Histone posttranslational modifications mediate establishment of structurally 
and functionally distinct chromatin compartments of eukaryotic nuclei. The 
association of different histone modifications with euchromatic and 
heterochromatic compartments is relatively conserved in highly divergent model 
organisms such as Drosophila and mammals. However, some differences between 
these model systems have been uncovered while limited data are available from 
organisms nearer the invertebrate-vertebrate transition. We identified a 
chromatin compartment in both diploid and endocycling cells of the urochordate, 
Oikopleura dioica, enriched in heterochromatic histone modifications and DNA 
methylation. Surprisingly, this compartment also contained high levels of 
histone H3 trimethylated at lysine 4 (H3 Me(3)K4), a modification thus far 
associated with actively transcribed sequences. Although in Drosophila and mouse 
cells, H3 Me(3)K4 was prevalently associated with euchromatin, we also detected 
it in their pericentromeric heterochromatin. We further showed that H3 Me(3)K4 
abundance was not necessarily proportional to local levels of transcriptional 
activity in either euchromatin or heterochromatin. Our data indicate greater 
plasticity across evolution in the association of histone lysine methylation 
with functionally distinct chromatin domains than previously thought and suggest 
that H3 Me(3)K4 participates in additional processes beyond marking 
transcriptionally active chromatin.