Antagonistic role of the BTB-zinc finger transcription factors chinmo and broad-complex in the juvenile/pupal transition and in growth control

  1. Sílvia Chafino
  2. Panagiotis Giannios
  3. Jordi Casanova
  4. David Martin  Is a corresponding author
  5. Xavier Franch-Marro  Is a corresponding author
  1. Barcelona Institute of Science and Technology, Spain
  2. Institute of Evolutionary Biology (CSIC-UPF), Spain

Abstract

During development, the growing organism transits through a series of temporally regulated morphological stages to generate the adult form. In humans, for example, development progresses from childhood through to puberty and then to adulthood, when sexual maturity is attained. Similarly, in holometabolous insects, immature juveniles transit to the adult form through an intermediate pupal stage when larval tissues are eliminated and the imaginal progenitor cells form the adult structures. The identity of the larval, pupal and adult stages depends on the sequential expression of the transcription factors chinmo, Br-C and E93. However, how these transcription factors determine temporal identity in developing tissues is poorly understood. Here we report on the role of the larval specifier chinmo in larval and adult progenitor cells during fly development. Interestingly, chinmo promotes growth in larval and imaginal tissues in a Br-C-independent and -dependent manner, respectively. In addition, we found that the absence of chinmo during metamorphosis is critical for proper adult differentiation. Importantly, we also provide evidence that, in contrast to the well-known role of chinmo as a pro-oncogene, Br-C and E93 act as tumour suppressors. Finally, we reveal that the function of chinmo as a juvenile specifier is conserved in hemimetabolous insects as its homolog has a similar role in Blatella germanica. Taken together, our results suggest that the sequential expression of the transcription factors Chinmo, Br-C and E93 during larva, pupa an adult respectively, coordinate the formation of the different organs that constitute the adut organism.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting file. Source Data files have been provided for Figures 1 A and E (Figure1- SourceData1), Figure 2B, C, D and E (Figure2-SourceData1), Figure 5 B, C , D, E and F (Figure5-SourceData1), Figure 8G (Figure8-SourceData1), Figure 9 A and D (Figure9-SourceData1) and Figure2-figure suplement 1 D, E and F (Figure2-figure suplement 1-SourceData1).

Article and author information

Author details

  1. Sílvia Chafino

    Institut de Biologia Molecular de Barcelona (CSIC), Barcelona Institute of Science and Technology, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  2. Panagiotis Giannios

    Institut de Recerca Biomèdica de Barcelona (IRB Barcelona), Barcelona Institute of Science and Technology, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7881-1431
  3. Jordi Casanova

    Institut de Recerca Biomèdica de Barcelona (IRB Barcelona), Barcelona Institute of Science and Technology, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6121-8589
  4. David Martin

    Functional genomics and evoloution, Institute of Evolutionary Biology (CSIC-UPF), Barcelona, Spain
    For correspondence
    david.martin@ibe.upf-csic.es
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9784-647X
  5. Xavier Franch-Marro

    Functional Genomics and Evolution, Institute of Evolutionary Biology (CSIC-UPF), Barcelona, Spain
    For correspondence
    xavier.franch@ibe.upf-csic.es
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7465-6729

Funding

Ministerio de Ciencia e Innovación (PGC2018-098427-B-I00)

  • David Martin
  • Xavier Franch-Marro

Ministerio de Ciencia e Innovación (PID2021-125661NB-100)

  • David Martin
  • Xavier Franch-Marro

Ministerio de Ciencia e Innovación (PGC2018-094254-B-100)

  • Jordi Casanova

Agència de Gestió d'Ajuts Universitaris i de Recerca (2017-SGR 1030)

  • David Martin
  • Xavier Franch-Marro

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Vilaiwan M Fernandes, University College London, United Kingdom

Version history

  1. Received: November 2, 2022
  2. Preprint posted: November 18, 2022 (view preprint)
  3. Accepted: April 27, 2023
  4. Accepted Manuscript published: April 28, 2023 (version 1)
  5. Version of Record published: June 1, 2023 (version 2)

Copyright

© 2023, Chafino et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Sílvia Chafino
  2. Panagiotis Giannios
  3. Jordi Casanova
  4. David Martin
  5. Xavier Franch-Marro
(2023)
Antagonistic role of the BTB-zinc finger transcription factors chinmo and broad-complex in the juvenile/pupal transition and in growth control
eLife 12:e84648.
https://doi.org/10.7554/eLife.84648

Share this article

https://doi.org/10.7554/eLife.84648

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