Abstract
The number of ribosomal RNA genes and the rate of ribosomal RNA synthesis have been analyzed in a mutant of Xenopus laevis carrying two partial nucleolar organizers (p 1−1/p1−2 nu). The p 1−1 and p 1−2 nucleolar organizers have fewer ribosomal RNA genes than the normal (+ nu) organizer, and each produces a smaller nucleolus than the + nu organizer in heterozygous embryos (+/p 1−1 and +/p 1−2). These heterozygotes develop normally and synthesize ribosomal RNA at normal rates. The p 1−1/p1−2 nu mutants die at an early stage of development, and they synthesize ribosomal RNA at only 50% of the normal rate even though they have 70% of the haploid number of ribosomal RNA genes. These results show that the ribosomal RNA genes contained in a partial nucleolar organizer are not transcribed with the same efficiency as those found in an intact organizer and suggest the existence of genes, within the nucleolar organizer, which control the transcription of ribosomal RNA.
Similar content being viewed by others
References
Birnstiel, M. L., Speirs, J., Purdom, I., Jones, K., and Loening, V. E. (1968). Properties and composition of the isolated ribosomal DNA satellite of Xenopus laevis. Nature 219454.
Brown, D. D. (1966). The nucleolus and synthesis of ribosomal RNA during oogenesis and embryogenesis of Xenopus laevis. Natl. Cancer Inst. Monograph 23297.
Brown, D. D., and Gurdon, J. B. (1964). Absence of ribosomal RNA synthesis in the anucleolate mutant of Xenopus laevis. Proc. Natl. Acad. Sci. 51139.
Brown, D. D., and Littna, E. (1964). RNA synthesis during the development of Xenopus laevis. J. Mol. Biol. 8669.
Brown, D. D., and Weber, C. S. (1968). Gene linkage by RNA-DNA hybridization. II. Arrangement of the redundant gene sequences for 28 s and 18 s ribosomal RNA. J. Mol. Biol. 34681.
Dawid, I. B., Brown, D. D., and Reeder, R. H. (1970). Composition and structure of chromosomal and amplified ribosomal DNA's of Xenopus laevis. J. Mol. Biol. 51341.
Eliceiri, G. L., and Greene, H. (1969). Ribosomal RNA synthesis in human-mouse hybrid cells. J. Mol. Biol. 41253.
Elsdale, T. R., Fischberg, M., and Smith, S. (1958). A mutation which reduces nucleolar number in Xenopus laevis. Exptl. Cell Res. 14642.
Gurdon, J. B. (1967). Control of gene activity during the early development of Xenopus laevis. In Brink, R. A. (ed.), Heritage from Mendel, University of Wisconsin Press, Madison, pp. 203–241.
Jacob, F., and Monod, J. (1963). Genetic repression, allosteric inhibition, and cellular differentiation. In Locke, M. (ed.). Cytodifferentiation and Macromolecular Synthesis, Academic Press, New York, pp. 30–64.
Keep, E. (1962). Satellite and nucleolar number of hybrids between Ribes nigrum and R. grossularia and in their backcrosses. Can. J. Genet. Cytol. 4206.
Knowland, J. (1970). Polyacrylamide gel electrophoresis of nucleic acids synthesised during the early development of Xenopus laevis (Daudin). Biochim. Biophys. Acta 204416.
Knowland, J., and Miller, L. (1970). Reduction of ribosomal RNA synthesis and ribosomal RNA genes in a mutant of Xenopus laevis which organizes only a partial nucleolus. I. Ribosomal RNA synthesis in embryos of different nucleolar types. J. Mol. Biol. 53321.
McClintock, B. (1934). The relation of a particular chromosomal element to the development of the nucleoli in Zea mays. Z. Zellforsch. Mikroskop. Anat. 21294.
Miller, L., and Brown, D. D. (1969). Variation in the activity of nucleolar organizers and their ribosomal gene content. Chromosoma (Berlin) 28430.
Miller, L., and Gurdon, J. B. (1970). Mutations affecting the size of the nucleolus in Xenopus laevis. Nature 2271108.
Miller, L., and Knowland, J. (1970). Reduction of ribosomal RNA synthesis and ribosomal RNA genes in a mutant of Xenopus laevis which organizes only a partial nucleolus. II. The number of ribosomal RNA genes in animals of different nucleolar types. J. Mol. Biol. 53329.
Mohan, J., and Ritossa, F. M. (1970). Regulation of ribosomal RNA synthesis and its bearing on the bobbed phenotype of Drosophila melanogaster. Develop. Biol. 22495.
Nieuwkoop, P. D., and Faber, J. (1956). Normal Tables of Xenopus laevis (Daudin), North Holland, Amsterdam, 1956.
Ritossa, F. M. (1968). Nonoperative DNA complementary to ribosomal RNA. Proc. Natl. Acad. Sci. 591124.
Ritossa, F. M., and Spiegelman, S. (1965). Localization of DNA complementary to ribosomal RNA in the nucleolus organizer region of Drosophila melanogaster. Proc. Natl. Acad. Sci. 53737.
Ritossa, F. M., Atwood, K. C., Lindsley, D. L., and Spiegelman, S. (1966). On the chromosomal distribution of DNA complementary to ribosomal and soluble RNA. Natl. Cancer Inst. Monograph 23449.
Perry, R. P., and Kelly, D. E. (1970). Inhibition of RNA synthesis by actinomycin D: Characteristic dose-response of different RNA species. J. Cell. Physiol. 76127.
Wallace, H., and Birnstiel, M. L. (1966). Ribosomal cistrons and the nucleolar organizer. Biochim. Biophys. Acta 114296.
Woodland, H. R., and Gurdon, J. B. (1968). The relative rates of synthesis of DNA, sRNA and rRNA in the endodermal region and other parts of developing Xenopus laevis embryos. J. Embryol. Exptl. Morphol. 19363.
Author information
Authors and Affiliations
Additional information
This investigation was supported by a U.S. Public Health Service Research Grant No. CA-39, 026-01A1 to L. M. from the National Cancer Institute and by a scholarship for training in research methods to J. K. from the Medical Research Council of Great Britain.
Rights and permissions
About this article
Cite this article
Miller, L., Knowland, J. The number and activity of ribosomal RNA genes in Xenopus laevis embryos carrying partial deletions in both nucleolar organizers. Biochem Genet 6, 65–73 (1972). https://doi.org/10.1007/BF00485967
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00485967