Publications in 1990

C. Dohrmann, N. Azpiazu and M. Frasch (1990). A new Drosophila homeo box gene is expressed in mesodermal precursor cells of distinct muscles during embryogenesis. Genes Dev 4, 2098-111.

Several Drosophila homeo box genes have been shown to control cell fates in specific positions or cell groups of the embryo. Because the mechanisms involved in the pattern formation of complex internal organs, such as the musculature and the nervous system, are still largely unknown, we sought to identify and analyze new homeo box genes specifically expressed in these tissues. Here, the molecular analysis and expression pattern of one such gene, containing both a homeo box and a PRD repeat, is described. This gene, designated S59, is expressed in a small number of segmentally repeated mesodermal cells approximately 2 hr postgastrulation. Gradually, four groups of S59-expressing mesodermal cells appear in each abdominal hemisegment, each one giving rise to a particular somatic muscle after fusion with surrounding myoblasts. Thus, individual precursors for particular muscles, which we call founder cells, are specified relatively early during mesodermal development. The expression of a particular homeo box gene in these cells suggests that distinct programs of gene expression are active in subsets of mesodermal cells after germ band elongation, resulting in a specification of their developmental fates. In addition to the mesoderm, S59 is expressed in a subset of neuronal cells of the CNS and their precursors and also in cells of a small region of the midgut.

W. Driever, V. Siegel and C. Nüsslein-Volhard (1990). Autonomous determination of anterior structures in the early Drosophila embryo by the bicoid morphogen. Development 109, 811-20.

A small number of maternal effect genes determine anterior-posterior pattern in the Drosophila embryo. Embryos from females mutant for the maternal gene bicoid lack head and thorax. bcd mRNA becomes localized to the anterior tip of the egg during oogenesis and is the source for the morphogen gradient of bcd protein. Here we show that in vitro transcribed bicoid mRNA that has its own leader sequences substituted by the Xenopus beta-globin 5' untranslated sequences is translated more efficiently than bicoid mRNA with the natural 5' mRNA leader when tested in vitro and in Drosophila Schneider cells. When injected into bicoid mutant embryos, only the bcd mRNA with the beta-globin leader sequence, substituted for the natural leader, is able to induce anterior development. We used P-transformation to show that sequences in the 5' leader are neither necessary for localization of the transcript nor for the translational block of the bcd mRNA during oogenesis. For our injection experiments, we used only one of the identified splicing forms of bcd mRNA. The bcd protein species derived from this mRNA is able to induce anterior development at any position along the anterior-posterior axis. Thus bicoid protein can induce development of head and thorax independent of any other specifically localized morphogenetic factor. Our findings further support the notion that the concentration gradient of bcd protein, and not the existence of different forms of bcd protein, is responsible for specifying subregions of the embryo.

C. Nüsslein-Volhard (1990). Axis determination in the Drosophila embryo. Harvey Lect 86, 129-48.

H. Saumweber, M. Frasch and G. Korge (1990). Two puff-specific proteins bind within the 2.5 kb upstream region of the Drosophila melanogaster Sgs-4 gene. Chromosoma 99, 52-60.

The Drosophila nuclear proteins Bj6 and Bx42 characterized previously are detected in a series of developmentally active puffs on salivary gland chromosomes. Here the binding of both proteins at puff 3C11-12 containing the glue protein gene Sgs-4 is described in more detail. By deletion analysis we show that both proteins bind within a chromosomal segment containing 17-19 kb of DNA surrounding the Sgs-4 gene. They are detectable at this site during the intermoult stages, before the puff regresses in response to the moulting hormone ecdysone. If the Sgs-4 gene together with flanking DNA sequences is brought into a different chromosomal position by P element transfer, both proteins are detected at this new location. Both proteins are bound to the chromosome within the range of 2.5 kb DNA upstream of the Sgs-4 gene. A strain containing a 52 bp deletion within this region fails to bind Bx42 protein suggesting that the missing DNA, which overlaps a hypersensitive region, may be required for the binding of the Bx42 protein.

L. M. Stevens, H. G. Frohnhöfer, M. Klingler and C. Nüsslein-Volhard (1990). Localized requirement for torso-like expression in follicle cells for development of terminal anlagen of the Drosophila embryo. Nature 346, 660-3.

The torso (tor) gene, one of six identified maternal genes essential for the development of the anterior and posterior terminal structures in the Drosophila embryo, is likely to function as a transmembrane receptor tyrosine kinase. Although tor protein is uniformly distributed in the membrane of the egg cell and syncytial embryo, genetic and molecular data suggest that tor is locally activated at the ends of the embryo by a ligand present in the perivitelline space. Local activation of tor could be achieved if the ligand were expressed by a subpopulation of the follicle cells that surround the developing oocyte. Here we describe torso-like (tsl), the sixth member of the terminal gene class, and show that it is unique among these genes in that its expression is required in the somatic follicle cells rather than in the germ line. Moreover, mosaic analysis demonstrates that tsl expression is necessary only in subpopulations of follicle cells located at the poles of the oocyte. Thus, the spatially regulated expression of tsl in the follicle cell layer may generate a localized signal that is transduced by tor, ultimately resulting in the formation of the terminal structures of the embryo.