Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1985 Aug;82(15):5045–5049. doi: 10.1073/pnas.82.15.5045

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

E J Belikoff, K Beckingham
PMCID: PMC390495  PMID: 2991906

Abstract

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.

Full text

PDF
5045

Images in this article

5046Image
on p.5046
5047Image
on p.5047
5048Image
on p.5048

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Beckingham K., Rubacha A. Different chromatin states of the intron- and type 1 intron+ rRNA genes of Calliphora erythrocephala. Chromosoma. 1984;90(4):311–316. doi: 10.1007/BF00287040. [DOI] [PubMed] [Google Scholar]
  2. Bird A. P. A study of early events in ribosomal gene amplification. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):1179–1183. doi: 10.1101/sqb.1978.042.01.118. [DOI] [PubMed] [Google Scholar]
  3. Botchan M., Topp W., Sambrook J. Studies on simian virus 40 excision from cellular chromosomes. Cold Spring Harb Symp Quant Biol. 1979;43(Pt 2):709–719. doi: 10.1101/sqb.1979.043.01.079. [DOI] [PubMed] [Google Scholar]
  4. Brown D. D. The role of stable complexes that repress and activate eucaryotic genes. Cell. 1984 Jun;37(2):359–365. doi: 10.1016/0092-8674(84)90366-0. [DOI] [PubMed] [Google Scholar]
  5. Dapples C. C., King R. C. The development of the nucleolus of the ovarian nurse cell of Drosophila melanogaster. Z Zellforsch Mikrosk Anat. 1970;103(1):34–47. doi: 10.1007/BF00335399. [DOI] [PubMed] [Google Scholar]
  6. Endow S. A., Glover D. M. Differential replication of ribosomal gene repeats in polytene nuclei of Drosophila. Cell. 1979 Jul;17(3):597–605. doi: 10.1016/0092-8674(79)90267-8. [DOI] [PubMed] [Google Scholar]
  7. Endow S. A. Nucleolar dominance in polytene cells of Drosophila. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4427–4431. doi: 10.1073/pnas.80.14.4427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Endow S. A. On ribosomal gene compensation in Drosophila. Cell. 1980 Nov;22(1 Pt 1):149–155. doi: 10.1016/0092-8674(80)90163-4. [DOI] [PubMed] [Google Scholar]
  9. Endow S. A. Polytenization of the ribosomal genes on the X and Y chromosomes of Drosophila melanogaster. Genetics. 1982 Mar;100(3):375–385. doi: 10.1093/genetics/100.3.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Franz G., Kunz W., Grimm C. Determination of the region of rDNA involved in polytenization in salivary glands of Drosophila hydei. Mol Gen Genet. 1983;191(1):74–80. doi: 10.1007/BF00330892. [DOI] [PubMed] [Google Scholar]
  11. Glover D. M. The rDNA of Drosophila melanogaster. Cell. 1981 Nov;26(3 Pt 1):297–298. doi: 10.1016/0092-8674(81)90197-5. [DOI] [PubMed] [Google Scholar]
  12. Hennig W., Meer B. Reduced polyteny of ribosomal RNA cistrons in giant chromosomes of Drosophila hydei. Nat New Biol. 1971 Sep 15;233(37):70–72. doi: 10.1038/newbio233070a0. [DOI] [PubMed] [Google Scholar]
  13. Macgregor H. C. Amplification, polytenisation, and nucleolus organisers. Nat New Biol. 1973 Nov 21;246(151):81–82. doi: 10.1038/newbio246081a0. [DOI] [PubMed] [Google Scholar]
  14. Renkawitz R., Kunz W. Independent replication of the ribosomal RNA genes in the polytrophic-meroistic ovaries of Calliphora erythrocephala, Drosophila hydei, and Sarcophaga barbata. Chromosoma. 1975 Nov 24;53(2):131–140. doi: 10.1007/BF00333041. [DOI] [PubMed] [Google Scholar]
  15. Ribbert D., Bier K. Multiple nucleoli and enhanced nucleolar activity in the nurse cells of the insect ovary. Chromosoma. 1969;27(2):178–197. doi: 10.1007/BF00326143. [DOI] [PubMed] [Google Scholar]
  16. Schäfer M., Wyman A. R., White R. Length variation in the non-transcribed spacer of Calliphora erythrocephala ribosomal DNA is due to a 350 base-pair repeat. J Mol Biol. 1981 Feb 25;146(2):179–199. doi: 10.1016/0022-2836(81)90431-9. [DOI] [PubMed] [Google Scholar]
  17. Spear B. B., Gall J. G. Independent control of ribosomal gene replication in polytene chromosomes of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1973 May;70(5):1359–1363. doi: 10.1073/pnas.70.5.1359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Spear B. B. The genes for ribosomal RNA in diploid and polytene chromosomes of Drosophila melanogaster. Chromosoma. 1974;48(2):159–179. doi: 10.1007/BF00283961. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES