Cytogenetic and molecular aspects of position-effect variegation in Drosophila melanogaster

The Drosophila Y-chromosome is gene poor and mainly consists of silenced, repetitive DNA. Nonetheless, the Y influences expression of hundreds of genes genome-wide, possibly by sequestering key components of the heterochromatin machinery away from other positions in the genome. To test the influence of the Y chromosome on the genome-wide chromatin landscape, we assayed the genomic distribution of histone modifications associated with gene activation (H3K4me3), or heterochromatin (H3K9me2 and H3K9me3) in fruit flies with varying sex chromosome complements (X0, XY and XYY males; XX and XXY females). Consistent with the general deficiency of active chromatin modifications on the Y, we find that Y gene dose has little influence on the genomic distribution of H3K4me3. In contrast, both the presence and the number of Y-chromosomes strongly influence genome-wide enrichment patterns of repressive chromatin modifications. Highly repetitive regions such as the pericentromeres, the dot, and the Y chromosome (if present) are enriched for heterochromatic modifications in wildtype males and females, and even more strongly in X0 flies. In contrast, the additional Y chromosome in XYY males and XXY females diminishes the heterochromatic signal in these normally silenced, repeat-rich regions, which is accompanied by an increase in expression of Y-linked repeats. We find hundreds of genes that are expressed differentially between individuals with aberrant sex chromosome karyotypes, many of which also show sex-biased expression in wildtype Drosophila. Thus, Y-chromosomes influence heterochromatin integrity genome-wide, and differences in the chromatin landscape of males and females may also contribute to sex-biased gene expression and sexual dimorphisms.

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“…5 and supplementary figs. S16 and S17 , Supplementary Material online; Belyaeva et al. 1993 ; Wallrath and Elgin 1995 ).…”

Section: Resultsmentioning

confidence: 99%

The Drosophila Y Chromosome Affects Heterochromatin Integrity Genome-Wide

Brown

Nguyen

Bachtrog

2020

Molecular Biology and Evolution

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“…We hypothesize that the associated loci, because of intimate (possibly molecular) contact, acquire the molecular features of heterochromatin. The chromatin of PEV-silenced genes acquire heterochromatic features such as a regular nucleosome array, insensitivity to nucleases [46], and binding of heterochromatin proteins [47,48]. This altered chromatin structure seems to occlude the affected gene's promoter, preventing the loading of RNA polymerase and transcriptional activators, thereby preventing gene expression [49].…”

Section: Discussionmentioning

confidence: 99%

Cell-by-Cell Dissection of Gene Expression and Chromosomal Interactions Reveals Consequences of Nuclear Reorganization

Harmon

Sedat

2005

PLoS Biol

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The functional consequences of long-range nuclear reorganization were studied in a cell-by-cell analysis of gene expression and long-range chromosomal interactions in the Drosophila eye and eye imaginal disk. Position-effect variegation was used to stochastically perturb gene expression and probe nuclear reorganization. Variegating genes on rearrangements of Chromosomes X, 2, and 3 were probed for long-range interactions with heterochromatin. Studies were conducted only in tissues known to express the variegating genes. Nuclear structure was revealed by fluorescence in situ hybridization with probes to the variegating gene and heterochromatin. Gene expression was determined alternately by immunofluorescence against specific proteins and by eye pigment autofluorescence. This allowed cell-by-cell comparisons of nuclear architecture between cells in which the variegating gene was either expressed or silenced. Very strong correlations between heterochromatic association and silencing were found. Expressing cells showed a broad distribution of distances between variegating genes and their own centromeric heterochromatin, while silenced cells showed a very tight distribution centered around very short distances, consistent with interaction between the silenced genes and heterochromatin. Spatial and temporal analysis of interactions with heterochromatin indicated that variegating genes primarily associate with heterochromatin in cells that have exited the cell cycle. Differentiation was not a requirement for association, and no differences in association were observed between cell types. Thus, long-range interactions between distal chromosome regions and their own heterochromatin have functional consequences for the organism.

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“…Most genes reside in euchromatin, and are thought to exist in a more open state than those found in compact heterochromatin. Genes that are ectopically placed within heterochromatin tend to be repressed [4], [5], [6], [7], which reflects a possible spreading of the heterochromatin structure into such genes. Heterochromatic regions are gene poor.…”

Section: Introductionmentioning

confidence: 99%

Genomic Organization of H2Av Containing Nucleosomes in Drosophila Heterochromatin

Zhang

Pugh

2011

PLoS ONE

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H2Av is a versatile histone variant that plays both positive and negative roles in transcription, DNA repair, and chromatin structure in Drosophila. H2Av, and its broader homolog H2A.Z, tend to be enriched toward 5′ ends of genes, and exist in both euchromatin and heterochromatin. Its organization around euchromatin genes and other features have been described in many eukaryotic model organisms. However, less is known about H2Av nucleosome organization in heterochromatin. Here we report the properties and organization of individual H2Av nucleosomes around genes and transposable elements located in Drosophila heterochromatic regions. We compare the similarity and differences with that found in euchromatic regions. Our analyses suggest that nucleosomes are intrinsically positioned on inverted repeats of DNA transposable elements such as those related to the “1360” element, but are not intrinsically positioned on retrotransposon-related elements.

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Cytogenetic and molecular aspects of position-effect variegation in Drosophila melanogaster

Cited by 54 publications

References 18 publications

The Drosophila Y Chromosome Affects Heterochromatin Integrity Genome-Wide

The Drosophila Y Chromosome Affects Heterochromatin Integrity Genome-Wide

Cell-by-Cell Dissection of Gene Expression and Chromosomal Interactions Reveals Consequences of Nuclear Reorganization

Genomic Organization of H2Av Containing Nucleosomes in Drosophila Heterochromatin

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