Sustained and rapid chromosome movements are critical for chromosome pairing and meiotic progression in budding yeast

Genetics

Volumn 188, Issue 1, 2011, Pages 21-32

  Brown, Megan Sonntag ^a   Zanders, Sarah ^b   Alani, Eric ^a  

^a Department of Obstetrics Gynecology   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE;

ALLELE; ARTICLE; CELL BUDDING; CELL CYCLE PROGRESSION; CELL VIABILITY; CHROMOSOME MOVEMENT; CHROMOSOME PAIRING; CHROMOSOMES AND CHROMOSOMAL PHENOMENA; DOUBLE STRANDED DNA BREAK; FUNGAL STRAIN; FUNGUS SPORE; GENE MUTATION; HOMOLOGOUS RECOMBINATION; MEIOSIS; MEIOTIC PROPHASE I; MUTAGENESIS; MUTANT; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; TELOMERE; WILD TYPE; YEAST;

ALLELES; AMINO ACID SEQUENCE; CHROMOSOME MAPPING; CHROMOSOME PAIRING; CHROMOSOMES, FUNGAL; GREEN FLUORESCENT PROTEINS; MEIOSIS; MICROBIAL VIABILITY; MOLECULAR SEQUENCE DATA; MOVEMENT; MUTATION; SACCHAROMYCES CEREVISIAE PROTEINS; SACCHAROMYCETALES; SPORES, FUNGAL;

SACCHAROMYCETALES;

EID: 79955932442     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.110.125575     Document Type: Article

References (78)

1. Alexandru, G., F. Uhlmann, K. Mechtler, M. A. Poupart and K. Nasmyth, 2001 Phosphorylation of the cohesin subunit Scc1 by Polo/Cdc5 kinase regulates sister chromatid separation in yeast. Cell 105: 459-472.
2. Allers, T., and M. Lichten, 2001 Intermediates of yeast meiotic recombination contain heteroduplex DNA. Mol. Cell 8: 225-231.
3. Argueso, J. L., A. W. Kijas, S. Sarin, J. Heck, M. Waase et al., 2003 Systematic mutagenesis of the Saccharomyces cerevisiae MLH1 gene reveals distinct roles for Mlh1p in meiotic crossing over and in vegetative and meiotic mismatch repair. Mol. Cell. Biol. 23: 873-886.
4. Argueso, J. L., J. Wanat and Z. Gemici, 2004 Competing crossover pathways act during meiosis in Saccharomyces cerevisiae. Genetics 168: 1805-1816.
5. Bass, W. H., 2003 Telomere dynamics unique to meiotic prophase: formation and significance of the bouquet. Cell. Mol. Life Sci. 60: 2319-2324.
6. Belgareh, N., and V. Doye, 1997 Dynamics of nuclear pore distribution in nucleoporin mutant yeast cells. J. Cell Biol. 136: 747-759.
7. Börner, G. V., N. Kleckner and N. Hunter, 2004 Crossover/ noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117: 29-45.
8. Börner, G. V., A. Barot and N. Kleckner, 2008 Yeast Pch2 promotes domainal axis organization, timely recombination progression, and arrest of defective recombinosomes during meiosis. Proc. Natl. Acad. Sci. USA 105: 3327-3332.
9. Brar, G. A., A. Hochwagen, L. S. Ee and A. Amon, 2009 The multiple roles of cohesin in meiotic chromosome morphogenesis and pairing. Mol. Biol. Cell 20: 1030-1047.
10. Buhler, C., V. Borde and M. Lichten, 2007 Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae. PLoS Biol 5: e324.
11. Burgess, S. M., N. Kleckner and B. M. Weiner, 1999 Somatic pairing of homologs in budding yeast: existence and modulation. Genes Dev 13: 1627-1641.
12. Chikashige, Y., C. Tsutsumi, M. Yamane, K. Okamasa, T. Haraguchi et al., 2006 Meiotic proteins Bqt1 and Bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell 125: 59-69.
13. Chikashige, Y., T. Haraguchi and Y. Hiraoka, 2007 Another way to move chromosomes. Chromosoma 116: 497-505.
14. Chua, P. R., and G. S. Roeder, 1997 Tam1, a telomere-associated meiotic protein, functions in chromosome synapsis and crossover interference. Genes Dev 11: 1786-1800.
15. Chua, P. R., and G. S. Roeder, 1998 Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93: 349-359.
16. Conrad, M. N., A. M. Dominguez and M. E. Dresser, 1997 Ndj1p, a meiotic telomere protein required for normal chromosome synapsis and segregation in yeast. Science 276: 1252-1255.
17. Conrad, M. N., C. Y. Lee, J. L. Wilkerson and M. E. Dresser, 2007 MPS3 mediates meiotic bouquet formation in Saccharomy- ces cerevisiae. Proc. Natl. Acad. Sci. USA 104: 8863-8868.
18. Conrad, M. N., C. Y. Lee, G. Chao, M. Shinohara, H. Kosaka et al., 2008 Rapid telomere movement in meiotic prophase is pro moted by NDJ1, MPS3, and CSM4 and is modulated by recombi nation. Cell 133: 1175-1187.
19. Davis, L., and G. R. Smith, 2006 The meiotic bouquet promotes homolog interactions and restricts ectopic recombination in Schizosaccharomyces pombe. Genetics 174: 167-177.
20. de los Santos, T., N. Hunter, C. Lee, B. Larkin, J. Loidl et al., 2003 The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote distinct subset of crossovers during meiosis in budding yeast. Genetics 164: 81-94.
21. Diaz, R. L., A. D. Alcid, J. M. Berger and S. Keeney, 2002 Identification of residues in yeast Spo11p critical for meiotic DNA double-strand break formation. Mol. Cell. Biol. 22: 1106-1115.
22. Galbraith, A. M., S. A. Bullard, K. Jiao, J. J. Nau and R. E. Malone, 1997 Recombination and the progression of meiosis in Saccha-romyces cerevisiae. Genetics 146: 481-489.
23. Gietz, R. D., R. H. Schiestl, A. R. Willems and R. A. Woods, 1995 Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11: 355-360.
24. Goldman, A. S., and M. Lichten, 2000 Restriction of ectopic recombination by interhomolog interactions during Saccharomyces cerevisiae meiosis. Proc. Natl. Acad. Sci. USA 97: 9537-9542.
25. Goldstein, A. L., and J. H. Mccusker, 1999 Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cer-evisiae. Yeast 15: 1541-1553.
26. Golubovskaya, I. N., L. C. Harper, W. P. Pawlowski, D. Schichnes and W. Z. Cande, 2002 The pam1 gene is required for meiotic bouquet formation and efficient homologous synapsis in maize (Zea mays L.). Genetics 162: 1979-1993.
27. Grushcow, J. M., T. M. Holzen, K. J. Park, T. T. Weinert, M. Lichten et al., 1999 Saccharomyces cerevisiae checkpoint genes MEC1, RAD17, and RAD24 are required for normal meiotic recombination partner choice. Genetics 153: 607-620.
28. Harper, L., I. Golubovskaya and W. Z. Cande, 2004 A bouquet of chromosomes. J. Cell Sci 117: 4025-4032.
29. Hassold, T., and P. Hunt, 2001 To err (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2: 280-291.
30. Henderson, K. A., and S. Keeney, 2004 Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks. Proc. Natl. Acad. Sci. USA 101: 4519-4524.
31. Hunter, N., and N. Kleckner, 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.
32. Joseph, I., and A. J. Lustig, 2007 Telomeres in meiotic recombination: the yeast side story. Cell. Mol. Life Sci. 64: 125-130.
33. Joshi, N., A. Barot, C. Jamison and G. V. Börner, 2009 Pch2 links chromosome axis remodeling at future crossover sites and crossover distribution during yeast meiosis. PLoS Genet 5: e1000557.
34. Keeney, S., 2001 Mechanism and control of meiotic recombination initiation Curr. Top. Dev. Biol. 52: 1-53.
35. Kosaka, H., M. Shinohara and A. Shinohara, 2008 Csm4-dependent telomere movement on nuclear envelope promotes meiotic recombination. PLoS Genet 4: e1000196.
36. Koszul, R., K. Kim, M. Prentiss, N. Kleckner and S. Kameoka, 2008 Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope. Cell 133: 1188-1201.
37. Koszul, R., S. Kameoka and B. M. Weiner, 2009 Real-time imaging of meiotic chromosomes in Saccharomyces cerevisiae. Methods Mol. Biol. 558: 81-89.
38. Lacefield, S., and A. W. Murray, 2007 The spindle checkpoint rescues the meiotic segregation of chromosomes whose crossovers are far from the centromere. Nat. Genet. 39: 1273-1277.
39. Lao, J. P., S. D. Oh, M. Shinohara, A. Shinohara and N. Hunter, 2008 Rad52 promotes postinvasion steps of meiotic double-strand-break repair. Mol. Cell 9: 517-524.
40. Loidl, J., F. Klein and H. Scherthan, 1994 Homologous pairing is reduced but not abolished in asynaptic mutants of yeast. J. Cell Biol. 125: 1191-1200.
41. Lydall, D., Y. Nikolsky, D. K. Bishop and T. A. Weinert, 1996 A meiotic recombination checkpoint controlled by mitotic checkpoint genes. Nature 383: 840-843.
42. Mancera, E., R. Bourgon, A. Brozzi, W. Huber and L. M. Steinmetz, 2008 High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454: 479-485.
43. Marston, A. L., W. H. Tham, H. Shah and A. Amon, 2004 A genome-wide screen identifies genes required for centromeric cohesion. Science 303: 367-370.
44. Martinez-Perez, E., and M. P. Colaiácovo, 2009 Distribution of meiotic recombination events: talking to your neighbors. Curr. Opin. Genet. Dev. 19: 105-112.
45. Martini, E., R. L. Diaz, N. Hunter and S. Keeney, 2006 Crossover homeostasis in yeast meiosis. Cell 126: 285-295.
46. Miki, F., A. Kurabayashi, Y. Tange, K. Okazaki, M. Shimanuki et al., 2004 Two- hybrid search for proteins that interact with Sad1 and Kms1, two membrane-bound components of the spindle pole body in fission yeast. Mol. Genet. Genomics 270: 449-461.
47. Niwa, O., M. Shimanuki and F. Miki, 2000 Telomere-led bouquet formation facilitates homologous chromosome pairing and restricts ectopic interaction in fission yeast meiosis. EMBO J. 19: 3831-3840.
48. Page, S. L., and R. S. Hawley, 2004 The genetics and molecular biology of the synaptonemal complex. Annu. Rev. Cell Dev. Biol. 20: 525-558.
49. Parvinen, M., and K. O. Soderstrom, 1976 Chromosome rotation and formation of synapsis. Nature 260: 534-535.
50. Peoples, T. L., E. Dean, O. Gonzalez, L. Lambourne and S. M. Burgess, 2002 Close, stable homolog juxtaposition during mei-osis in budding yeast is dependent on meiotic recombination, occurs independently of synapsis, and is distinct from DSB- independent pairing contacts. Genes Dev. 16: 1682-1695.
51. Rabitsch, K. P., A. Tóth, M. Gálová, A. Schleiffer, G. Schaffner et al., 2001 A screen for genes required for meiosis and spore formation based on whole-genome expression. Curr. Biol. 11: 1001-1009.
52. Rasmussen, S. W., 1986 Chromosome interlocking during synapsis-a transient disorder. Tokai J. Exp. Clin. Med. 11: 437-451.
53. Rockmill, B., and G. S. Roeder, 1998 Telomere-mediated chromosome pairing during meiosis in budding yeast. Genes Dev. 12: 2574-2586.
54. Rockmill, B., K. Voelkel-Meiman and G. S. Roeder, 2006 Centromere-proximal crossovers are associated with precocious separation of sister chromatids during meiosis in Saccharomyces cerevisiae. Genetics 174: 1745-1754.
55. Roeder, G. S., 1997 Meiotic chromosomes: it takes two to tango. Genes Dev. 11: 2600-2621.
56. Rose, M. D., F. Winston and P. Hieter, 1990 Methods in Yeast Genetics: A Laboratory Course Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
57. San-Segundo, P. A., and G. S. Roeder, 1999 Pch2 links chromatin silencing to meiotic checkpoint control. Cell 97: 313-324.
58. Sato, A., B. Isaac, C. M. Phillips, R. Rillo, P. M. Carlton et al., 2009 Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 139: 907-919.
59. Scherthan, H., J. Bahler and J. Kohli, 1994 Dynamics of chromosome organization and pairing during meiotic prophase in fission yeast. J. Cell Biol. 127: 273-285.
60. Scherthan, H., S. Weich, H. Schwegler, C. Heyting, M. Härle et al., 1996 Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J. Cell Biol. 134: 1109-1125.
61. Scherthan, H., H. Wang, C. Adelfalk, E. J. White, C. Cowan et al., 2007 Chromosome mobility during meiotic prophase in Saccha-romyces cerevisiae. Proc. Natl. Acad. Sci. USA 104: 16934-16939.
62. Schwacha, A., and N. Kleckner, 1995 Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83: 783-791.
63. Storlazzi, A., S. Gargano, G. Ruprich-Robert, M. Falque, M. David et al., 2010 Recombination proteins mediate meiotic spatial organization and pairing. Cell 141: 94-106.
64. Tóth, A., K. P. Rabitsch, M. Gálová, A. Schleiffer, S. B. Buonomo et al., 2000 Functional genomics identifies monopolin: a kineto-chore protein required for segregation of homologs during meiosis I. Cell 103: 1155-1168.
65. Trelles-Sticken, E., J. Loidl and H. Scherthan, 1999 Bouquet formation in budding yeast: initiation of recombination is not required for meiotic telomere clustering. J. Cell Sci. 112: 651-658.
66. Trelles-Sticken, E., M. E. Dresser and H. Scherthan, 2000 Meiotic telomere protein Ndj1p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing. J. Cell Biol. 151: 95-106.
67. Trelles-Sticken, E., C. Adelfalk, J. Loidl and H. Scherthan, 2005 Meiotic telomere clustering requires actin for its formation and cohesin for its resolution. J. Cell Biol. 170: 213-223.
68. Tsubouchi, H., and G. S. Roeder, 2003 The importance of genetic recombination for fidelity of chromosome pairing in meiosis. Dev. Cell 5: 915-925.
69. Wach, A., A. Brachat, R. Pohlmann and P. Philippsen, 1994 New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10: 1793-1808.
70. Wanat, J. J., K. P. Kim, R. Koszul, S. Zanders, B. Weiner et al., 2008 Csm4, in collaboration with Ndj1, mediates telomere-led chromosome dynamics and recombination during yeast meiosis. PLoS Genet. 4: e1000188.
71. Weiner, B. M., and N. Kleckner, 1994 Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77: 977-991.
72. Wu, H. Y., and S. M. Burgess, 2006 Ndj1, a telomere-associated protein, promotes meiotic recombination in budding yeast. Mol. Cell. Biol. 26: 3683-3694.
73. Wu, H. Y., H. C. Ho and S. M. Burgess, 2010 Mek1 kinase governs outcomes of meiotic recombination and the checkpoint response. Curr. Biol. 20: 1707-1716.
74. Yamamoto, A., R. R. West, J. R. McIntosh and Y. Hiraoka, 1999 A cytoplasmic dynein heavy chain is required for oscillatory nuclear movement of meiotic prophase and efficient meiotic recombination in fission yeast. J. Cell Biol. 145: 1233-1249.
75. Yang, H. D., and L. A. Pon, 2002 Actin cable dynamics in budding yeast. Proc. Natl. Acad. Sci. USA 99: 751-756.
76. Zanders, S., and E. Alani, 2009 The pch2Delta mutation in baker's yeast alters meiotic crossover levels and confers a defect in crossover interference. PLoS Genet 5: e1000571.
77. Zickler, D., 2006 From early homologue recognition to synaptonemal complex formation. Chromosoma 115: 158-174.
78. Zickler, D., and N. Kleckner, 1999 Meiotic chromosomes: integrating structure and function. Annu. Rev. Genet. 33: 603-754.