Chromodomain protein Tcd1 is required for macronuclear genome rearrangement and repair in Tetrahymena

The survival of an organism’s progeny depends on the maintenance of its genome. Programmed DNA rearrangement and repair in Tetrahymena occur during the differentiation of the developing somatic macronuclear genome from the germ line micronuclear genome. Tetrahymena chromodomain protein (Tcd1) exhibited dynamic localization from the parental to the developing macronuclei. In the developing macronuclei, Tcd1 colocalized with Pdd1 and H3K9me3. Furthermore, Tcd1 colocalized with Pdd1 in the conjusome and “donut structure” of DNA elimination heterochromatin region. During the growth and conjugation stages, TCD1 knockout cells appeared normal and similar to wild-type strains. In addition, these knockout cells proceeded to the 2MAC-1MIC stage. However, the progeny of the TCD1 knockout cells did not grow upon return to SPP medium and eventually died. The deletion of the internal elimination sequence R element was partially disrupted in the developing new macronuclei. Gamma H2A staining showed that Tcd1 loss induced the accumulation of DNA double-strand breaks and the failure of genome repair. These results suggest that the chromodomain protein Tcd1 is required for the rearrangement and repair of new macronuclear genome in Tetrahymena.