Differential acetylation of histones H3 and H4 in paternal and maternal germline chromosomes during development of sciarid flies

Abstract

A classic example of chromosome elimination and genomic imprinting is found in sciarid flies (Diptera. Sciaridae), where whole chromosomes of exclusively paternal origin are discarded from the genome at different developmental stages. Two types of chromosome elimination event occur in the germline. In embryos of both sexes, the extrusion of a single paternal X chromosome occurs in early germ nuclei and in male meiotic cells the whole paternal complement is discarded. In sciarids, early germ nuclei remain undivided for a long time and exhibit a high degree of chromatin compaction,so that chromosomes are cytologically individualized. We investigated chromatin differences between parental chromosomes in Sciara ocellaris and S. coprophila by analyzing histone acetylation modifications in early germ nuclei. We examined germ nuclei from early embryonic stages to premeiotic larval stages, male meiotic cell and early somatic nuclei following fertilization. In early germ cells, only half of the regular chromosome complement is highly acetylated for histones H4 and H3. The chromosomes that are highly acetylated are paternally derived. An exception is the paternal X chromosome that is eliminated from germ nuclei. At later stages preceding the initiation of mitotic gonial divisions, all chromosomes of the germline complement show similar high levels of histone H4/H3 acetylation. In male meiosis, maternal chromosomes are highly acetylated for histones H4 and H3, whereas the entire paternal chromosome set undergoing elimination appears under-acetylated. The results suggest that histone acetylation contributes towards specifying the imprinted behavior of germline chromosomes in sciarids.