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Development of Drosophila Larval Sensory Organs: Spatiotemporal Pattern of Sensory Neurones, Peripheral Axonal Pathways and Sensilla Differentiation

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Development of Drosophila Larval Sensory Organs: Spatiotemporal Pattern of Sensory Neurones, Peripheral Axonal Pathways and Sensilla Differentiation Development 102, 869-886 (1988) 869 Printed in Great Britain © The Company of Biologists Limited 1988 Development of Drosophila larval sensory organs: spatiotemporal pattern of sensory neurones, peripheral axonal pathways and sensilla differentiation VOLKER HARTENSTEIN* Institut fuer Entwicklungsphysiologie der Umversilaet zu Koeln, Gyrhofstr. 17, 5000 Koeln 41, FRC * Present address: Department of Biology, University of California, San Diego La Jolla, California 92093, USA Summary The sensilla of Drosophila larval thoracic and abdomi- of the sensillum cells resembles the development of nal segments appear in a constant temporal sequence larval epidermal cells in many aspects. Thus, the during stage 13/14 (9-5-11-5 h) of embryonic develop- sheath processes formed by sensillum accessory cells ment. Those sensilla innervated by more than one and the axons formed by sensory neurones develop dendrite (basiconical sensilla, chordotonal organs, from processes transiently formed by all cells. During some of the trichoid sensilla and campaniform sensilla) the phase of cuticle secretion, apical portions of the appear earlier than sensilla innervated by a single presumptive accessory cells are modified to form the dendrite (majority of trichoid sensilla and campani- cuticular apparatus responsible for receiving the sen- form sensilla). Furthermore, a dorsoventrally directed sory stimuli. Finally, two sets of subepidermally gradient underlies the sequence in which sensilla of a located cells which differ with respect to their mor- given type appear. Sensory axons are emitted in the phology and, probably, their origin envelop somata same sequence. Thus, axons of the polyinnervated and axons of the sensory neurones. sensilla appear first. Together with a distinct set of efferent axons they form 'pioneer tracts' of the two Key words: sensory organs, Drosophila, morphogenesis, fascicles of the segmental nerves. Cytodifferentiation axonogenesis. Introduction of sensillum this neurone belongs to (Ghysen, 1980; Ghysen et al. 1983). Sensillum quality, on the other Insect sensilla described as 'Kleinorgane' (Henke, hand, seems to be determined by factors such as the 1953) or organules (Lawrence, 1966) are composed of small sets of highly specialized cells, each with pre- time during development when the sensilla are gener- cisely defined morphological and functional charac- ated, their position within a segment and the identity teristics. Sensilla possess one or more bipolar of this segment (Murphey et al. 1980; Shankland & neurones and a set of accessory cells which forms Bentley, 1983; Dambly-Chaudiere & Ghysen, 1986). sheaths around the neurone(s) and produce the Thus, developmental mechanisms controlling the pat- stimulus-receiving cuticular apparatus. The pattern of terning, differentiation and axonal projection of the distribution, architecture and axonal projection of sensilla seem to be closely interrelated. Further sensilla is highly invariant among different individuals analyses directed at unravelling the control of sensil- of one species. Therefore, sensilla are a favourable lum development require a detailed knowledge of the system to analyse the determinants of cell patterning, temporal and spatial frame in which these different cell differentiation and axonal projection during phenotypic traits of the sensilla unfold. neural development. Experimental studies have Since the application of genetic and molecular shown that one of the determinants of the axonal methods is well advanced in Drosophila melanogas- projection pattern of a sensory neurone is the quality ter, this animal represents one of the favourite objects 870 V. Hartenstein to study developmental mechanisms. Though its propylene oxide and then for 5-10 h in unpolymerized anatomy and general development is known in con- Epon. They were oriented sagittally or horizontally and siderable detail (Hertweck, 1931; Poulson, 1950; placed at 60°C for 12 h to permit polymerization of the Bownes, 1975; Kankel et al. 1980; Campos-Ortega & Epon. Blocks were sectioned with a LKB Ultrotome III. Hartenstein, 1985; Dambly-Chaudiere & Ghysen, For reconstruction of sense organs, the lateral body wall of 12 saggitally oriented specimens of different stages was 1986), our knowledge of the pattern in which the sectioned in almost complete series of ultrathin sections sensory organs are assembled and the morphogenetic (5-10 nm). For the analysis of developing peripheral events shaping their development is scarce. In the nerves, ultrathin sections were cut at intervals of 5 ^m from present study, labelling of peripheral neurones in five horizontally oriented specimens. Sections were whole-mount preparations of embryos and recon- mounted on formvar-coated slot grids and treated with structing the architecture of thoracic and abdominal uranyl acetate and lead citrate (Reynolds, 1963). Sections sensilla at sequential embryonic stages (from serial were inspected and photographed with a Siemens Elmiskop EM sections) were combined to investigate sensilla 101. For reconstruction of sensilla, photographs of sections development in the larva of Drosophila melanogaster. of representative sensilla (lateral basiconical sensillum of Special attention was attributed to (i) the time se- thoracic segments; lateral pentascolopidial chordotonal quence in which sensory neurones appear and their organ, lateral trichoid sensilla and lateral campaniform axons grow out, (ii) the projection pattern of a subset sensillum of abdominal segments) at approximately 1 fim intervals were taken. From the prints, contours and ultra- of early appearing axons which form 'pioneer tracts' structural details of sensilla cells were drawn on translucent for the peripheral nerves and (iii) the movements and plastic sheets. By superimposing the drawings of sequential differentiative events performed by the developing sections three-dimensional reconstructions of the sensilla sensillum cells. were obtained. Materials and methods Results A series of staged embryos of wild-type Drosophila melano- gaster (Oregon R) was stained with antibody against Time sequence of development of the thoracic and horseradish peroxidase (HRP) and the mouse monoclonal abdominal sensilla antibody 22C10. Both antibodies show an affinity for the membranes of immature neural cells (Jan & Jan, 1982; The distribution and external morphology of the Canal & Ferrus, 1986). A second series of staged embryos various types of Drosophila larval sensory organs has was processed for transmission electron microscopy. been investigated in a number of studies (Hertweck, For precise staging, freshly laid eggs were dechorionated, 1931; Kankel et al. 1980; Singh & Singh, 1984; mounted on Scotch tape, covered with halofiuorocarbon oil Campos-Ortega & Hartenstein, 1985; Dambly-Chau- (Voltalef 3S) and left at 25°C. For each specimen, the time diere & Ghysen, 1986). In the thoracic and abdominal when the germ band had retracted to 50 % egg length was segments, four classes of sensory organs are present: recorded. This stage, which is easily identified in the living hairs (sensilla trichoidea), papillae (sensilla campani- embryo, lasts for less than lOmin; it was taken as time Oa.r. formia), 'Koelbchen' (Hertweck, 1931; classified as (after 50 % retraction). Time 0 a.r., at 25°C, corresponds to sunken sensilla basiconica in Campos-Ortega & Har- 8h40min-8h50min after egg fertilization. Embryos were fixed and devitellinized according to the methods of tenstein, 1985) and chordotonal organs. These sen- Zalokar & Erk (1977) and Mitchison & Sedat (1983) at the silla are assembled into distinct patterns different for desired intervals (0—4ha.r. at increments of 20 min; 5ha.r.; the prothoracic, meso- and metathoracic, first 6ha.r.; first instar larva). through seventh abdominal, and terminal abdominal Antibody staining followed the protocol described in a segments (Campos-Ortega & Hartenstein, 1985; previous publication (Hartenstein & Campos-Ortega, Dambly-Chaudiere & Ghysen, 1986; see Fig. 1A). 1986). For electron microscopy, 25 % glutaraldehyde mixed Presumptive sensory neurones first develop an with heptane was used as a fixative. After devitellinization, antigenity towards the antibodies anti-HRP and embryos were washed in 015M-cacodylate buffer (pH6-9) 22C10 at the beginning of dendrite formation (Figs and postfixed for 30 min in a 1:1 mixture of 2-5 % glutaral- IB, 2). Shortly thereafter, axons grow out of the dehyde and 2% osmium tetroxide, then for 2 h in 2% somata opposite the dendrites and contact one of the osmium tetroxide in 015M-cacodylate buffer. Larvae had to be cut into halves in order to allow sufficient fixation. tracts pioneering the peripheral nerves. Within each Specimens were washed several times in distilled water and segment, a dorsoventral and a rostrocaudal temporal dehydrated in graded ethanol and propylene oxide (ethanol gradient characterizes the sequence in which sensilla 70%, 90%, 95%, 5min each; 100% 15min; propylene of equal morphological type appear. Homologous oxide (15 min). Postfixation, washing and dehydration was sensory neurones of different segments, on the other carried out in ice to prevent precipitation of osmium. hand, appear at the same time (Fig. 2). Sensilla Embryos were left overnight in a 1:1 mixture of Epon and appear in two waves: chordotonal organs, basiconical Development of Drosophila larval sensory organs 871 MDMX LB 11 -I AI-7 AS-10 Fig. 1. Distribution and development of the Drosophila larval sensilla. (A) Schematic depiction
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