The Differences between Cis- and Trans- Gene Inactivation Caused by Heterochromatin in Drosophila

Position-effect variegation (PEV) is the epigenetic disruption of gene expression near the de novo –formed euchromatin-heterochromatin border. Heterochromatic cis -inactivation may be accompanied by the trans -inactivation of genes on a normal homologous chromosome in trans -heterozygous combination with a PEV-inducing rearrangement. We characterize a new genetic system, inversion In(2)A4 , demonstrating cis -acting PEV as well as trans -inactivation of the reporter transgenes on the homologous nonrearranged chromosome. The cis -effect of heterochromatin in the inversion results not only in repression but also in activation of genes, and it varies at different developmental stages. While cis -actions affect only a few juxtaposed genes, trans -inactivation is observed in a 500-kb region and demonstrates а nonuniform pattern of repression with intermingled regions where no transgene repression occurs. There is no repression around the histone gene cluster and in some other euchromatic sites. trans -Inactivation is accompanied by dragging of euchromatic regions into the heterochromatic compartment, but the histone gene cluster, located in the middle of the trans -inactivated region, was shown to be evicted from the heterochromatin. We demonstrate that trans -inactivation is followed by de novo HP1a accumulation in the affected transgene; trans -inactivation is specifically favored by the chromatin remodeler SAYP and prevented by Argonaute AGO2.