Regulation of Nucleolar Dominance in <i>Drosophila melanogaster</i>

Warsinger-Pepe, Natalie; Li, Duojia; Yamashita, Yukiko

doi:10.1534/genetics.119.302471

Cited by 19 publications

(18 citation statements)

References 70 publications

(100 reference statements)

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“…Silent rRNA genes in mammalian cells are known to have hypermethylated DNA and regular nucleosomes carrying repressive histone modifications, such as H3K9me3, H4K20me3 and H3K27me3 ( 94 , 95 , 102 , 103 ) (see ( 26–29 ) for reviews). In D. melanogaster , heterochromatin components have been shown to be implicated in maintaining the nucleolar structure and preventing recombination between rDNA repeats ( 22 ), as well as in nucleolar dominance, a phenomenon whereby an entire rDNA cluster is silenced ( 104 ). However, the association of repressive chromatin marks with silencing of individual rDNA units in Drosophila was not evident.…”

Section: Discussionmentioning

confidence: 99%

Impaired function of rDNA transcription initiation machinery leads to derepression of ribosomal genes with insertions of R2 retrotransposon

Fefelova

Pleshakova

Mikhaleva

et al. 2022

Nucleic Acids Research

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Eukaryotic genomes harbor hundreds of rRNA genes, many of which are transcriptionally silent. However, little is known about selective regulation of individual rDNA units. In Drosophila melanogaster, some rDNA repeats contain insertions of the R2 retrotransposon, which is capable to be transcribed only as part of pre-rRNA molecules. rDNA units with R2 insertions are usually inactivated, although R2 expression may be beneficial in cells with decreased rDNA copy number. Here we found that R2-inserted rDNA units are enriched with HP1a and H3K9me3 repressive mark, whereas disruption of the heterochromatin components slightly affects their silencing in ovarian germ cells. Surprisingly, we observed a dramatic upregulation of R2-inserted rRNA genes in ovaries lacking Udd (Under-developed) or other subunits (TAF1b and TAF1c-like) of the SL1-like complex, which is homologues to mammalian Selective factor 1 (SL1) involved in rDNA transcription initiation. Derepression of rRNA genes with R2 insertions was accompanied by a reduction of H3K9me3 and HP1a enrichment. We suggest that the impairment of the SL1-like complex affects a mechanism of selective activation of intact rDNA units which competes with heterochromatin formation. We also propose that R2 derepression may serve as an adaptive response to compromised rRNA synthesis.

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Section: Discussionmentioning

confidence: 99%

Impaired function of rDNA transcription initiation machinery leads to derepression of ribosomal genes with insertions of R2 retrotransposon

Fefelova

Pleshakova

Mikhaleva

et al. 2022

Nucleic Acids Research

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“…The In(1)sc 8 inversion was created in the laboratory of A. Serebrovsky by X-ray mutagenesis of w a flies [ 21 , 22 , 25 , 26 , 27 ]. The In(1)sc 8 , sc 8 y 31d w a stock was transferred to the Bloomington Drosophila Stock Center (BDSC) from the California Institute of Technology (Caltech) in 1986 and assigned the stock number 798.…”

Section: Resultsmentioning

confidence: 99%

“…In various organisms, the phenomenon of inactivation of individual rDNA clusters, known as “nucleolar dominance”, has been described. In males of D. melanogaster , the Y chromosome rDNA locus is usually thought to dominate over the X chromosome locus [ 19 , 20 , 21 ]. The choice of an active rDNA cluster is a complex phenomenon, which depends, among other things, on cis -acting factors, such as the distal pericentromeric heterochromatin of the X chromosome [ 21 , 22 ].…”

Section: Introductionmentioning

confidence: 99%

A Spontaneous Inversion of the X Chromosome Heterochromatin Provides a Tool for Studying the Structure and Activity of the Nucleolus in Drosophila melanogaster

Колесникова

Klenov

Nokhova

et al. 2022

Cells

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The pericentromeric heterochromatin is largely composed of repetitive sequences, making it difficult to analyze with standard molecular biological methods. At the same time, it carries many functional elements with poorly understood mechanisms of action. The search for new experimental models for the analysis of heterochromatin is an urgent task. In this work, we used the Rif1 mutation, which suppresses the underreplication of all types of repeated sequences, to analyze heterochromatin regions in polytene chromosomes of Drosophila melanogaster. In the Rif1 background, we discovered and described in detail a new inversion, In(1)19EHet, which arose on a chromosome already carrying the In(1)sc8 inversion and transferred a large part of X chromosome heterochromatin, including the nucleolar organizer to a new euchromatic environment. Using nanopore sequencing and FISH, we have identified the eu- and heterochromatin breakpoints of In(1)19EHet. The combination of the new inversion and the Rif1 mutation provides a promising tool for studies of X chromosome heterochromatin structure, nucleolar organization, and the nucleolar dominance phenomenon. In particular, we found that, with the complete polytenization of rDNA repeats, the nucleolus consists of a cloud-like structure corresponding to the classical nucleolus of polytene chromosomes, as well as an unusual intrachromosomal structure containing alternating transcriptionally active and inactive regions.

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“…Repressive epigenetic modifiers play vital roles in the allele-specific expression of SNULs, and also rRNAs during NuD 46,48,49 . Interestingly, specific sequence elements located near the NORs are implicated to control NuD [50][51][52] . For example, in the germ cells of male Drosophila, Y chromosome sequence elements promote developmentally-regulated NuD of the Y chromosomeencoded rRNA over the X-chromosome rRNA 52 .…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, specific sequence elements located near the NORs are implicated to control NuD [50][51][52] . For example, in the germ cells of male Drosophila, Y chromosome sequence elements promote developmentally-regulated NuD of the Y chromosomeencoded rRNA over the X-chromosome rRNA 52 . It is possible that SNULs, by associating with an NOR allele could dictate allele-specific expression of rRNA arrays in human cells.…”

Section: Discussionmentioning

confidence: 99%

Monoallelically-expressed Noncoding RNAs form nucleolar territories on NOR-containing chromosomes and regulate rRNA expression

Hao

Liu

Daulatabad

et al. 2022

Preprint

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Out of the several hundred copies of rRNA genes that are arranged in the nucleolar organizing regions (NOR) of the five human acrocentric chromosomes, ~50% remain transcriptionally inactive. NOR-associated sequences and epigenetic modifications contribute to differential expression of rRNAs. However, the mechanism(s), controlling the dosage of active versus inactive rRNA genes in mammals is yet to be determined. We have discovered a family of ncRNAs, SNULs (Single NUcleolus Localized RNA), which form constrained sub-nucleolar territories on individual NORs and influences rRNA expression. Individual members of the SNULs monoallelically associate with specific NOR-containing chromosome. SNULs share sequence similarity to pre-rRNA and localize in the sub-nucleolar compartment with pre-rRNA. Finally, SNULs control rRNA expression by influencing pre-rRNA sorting to the DFC compartment and pre-rRNA processing. Our study discovered a novel class of ncRNAs that by forming constrained nucleolar territories on individual NORs contribute to rRNA expression.

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Regulation of Nucleolar Dominance in Drosophila melanogaster

Cited by 19 publications

References 70 publications

Impaired function of rDNA transcription initiation machinery leads to derepression of ribosomal genes with insertions of R2 retrotransposon

Impaired function of rDNA transcription initiation machinery leads to derepression of ribosomal genes with insertions of R2 retrotransposon

A Spontaneous Inversion of the X Chromosome Heterochromatin Provides a Tool for Studying the Structure and Activity of the Nucleolus in Drosophila melanogaster

Monoallelically-expressed Noncoding RNAs form nucleolar territories on NOR-containing chromosomes and regulate rRNA expression

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