Gene Regulation by Chromatin Structure: Paradigms Established in<i>Drosophila melanogaster</i>

Schulze, Sandra; Wallrath, Lori L.

doi:10.1146/annurev.ento.51.110104.151007

Cited by 57 publications

(46 citation statements)

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“…PEV in white mutants (e.g., w[m4h], whitemottled 4) is attributed to the spreading of heterochromatinassociated proteins and other modifications into the adjacent euchromatin (6,20). To address whether Y chromosomes are polymorphic for variation affecting PEV, we generated 16 Y chromosome substitution lines of Drosophila that are identical for all autosomes and X chromosomes and differ only in the origin of the Y chromosome.…”

Section: Resultsmentioning

confidence: 99%

“…To address whether Y chromosomes are polymorphic for variation affecting PEV, we generated 16 Y chromosome substitution lines of Drosophila that are identical for all autosomes and X chromosomes and differ only in the origin of the Y chromosome. In white (w[m4h]) mutants, the diagnostic mosaic phenotype arises due to a chromosomal inversion that moves the white gene from its native euchromatic environment to the euchromatic-heterochromatic boundary in the X chromosome (6,20). Expression of the white gene occurs in cell lineages in which the heterochromatin-euchromatin balance is tipped toward a greater abundance of euchromatin.…”

Section: Resultsmentioning

confidence: 99%

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Epigenetic effects of polymorphic Y chromosomes modulate chromatin components, immune response, and sexual conflict

Lemos

Branco²,

Hartl³

2010

Proc. Natl. Acad. Sci. U.S.A.

174

190

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Genetic conflicts between sexes and generations provide a foundation for understanding the functional evolution of sex chromosomes and sexually dimorphic phenotypes. Y chromosomes of Drosophila contain multi-megabase stretches of satellite DNA repeats and a handful of protein-coding genes that are monomorphic within species. Nevertheless, polymorphic variation in heterochromatic Y chromosomes of Drosophila result in genome-wide gene expression variation. Here we show that such naturally occurring Y-linked regulatory variation (YRV) can be detected in somatic tissues and contributes to the epigenetic balance of heterochromatin/ euchromatin at three distinct loci showing position-effect variegation (PEV). Moreover, polymorphic Y chromosomes differentially affect the expression of thousands of genes in XXY female genotypes in which Y-linked protein-coding genes are not transcribed. The data show a disproportionate influence of YRV on the variable expression of genes whose protein products localize to the nucleus, have nucleic-acid binding activity, and are involved in transcription, chromosome organization, and chromatin assembly. These include key components such as HP1, Trithorax-like (GAGA factor), Su(var)3-9, Brahma, MCM2, ORC2, and inner centromere protein. Furthermore, mitochondria-related genes, immune response genes, and transposable elements are also disproportionally affected by Y chromosome polymorphism. These functional clusterings may arise as a consequence of the involvement of Y-linked heterochromatin in the origin and resolution of genetic conflicts between males and females. Taken together, our results indicate that Y chromosome heterochromatin serves as a major source of epigenetic variation in natural populations that interacts with chromatin components to modulate the expression of biologically relevant phenotypic variation.evolution | heterochromatin | position-effect variegation | regulatory

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Epigenetic effects of polymorphic Y chromosomes modulate chromatin components, immune response, and sexual conflict

Lemos

Branco²,

Hartl³

2010

Proc. Natl. Acad. Sci. U.S.A.

174

190

View full text Add to dashboard Cite

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“…The repressed and variegated expression of telomeric transgenes is phenotypically similar to position effect variegation (PEV), the clonal inactivation of a euchromatic gene positioned close to or within pericentric heterochromatin (78,79).…”

Section: Telomere Associated Repeat Sequencesmentioning

confidence: 99%

Drosophila telomeres: an exception providing new insights

2007

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SummaryDrosophila telomeres are comprised of DNA sequences that differ dramatically from those of other eukaryotes. Telomere functions, however, are similar to those found in telomerase-based telomeres, even though the underlying mechanisms may differ. Drosophila telomeres use arrays of retrotransposons to maintain chromosome length, while nearly all other eukaryotes rely on telomerase-generated short repeats. Regardless of the DNA sequence, several end-binding proteins are evolutionarily conserved. Away from the end, the Drosophila telomeric and subtelomeric DNA sequences are complexed with unique combinations of proteins that also modulate chromatin structure elsewhere in the genome. Maintaining and regulating the transcriptional activity of the telomeric retrotransposons in Drosophila requires specific chromatin structures, and while telomeric silencing spreads from the terminal repeats in yeast, the source of telomeric silencing in Drosophila is the subterminal arrays. However, the subterminal arrays in both species may be involved in telomere-telomere associations and/or communication.

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“…One phenomenon in which the Y chromosome affects expression of genes is position-effect variegation (PEV) (Muller 1930;Gatti and Pimpinelli 1992;Talbert and Henikoff 2006;Schulze and Wallrath 2007). PEV occurs when genes are relocated next to a heterochromatin-euchromatin boundary.…”

Section: Introductionmentioning

confidence: 99%

“…The variegated expression of w[m4] results in a mosaic, redwhite eye-color phenotype. PEV-associated repression of gene transcription is thought to result from the spread of pericentromeric heterochromatin into neighboring genes with consequent transcriptional silencing of those genes (Schulze and Wallrath 2007). Y-chromosomal heterochromatin is known to suppress PEV in both XY males and XXY females (Dorer and Henikoff 1994), with the level of suppression proportional to the amount of the Y chromosome heterochromatin present (Dimitri and Pisano 1989).…”

mentioning

confidence: 99%

YNot a Dead End: Epistatic Interactions BetweenY-Linked Regulatory Polymorphisms and Genetic Background Affect Global Gene Expression inDrosophila melanogaster

2010

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The Y chromosome, inherited without meiotic recombination from father to son, carries relatively few genes in most species. This is consistent with predictions from evolutionary theory that nonrecombining chromosomes lack variation and degenerate rapidly. However, recent work has suggested a dynamic role for the Y chromosome in gene regulation, a finding with important implications for spermatogenesis and male fitness. We studied Y chromosomes from two populations of Drosophila melanogaster that had previously been shown to have major effects on the thermal tolerance of spermatogenesis. We show that these Y chromosomes differentially modify the expression of hundreds of autosomal and X-linked genes.Genes showing Y-linked regulatory variation (YRV) also show an association with immune response and pheromone detection. Indeed, genes located proximal to the euchromatin-heterochromatin boundary of the X chromosome appear particularly responsive to Y-linked variation, including a substantial number of odorant-binding genes. Furthermore, the data show significant regulatory interactions between the Y chromosome and the genetic background of autosomes and X chromosome. Altogether, our findings support the view that interpopulation, Y-linked regulatory polymorphisms can differentially modulate the expression of many genes important to male fitness, and they also point to complex interactions between the Y chromosome and genetic background affecting global gene expression.T HE Y chromosome is transmitted without sexual recombination from father to son. In the Y chromosome, as in other nonrecombining regions, complete linkage between genes results in the accumulation of deleterious alleles and the loss of genetic diversity due to the evolutionary processes of Muller's ratchet, background selection, and genetic hitchhiking (Bull 1983;Rice 1987;Charlesworth and Charlesworth 2000;Bachtrog et al. 2008). Consistent with theory, the Y chromosome of Drosophila melanogaster carries only 13 known protein-coding genes (Carvalho et al. 2001;Carvalho and Clark 2005;Koerich et al. 2008;Vibranovski et al. 2008;Krsticevic et al. 2010), whereas .5000 genes would be expected from typical gene densities in euchromatic regions.Six of the 13 genes discovered on the Y chromosome are male fertility factors that either encode structural components of spermatogenesis or regulate spermatogenesis-specific processes such as individualization (Carvalho et al. 2000(Carvalho et al. , 2009. Spermatogenesis in Drosophila males is extremely sensitive to heat, with males becoming sterile anywhere from 23°in heatsensitive species to 31°in heat-tolerant species (Chakir et al. 2002;David et al. 2005). In D. melanogaster, Rohmer et al. (2004) found that differences between Y chromosome lineages from tropical and temperate regions are responsible for much of the variation in thermal sensitivity of spermatogenesis. Since spermatogenesis is essential for male fitness, we expect a Y chromosome effect on thermal sensitivity to translate into effects on mal...

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Gene Regulation by Chromatin Structure: Paradigms Established inDrosophila melanogaster

Cited by 57 publications

References 147 publications

Epigenetic effects of polymorphic Y chromosomes modulate chromatin components, immune response, and sexual conflict

Epigenetic effects of polymorphic Y chromosomes modulate chromatin components, immune response, and sexual conflict

Drosophila telomeres: an exception providing new insights

YNot a Dead End: Epistatic Interactions BetweenY-Linked Regulatory Polymorphisms and Genetic Background Affect Global Gene Expression inDrosophila melanogaster

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