Summary
The Y chromosome of Drosophila hydei carries information that is necessary for the development of the spermatozoa. In primary spermatocytes Y chromosomal genes become active: five of the male fertility factors form giant lampbrush loops. Our prior work indicated interactions between the Y chromosomal genes and autosomal loci. It is of interest to identify loci regulating the activity of the Y chromosomal genes. We, therefore, screened a total of about 14,000 chromosomes (X, 2, 3 and 4) for mutations that interfere with the expression of the lampbrush loops. Two mutations with substantial effects on the loop morphology were recovered. One of them, a recessive male sterile mutation (ms (3) 5) on chromosome 3, is described in this paper. Its homozygous state results in a complete absence of all Y chromosomal lampbrush loops at 26° C; at 18° C the loops are formed. Temperature shifts with homozygous males indicate that the function early during the spermatogonial stage is crucial for the development of lampbrush loops in the primary spermatocyte. Meiosis is entirely absent in the male, but normal in females. Females homozygous for ms (3) 5 display a maternal effect, which reduces the viability and fertility of homozygous daughters and produces sons with signs of intersexuality. Linkage studies indicated that the effect on the male germ line and the maternal effects cannot be separated and may hence be induced by a single gene.
Similar content being viewed by others
References
Baker BS, Belote JM (1983) Sex determination and dosage compensation in Drosophila melanogaster. Ann Rev Genet 17:345–393
Belote JM, Lucchesi JC (1980) Control of X chromosome transcription by the maleless gene in Drosophila. Nature (Lond) 285:573–575
Berendes HD (1963) The salivary gland chromosomes of D. hydei Sturtevant. Chromosoma 14:195–206
Bridges CB (1916) Non-disjunction as proof of the chromosome theory of heredity. Genetics 1:1–52, 107–163
Cline TW (1976) A sex-specific temperature-sensitive maternal effect of the daughterless mutation of Drosophila melanogaster. Genetics 84:723–742
Cline TW (1983) The interaction between daughterless and sexlethal in triploids: a novel sex-transforming maternal effect linking sex determination and dosage compensation in Drosophila melanogaster. Dev Biol 95:260–274
Cline TW (1985) Primary events in the determination of sex in Drosophila melanogaster. In: Halvorson H, Monroy A (eds) The origin and evolution of sex. Alan R. Liss, New York, pp 301–327
Garcia-Bellido A (1975) Genetic control of wing disc development in Drosophila. In: Brenner S (ed) Cell patterning. Ciba Found Symposium 29:161–178
Gloor H (1971) New mutants. Drosoph Inf Serv 47:47–52
Grond CJ (1984) Spermatogenesis of Drosophila hydei. Ph.D. Thesis, University of Nijmegen, The Netherlands
Hackstein JHP, Leoncini O, Beck H, Peelen G, Hennig W (1982) Genetic fine structure of the Y chromosome of Drosophila hydei. Genetics 101:257–277
Hennig I (1982) “Hybrid” X-Y translocation chromosomes of Drosophila hydei and D. neohydei. Chromosoma 86:491–508
Hennig W (1967) Untersuchungen zur Struktur und Funktion des Lampenbürsten-Y-Chromosoms in der Spermatogenese von Drosophila. Chromosoma 22:294–357
Hennig W (1985) Y chromosome function and spermatogenesis in Drosophila hydei. Adv Genet 23:179–234
Hennig W, Hennig I, Leoncini O (1974) Some observations on spermatogenesis of Drosophila hydei. Drosoph Inf Serv 51:127
Hess O (1965a) The effect of X-rays on the functional structures of the Y chromosome in spermatocytes of Drosophila hydei. J Cell Biol 25:169–173
Hess O (1965b) Struktur-Differenzierungen im Y Chromosom von Drosophila hydei und ihre Beziehungen zu Gen-Aktivitälen. III. Sequenz und Lokalisation der Schleifenbildungsorte. Chromosoma 16:222–248
Hess O (1967) Complementation of genetic activity in translocated fragments of the Y chromosome in Drosophila hydei. Genetics 56:283–295
Leoncini O (1977) Temperatursensitive Mutanten im Y Chromosom von Drosophila hydei. Chromosoma 63:329–357
Lewis EB (1978) A gene complex controlling segmentation in Drosophila. Nature (Lond) 276:265–570
Lifschytz E (1974) Genes controlling chromosome activity. An X- linked mutation affecting Y-lampbrush loop activity in Drosophila hydei. Chromosoma 47:415–427
Lifschytz E (1975) Genes controlling chromosome activity. The role of genes blocking Y-lampbrush loop propagation. Chromosoma 53:231–241
Lifschytz E, Hareven D, Azriel A, Brodsley H (1983) DNA clones and RNA transcripts of four lampbrush loops from the Y chromosome of Drosophila hydei. Cell 32:191–199
Marsh JL, Wieshaus E (1978) Is sex determination in germ line and soma controlled by separate genetic mechanisms? Nature (Lond) 272:249–251
Meyer GF (1963) Die Funktionsstrukturen des Y-Chromosoms in den Spermatocytenkernen von Drosophila hydei, D. neohydei, D. repleta und einigen anderen Drosophila-Arten. Chromosoma 14:207–255
Meyer GF, Hess O (1965) Strukturdifferenzierungen im Y-Chromosom von Drosophila hydei und ihre Beziehungen zu GenAktivitäten. II. Effect der RNS-Synthese-Hemmung durch Actinomycin. Chromosoma 16:249–270
Nöthiger R, Steinmann-Zwicky M (1985) Sex determination in Drosophila. Trends Genet 1: 209–215
Schüpbach T (1982) Autosomal mutations that interfere with sex determination in somatic cells of Drosophila have no direct effect on the germ line. Dev Biol 89:117–127
Schüpbach T (1985) A proper X-chromosome-autosome ratio and expression of the sex-lethal locus are necessary for normal differentiation of female germ cells in Drosophila melanogaster. Genetics 109:529–548
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Hackstein, J., Hennig, W. & Steinmann-Zwicky, M. Autosomal control of lampbrush-loop formation during spermatogenesis in Drosophila hydei by a gene also affecting somatic sex determination. Roux's Arch Dev Biol 196, 119–123 (1987). https://doi.org/10.1007/BF00402033
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00402033