title: Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC.
abstract: Homologous chromosome pairs (bivalents) undergo restructuring during meiotic prophase to convert a configuration that promotes crossover recombination into one that promotes bipolar spindle attachment and localized cohesion loss. We have imaged remodeling of meiotic chromosome structures after pachytene exit in Caenorhabditis elegans. Chromosome shortening during diplonema is accompanied by coiling of chromosome axes and highly asymmetric departure of synaptonemal complex (SC) central region proteins SYP-1 and SYP-2, which diminish over most of the length of each desynapsing bivalent while becoming concentrated on axis segments distal to the single emerging chiasma. This and other manifestations of asymmetry along chromosomes are lost in synapsis-proficient crossover-defective mutants, which often retain SYP-1,2 along the full lengths of coiled diplotene axes. Moreover, a gamma-irradiation treatment that restores crossovers in the spo-11 mutant also restores asymmetry of SYP-1 localization. We propose that crossovers or crossover precursors serve as symmetry-breaking events that promote differentiation of subregions of the bivalent by triggering asymmetric disassembly of the SC.
authors.affiliation: Department of Developmental Biology, Stanford University School of Medicine, Stanford, CA 94305, USA.
authors.forename: Kentaro
authors.initials: K
authors.lastname: Nabeshima
authors.forename: Anne M
authors.initials: AM
authors.lastname: Villeneuve
authors.forename: Monica P
authors.initials: MP
authors.lastname: Colaiácovo
mesh_terms: D000818:Animals; D064107:Aurora Kinase B; D017173:Caenorhabditis elegans / Q000235:genetics* / Q000502:physiology; D029742:Caenorhabditis elegans Proteins / Q000378:metabolism; D003434:Crossing Over, Genetic / Q000502:physiology*; D007150:Immunohistochemistry; D049469:Meiotic Prophase I / Q000235:genetics / Q000502:physiology*; D009419:Nerve Tissue Proteins / Q000378:metabolism; D017346:Protein Serine-Threonine Kinases / Q000378:metabolism; D013573:Synaptonemal Complex / Q000502:physiology*
chemical_list: D029742:Caenorhabditis elegans Proteins; D009419:Nerve Tissue Proteins; C478060:SYP-2 protein, C elegans; D064107:Aurora Kinase B; D017346:Protein Serine-Threonine Kinases; C491506:air-2 protein, C elegans
references.citation: Genes Dev. 2001 Jun 1;15(11):1349-60
references.pmid: 11390355
references.citation: Genetics. 2000 Oct;156(2):617-30
references.pmid: 11014811
references.citation: J Cell Biol. 2002 Apr 15;157(2):219-29
references.pmid: 11940606
references.citation: Curr Biol. 2002 May 14;12(10):798-812
references.pmid: 12015116
references.citation: Genes Dev. 2002 Sep 15;16(18):2428-42
references.pmid: 12231631
references.citation: Science. 2003 Aug 8;301(5634):785-9
references.pmid: 12907787
references.citation: Dev Cell. 2003 Sep;5(3):463-74
references.pmid: 12967565
references.citation: Nature. 2004 Feb 5;427(6974):510-7
references.pmid: 14730319
references.citation: Proc Natl Acad Sci U S A. 2004 Aug 24;101(34):12592-7
references.pmid: 15299144
references.citation: J Cell Biol. 1998 Mar 9;140(5):1003-12
references.pmid: 9490715
references.citation: Cell. 1998 Aug 7;94(3):387-98
references.pmid: 9708740
references.citation: J Cell Biol. 1998 Dec 14;143(6):1635-46
references.pmid: 9852156
references.citation: Genes Dev. 1999 Sep 1;13(17):2258-70
references.pmid: 10485848
references.citation: J Cell Biol. 2004 Nov 22;167(4):613-25
references.pmid: 15557118
references.citation: Genetics. 2004 Nov;168(3):1275-92
references.pmid: 15579685
references.citation: Genetics. 1999 Nov;153(3):1271-83
references.pmid: 10545458
references.citation: Dev Cell. 2002 Mar;2(3):319-30
references.pmid: 11879637