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PLOS Genetics  2011 

Chromosome Painting Reveals Asynaptic Full Alignment of Homologs and HIM-8–Dependent Remodeling of X Chromosome Territories during Caenorhabditis elegans Meiosis

DOI: 10.1371/journal.pgen.1002231

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Abstract:

During early meiotic prophase, a nucleus-wide reorganization leads to sorting of chromosomes into homologous pairs and to establishing associations between homologous chromosomes along their entire lengths. Here, we investigate global features of chromosome organization during this process, using a chromosome painting method in whole-mount Caenorhabditis elegans gonads that enables visualization of whole chromosomes along their entire lengths in the context of preserved 3D nuclear architecture. First, we show that neither spatial proximity of premeiotic chromosome territories nor chromosome-specific timing is a major factor driving homolog pairing. Second, we show that synaptonemal complex-independent associations can support full lengthwise juxtaposition of homologous chromosomes. Third, we reveal a prominent elongation of chromosome territories during meiotic prophase that initiates prior to homolog association and alignment. Mutant analysis indicates that chromosome movement mediated by association of chromosome pairing centers (PCs) with mobile patches of the nuclear envelope (NE)–spanning SUN-1/ZYG-12 protein complexes is not the primary driver of territory elongation. Moreover, we identify new roles for the X chromosome PC (X-PC) and X-PC binding protein HIM-8 in promoting elongation of X chromosome territories, separable from their role(s) in mediating local stabilization of pairing and association of X chromosomes with mobile SUN-1/ZYG-12 patches. Further, we present evidence that HIM-8 functions both at and outside of PCs to mediate chromosome territory elongation. These and other data support a model in which synapsis-independent elongation of chromosome territories, driven by PC binding proteins, enables lengthwise juxtaposition of chromosomes, thereby facilitating assessment of their suitability as potential pairing partners.

References

[1]  Mlynarczyk-Evans S, Villeneuve AM (2010) Homologous Chromosome Pairing and Synapsis during Oogenesis. In: Verlhac M, Villeneuve AM, editors. Oogenesis: The Universal Process. Hoboken, NJ: WILEY. pp. 117–140.
[2]  Hiraoka Y, Dernburg AF (2009) The SUN rises on meiotic chromosome dynamics. Dev Cell 17: 598–605.
[3]  Chikashige Y, Haraguchi T, Hiraoka Y (2007) Another way to move chromosomes. Chromosoma 116: 497–505.
[4]  Goldman AS, Hulten MA (1992) Chromosome in situ suppression hybridisation in human male meiosis. J Med Genet 29: 98–102.
[5]  Barlow AL, Hulten MA (1996) Combined immunocytogenetic and molecular cytogenetic analysis of meiosis I human spermatocytes. Chromosome Res 4: 562–573.
[6]  Scherthan H, Eils R, Trelles-Sticken E, Dietzel S, Cremer T, et al. (1998) Aspects of three-dimensional chromosome reorganization during the onset of human male meiotic prophase. J Cell Sci 111: 2337–2351.
[7]  Schwarzacher T (1997) Three stages of meiotic homologous chromosome pairing in wheat: cognition, alignment and synapsis. Sexual Plant Reproduction 10: 324–331.
[8]  Martinez-Perez E, Shaw P, Reader S, Aragon-Alcaide L, Miller T, et al. (1999) Homologous chromosome pairing in wheat. J Cell Sci 112: 1761–1769.
[9]  Bass HW, Riera-Lizarazu O, Ananiev EV, Bordoli SJ, Rines HW, et al. (2000) Evidence for the coincident initiation of homolog pairing and synapsis during the telomere-clustering (bouquet) stage of meiotic prophase. J Cell Sci 113: 1033–1042.
[10]  Scherthan H, Weich S, Schwegler H, Heyting C, Harle M, 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.
[11]  Prieto P, Shaw P, Moore G (2004) Homologue recognition during meiosis is associated with a change in chromatin conformation. Nat Cell Biol 6: 906–908.
[12]  Prieto P, Moore G, Reader S (2005) Control of conformation changes associated with homologue recognition during meiosis. Theoretical and Applied Genetics 111: 505–510.
[13]  Colas I, Shaw P, Prieto P, Wanous M, Spielmeyer W, et al. (2008) Effective chromosome pairing requires chromatin remodeling at the onset of meiosis. Proceedings of the National Academy of Sciences 105: 6075–6080.
[14]  Schedl T (1997) Developmental genetics of the germ line. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR, editors. C elegans II. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. pp. 241–269.
[15]  Albertson DG, Rose AM, Villeneuve AM (1997) Chromsome organization, mitosis, and meiosis. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR, editors. C elegans II. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. pp. 47–78.
[16]  Zetka M (2009) Homologue pairing, recombination and segregation in Caenorhabditis elegans. Genome Dyn 5: 43–55.
[17]  McKim KS, Peters K, Rose AM (1993) Two types of sites required for meiotic chromosome pairing in Caenorhabditis elegans. Genetics 134: 749–768.
[18]  Villeneuve AM (1994) A cis-acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans. Genetics 136: 887–902.
[19]  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.
[20]  MacQueen AJ, Phillips CM, Bhalla N, Weiser P, Villeneuve AM, et al. (2005) Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123: 1037–1050.
[21]  Phillips CM, Wong C, Bhalla N, Carlton PM, Weiser P, et al. (2005) HIM-8 binds to the X chromosome pairing center and mediates chromosome-specific meiotic synapsis. Cell 123: 1051–1063.
[22]  Phillips CM, Dernburg AF (2006) A family of zinc-finger proteins is required for chromosome-specific pairing and synapsis during meiosis in C. elegans. Dev Cell 11: 817–829.
[23]  Phillips CM, Meng X, Zhang L, Chretien JH, Urnov FD, et al. (2009) Identification of chromosome sequence motifs that mediate meiotic pairing and synapsis in C. elegans. Nat Cell Biol 11: 934–942.
[24]  Penkner A, Tang L, Novatchkova M, Ladurner M, Fridkin A, et al. (2007) The Nuclear Envelope Protein Matefin/SUN-1 Is Required for Homologous Pairing in C. elegans Meiosis. Dev Cell 12: 873–885.
[25]  Sato A, Isaac B, Phillips CM, Rillo R, Carlton PM, et al. (2009) Cytoskeletal Forces Span the Nuclear Envelope to Coordinate Meiotic Chromosome Pairing and Synapsis. Cell 139: 907–919.
[26]  Penkner AM, Fridkin A, Gloggnitzer J, Baudrimont A, Machacek T, et al. (2009) Meiotic Chromosome Homology Search Involves Modifications of the Nuclear Envelope Protein Matefin/SUN-1. Cell 139: 920–933.
[27]  Martinez-Perez E, Villeneuve AM (2005) HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev 19: 2727–2743.
[28]  Couteau F, Zetka M (2005) HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev 19: 2744–2756.
[29]  Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, et al. (1998) Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94: 387–398.
[30]  MacQueen AJ, Villeneuve AM (2001) Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev 15: 1674–1687.
[31]  Nabeshima K, Villeneuve AM, Hillers KJ (2004) Chromosome-wide regulation of meiotic crossover formation in Caenorhabditis elegans requires properly assembled chromosome axes. Genetics 168: 1275–1292.
[32]  Couteau F, Nabeshima K, Villeneuve A, Zetka M (2004) A component of C. elegans meiotic chromosome axes at the interface of homolog alignment, synapsis, nuclear reorganization, and recombination. Curr Biol 14: 585–592.
[33]  Jantsch V, Tang L, Pasierbek P, Penkner A, Nayak S, et al. (2007) Caenorhabditis elegans prom-1 Is Required for Meiotic Prophase Progression and Homologous Chromosome Pairing. Mol Biol Cell 18: 4911–4920.
[34]  Smolikov S, Schild-Pruert K, Colaiacovo MP (2008) CRA-1 Uncovers a Double-Strand Break-Dependent Pathway Promoting the Assembly of Central Region Proteins on Chromosome Axes During C. elegans Meiosis. PLoS Genet 4: e1000088. doi:10.1371/journal.pgen.1000088.
[35]  Pasierbek P, Jantsch M, Melcher M, Schleiffer A, Schweizer D, et al. (2001) A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev 15: 1349–1360.
[36]  Zetka MC, Kawasaki I, Strome S, Muller F (1999) Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes Dev 13: 2258–2270.
[37]  Baudrimont A, Penkner A, Woglar A, Machacek T, Wegrostek C, et al. (2010) Leptotene/Zygotene Chromosome Movement Via the SUN/KASH Protein Bridge in Caenorhabditis elegans. PLoS Genet 6: e1001219. doi:10.1371/journal.pgen.1001219.
[38]  Broverman SA, Meneely PM (1994) Meiotic mutants that cause a polar decrease in recombination on the X chromosome in Caenorhabditis elegans. Genetics 136: 119–127.
[39]  Sun H, Nelms BL, Sleiman SF, Chamberlin HM, Hanna-Rose W (2007) Modulation of Caenorhabditis elegans transcription factor activity by HIM-8 and the related Zinc-Finger ZIM proteins. Genetics 177: 1221–1226.
[40]  McKim KS, Hayashi-Hagihara A (1998) mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: evidence that the mechanism for initiating meiotic recombination is conserved. Genes Dev 12: 2932–2942.
[41]  Villeneuve AM, Hillers KJ (2001) Whence meiosis? Cell 106: 647–650.
[42]  Gong WJ, McKim KS, Hawley RS (2005) All paired up with no place to go: pairing, synapsis, and DSB formation in a balancer heterozygote. PLoS Genet 1: e67. doi:10.1371/journal.pgen.0010067.
[43]  Sherizen D, Jang JK, Bhagat R, Kato N, McKim KS (2005) Meiotic Recombination in Drosophila Females Depends on Chromosome Continuity Between Genetically Defined Boundaries. Genetics 169: 767–781.
[44]  Scherthan H, Loidl J, Schuster T, Schweizer D (1992) Meiotic chromosome condensation and pairing in Saccharomyces cerevisiae studied by chromosome painting. Chromosoma 101: 590–595.
[45]  Trelles-Sticken E, Loidl J, Scherthan H (1999) Bouquet formation in budding yeast: initiation of recombination is not required for meiotic telomere clustering. J Cell Sci 112: 651–658.
[46]  Loidl J, Scherthan H (2004) Organization and pairing of meiotic chromosomes in the ciliate Tetrahymena thermophila. J Cell Sci 117: 5791–5801.
[47]  Dawe RK, Sedat JW, Agard DA, Cande WZ (1994) Meiotic chromosome pairing in maize is associated with a novel chromatin organization. Cell 76: 901–912.
[48]  Kelly WG, Schaner CE, Dernburg AF, Lee M-H, Kim SK, et al. (2002) X-chromosome silencing in the germline of C. elegans. Development 129: 479–492.
[49]  Zickler D (1977) Development of the synaptonemal complex and the “recombination nodules” during meiotic prophase in seven bivalents of fungus Sordaria macrospora Auersw. Chromosoma 61: 289–316.
[50]  Sym M, Engebrecht JA, Roeder GS (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72: 365–378.
[51]  de Vries FA, de Boer E, van den Bosch M, Baarends WM, Ooms M, et al. (2005) Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev 19: 1376–1389.
[52]  Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33: 603–754.
[53]  de Boer E, Heyting C (2006) The diverse roles of transverse filaments of synaptonemal complexes in meiosis. Chromosoma 115: 220–234.
[54]  Loidl J, Pasierbek P, Rose AM (2004) Conservation and variability of meiotic processes - Lessons from the unconventional meiosis of C. elegans. In: Schmid M, editor. Chromosomes Today, Vol 14. Dordrecht: Springer. pp. 93–101.
[55]  Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71–94.
[56]  Chen H, Hughes DD, Chan TA, Sedat JW, Agard DA (1996) IVE (Image Visualization Environment): a software platform for all three-dimensional microscopy applications. J Struct Biol 116: 56–60.
[57]  Nabeshima K, Villeneuve AM, Colaiacovo MP (2005) Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC. J Cell Biol 168: 683–689.

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