Separable Crossover-Promoting and Crossover-Constraining Aspects of Zip1 Activity during Budding Yeast Meiosis

PLoS Genetics

Volumn 11, Issue 6, 2015, Pages

  Voelkel Meiman, Karen ^a   Johnston, Cassandra ^a,c   Thappeta, Yashna ^a,d   Subramanian, Vijayalakshmi V ^b   Hochwagen, Andreas ^b   MacQueen, Amy J ^a  

^a WESLEYAN UNIVERSITY   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c YALE UNIVERSITY   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ECM11 PROTEIN; FUNGAL PROTEIN; MLH3 PROTEIN; MSH4 PROTEIN; MSH5 PROTEIN; SPO16 PROTEIN; UNCLASSIFIED DRUG; ZIP1 PROTEIN; ZIP3 PROTEIN; ZIP4 PROTEIN; DNA BINDING PROTEIN; MLH3 PROTEIN, S CEREVISIAE; MSH4 PROTEIN, S CEREVISIAE; MSH5 PROTEIN, S CEREVISIAE; NUCLEAR PROTEIN; PROTEIN MUTL; PROTEIN MUTS; SACCHAROMYCES CEREVISIAE PROTEIN; ZIP1 PROTEIN, S CEREVISIAE;

ARTICLE; BUDDING; CENTROMERE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CONTROLLED STUDY; CROSSING OVER; CROSSOVER CONSTRAINING; CROSSOVER PROMOTING; FUNGUS SPORE; GENE; KLUYVEROMYCES LACTIS; MEIOSIS; MEIOTIC RECOMBINATION; MUTLY GENE; MUTSY GENE; NONHUMAN; NUCLEIC ACID ANALYSIS; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN FUNCTION; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; SUMOYLATION; SYNAPTONEMAL COMPLEX; YEAST; AMINO ACID SEQUENCE; GENETIC COMPLEMENTATION; GENETICS; KLUYVEROMYCES; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE;

KLUYVEROMYCES LACTIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES; SYNAPSIS;

AMINO ACID SEQUENCE; BASE SEQUENCE; CENTROMERE; CHROMOSOME SEGREGATION; CROSSING OVER, GENETIC; DNA-BINDING PROTEINS; FUNGAL PROTEINS; GENETIC COMPLEMENTATION TEST; KLUYVEROMYCES; MEIOSIS; MOLECULAR SEQUENCE DATA; MUTL PROTEINS; MUTS DNA MISMATCH-BINDING PROTEIN; NUCLEAR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SYNAPTONEMAL COMPLEX;

EID: 84937797598     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005335     Document Type: Article

References (95)

1. Zickler D, Kleckner N, (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33: 603–754. 10690419
2. Bhalla N, Dernburg AF, (2008) Prelude to a division. Annu Rev Cell Dev Biol 24: 397–424. doi: 10.1146/annurev.cellbio.23.090506.123245 18597662
3. Allers T, Lichten M, (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106: 47–57. 11461701
4. De Muyt A, Jessop L, Kolar E, Sourirajan A, Chen J, et al. (2012) BLM helicase ortholog Sgs1 is a central regulator of meiotic recombination intermediate metabolism. Mol Cell 46: 43–53. doi: 10.1016/j.molcel.2012.02.020 22500736
5. Schwacha A, Kleckner N, (1995) Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83: 783–791. 8521495
6. Moses MJ, (1968) Synaptonemal complex. Annu Rev Genet 2: 363–412.
7. Page SL, Hawley RS, (2004) The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20: 525–558. 15473851
8. de Boer E, Heyting C, (2006) The diverse roles of transverse filaments of synaptonemal complexes in meiosis. Chromosoma 115: 220–234. 16523321
9. Dong H, Roeder GS, (2000) Organization of the yeast Zip1 protein within the central region of the synaptonemal complex. J Cell Biol 148: 417–426. 10662769
10. Sym M, Engebrecht J, Roeder GS, (1993) Zip1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72: 365–378. 7916652
11. Hooker GW, Roeder GS, (2006) A role for SUMO in meiotic chromosome synapsis. Curr Biol 16: 1238–1243. 16782016
12. Humphryes N, Leung WK, Argunhan B, Terentyev Y, Dvorackova M, et al. (2013) The Ecm11-Gmc2 complex promotes synaptonemal complex formation through assembly of transverse filaments in budding yeast. PLoS Genet 9: e1003194. doi: 10.1371/journal.pgen.1003194 23326245
13. Voelkel-Meiman K, Taylor LF, Mukherjee P, Humphryes N, Tsubouchi H, et al. (2013) SUMO localizes to the central element of synaptonemal complex and is required for the full synapsis of meiotic chromosomes in budding yeast. PLoS Genet 9: e1003837. doi: 10.1371/journal.pgen.1003837 24098146
14. Fung JC, Rockmill B, Odell M, Roeder GS, (2004) Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116: 795–802. 15035982
15. Agarwal S, Roeder GS, (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102: 245–255. 10943844
16. Chua PR, Roeder GS, (1998) Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93: 349–359. 9590170
17. Shinohara M, Oh SD, Hunter N, Shinohara A, (2008) Crossover assurance and crossover interference are distinctly regulated by the ZMM proteins during yeast meiosis. Nat Genet 40: 299–309. doi: 10.1038/ng.83 18297071
18. Tsubouchi T, Zhao H, Roeder GS, (2006) The meiosis-specific Zip4 protein regulates crossover distribution by promoting synaptonemal complex formation together with Zip2. Dev Cell 10: 809–819. 16740482
19. Sourirajan A, Lichten M, (2008) Polo-like kinase Cdc5 drives exit from pachytene during budding yeast meiosis. Genes Dev 22: 2627–2632. doi: 10.1101/gad.1711408 18832066
20. Roeder GS, (1997) Meiotic chromosomes: it takes two to tango. Genes Dev 11: 2600–2621. 9334324
21. MacQueen AJ, Hochwagen A, (2011) Checkpoint mechanisms: the puppet masters of meiotic prophase. Trends Cell Biol 21: 393–400. doi: 10.1016/j.tcb.2011.03.004 21531561
22. Bhalla N, Dernburg AF, (2005) A conserved checkpoint monitors meiotic chromosome synapsis in Caenorhabditis elegans. Science 310: 1683–1686. 16339446
23. Zakharyevich K, Tang S, Ma Y, Hunter N, (2012) Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase. Cell 149: 334–347. doi: 10.1016/j.cell.2012.03.023 22500800
24. Kohl KP, Sekelsky J, (2013) Meiotic and mitotic recombination in meiosis. Genetics 194: 327–334. doi: 10.1534/genetics.113.150581 23733849
25. Nishant KT, Chen C, Shinohara M, Shinohara A, Alani E, (2010) Genetic analysis of baker's yeast Msh4-Msh5 reveals a threshold crossover level for meiotic viability. PLoS Genet 6. e1001083. doi: 10.1371/journal.pgen.1001083 20865162
26. de los Santos T, Hunter N, Lee C, Larkin B, Loidl J, et al. (2003) The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics 164: 81–94. 12750322
27. Borner GV, Kleckner N, Hunter N, (2004) Crossover/noncrossover differentiation, synaptonemal complex formation and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 1127: 29–45.
28. Argueso JL, Wanat J, Gemici Z, Alani E, (2004) Competing crossover pathways act during meiosis in Saccharomyces cerevisiae. Genetics 168: 1805–1816. 15611158
29. Mercier R, Jolivet S, Vezon D, Huppe E, Chelysheva L, et al. (2005) Two meiotic crossover classes cohabit in Arabidopsis: one is dependent on MER3, whereas the other one is not. Curr Biol 15: 692–701. 15854901
30. Novak JE, Ross-Macdonald P, Roeder GS, (2001) The budding yeast Msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics 158: 1013–1025. 11454751
31. Hunter N, Borts RH, (1997) Mlh1 is unique among mismatch repair proteins in its ability to promote crossing-over during meiosis. Genes Dev 11: 1573–1582. 9203583
32. Santucci-Damanin S, Walpita D, Lespinasse F, Desnuelle C, Ashley T, et al. (2000) MSH4 acts in conjunction with MLH1 during mammalian meiosis. FASEB J 1539–1547.
33. Rogacheva MV, Manhart CM, Chen C, Guarne A, Surtees J, et al. (2014) Mlh1-Mlh3, a meiotic crossover and DNA mismatch repair factor, is a Msh2-Msh3-stimulated endonuclease. J Biol Chem 289: 5664–5673. doi: 10.1074/jbc.M113.534644 24403070
34. Sonntag Brown M, Lim E, Chen C, Nishant KT, Alani E, (2013) Genetic analysis of mlh3 mutations reveals interactions between crossover promoting factors during meiosis in baker's yeast. G3 (Bethesda) 3: 9–22.
35. Hunter N, 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. 11461702
36. Snowden T, Acharya S, Butz C, Berardini M, Fishel R, (2004) hMSH4-hMSH5 recognizes Holliday Junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes. Mol Cell 15: 437–451. 15304223
37. Wang TF, Kleckner N, Hunter N, (1999) Functional specificity of MutL homologs in yeast: evidence for three Mlh1-based heterocomplexes with distinct roles during meiosis in recombination and mismatch correction. Proc Natl Acad Sci U S A 96: 13914–13919. 10570173
38. Ranjha L, Anand R, Cejka P, (2014) The Saccharomyces cerevisiae Mlh1-Mlh3 heterodimer is an endonuclease that preferentially binds to Holliday junctions. J Biol Chem 289: 5674–5686. doi: 10.1074/jbc.M113.533810 24443562
39. Oke A, Anderson CM, Yam P, Fung JC, (2014) Controlling Meiotic Recombinational Repair—Specifying the Roles of ZMMs, Sgs1 and Mus81/Mms4 in Crossover Formation. PLoS Genet 10: e1004690. doi: 10.1371/journal.pgen.1004690 25329811
40. Jessop L, Rockmill B, Roeder GS, Lichten M, (2006) Meiotic chromosome synapsis-promoting proteins antagonize the anti-crossover activity of Sgs1. PLoS Genet 2: e155. 17002499
41. Oh SD, Lao JP, Hwang PY, Taylor AF, Smith GR, et al. (2007) BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules. Cell 130: 259–272. 17662941
42. Zakharyevich K, Ma Y, Tang S, Hwang PY, Boiteux S, et al. (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. doi: 10.1016/j.molcel.2010.11.032 21172664
43. Villeneuve AM, Hillers KJ, (2001) Whence meiosis? Cell 106: 647–650. 11572770
44. Colaiacovo MP, MacQueen AJ, Martinez-Perez E, McDonald K, Adamo A, et al. (2003) Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev Cell 5: 463–474. 12967565
45. Kelly KO, Dernburg AF, Stanfield GM, Villeneuve AM, (2000) Caenorhabditis elegans msh-5 is required for both normal and radiation-induced meiotic crossing over but not for completion of meiosis. Genetics 156: 617–630. 11014811
46. MacQueen AJ, Colaiacovo MP, McDonald K, Villeneuve AM, (2002) Synapsis-dependent and-independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev 16: 2428–2442. 12231631
47. Zalevsky J, MacQueen AJ, Duffy JB, Kemphues KJ, Villeneuve AM, (1999) Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast. Genetics 153: 1271–1283. 10545458
48. Saito TT, Lui DY, Kim HM, Meyer K, Colaiacovo MP, (2013) Interplay between structure-specific endonucleases for crossover control during Caenorhabditis elegans meiosis. PLoS Genet 9: e1003586. doi: 10.1371/journal.pgen.1003586 23874210
49. Agostinho A, Meier B, Sonneville R, Jagut M, Woglar A, et al. (2013) Combinatorial regulation of meiotic holliday junction resolution in C. elegans by HIM-6 (BLM) helicase, SLX-4, and the SLX-1, MUS-81 and XPF-1 nucleases. PLoS Genet 9: e1003591. doi: 10.1371/journal.pgen.1003591 23901331
50. O'Neil NJ, Martin JS, Youds JL, Ward JD, Petalcorin MI, et al. (2013) Joint molecule resolution requires the redundant activities of MUS-81 and XPF-1 during Caenorhabditis elegans meiosis. PLoS Genet 9: e1003582. doi: 10.1371/journal.pgen.1003582 23874209
51. Page SL, Hawley RS, (2001) c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev 15: 3130–3143. 11731477
52. Kohl KP, Jones CD, Sekelsky J, (2012) Evolution of an MCM complex in flies that promotes meiotic crossovers by blocking BLM helicase. Science 338: 1363–1365. doi: 10.1126/science.1228190 23224558
53. Lynn A, Soucek R, Borner GV, (2007) ZMM proteins during meiosis: crossover artists at work. Chromosome Res 15: 591–605. 17674148
54. Storlazzi A, Xu L, Cao L, Kleckner N, (1995) Crossover and noncrossover recombination during meiosis: Timing and pathway relationships. Proc Natl Acad Sci USA 92: 8512–8516. 7667321
55. Storlazzi A, Xu L, Schwacha A, Kleckner N, (1996) Synaptonemal complex (SC) component Zip1 plays a role in meiotic recombination independent of SC polymerization along the chromosomes. Proc Natl Acad Sci USA 93: 9043–9048. 8799151
56. Rockmill B, Fung JC, Branda SS, Roeder GS, (2003) The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over. Curr Biol 13: 1954–1962. 14614820
57. San-Segundo P, Roeder GS, (1999) Pch2 links chromatin silencing to meiotic checkpoint control. Cell 97: 313–324. 10319812
58. Voelkel-Meiman K, Moustafa SS, Lefrancois P, Villeneuve AM, MacQueen AJ, (2012) Full-length synaptonemal complex grows continuously during meiotic prophase in budding yeast. PLoS Genet 8: e1002993. doi: 10.1371/journal.pgen.1002993 23071451
59. Xu L, Ajimura M, Padmore R, Klein C, Kleckner N, (1995) NDT80, a meiosis-specific gene required for exit from pachytene in Saccharomyces cerevisiae. Mol Cell Biol 15: 6572–6581. 8524222
60. Scherthan H, Wang H, Adelfalk C, White EJ, Cowan C, et al. (2007) Chromosome mobility during meiotic prophase in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 104: 16934–16939. 17939997
61. Smith AV, Roeder GS, (1997) The yeast Red1 protein localizes to the cores of meiotic chromosomes. J Cell Biol 136: 957–967. 9060462
62. Rockmill B, Sym M, Scherthan H, Roeder GS, (1995) Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes Dev 9: 2684–2695. 7590245
63. Tsubouchi T, Macqueen AJ, Roeder GS, (2008) Initiation of meiotic chromosome synapsis at centromeres in budding yeast. Genes Dev 22: 3217–3226. doi: 10.1101/gad.1709408 19056898
64. Serrentino ME, Chaplais E, Sommermeyer V, 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. doi: 10.1371/journal.pgen.1003416 23593021
65. Tsubouchi T, Roeder GS, (2005) A synaptonemal complex protein promotes homology-independent centromere coupling. Science 308: 870–873. 15879219
66. Falk JE, Chan AC, Hoffmann E, Hochwagen A, (2010) A Mec1- and PP4-dependent checkpoint couples centromere pairing to meiotic recombination. Dev Cell 19: 599–611. doi: 10.1016/j.devcel.2010.09.006 20951350
67. Newnham L, Jordan P, Rockmill B, Roeder GS, Hoffmann E, (2010) The synaptonemal complex protein, Zip1, promotes the segregation of nonexchange chromosomes at meiosis I. Proc Natl Acad Sci U S A 107: 781–785. doi: 10.1073/pnas.0913435107 20080752
68. Hyland KM, Kingsbury J, Koshland D, Hieter P, (1999) Ctf19p: A novel kinetochore protein in Saccharomyces cerevisiae and a potential link between the kinetochore and mitotic spindle. J Cell Biol 145: 15–28. 10189365
69. Rockmill B, Roeder GS, (1998) Telomere-mediated chromosome pairing during meiosis in budding yeast. Genes Dev 12: 2574–2586. 9716409
70. Sym M, Roeder GS, (1994) Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell 79: 283–292. 7954796
71. Chen SY, Tsubouchi T, Rockmill B, Sandler JS, Richards DR, et al. (2008) Global analysis of the meiotic crossover landscape. Dev Cell 15: 401–415. doi: 10.1016/j.devcel.2008.07.006 18691940
72. Rockmill B, Voelkel-Meiman K, Roeder GS, (2006) Centromere-proximal crossovers are associated with precocious separation of sister chromatids during meiosis in Saccharomyces cerevisiae. Genetics 174: 1745–1754. 17028345
73. Chua PR, Roeder GS, (1997) Tam1, a telomere-associated meiotic protein, functions in chromosome synapsis and crossover interference. Genes Dev 11: 1786–1800. 9242487
74. Malkova A, Swanson J, German M, McCusker JH, Housworth EA, et al. (2004) Gene conversion and crossing over along the 405-kb left arm of Saccharomyces cerevisiae chromosome VII. Genetics 168: 49–63. 15454526
75. Martini E, Diaz RL, Hunter N, Keeney S, (2006) Crossover homeostasis in yeast meiosis. Cell 126: 285–295. 16873061
76. Papazian HP, (1952) The analysis of tetrad data. Genetics 37: 175–188. 17247384
77. Thacker D, Mohibullah N, Zhu X, Keeney S, (2014) Homologue engagement controls meiotic DNA break number and distribution. Nature 510: 241–246. doi: 10.1038/nature13120 24717437
78. Pochart P, Woltering D, Hollingsworth N, (1997) Conserved properties between functionally distinct MutS homologs in yeast. J Biol Chem 272: 30345–30349. 9374523
79. Game JC, Sitney KC, Cook VE, Mortimer RK, (1989) Use of a ring chromosome and pulsed-field gels to study interhomolog recombination, double-strand DNA breaks and sister-chromatid exchange in yeast. Genetics 123: 695–713. 2693206
80. Joshi N, Brown MS, Bishop DK, Borner GV, (2015) Gradual Implementation of the Meiotic Recombination Program via Checkpoint Pathways Controlled by Global DSB Levels. Mol Cell 57: 797–811. doi: 10.1016/j.molcel.2014.12.027 25661491
81. Lao JP, Cloud V, Huang CC, Grubb J, Thacker D, et al. (2013) Meiotic crossover control by concerted action of Rad51-Dmc1 in homolog template bias and robust homeostatic regulation. PLoS Genet 9: e1003978. doi: 10.1371/journal.pgen.1003978 24367271
82. Snowden T, Shim KS, Schmutte C, Acharya S, Fishel R, (2008) hMSH4-hMSH5 adenosine nucleotide processing and interactions with homologous recombination machinery. J Biol Chem 283: 145–154. 17977839
83. Kellis M, Birren BW, Lander ES, (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428: 617–624. 15004568
84. Mitra N, Roeder GS, (2007) A novel nonnull ZIP1 allele triggers meiotic arrest with synapsed chromosomes in Saccharomyces cerevisiae. Genetics 176: 773–787. 17435220
85. Wu H-Y, Burgess SM, (2006) Two distinct surveillance mechanisms monitor meiotic chromosome metabolism in budding yeast. Curr Biol 16: 2473–2479. 17174924
86. Borner GV, Barot A, Kleckner N, (2008) Yeast Pch2 promotes domainal axis organization, timely recombination progression, and arrest of defective recombinosomes during meiosis. Proc Natl Acad Sci U S A 105: 3327–3332. doi: 10.1073/pnas.0711864105 18305165
87. Ho HC, Burgess SM, (2011) Pch2 acts through Xrs2 and Tel1/ATM to modulate interhomolog bias and checkpoint function during meiosis. PLoS Genet 7: e1002351. doi: 10.1371/journal.pgen.1002351 22072981
88. Daniel K, Lange J, Hached K, Fu J, Anastassiadis K, et al. (2011) Meiotic homologue alignment and its quality surveillance are controlled by mouse HORMAD1. Nat Cell Biol 13: 599–610. doi: 10.1038/ncb2213 21478856
89. Santucci-Darmanin S, Neyton S, Lespinasse F, Saunieres A, Gaudray P, et al. (2002) The DNA mismatch-repair MLH3 protein interacts with MSH4 in meiotic cells, supporting a role for this MutL homolog in mammalian meiotic recombination. Hum Mol Genet 11: 1697–1706. 12095912
90. Chan AC, Borts RH, Hoffmann E, (2009) Temperature-dependent modulation of chromosome segregation in msh4 mutants of budding yeast. PLoS One 4: e7284. doi: 10.1371/journal.pone.0007284 19816584
91. Zhang L, Wang S, Yin S, Hong S, Kim KP, et al. (2014) Topoisomerase II mediates meiotic crossover interference. Nature 511: 551–556. doi: 10.1038/nature13442 25043020
92. Perkins DD, (1949) Biochemical Mutants in the Smut Fungus Ustilago Maydis. Genetics 34: 607–626. 17247336
93. Schwacha A, Kleckner N, (1994) Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell 76: 51–63. 8287479
94. Kumar S, Nei M, Dudley J, Tamura K, (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9: 299–306. doi: 10.1093/bib/bbn017 18417537
95. Lupas A, Dyke MV, Stock J, (1991) Predicting coiled-coils from protein sequences. Science 252: 1162–1164. 2031185