Centromeric motion facilitates the mobility of interphase genomic regions in fission yeast

J Cell Sci. 2013 Nov 15;126(Pt 22):5271-83. doi: 10.1242/jcs.133678. Epub 2013 Aug 28.

Abstract

Dispersed genetic elements, such as retrotransposons and Pol-III-transcribed genes, including tRNA and 5S rRNA, cluster and associate with centromeres in fission yeast through the function of condensin. However, the dynamics of these condensin-mediated genomic associations remains unknown. We have examined the 3D motions of genomic loci including the centromere, telomere, rDNA repeat locus, and the loci carrying Pol-III-transcribed genes or long-terminal repeat (LTR) retrotransposons in live cells at as short as 1.5-second intervals. Treatment with carbendazim (CBZ), a microtubule-destabilizing agent, not only prevents centromeric motion, but also reduces the mobility of the other genomic loci during interphase. Further analyses demonstrate that condensin-mediated associations between centromeres and the genomic loci are clonal, infrequent and transient. However, when associated, centromeres and the genomic loci migrate together in a coordinated fashion. In addition, a condensin mutation that disrupts associations between centromeres and the genomic loci results in a concomitant decrease in the mobility of the loci. Our study suggests that highly mobile centromeres pulled by microtubules in cytoplasm serve as 'genome mobility elements' by facilitating physical relocations of associating genomic regions.

Keywords: Condensin; Fission yeast; Genome dynamics; Live-cell imaging; Nuclear organization.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphatases / genetics
  • Adenosine Triphosphatases / ultrastructure
  • Benzimidazoles / pharmacology
  • Carbamates / pharmacology
  • Centromere / genetics*
  • DNA, Ribosomal / genetics
  • DNA, Ribosomal / ultrastructure
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / ultrastructure
  • Genome, Fungal
  • Interphase / genetics*
  • Microtubules / drug effects
  • Microtubules / ultrastructure
  • Mitosis / drug effects
  • Mitosis / genetics*
  • Multiprotein Complexes / genetics
  • Multiprotein Complexes / ultrastructure
  • RNA, Ribosomal, 5S / genetics
  • RNA, Ribosomal, 5S / ultrastructure
  • RNA, Transfer / genetics
  • RNA, Transfer / ultrastructure
  • Retroelements / genetics
  • Schizosaccharomyces / cytology
  • Schizosaccharomyces / genetics*
  • Telomere / genetics
  • Telomere / ultrastructure

Substances

  • Benzimidazoles
  • Carbamates
  • DNA, Ribosomal
  • DNA-Binding Proteins
  • Multiprotein Complexes
  • RNA, Ribosomal, 5S
  • Retroelements
  • condensin complexes
  • RNA, Transfer
  • Adenosine Triphosphatases
  • carbendazim