Functional Correlates of Positional and Gender-Specific Renal Asymmetry in Drosophila

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.

Mechanisms of calcium sequestration by isolated Malpighian tubules of the house cricket Acheta domesticus

“…Conversely, the lack of Ca 2+ transport by the distal tubules is consistent with the absence of granules. Segment-specific Ca 2+ transport has been demonstrated previously: in specialized tubule segments of the alkali fly, Eulima hians (Herbst & Bradley, 1989), in the upper tubules of the kissing bug, R. prolixus (Maddrell et al, 1991), and in distal tubules of the fruit fly, D. melanogaster (Browne & O'Donnell, 2016 (Chintapalli et al, 2012).…”

A comprehensive transcriptomic view of renal function in the malaria vector, Anopheles gambiae

“…By contrast, expression of the kinin receptor is stable between larva and adult in both Anopheles and Drosophila. Data from the gene expression database FlyAtlas shows some similarities with Drosophila, as DH31 receptor (DH31-R1) is massively enriched in the adult tubules compared to the larval tubules, and DH44-R2 isn't enriched in either life-stage (Chintapalli et al, 2007a).…”

“…We would expect mechanisms of secretion to be essential for survival, but what about less obvious transport functions of the tubule? We mined the Anopheles microarray data in combination with FlyAtlas (Chintapalli et al, 2007a), to identify transporters that are significantly up-regulated in the Anopheles tubule, that have conserved orthologues that also show up-regulated expression in the Drosophila tubules. We selected four genes for functional analysis: the putative sugar transporters AGAP007752 and CG15406, the inorganic phosphate transporters AGAP011251 and Picot, the zinc transporters AGAP009005 and Znt35c, and the monocarboxylate transporters AGAP002587 and CG8028.…”

“…Transcriptomic analysis has identified a range of abundantly expressed transporters that have been shown experimentally to underpin tubule function (Chintapalli et al, 2012;Wang et al, 2004); and by comparing epithelial transcriptomes by meta-analysis of the online FlyAtlas.org resource (Chintapalli et al, 2007b;Chintapalli et al, 2013), it has been shown that the key fluid secreting epithelia of Drosophila (salivary glands, midgut, tubules, hindgut) all shared a transcriptomic fingerprint, or 'epitheliome' (Chintapalli et al, 2013). Although unsupported transcriptomic studies should be interpreted cautiously, downstream experimental testing has validated the models so obtained (Allan et al, 2005;Cabrero et al, 2014;Wang et al, 2004).…”

Cell signalling mechanisms for insect stress tolerance

“…Recent work indicates that the anterior and posterior tubules exhibit transcriptome and functional asymmetry (Chintapalli et al, 2012), suggesting further intriguing possibilities of anterior-and posterior-specific roles for each pair of tubules. Tubules consist of two major cell types, the principal and stellate cells (Dow, 2009), which allow functional separation of ion transport and cell signalling pathways for physiological function.…”