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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Main Authors: 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
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-03-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/39748
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spelling 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
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