Ecdysone promotes growth of imaginal discs through the regulation of Thor in D. melanogaster

Abstract

Animals have a determined species-specific body size that results from the combined action of hormones and signaling pathways regulating growth rate and duration. In Drosophila, the steroid hormone ecdysone controls developmental transitions, thereby regulating the duration of the growth period. Here we show that ecdysone promotes the growth of imaginal discs in mid-third instar larvae, since imaginal discs from larvae with reduced or no ecdysone synthesis are smaller than wild type due to smaller and fewer cells. We show that insulin-like peptides are produced and secreted normally in larvae with reduced ecdysone synthesis, and upstream components of insulin/insulin-like signaling are activated in their discs. Instead, ecdysone appears to regulate the growth of imaginal discs via Thor/4E-BP, a negative growth regulator downstream of the insulin/insulin-like growth factor/Tor pathways. Discs from larvae with reduced ecdysone synthesis have elevated levels of Thor, while mutations in Thor partially rescue their growth. The regulation of organ growth by ecdysone is evolutionarily conserved in hemimetabolous insects, as shown by our results obtained using Blattella germanica. In summary, our data provide new insights into the relationship between components of the insulin/insulin-like/Tor and ecdysone pathways in the control of organ growth.

Drosophila Lgr3 Couples Organ Growth with Maturation and Ensures Developmental Stability

“…This suggests that Dilp8/Lgr3 signaling in GCL neurons could modulate systemic growth through the control of ecdysone production. This is in line with previous findings showing that ecdysone promotes growth of imaginal tissues [16][17][18][19] and that feeding animals with ecdysone is sufficient to abrogate inter-organ growth coordination [6].…”

“…Interestingly, our data also suggest that Dilp8/Lgr3 signaling in the GCL neurons controls growth coordination of peripheral organs through systemic ecdysone levels. It was previously proposed that inter-disc growth coordination relies on systemic effects mediated by ecdysone [6], and several reports indicate that ecdysone is required for imaginal tissue growth both in flies and in Lepidoptera [16][17][18][19]21]. Future research will aim at deciphering the exact mechanism by which systemic ecdysone controls local tissue growth in order to mediate organ growth coordination.…”

The Hippo signalling pathway coordinates organ growth and limits developmental variability by controlling dilp8 expression

“…Whether ecdysone acts downstream of Dilp8/Lgr3 to mediate such continuous feedback on organ growth remains to be determined. Several reports indicate that ecdysone is required for imaginal tissue growth both in flies and in Lepidoptera452526, and previous data suggest that organ growth coordination relies on systemic effects mediated by ecdysone. Interestingly, Taiman, a co-activator of ecdysone receptor mediates Yki-dependent dilp8 expression, therefore suggesting that the ecdysone signal itself feeds back on dilp8 expression27.…”

A Search for Genes Mediating the Growth-Promoting Function of TGFβ in the Drosophila melanogaster Wing Disc

“…On the one hand, TGFb signaling is required in the ring gland, the main endocrine organ of the Drosophila larva, where it regulates the production of the steroid hormone Ecdyson (Gibbens et al 2011). Ecdyson not only promotes the progression through larval stages and metamorphosis, but is also required in the imaginal discs to sustain cell proliferation in the third larval instar (Herboso et al 2015). On the other hand, TGFb signaling acting in epithelial cells is also required for the wing disc to reach its normal size (Brummel et al 1999;Hevia and de Celis 2013).…”