Skip to main content
Log in

The nature of meiotic chromosome dynamics and recombination in budding yeast

  • Minireview
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

During meiosis, crossing over allows for the exchange of genes between homologous chromosomes, enabling their segregation and leading to genetic variation in the resulting gametes. Spo11, a topoisomerase-like protein expressed in eukaryotes, and diverse accessory factors induce programmed double-strand breaks (DSBs) to initiate meiotic recombination during the early phase of meiosis after DNA replication. DSBs are further repaired via meiosis-specific homologous recombination. Studies on budding yeast have provided insights into meiosis and genetic recombination and have improved our understanding of higher eukaryotic systems. Cohesin, a chromosome-associated multiprotein complex, mediates sister chromatid cohesion (SCC), and is conserved from yeast to humans. Diverse cohesin subunits in budding yeast have been identified in DNA metabolic pathways, such as DNA replication, chromosome segregation, recombination, DNA repair, and gene regulation. During cell cycle, SCC is established by multiple cohesin subunits, which physically bind sister chromatids together and modulate proteins that involve in the capturing and separation of sister chromatids. Cohesin components include at least four core subunits that establish and maintain SCC: two structural maintenance chromosome subunits (Smc1 and Smc3), an α-kleisin subunit (Mcd1/Scc1 during mitosis and Rec8 during meiosis), and Scc3/Irr1 (SA1 and SA2). In addition, the cohesin-associated factors Pds5 and Rad61 regulate structural modifications and cell cyclespecific dynamics of chromatin to ensure accurate chromosome segregation. In this review, we discuss SCC and the recombination pathway, as well as the relationship between the two processes in budding yeast, and we suggest a possible conserved mechanism for meiotic chromosome dynamics from yeast to humans.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Agarwal, S. and Roeder, G.S. 2000. Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102, 245–255.

    CAS  PubMed  Google Scholar 

  • Bishop, D.K. and Zickler, D. 2004. Early decision: Meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117, 9–15.

    Article  CAS  PubMed  Google Scholar 

  • Börner, G.V., Kleckner, N., and Hunter, N. 2004. Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117, 29–45.

    Article  PubMed  Google Scholar 

  • Brar, G.A., Kiburz, B.M., Zhang, Y., Kim, J.E., White, F., and Amon, A. 2006. Rec8 phosphorylation and recombination promote the step-wise loss of cohesins in meiosis. Nature 441, 532–536.

    Article  CAS  PubMed  Google Scholar 

  • Brooker, A.S. and Berkowitz, K.M. 2014. The roles of cohesins in mitosis, meiosis, and human health and disease. Methods Mol. Biol. 1170, 229–266.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown, M.S., Grubb, J., Zhang, A., Rust, M.J., and Bishop, D.K. 2015. Small Rad51 and Dmc1 complexes often co-occupy both ends of a meiotic DNA double strand break. PLoS Genet. 11, e1005653.

    Article  CAS  Google Scholar 

  • Cejka, P., Cannavo, E., Polaczek, P., Masuda-Sasa, T., Pokharel, S., Campbell, J.L., and Kowalczykowski, S.C. 2010. DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature 467, 112–116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Challa, K., Lee, M.S., Shinohara, M., Kim, K.P., and Shinohara, A. 2016. Rad61/Wpl1 (Wapl), a cohesin regulator, controls chromosome compaction during meiosis. Nucleic Acids Res. 44, 3190–3203.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan, K.L., Gligoris, T., Upcher, W., Kato, Y., Shirahige, K., Nasmyth, K., and Beckouët, F. 2013. Pds5 promotes and protects cohesin acetylation. Proc. Natl. Acad. Sci. USA 110, 13020–13025.

    Article  PubMed  Google Scholar 

  • Cheng, C.H., Lo, Y.H., Liang, S.S., Ti, S.C., Lin, F.M., Yeh, C.H., Huang, H.Y., and Wang, T.F. 2006. SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev. 20, 2067–2081.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi, D.H., Lee, R., Kwon, S.H., and Bae, S.H. 2013. Hrq1 functions independently of Sgs1 to preserve genome integrity in Saccharomyces cerevisiae. J. Microbiol. 51, 105–112.

    Article  CAS  PubMed  Google Scholar 

  • Chua, P.R. and Roeder, G.S. 1998. Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93, 349–359.

    Article  CAS  PubMed  Google Scholar 

  • Chung, W.H. 2014. To peep into Pif1 helicase: Multifaceted all the way from genome stability to repair-associated DNA synthesis. J. Microbiol. 52, 89–98.

    Article  CAS  PubMed  Google Scholar 

  • Cloud, V., Chan, Y.L., Grubb, J., Budke, B., and Bishop, D.K. 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 

  • Deardorff, M.A., Wilde, J.J., Albrecht, M., Dickinson, E., Tennstedt, S., Braunholz, D., Mönnich, M., Yan, Y., Xu, W., Gil-Rodríguez, M.C., et al. 2012. RAD21 mutations cause a human cohesinopathy. Am. J. Hum. Genet. 90, 1014–1027.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DeMare, L.E., Leng, J., Cotney, J., Reilly, S.K., Yin, J., Sarro, R., and Noonan, J.P. 2013. The genomic landscape of cohesin-associated chromatin interactions. Genome Res. 23, 1224–1234.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denison, S.H., Käfer, E., and May, G.S. 1993. Mutation in the bimD gene of Aspergillus nidulans confers a conditional mitotic block and sensitivity to DNA damaging agents. Genetics 134, 1085–1096.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gligoris, T.G., Scheinost, J.C., Bürmann, F., Petela, N., Chan, K.L., Uluocak, P., Beckouët, F., Gruber, S., Nasmyth, K., and Löwe, J. 2014. Closing the cohesin ring: structure and function of its Smc3- kleisin interface. Science 346, 963–967.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gruber, S., Haering, C.H., and Nasmyth, K. 2003. Chromosomal cohesin forms a ring. Cell 112, 765–777.

    Article  CAS  PubMed  Google Scholar 

  • Guacci, V., Yamamoto, A., Strunnikov, A., Kingsbury, J., Hogan, E., Meluh, P., and Koshland, D. 1993. Structure and function of chromosomes in mitosis of budding yeast, pp. 677–685. In Cold spring harbor symposia on quantitative biology Vol. 58. Cold Spring Harbor Laboratory Press.

    Google Scholar 

  • Gullerova, M. and Proudfoot, N.J. 2008. Cohesin complex promotes transcriptional termination between convergent genes in S. pombe. Cell 132, 983–995.

    Article  CAS  PubMed  Google Scholar 

  • Haering, C.H., Farcas, A.M., Arumugam, P., Metson, J., and Nasmyth, K. 2008. The cohesin ring concatenates sister DNA molecules. Nature 454, 297–301.

    Article  CAS  PubMed  Google Scholar 

  • Haering, C.H., Löwe, J., Hochwagen, A., and Nasmyth, K. 2002. Molecular architecture of SMC proteins and the yeast cohesin complex. Mol. Cell 9, 773–788.

    Article  CAS  PubMed  Google Scholar 

  • Haering, C.H., Schoffnegger, D., Nishino, T., Helmhart, W., Nasmyth, K., and Löwe, J. 2004. Structure and stability of cohesin’s Smc1-kleisin interaction. Mol. Cell 15, 951–964.

    Article  CAS  PubMed  Google Scholar 

  • Hartman, T., Stead, K., Koshland, D., and Guacci, V. 2000. Pds5p is an essential chromosomal protein required for both sister chromatid cohesion and condensation in Saccharomyces cerevisiae. J. Cell Biol. 151, 613–626.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirano, M. and Hirano, T. 2002. Hinge-mediated dimerization of SMC protein is essential for its dynamic interaction with DNA. EMBO J. 21, 5733–5744.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong, S., Sung, Y., Yu, M., Lee, M., Kleckner, N., and Kim, K.P. 2013. The logic and mechanism of homologous recombination partner choice. Mol. Cell 51, 440–453.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horsfield, J.A., Print, C.G., and Mönnich, M. 2012. Diverse developmental disorders from the one ring: distinct molecular pathways underlie the cohesinopathies. Front. Genet. 3, 171.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hunter, N. and Kleckner, N. 2001. The single-end invasion: an asymmetric intermediate at the double-strand break to double-Holliday junction transition of meiotic recombination. Cell 106, 59–70.

    Article  CAS  PubMed  Google Scholar 

  • Jin, H., Guacci, V., and Yu, H.G. 2009. Pds5 is required for homologue pairing and inhibits synapsis of sister chromatids during yeast meiosis. J. Cell Biol. 186, 713–725.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katis, V.L., Lipp, J.J., Imre, R., Bogdanova, A., Okaz, E., Habermann, B., Mechtler, K., Nasmyth, K., and Zachariae, W. 2010. Rec8 phosphorylation by casein kinase 1 and Cdc7-Dbf4 kinase regulates cohesin cleavage by separase during meiosis. Dev. Cell 18, 397–409.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keeney, S. 2001. Mechanism and control of meiotic recombination initiation. Curr. Top. Dev. Biol. 52, 1–53.

    Article  CAS  PubMed  Google Scholar 

  • Kim, K.P. and Mirkin, E.V. 2018. So similar yet so different: The two ends of a double strand break. Mutat. Res. 809, 70–80.

    Article  CAS  PubMed  Google Scholar 

  • Kim, K.P., Weiner, B.M., Zhang, L., Jordan, A., Dekker, J., and Kleckner, N. 2010. Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143, 924–937.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klein, F., Mahr, P., Galova, M., Buonomo, S.B., Michaelis, C., Nairz, K., and Nasmyth, K. 1999. A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98, 91–103.

    Article  CAS  PubMed  Google Scholar 

  • Kowalec, P., Fronk, J., and Kurlandzka, A. 2017. The Irr1/Scc3 protein implicated in chromosome segregation in Saccharomyces cerevisiae has a dual nuclear-cytoplasmic localization. Cell Div. 12, 1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krantz, I.D., McCallum, J., DeScipio, C., Kaur, M., Gillis, L.A., Yaeger, D., Jukofsky, L., Wasserman, N., Bottani, A., Morris, C.A., et al. 2004. Cornelia de Lange syndrome is caused by mutations in NIPBL, the human homolog of Drosophila melanogaster Nipped- B. Nat. Genet. 36, 631–635.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kueng, S., Hegemann, B., Peters, B.H., Lipp, J.J., Schleiffer, A., Mechtler, K., and Peters, J.M. 2006. Wapl controls the dynamic association of cohesin with chromatin. Cell 127, 955–967.

    Article  CAS  PubMed  Google Scholar 

  • Kulemzina, I., Schumacher, M.R., Verma, V., Reiter, J., Metzler, J., Failla, A.V., Lanz, C., Sreedharan, V.T., Rätsch, G., and Ivanov, D. 2012. Cohesin rings devoid of Scc3 and Pds5 maintain their stable association with the DNA. PLoS Genet. 8, e1002856.

    Article  CAS  Google Scholar 

  • Lao, J.P., Cloud, V., Huan, C.C., Grubb, J., Thacker, D., Lee, C.Y., Dresser, M.E., Hunter, N., and Bishop, D.K. 2013. Meiotic crossover control by concerted action of Rad51-Dmc1 in homolog template bias and robust homeostatic regulation. PLoS Genet. 9, e1003978.

    Article  CAS  Google Scholar 

  • Lao, O., Lu, T.T., Nothnagel, M., Junge, O., Freitag-Wolf, S., Caliebe, A., Balascakova, M., Bertranpetit, J., Bindoff, L.A., Comas, D., et al. 2008. Correlation between genetic and geographic structure in Europe. Curr. Biol. 18, 1241–1248.

    Article  CAS  PubMed  Google Scholar 

  • Lara-Pezzi, E., Pezzi, N., Prieto, I., Barthelemy, I., Carreiro, C., Martínez, A., Maldonado-Rodríguez, A., López-Cabrera, M., and Barbero, J.L. 2004. Evidence of a transcriptional co-activator function of cohesin STAG/SA/Scc3. J. Biol. Chem. 279, 6553–6559.

    Article  CAS  PubMed  Google Scholar 

  • Larionov, V., Karpova, T., Kouprina, N., and Jouravleva, G. 1985. A mutant of Saccharomyces cerevisiae with impaired maintenance of centromeric plasmids. Curr. Genet. 10, 15–20.

    Article  CAS  PubMed  Google Scholar 

  • Laurent, J.M., Young, J.H., Kachroo, A.H., and Marcotte, E.M. 2016. Efforts to make and apply humanized yeast. Brief Funct. Genomics 15, 155–163.

    Article  CAS  PubMed  Google Scholar 

  • Lee, J., Okada, K., Ogushi, S., Miyano, T., Miyake, M., and Yamashita, M. 2006. Loss of Rec8 from chromosome arm and centromere region is required for homologous chromosome separation and sister chromatid separation, respectively, in mammalian meiosis. Cell Cycle 5, 1448–1455.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y., Muir, K.W., Bowler, M.W., Metz, J., Haering, C.H., and Panne, D. 2018. Structural basis for Scc3-dependent cohesin recruitment to chromatin. Elife 7, e38356.

    Article  Google Scholar 

  • Lin, W., Jin, H., Liu, X., Hampton, K., and Yu, H.G. 2011. Scc2 regulates gene expression by recruiting cohesin to the chromosome as a transcriptional activator during yeast meiosis. Mol. Biol. Cell 22, 1985–1996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, J., Feldman, R., Zhang, Z., Deardorff, M.A., Haverfield, E.V., Kaur, M., Li, J.R., Clark, D., Kline, A.D., Waggoner, D.J., et al. 2009. SMC1A expression and mechanism of pathogenicity in probands with X-linked Cornelia de Lange syndrome. Hum. Mutat. 30, 1535–1542.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Longhese, M.P., Bonetti, D., Guerini, I., Manfrini, N., and Clerici, M. 2009. DNA double-strand breaks in meiosis: checking their formation, processing and repair. DNA Repair (Amst.) 8, 1127–1138.

    Article  CAS  Google Scholar 

  • Lopez-Serra, L., Lengronne, A., Borges, V., Kelly, G., and Uhlmann, F. 2013. Budding yeast Wapl controls sister chromatid cohesion maintenance and chromosome condensation. Curr. Biol. 23, 64–69.

    Article  CAS  PubMed  Google Scholar 

  • Losada, A. and Hirano, T. 2005. Dynamic molecular linkers of the genome: the first decade of SMC proteins. Genes Dev. 19, 1269–1287.

    Article  CAS  PubMed  Google Scholar 

  • Lukaszewicz, A., Shodhan, A., and Loidl, J. 2015. Exo1 and Mre11 execute meiotic DSB end resection in the protist Tetrahymena. DNA Repair 35, 137–143.

    Article  CAS  PubMed  Google Scholar 

  • Makrantoni, V. and Marston, A.L. 2018. Cohesin and chromosome segregation. Curr. Biol. 28, R688–R693.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mannini, L., Liu, J., Krantz, I.D., and Musio, A. 2010. Spectrum and consequences of SMC1A mutations: the unexpected involvement of a core component of cohesin in human disease. Hum. Mutat. 31, 5–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marcon, E. and Moens, P.B. 2005. The evolution of meiosis: recruitment and modification of somatic DNA-repair proteins. Bioessays 27, 795–808.

    Article  CAS  PubMed  Google Scholar 

  • Markowitz, T.E., Suarez, D., Blitzblau, H.G., Patel, N.J., Markhard, A.L., MacQueen, A.J., and Hochwagen, A. 2017. Reduced dosage of the chromosome axis factor Red1 selectively disrupts the meiotic recombination checkpoint in Saccharomyces cerevisiae. PLoS Genet. 13, e1006928.

    Article  CAS  Google Scholar 

  • Marston, A.L. 2014. Chromosome segregation in budding yeast: sister chromatid cohesion and related mechanisms. Genetics 196, 31–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Melby, T.E., Ciampaglio, C.N., Briscoe, G., and Erickson, H.P. 1998. The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long, antiparallel coiled coils, folded at a flexible hinge. J. Cell Biol. 142, 1595–1604.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Misulovin, Z., Pherson, M., Gause, M., and Dorsett, D. 2018. Brca2, Pds5 and Wapl differentially control cohesin chromosome association and function. PLoS Genet. 14, e1007225.

    Article  CAS  Google Scholar 

  • Molnar, M., Bahler, J., Sipiczki, M., and Kohli, J. 1995. The rec8 gene of Schizosaccharomyces pombe is involved in linear element formation, chromosome pairing and sister-chromatid cohesion during meiosis. Genetics 141, 61–73.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Monnich, M., Kuriger, Z., Print, C.G., and Horsfield, J.A. 2011. A zebrafish model of Roberts syndrome reveals that Esco2 depletion interferes with development by disrupting the cell cycle. PLoS One 6, e20051.

    Article  CAS  Google Scholar 

  • Morin, I., Ngo, H.P., Greenall, A., Zubko, M.K., Morrice, N., and Lydall, D. 2008. Checkpoint-dependent phosphorylation of Exo1 modulates the DNA damage response. EMBO J. 27, 2400–2410.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moynahan, M.E. and Jasin, M. 2010. Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat. Rev. Mol. Cell Biol. 11, 196–207.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muir, K.W., Kschonsak, M., Li, Y., Metz, J., Haering, C.H., and Panne, D. 2016. Structure of the Pds5-Scc1 complex and implications for cohesin function. Cell Rep. 14, 2116–2126.

    Article  CAS  PubMed  Google Scholar 

  • Musio, A., Selicorni, A., Focarelli, M.L., Gervasini, C., Milani, D., Russo, S., Vezzoni, P., and Larizza, L. 2006. X-linked Cornelia de Lange syndrome owing to SMC1L1 mutations. Nat. Genet. 38, 528–530.

    Article  CAS  PubMed  Google Scholar 

  • Nanbu, T., Nguyễn, L.C., Habib, A.G., Hirata, N., Ukimori, S., Tanaka, D., Masuda, K., Takahashi, K., Yukawa, M., Tsuchiya, E., et al. 2015. Fission yeast Exo1 and Rqh1-Dna2 redundantly contribute to resection of uncapped telomeres. PLoS One 10, e0140456.

    Article  CAS  Google Scholar 

  • Nasmyth, K. and Haering, C.H. 2009. Cohesin: its roles and mechanisms. Annu. Rev. Genet. 43, 525–558.

    Article  CAS  PubMed  Google Scholar 

  • Nasmyth, K., Peters, J.M., and Uhlmann, F. 2000. Splitting the chromosome: Cutting the ties that bind sister chromatids. Science 288, 1379–1385.

    Article  CAS  PubMed  Google Scholar 

  • Neale, M.J., Pan, J., and Keeney, S. 2005. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436, 1053–1057.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • New, J.H., Sugiyama, T., Zaitseva, E., and Kowalczykowski, S.C. 1998. Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature 391, 407–410.

    Article  CAS  PubMed  Google Scholar 

  • Niu, H., Chung, W.H., Zhu, Z., Kwon, Y., Zhao, W., Chi, P., Prakash, R., Seong, C., Liu, D., Lu, L., et al. 2010. Mechanism of the ATPdependent DNA end-resection machinery from Saccharomyces cerevisiae. Nature 467, 108–111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orgil, O., Matityahu, A., Eng, T., Guacci, V., Koshland, D., and Onn, I. 2015. A conserved domain in the Scc3 subunit of cohesin mediates the interaction with both Mcd1 and the cohesin loader complex. PLoS Genet. 11, e1005036.

    Article  CAS  Google Scholar 

  • Panizza, S., Tanaka, T., Hochwagen, A., Eisenhaber, F., and Nasmyth, K. 2000. Pds5 cooperates with cohesin in maintaining sister chromatid cohesion. Curr. Biol. 10, 1557–1564.

    Article  CAS  PubMed  Google Scholar 

  • Remeseiro, S., Cuadrado, A., Kawauchi, S., Calof, A.L., Lander, A.D., and Losada, A. 2013. Reduction of Nipbl impairs cohesin loading locally and affects transcription but not cohesion-dependent functions in a mouse model of Cornelia de Lange Syndrome. Biochim. Biophys. Acta 1831, 2097–2102.

    Article  CAS  Google Scholar 

  • Remeseiro, S. and Losada, A. 2013. Cohesin, a chromatin engagement ring. Curr. Opin. Cell Biol. 25, 63–71.

    Article  CAS  PubMed  Google Scholar 

  • Rogacheva, M.V., Manhart, C.M., Chen, C., Guarne, A., Surtees, J., and Alani, E. 2014. Mlh1-Mlh3, a meiotic crossover and DNA mismatch repair factor, is a Msh2-Msh3-stimulated endonuclease. J. Biol. Chem. 289, 5664–5673.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rowland, B.D., Roig, M.B., Nishino, T., Kurze, A., Uluocak, P., Mishra, A., Beckouët, F., Underwood, P., Metson, J., Imre, R., et al. 2009. Building sister chromatid cohesion: Smc3 acetylation counteracts an antiestablishment activity. Mol. Cell 33, 763–774.

    Article  CAS  PubMed  Google Scholar 

  • Sasanuma, H., Tawaramoto, M.S., Lao, J.P., Hosaka, H., Sanda, E., Suzuki, M., Yamashita, E., Hunter, N., Shinohara, M., Nakagawa, A., et al. 2013. A new protein complex promoting the assembly of Rad51 filaments. Nat. Commun. 4, 1676.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sekigawa, M., Kunoh, T., Wada, S., Mukai, Y., Ohshima, K., Ohta, S., Goshima, N., Sasaki, R., and Mizukami, T. 2010. Comprehensive screening of human genes with inhibitory effects on yeast growth and validation of a yeast cell-based system for screening chemicals. J. Biomol. Screen 15, 368–378.

    Article  CAS  PubMed  Google Scholar 

  • Serrentino, M.E., Chaplais, E., Sommermeyer, V., and Borde, V. 2013. Differential association of the conserved SUMO ligase Zip3 with meiotic double-strand break sites reveals regional variations in the outcome of meiotic recombination. PLoS Genet. 9, e1003416.

    Article  CAS  Google Scholar 

  • Shinohara, M., Oh, S.D., Hunter, N., and Shinohara, A. 2008. Crossover assurance and crossover interference are distinctly regulated by the ZMM proteins during yeast meiosis. Nat. Genet. 40, 299–309.

    Article  CAS  PubMed  Google Scholar 

  • Storlazzi, A., Tesse, S., Ruprich-Robert, G., Gargano, S., Pöggeler, S., Kleckner, N., and Zickler, D. 2008. Coupling meiotic chromosome axis integrity to recombination. Genes Dev. 22, 796–809.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strunnikov, A.V., Larionov, V.L., and Koshland, D. 1993. SMC1: An essential yeast gene encoding a putative head-rod-tail protein is required for nuclear division and defines a new ubiquitous family. J. Cell Biol. 123, 1635–1648.

    Article  CAS  PubMed  Google Scholar 

  • Sugiyama, T., Zaitseva, E.M., and Kowalczykowski, S.C. 1997. A single-stranded DNA-binding protein is needed for efficient presynaptic complex formation by the Saccharomyces cerevisiae Rad51 protein. J. Biol. Chem. 272, 7940–7945.

    Article  CAS  PubMed  Google Scholar 

  • Sumara, I., Vorlaufer, E., Gieffers, C., Peters, B.H., and Peters, J.M. 2000. Characterization of vertebrate cohesin complexes and their regulation in prophase. J. Cell Biol. 151, 749–762.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun, X., Huang, L., Markowitz, T.E., Blitzblau, H.G., Chen, D., Klein, F., and Hochwagen, A. 2015. Transcription dynamically patterns the meiotic chromosome-axis interface. Elife 10, 4.

    Google Scholar 

  • Sung, P. 1994. Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265, 1241–1243.

    Article  CAS  PubMed  Google Scholar 

  • Sutani, T., Kawaguchi, T., Kanno, R., Itoh, T., and Shirahige, K. 2009. Budding yeast Wpl1(Rad61)-Pds5 complex counteracts sister chromatid cohesion-establishing reaction. Curr. Biol. 19, 492–427.

    Article  CAS  PubMed  Google Scholar 

  • Sym, M., Engebrecht, J.A., and Roeder, G.S. 1993. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72, 365–378.

    Article  CAS  PubMed  Google Scholar 

  • Symington, L.S., Rothstein, R., and Lisby, M. 2014. Mechanisms and regulation of mitotic recombination in Saccharomyces cerevisiae. Genetics 198, 795–835.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szankasi, P. and Smith, G.R. 1995. A role for exonuclease I from S. pombe in mutation avoidance and mismatch correction. Science 267, 1166–1169.

    Article  CAS  PubMed  Google Scholar 

  • Tanaka, K., Hao, Z., Kai, M., and Okayama, H. 2001. Establishment and maintenance of sister chromatid cohesion in fission yeast by a unique mechanism. EMBO J. 20, 5779–5790.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tonkin, E.T., Wang, T.J., Lisgo, S., Bamshad, M.J., and Strachan, T. 2004. NIPBL, encoding a homolog of fungal Scc2-type sister chromatid cohesion proteins and fly Nipped-B, is mutated in Cornelia de Lange syndrome. Nat. Genet. 36, 636–641.

    Article  CAS  PubMed  Google Scholar 

  • Tran, P.T., Erdeniz, N., Symington, L.S., and Liskay, R.M. 2004. EXO1- A multi-tasking eukaryotic nuclease. DNA Repair 3, 1549–1559.

    Article  CAS  PubMed  Google Scholar 

  • Tsubouchi, H. and Ogawa, H. 2000. Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevisiae. Mol. Biol. Cell 11, 2221–2233.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsutsumi, M., Fujiwara, R., Nishizawa, H., Ito, M., Kogo, H., Inagaki, H., Ohye, T., Kato, T., Fujii, T., and Kurahashi, H. 2014. Age-related decrease of meiotic cohesins in human oocytes. PLoS One 9, e96710.

    Article  CAS  Google Scholar 

  • van Heemst, D., James, F., Pöggeler, S., Berteaux-Lecellier, V., and Zickler, D. 1999. Spo76p is a conserved chromosome morphogenesis protein that links the mitotic and meiotic programs. Cell 98, 261–271.

    Article  PubMed  Google Scholar 

  • Vega, H., Waisfisz, Q., Gordillo, M., Sakai, N., Yanagihara, I., Yamada, M., van Gosliga, D., Kayserili, H., Xu, C., Ozono, K., et al. 2005. Roberts syndrome is caused by mutations in ESCO2, a human homolog of yeast ECO1 that is essential for the establishment of sister chromatid cohesion. Nat. Genet. 37, 468–470.

    Article  CAS  PubMed  Google Scholar 

  • Wold, M.S. 1997. Replication protein A: a heterotrimeric, singlestranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem. 66, 61–92.

    Article  CAS  PubMed  Google Scholar 

  • Xu, B., Lu, S., and Gerton, J.L. 2014. A deficit in acetylated cohesin leads to nucleolar dysfunction. Rare Dis. 2, e27743.

    Article  Google Scholar 

  • Yoon, S.W., Lee, M.S., Xaver, M., Zhang, L., Hong, S.G., Kong, Y.J., Cho, H.R., Kleckner, N., and Kim, K.P. 2016. Meiotic prophase roles of Rec8 in crossover recombination and chromosome structure. Nucleic Acids Res. 44, 9296–9314.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yu, H.G. and Koshland, D.E. 2003. Meiotic condensin is required for proper chromosome compaction, SC assembly, and resolution of recombination-dependent chromosome linkages. J. Cell Biol. 163, 937–947.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zakharyevich, K., Ma, Y., Tang, S., Hwang, P.Y., Boiteux, S., and Hunter, N. 2010. Temporally and biochemically distinct activities of Exo1 during meiosis: double-strand break resection and resolution of double holliday junctions. Mol. Cell 40, 1001–1015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, B., Chang, J., Fu, M., Huang, J., Kashyap, R., Salavaggione, E., Jain, S., Shashikant, K., Deardorff, M.A., Uzielli, M.L., et al. 2009. Dosage effects of cohesin regulatory factor PDS5 on mammalian development: implications for cohesinopathies. PLoS One 4, e5232.

    Article  CAS  Google Scholar 

  • Zhang, B., Jain, S., Song, H., Fu, M., Heuckeroth, R.O., Erlich, J.M., Jay, P.Y., and Milbrandt, J. 2007. Mice lacking sister chromatid cohesion protein PDS5B exhibit developmental abnormalities reminiscent of Cornelia de Lange syndrome. Development 134, 3191–3201.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Z., Ren, Q., Yang, H., Conrad, M.N., Guacci, V., Kateneva, A., and Dresser, M.E. 2005. Budding yeast PDS5 plays an important role in meiosis and is required for sister chromatid cohesion. Mol. Microbiol. 56, 670–680.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Keunpil Kim.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hong, S., Joo, J.H., Yun, H. et al. The nature of meiotic chromosome dynamics and recombination in budding yeast. J Microbiol. 57, 221–231 (2019). https://doi.org/10.1007/s12275-019-8541-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-019-8541-9

Keywords

Navigation