A transcriptomics resource reveals a transcriptional transition during ordered sarcomere morphogenesis in flight muscle
- Max Planck Institute of Biochemistry, Germany
- Aix Marseille University, France
- University of Zurich, Switzerland
Abstract
Muscles organise pseudo-crystalline arrays of actin, myosin and titin filaments to build force-producing sarcomeres. To study sarcomerogenesis, we have generated a transcriptomics resource of developing Drosophila flight muscles and identified 40 distinct expression profile clusters. Strikingly, most sarcomeric components group in two clusters, which are strongly induced after all myofibrils have been assembled, indicating a transcriptional transition during myofibrillogenesis. Following myofibril assembly, many short sarcomeres are added to each myofibril. Subsequently, all sarcomeres mature, reaching 1.5 µm diameter and 3.2 µm length and acquiring stretch-sensitivity. The efficient induction of the transcriptional transition during myofibrillogenesis, including the transcriptional boost of sarcomeric components, requires in part the transcriptional regulator Spalt major. As a consequence of Spalt knock-down, sarcomere maturation is defective and fibers fail to gain stretch-sensitivity. Together, this defines an ordered sarcomere morphogenesis process under precise transcriptional control - a concept that may also apply to vertebrate muscle or heart development.
Data availability
Processed data from DESeq2, Mfuzz and GO-Elite are available in Supplementary Files 1, 2, 4. mRNA-Seq data are publicly available from NCBI's Gene Expression Omnibus (GEO) under accession number GSE107247. Fiji scripts for analysis of sarcomere length, myofibril width and myofibril diameter are available from https://imagej.net/MyofibrilJ. Raw data used to generate all plots presented in figure panels are available in the source data files for Figures 1, 5, 6, 7 and 8. Data on statistical test results are presented in Supplementary File 5.
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Systematic transcriptomics reveals a biphasic mode of sarcomere morphogenesis in flight muscles regulated by SpaltPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE107247).
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The RNA binding protein Arrest (Aret) regulates myofibril maturation in Drosophila flight musclePublicly available at the NCBI Gene Expression Omnibus (accession no: GSE63707).
Article and author information
Author details
Funding
Max-Planck-Gesellschaft
- Maria L Spletter
- Christiane Barz
- Assa Yeroslaviz
- Xu Zhang
- Sandra B Lemke
- Bianca H Habermann
- Frank Schnorrer
Agence Nationale de la Recherche (ANR-10-INBS-04- 01)
- Frank Schnorrer
Agence Nationale de la Recherche (ANR ACHN)
- Frank Schnorrer
Centre National de la Recherche Scientifique
- Xu Zhang
- Adrien Bonnard
- Bianca H Habermann
- Frank Schnorrer
European Molecular Biology Organization (EMBO-LTR 688-2011)
- Maria L Spletter
Alexander von Humboldt-Stiftung
- Maria L Spletter
National Institute for Health Research (5F32AR062477)
- Maria L Spletter
H2020 European Research Council (ERC Grant 310939)
- Frank Schnorrer
Aix-Marseille Université (ANR-11-IDEX-0001-02)
- Bianca H Habermann
- Frank Schnorrer
Agence Nationale de la Recherche (ANR-11- LABX-0054)
- Frank Schnorrer
European Molecular Biology Organization (EMBO-YIP)
- Frank Schnorrer
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India
Version history
- Received: December 4, 2017
- Accepted: May 26, 2018
- Accepted Manuscript published: May 30, 2018 (version 1)
- Version of Record published: June 18, 2018 (version 2)
Copyright
© 2018, Spletter 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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A transcriptomics resource reveals a transcriptional transition during ordered sarcomere morphogenesis in flight muscle
eLife 7:e34058.
https://doi.org/10.7554/eLife.34058
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