Myofibril and mitochondria morphogenesis are coordinated by a mechanical feedback mechanism in muscle
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Abstract
Complex animals build specialised muscles to match specific biomechanical and energetic needs. Hence, composition and architecture of sarcomeres and mitochondria are muscle type specific. However, mechanisms coordinating mitochondria with sarcomere morphogenesis are elusive. Here we use Drosophila muscles to demonstrate that myofibril and mitochondria morphogenesis are intimately linked. In flight muscles, the muscle selector spalt instructs mitochondria to intercalate between myofibrils, which in turn mechanically constrain mitochondria into elongated shapes. Conversely in cross-striated leg muscles, mitochondria networks surround myofibril bundles, contacting myofibrils only with thin extensions. To investigate the mechanism causing these differences, we manipulated mitochondrial dynamics and found that increased mitochondrial fusion during myofibril assembly prevents mitochondrial intercalation in flight muscles. Strikingly, this causes the expression of cross-striated muscle specific sarcomeric proteins. Consequently, flight muscle myofibrils convert towards a partially cross-striated architecture. Together, these data suggest a biomechanical feedback mechanism downstream of spalt synchronizing mitochondria with myofibril morphogenesis.
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Mitochondrial fission is essential for skeletal muscle health.
“Taken altogether, the findings discussed above clearly indicate that mitochondrial fission is essential for skeletal muscle health.”
From Mitochondrial Dynamics and Mitophagy in Skeletal Muscle Health and Aging (2021) · cites this paper as [44]
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Muscle growth by sarcomere divisions
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Titin-dependent biomechanical feedback tailors sarcomeres to specialized muscle functions in insects
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Self-citationM1BP is an essential transcriptional activator of oxidative metabolism during Drosophila development
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SARS-CoV-2 Orphan Gene ORF10 Contributes to More Severe COVID-19 DiseasePreprint
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Spatial transcriptomics in the adult Drosophila brain and bodyPreprint
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Self-citationDe novo clustering of long-read amplicons improves phylogenetic insight into microbiome data
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A transcriptional enhancer regulates cardiac maturation
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A Candidate RNAi Screen Reveals Diverse RNA-Binding Protein Phenotypes in Drosophila Flight Muscle
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Shortening deactivation: quantifying a critical component of cyclical muscle contraction
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Self-citationThe varied functions of the giant muscle scaffold protein obscurin
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RHOT Proteins Link Mitochondrial Motility to Cardiomyocyte Sarcomere Maturation
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Spatial transcriptomics in the adult Drosophila brain and body
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Mitochondrial fission regulates midgut muscle assembly and tick feeding capacity
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Self-citationTitin-dependent biomechanical feedback tailors sarcomeres to specialised muscle functions in insectsPreprint
Loreau, V., Koolhaas, W. H., Chan, E. H., de Boissier, P., Brouilly, N., Avosani, S., Sane, A., Pitaval, C., Reiter, S., Luis, N. M., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.30.615857 · Cited by 2 · see citing works
Self-citationOxoglutarate dehydrogenase coordinates myofibril growth by maintaining amino acid homeostasisPreprint
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E2VD: a unified evolution-driven framework for virus variation drivers predictionPreprint
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Self-citationKLHL41 orchestrates sarcomere assembly and size to drive skeletal muscle hypertrophy in vivoPreprint
Han, H., Shi, J., Bongiorno, A. H., Mansur, A., Widrick, J. J., Tate, G., Gill, S., Karimi, E., Granzier, H., Moore, J. R., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.05.30.655367 · Cited by 1 · see citing works
Arginine Kinase 1 regulates energy homeostasis in Drosophila muscle developmentPreprint
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SPRI: Spatial Pattern Recognition using Information based method for spatial gene expression dataPreprint
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Muscle physiology and insect flight
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Self-citationCardiac myofibril networks induce shear stressPreprint
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Cardiac myofibril networks induce shear stress
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Arginine Kinase 1 supports energy homeostasis in Drosophila flight muscle development
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Klhl41b orchestrates sarcomere assembly and growth to drive skeletal muscle hypertrophy in vivo
Han, H., Tate, G. R., Shi, J., Bongiorno, A., Mansur, A., Widrick, J. J., Gill, S., Karimi, E., Granzier, H. L. M., Moore, J. R., et al. (2026) · Skeletal Muscle · doi:10.1186/s13395-026-00453-2
- Authors
- Avellaneda, J., Rodier, C., Daian, F., Brouilly, N., Rival, T., Luis, N. M., & Schnorrer, F.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Luis, Nuno Miguel
- Schnorrer, Frank
- ORCID
- Venue
- Nature Communications
- Published
- 2021-04-07
- Volume
- 12
- Issue
- 1
- Pages
- 2091-2091
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC8027795
- OpenAlex
- W3146153743
- Cited by
- 92
- References
- 65
- Citations by year
- 2026: 10 · 2025: 14 · 2024: 23 · 2023: 19 · 2022: 16 · 2021: 10
- FWCI
- 5.33
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- HAL (submittedVersion)
- HAL (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Aix-Marseille Université (ANR 11-IDEX-0001-02)
- European Commission (2007–2013, FP/2007-2013)/ERC, FP/2007/2013)
- Agence Nationale de la Recherche (ANR-11-IDEX-0001, ANR11IDEX000102, ANR-18-CE45-0016, ANR-10-INBS-04-01, 10-INBS-04-01, ANR‐10_INBS‐04, ANR18, ANR-11-IDEX, FP/2007-2013, ANR-10, IDEX-0001-02, ANR-16-ACHN-0015)
- Centre National de la Recherche Scientifique (ANR-11-IDEX-0001-02)
- National Institutes of Health (FP/2007-2013, -0001, NIH P40OD018537, P40OD018537)
- FP7 Ideas: European Research Council (310939)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- mitochondrial morphogenesis, spalt, mitochondrial fusion, mitochondrial dynamics, striated muscle, flight muscle, lower limb muscles, biomechanical feedback, Drosophila muscle
- MeSH terms
- Animals, Biomechanical Phenomena, Drosophila, Drosophila melanogaster, Feedback, Flight, Animal, Male, Mitochondria, Morphogenesis, Myofibrils, Sarcomeres, Transcription Factors, Myogenic Regulatory Factors, Muscle, Skeletal, Muscle Development, Drosophila Proteins, Mechanical Phenomena
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