Excess crossovers impede faithful meiotic chromosome segregation in C. elegans
Autoři:
Jeremy A. Hollis aff001; Marissa L. Glover aff002; Aleesa J. Schlientz aff002; Cori K. Cahoon aff002; Bruce Bowerman aff002; Sarah M. Wignall aff001; Diana E. Libuda aff002
Působiště autorů:
Department of Molecular Biosciences, Northwestern University, Evanston, IL, United States of America
aff001; Institute of Molecular Biology, Department of Biology, University of Oregon, Eugene, OR, United States of America
aff002
Vyšlo v časopise:
Excess crossovers impede faithful meiotic chromosome segregation in C. elegans. PLoS Genet 16(9): e32767. doi:10.1371/journal.pgen.1009001
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009001
Souhrn
During meiosis, diploid organisms reduce their chromosome number by half to generate haploid gametes. This process depends on the repair of double strand DNA breaks as crossover recombination events between homologous chromosomes, which hold homologs together to ensure their proper segregation to opposite spindle poles during the first meiotic division. Although most organisms are limited in the number of crossovers between homologs by a phenomenon called crossover interference, the consequences of excess interfering crossovers on meiotic chromosome segregation are not well known. Here we show that extra interfering crossovers lead to a range of meiotic defects and we uncover mechanisms that counteract these errors. Using chromosomes that exhibit a high frequency of supernumerary crossovers in Caenorhabditis elegans, we find that essential chromosomal structures are mispatterned in the presence of multiple crossovers, subjecting chromosomes to improper spindle forces and leading to defects in metaphase alignment. Additionally, the chromosomes with extra interfering crossovers often exhibited segregation defects in anaphase I, with a high incidence of chromatin bridges that sometimes created a tether between the chromosome and the first polar body. However, these anaphase I bridges were often able to resolve in a LEM-3 nuclease dependent manner, and chromosome tethers that persisted were frequently resolved during Meiosis II by a second mechanism that preferentially segregates the tethered sister chromatid into the polar body. Altogether these findings demonstrate that excess interfering crossovers can severely impact chromosome patterning and segregation, highlighting the importance of limiting the number of recombination events between homologous chromosomes for the proper execution of meiosis.
Klíčová slova:
Anaphase – Crossover interference – Homologous chromosomes – Chromatin – Chromosome structure and function – Meiosis – Metaphase – Oocytes
Zdroje
1. Gray S, Cohen PE. Control of Meiotic Crossovers: From Double-Strand Break Formation to Designation. Annual Review of Genetics. 2016. p. 175–210. doi: 10.1146/annurev-genet-120215-035111 27648641
2. Muller HJ. The mechanism of crossing-over. Am Nat. 1916;L.(592):193–221.
3. Sturtevant AH. The linear arrangement of six sex-linked factors in Drosophila, as shown by their mode of association. J Exp Zool. 1913;14(1):43–59.
4. Martinez-Perez E, Colaiácovo MP. Distribution of meiotic recombination events: talking to your neighbors. Curr Opin Genet Dev. 2009;19(2):105–12. doi: 10.1016/j.gde.2009.02.005 19328674
5. Libuda DE, Uzawa S, Meyer BJ, Villeneuve AM. Meiotic chromosome structures constrain and respond to designation of crossover sites. Nature. 2013;502(7473):703–6. doi: 10.1038/nature12577 24107990
6. Yokoo R, Zawadzki KA, Nabeshima K, Drake M, Arur S, Villeneuve AM. COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell. 2012;149(1):75–87. doi: 10.1016/j.cell.2012.01.052 22464324
7. Hillers KJ, Villeneuve AM. Chromosome-wide control of meiotic crossing over in C. elegans. Curr Biol. 2003;13(18):1641–7. doi: 10.1016/j.cub.2003.08.026 13678597
8. Martinez-Perez E, Schvarzstein M, Barroso C, Lightfoot J, Dernburg AF, Villeneuve AM. Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion. Genes Dev. 2008;22(20):2886–901. doi: 10.1101/gad.1694108 18923085
9. Nabeshima K, Villeneuve AM, Colaiácovo MP. Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC. J Cell Biol. 2005;168(5):683–9. doi: 10.1083/jcb.200410144 15738262
10. Kaitna S, Pasierbek P, Jantsch M, Loidl J, Glotzer M. The aurora B kinase AIR-2 regulates kinetochores during mitosis and is required for separation of homologous chromosomes during meiosis. Curr Biol. 2002;12(10):798–812. doi: 10.1016/s0960-9822(02)00820-5 12015116
11. Rogers E, Bishop JD, Waddle JA, Schumacher JM, Lin R. The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis. J Cell Biol. 2002;157(2):219–29. doi: 10.1083/jcb.200110045 11940606
12. Wignall SM, Villeneuve AM. Lateral microtubule bundles promote chromosome alignment during acentrosomal oocyte meiosis. Nat Cell Biol. 2009;11(7):839–44. doi: 10.1038/ncb1891 19525937
13. Dumont J, Oegema K, Desai A. A kinetochore-independent mechanism drives anaphase chromosome separation during acentrosomal meiosis. Nat Cell Biol. 2010;12(9):894–901. doi: 10.1038/ncb2093 20729837
14. Mullen TJ, Davis-Roca AC, Wignall SM. Spindle assembly and chromosome dynamics during oocyte meiosis. Curr Opin Cell Biol. 2019;60:53–9. doi: 10.1016/j.ceb.2019.03.014 31082633
15. Connolly AA, Sugioka K, Chuang CH, Lowry JB, Bowerman B. KLP-7 acts through the Ndc80 complex to limit pole number in C. elegans oocyte meiotic spindle assembly. J Cell Biol. 2015;210(6):917–32. doi: 10.1083/jcb.201412010 26370499
16. Han X, Adames K, Sykes EME, Srayko M. The KLP-7 residue S546 is a putative Aurora kinase site required for microtubule regulation at the centrosome in C. elegans. PLoS One. 2015;10(7).
17. Davis-Roca AC, Divekar NS, Ng RK, Wignall SM. Dynamic SUMO remodeling drives a series of critical events during the meiotic divisions in Caenorhabditis elegans. PLoS Genet. 2018;14(9).
18. Pelisch F, Tammsalu T, Wang B, Jaffray EG, Gartner A, Hay RT. A SUMO-Dependent Protein Network Regulates Chromosome Congression during Oocyte Meiosis. Mol Cell. 2017;65(1):66–77. doi: 10.1016/j.molcel.2016.11.001 27939944
19. Muscat CC, Torre-Santiago KM, Tran M V., Powers JA, Wignall SM. Kinetochore-independent chromosome segregation driven by lateral microtubule bundles. Elife. 2015;4:e06462. doi: 10.7554/eLife.06462 26026148
20. Laband K, Le Borgne R, Edwards F, Stefanutti M, Canman JC, Verbavatz JM, et al. Chromosome segregation occurs by microtubule pushing in oocytes. Nat Commun. 2017;8(1).
21. Pelisch F, Bel Borja L, Jaffray EG, Hay RT. Sumoylation regulates protein dynamics during meiotic chromosome segregation in C. elegans oocytes. J Cell Sci. 2019;132(14).
22. Romano A, Guse A, Krascenicova I, Schnabel H, Schnabel R, Glotzer M. CSC-1: A subunit of the Aurora B kinase complex that binds to the survivin-like protein BIR-1 and the incenp-like protein ICP-1. J Cell Biol. 2003;161(2):229–36. doi: 10.1083/jcb.200207117 12707312
23. Schumacher JM, Golden A, Donovan PJ. AIR-2: An Aurora/Ipl1-related protein kinase associated with chromosomes and midbody microtubules is required for polar body extrusion and cytokinesis in Caenorhabditis elegans embryos. J Cell Biol. 1998;143(6):1635–46. doi: 10.1083/jcb.143.6.1635 9852156
24. Siomos MF, Badrinath A, Pasierbek P, Livingstone D, White J, Glotzer M, et al. Separase is required for chromosome segregation during meiosis I in Caenorhabditis elegans. Curr Biol. 2001;11(23):1825–35. doi: 10.1016/s0960-9822(01)00588-7 11728305
25. Davis-Roca AC, Muscat CC, Wignall SM. Caenorhabditis elegans oocytes detect meiotic errors in the absence of canonical end-on kinetochore attachments. J Cell Biol. 2017;216(5):1243–53. doi: 10.1083/jcb.201608042 28356326
26. Mullen TJ, Wignall SM. Interplay between microtubule bundling and sorting factors ensures acentriolar spindle stability during C. elegans oocyte meiosis. PLoS Genet. 2017;
27. Cahoon CK, Helm JM, Libuda DE. Synaptonemal complex central region proteins promote localization of pro-crossover factors to recombination events during caenorhabditis elegans meiosis. Genetics. 2019;213(2):395–409. doi: 10.1534/genetics.119.302625 31431470
28. Nguyen H, Labella S, Silva N, Jantsch V, Zetka M. C. elegans ZHP-4 is required at multiple distinct steps in the formation of crossovers and their transition to segregation competent chiasmata. PLoS Genet. 2018;14(10).
29. Zhang L, Köhler S, Rillo-Bohn R, Dernburg AF. A compartmentalized signaling network mediates crossover control in meiosis. Elife. 2018;7:e30789. doi: 10.7554/eLife.30789 29521627
30. Tzur YB, Egydio de Carvalho C, Nadarajan S, Van Bostelen I, Gu Y, Chu DS, et al. LAB-1 Targets PP1 and Restricts Aurora B Kinase upon Entrance into Meiosis to Promote Sister Chromatid Cohesion. PLoS Biol. 2012;10(8).
31. Howe M, McDonald KL, Albertson DG, Meyer BJ. HIM-10 is required for kinetochore structure and function on Caenorhabditis elegans holocentric chromosomes. J Cell Biol. 2001;153(6):1227–38. doi: 10.1083/jcb.153.6.1227 11402066
32. Monen J, Maddox PS, Hyndman F, Oegema K, Desai A. Differential role of CENP-A in the segregation of holocentric C. elegans chromosomes during meiosis and mitosis. Nat Cell Biol. 2005;7(12):1148–55.
33. Hong Y, Sonneville R, Wang B, Scheidt V, Meier B, Woglar A, et al. LEM-3 is a midbody-tethered DNA nuclease that resolves chromatin bridges during late mitosis. Nat Commun. 2018;9(1).
34. Hong Y, Velkova M, Silva N, Jagut M, Scheidt V, Labib K, et al. The conserved LEM-3/Ankle1 nuclease is involved in the combinatorial regulation of meiotic recombination repair and chromosome segregation in Caenorhabditis elegans. PLoS Genet. 2018;14(6).
35. Wang S, Hassold T, Hunt P, White MA, Zickler D, Kleckner N, et al. Inefficient Crossover Maturation Underlies Elevated Aneuploidy in Human Female Meiosis. Cell. 2017;168(6):977–989.e17. doi: 10.1016/j.cell.2017.02.002 28262352
36. Ferrandiz N, Barroso C, Telecan O, Shao N, Kim HM, Testori S, et al. Spatiotemporal regulation of Aurora B recruitment ensures release of cohesion during C. Elegans oocyte meiosis. Nat Commun. 2018;9(1).
37. Albertson DG, Thomson JN. Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosom Res. 1993;1(1):15–26.
38. Nokkala S, Kuznetsova VG, Maryanska-Nadachowska A, Nokkala C. Holocentric chromosomes in meiosis. I. Restriction of the number of chiasmata in bivalents. Chromosom Res. 2004;12(7):733–9.
39. Wendel JF, Greilhuber J, Leitch IJ, Doležel J. Plant genome diversity. Plant Genome Diversity. 2012. 1–279 p.
40. Melters DP, Paliulis L V., Korf IF, Chan SWL. Holocentric chromosomes: Convergent evolution, meiotic adaptations, and genomic analysis. Chromosom Res. 2012;20(5):579–93.
41. Schvarzstein M, Wignall SM, Villeneuve AM. Coordinating cohesion, co-orientation, and congression during meiosis: Lessons from holocentric chromosomes. Genes Dev. 2010;24(3):219–28. doi: 10.1101/gad.1863610 20123904
42. Altendorfer E, Láscarez-Lagunas LI, Nadarajan S, Mathieson I, Colaiácovo MP. Crossover Position Drives Chromosome Remodeling for Accurate Meiotic Chromosome Segregation. Curr Biol. 2020;30(7):1329–1338.e7. doi: 10.1016/j.cub.2020.01.079 32142707
43. Woglar A, Villeneuve AM. Dynamic Architecture of DNA Repair Complexes and the Synaptonemal Complex at Sites of Meiotic Recombination. Cell. 2018;173(7):1678–1691.e16. doi: 10.1016/j.cell.2018.03.066 29754818
44. Chan KL, Palmai-Pallag T, Ying S, Hickson ID. Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat Cell Biol. 2009;11(6):753–60. doi: 10.1038/ncb1882 19465922
45. Chan KL, North PS, Hickson ID. BLM is required for faithful chromosome segregation and its localization defines a class of ultrafine anaphase bridges. EMBO J. 2007;26(14):3397–409. doi: 10.1038/sj.emboj.7601777 17599064
46. Chan YW, Fugger K, West SC. Unresolved recombination intermediates lead to ultra-fine anaphase bridges, chromosome breaks and aberrations. Nat Cell Biol. 2018;20(1):92–103. doi: 10.1038/s41556-017-0011-1 29255170
47. Hong Y, Sonneville R, Agostinho A, Meier B, Wang B, Blow JJ, et al. The SMC-5/6 Complex and the HIM-6 (BLM) Helicase Synergistically Promote Meiotic Recombination Intermediate Processing and Chromosome Maturation during Caenorhabditis elegans Meiosis. PLoS Genet. 2016;12(3).
48. McVey M, Andersen SL, Broze Y, Sekelsky J. Multiple functions of drosophila BLM helicase in maintenance of genome stability. Genetics. 2007;176(4):1979–92. doi: 10.1534/genetics.106.070052 17507683
49. Schvarzstein M, Pattabiraman D, Libuda DE, Ramadugu A, Tam A, Martinez-Perez E, et al. DNA helicase HIM-6/BLM both promotes mutSγ-dependent crossovers and antagonizes mutSγ-independent interhomolog associations during Caenorhabditis elegans meiosis. Genetics. 2014;198(1):193–207. doi: 10.1534/genetics.114.161513 25053665
50. Agostinho A, Meier B, Sonneville R, Jagut M, Woglar A, Blow J, et al. 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. 2013;9(7).
51. Hughes SE, Hawley RS. Topoisomerase II Is Required for the Proper Separation of Heterochromatic Regions during Drosophila melanogaster Female Meiosis. PLoS Genet. 2014;10(10).
52. Cortes D, McNally K, Mains PE, McNally FJ. The asymmetry of female meiosis reduces the frequency of inheritance of unpaired chromosomes. Elife. 2015;4:e06056. doi: 10.7554/eLife.06056 25848744
53. Vargas E, McNally K, Friedman JA, Cortes DB, Wang DY, Korf IF, et al. Autosomal trisomy and triploidy are corrected during female meiosis in caenorhabditis elegans. Genetics. 2017;207(3):911–22. doi: 10.1534/genetics.117.300259 28882988
54. Akera T, Chmátal L, Trimm E, Yang K, Aonbangkhen C, Chenoweth DM, et al. Spindle asymmetry drives non-Mendelian chromosome segregation. Science (80-). 2017;358(6363):668–72.
55. Crismani W, Girard C, Froger N, Pradillo M, Santos JL, Chelysheva L, et al. FANCM limits meiotic crossovers. Science (80-). 2012;336(6088):1588–90.
56. Girard C, Crismani W, Froger N, Mazel J, Lemhemdi A, Horlow C, et al. FANCM-associated proteins MHF1 and MHF2, but not the other Fanconi anemia factors, limit meiotic crossovers. Nucleic Acids Res. 2014;42(14):9087–95. doi: 10.1093/nar/gku614 25038251
57. Munz P. An analysis of interference in the fission yeast Schizosaccharomyces pombe. Genetics. 1994;137(3):701–7. 8088515
58. Strickland W. An analysis of interference in Aspergillus nidulans. Proc R Soc London Ser B, Biol Sci. 1957;149(934):82–101.
59. Youds JL, Mets DG, McIlwraith MJ, Martin JS, Ward JD, Oneil NJ, et al. RTEL-1 enforces meiotic crossover interference and homeostasis. Science (80-). 2010;327(5970):1254–8.
60. Barber LJ, Youds JL, Ward JD, McIlwraith MJ, O’Neil NJ, Petalcorin MIR, et al. RTEL1 Maintains Genomic Stability by Suppressing Homologous Recombination. Cell. 2008;135(2):261–71. doi: 10.1016/j.cell.2008.08.016 18957201
61. Bilgir C, Dombecki CR, Chen PF, Villeneuve AM, Nabeshima K. Assembly of the Synaptonemal Complex Is a Highly Temperature-Sensitive Process That Is Supported by PGL-1 During Caenorhabditis elegans Meiosis. G3 Genes, Genomes, Genet. 2013;3(4):585–95.
62. MacQueen AJ, Colaiácovo MP, McDonald K, Villeneuve AM. Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev. 2002;16(18):2428–42. doi: 10.1101/gad.1011602 12231631
63. Wang S, Wu D, Quintin S, Green RA, Cheerambathur DK, Ochoa SD, et al. NOCA-1 functions with γ-tubulin and in parallel to Patronin to assemble non-centrosomal microtubule arrays in C. elegans. Elife. 2015;4:e08649. doi: 10.7554/eLife.08649 26371552
64. Kamath RS, Ahringer J. Genome-wide RNAi screening in Caenorhabditis elegans. Methods. 2003;30(4):313–21. doi: 10.1016/s1046-2023(03)00050-1 12828945
65. Zetka MC, Kawasaki I, Strome S, Müller F. Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes Dev. 1999;13(17):2258–70. doi: 10.1101/gad.13.17.2258 10485848
66. MacQueen AJ, Phillips CM, Bhalla N, Weiser P, Villeneuve AM, Dernburg AF. Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell. 2005;123(6):1037–50. doi: 10.1016/j.cell.2005.09.034 16360034
67. Oegema K, Desai A, Rybina S, Kirkham M, Hyman AA. Functional analysis of kinetochore assembly in Caenorhabditis elegans. J Cell Biol. 2001;153(6):1209–25. doi: 10.1083/jcb.153.6.1209 11402065
68. Wolff ID, Tran M V., Mullen TJ, Villeneuve AM, Wignall SM. Assembly of Caenorhabditis elegans acentrosomal spindles occurs without evident microtubuleorganizing centers and requires microtubule sorting by KLP-18/kinesin-12 and MESP-1. Mol Biol Cell. 2016;27(20):3122–31. doi: 10.1091/mbc.E16-05-0291 27559133
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 9
- Může hubnutí souviset s vyšším rizikem nádorových onemocnění?
- Raději si zajděte na oční! Jak souvisí citlivost zraku s rozvojem demence?
- Co způsobuje pooperační infekce? Na vině může být i naše vlastní mikrobiota
- Čeká nás průlom v diagnostice karcinomu pankreatu?
- Polibek, který mi „vzal nohy“ aneb vzácný výskyt EBV u 70leté ženy – kazuistika
Nejčtenější v tomto čísle
- Alleviating chronic ER stress by p38-Ire1-Xbp1 pathway and insulin-associated autophagy in C. elegans neurons
- Cocoonase is indispensable for Lepidoptera insects breaking the sealed cocoon
- A mega-analysis of expression quantitative trait loci in retinal tissue
- Adiponectin GWAS loci harboring extensive allelic heterogeneity exhibit distinct molecular consequences