RECOMBINATIONAL CONTROLS OF rDNA REDUNDANCY IN <i>DROSOPHILA</i>

Hawley, R. Scott; Marcus, C.

doi:10.1146/annurev.ge.23.120189.000511

Cited by 87 publications

(78 citation statements)

References 51 publications

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“…The promoter of each rDNA gene lies in a nontranscribed repetitive spacer. Spacers with varying numbers of repeats have been identified, and long variants are enriched in the Y chromosome rDNA array (Hawley and Marcus 1989). Additionally, X chromosome arrays are known to contain a higher proportion of genes disrupted by the R1 and R2 retrotransposons than Y chromosome arrays (Hawley and Marcus 1989).…”

Section: Discussionmentioning

confidence: 99%

“…In D. melanogaster both the X and the Y chromosomes carry an rDNA array, and the transcripts generated from these loci are identical (Tautz et al 1988). Genetic experiments have demonstrated that either of these loci is sufficient for full function (Hawley and Marcus 1989), but the lack of a transcribed polymorphism between the X and the Y rDNA genes has precluded the measurement of array-specific expression.…”

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confidence: 99%

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Nucleolar Dominance of the Y Chromosome in Drosophila melanogaster

Greil

Ahmad

2012

Genetics

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The rDNA genes are transcribed by RNA polymerase I to make structural RNAs for ribosomes. Hundreds of rDNA genes are typically arranged in an array that spans megabase pairs of DNA. These arrays are the major sites of transcription in growing cells, accounting for as much as 50% of RNA synthesis. The repetitive rDNA arrays are thought to use heterochromatic gene silencing as a mechanism for metabolic regulation, since repeated sequences nucleate heterochromatin formation in eukaryotes. Drosophila melanogaster carries an rDNA array on the X chromosome and on the Y chromosome, and genetic analysis has suggested that both are transcribed. However, using a chromatin-marking assay, we find that the entire X chromosome rDNA array is normally silenced in D. melanogaster males, while the Y chromosome rDNA array is dominant and expressed. This resembles "nucleolar dominance," a phenomenon that occurs in interspecific hybrids where an rDNA array from one parental species is silenced, and that from the other parent is preferentially transcribed. Interspecies nucleolar dominance is thought to result from incompatibilities between speciesspecific transcription factors and the rDNA promoters in the hybrid, but our results show that nucleolar dominance is a normal feature of rDNA regulation. Nucleolar dominance within D. melanogaster is only partially dependent on known components of heterochromatic gene silencing, implying that a distinctive chromatin regulatory system may act at rDNA genes. Finally, we isolate variant Y chromosomes that allow X chromosome array expression and suggest that the large-scale organization of rDNA arrays contribute to nucleolar dominance. This is the first example of allelic inactivation in D. melanogaster.

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Nucleolar Dominance of the Y Chromosome in Drosophila melanogaster

Greil

Ahmad

2012

Genetics

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“…As in yeast, meiotic recombination between the rDNA loci on X chromosomes ($10 À4 per generation) was found to be about two orders of magnitude below that expected for a similar length of DNA elsewhere on the chromosome (Williams et al 1989). Interestingly, these crossovers may not represent the typical meiotic recombination events found elsewhere in the genome because the rate of recombination between the rDNA loci on the X and Y chromosomes in males was found to be the same as that observed between X chromosomes, even though recombination is generally absent in D. melanogaster males (Hawley and Marcus 1989;Williams and Robins 1992).…”

Section: Observations In Higher Eukaryotesmentioning

confidence: 94%

“…Remarkably when a bb X chromosome was maintained with a Y chromosome also deficient for many of its rDNA repeats, progeny would appear with a normal number of rDNA units (Ritossa 1968). This phenomenon, referred to as rDNA magnification, induced a series of studies focusing on both the mechanism and the possible genes involved in these dramatic changes within the rDNA locus (reviewed in Tartof 1988;Hawley and Marcus 1989). While magnification generally is assumed to involve multiple rounds of unequal crossover, the mechanism remains undefined.…”

Section: Observations In Higher Eukaryotesmentioning

confidence: 99%

Finely Orchestrated Movements: Evolution of the Ribosomal RNA Genes

2007

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Evolution of the tandemly repeated ribosomal RNA (rRNA) genes is intriguing because in each species all units within the array are highly uniform in sequence but that sequence differs between species. In this review we summarize the origins of the current models to explain this process of concerted evolution, emphasizing early studies of recombination in yeast and more recent studies in Drosophila and mammalian systems. These studies suggest that unequal crossover is the major driving force in the evolution of the rRNA genes with sister chromatid exchange occurring more often than exchange between homologs. Gene conversion is also believed to play a role; however, direct evidence for its involvement has not been obtained. Remarkably, concerted evolution is so well orchestrated that even transposable elements that insert into a large fraction of the rRNA genes appear to have little effect on the process. Finally, we summarize data that suggest that recombination in the rDNA locus of higher eukaryotes is sufficiently frequent to monitor changes within a few generations.

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“…In addition, nucleolar dominance is observed when only one NOR forms a nucleolus in interspecies hybrids 12 . rDNA magnification occurs in yeast and flies with low rDNA content; this process is likely to be mediated by unequal sisterchromatid recombination 13 . Finally, mutations in a protein that regulates silencing in Saccharomyces cerevisiae (SIR2) result in ecc rDNA formation, which is thought to influence cell senescence and aging 14 .…”

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H3K9 methylation and RNA interference regulate nucleolar organization and repeated DNA stability

2006

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Investigations aimed at identifying regulators of nuclear architecture in Drosophila demonstrated that cells lacking H3K9 methylation and RNA interference (RNAi) pathway components displayed disorganized nucleoli, ribosomal DNA (rDNA) and satellite DNAs. The levels of H3K9 dimethylation (H3K9me2) in chromatin associated with repeated DNAs decreased dramatically in Su(var)3-9 and dcr-2 (dicer-2) mutant tissues compared with wild type. We also observed a substantial increase in extrachromosomal circular (ecc) repeated DNAs in mutant tissues. The disorganized nucleolus phenotype depends on the presence of Ligase 4 and ecc DNA formation is not induced by removal of cohesin. We conclude that the structural integrity and organization of repeated DNAs and nucleoli are regulated by the H3K9 methylation and RNAi pathways, and other regulators of heterochromatin-mediated silencing. In addition, repeated DNA stability involves suppression of non-homologous end joining (NHEJ) or other recombination pathways. These results suggest a mechanism for how local chromatin structure can regulate genome stability, and the organization of chromosomal elements and nuclear organelles.Nuclei and chromosomes maintain specific and dynamic architectures that are required for many essential functions 1 . Nuclear bodies are involved in diverse biological processes and exhibit dynamic mobility, and individual chromosomes occupy distinct domains within interphase nuclei2. Chromosomes in the metazoan interphase nucleus are comprised of two types of cytologically and functionally distinct chromatin, euchromatin and heterochromatin3. Patterns of posttranslational histone modifications associated with these domains are strongly correlated with functions such as gene regulation, chromosome inheritance and replication timing4. For example, regions that display heterochromatinmediated gene silencing are rich in histone H3K9 methylation and lack many histone acetylations, whereas histones in transcriptionally active euchromatic regions are highly acetylated and methylated at H3K4 (ref. 5).The first indication that chromosome organization can affect gene expression stems from the discovery of position effect variegation (PEV) in Drosophila 6 . PEV describes the epigenetic inactivation or silencing of a euchromatic gene that has been positioned close to or within ©2007 Nature Publishing Group 3 Correspondence should be addressed to G.H.K. (karpen@fruitfly.org). AUTHOR CONTRIBUTIONS I.P. performed all the experiments, and J.P. and G.K. collaborated on data analysis and project planning.Note: Supplementary Information is available on the Nature Cell Biology website. COMPETING FINANCIAL INTERESTSThe authors declare that they have no competing financial interests. The nucleolus, the site of ribosome assembly, is an example of an essential nuclear organelle. The nucleolus organizer region (NOR) contains tandemly repeated ribosomal DNAs (rDNAs), and is embedded in heterochromatin in most eukaryotes. Single rDNA genes inserted into euchromatin are able...

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RECOMBINATIONAL CONTROLS OF rDNA REDUNDANCY IN DROSOPHILA

Cited by 87 publications

References 51 publications

Nucleolar Dominance of the Y Chromosome in Drosophila melanogaster

Nucleolar Dominance of the Y Chromosome in Drosophila melanogaster

Finely Orchestrated Movements: Evolution of the Ribosomal RNA Genes

H3K9 methylation and RNA interference regulate nucleolar organization and repeated DNA stability

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