Three distinct condensin complexes control C. elegans chromosome dynamics

Curr Biol. 2009 Jan 13;19(1):9-19. doi: 10.1016/j.cub.2008.12.006.

Abstract

Background: Condensin complexes organize chromosome structure and facilitate chromosome segregation. Higher eukaryotes have two complexes, condensin I and condensin II, each essential for chromosome segregation. The nematode Caenorhabditis elegans was considered an exception, because it has a mitotic condensin II complex but appeared to lack mitotic condensin I. Instead, its condensin I-like complex (here called condensin I(DC)) dampens gene expression along hermaphrodite X chromosomes during dosage compensation.

Results: Here we report the discovery of a third condensin complex, condensin I, in C. elegans. We identify new condensin subunits and show that each complex has a conserved five-subunit composition. Condensin I differs from condensin I(DC) by only a single subunit. Yet condensin I binds to autosomes and X chromosomes in both sexes to promote chromosome segregation, whereas condensin I(DC) binds specifically to X chromosomes in hermaphrodites to regulate transcript levels. Both condensin I and II promote chromosome segregation, but associate with different chromosomal regions during mitosis and meiosis. Unexpectedly, condensin I also localizes to regions of cohesion between meiotic chromosomes before their segregation.

Conclusions: We demonstrate that condensin subunits in C. elegans form three complexes, one that functions in dosage compensation and two that function in mitosis and meiosis. These results highlight how the duplication and divergence of condensin subunits during evolution may facilitate their adaptation to specialized chromosomal roles and illustrate the versatility of condensins to function in both gene regulation and chromosome segregation.

Publication types

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

MeSH terms

  • Adenosine Triphosphatases / genetics*
  • Adenosine Triphosphatases / metabolism
  • Adenosine Triphosphatases / physiology*
  • Animals
  • Caenorhabditis elegans / genetics*
  • Caenorhabditis elegans / physiology
  • Cell Nucleus Division / physiology
  • Chromosome Segregation / physiology*
  • Chromosomes / genetics*
  • Chromosomes / metabolism
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism
  • DNA-Binding Proteins / physiology*
  • Dosage Compensation, Genetic / genetics*
  • Dosage Compensation, Genetic / physiology
  • Evolution, Molecular
  • Gene Expression Regulation / genetics*
  • Gene Expression Regulation / physiology
  • Immunoprecipitation
  • Models, Biological*
  • Multiprotein Complexes / genetics*
  • Multiprotein Complexes / metabolism
  • Multiprotein Complexes / physiology*
  • Proteomics / methods
  • RNA Interference

Substances

  • DNA-Binding Proteins
  • Multiprotein Complexes
  • condensin complexes
  • Adenosine Triphosphatases