Chromatin environments differ greatly within a eukaryotic genome, depending on 
expression state, chromosomal location, and nuclear position. In genomic regions 
characterized by high repeat content and high gene density, chromatin structure 
must silence transposable elements but permit expression of embedded genes. We 
have investigated one such region, chromosome 4 of Drosophila melanogaster. 
Using chromatin-immunoprecipitation followed by microarray (ChIP-chip) analysis, 
we examined enrichment patterns of 20 histone modifications and 25 chromosomal 
proteins in S2 and BG3 cells, as well as the changes in several marks resulting 
from mutations in key proteins. Active genes on chromosome 4 are distinct from 
those in euchromatin or pericentric heterochromatin: while there is a depletion 
of silencing marks at the transcription start sites (TSSs), HP1a and H3K9me3, 
but not H3K9me2, are enriched strongly over gene bodies. Intriguingly, genes on 
chromosome 4 are less frequently associated with paused polymerase. However, 
when the chromatin is altered by depleting HP1a or POF, the RNA pol II 
enrichment patterns of many chromosome 4 genes shift, showing a significant 
decrease over gene bodies but not at TSSs, accompanied by lower expression of 
those genes. Chromosome 4 genes have a low incidence of TRL/GAGA factor binding 
sites and a low T(m) downstream of the TSS, characteristics that could 
contribute to a low incidence of RNA polymerase pausing. Our data also indicate 
that EGG and POF jointly regulate H3K9 methylation and promote HP1a binding over 
gene bodies, while HP1a targeting and H3K9 methylation are maintained at the 
repeats by an independent mechanism. The HP1a-enriched, POF-associated chromatin 
structure over the gene bodies may represent one type of adaptation for genes 
embedded in repetitive DNA.