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

Jerome Avellaneda, Clement Rodier, Fabrice Daian, Nicolas Brouilly, Thomas Rival, Nuno Miguel Luis () and Frank Schnorrer ()
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Jerome Avellaneda: Aix Marseille University, CNRS, IBDM, Turing Center for Living Systems
Clement Rodier: Aix Marseille University, CNRS, IBDM, Turing Center for Living Systems
Fabrice Daian: Aix Marseille University, CNRS, IBDM, Turing Center for Living Systems
Nicolas Brouilly: Aix Marseille University, CNRS, IBDM, Turing Center for Living Systems
Thomas Rival: Aix Marseille University, CNRS, IBDM, Turing Center for Living Systems
Nuno Miguel Luis: Aix Marseille University, CNRS, IBDM, Turing Center for Living Systems
Frank Schnorrer: Aix Marseille University, CNRS, IBDM, Turing Center for Living Systems

Nature Communications, 2021, vol. 12, issue 1, 1-18

Abstract: 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.

Date: 2021
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DOI: 10.1038/s41467-021-22058-7

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