E93 controls adult differentiation by repressing broad in Drosophila

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  • dc.contributor.author Cruz, Josefa
  • dc.contributor.author Ureña, Enric
  • dc.contributor.author Iñiguez, Luis P.
  • dc.contributor.author Irimia Martínez, Manuel
  • dc.contributor.author Franch i Marro, Xavier
  • dc.contributor.author Martín, David
  • dc.date.accessioned 2025-02-05T07:09:40Z
  • dc.date.available 2025-02-05T07:09:40Z
  • dc.date.issued 2024
  • dc.description.abstract In Drosophila melanogaster, successful development relies on the precise coordination of both spatial and temporal regulatory axes. The temporal axis governs stage-specific identity and developmental transitions through a number of genes, collectively forming the Metamorphic Gene Network. Among these, Ecdysone inducible protein 93F (E93) serves as the critical determinant for adult specification, but its mechanism of action remains unclear. Here, we found that, rather than acting mainly as an instructive signal, E93 promotes adult differentiation through the repression of the pupal specifier broad (br). In the absence of E93, sustained high levels of Br during the pupal stage strongly represses pupal-specific enhancers that are essential for the terminal differentiation of the wing. Notably, RNA-seq analysis confirmed that the majority of E93-dependent transcriptomic changes in pupal wings are primarily driven by br repression. In addition, we also show that Br represses the pupal-enhancers during the larval and prepupal stages preventing the premature implementation of the adult genetic program, and that it also dampens the activity of larval enhancers during the latter stages of larval development. This mechanism of action seems to be a derived feature acquired in Diptera, as in the coleopteran Tribolium castaneum, repression of br by E93 is not sufficient to allow adult differentiation. In summary, our study elucidates the crucial role of the intricate interplay between E93 and Br as the governing mechanism in the process of terminal differentiation in Drosophila. This finding holds significant implications for advancing our understanding of the evolution of insect metamorphosis.
  • dc.description.sponsorship This project is supported by grants PGC2018-098427-B-I00 and PID2021-125661NB-I00 to X.F.-M. and D.M. funded by MICIU/AEI/10.13039/501100011033 and by FEDER, EU. The project is supported also by Grants 2017 SGR 1030 and 2021 SGR 00417 to X.F.-M. and D.M. funded by the Departament de Recerca i Universitats de la Generalitat de Catalunya. Additional support for this research was provided by Grants PGC2020:PID2020-115040 GB-I00 to M.I. and IJC2020-044783-I funded by MCIN/AEI/10.13039/501100011033 and by the European Union Next Generation EU/PRTR to L.P.I. We thank the Genomics Unit at the Center for Genomic Regulation for assistance with the sequencing, and Carolina Reisenman for critical reading of the manuscript.
  • dc.format.mimetype application/pdf
  • dc.identifier.citation Cruz J, Ureña E, Iñiguez LP, Irimia M, Franch-Marro X, Martín D. E93 controls adult differentiation by repressing broad in Drosophila. Proc Natl Acad Sci U S A. 2024 Dec 17;121(51):e2403162121. DOI: 10.1073/pnas.2403162121
  • dc.identifier.doi http://dx.doi.org/10.1073/pnas.2403162121
  • dc.identifier.issn 0027-8424
  • dc.identifier.uri http://hdl.handle.net/10230/69491
  • dc.language.iso eng
  • dc.publisher National Academy of Sciences
  • dc.relation.ispartof Proc Natl Acad Sci U S A. 2024 Dec 17;121(51):e2403162121
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/PGC2018-098427-B-I00
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/3PE/PID2021-125661NB-I00
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/PID2020-115040 GB-I00
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/IJC2020-044783-I
  • dc.rights Copyright © 2024 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).
  • dc.rights.accessRights info:eu-repo/semantics/openAccess
  • dc.rights.uri http://creativecommons.org/licenses/by-nc-nd/4.0/
  • dc.subject.keyword Drosophila
  • dc.subject.keyword E93
  • dc.subject.keyword Broad
  • dc.subject.keyword Metamorphic transition
  • dc.subject.keyword Temporal development
  • dc.title E93 controls adult differentiation by repressing broad in Drosophila
  • dc.type info:eu-repo/semantics/article
  • dc.type.version info:eu-repo/semantics/publishedVersion

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