984 Mar;98(3):934-45 PMID: 6365931
  51. Immunolocalization of Kex2 protease identifies a putative late Golgi compartment in the yeast Saccharomyces cerevisiae.
    J Cell Biol. 1991 May;113(3):527-38 PMID: 2016334
  52. Sequence of the CDC10 region at chromosome III of Saccharomyces cerevisiae.
    Yeast. 1991 May-Jun;7(4):425-9 PMID: 1872033
  53. Putting the HO gene to work: practical uses for mating-type switching.
    Methods Enzymol. 1991;194:132-46 PMID: 2005783
  54. Isolation and characterization of sporulation-specific promoters in the yeast Saccharomyces cerevisiae.
    Mol Microbiol. 1992 Jan;6(1):75-81 PMID: 1738316
  55. The Saccharomyces cerevisiae SPR1 gene encodes a sporulation-specific exo-1,3-beta-glucanase which contributes to ascospore thermoresistance.
    J Bacteriol. 1993 Jan;175(2):386-94 PMID: 8419289
  56. Spindles, spindle plaques, and meiosis in the yeast Saccharomyces cerevisiae (Hansen).
    J Cell Biol. 1971 Aug;50(2):344-61 PMID: 5112645
  57. High-expression vectors with multiple cloning sites for construction of trpE fusion genes: pATH vectors.
    Methods Enzymol. 1991;194:477-90 PMID: 2005804
  58. 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
  59. A highly ordered ring of membrane-associated filaments in budding yeast.
    J Cell Biol. 1976 Jun;69(3):717-21 PMID: 773946
  60. Development of the spore wall during ascospore formation in Saccharomyces cerevisiae.
    J Cell Biol. 1970 Mar;44(3):688-92 PMID: 4190070
  61. Carbohydrate metabolism during ascospore development in yeast.
    J Bacteriol. 1974 Apr;118(1):8-14 PMID: 4595206
  62. Morphogenesis of ascospores in Saccharomyces cerevisiae.
    J Bacteriol. 1972 Feb;109(2):869-80 PMID: 4110145
  63. Chemical composition of the yeast ascospore wall. The second outer layer consists of chitosan.
    J Biol Chem. 1988 Aug 15;263(23):11569-74 PMID: 3042773
  64. The P-loop--a common motif in ATP- and GTP-binding proteins.
    Trends Biochem Sci. 1990 Nov;15(11):430-4 PMID: 2126155
  65. Role of Bud3p in producing the axial budding pattern of yeast.
    J Cell Biol. 1995 May;129(3):767-78 PMID: 7730410
  66. Mutation of the SPS1-encoded protein kinase of Saccharomyces cerevisiae leads to defects in transcription and morphology during spore formation.
    Genes Dev. 1994 Sep 15;8(18):2162-75 PMID: 7958886
  67. The isolation and genetic analysis of sporulation-deficient mutants in Saccharomyces cerevisiae.
    Mol Gen Genet. 1983;191(1):17-21 PMID: 6350825
  68. The SPR3 gene encodes a sporulation-specific homologue of the yeast CDC3/10/11/12 family of bud neck microfilaments and is regulated by ABFI.
    Gene. 1995 Oct 16;164(1):157-62 PMID: 7590307
  69. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites.
    Gene. 1988 Dec 30;74(2):527-34 PMID: 3073106
  70. DIT101 (CSD2, CAL1), a cell cycle-regulated yeast gene required for synthesis of chitin in cell walls and chitosan in spore walls.
    Yeast. 1992 Dec;8(12):1089-99 PMID: 1293886
  71. Fluorescence microscopy methods for yeast.
    Methods Cell Biol. 1989;31:357-435 PMID: 2476649
  72. SMK1, a developmentally regulated MAP kinase, is required for spore wall assembly in Saccharomyces cerevisiae.
    Genes Dev. 1994 Sep 15;8(18):2151-61 PMID: 7958885
  73. Predicting coiled coils from protein sequences.
    Science. 1991 May 24;252(5009):1162-4 PMID: 2031185
  74. Genes controlling meiosis and spore formation in yeast.
    Genetics. 1974 Sep;78(1):215-25 PMID: 4613605
  75. The SPS100 gene of Saccharomyces cerevisiae is activated late in the sporulation process and contributes to spore wall maturation.
    Mol Cell Biol. 1988 Feb;8(2):912-22 PMID: 3280971
  76. Immunofluorescence localization of the Saccharomyces cerevisiae CDC12 gene product to the vicinity of the 10-nm filaments in the mother-bud neck.
    Mol Cell Biol. 1987 Oct;7(10):3678-87 PMID: 3316985
  77. Components required for cytokinesis are important for bud site selection in yeast.
    J Cell Biol. 1993 Jul;122(2):373-86 PMID: 8320260
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1996-02-00
Pages
399-411
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2120726
Subset
IM
Grants
NIGMS NIH HHS · GM18541 · United States
NIGMS NIH HHS · GM31006 · United States
Databases
GENBANK
L31767
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]