Abstract
BackgroundIn humans and other animals, the internal organs are positioned asymmetrically in the body cavity, and disruption of this body plan can be fatal in humans. The mechanisms by which internal asymmetry are established are presently the subject of intense study; however, the functional significance of internal asymmetry (outside the brain) is largely unexplored. Is internal asymmetry functionally significant, or merely an expedient way of packing organs into a cavity?Methodology/Principal FindingsLike humans, Drosophila shows internal asymmetry, with the gut thrown into stereotyped folds. There is also renal asymmetry, with the rightmost pair of renal (Malpighian) tubules always ramifying anteriorly, and the leftmost pair always sitting posteriorly in the body cavity. Accordingly, transcriptomes of anterior-directed (right-side) and posterior-directed (left-side) Malpighian (renal) tubules were compared in both adult male and female Drosophila. Although genes encoding the basic functions of the tubules (transport, signalling) were uniformly expressed, some functions (like innate immunity) showed positional or gender differences in emphasis; others, like calcium handling or the generation of potentially toxic ammonia, were reserved for just the right-side or left-side tubules, respectively. These findings correlated with the distinct locations of each tubule pair within the body cavity. Well known developmental genes (like dorsocross, dachshund and doublesex) showed continuing, patterned expression in adult tubules, implying that somatic tissues maintain both left-right and gender identities throughout life. Gender asymmetry was also noted, both in defence and in male-specific expression of receptors for neuropeptide F and sex-peptide: NPF elevated calcium only in male tubules.Conclusions/SignificanceAccordingly, the physical asymmetry of the tubules in the body cavity is directly adaptive. Now that the detailed machinery underlying internal asymmetry is starting to be delineated, our work invites the investigation, not just of tissues in isolation, but in the context of their unique physical locations and milieux.
Highlights
The vertebrate body plan is internally asymmetric [1,2,3], and complete situs inversus is benign in humans, partial disruption of this asymmetric organization can be lethal [4,5,6]
BLASTP searches reveal that proteins closely similar to CG14963 are found throughout the Diptera, but that the Dipteran branch is rather diverged from the Lepidopteran branch
A transporting epithelium has been profiled for expression according to both its gender and its disposition within the body
Summary
The vertebrate body plan is internally asymmetric [1,2,3], and complete situs inversus is benign in humans, partial disruption of this asymmetric organization (for example in heterotaxy) can be lethal [4,5,6]. Separated by 450 M year of divergent evolution, many insect body plans show similar internal asymmetry; for example, the alimentary canal of the classical developmental model Drosophila starts development symmetrically, but is thrown into highly stereotyped folds within the body cavity. Just as human kidneys sit slightly differently in the abdomen, so the Drosophila Malpighian (renal) tubules show marked asymmetry; the two tubule primordia initially sit dorsoventrally at the midgut / hindgut boundary, a rotation of the developing alimentary canal sets the dorsal tubules on the right side, and the ventral tubules on the left side, of the body [7]. Is internal asymmetry functionally significant, or merely an expedient way of packing organs into a cavity?
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