Small open reading frames (smORFs) encoding ‘micropeptides’ exhibit remarkable evolutionary complexity. Conserved peptides encoded by mille-pattes (mlpt)/polished rice (pri)/ tarsal less (tal) are essential for embryo segmentation in Tribolium but, in Drosophila, function in terminal epidermal differentiation and patterning of adult legs. Here, we show that a molecular complex identified in Drosophila epidermal differentiation, comprising Mlpt peptides, ubiquitin- ligase Ubr3 and transcription factor Shavenbaby (Svb), represents an ancient developmental module required for early insect embryo patterning. We find that loss of segmentation function for this module in flies evolved concomitantly with restriction of Svb expression in early Drosophila embryos. Consistent with this observation, artificially restoring early Svb expression in flies causes segmentation defects that depend on mlpt function, demonstrating enduring potency of an ancestral developmental switch despite evolving embryonic patterning modes. These results highlight the evolutionary plasticity of conserved molecular complexes under the constraints of essential genetic networks. Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor’s assessment is that all the issues have been addressed (see decision letter).
Bibliographical noteFunding Information:
We would like to thank Ariel Chipman, Claude Desplan, and Igor Ulitsky for warm support during the course of this work, and for discussions and critical reading of the manuscript, Julien Favier, Amélie Destenabes and Cleopatra Tsanis for embryo injection and help with transgenics. European Research Council 616346 Abderrahman Khila H2020 Marie Skłodowska-Curie Actions 654719 Miriam I Rosenberg Fulbright Association Miriam I Rosenberg Deutsche Forschungsge- meinschaft KL656-5 Martin Klingler Friedrich-Alexander-Universität Erlangen-Nürnberg Martin Klingler Agence Nationale de la Re- cherche ChronoNet François Payre Fondation pour la Recherche Médicale DEQ20170336739 François Payre.
© Ray et al.