The programmed elimination of part of the genome through chromosome loss or chromatin diminution constitutes an exceptional biological process found to be present in several diverse groups of organisms. The occurrence of this phenomenon during early embryogenesis is generally correlated to somatic versus germ-line differentiation. A most outstanding example of chromosome elimination and genomic imprinting is found in sciarid flies, where whole chromosomes of exclusive parental origin are selectively eliminated at different developmental stages. Three types of tissue-specific chromosome elimination events occur in sciarids. During early cleavages, one or two X paternal chromosomes is/are discarded from somatic cells of embryos which then develop as females or males respectively. Thus, the sex of the embryo is determined by the number of eliminated paternal X chromosomes. In germ cells, instead, a single paternal X chromosome is eliminated in embryos of both sexes. In addition, while female meiosis is orthodox, male meiosis is highly unusual as the whole paternal chromosome set is discarded from spermatocytes. As a consequence, only maternally derived chromosomes are included in the functional sperm. This paper reviews current cytological and molecular knowledge on the tissue-specific cell mechanisms evolved to achieve chromosome elimination in sciarids.
This paper reports a comparative analysis of heterochromatin organization in the sex chromosomes of the fruit fly Anastrepha. Mitotic chromosomes of eight Anastrepha species from different taxonomic groups were stained with DAPI and chromomycin A3 fluorochromes followed by C-banding. A specific sex-chromosome banding pattern was obtained for each of the analyzed species. Fluorescence in situ hybridization (FISH) was performed to investigate the chromosomal location of rDNA loci. In all cases the rDNA sequences were found to localize exclusively to the sex chromosomes. The results further extend the chromosomal knowledge of Anastrepha and allow a precise species identification.
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.
This article reports the cloning and characterization of the gene homologous to Sex-lethal (Sxl) of Drosophila melanogaster from Sciara coprophila, Rhynchosciara americana, and Trichosia pubescens. This gene plays the key role in controlling sex determination and dosage compensation in D. melanogaster. The Sxl gene of the three species studied produces a single transcript encoding a single protein in both males and females. Comparison of the Sxl proteins of these Nematocera insects with those of the Brachycera showed their two RNA-binding domains (RBD) to be highly conserved, whereas significant variation was observed in both the N-and C-terminal domains. The great majority of nucleotide changes in the RBDs were synonymous, indicating that purifying selection is acting on them. In both sexes of the three Nematocera insects, the Sxl protein colocalized with transcription-active regions dependent on RNA polymerase II but not on RNA polymerase I. Together, these results indicate that Sxl does not appear to play a discriminatory role in the control of sex determination and dosage compensation in nematocerans. Thus, in the phylogenetic lineage that gave rise to the drosophilids, evolution coopted for the Sxl gene, modified it, and converted it into the key gene controlling sex determination and dosage compensation. At the same time, however, certain properties of the recruited ancestral Sxl gene were beneficial, and these are maintained in the evolved Sxl gene, allowing it to exert its sex-determining and dose compensation functions in Drosophila.
In the zebra finch (Taeniopygia guttata) a germline-restricted chromosome (GRC) is regularly present in males and females. While the GRC is euchromatic in oocytes, in spermatocytes this chromosome is cytologically seen as entirely heterochromatic and presumably inactive. At the end of male meiosis, the GRC is eliminated from the nucleus. By immunofluorescence on microspreads, we investigated HP1 proteins and histone modifications throughout male meiotic prophase, as well as in young spermatid stages after the GRC elimination. We found that in prophase spermatocytes the GRC chromatin differs from that of the regular chromosome complement. The GRC is highly enriched in HP1 beta and exhibits high levels of di- and tri-methylated histone H3 at lysine 9 and tri- and di-methylated histone H4 at lysine 20. The GRC does not exhibit neither detectable levels of di- and tri-methylated histone H3 at lysine 4 nor acetylated histone H4 at lysine 5 and 8. The results prove the heterochromatic organization of the GRC in male germline and strongly suggest its transcriptional inactive state during male prophase. Following elimination, in young spermatids the GRC lacks HP1 beta signals but maintains high levels of methylated histone H3 at lysine 9 and methylated histone H4 at lysine 20. The release of HP1 from the GRC with respect to its elimination is discussed.
The equine ascarid parasite Parascaris equorum is well known as a ubiquitous parasite infecting foals. A sibling species, Parascaris univalens, was first described over 130 years ago, but very little attention has been given to its existence and possible implications for anthelmintic resistance, clinical disease, or host age spectrum. P. univalens only possesses one germ line chromosome pair as opposed to two for P. equorum, but the two species are otherwise considered morphologically identical. For the present study, live worms obtained from the University of Kentucky parasitology horse herd were dissected and identified using karyotyping techniques. With no exception, all specimens (n = 30) were identified to be P. univalens. Further, the karyotyping technique was adapted to ascarid eggs derived from fecal samples and carried out on samples collected from 25 Thoroughbred foals from three farms in Central Kentucky. P. equorum was not identified among these, whereas P. univalens was found in 17 samples, with the remaining being inconclusive. The mitochondrial genome was sequenced, assembled, and annotated from one male worm identified as P. univalens, and comparison with available sequence reads labeled as P. equorum revealed only 0.16% nucleotide differences. However, it is unlikely that the sequences available in public databases have been unequivocally identified to species level by karyotyping. Taken together, these data suggest that P. univalens is likely the main species now observed in equines and that perhaps the designation Parascaris spp. should be used unless cytological characterization has confirmed the species.
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