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.

Histone H3 phosphorylation and non-disjunction of the maternal X chromosome during male meiosis in sciarid flies

“…The proximity of maternal chromatin to a single giant pole generating numerous microtubules ensures that, following breakdown of the nuclear membrane, the maternal chromosomes are retained at the polar complex during meiosis I (Gerbi, 1986;Goday and Esteban, 2001). When covalent histone modifications were analysed during germline development in S. ocellaris, differences in the acetylation or methylation of histones H3 and H4 were found between maternal and parental chromosomes (Goday and Ruiz, 2002;Greciano and Goday, 2006). Concerning male meiosis I, whereas maternal chromosomes at the polar complex are acetylated at histones H3 and H4, the eliminating paternal chromosomes are, instead, under-acetylated and methylated at histones H3 and H4 (Goday and Ruiz, 2002;Greciano and Goday, 2006).…”

“…When covalent histone modifications were analysed during germline development in S. ocellaris, differences in the acetylation or methylation of histones H3 and H4 were found between maternal and parental chromosomes (Goday and Ruiz, 2002;Greciano and Goday, 2006). Concerning male meiosis I, whereas maternal chromosomes at the polar complex are acetylated at histones H3 and H4, the eliminating paternal chromosomes are, instead, under-acetylated and methylated at histones H3 and H4 (Goday and Ruiz, 2002;Greciano and Goday, 2006). Here, we show that phosphorylation of histone H3 differs between the two separating parental sets of chromosomes at male meiosis I, and that such differences in H3 phosphorylation coincide with the extent of chromosome condensation.…”

“…During the anaphase-I-like stage, the monopolar spindle directs the segregation of maternal chromosomes to the single pole, whereas paternal chromosomes move in the opposite direction into a cytoplasmic bud to be discarded later (Metz, 1925;Smith-Stocking, 1936). Importantly, cytological and ultrastructural data indicate that the two parental sets of chromosomes occupy distinct nuclear compartments in germ nuclei from the initial stages of development until the occurrence of meiosis (Rieffel and Crouse, 1966;Kubai, 1982;Kubai, 1987;Goday and Esteban, 2001;Goday and Ruiz, 2002). Moreover, the precocious intranuclear segregation of the maternal chromosomes with respect to the paternal ones is considered to be essential in determining which chromosomal set will be lost during male meiosis I (Kubai, 1987;Goday and Esteban, 2001).…”

Methylation of histone H3 at Lys4 differs between paternal and maternal chromosomes inSciara ocellarisgermline development

“…In early germ cells a single paternal X chromosome is eliminated in embryos of both sexes and in male meiotic cells the whole paternal complement is discarded. In sciarids, differential acetylation of histones H3 and H4 occurs between chromosomes of different parental origin, both in early germ nuclei and in male meiotic cells (Goday and Ruiz, 2002). We here investigated histone methylation modifications between chromosomes in germline cells of Sciara ocellaris.…”

“…More recently, the organization of germline chromosomes of sciarid flies has been further analyzed by looking at molecular chromatin modifications in relation to the parental origin of chromosomes (Goday and Ruiz, 2002). From this analysis, it emerged that during germline development there is a differential acetylation of histones H3 and H4 between paternal and maternal chromosomes.…”