Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion (original) (raw)

  1. Enrique Martinez-Perez1,5,
  2. Mara Schvarzstein2,
  3. Consuelo Barroso1,
  4. James Lightfoot1,
  5. Abby F. Dernburg3,4, and
  6. Anne M. Villeneuve2
  7. 1 Department of Molecular Biology and Biotechnology, University of Sheffield, Sheffield S10 2TN, United Kingdom;
  8. 2 Department of Developmental Biology, Stanford University, Stanford, California 94305, USA;
  9. 3 Life Sciences Division, E.O. Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA;
  10. 4 Department of Molecular and Cell Biology, University of California at Berkeley, Berkeley, California 94720, USA

Abstract

Segregation of homologous chromosomes during meiosis depends on linkages (chiasmata) created by crossovers and on selective release of a subset of sister chromatid cohesion at anaphase I. During Caenorhabditis elegans meiosis, each chromosome pair forms a single crossover, and the position of this event determines which chromosomal regions will undergo cohesion release at anaphase I. Here we provide insight into the basis of this coupling by uncovering a large-scale regional change in chromosome axis composition that is triggered by crossovers. We show that axial element components HTP-1 and HTP-2 are removed during late pachytene, in a crossover-dependent manner, from the regions that will later be targeted for anaphase I cohesion release. We demonstrate correspondence in position and number between chiasmata and HTP-1/2-depleted regions and provide evidence that HTP-1/2 depletion boundaries mark crossover sites. In htp-1 mutants, diakinesis bivalents lack normal asymmetrical features, and sister chromatid cohesion is prematurely lost during the meiotic divisions. We conclude that HTP-1 is central to the mechanism linking crossovers with late-prophase bivalent differentiation and defines the domains where cohesion will be protected until meiosis II. Further, we discuss parallels between the pattern of HTP-1/2 removal in response to crossovers and the phenomenon of crossover interference.

Footnotes