Genome maintenance, function and transmission requires the adequate
structural organisation of chromosomes. Central to this is the conserved ring-shaped
protein complex, cohesin, that associates with chromosomes. The
property to engage more than one DNA fragment simultaneously allows
cohesin to structure chromosomes by linking distant chromosomal loci, as well
as to provide cohesion during cell division by co-entrapping replicated sister
chromatids. Notably, cohesin is concentrated on chromosomes at specialised
chromosomal domains flanking centromeres, called pericentromeres.
Pericentromeric cohesin enrichment is instrumental for the biorientation of
sister chromatids which in turn is a requisite for accurate chromosome
segregation. Although the significance of high pericentromeric cohesin density
has been widely studied in budding yeast, the structural organisation of
pericentromeres and its implications for chromosome segregation are
unknown. This study reports the 3D organisation of budding yeast
pericentromeres and its function in chromosome segregation. Centromeres
along with centromere-flanking convergent gene pairs structure
pericentromeres by loading and restricting cohesin to the pericentromere,
respectively. Each side of the pericentromere folds into a separate loop which
are then extended into a single open loop by microtubules attaching to
kinetochores. In the absence of convergent genes cohesin is repositioned, the
pericentromere is enlarged and this leads to impairment in chromosome
biorientation. Thus, pericentromere structure that makes budding yeast
chromosomes competent for their segregation, is defined by the arrangement
of transcriptional units and high cohesin density. Importantly, these results
indicate that there is a direct, causal relationship between the 3D organization
of a specific chromosomal domain and cellular function