Unstable redundancy of genes for ribosomal RNA.

Ritossa, Ferruccio

doi:10.1073/pnas.60.2.509

Cited by 178 publications

(85 citation statements)

References 10 publications

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“…Some short rDNA arrays can increase in size through meiotic magnification, resulting in heritable alterations in mean rDNA array size in a population (38,39). The deletions we generated possess the ability to magnify at a rate of up to 15 copies per fly generation (34), which provided us the opportunity to confirm the correlation between expression and rDNA deletion.…”

mentioning

confidence: 77%

Ribosomal DNA contributes to global chromatin regulation

Paredes

Maggert

2009

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

142

144

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The 35S ribosomal RNA genes (rDNA) are organized as repeated arrays in many organisms. Epigenetic regulation of transcription of the rRNA results in only a subset of copies being transcribed, making rDNA an important model for understanding epigenetic chromatin modification. We have created an allelic series of deletions within the rDNA array of the Drosophila Y chromosome that affect nucleolus size and morphology, but do not limit steady-state rRNA concentrations. These rDNA deletions result in reduced heterochromatin-induced gene silencing elsewhere in the genome, and the extent of the rDNA deletion correlates with the loss of silencing. Consistent with this, chromosomes isolated from strains mutated in genes required for proper heterochromatin formation have very small rDNA arrays, reinforcing the connection between heterochromatin and the rDNA. In wild-type cells, which undergo spontaneous natural rDNA loss, we observed the same correlation between loss of rDNA and loss of heterochromatin-induced silencing, showing that the volatility of rDNA arrays may epigenetically influence gene expression through normal development and differentiation. We propose that the rDNA contributes to a balance between heterochromatin and euchromatin in the nucleus, and alterations in rDNA-induced or natural-affect this balance.Drosophila ͉ epigenetics ͉ heterochromatin ͉ nucleolus ͉ rDNA C hromatin within the nucleus is divided into cytologically heterochromatic and euchromatic compartments (1). This division reflects very different functional influences on gene expression (2). Many genes adopt more ''heterochromatin-like'' features when inactivated, including cytological appearance and association with specific proteins or post-translational modifications. This has led to hypotheses that similar mechanisms regulate facultatively inactivated genes or chromosomes, constitutively heterochromatic regions of the genome, and developmentally repressed genes (3). Understanding the interplay between heterochromatin and euchromatin, then, is fundamental in understanding the control of epigenetic regulation of the genome.Gene products involved in heterochromatin formation have been primarily identified by observing the effect of mutations on position effect variegation (PEV), which manifests as mosaic expression of a gene placed in a heterochromatic context. Many of these mutations act dominantly, thus the genes are thought to encode dosesensitive components of heterochromatin (4). Equally important to models of heterochromatin formation is the observation that the amount of constitutive heterochromatin in the nucleus affects heterochromatin-induced PEV at unlinked genes (5). In this model, gene products act as a ''source'' of heterochromatin forming potential, and DNA sequences destined to be heterochromatic as a ''sink.'' A balance is normally maintained between gene products and target DNA in the genome, although no proposed mechanism satisfactorily accounts for how this balance is maintained during division, determination, and differe...

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mentioning

confidence: 77%

Ribosomal DNA contributes to global chromatin regulation

Paredes

Maggert

2009

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

142

144

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“…At this point it is important to make a distinction between the purely somatic phenomenon reported by Tartof and the inherited rDNA increase described by Ritossa under the name "magnification" (26,27). Magnification involves the bobbed mutations, which are partial deficiencies for the rDNA.…”

Section: Discussionmentioning

confidence: 99%

Independent Control of Ribosomal Gene Replication in Polytene Chromosomes of Drosophila melanogaster

Spear

Gall

1973

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

143

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The saturation values for ribosomal RNA hybridization have been determined for DNA from diploid and polytene tissues of Drosophila melanogaster. These values have been measured in XO and XX larvae which have, respectively, one and two nucleolus organizers in the diploid chromosome set. The results show that (1) in diploid cells the ribosomal (r)DNA is present in amounts proportional to the number of nucleolus organizers, (2) in polytene cells the rDNA is under-replicated with respect to the euchromatic DNA, and (3) in polytene cells the amount of rDNA is independent of the diploid number of nucleolus organizers. These observations suggest that somatic variations in rDNA content may involve independent polytenization of the nucleolus organizer without change in the number of ribosomal cistrons per organizer. The independent polytenization of rl)NA is proposed as the chromosomal explanation for the relative increase in rDNA in flies of the XO constitution.The chromosomes of Drosophila melanogaster, like those of most eukaryotes, contain two distinct types of chromatin, the euchromatin and the heterochromatin. The euchromatin is diffuse during interphase, is lightly staining in mitotic prophase, and contains almost all of the known genes (1). The heterochromatin, contrastingly, remains condensed during interphase, is consequently darkly staining in mitotic prophase, and contains very few genes. In addition to these genetic and cytological distinctions, the euchromatin consists mainly of unique DNA sequences, while most of the heterochromatin in diploid cells is highly repeated satellite DNA (2)(3)(4).During the formation of the giant polytene chromosomes of the Drosophila salivary gland, the differences between the euchromatin and heterochromatin become even more pronounced. The euchromatic arms proceed through a series of DNA replications resulting in as many as 1024 DNA fibers (5). The heterochromatic regions of the chromosomes, on the other hand, clump together forming the chromocenter and replicate little or not at all (2, 6). The resulting polytene nucleus has a large increase in unique DNA, but little or no increase in the heterochromatic satellite DNA (2, 7).In D. melanogaster the DNA that codes for ribosomal RNA is located at or near the nucleolus organizer, a region within the heterochromatin of the X and Y chromosomes (8). The ribosomal cistrons are repeated about 250 times in the nucleolus organizer of wild-type stocks (9). The properties of the ribosomal (r)DNA are quite different from those of the heterochromatic DNA that surrounds it. For instance, the rDNA is genetically active, transcribing rRNA and forming a prominent nucleolus in both diploid and polytene tissues. Unlike the satellite DNA, the rDNA replicates during the formation of polytene tissue. This has been demonstrated by thymidine incorporation in D. melanogaster (10, 28), and by rRNA hybridization to DNA from salivary glands of D. hydei (11, 12), Sciara (13), and Rhynchosciara (14).Because the rDNA in polytene nuclei is near the n...

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“…Work on the rDNA loci of D. melanogaster also began well before the advent of DNA cloning when it was found that a short bristle phenotype known as bobbed (bb) was associated with low numbers of rRNA genes on the X chromosome (Ritossa et al 1966). 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).…”

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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Unstable redundancy of genes for ribosomal RNA.

Cited by 178 publications

References 10 publications

Ribosomal DNA contributes to global chromatin regulation

Ribosomal DNA contributes to global chromatin regulation

Independent Control of Ribosomal Gene Replication in Polytene Chromosomes of Drosophila melanogaster

Finely Orchestrated Movements: Evolution of the Ribosomal RNA Genes

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