Abstract
In budding yeast, mitotic DNA replication initiates at sequence-specific replication origins, the prototype for which is ARS1. Initiation serves as the primary control point for mitotic DNA replication, and is catalyzed by the Cdc7 protein kinase. In contrast, premeiotic DNA replication apparently does not require Cdc7, and the existence and nature of specific replication origins in the meiotic division cycle have not been previously reported. We have begun to investigate the mechanism of premeiotic DNA synthesis by determining whether or not ARS1 functions as a DNA replication origin in meiosis. We have taken advantage of the fact that transcription through ARS1 disrupts its ability to function as an origin to show that ARS1 is required for premeiotic DNA replication of a plasmid bearing this element. Further, premeiotic replication from ARS1 still occurs in a cdc7 mutant strain held at conditions non-permissive for Cdc7 protein kinase activity. These findings reveal that premeiotic DNA replication can initiate from origins also used in mitosis, and is not regulated by Cdc7. Taken together with previous findings implicating Cdc7 in meiotic DNA recombination and induced mutagenesis, these findings prompt us to postulate that the Cdc7 protein kinase regulates some step common to several DNA metabolic processes such as local disassembly of chrommatin or activation of a key component of the DNA metabolic machinery.
Similar content being viewed by others
References
BartlettR, Nurse P (1990) Yeast as a model system for eukaryotic DNA replication. Bioessays 12: 457–463
Elledge SJ, Davis RW (1988) A family of versatile centromeric vectors designed for use in the sectoring-shuffle mutagenesis assay in Saccharomyces cerevisiae. Gene 70: 303–312
Esposito RE, Esposito MS (1974) Genetic recombination and commitment to meiosis in Saccharomyces. Proc Natl Acad Sci USA 71: 3172–3176
Esposito RE, Klapholz S (1981) Meiosis and ascospore development. In: Strathern JN, Jones EW, Broach JR (eds) The molecular biology of the yeast Saccharomyces, p 288. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
Ganesan AT, Holter T, Roberts C (1958) Some observations on sporulation in Saccharomyces. C R Trav Lab Carlsberg 31: 1–6
Harland RM, Laskey RA (1980) Regulated replicaation of DNA microinjected in eggs of Xenopus laevis. Cell 21: 761–771
Hollingsworth RE, Sclafani RA (1990) DNA metabolism gene CDC7 from yeasr encodes a serine (threonine) protein kinase. Proc Natl Acad Sci USA 87: 6272–6276
Hollingsworth REJr, Ostroff RM, Klein MB, Niswander LA, Sclafani RA (1992) Molecular genetic studies of the Cdc7 protein kinase and induced mutagenesis in yeast. Genetics 132: 53–62
Johnston M, Davis RW (1984) Sequences that regulate the divergent GAL1,10 promoter in Saccharomyces cerevisiae. Mol Cell Biol 4: 1440–1448
Koshland D, Kent JC, Hartwell LH (1985) Genetic analysis of the mitotic transmission of minichromosomes. Cell 40: 393–403
Krysan PJ, Calos MP (1991) Replication initiates at multiple locations on an autonomously replicating plasmid in human cells. Mol Cell Biol 11: 1464–1472
Kuenzi MT, Roth R (1974) Timing of mitochondrial DNA synthesis in meiosis in Saccharomyces cerevisiae. Exp Cell Res 85: 377–383
Linskens MHK, Huberman JA (1990) The two faces of higher eukaryotic DNA replication origins. Cell 62: 845–847
Martin RG, Setlow VP (1980) The initiation of SV40 DNA synthesis is not unique to the replication origin. Cell 20: 381–391
Newlon CS (1988) Yeast chromosome replication and segregation, Microbiol Rev 52: 568–601
Newlon CS, Greenfeder SA, Collins I, Deshpande A, Ong L, Dershowitz A (1992) Replication of Saccharomyces cerevisiae chromosome III. Yeast 8: S234
Njagi GDE, Kilbey BJ (1982) cdc7-1, A temperature sensitive cell-cycle mutant which interferes with induced mutagenesis in Saccharomyces cerevisiae. Mol Gen Genet 186: 478–481
Patterson M, Sclafani RA, Fangman WL, Rosamond J (1986) Molecular characterization of cell cycle gene CDC7 from Saccharomyces cerevisiae. Mol Cell Biol 6: 1590–1598
Schild D, Byers B (1978) Meiotic effects of DNA-defective cell division cycle mutations of Saccharomyces cerevisiae. Chromosoma 70: 109–130
Sclafani RA, Fangman WL (1986) Thymidine utilization by tut mutants and facile cloning of mutant alleles by plasmid conversion in S. cerevisiae. Genetics 114: 753–767
Sherman F, Roman H (1963) Evidence for two types of allelic recombination in yeast. Genetics 48: 255–261
Shuster EO, Byers B (1989) Pachytene arrest and other meiotic effects of the Start mutations in Saccharomyces cerevisiae. Genetics 123: 29–43
Simchen G (1974) Are mitotic functions required in meiosis? Genetics 76: 745–753
Simchen G, Idar D, Kassir Y (1976) Recombination and hydroxyurea inhibirion of DNA synthesis in yeast meiosis. Mol Gen Genet 144: 21–27
Snyder M, Sapolsky RJ, Davis RW (1988) Transcription interferes with elements important for chromosome maintenance in Saccharomyces cerevisiae. Mol Cell Biol 8: 2184–2194
Tschumper G, Carbon J (1980) Sequence of a yeast DNA fragment containing a chromosomal replicator and the TRP1 gene. Gene 10: 157–166
Williamson DH, Johnston LH, Fennell DJ, Simchen G (1980) Premeiotic DNA synthesis in Saccharomyces cereevisiae: replicon size and rate of fork movement. In: Tenth international conference on yeast genetics and molecular biology. Louvain-la-Neuve, Belgium, p 181
Author information
Authors and Affiliations
Additional information
Communicated by: J. Huberman
Rights and permissions
About this article
Cite this article
Hollingsworth, R.E., Sclafani, R.A. Yeast pre-meiotic DNA replication utilizes mitotic origin ARS1 independently of CDC7 function. Chromosoma 102, 415–420 (1993). https://doi.org/10.1007/BF00360406
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00360406