Skip to main content
Log in

Salivary gland function and chromosomal puffing patterns in Drosophila hydei

  • Published:
Chromosoma Aims and scope Submit manuscript

Summary

The salivary glands of D. hydei larvae show differences between the cells in the distal (posterior) part and those of the proximal (anterior) part during the third instar. The first sign of these differences is an increase in cellular and nuclear volume in the distal cells of the gland, beginning at 103 hours after oviposition. After 125 hours the cytoplasm of the extreme distal cells acquires a reticulated structure, and at 130 hours these cells contain large granules or droplets of mucoprotein. From this moment up to puparium formation the number of cells containing these granules increases and the boundary of this type of cells shows a shift in the proximal direction. Just before puparium formation the granules disappear from the cells and a glue substance is secreted by the larvae. At this moment only a few cells in the extreme proximal part still lack granules. Electron-microscopical observations indicate that these cells were active in secretion, whereas all cells containing large granules are inactive in this respect during most of the third instar.

During the early third instar a change in cell function occurs, i.e. from synthesis of substances presumed to be digestive enzymes which are secreted, to a synthesis of a glue substance which is stored. This change begins in the extreme distal cells of the gland.

Investigation of the chromosomal puffing pattern revealed that a total number of 148 puffs were present during some period of the third instar, prepupal, and early pupal stages. The activity of 110 puffs was evaluated during a series of successive time intervals. Changes in the puffing pattern during puparium formation were compared with those observed during pupation.

Proximal and distal nuclei differ in the activity level of a number of puffs, but only puff 47 B is restricted in activity to the distal cells. This puff becomes active at 119 hours and disappears 4 hours before puparium formation (156 hours). Determination of nuclear diameter and DNA in nuclei of both parts of the gland revealed a correlation between a particular DNA content and the function of the cell. Distal cells show higher nuclear diameters than proximal cells after the onset of granule production. The first differences in nuclear diameter can be seen at 103 hours. Cells in the transitional part of the gland, located between distal granulecontaining and proximal granule-negative cells, always show the same DNA content. These cells are found at different locations within the gland during the third instar. This zone of cells shows a shift in proximal direction during the third instar, identical to that of the neighbouring granule-containing cells.

The possible interrelation between nuclear DNA content, the activity of puff 47 B, and the production of the glue substance were discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Allfrey, V. G., and A. E. Mirsky: Evidence for the complete DNA-dependence of RNA synthesis in isolated thymus nuclei. Proc. nat. Acad. Sci. (Wash.) 48, 1590–1596 (1962); - Mechanisms of synthesis and control of protein and ribonueleic acid synthesis in the cell nucleus. Cold Spr. Harb. Symp. quant. Biol. 28, 247–262 (1963).

    Google Scholar 

  • Bakker, K.: Feeding period, growth, and pupation in larvae of Drosophila melanogaster. Entomol. exp. et appl. 2, 171–186 (1959).

    Google Scholar 

  • Bargmann, W., and A. Knoop: Über die Morphologie der Milchsecretion. Licht- und Elektronenmikroskopische Studien an der Milchdräuse der Ratte. Z. Zell- forsch. 49, 344–388 (1959).

    Google Scholar 

  • Baudisch, W.: Aminosäurezusammensetzung der Speicheldräusen von Acricotopus lucidus. Biol. Zbl. 82, 351–361 (1963).

    Google Scholar 

  • Becker, H. J.: Die Puffs der Speicheldrüsenchromosomen von Drosophila melanogaster. I. Mitt.: Beobachtungen zum Verhalten des Puffmusters im Normalstamm und bei zwei Mutanten, giant und lethal-giant-larvae. Chromosoma(Berl.) 10, 645–678 (1959); - II. Mitt.: Die Auslösung der Puffbildung, ihre Spezifität und ihre Beziehung zur Funktion der Ringdrüse. Chromosoma (Berl.) 13, 341–384 (1962a) ; - Stadienspezifische Genaktivierungen in Speicheldrüsen nach Transplantation bei Drosophila melanogaster. Zool. Anz., Suppl. 25, 92–101 (1962b).

    Google Scholar 

  • Beermann, W.: Chromomerenkonstanz und spezifische Modifikationen der Chromosomenstruktur in der Entwicklung und Organdifferenzierung von Chironomus tentans. Chromosoma (Berl.) 5, 139–198 (1952); - Ein Balbianiring als Locus einer Speicheldräusenmutation. Chromosoma (Berl.) 12, 1–25 (1961); - Genaktivität und Genaktivierung in Riesenchromosomen. Zool. Anz., Suppl. 25, 44–75 (1962); - Structure and function of interphase chromosomes. Genetics Today, Proc. XIth Int. Congr. Genet, The Hague 2, 373–384 (1965).

    Google Scholar 

  • —, and G. F. Bahr: The submicroscopic structure of the Balbianiring. Exp. Cell Res. 6, 195–201 (1954).

    Google Scholar 

  • Berendes, H. D.: The salivary gland chromosomes of Drosophila hydei Sturtevant. Chromosoma (Berl.) 14, 195–206 (1963).

    Google Scholar 

  • —, F. M. A. van Breugel, and Th. K. H. Holt: Experimental puffs in Drosophila hydei salivary gland chromosomes. Chromosoma (Berl.) 16, 35–47 (1965).

    Google Scholar 

  • —, and W. C. de Bruyn: Submicroscopic structure of Drosophila hydei salivary gland cells. Z. Zellforsch. 59, 142–152 (1963).

    Google Scholar 

  • Bergeron, J. A.: Controlled staining of autoradiographs. Stain Technol. 33, 221–223 (1958).

    Google Scholar 

  • Chen, P. S., N. Farnella-Feruzza, and M. Oelhafen-Gandolla: Contents of DNA and RNA in the salivary glands of normal and lethal larvae of the mutant “lethal-meander” of Drosophila melanogaster. Exp. Cell Res. 31, 538–548 (1963).

    Google Scholar 

  • Clever, U.: Genaktivitäten in den Riesenchromosomen von Chironomus tentans. I. Mitt.: Genaktivierung durch Ecdyson. Chromosoma (Berl.) 12, 607–675 (1961); - II. Mitt.: Das Verhalten der Puffs während des letzten Larven-stadiums und der Puppenhäutung. Chromosoma (Berl.) 13, 385–436 (1962a); - IV. Mitt.: Das Verhalten der Puffs in der Larvenhäutung. Chromosoma (Berl.) 14, 651–675 (1963a); - Von der Ecdysonkonzentration abhängige Genaktivitätsmuster in den Speicheldrüausenchromosomen von Chironomus tentans. Develop. Biol. 6, 73–98 (1963b); - Genaktivitäten und ihre Kontrolle in der tierischen Entwicklung. Naturwissenschaften 19, 449–459 (1964a); - Actinomycin and puromycin: Effects on sequential gene activiation by ecdysone. Science 146, 794–795 (1964b).

    Google Scholar 

  • Clever, U., and P. Karlson: Induktion von Puffänderungen in den Speichel-drüsen von Chironomus tentans durch Ecdyson. Exp. Cell Res. 20, 623–627 (1960).

    Google Scholar 

  • Duyn, P. Van: Acrolein-Schiff, a new staining method for proteins. J. Histochem. Cytochem. 10, 234–241 (1961).

    Google Scholar 

  • E. M. Den Tonkelaar, and M. J. Hardonk: An improved apparatus for quantitative cytochemical model studies and its use in an experimental test of the two-wavelength method. J. Histochem. Cytochem. 10, 437–480 (1962).

    Google Scholar 

  • Edström, J.-E., and W. Beermann: The base composition of nucleic acids in chromosomes, puffs, nucleoli, and cytoplasm of Chironomus salivary glands. J. Cell Biol. 14, 371–379 (1962).

    Google Scholar 

  • Essner, E., and A. B. Novikoff: Cytological studies on two functional hepatomas. Interrelations of endoplasmatic reticulum, Golgi apparatus and lysosomes. J. Cell. Biol. 15, 289–312 (1962).

    Google Scholar 

  • Fraenkel, G.: A function of the salivary glands of the larvae of Drosophila and other flies. Biol. Bull. 103, 285–286 (1952).

    Google Scholar 

  • — and V. J. Brookes: The process by which the puparia of many species of flies become fixed to a substrate. Biol. Bull. 105, 442–449 (1953).

    Google Scholar 

  • Gay, H.: Nucleo-cytoplasmic relations in Drosophila. Cold Spr. Harb. Symp. quant. Biol. 21, 257–270 (1956).

    Google Scholar 

  • Huskins, C. L., and L. M. Steinitz: The nucleus in differentiation and development. I. Heterochromatic bodies in energic nuclei of Rhoeo roots. J. Hered. 39, 35–43 (1948).

    Google Scholar 

  • Kaufmann, B. P., and H. Gay: The nuclear membrane as an intermediary in gene-controlled reactions. Nucleus 1, 57–74 (1958).

    Google Scholar 

  • Keyl, H.-G.: Erhöhung der chromosomalen Replikationsrate durch Mikro-sporidieninfektion in Speicheldrüsenzellen von Chironomus. Naturwissenschaften 47, 212–213 (1960).

    Google Scholar 

  • Kodani, M.: The protein of the salivary gland secretion in Drosophila. Proc. nat. Acad. Sci. (Wash.) 34, 131–135 (1948).

    Google Scholar 

  • Koltzoff, N. K.: The structure of the chromosomes in the salivary glands of Drosophila. Science 80, 312–313 (1934).

    Google Scholar 

  • Kroeger, H.: Experiments on the extranuclear control of gene activity in Dipteran polytene chromosomes. J. cell. comp. Physiol. 62, Suppl. 1, 45–59 (1963); - Zellphysiologische Mechanismen bei der Regulation von Genaktivitäten in den Riesenchromosomen. Chromosoma (Berl.) 15, 36–70 (1964).

    Google Scholar 

  • Läufer, H.: Hormones and the development of insects. Proc. 16th Int. Congr. Zool. Wash. 4, 215–220 (1963).

    Google Scholar 

  • Lesher, S.: Studies on the larval salivary gland of Drosophila. Anat. Rec. 114, 633–652 (1952).

    Google Scholar 

  • Leuchtenberger, C., and F. Schrader: Variation in the amounts of desoxyribonucleic acid (DNA) in cells of the same tissue and its correlation with secretory function. Proc. nat. Acad. Sci. (Wash.) 38, 99–105 (1952).

    Google Scholar 

  • Lewis, E. B.: In: W. Beermann, Nuclear differentiation and functional morphology of chromosomes. Cold Spr. Harb. Symp. quant. Biol. 21, 217–232 (1956).

  • Luft, J. H.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961).

    Google Scholar 

  • Matuszewski, B.: Polyploidy and polyteny induced by a Hymenopteran parasite in Dasyneura urticae (Diptera, Cecidomyiidae). Chromosoma (Berl.) 15, 31–35 (1964).

    Google Scholar 

  • McMaster-Kaye, R.: The metabolism of nuclear ribonucleic acid in salivary glands of Drosophila repleta. J. Histochem. Cytoehem. 10, 154–161 (1962).

    Google Scholar 

  • Mechelke, F.: The timetable of physiological activity of several loci in the salivary gland chromosomes of Acricotopus lucidus. Proc. Xth Int. Congr. Genet. 2, 158 (1958); - Beziehungen zwischen der Menge der DNS und dem Ausmaß der potentiellen Oberflächenentfaltung von Riesenchromosomen. Naturwissenschaften 46, 609 (1959); - Das Wandern des Aktivitätsmaximums im BR4-Locus von Acricotopus lucidus als Modell für die Wirkungsweise eines komplexen Locus. Naturwissenschaften 48, 29 (1961);- Spezielle Funktionszustände des genetischen Materials, in: Funktionelle und morphologische Organization der Zelle (Ed. P. Karlson), p. 15–29. Berlin-Göttingen-Heidelberg: Springer 1963.

    Google Scholar 

  • Meyer, K.: Mucoids and glycoproteins. Advanc. Protein Chem. 2, 249–275 (1945).

    Google Scholar 

  • Panitz, R.: Innersekretorische Wirkung auf Strukturmodifikationen der Speicheldrüsenchromosomen von Acricotopus lucidus (Chironomide). Naturwissenschaften 47, 838 (1960); - Hormonkontrollierte Genaktivitäten in den Riesenchromosomen von Acricotopus lucidus. Biol. Zbl. 83, 197–230 (1964).

    Google Scholar 

  • Pears, A. G. E.: Histochemistry. Theoretical and applied. London: J. & A. Churchill 1961.

    Google Scholar 

  • Pelling, C.: Chromosomal synthesis of ribonucleic acid as shown by incorporation of uridine labelled with tritium. Nature (Lond.) 184, 655–656 (1959); - Ribonukleinsäure-Synthese der Riesenchromosomen. Autoradiografische Untersuchungen an Chironomus tentans. Chromosoma (Berl.) 15, 71–122 (1964).

    Google Scholar 

  • Perkowska, E.: Some characteristics of the salivary gland secretion of Drosophila virilis. Exp. Cell Res. 32, 259–271 (1963).

    Google Scholar 

  • Persijn, J. P., and P. van Duyn: Studies on the Feulgen reaction with the aid of DNA incorporated cellulose films. Histochemie 2, 283–297 (1961).

    Google Scholar 

  • Risler, H.: Polyploidie und somatische Reduktion in der Larvenepidermis von Aedes aegypti L. (Culicidae). Chromosoma (Berl.) 10, 184–209 (1959).

    Google Scholar 

  • Ritossa, F.: Experimental activation of specific loci in polytene chromosomes of Drosophila. Exp. Cell Res. 35, 601–607 (1964).

    Google Scholar 

  • Ross, E. B.: The post-embryonic development of the salivary glands of Drosophila melanogaster. J. Morph. 65, 471–496 (1939).

    Google Scholar 

  • Sirlin, J. L.: Cell sites of RNA and protein synthesis in the salivary glands of Smittia (Chironomidae). Exp. Cell Res. 19, 177–181 (1960).

    Google Scholar 

  • Slyzinsky, B. M.: Functional changes in the polytene chromosomes of Drosophila melanogaster. Genetics Today, Proc. XIth Int. Congr. Genet. The Hague 1, 108 (1963).

    Google Scholar 

  • Swift, H.: The constancy of desoxyribose nucleic acid in plant nuclei. Proc. nat. Acad. Sci. (Wash.) 36, 634–654 (1950).

    Google Scholar 

  • Vogt, M.: Die Puparisierung als Ringdrüsenwirkung. Biol. Zbl. 62, 149–154 (1942a); - Induktion von Metamorphoseprozessen durch implantierte Ringdrüsen bei Drosophila. Wilhelm Roux' Arch. Entwickl.-Mech. Org. 142, 131–182 (1942b); - Zur Produktion und Bedeutung metamorphosefördernder Hormone während der Larvenentwicklung von Drosophila. Biol. Zbl. 63, 395–446 (1943).

    Google Scholar 

  • Vogt-Köhne, L., and L. Carlson: Cytochemische Untersuchungen an Balbianiringen des 4 Speicheldrüsenchromosoms von Chironomus tentans. Chromosoma (Berl.) 14, 186–194 (1963).

    Google Scholar 

  • Walker, B. E.: Polyploidy and differentiation in the transitional epithelium of mouse urinary bladder. Chromosoma (Berl.) 9, 105–110 (1958).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Berendes, H.D. Salivary gland function and chromosomal puffing patterns in Drosophila hydei. Chromosoma 17, 35–77 (1965). https://doi.org/10.1007/BF00285155

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00285155

Keywords

Navigation