A Distinct Type of Heterochromatin Within <i>Drosophila melanogaster</i> Chromosome 4

Haynes, Karmella A.; Gracheva, Elena; Elgin, Sarah C. R.

doi:10.1534/genetics.106.066407

Cited by 27 publications

(37 citation statements)

References 26 publications

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“…This finding is consistent with reports that Su(var)3-9 06 acts not as a suppressor but as a weak dominant enhancer of PEV with reporters located in the fourth chromosome arm (Haynes et al 2007). This enhancement of PEV has been suggested to be the consequence of redistribution of the heterochromatin components made available upon loss of pericentric targets (Haynes et al 2007). Since the putative enhancement effect seen in this case was subtle, we repeated the assay at a greater level of sensitivity, using three different mutant alleles of Su(var)3-9.…”

Section: Methodssupporting

confidence: 93%

“…In addition, the fourth chromosome morphology was altered in these mutants, most often appearing elongated and constricted, with HP1 bands more well defined in the polytene chromosomes (Figure 4, A and B). As previously suggested, this configuration may arise as an effect of surplus heterochromatin components liberated from pericentric heterochromatin by loss of SU (VAR)3-9 function (Haynes et al 2007). Liberated heterochromatin components may thereby become available to the fourth chromosome heterochromatin forming mechanism, increasing the heterochromatic character of chromosome four.…”

mentioning

confidence: 84%

“…Mutant alleles of the Su(var)3-9 gene, which produces the third H3K9-specific methyltransferase, are potent suppressors of PEV when present with a variegating rearrangement of the white gene or with hsp70-w reporters in pericentric heterochromatin (Tschiersch et al 1994;Haynes et al 2007). SU(VAR)3-9 has been described as the main chromocenter-specific histone methyltransferase (HMT) in Drosophila (Schotta et al 2003b).…”

Section: Methodsmentioning

confidence: 99%

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Multiple SET Methyltransferases Are Required to Maintain Normal Heterochromatin Domains in the Genome of Drosophila melanogaster

et al. 2009

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Methylation of histone H3 lysine 9 (H3K9) is a key feature of silent chromatin and plays an important role in stabilizing the interaction of heterochromatin protein 1 (HP1) with chromatin. Genomes of metazoans such as the fruit fly Drosophila melanogaster generally encode three types of H3K9-specific SET domain methyltransferases that contribute to chromatin homeostasis during the life cycle of the organism. SU(VAR)3-9, dG9a, and dSETDB1 all function in the generation of wild-type H3K9 methylation levels in the Drosophila genome. Two of these enzymes, dSETDB1 and SU(VAR)3-9, govern heterochromatin formation in distinct but overlapping patterns across the genome. H3K9 methylation in the small, heterochromatic fourth chromosome of D. melanogaster is governed mainly by dSETDB1, whereas dSETDB1 and SU(VAR)3-9 function in concert to methylate H3K9 in the pericentric heterochromatin of all chromosomes, with dG9a having little impact in these domains, as shown by monitoring position effect variegation. To understand how these distinct heterochromatin compartments may be differentiated, we examined the developmental timing of dSETDB1 function using a knockdown strategy. dSETDB1 acts to maintain heterochromatin during metamorphosis, at a later stage in development than the reported action of SU(VAR)3-9. Surprisingly, depletion of both of these enzymes has less deleterious effect than depletion of one. These results imply that dSETDB1 acts as a heterochromatin maintenance factor that may be required for the persistence of earlier developmental events normally governed by SU(VAR)3-9. In addition, the genetic interactions between dSETDB1 and Su(var)3-9 mutations emphasize the importance of maintaining the activities of these histone methyltransferases in balance for normal genome function.

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Section: Methodssupporting

confidence: 93%

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confidence: 84%

Section: Methodsmentioning

confidence: 99%

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Multiple SET Methyltransferases Are Required to Maintain Normal Heterochromatin Domains in the Genome of Drosophila melanogaster

et al. 2009

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“…This is interesting as the dosage-compensated male X chromosome is particularly sensitive to loss of ISWI (Corona et al 2002). Finally, PEV of insertions on the distal fourth chromosome are modified by the dose of the fourth chromosome, while insertions on the second chromosome are not (Haynes et al 2007). This reinforces the idea that factors required for fourth chromosome heterochromatin differ from other heterochromatic regions.…”

Section: Discussionmentioning

confidence: 99%

Coordinated Regulation of Heterochromatic Genes inDrosophila melanogasterMales

et al. 2009

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Dosage compensation modifies the chromatin of X-linked genes to assure equivalent expression in sexes with unequal X chromosome dosage. In Drosophila dosage compensation is achieved by increasing expression from the male X chromosome. The ribonucleoprotein dosage compensation complex (DCC) binds hundreds of sites along the X chromosome and modifies chromatin to facilitate transcription. Loss of roX RNA, an essential component of the DCC, reduces expression from X-linked genes. Surprisingly, loss of roX RNA also reduces expression from genes situated in proximal heterochromatin and on the small, heterochromatic fourth chromosome. Mutation of some, but not all, of the genes encoding DCC proteins produces a similar effect. Reduction of roX function suppresses position effect variegation (PEV), revealing functional alteration in heterochromatin. The effects of roX mutations on heterochromatic gene expression and PEV are limited to males. A sex-limited role for the roX RNAs in autosomal gene expression was unexpected. We propose that this reflects a difference in the heterochromatin of males and females, which serves to accommodate the heterochromatic Y chromosome present in the male nucleus. roX transcripts may thus participate in two distinct regulatory systems that have evolved in response to highly differentiated sex chromosomes: compensation of X-linked gene dosage and modulation of heterochromatin.

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“…Recent studies have illuminated the diversity of heterochromatin that exists throughout the genome (Haynes et al 2007;Riddle et al 2011;Wang et al 2014). These different types of heterochromatin may rely on H3K9me to differing extents.…”

Section: H3k9 Regulation Of Chromatin Architecture and Compositionmentioning

confidence: 99%

Direct interrogation of the role of H3K9 in metazoan heterochromatin function

et al. 2016

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A defining feature of heterochromatin is methylation of Lys9 of histone H3 (H3K9me), a binding site for heterochromatin protein 1 (HP1). Although H3K9 methyltransferases and HP1 are necessary for proper heterochromatin structure, the specific contribution of H3K9 to heterochromatin function and animal development is unknown. Using our recently developed platform to engineer histone genes in Drosophila, we generated H3K9R mutant flies, separating the functions of H3K9 and nonhistone substrates of H3K9 methyltransferases. Nucleosome occupancy and HP1a binding at pericentromeric heterochromatin are markedly decreased in H3K9R mutants. Despite these changes in chromosome architecture, a small percentage of H3K9R mutants complete development. Consistent with this result, expression of most protein-coding genes, including those within heterochromatin, is similar between H3K9R and controls. In contrast, H3K9R mutants exhibit increased open chromatin and transcription from piRNA clusters and transposons, resulting in transposon mobilization. Hence, transposon silencing is a major developmental function of H3K9.

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A Distinct Type of Heterochromatin Within Drosophila melanogaster Chromosome 4

Cited by 27 publications

References 26 publications

Multiple SET Methyltransferases Are Required to Maintain Normal Heterochromatin Domains in the Genome of Drosophila melanogaster

Multiple SET Methyltransferases Are Required to Maintain Normal Heterochromatin Domains in the Genome of Drosophila melanogaster

Coordinated Regulation of Heterochromatic Genes inDrosophila melanogasterMales

Direct interrogation of the role of H3K9 in metazoan heterochromatin function

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