Chromosome arm length and nuclear constraints determine the dynamic relationship of yeast subtelomeres

Abstract

Physical interactions between distinct chromosomal genomic loci are important for genomic functions including recombination and gene expression, but the mechanisms by which these interactions occur remain obscure. Using telomeric association as a model system, we analyzed here the in vivo organization of chromosome ends of haploid yeast cells during interphase. We separately labeled most of the 32 subtelomeres and analyzed their positions both in nuclear space and relative to three representative reference subtelomeres by high-throughput 3D microscopy and image processing. We show that subtelomeres are positioned nonrandomly at the nuclear periphery, depending on the genomic size of their chromosome arm, centromere attachment to the microtubule organizing center (spindle pole body, SPB), and the volume of the nucleolus. The distance of subtelomeres to the SPB increases consistently with chromosome arm length up to ≈300 kb; for larger arms the influence of chromosome arm length is weaker, but the effect of the nucleolar volume is stronger. Distances between pairs of subtelomeres also exhibit arm-length dependence and suggest, together with dynamic tracking experiments, that potential associations between subtelomeres are unexpectedly infrequent and transient. Our results suggest that interactions between subtelomeres are nonspecific and instead governed by physical constraints, including chromosome structure, attachment to the SPB, and nuclear crowding.genome organization | telomeric foci | image analysis

Keep moving and stay in a good shape to find your homologous recombination partner

“…This organization largely favours interaction between centromeric proximal sequences as well as contact between subtelomeres (Bystricky et al 2005;Schober et al 2008;Therizols et al 2010;Duan et al 2010;Agmon et al 2013). Consistently, recombination between centromeres on one hand and between subtelomeric sequences on the other hand occurs efficiently (Burgess and Kleckner 1999;Brown et al 2010;Agmon et al 2013;Lee et al 2016).…”

The Nuts and Bolts of Transcriptionally Silent Chromatin in Saccharomyces cerevisiae

“…Clustering is a dynamic process where individual telomeres split from clusters and rejoin on a time scale of minutes (Schober et al 2008). Telomeres at the ends of chromosome arms of similar length associate with one another more frequently, owing to the comigration of centromeres at anaphase (Schober et al 2008;Therizols et al 2010). Interestingly, long-lived stationary-phase cells group all telomeres into a single Sir3-dependent cluster, a genomic restructuring event that extends chronological life span (Guidi et al 2015).…”

High-throughput chromatin motion tracking in living yeast reveals the flexibility of the fiber throughout the genome

“…Structural data obtained by statistical positioning of a gene in a yeast cell population led to a surprisingly simple model to define yeast nuclear architecture (Zimmer and Fabre 2011): Chromosome position can be predicted by a few parameters such as genomic arm length, telomeres (TEL), and centromeres (CEN) tethered to the NE via nuclear-envelope-tethered proteins and to the SPB via microtubules, respectively (Bystricky et al 2005;Therizols et al 2010;Zimmer and Fabre 2011). This description was recently complemented by the first Hi-C comprehensive maps (Rodley et al 2009;Duan et al 2010), which confirmed an organization guided by nuclear landmarks, including TEL that congregate in foci (Gotta et al 1996;Schober et al 2008).…”