Spatial and temporal plasticity of chromatin during programmed DNA-reorganization in Stylonychia macronuclear development

Background: In this study we exploit the unique genome organization
of ciliates to characterize the biological function of histone
modification patterns and chromatin plasticity for the processing
of specific DNA sequences during a nuclear differentiation process.
Ciliates are single-cell eukaryotes containing two morphologically
and functionally specialized types of nuclei, the somatic
macronucleus and the germline micronucleus. In the course of sexual
reproduction a new macronucleus develops from a micronuclear
derivative. During this process specific DNA sequences are
eliminated from the genome, while sequences that will be
transcribed in the mature macronucleus are retained. Results: We
show by immunofluorescence microscopy, Western analyses and
chromatin immunoprecipitation (ChIP) experiments that each nuclear
type establishes its specific histone modification signature. Our
analyses reveal that the early macronuclear anlage adopts a
permissive chromatin state immediately after the fusion of two
heterochromatic germline micronuclei. As macronuclear development
progresses, repressive histone modifications that specify sequences
to be eliminated are introduced de novo. ChIP analyses demonstrate
that permissive histone modifications are associated with sequences
that will be retained in the new macronucleus. Furthermore, our
data support the hypothesis that a PIWI-family protein is involved
in a transnuclear cross-talk and in the RNAi-dependent control of
developmental chromatin reorganization. Conclusion: Based on these
data we present a comprehensive analysis of the spatial and
temporal pattern of histone modifications during this nuclear
differentiation process. Results obtained in this study may also be
relevant for our understanding of chromatin plasticity during
metazoan embryogenesis.