NDT80 and the meiotic recombination checkpoint regulate expression of middle sporulation-specific genes in Saccharomyces cerevisiae

Molecular and Cellular Biology

Volumn 18, Issue 10, 1998, Pages 5750-5761

  Hepworth, Shelley R ^a,c   Friesen, Helena ^a   Segall, Jacqueline ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; DNA SYNTHESIS INHIBITION; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE MUTATION; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; MEIOSIS; NONHUMAN; PACHYTENE; PRIORITY JOURNAL; REGULATOR GENE; REPORTER GENE; SACCHAROMYCES CEREVISIAE; SPOROGENESIS;

ANIMALIA; SACCHAROMYCES CEREVISIAE;

EID: 0031708269     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.18.10.5750     Document Type: Article

References (80)

1. Alani, E., L. Cao, and N. Kleckner. 1987. A method for gene disruption that allows repeated use of URA3 selection in the construction of multiply disrupted yeast strains. Genetics 116:541-545.
2. Alani, E., R. Padmore, and N. Kleckner. 1990. Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell 61:419-136.
3. 1 cyclin turnover and nutrient uptake are controlled by a common pathway in yeast. Genes Dev. 9:399-409.
4. Bishop, D. K., D. Park, L. Xu, and N. Kleckner. 1992. DMC1:a meiosisspecific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69:439-456.
5. Boeke, D., F. LaCroute, and G. R. Fink. 1984. A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast:5-fluoro-orotic acid resistance. Mol. Gen. Genet. 197:345-346.
6. Bowdish, K. S., and A. P. Mitchell. 1993. Bipartite structure of an early meiotic upstream activation sequence from Saccharomyces cerevisiae. Mol. Cell. Biol. 13:2172-2181.
7. Bowdish, K. S., H. E. Yuan, and A. P. Mitchell. 1994. Analysis of RIM11, a yeast protein kinase that phosphorylates the meiotic activator IME1. Mol. Cell. Biol. 14:7909-7919.
8. Buckingham, L. E., H.-T. Wang, R. T. Elder, R. M. McCarroll, M. R. Slater, and R. E. Esposito. 1990. Nucleotide sequence and promoter analysis of SPO13, a meiosis-specific gene of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 87:9406-9410.
9. Byers, B. 1981. Cytology of the yeast life cycle, p. 59-96. In J. N. Strathern, E. W. Jones, and J. R. Broach (ed.), The molecular biology of the yeast Saccharomyces:life cycle and inheritance. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
10. Chu, S., and I. Herskowitz. 1998. Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80. Mol. Cell 1:685-696.
11. Clancy, M. J., L. M. Smith, and P. T. Magee. 1982. Developmental regulation of a sporulation-specific enzyme activity in Saccharomyces cerevisiae. Mol. Cell. Biol. 2:171-178.
12. Connolly, B., C. I. White, and J. E. Haber. 1988. Physical monitoring of mating-type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 8:2342-2349.
13. Dahmann, C., and B. Futcher. 1995. Specialization of B-type cyclins for mitosis or meiosis in S. cerevisiae. Genetics 140:957-963.
14. Friesen, H., R. Lunz, S. Doyle, and J. Segall. 1994. Mutation of the SPS1-encoded protein kinase of Saccharomyces cerevisiae leads to defects in transcription and morphology during spore formation. Genes Dev. 8:2162-2175.
15. Gailus-Durner, V., J. Xie, C. Chintamaneni, and A. K. Vershon. 1996. Participation of the yeast activator Abf1 in meiosis-specific expression of the HOP1 gene. Mol. Cell. Biol. 16:2777-2786.
16. Garber, A. T., and J. Segall. 1986. The SPS4 gene of Saccharomyces cerevisiae encodes a major sporulation-specific mRNA. Mol. Cell. Biol. 6:4478-4485.
17. Gietz, D., A. St. Jean, R. A. Woods, and R. H. Schiestl. 1992. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20:1425.
18. Grandin, N., and S. I. Reed. 1993. Differential function and expression of Saccharomyces cerevisiae B-type cyclins in mitosis and meiosis. Mol. Cell. Biol. 13:2113-2125.
19. Hepworth, S. R., L. K. Ebisuzaki, and J. Segall. 1995. A 15-base-pair element activates the SPS4 gene midway through sporulation in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:3934-3944.
20. Hollingsworth, N. M., L. Goetsch, and B. Byers. 1990. The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell 61:73-84.
21. + gene encodes a meiosis-specific transcription factor containing a forkhead DNA-binding domain. Mol. Cell. Biol. 18:2118-2129.
22. Jensen, R. E., and I. Herskowitz. 1984. Directionality and regulation of cassette substitution in yeast. Cold Spring Harbor Symp. Quant. Biol. 49:97-104.
23. Kadosh, D., and K. Struhl. 1997. Repression by Ume6 involves recruitment of a complex containing Sin3 corepressor and Rpd3 histone deacetylase to target promoters. Cell 89:365-371.
24. Kadosh, D., and K. Struhl. 1998. Histone deacetylase activity of Rpd3 is important for transcriptional repression in vivo. Genes Dev. 12:797-805.
25. Kao, G., D. G. Mannix, B. L. Holaway, M. C. Finn, A. E. Bonny, and M. J. Clancy. 1989. Dependence of inessential late gene expression on early meiotic events in Saccharomyces cerevisiae. Mol. Gen. Genet. 215:490-500.
26. Kasten, M. M., S. Dorian, and D. J. Stillman. 1997. A large protein complex containing the yeast Sin3p and Rpd3p transcriptionai regulators. Mol. Cell. Biol. 17:4852-4858.
27. Keeney, S., C. N. Giroux, and N. Kleckner. 1997. Meiosis-specific DNA double-strand breaks are catalyzed by Spoil, a member of a widely conserved protein family. Cell 88:375-384.
28. Kihara, K., M. Nakamura, R. Akada, and I. Yamashita. 1991. Positive and negative elements upstream of the meiosis-specific glucoamylase gene in Saccharomyces cerevisiae. Mol. Gen. Genet. 226:383-392.
29. Krisak, L., R. Strich, R. S. Winters, P. Hall, M. J. Mallory, D. Dreitzer, R. S. Tuan, and E. Winter. 1994. SMK1, a developmentally regulated MAP kinase, is required for spore wall assembly in Saccharomyces cerevisiae. Genes Dev. 8:2151-2161.
30. Kupiec, M., B. Byers, R. E. Esposito, and A. P. Mitchell. 1997. Meiosis and sporulation in Saccharomyces cerevisiae, p. 899-1036. In J. R. Pringle, J. R. Broach, and E. W. Jones (ed.), The molecular biology of the yeast Saccharomyces:cell cycle and cell biology. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
31. Lamb, T., and A. P. Mitchell. 1996. Control of meiotic gene expression by a DNA synthesis checkpoint, p. 156. In Abstracts of the 1996 Yeast Genetics and Molecular Biology Meeting. The Genetics Society of America. Bethesda, Md.
32. Law, D. T. S., and J. Segall. 1988. The SPS100 gene of Saccharomyces cerevisiae is activated late in the sporulation process and contributes to spore wall maturation. Mol. Cell. Biol. 8:912-922.
33. Lawrence, C. W. 1991. Classical mutagenesis techniques, p. 273-281. In C. Guthrie and G. R. Fink (ed.), Guide to yeast genetics and molecular biology. Academic Press, Inc., New York, N.Y.
34. Lee, R. H., and S. M. Honigberg. 1996. Nutritional regulation of late meiotic events in Saccharomyces cerevisiae through a pathway distinct from initiation. Mol. Cell. Biol. 16:3222-3232.
35. Lydall, D., V. Nikolsky, D. K. Bishop, and T. Weinert. 1996. A meiotic recombination checkpoint controlled by mitotic checkpoint genes. Nature (London) 383:840-841.
36. Malathi, K., Y. Xiao, and A. P. Mitchell. 1997. Interaction of yeast represser-activator protein Umeop with glycogen synthase kinase 3 homolog Rim11p. Mol. Cell. Biol. 17:7230-7236.
37. McKee, A. H. Z., and N. Kleckner. 1997a. Mutations in Saccharomyces cerevisiae that block meiotic prophase chromosome metabolism and confer cell cycle arrest at pachytene identify two new meiosis-specific genes SAE1 and SAE2. Genetics 146:817-834.
38. McKee, A. H. Z., and N. Kleckner. 1997b. A general method for identifying recessive diploid-specific mutations in Saccharomyces cerevisiae, its application to the isolation of mutants blocked at intermediate stages of meiotic prophase and characterization of new gene SAE2. Genetics 146:797-816.
39. Mitchell, A. P. 1994. Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiol. Rev. 58:56-70.
40. Mitchell, A. P., S. E. Driscoll, and H. E. Smith. 1990. Positive control of sporulation-specific genes by the IME1 and IME2 products in Saccharomyces cerevisiae. Mol. Cell. Biol. 10:2104-2110.
41. Morgan, B. A., F. L. Conlon, M. Manzanares, J. B. A. Millar, N. Kanuga, J. Sharpe, R. Krumlauf, J. C. Smith, and S. G. Sedgwick. 1996. Transposon tool for recombinant DNA manipulation:characterization of transcriptionai regulators from yeast, Xenopus, and mouse. Proc. Natl. Acad. Sci. USA 93:2801-2806.
42. Neiman, A. M. 1998. Prospore membrane formation defines a developmentally regulated branch of the secretory pathway in yeast. J. Cell Biol. 140:29-37.
43. Ozsarac, N., M. J. Straffon, H. E. Dalton, and I. W. Dawes. 1997. Regulation of gene expression during meiosis in Saccharomyces cerevisiae:SPR3 is controlled by both ABFI and a new sporulation control element. Mol. Cell. Biol. 17:1152-1159.
44. Page, A. W., and T. L. Orr-Weaver. 1997. Stopping and starting the meiotic cell cycle. Curr. Opin. Genet. Dev. 7:23-31.
45. Pazin, M. J., and J. T. Kadonaga. 1997. What's up and down with histone deacetylation and transcription. Cell 89:325-328.
46. Percival-Smith, A., and J. Segall. 1984. Isolation of DNA sequences preferentially expressed during sporulation in Saccharomyces cerevisiae. Mol. Cell. Biol. 4:142-150.
47. Petko, L., and S. Lindquist. 1986. Hsp26 is not required for growth at high temperatures, nor for thermotolerance, spore development, or germination. Cell 45:885-594.
48. Prinz, S., A. Amon, and F. Klein. 1997. Isolation of COM1, a new gene required to complete meiotic double-strand break-induced recombination in Saccharomyces cerevisiae. Genetics 146:781-795.
49. Rose, D., and C. Holm. 1993. Meiosis-specific arrest revealed in DNA topoisomerase II mutants. Mol. Cell. Biol. 13:3445-3455.
50. Rose, M. D., and J. R. Broach. 1991. Cloning genes by complementation, p. 195-229. In C. Guthrie and G. R. Fink (ed.), Guide to yeast genetics and molecular biology. Academic Press, Inc., New York, N.Y.
51. Rothstein, R. 1983. One-step gene replacement in yeast. Methods Enzymol. 101:202-211.
52. Rubin-Berjerano, I., S. Mandel, K. Robzyk, and Y. Kassir. 1996. Induction of meiosis in Saccharomyces cerevisiae depends on conversion of the transcriptional represser Ume6 to a positive regulator by its regulated association with the transcriptional activator Ime1. Mol. Cell. Biol. 16:2518-2526.
53. Rundlett, S. E., A. A. Carmen, R. Kobayashi, S. Bavykin, B. M. Turner, and M. Grunstein. 1996. HDA1 and RPD3 are members of distinct yeast histone deacetylase complexes that regulate silencing and transcription. Proc. Natl. Acad. Sci. USA 93:14503-14508.
54. Rundlett, S. E., A. A. Carmen, N. Suyka, B. M. Turner, and M. Grunstein. 1998. Transcription repression by UME6 involves deacetylation of lysine 5 of histone H4 by RPD3. Nature 392:831-835.
55. Schmitt, M. E., Brown, T. A., and B. L. Trumpower. 1990. A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res. 18:3091-3092.
56. Sedgwick, S. G., and B. A. Morgan. 1994. Locating, DNA sequencing, and disrupting yeast genes using tagged Tn1000. Methods Mol. Gen. 3:131-140.
57. Sherman, F. 1991. Getting started with yeast, p. 3-20. In C. Guthrie and G. R. Fink (ed.), Guide to yeast genetics and molecular biology. Academic Press, Inc., New York, N.Y.
58. Sherman, F., and J. Hicks. 1991. Micromanipulation and dissection of asci, p. 21-37. In C. Guthrie and G. R. Fink (ed.), Guide to yeast genetics and molecular biology. Academic Press, Inc., New York, N.Y.
59. Sinister, E. O., and B. Byers. 1989. Pachytene arrest and other meiotic effects of start mutations in Saccharomyces cerevisiae. Genetics 123:29-43.
60. Sia, R. A. L., and A. P. Mitchell. 1995. Stimulation of later functions of the yeast meiotic protein kinase Ime2p by the IDS2 gene product. Mol. Cell. Biol. 15:5279-5287.
61. Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19-27.
62. Smith, H. E., S. S. Y. Su, L. Neigeborn, S. E. Driscoll, and A. P. Mitchell. 1990. Role of IME1 expression in regulation of meiosis in Saccharomyces cerevisiae. Mol. Cell. Biol. 10:6103-6113.
63. Steber, C. M., and R. E. Esposito. 1995. UME6 is a central component of a developmental regulatory switch controlling meiosis-specific gene expression. Proc. Natl. Acad. Sci. USA 92:12490-12494.
64. Stillman, D. J., S. Dorland, and Y. Yu. 1994. Epistasis analysis of suppressor mutations that allow HO expression in the absence of the yeast SW15 transcriptional activator. Genetics 136:781-788.
65. Strich, R., M. R. Slater, and R. E. Esposito. 1989. Identification of negative regulatory genes that govern the expression of early meiotic genes in yeast. Proc. Natl. Acad. Sci. USA 86:10018-10022.
66. Strich, K., R. T. Surosky, C. Steber, E. Dubois, F. Messenguy, and R. E. Esposito. 1994. UME6 is a key regulator of nitrogen repression and meiotic development. Genes Dev. 8:796-810,
67. Struhl, K. 1998. Histone acetylation and transcriptional regulatory mechanisms. Genes Dev. 12:599-606.
68. Sym, M. J. A. Engebrecht, and G. S. Roeder. 1993. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72:365-378.
69. Taunton, J., C. A. Hassig, and S. L. Schreiber. 1996. A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p. Science 272:408-411.
70. Tishkoff, D. X., B. Rockmill, G. S. Roeder, and R. D. Kolodner, 1995. The sep1 mutant of Saccharomyces cerevisiae arrests in pachytene and is deficient in meiotic recombination. Genetics 139:495-509.
71. Tsui, K., L. Simon, and D. Norris. 1997. Progression into the first meiotic division is sensitive to histone H2A-H2B dimer concentration in Saccharomyces cerevisiae. Genetics 145:647-659.
72. Vershon, A. K., N. M. Hollings worth, and A. D. Johnson. 1992. Meiotic induction of the yeast HOP1 gene is controlled by positive and negative regulatory sites. Mol. Cell. Biol. 12:3706-3714.
73. Vidai, M., and R. F. Gaber. 1991. RPD3 encodes a second factor required to achieve maximum positive and negative transcriptional states in Saccharomyces cerevisiae. Mol. Cell. Biol. 11:6317-6327.
74. Vidai, M., R. Strich, R. E. Esposito, and R. F. Gaber. 1991. RPD1 (SIN3/ UME4) is required for maximal activation and repression of diverse yeast genes. Mol. Cell. Biol. 11:6306-6316.
75. Wagner, M., M. Pierce, and E. Winter. 1997. The CDK-activating kinase CAK1 can dosage suppress sporulation defects of smk1 MAP kinase mutants and is required for spore wall morphogenesis in Saccharomyces cerevisiae. EMBO J. 16:1305-1317.
76. Wang, H., and D. J. Stillman. 1990. In vitro regulation of a SIN3-dependent DNA-binding activity by stimulatory and inhibitory factors. Proc. Natl. Acad. Sci. USA 87:9761-9765.
77. Wolffe, A. P. 1996. Histone deacetylase:a regulator of transcription. Science 272:371-372.
78. Xu, L., B. M. Weiner, and N. Kleckner. 1997. Meiotic cells monitor the status of the interhomolog recombination complex. Genes Dev. 11:106-118.
79. Xu, L., M. Ajimura, R. Padmore, C. Klein, and N. Kleckner. 1995. NDT80, a meiosis-specific gene required for exit from pachytene in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:6572-6581.
80. Yamashita, I., and S. Fukui. 1985. Transcriptional control of the sporulation-specific glucoamylase gene in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 5:3069-3073.