Conserved patterns of nuclear compartmentalization are not observed in the chordate Oikopleura

Abstract

Recent results from a limited number of eukaryotic model organisms suggest that major principles governing spatial organization of the genome in functionally distinct nuclear compartments are conserved through evolution. We examined the in situ spatial organization of major nuclear components and nuclear patterns of gene loci with strictly defined expression patterns in endocycling cells of the transparent urochordate Oikopleura dioica, a complex metazoan with a very compact genome. Endocycling cells with different functions and similar DNA content displayed distinct topologies of nuclear components. However, the generation of the diverse nuclear architectures did not involve specific local organization of active genes or their preferential amplification. Interestingly, endocycling cells lacked nuclear-envelope-associated heterochromatin and prominent splicing-factor domains, which in mammalian cells associate with transcriptionally silent and active loci respectively. In addition, no correlation was found between transcriptional activity of a locus and its association with chromatin domains rich in specific histone modifications. Together, these findings and the absence of typical eukaryotic replication patterns reveal a surprisingly limited functional compartmentalization of O. dioica endocycling nuclei. This indicates that robust cell-type-specific gene expression does not necessarily require high levels of spatial genome organization.