Home LiteratureArticle Details
PMID: 16555016 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Review

Chiasma formation: chromatin/axis interplay and the role(s) of the synaptonemal complex.

Chromosoma ·Vol. 115 ·No. 3 ·2006-06-00 ·Pages 175-94

Kleckner N

Abstract

Meiotic recombination proceeds in biochemical complexes that are physically associated with underlying chromosome structural axes. In this study, we discuss the organizational basis for these axes, the timing and nature of recombinosome/axis organization with respect to the prophase program of DNA and to structural changes, and the possible significance of axis organization. Furthermore, we discuss implications and extensions of our recently proposed mechanical model for chiasma formation. Finally, we give a broader consideration to past and present models for the role of the synaptonemal complex.

MeSH Terms
Chromatin/genetics,physiology Chromosome Pairing/genetics Crossing Over, Genetic/physiology Meiosis Models, Biological Synaptonemal Complex/physiology
Chemicals
Chromatin
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Kleckner Nancy
Harvard University, Cambridge, MA 02138, USA. [email protected]
References (85)
85 references, click to expand
  1. Localization and roles of Ski8p protein in Sordaria meiosis and delineation of three mechanistically distinct steps of meiotic homolog juxtaposition.
    Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):12865-70 PMID: 14563920
  2. Chiasma interference and the distribution of exchanges in Drosophila melanogaster.
    Cold Spring Harb Symp Quant Biol. 1993;58:543-52 PMID: 7956068
  3. Cohesins are required for meiotic DNA breakage and recombination in Schizosaccharomyces pombe.
    Proc Natl Acad Sci U S A. 2005 Aug 2;102(31):10952-7 PMID: 16043696
  4. Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation.
    Cell. 2002 Dec 13;111(6):791-802 PMID: 12526806
  5. Electron microscopy of meiosis in Drosophila melanogaster females: II. The recombination nodule--a recombination-associated structure at pachytene?
    Proc Natl Acad Sci U S A. 1975 Aug;72(8):3186-9 PMID: 810799
  6. RAD51 and DMC1 form mixed complexes associated with mouse meiotic chromosome cores and synaptonemal complexes.
    J Cell Biol. 1999 Oct 18;147(2):207-20 PMID: 10525529
  7. Meiotic chromosomes: integrating structure and function.
    Annu Rev Genet. 1999;33:603-754 PMID: 10690419
  8. The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination.
    J Cell Sci. 2002 Apr 15;115(Pt 8):1611-22 PMID: 11950880
  9. Coordinating the events of the meiotic prophase.
    Trends Cell Biol. 2005 Dec;15(12):674-81 PMID: 16257210
  10. The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination.
    Cell. 2001 Jul 13;106(1):59-70 PMID: 11461702
  11. The time and duration of meiosis.
    Philos Trans R Soc Lond B Biol Sci. 1977 Mar 21;277(955):201-26 PMID: 16285
  12. Dynamic behavior of microtubules during dynein-dependent nuclear migrations of meiotic prophase in fission yeast.
    Mol Biol Cell. 2001 Dec;12(12):3933-46 PMID: 11739791
  13. Structure and function of the synaptonemal complex.
    Genetics. 1969;61(1):Suppl:41-51 PMID: 5345399
  14. Absence of mouse REC8 cohesin promotes synapsis of sister chromatids in meiosis.
    Dev Cell. 2005 Jun;8(6):949-61 PMID: 15935783
  15. Synaptonemal complex karyotyping in spermatocytes of the Chinese hamster (Cricetulus griseus). IV. Light and electron microscopy of synapsis and nucleolar development by silver staining.
    Chromosoma. 1980;76(1):1-22 PMID: 6153596
  16. Metaphase chromosome structure: bands arise from a differential folding path of the highly AT-rich scaffold.
    Cell. 1994 Feb 25;76(4):609-22 PMID: 7510215
  17. Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1beta and SMC3.
    J Cell Biol. 2003 Mar 3;160(5):657-70 PMID: 12615909
  18. Meiotic transverse filament proteins: essential for crossing over.
    Transgenic Res. 2005 Oct;14(5):547-50 PMID: 16245145
  19. A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis.
    Cell. 1999 Jul 9;98(1):91-103 PMID: 10412984
  20. Crossover site determination and interference.
    J Theor Biol. 1988 Oct 21;134(4):565-70 PMID: 3255012
  21. Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination.
    Cell. 1990 May 4;61(3):419-36 PMID: 2185891
  22. Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans.
    Genes Dev. 2002 Sep 15;16(18):2428-42 PMID: 12231631
  23. Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes.
    Cell. 2004 Mar 19;116(6):795-802 PMID: 15035982
  24. Spo76p is a conserved chromosome morphogenesis protein that links the mitotic and meiotic programs.
    Cell. 1999 Jul 23;98 (2):261-71 PMID: 10428037
  25. The DIF1 gene of Arabidopsis is required for meiotic chromosome segregation and belongs to the REC8/RAD21 cohesin gene family.
    Plant J. 1999 Aug;19(4):463-72 PMID: 10504568
  26. Linear element formation and their role in meiotic sister chromatid cohesion and chromosome pairing.
    J Cell Sci. 2003 May 1;116(Pt 9):1719-31 PMID: 12665553
  27. Chromatin organization at meiosis.
    Bioessays. 1988 Nov;9(5):151-3 PMID: 3071365
  28. SARs are cis DNA elements of chromosome dynamics: synthesis of a SAR repressor protein.
    Cell. 1995 Dec 29;83(7):1137-48 PMID: 8548801
  29. Meiotic chromosome pairing in maize is associated with a novel chromatin organization.
    Cell. 1994 Mar 11;76(5):901-12 PMID: 8124724
  30. Meiotic chromosome metabolism: one view.
    Cold Spring Harb Symp Quant Biol. 1991;56:729-43 PMID: 1819520
  31. Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae.
    Cell. 1991 Sep 20;66(6):1239-56 PMID: 1913808
  32. Polo-like kinase Cdc5 promotes chiasmata formation and cosegregation of sister centromeres at meiosis I.
    Nat Cell Biol. 2003 May;5(5):480-5 PMID: 12717442
  33. Meiotic recombination and chromosome segregation in Drosophila females.
    Annu Rev Genet. 2002;36:205-32 PMID: 12429692
  34. The Synaptonemal complex component C(2)M regulates meiotic crossing over in Drosophila.
    Curr Biol. 2003 Feb 18;13(4):276-85 PMID: 12593793
  35. Crossover interference is abolished in the absence of a synaptonemal complex protein.
    Cell. 1994 Oct 21;79(2):283-92 PMID: 7954796
  36. Gene conversion, recombination nodules, and the initiation of meiotic synapsis.
    Bioessays. 1987 May;6(5):232-6 PMID: 3606589
  37. Meiotic arrest and aneuploidy in MLH3-deficient mice.
    Nat Genet. 2002 Aug;31(4):385-90 PMID: 12091911
  38. Chromatin architecture of the human genome: gene-rich domains are enriched in open chromatin fibers.
    Cell. 2004 Sep 3;118(5):555-66 PMID: 15339661
  39. DNA double-strand breaks, recombination and synapsis: the timing of meiosis differs in grasshoppers and flies.
    EMBO Rep. 2004 Apr;5(4):385-91 PMID: 15105829
  40. A postprophase topoisomerase II-dependent chromatid core separation step in the formation of metaphase chromosomes.
    J Cell Biol. 1995 Oct;131(1):7-17 PMID: 7559788
  41. Synapsis or silence.
    Nat Genet. 2005 Jan;37(1):11-3 PMID: 15624015
  42. Silver staining two types of meiotic nodules.
    Genome. 1992 Dec;35(6):907-15 PMID: 1473725
  43. Meiosis: how could it work?
    Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8167-74 PMID: 8710842
  44. Differential timing and control of noncrossover and crossover recombination during meiosis.
    Cell. 2001 Jul 13;106(1):47-57 PMID: 11461701
  45. A meiotic chromosomal core consisting of cohesin complex proteins recruits DNA recombination proteins and promotes synapsis in the absence of an axial element in mammalian meiotic cells.
    Mol Cell Biol. 2001 Aug;21(16):5667-77 PMID: 11463847
  46. The temporal sequence of synaptic initiation, crossing over and synaptic completion.
    Genetics. 1972 Mar;70(3):353-70 PMID: 4554285
  47. The synaptonemal complex and the distribution of meiotic recombination events.
    Trends Genet. 1995 Jun;11(6):206-8 PMID: 7638896
  48. Crossover interference in Arabidopsis.
    Genetics. 2002 Apr;160(4):1631-9 PMID: 11973316
  49. Crossing over analysis at pachytene in man.
    Eur J Hum Genet. 1998 Jul-Aug;6(4):350-8 PMID: 9781043
  50. The synaptonemal complex in genetic segregation.
    Annu Rev Genet. 1984;18:331-413 PMID: 6241453
  51. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression.
    Cell. 1992 May 1;69(3):439-56 PMID: 1581960
  52. Sister chromatid cohesion and recombination in meiosis.
    Chromosoma. 2000;109(1-2):10-26 PMID: 10855491
  53. DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain.
    Mol Cell. 2004 Dec 22;16(6):991-1002 PMID: 15610741
  54. The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over.
    Genes Dev. 2005 Oct 15;19(20):2488-500 PMID: 16230536
  55. Mechanism and control of meiotic recombination initiation.
    Curr Top Dev Biol. 2001;52:1-53 PMID: 11529427
  56. The mismatch repair system contributes to meiotic sterility in an interspecific yeast hybrid.
    EMBO J. 1996 Apr 1;15(7):1726-33 PMID: 8612597
  57. Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis.
    Cell. 2004 Apr 2;117(1):29-45 PMID: 15066280
  58. Juxtaposition of C(2)M and the transverse filament protein C(3)G within the central region of Drosophila synaptonemal complex.
    Proc Natl Acad Sci U S A. 2005 Mar 22;102(12):4482-7 PMID: 15767569
  59. Development of the synaptonemal complex and the "recombination nodules" during meiotic prophase in the seven bivalents of the fungus Sordaria macrospora Auersw.
    Chromosoma. 1977 Jun 23;61(4):289-316 PMID: 880839
  60. Meiotic double-strand breaks at the interface of chromosome movement, chromosome remodeling, and reductional division.
    Genes Dev. 2003 Nov 1;17(21):2675-87 PMID: 14563680
  61. A mechanical basis for chromosome function.
    Proc Natl Acad Sci U S A. 2004 Aug 24;101(34):12592-7 PMID: 15299144
  62. Crossover and noncrossover recombination during meiosis: timing and pathway relationships.
    Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8512-6 PMID: 7667321
  63. Cytochemical study of the distribution of RNA and DNA in the synaptonemal complex of guinea-pig and rat spermatocytes.
    Eur J Histochem. 2002;46(2):133-42 PMID: 12152791
  64. The genetics and molecular biology of the synaptonemal complex.
    Annu Rev Cell Dev Biol. 2004;20:525-58 PMID: 15473851
  65. Three-dimensional microscopy of the Rad51 recombination protein during meiotic prophase.
    Plant Cell. 1999 May;11(5):809-24 PMID: 10330467
  66. The HOP1 gene encodes a meiosis-specific component of yeast chromosomes.
    Cell. 1990 Apr 6;61(1):73-84 PMID: 2107981
  67. Anti-topoisomerase II recognizes meiotic chromosome cores.
    Chromosoma. 1989 Nov;98(5):317-22 PMID: 2558860
  68. Early decision; meiotic crossover interference prior to stable strand exchange and synapsis.
    Cell. 2004 Apr 2;117(1):9-15 PMID: 15066278
  69. Cohesin SMC1 beta is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination.
    Nat Cell Biol. 2004 Jun;6(6):555-62 PMID: 15146193
  70. ATM and RPA in meiotic chromosome synapsis and recombination.
    Nat Genet. 1997 Dec;17(4):457-61 PMID: 9398850
  71. Is the synaptonemal complex a disjunction machine?
    J Hered. 1995 Sep-Oct;86(5):330-40 PMID: 7560869
  72. The relationship of crossing over to chromosome synapsis in a short paracentric inversion.
    Genetics. 1966 Jun;53(6):1071-7 PMID: 5958910
  73. Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation.
    Genes Dev. 2005 Jun 1;19(11):1376-89 PMID: 15937223
  74. Presynaptic events in meiocytes of Lilium longiflorum and their relation to crossing-over: a preselection hypothesis.
    Proc Natl Acad Sci U S A. 1975 Mar;72(3):961-5 PMID: 1055394
  75. A polymerization model of chiasma interference and corresponding computer simulation.
    Genetics. 1990 Dec;126(4):1127-38 PMID: 2127577
  76. Positional cloning and characterization of mouse mei8, a disrupted allelle of the meiotic cohesin Rec8.
    Genesis. 2004 Nov;40(3):184-94 PMID: 15515002
  77. Crossover and noncrossover pathways in mouse meiosis.
    Mol Cell. 2005 Nov 23;20(4):563-73 PMID: 16307920
  78. Silencing of unsynapsed meiotic chromosomes in the mouse.
    Nat Genet. 2005 Jan;37(1):41-7 PMID: 15580272
  79. Inter-sex variation in synaptonemal complex lengths largely determine the different recombination rates in male and female germ cells.
    Cytogenet Genome Res. 2004;107(3-4):208-15 PMID: 15467366
  80. Making crossovers during meiosis.
    Biochem Soc Trans. 2005 Dec;33(Pt 6):1451-5 PMID: 16246144
  81. EM autoradiographic evidence that DNA synthesis occurs at recombination nodules during meiosis in Drosophila melanogaster females.
    Chromosoma. 1981;83(1):59-80 PMID: 6790251
  82. Meiosis in Aspergillus nidulans: another example for lacking synaptonemal complexes in the absence of crossover interference.
    Hereditas. 1982;97(2):179-87 PMID: 6761318
  83. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks.
    Nature. 2005 Aug 18;436(7053):1053-7 PMID: 16107854
  84. Genome-wide mapping of the cohesin complex in the yeast Saccharomyces cerevisiae.
    PLoS Biol. 2004 Sep;2(9):E259 PMID: 15309048
  85. Coordinate variation in meiotic pachytene SC length and total crossover/chiasma frequency under conditions of constant DNA length.
    Trends Genet. 2003 Nov;19(11):623-8 PMID: 14585614
Article Info
Journal
Chromosoma
Abbr.
Chromosoma
ISSN
0009-5915
DOI
10.1007/s00412-006-0055-7
Email
[email protected]
Published
2006-06-00
Epub
2006-00-23
Pages
175-94
Language
English
Region
Austria
NLM ID
2985138R
Subset
IM
Grants
NIGMS NIH HHS · GM25326 · United States
NIGMS NIH HHS · GM44794 · United States
External Links
PubMed source DOI: 10.1007/s00412-006-0055-7 View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2