Three Distinct Condensin Complexes Control C. elegans Chromosome Dynamics

Abstract

Summary 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 IDC) 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 IDC by only a single subunit. Yet condensin I binds to autosomes and X chromosomes in both sexes to promote chromosome segregation, whereas condensin IDC 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.

Different roles for Aurora B in condensin targeting during mitosis and meiosis

“…Despite this difference, chromosomal proteins and their functions are conserved between worms and other eukaryotes (Maddox et al, 2004). C. elegans also has two mitotic and meiotic condensin complexes, and an additional third condensin, condensin I DC , which functions in the hermaphrodite and X-chromosome-specific process of dosage compensation (Csankovszki et al, 2009;Mets and Meyer, 2009). The two mitotic complexes have identical SMC subunits, SMC-4 and MIX-1, and distinct sets of CAP proteins.…”

“…1A). Whereas condensins I and II associate with all chromosomes, condensin I DC only binds to the X chromosomes in hermaphrodites to halve gene expression, equalizing X-linked product in XX hermaphrodites and XO males (Csankovszki et al, 2009). …”

Proteomic identification of germline proteins inCaenorhabditis elegans

“…3; see also ref. 26 ). Cytological evidence for germline defects was also seen in gonads of animals depleted for B0393.1, F17C11.9, K07F5.13, R02D3.3, and T10F2.4 ( Table 3; Fig.…”

Linking dosage compensation and X chromosome nuclear organization inC. elegans

“…11 The DCC is structurally similar to a condensin I complex, with 2 SMC-like components, DPY-27 and MIX-1, the latter being also part of the mitotic and meiotic condensin complexes. 11 Loading of the DCC on the X chromosome is nucleated at rex (recruitment element on X) sites characterized by a 12 bp consensus sequence called MEX (Motif Enriched on X). 12,13 Interestingly, these sites also seem to recruit the mitotic and meiotic Condensin I/II complexes in an sdc-2 dependent manner.…”