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First published online 26 November 2003
doi: 10.1242/dev.00879

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Integration of complex larval chemosensory organs into the adult nervous system of Drosophila

¹ Department of Biology and Program in Neuroscience, University of Fribourg, CH-1700 Fribourg, Switzerland
² Institute of Genetics, University of Mainz, D-55099 Mainz, Germany

View larger version (26K): [in a new window]   Fig. 5. Fate of pharyngeal sensory neurons through metamorphosis. Persisting neurons are shown in color, neurons undergoing apoptosis in black, and newly born neurons with a dot. Individual sensilla are shown as arrowhead symbols. (A) Third larval instar: the dorsal pharyngeal sense organ (dps) consists of two groups of neurons, a and p1. Precise numbers of sensilla in the dps, dpo (dorsal pharyngeal organ) and vps (ventral pharyngeal sense organ) are unclear. lbn, labial nerve; lrn, labral nerve; pps, posterior pharyngeal sense organ. (B) Adult: the dorsal cibarial sense organ (dcso) corresponds to the conserved pps. The labral sense organ (lso) and the ventral cibarial sense organ (vcso) derive essentially from the dps. However, the vcso also includes two neurons of the dpo. Seven small sensilla of the lso as well as the fishtrap bristles (ftb; numbers in the diagram reduced) are born during metamorphosis. Remaining neurons of the dps and dpo are located along the accessory pharyngeal nerve (apn). pn, pharyngeal nerve.

View larger version (79K): [in a new window]   Fig. 1. Pharyngeal sense organs in third instar larvae (A,B,G-J) and adults (C-F,K-N) of D. melanogaster, as shown by the P[GAL4] driver line MJ94, expressed in all pharyngeal neurons (all panels except H,L) and the prosV1 line, which labels subsets of accessory cells (H,L). Expression patterns are shown by the reporters lacZ (A-F: blue) or mCD8-GFP (G-N: green). Neuronal nuclei in G-N are labeled with anti-Elav antibody (red). (A) The larval pharynx is equipped with a dorsal and a ventral pharyngeal sense organ located behind the mouth-hooks (dps, vps), and a smaller sense organ far more posterior (pps), in a region characterized by cuticular ridges (ri). Additional expression is seen in Bolwig's organ (bo), in the presumed dorsal pharyngeal organ (dpo) and in the dorsal and terminal organs (do, to). (B) The pps is composed of an anterior and a posterior sensillum (a, p). (C) The adult pharynx comprises the dorsal and ventral cibarial sense organs (dcso, vcso) and the labral sense organ (lso). MJ94 drives expression also in maxillary palp sensilla (ms) and in labial palp taste bristles (tb). Higher magnifications reveal an anterior and a posterior sensillum in the dcso (D: a, p), three sensilla in the vcso (E: 1-3) and nine sensilla in the lso (F: 1-9; opposite lso shown on top). Label occurs also in the neurons of the fishtrap bristles (E: ftb). Both the larval pps (G,H) and the adult dcso (K,L) are composed of two sensilla (G,K: arrows) of three neurons each. In both sense organs, prosV1 labels two accessory cells (H,L: arrowheads). The larval dps (I) and vps (J) contain 17-18 and 16 neurons, respectively. The dps is accompanied further back by the dorsal pharyngeal organ (I: dpo). (M) In the adult, the vcso includes three sensilla (1-3) comprising eight neurons (between arrowheads). The vcso is accompanied by two rows of mononeuronal fishtrap bristles (ftb) and by a few extra neurons (arrows). (N) The nine sensilla of the lso contain a total of 18 neurons. (A,B,F,G) Lateral view, distal to the left. (C-E,H-N) Frontal view, distal to the bottom. Scale bars, 100 µm (A,C), 50 µm (N), 40 µm (D-F), 20 µm (B,G-M)

View larger version (88K): [in a new window]   Fig. 2. Embryonic origin of subsets of neurons and nonneuronal cells in the pharyngeal sense organs, as shown by HRP injection at the syncytial blastoderm stage (A D) and by FLPout (Wong et al., 2002) induced in F1 embryos of the cross MJ94 x y w hs-flp; Sp/CyO; UAS>CD2 y+>mCD8-GFP (E-L). (E-L) Neuronal nuclei are labeled with anti-Elav antibody (red). (A-C') HRP product is present in dendritic tips of the lso sensillum 7 (A: arrow) and of the vcso (B: arrow), as well as in dendrites, cell bodies and axons of dcso neurons (consecutive sections C,C': arrows). (D) Fishtrap bristles labeled by MJ94/UAS-lacZ (arrows) lack HRP staining, in contrast to the vcso (arrowhead). (E-I) When FLPouts are induced in the MJ94 line at 12-24 hours after egg laying (AEL), single neurons are labeled in the lso, in both sensillum 7 (composed of eight neurons) (E-G: 7) and the mononeuronal sensilla 1-6 (G: 3). By contrast, the bineuronal sensilla 8 and 9 always exhibit paired labeled neurons (H,I: arrows). Simultaneous labeling of two sensilla suggests the occurrence of two independent FLPout events (F,G). (J) FLPouts induced earlier (6-18 hours AEL) lead to simultaneous label in many neurons (e.g. three in sensillum 7). (K,L) FLPout induced at 12-24 hours AEL invariably leads to single labeled neurons in the multineuronal sensilla of the vcso (K) and dcso (L). The two large neurons in K (arrows) are outside the vcso. ftb, fishtrap bristles. Distal is to the bottom except in (A) in which distal is to the left. F shows both left and right lso. Scale bars, 20 µm (A shows scale for A-D; E shows scale for E-L).

View larger version (85K): [in a new window]   Fig. 3. Early pupal origin of subsets of neuronal and non-neuronal cells in the adult pharyngeal sense organs, as shown by BrdU incorporation at 3 hours APF in MJ94 (G: 18 hours APF). The patterns were visualized by lacZ expression (blue) in the light microscope (A,B,F,G) or by mCD8-GFP expression (green) in the confocal microscope (C-E,H,I). The anti-BrdU product is shown in brown (A,B,F,G) or red (C-E,H,I). (A-E) In the lso, BrdU label is particularly obvious in the neurons of the distal sensilla 8 and 9. Additional BrdU take-up is visible in the neuron of the mononeuronal sensillum 6 (D) and in subsets of accessory cells (C-E: arrows). (F-I) In both vcso (F,H) and dcso (G,I), two accessory cells (arrowheads) but none of the neurons (large arrows) are BrdU positive. However, BrdU label is present in the neurons of the fishtrap bristles (H: small arrows). Asterisks in G,H indicate BrdU uptake in cells of the pharyngeal wall. (A,C,D,E) Sagittal sections; all others panels represent frontal views. Dots indicate midline. Distal is to the left (A-E) or to the bottom (F-I). Scale bars, 10 µm (F,G), 20 µm (A,B,H), 40 µm (C-E,I).

View larger version (98K): [in a new window]   Fig. 4. Metamorphic transformation of pharyngeal sense organs, as shown by MJ94/UAS-mCD8-GFP (green). Red indicates the Elav marker except in E,F, in which it indicates -caspase antibody. Stages are indicated in hours APF. (A-C) The pps maintains two sensilla throughout metamorphosis (arrows) each comprising three differentiated neurons, and becomes the dcso. (D-F) By contrast, the vps disintegrates in the early pupa and its neurons lose Elav immunoreactivity (D: arrows) or give rise to Elav-positive debris (D: arrowheads). Evidence for apoptosis is shown by staining with anti-caspase antibody (E). Neuronal identity of the apoptotic cells is indicated by mCD8 expression in the same optical section (E'). By contrast, anti-caspase antibody does not bind to the neurons of the dps (F,F'). (G-I) The dps with its clusters a and p1 is joined by two additional neurons (p2) from the dpo, forming a dps complex (dps c.). (J-O) Later on, the dps c. splits into two distinct sense organs, vcso and lso. The vcso includes p1 and p2, with six and two neurons, respectively (J-L). The p1 cluster comprises the distal and middle sensilla of the vcso, and the p2 cluster comprises the proximal sensillum. Five to six additional neurons deriving from dps and dpo remain outside the vcso (J-L: asterisks). At 24 hours APF, the neurons of the fishtrap bristles appear (L: arrowheads). In the lso, the a cluster (consisting of nine neurons) will form sensillum 7 (eight neurons; M: arrowheads) and an extra mononeuronal sensillum (M: small arrow). An additional nine neurons appear in the distal part of the lso (M,N: large arrows), four of which are associated with bineuronal sensilla 8 and 9 (M-O: asterisks). White dots indicate midline; distal is to the bottom except in F,F', in which distal is to the left. Scale bar, 20 µm.