Abstract
In dividing cells, each sequence replicates exactly once in each S-phase, but in cells with polytene chromosomes, some sequences may replicate more than once or fail to replicate during S-phase. Because of this differential replication, the control of replication in polytene cells must have some unusual features. Dennhöfer (1982a) has recently concluded that the total DNA content of the polytene cells of Drosophila salivary glands exactly doubles in each S-phase. This observation, along with previous studies demonstrating satellite underreplication in salivary gland cells, led us to consider the hypothesis that there is a “doubling of DNA” mechanism for the control of DNA replication in polytene cells. With this mechanism, a doubling of DNA content, rather than the replication of each sequence, would signal the end of a cycle of DNA replication. To test this hypothesis, we have reinvestigated the replication of several sequences (satellite, ribosomal, histone and telomere) in salivary gland cells using quantitative in situ hybridization. We find that underreplication of some sequences does occur. In addition we have repeated Dennhöfer's cytophotometric and labeling studies. In contrast to Dennhöfer, we find that the total DNA contents of nonreplicating nuclei do reflect this partial replication, in accord with Rudkin's (1969) result. We conclude that DNA replication in polytene cells is controlled by modifications of the mechanism operating in dividing cells, where control is sequence autonomous, and not by a “doubling of DNA” mechanism. — In situ hybridization to unbroken salivary gland nuclei reveals the distribution of specific sequences. As expected, satellite, histone and 5S sequences are usually in a single cluster. This rules out the possibility that sequences known to be underreplicated in chromosomal DNA exist as extrachromosomal copies. Telomere sequences are grouped into two to six clusters, as if the chromosome ends are partially but not completely paired in salivary gland nuclei.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Agard DA, Sedat JW (1983) Three-dimensional architecture of a polytene nucleus. Nature 302:676–681
Appels R, Steffensen DM, Craig S (1979) A new method for mapping the three-dimensional distribution of DNA sequences in nuclei. Exp Cell Res 124:436–441
Artavanis-Tsakonas S, Schedl P, Tschudi C, Pirotta V, Steward R, Gehring WJ (1977) The 5S genes of Drosophila melanogaster. Cell 12:1057–1067
Bedi KS, Goldstein DJ (1976) Apparent anomalies in nuclear Feulgen-DNA contents. J Cell Biol 71:68–88
Berendes HD, Keyl H-G (1967) Distribution of DNA in heterochromatin and euchromatin of polytene nuclei of Drosophila hydei. Genetics 57:1–13
Crouse HV, Keyl H-G (1968) Extra replications in the “DNApuffs” of Sciara coprophila. Chromosoma 25:357–364
Dawid IB, Wellauer PK, Long EO (1978) Ribosomal DNA in Drosophila melanogaster. I. Isolation and characterization of cloned fragments. J Mol Biol 126:749–768
Dennhöfer L (1979) Cytophotometric measurements of DNA in salivary gland nuclei of Drosophila melanogaster. Plant Syst Evol Suppl 2:91–94
Dennhöfer L (1981) Complete replication of DNA in polytene nuclei of salivary glands of Drosophila melanogaster. Wilhelm Roux's Arch 190:237–240
Dennhöfer L (1982a) Cytophotometric DNA determinations and autoradiographic studies in salivary gland nuclei from larvae with different karyotypes in Drosophila melanogaster. Chromosoma 86:123–147
Dennhöfer L (1982b) Underreplication during polytenization? Recent Cytophotometric DNA determinations and related biochemical results concerning polytene salivary gland nuclei of Drosophila melanogaster. Theor Appl Genet 63:193–199
Dickson E, Boyd JB, Laird CD (1971) Sequence diversity of polytene chromosome DNA from Drosophila hydei. J Mol Biol 61:615–627
Gall JG, Cohen EH, Polan ML (1971) Repetitive DNA sequences in Drosophila. Chromosoma 33:319–344
Goldstein DJ (1970) Aspects of scanning microdensitometry. I. Stray light (glare). J Microsc 92:1–16
Goldstein DJ (1971) Aspects of scanning microdensitometry. II. Spot size, focus and resolution. J Microsc 93:15–42
Graves BJ, Schubiger G (1982) Cell cycle changes during growth and differentiation of imaginal leg discs in Drosophila melanogaster. Dev Biol 93:104–110
Hammond MP (1984) Chromosome structure and DNA replication in the giant nuclei of nurse and salivary gland cells of Drosophila melanogaster. Ph D thesis, University of Washington
Hammond MP, Laird CD (1985) Chromosome structure and DNA replication in nurse and follicle cells of Drosophila melanogaster. Chromosoma 91:267–278
Harland R (1981) Initiation of DNA replication in eukaryotic chromosomes. Trends Biochem Sci 6:71–74
Hartmann-Goldstein I, Goldstein DJ (1979) Effect of temperature on morphology and DNA-content of polytene chromosomes in Drosophila. Chromosoma 71:333–346
Heitz E (1934) Über α- und β-Heterochromatin sowie Konstanz und Bau der Chromomeren bei Drosophila. Biol Zentralbl 54:588–609
Henikoff S (1981) Position-effect variegation and chromosome structure of a heat shock puff in Drosophila. Chromosoma 83:381–393
Henikoff S, Meselson M (1977) Transcription at two heat shock loci in Drosophila. Cell 12:441–451
Hinton T (1945) A study of chromosome ends in salivary gland nuclei of Drosophila. Biol Bull 88:144–165
Jacobs-Lorena M (1980) Dosage of 5S and ribosomal genes during oogenesis of Drosophila melanogaster. Dev Biol 80:134–145
Laird CD (1980) Structural paradox of polytene chromosomes. Cell 22:869–874
Laird CD, Ashburner M, Wilkinson L (1980) Relationship between relative dry mass and average band width in regions of polytene chromosomes of Drosophila. Chromosoma 76:175–189
Lakhotia SC (1974) EM autoradiographic studies on polytene nuclei of Drosophila melanogaster. III. Localization of non-replicating chromatin in the chromocentre heterochromatin. Chromosoma 46:145–159
Lamb MJ (1982) The DNA content of polytene nuclei in midgut and M. talpighian tubule cells of adult Drosophila melanogaster. Wilhelm Roux's Arch Dev Biol 191:381–384
Lifschytz E (1983) Sequence replication and banding organisation in the polytene chromosomes of Drosophia melanogaster. J Mol Biol 164:17–34
Lifton RP, Goldberg ML, Karp RW, Hogness DS (1978) The organization of the histone genes in Drosophila melanogaster: functional and evolutionary implications. Cold Spring Harbor Symp Quant Biol 42:1047–1063
Mishra A, Lakhotia SC (1982) Replication in Drosophila chromosomes. VII. Influence of prolonged larval life on patterns of replication in polytene chromosomes of Drosophila melanogaster. Chromosoma 85:221–236
Mukherjee AS, Duttagupta AK, Chatterjee SN, Chatterjee RN, Majumdar D, Chatterjee C, Ghosh M, Achary PM, Dey A, Banerjee I (1980) Regulation of DNA replication in Drosophila. In: Siddiqi O, Babu P, Hall LM, Hall JC (eds) Development and neurobiology of Drosophila. Plenum, New York, pp 57–83
Mulder MP, van Duijn P, Gloor HJ (1968) The replicative organization of DNA in the polytene chromosomes of Drosophila hydei. Genetica 39:385–428
Newport J, Kirschner M (1982) A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell 30:687–696
Rasch EM (1970) DNA cytophotometry of salivary gland nuclei and other tissue systems in dipteran larvae. In: Wied GL, Bahr GF (eds) Introduction to quantitative cytochemistry vol. 2. Academic Press, New York London, pp 357–397
Rasch EM, King RC, Rasch RW (1984) Cytophotometric studies on cells from the ovaries of otu mutants of Drosophila melanogaster. Histochemistry 81:105–110
Renkawitz-Pohl R (1978) Number of the repetitive euchromatic 5S RNA genes in polyploid tissues of Drosophila hydei. Chromosoma 66:249–258
Rodman TC (1967) DNA replication in salivary gland nuclei of Drosophila melanogaster at successive larval and prepupal stages. Genetics 55:376–386
Rodman TC (1968) Relationship of developmental stage to initiation of replication in polytene nuclei. Chromosoma 23:271–287
Rubin GM (1978) Isolation of a telomeric DNA sequence from Drosophila melanogaster. Cold Spring Harbor Symp Quant Biol 42:1041–1046
Rudkin GT (1969) Non replicating DNA in Drosophila. Genetics 61:Suppl 1:227–238
Rudkin GT (1973) Cyclic synthesis of DNA in polytene chromosomes of Diptera. In: Balls M, Billet FS (eds) The cell cycle in development and differentiation. Cambridge University Press, London, pp 279–292
Spear BB, Gall JG (1973) Independent control of ribosomal gene replication in polytene chromosomes of Drosophila melanogaster. Proc Natl Acad Sci USA 70:1359–1363
Spradling AC, Mahowald AP (1981) A chromosome inversion alters the pattern of specific DNA replication in Drosophila follicle cells. Cell 27:203–209
Szabo P, Elder R, Steffensen DM, Uhlenbeck OC (1977) Quantitative in situ hybridization of ribosomal RNA species to polytene chromosomes of Drosophila melanogaster. J Mol Biol 115:539–563
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Hammond, M.P., Laird, C.D. Control of DNA replication and spatial distribution of defined DNA sequences in salivary gland cells of Drosophila melanogaster . Chromosoma 91, 279–286 (1985). https://doi.org/10.1007/BF00328223
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00328223