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Myofibril and mitochondria morphogenesis are coordinated by a mechanical feedback mechanism in muscle

Jerome Avellaneda, Clement Rodier, Fabrice Daian, Thomas Rival, Nuno Miguel Luis, View ORCID ProfileFrank Schnorrer
doi: https://doi.org/10.1101/2020.07.18.209957
Jerome Avellaneda
1Aix Marseille University, CNRS, IBDM, Turing Center for Living Systems, 13288 Marseille, France
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Clement Rodier
1Aix Marseille University, CNRS, IBDM, Turing Center for Living Systems, 13288 Marseille, France
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Fabrice Daian
1Aix Marseille University, CNRS, IBDM, Turing Center for Living Systems, 13288 Marseille, France
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Thomas Rival
1Aix Marseille University, CNRS, IBDM, Turing Center for Living Systems, 13288 Marseille, France
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Nuno Miguel Luis
1Aix Marseille University, CNRS, IBDM, Turing Center for Living Systems, 13288 Marseille, France
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  • For correspondence: nuno.luis@univ-amu.fr frank.schnorrer@univ-amu.fr
Frank Schnorrer
1Aix Marseille University, CNRS, IBDM, Turing Center for Living Systems, 13288 Marseille, France
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  • ORCID record for Frank Schnorrer
  • For correspondence: nuno.luis@univ-amu.fr frank.schnorrer@univ-amu.fr
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Abstract

Complex animals build specialised muscle to match specific biomechanical and energetic needs. Hence, composition and architecture of sarcomeres as well as 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 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 coincides with 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.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted July 18, 2020.
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Myofibril and mitochondria morphogenesis are coordinated by a mechanical feedback mechanism in muscle
Jerome Avellaneda, Clement Rodier, Fabrice Daian, Thomas Rival, Nuno Miguel Luis, Frank Schnorrer
bioRxiv 2020.07.18.209957; doi: https://doi.org/10.1101/2020.07.18.209957
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Myofibril and mitochondria morphogenesis are coordinated by a mechanical feedback mechanism in muscle
Jerome Avellaneda, Clement Rodier, Fabrice Daian, Thomas Rival, Nuno Miguel Luis, Frank Schnorrer
bioRxiv 2020.07.18.209957; doi: https://doi.org/10.1101/2020.07.18.209957

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