Chromosoma

, Volume 91, Issue 3–4, pp 279–286 | Cite as

Control of DNA replication and spatial distribution of defined DNA sequences in salivary gland cells of Drosophila melanogaster

  • Martin P. Hammond
  • Charles D. Laird
Article

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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Agard DA, Sedat JW (1983) Three-dimensional architecture of a polytene nucleus. Nature 302:676–681Google Scholar
  2. Appels R, Steffensen DM, Craig S (1979) A new method for mapping the three-dimensional distribution of DNA sequences in nuclei. Exp Cell Res 124:436–441Google Scholar
  3. Artavanis-Tsakonas S, Schedl P, Tschudi C, Pirotta V, Steward R, Gehring WJ (1977) The 5S genes of Drosophila melanogaster. Cell 12:1057–1067Google Scholar
  4. Bedi KS, Goldstein DJ (1976) Apparent anomalies in nuclear Feulgen-DNA contents. J Cell Biol 71:68–88Google Scholar
  5. Berendes HD, Keyl H-G (1967) Distribution of DNA in heterochromatin and euchromatin of polytene nuclei of Drosophila hydei. Genetics 57:1–13Google Scholar
  6. Crouse HV, Keyl H-G (1968) Extra replications in the “DNApuffs” of Sciara coprophila. Chromosoma 25:357–364Google Scholar
  7. Dawid IB, Wellauer PK, Long EO (1978) Ribosomal DNA in Drosophila melanogaster. I. Isolation and characterization of cloned fragments. J Mol Biol 126:749–768Google Scholar
  8. Dennhöfer L (1979) Cytophotometric measurements of DNA in salivary gland nuclei of Drosophila melanogaster. Plant Syst Evol Suppl 2:91–94Google Scholar
  9. Dennhöfer L (1981) Complete replication of DNA in polytene nuclei of salivary glands of Drosophila melanogaster. Wilhelm Roux's Arch 190:237–240Google Scholar
  10. Dennhöfer L (1982a) Cytophotometric DNA determinations and autoradiographic studies in salivary gland nuclei from larvae with different karyotypes in Drosophila melanogaster. Chromosoma 86:123–147Google Scholar
  11. 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 63:193–199Google Scholar
  12. Dickson E, Boyd JB, Laird CD (1971) Sequence diversity of polytene chromosome DNA from Drosophila hydei. J Mol Biol 61:615–627Google Scholar
  13. Gall JG, Cohen EH, Polan ML (1971) Repetitive DNA sequences in Drosophila. Chromosoma 33:319–344Google Scholar
  14. Goldstein DJ (1970) Aspects of scanning microdensitometry. I. Stray light (glare). J Microsc 92:1–16Google Scholar
  15. Goldstein DJ (1971) Aspects of scanning microdensitometry. II. Spot size, focus and resolution. J Microsc 93:15–42Google Scholar
  16. Graves BJ, Schubiger G (1982) Cell cycle changes during growth and differentiation of imaginal leg discs in Drosophila melanogaster. Dev Biol 93:104–110Google Scholar
  17. 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 WashingtonGoogle Scholar
  18. Hammond MP, Laird CD (1985) Chromosome structure and DNA replication in nurse and follicle cells of Drosophila melanogaster. Chromosoma 91:267–278Google Scholar
  19. Harland R (1981) Initiation of DNA replication in eukaryotic chromosomes. Trends Biochem Sci 6:71–74Google Scholar
  20. Hartmann-Goldstein I, Goldstein DJ (1979) Effect of temperature on morphology and DNA-content of polytene chromosomes in Drosophila. Chromosoma 71:333–346Google Scholar
  21. Heitz E (1934) Über α- und β-Heterochromatin sowie Konstanz und Bau der Chromomeren bei Drosophila. Biol Zentralbl 54:588–609Google Scholar
  22. Henikoff S (1981) Position-effect variegation and chromosome structure of a heat shock puff in Drosophila. Chromosoma 83:381–393Google Scholar
  23. Henikoff S, Meselson M (1977) Transcription at two heat shock loci in Drosophila. Cell 12:441–451Google Scholar
  24. Hinton T (1945) A study of chromosome ends in salivary gland nuclei of Drosophila. Biol Bull 88:144–165Google Scholar
  25. Jacobs-Lorena M (1980) Dosage of 5S and ribosomal genes during oogenesis of Drosophila melanogaster. Dev Biol 80:134–145Google Scholar
  26. Laird CD (1980) Structural paradox of polytene chromosomes. Cell 22:869–874Google Scholar
  27. Laird CD, Ashburner M, Wilkinson L (1980) Relationship between relative dry mass and average band width in regions of polytene chromosomes of Drosophila. Chromosoma 76:175–189Google Scholar
  28. Lakhotia SC (1974) EM autoradiographic studies on polytene nuclei of Drosophila melanogaster. III. Localization of non-replicating chromatin in the chromocentre heterochromatin. Chromosoma 46:145–159Google Scholar
  29. 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 191:381–384Google Scholar
  30. Lifschytz E (1983) Sequence replication and banding organisation in the polytene chromosomes of Drosophia melanogaster. J Mol Biol 164:17–34Google Scholar
  31. 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 42:1047–1063Google Scholar
  32. 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 85:221–236Google Scholar
  33. 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 57–83Google Scholar
  34. Mulder MP, van Duijn P, Gloor HJ (1968) The replicative organization of DNA in the polytene chromosomes of Drosophila hydei. Genetica 39:385–428Google Scholar
  35. Newport J, Kirschner M (1982) A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell 30:687–696Google Scholar
  36. 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 357–397Google Scholar
  37. Rasch EM, King RC, Rasch RW (1984) Cytophotometric studies on cells from the ovaries of otu mutants of Drosophila melanogaster. Histochemistry 81:105–110Google Scholar
  38. Renkawitz-Pohl R (1978) Number of the repetitive euchromatic 5S RNA genes in polyploid tissues of Drosophila hydei. Chromosoma 66:249–258Google Scholar
  39. Rodman TC (1967) DNA replication in salivary gland nuclei of Drosophila melanogaster at successive larval and prepupal stages. Genetics 55:376–386Google Scholar
  40. Rodman TC (1968) Relationship of developmental stage to initiation of replication in polytene nuclei. Chromosoma 23:271–287Google Scholar
  41. Rubin GM (1978) Isolation of a telomeric DNA sequence from Drosophila melanogaster. Cold Spring Harbor Symp Quant Biol 42:1041–1046Google Scholar
  42. Rudkin GT (1969) Non replicating DNA in Drosophila. Genetics 61:Suppl 1:227–238Google Scholar
  43. 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 279–292Google Scholar
  44. Spear BB, Gall JG (1973) Independent control of ribosomal gene replication in polytene chromosomes of Drosophila melanogaster. Proc Natl Acad Sci USA 70:1359–1363Google Scholar
  45. Spradling AC, Mahowald AP (1981) A chromosome inversion alters the pattern of specific DNA replication in Drosophila follicle cells. Cell 27:203–209Google Scholar
  46. 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 115:539–563Google Scholar

Copyright information

© Springer-Verlag 1985

Authors and Affiliations

  • Martin P. Hammond
    • 1
  • Charles D. Laird
    • 1
  1. 1.Department of Zoology, NJ-15University of WashingtonSeattleUSA

Personalised recommendations