Reduced Polyteny of Ribosomal RNA Cistrons in Giant Chromosomes of Drosophila hydei*

Hennig, Wolfgang; Meer, Barbara

doi:10.1038/newbio233070a0

Cited by 138 publications

(21 citation statements)

References 23 publications

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“…A reduced level of rDNA in the salivary gland compared to other tissues has been demonstrated previously in Drosophila hydei (12) and in Rhynchosciara (14). There is also a reduction of rDNA in D. melanogaster larvae as compared to adults (19).…”

Section: Resultsmentioning

confidence: 62%

“…In diploid DNA we found that, as expected, the amount of rDNA was in proportion to the number of nucleolus organizers. However, the rDNA content of polytene cells is not only lower than expected, as previously reported by Hennig and Meer (12), but it is also independent of the number of nucleolus organizers in the zygote. We have concluded that the rDNA in polytene chromosomes is under different replicative control than either the euchromatic DNA or the heterochromatic DNA.…”

mentioning

confidence: 60%

“…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).…”

mentioning

confidence: 99%

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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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Section: Resultsmentioning

confidence: 62%

mentioning

confidence: 60%

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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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“…In contrast, the copy number per haploid genome (representation) of numerous sequences changes in many endocycling cells. For example, many polyploid and polytene cells contain greatly reduced amounts of DNAs residing in heterochromatic regions (Heitz 1934; for review, see Spradling and OrrWeaver 1987), including DNA satellites (Gall et al 1971) and rDNAs (Hennig and Meer 1971). In eukaryotes, genomes are replicated in temporally distinct intervals of the S phase (reviewed in Hand 1978).…”

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confidence: 99%

The Drosophila endocycle is controlled by Cyclin E and lacks a checkpoint ensuring S-phase completion.

Lilly

Spradling²

1996

Genes Dev.

262

289

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Early during Drosophila oogenesis the 16 interconnected cells of each germ-line cyst choose between two alternative fates. The single future oocyte enters meiosis, arrests, and becomes transcriptionally quiescent. The remaining 15 cells initiate a series of polyploid cell cycles to prepare for their role as nurse cells. Like many other polyploid and polytene cells, during nurse cell growth the major satellite DNAs become highly under-represented by a mechanism that has remained obscure. We implicate the cell-cycle regulator cyclin E in DNA under-representation by identifying a hypomorphic, female sterile cycE mutation, cycE 01672, that increases the amount of satellite DNA propagated in nurse cells. In mutant but not wild-type endomitotic nurse cells, "late S" patterns of bromodeoxyuridine incorporation are observed similar to those in mitotic cells. CycE protein still cycles in cycE °167z germ-line cysts but at reduced levels, and it is found throughout a longer fraction of the cell cycle. Our experiments support the view that oscillating levels of CycE control the polyploid S phase. Moreover, they indicate that a checkpoint linking the presence of unreplicated DNA to the CycE oscillator is lacking, leading to incomplete replication of late-replicating sequences such as satellite DNAs. Unexpectedly, two to three of the 16 cells in cFcE 01672 cysts frequently differentiate as oocytes, implicating cell-cycle programming in oocyte determination.

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“…Within the Diptera, the replication of the rRNA genes (rDNA) during polyploidization has long been known to be independent of the replication of the euchromatic genome (1)(2)(3)(4). The mechanisms underlying this independent regulation of rDNA polyploidization are not understood but the studies of Spear and Gall (2,3) have established that in polytene salivary gland tissue, the rDNA is autonomously replicated to a constant level that is independent of both the amount of rDNA initially present in the diploid genome and the number of nucleolar organizer (NO) regions within the genome in which this rDNA is distributed.…”

mentioning

confidence: 99%

A stochastic mechanism controls the relative replication of equally competent ribosomal RNA gene sets in individual dipteran polyploid nuclei.

Belikoff¹,

Beckingham²

1985

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

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The endoreplication of the two nucleolar organizers (NOs) of the diploid genome has been examined in individual polyploid nuclei of the dipteran Calliphora erythrocephala. Crosses between two strains with diagnostic nontranscribed spacer polymorphisms in their rRNA genes were used to provide progeny with distinguishable NOs, and single nuclei of two highly polyploid cell types-salivary gland and nurse cells--were examined from individual F1 animals.Initially the representation of the two NOs in total polyploid tissue DNA was determined. This revealed that, although the NO regions present in one of the strains (Tom) were very similar in spacer composition, they displayed two types of behavior in the hybrids containing the single NO region typical of the second strain (Karla). In TW phenotype F1 progeny, very little replication of the Tom NO relative to the Karla NO occurred, whereas in TS phenotype progeny replication of the Tom and Karla NOs was approximately equivalent. When individual polyploid nuclei of the TS phenotype animals were examined, however, the relative replication of the Tom and Karla NOs was found not to be a fixed genetic property but to vary dramatically from cell to cell. This was true even for the nurse cell nuclei within a single ovarian follicle, which are the products of only four mitotic divisions of a single germ-line cell. These findings indicate that for NOs of similar replicative competence, a stochastic mechanism governs the relative usage of each NO for endoreplication and that the relative activity of the two NOs is not stably determined through the mitotic divisions preceding polyploidization. Stochastic selection after mitotic DNA replication could be a general phenomenon governing the relative usage (transcription) of different, but equally competent, alleles of any gene in individual cells, if the required factors are in short supply.Within the Diptera, the replication of the rRNA genes (rDNA) during polyploidization has long been known to be independent of the replication of the euchromatic genome (1-4). The mechanisms underlying this independent regulation of rDNA polyploidization are not understood but the studies of Spear and Gall (2, 3) have established that in polytene salivary gland tissue, the rDNA is autonomously replicated to a constant level that is independent of both the amount of rDNA initially present in the diploid genome and the number of nucleolar organizer (NO) regions within the genome in which this rDNA is distributed. It has been suggested that endoreplication of rDNA cistrons from only one NO may in part explain these observations (1, 5-7).Recent studies have established that, at the level of the total polyploid tissue DNA, the overall contribution of the two NOs to the polyploidization of the rDNA is a function of the pair of NOs examined (6,(8)(9)(10)(11)(12). In some cases, one NO is replicated to the virtual exclusion of the other, whereas for other NO pairs, cistrons from both NOs are equally well represented in the total polyploid tissue DNA...

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Reduced Polyteny of Ribosomal RNA Cistrons in Giant Chromosomes of Drosophila hydei*

Cited by 138 publications

References 23 publications

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

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

The Drosophila endocycle is controlled by Cyclin E and lacks a checkpoint ensuring S-phase completion.

A stochastic mechanism controls the relative replication of equally competent ribosomal RNA gene sets in individual dipteran polyploid nuclei.

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