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

Abstract

The sense organs of adult Drosophila, and holometabolous insects in general, derive essentially from imaginal discs and hence are adult specific. Experimental evidence presented here, however, suggests a different developmental design for the three largely gustatory sense organs located along the pharynx. In a comprehensive cellular analysis, we show that the posteriormost of the three organs derives directly from a similar larval organ and that the two other organs arise by splitting of a second larval organ. Interestingly, these two larval organs persist despite extensive reorganization of the pharynx. Thus, most of the neurons of the three adult organs are surviving larval neurons. However, the anterior organ includes some sensilla that are generated during pupal stages. Also, we observe apoptosis in a third larval pharyngeal organ. Hence, our experimental data show for the first time the integration of complex, fully differentiated larval sense organs into the nervous system of the adult fly and demonstrate the embryonic origin of their neurons. Moreover, they identify metamorphosis of this sensory system as a complex process involving neuronal persistence, generation of additional neurons and neuronal death. Our conclusions are based on combined analysis of reporter expression from P[GAL4] driver lines, horseradish peroxidase injections into blastoderm stage embryos, cell labeling via heat-shock-induced flip-out in the embryo, bromodeoxyuridine birth dating and staining for programmed cell death. They challenge the general view that sense organs are replaced during metamorphosis.

Candidate ionotropic taste receptors in the Drosophila larva

“…A remarkable feature of the larval pharynx is that some of its organs are incorporated into the adult pharynx. Whereas most larval sense organs disintegrate and are replaced by adult organs deriving from imaginal discs, the DPS and PPS survive (5). The DPS splits and is remodelled into the ventral cibarial sense organ and the labral sense organ (LSO) of the adult pharynx.…”

“…4 and 7 and Fig. S3 F-H were based on a previously published technique (5). Samples of CNS tissue or larval heads were dissected, permeabilized, and fixed in a solution of PBS plus 0.4% Triton-X (PBS-T) and 3.7% (vol/vol) formaldehyde for at least 1 h. They were washed three times for at least 20 min each time in PBS.…”

“…1). Each organ contains ∼17, 16, and 6 neurons, respectively, most of which are likely to be gustatory (5). Another organ, the dorsal pharyngeal organ (DPO), contains five neurons (3,5,8).…”

“…Each organ contains ∼17, 16, and 6 neurons, respectively, most of which are likely to be gustatory (5). Another organ, the dorsal pharyngeal organ (DPO), contains five neurons (3,5,8). A variety of other neurons in the body wall of the thorax and abdomen, and at the posterior tip of the larva, are also likely to be chemosensory (9)(10)(11).…”

Role of proneural genes in the formation of the larval olfactory organ of Drosophila

“…The larva, in contrast, comprises only a small fraction of the numbers of adult olfactory and gustatory neurons, and the larval neurons are collected in very few chemosensory organs. The two dominant among them are the dorsal organ (DO) and the terminal organ on the cephalic hemispheres (Singh and Singh 1984;Python and Stocker 2002;Gendre et al 2004). Whereas the terminal organ serves essentially gustatory function, the DO is a mixed smell and taste organ.…”