The mlpt/Ubr3/Svb module comprises an ancient developmental switch for embryonic patterning
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 differ...
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doaj-bee44403534a43f8a16ce9a5c95c057d2021-05-05T17:29:12ZengeLife Sciences Publications LtdeLife2050-084X2019-03-01810.7554/eLife.39748The mlpt/Ubr3/Svb module comprises an ancient developmental switch for embryonic patterningSuparna Ray0Miriam I Rosenberg1https://orcid.org/0000-0001-5348-8247Hélène Chanut-Delalande2Amélie Decaras3Barbara Schwertner4William Toubiana5Tzach Auman6https://orcid.org/0000-0002-2233-4234Irene Schnellhammer7Matthias Teuscher8https://orcid.org/0000-0003-2340-5716Philippe Valenti9Abderrahman Khila10https://orcid.org/0000-0003-0908-483XMartin Klingler11https://orcid.org/0000-0001-8859-1965François Payre12https://orcid.org/0000-0002-8144-6711Department of Biology, Developmental Biology, University of Erlangen-Nuremberg, Erlangen, GermanyDepartment of Ecology, Evolution and Behavior, Hebrew University of Jerusalem, Jerusalem, IsraelCentre de Biologie du Développement, Université Paul Sabatier de Toulouse, Toulouse, FranceInstitut de Génomique Fonctionelle de Lyon, Lyon, FranceDepartment of Biology, Developmental Biology, University of Erlangen-Nuremberg, Erlangen, GermanyInstitut de Génomique Fonctionelle de Lyon, Lyon, FranceDepartment of Ecology, Evolution and Behavior, Hebrew University of Jerusalem, Jerusalem, IsraelDepartment of Biology, Developmental Biology, University of Erlangen-Nuremberg, Erlangen, GermanyDepartment of Biology, Developmental Biology, University of Erlangen-Nuremberg, Erlangen, GermanyCentre de Biologie du Développement, Université Paul Sabatier de Toulouse, Toulouse, FranceInstitut de Génomique Fonctionelle de Lyon, Lyon, FranceDepartment of Biology, Developmental Biology, University of Erlangen-Nuremberg, Erlangen, GermanyCentre de Biologie du Développement, Université Paul Sabatier de Toulouse, Toulouse, FranceSmall 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).https://elifesciences.org/articles/39748N. vitripennisG. buenoimicropeptideevolutiondevelopmentembryogenesis |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Suparna Ray Miriam I Rosenberg Hélène Chanut-Delalande Amélie Decaras Barbara Schwertner William Toubiana Tzach Auman Irene Schnellhammer Matthias Teuscher Philippe Valenti Abderrahman Khila Martin Klingler François Payre |
spellingShingle |
Suparna Ray Miriam I Rosenberg Hélène Chanut-Delalande Amélie Decaras Barbara Schwertner William Toubiana Tzach Auman Irene Schnellhammer Matthias Teuscher Philippe Valenti Abderrahman Khila Martin Klingler François Payre The mlpt/Ubr3/Svb module comprises an ancient developmental switch for embryonic patterning eLife N. vitripennis G. buenoi micropeptide evolution development embryogenesis |
author_facet |
Suparna Ray Miriam I Rosenberg Hélène Chanut-Delalande Amélie Decaras Barbara Schwertner William Toubiana Tzach Auman Irene Schnellhammer Matthias Teuscher Philippe Valenti Abderrahman Khila Martin Klingler François Payre |
author_sort |
Suparna Ray |
title |
The mlpt/Ubr3/Svb module comprises an ancient developmental switch for embryonic patterning |
title_short |
The mlpt/Ubr3/Svb module comprises an ancient developmental switch for embryonic patterning |
title_full |
The mlpt/Ubr3/Svb module comprises an ancient developmental switch for embryonic patterning |
title_fullStr |
The mlpt/Ubr3/Svb module comprises an ancient developmental switch for embryonic patterning |
title_full_unstemmed |
The mlpt/Ubr3/Svb module comprises an ancient developmental switch for embryonic patterning |
title_sort |
mlpt/ubr3/svb module comprises an ancient developmental switch for embryonic patterning |
publisher |
eLife Sciences Publications Ltd |
series |
eLife |
issn |
2050-084X |
publishDate |
2019-03-01 |
description |
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). |
topic |
N. vitripennis G. buenoi micropeptide evolution development embryogenesis |
url |
https://elifesciences.org/articles/39748 |
work_keys_str_mv |
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