Skip to main content
Log in

Exiting prophase I: no clear boundary

  • Review
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

The meiotic cell cycle provides a unique model to study the relationship between recombinational DNA repair and the cell cycle, since homologous recombination, induced by programmed DNA double-strand breaks (DSBs), is integrated as an essential step during meiosis. The pachytene checkpoint, which is situated towards the end of meiotic prophase I, coordinates homologous recombination and cell cycle progression, similar to the DNA damage checkpoint mechanisms operating in vegetative cells. However, there are a number of features unique to meiosis, making the system optimized for the purpose of meiosis. Our recent work highlights the involvement of three major cell cycle kinases, Dbf4-dependent Cdc7 kinase, Polo kinase and CDK, in coordinating homologous recombination and the meiotic cell cycle. In this review, we will discuss the unique interplay between meiotic cell cycle control and homologous recombination during meiosis I.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Argunhan B, Farmer S, Leung W-K et al (2013) Direct and indirect control of the initiation of meiotic recombination by DNA damage checkpoint mechanisms in budding yeast. PLoS One 8:e65875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Argunhan B, Leung W, Afshar N et al (2017) Fundamental cell cycle kinases collaborate to ensure timely destruction of the synaptonemal complex during meiosis. EMBO J 36:2488–2509

    CAS  PubMed  Google Scholar 

  • Bailis JM, Roeder GS (1998) Synaptonemal complex morphogenesis and sister-chromatid cohesion require Mek1-dependent phosphorylation of a meiotic chromosomal protein. Genes Dev 12:3551–3563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bartek J, Lukas J (2007) DNA damage checkpoints: from initiation to recovery or adaptation. Curr Opin Cell Biol 19:238–245

    Article  CAS  PubMed  Google Scholar 

  • Cahoon CK, Hawley RS (2016) Regulating the construction and demolition of the synaptonemal complex. Nat Struct Mol Biol 23:369–377

    Article  PubMed  Google Scholar 

  • Carlile TM, Amon A (2008) Meiosis I is established through division-specific translational control of a cyclin. Cell 133:280–291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chu S, DeRisi J, Eisen M et al (1998) The transcriptional program of sporulation in budding yeast. Science 282:699–705

    Article  CAS  PubMed  Google Scholar 

  • Cloud V, Chan Y-L, Grubb J et al (2012) Rad51 is an accessory factor for Dmc1-mediated joint molecule formation during meiosis. Science 337:1222–1225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding DQ, Haraguchi T, Hiraoka Y (2016) A cohesin-based structural platform supporting homologous chromosome pairing in meiosis. Curr Genet 62:499–502

    Article  CAS  PubMed  Google Scholar 

  • Falck J, Coates J, Jackson SP (2005) Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434:605–611

    Article  CAS  PubMed  Google Scholar 

  • Gerton JL, Hawley RS (2005) Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat Rev Genet 6:477–487

    Article  CAS  PubMed  Google Scholar 

  • Gimble FS, Thorner J (1992) Homing of a DNA endonuclease gene by meiotic gene conversion in Saccharomyces cerevisiae. Nature 357:301–306

    Article  CAS  PubMed  Google Scholar 

  • Gray S, Allison M, Garcia V et al (2013) Positive regulation of meiotic DNA double-strand break formation by activation of the DNA damage checkpoint kinase Mec1(ATR). Open Biol 3:130019

    Article  PubMed  PubMed Central  Google Scholar 

  • Hartwell LH, Weinert TA (1989) Checkpoints: controls that ensure the order of cell cycle events. Science 246:629–634

    Article  CAS  PubMed  Google Scholar 

  • Humphryes N, Leung WK, Argunhan B et al (2013) The Ecm11-Gmc2 complex promotes synaptonemal complex formation through assembly of transverse filaments in budding yeast. PLoS Genet 9:e1003194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin L, Neiman AM (2016) Post-transcriptional regulation in budding yeast meiosis. Curr Genet 62:313–315

    Article  CAS  PubMed  Google Scholar 

  • Lee SE, Moore JK, Holmes A et al (1998) Saccharomyces Ku70, Mre11/Rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94:399–409

    Article  CAS  PubMed  Google Scholar 

  • Leung WK, Humphryes N, Afshar N et al (2015) The synaptonemal complex is assembled by a polySUMOylation-driven feedback mechanism in yeast. J Cell Biol 211:785–793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lo HC, Kunz RC, Chen X et al (2012) Cdc7–Dbf4 is a gene-specific regulator of meiotic transcription in yeast. Mol Cell Biol 32:541–557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matos J, Lipp JJ, Bogdanova A et al (2008) Dbf4-dependent Cdc7 kinase links DNA replication to the segregation of homologous chromosomes in meiosis I. Cell 135:662–678

    Article  CAS  PubMed  Google Scholar 

  • Nogami S, Fukuda T, Nagai Y et al (2002) Homing at an extragenic locus mediated by VDE (PI-SceI) in Saccharomyces cerevisiae. Yeast 19:773–782

    Article  CAS  PubMed  Google Scholar 

  • Okaz E, Argüello-Miranda O, Bogdanova A et al (2012) Meiotic prophase requires proteolysis of M phase regulators mediated by the meiosis-specific APC/CAma1. Cell 151:603–618

    Article  CAS  PubMed  Google Scholar 

  • Petronczki M, Siomos MF, Nasmyth K (2003) Un ménage à quatre: the molecular biology of chromosome segregation in meiosis. Cell 112:423–440

    Article  CAS  PubMed  Google Scholar 

  • Princz LN, Wild P, Bittmann J et al (2017) Dbf4-dependent kinase and the Rtt107 scaffold promote Mus81–Mms4 resolvase activation during mitosis. EMBO J:e201694831

  • Prugar E, Burnett C, Chen X et al (2017) Coordination of double strand break repair and meiotic progression in yeast by a Mek1-Ndt80 negative feedback loop. Genetics 206:497–512

    Article  PubMed  Google Scholar 

  • Rockmill B, Lichten M, Lefrançois P et al (2013) High throughput sequencing reveals alterations in the recombination signatures with diminishing Spo11 activity. PLoS Genet 9:e1003932

    Article  PubMed  PubMed Central  Google Scholar 

  • Roeder GS (1997) Meiotic chromosomes: it takes two to tango. Genes Dev 11:2600–2621

    Article  CAS  PubMed  Google Scholar 

  • Roeder GS, Bailis JM (2000) The pachytene checkpoint. Trends Genet 16:395–403

    Article  CAS  PubMed  Google Scholar 

  • Sasanuma H, Hirota K, Fukuda T et al (2008) Cdc7-dependent phosphorylation of Mer2 facilitates initiation of yeast meiotic recombination. Genes Dev 22:398–410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwacha A, Kleckner N (1997) Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 90:1123–1135

    Article  CAS  PubMed  Google Scholar 

  • Shiloh Y (2003) ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 3:155–168

    Article  CAS  PubMed  Google Scholar 

  • Sourirajan A, Lichten M (2008) Polo-like kinase Cdc5 drives exit from pachytene during budding yeast meiosis. Genes Dev 22:2627–2632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Subramanian VV, Hochwagen A (2014) The meiotic checkpoint network: step-by-step through meiotic prophase. Cold Spring Harb Perspect Biol 6:a016675-a016675

    Article  Google Scholar 

  • Subramanian VV, MacQueen AJ, Vader G et al (2016) Chromosome synapsis alleviates Mek1-dependent suppression of meiotic DNA repair. PLoS Biol 14:e1002369

    Article  PubMed  PubMed Central  Google Scholar 

  • Thacker D, Mohibullah N, Zhu X et al (2014) Homologue engagement controls meiotic DNA break number and distribution. Nature 510:241–246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsubouchi H, Roeder GS (2006) Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. Genes Dev 20:1766–1775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • West SC, Blanco MG, Chan YW et al (2015) Resolution of recombination intermediates: mechanisms and regulation. Cold Spring Harbor Symp Quant Biol 80:103–109

    Article  PubMed  Google Scholar 

  • Winter E (2012) The Sum1/Ndt80 transcriptional switch and commitment to meiosis in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 76:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu L, Ajimura M, Padmore R et al (1995) NDT80, a meiosis-specific gene required for exit from pachytene in Saccharomyces cerevisiae. Mol Cell Biol 15:6572–6581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33:603–754

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hideo Tsubouchi.

Additional information

Communicated by M. Kupiec.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tsubouchi, H., Argunhan, B. & Tsubouchi, T. Exiting prophase I: no clear boundary. Curr Genet 64, 423–427 (2018). https://doi.org/10.1007/s00294-017-0771-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-017-0771-y

Keywords

Navigation