An embryonic myosin converter domain influences Drosophila indirect flight muscle stretch activation, power generation and flight

Abstract

Summary Stretch activation (SA) is critical to the flight ability of insects powered by asynchronous, indirect flight muscles (IFM). An essential muscle protein component for SA and power generation is myosin. Which structural domains of myosin are significant for setting SA properties and power generation levels is poorly understood. We made use of Drosophila's transgenic techniques and unique single muscle myosin heavy chain gene to test the influence of the myosin converter domain on IFM SA and power generation. Replacing the endogenous converter with an embryonic version decreased SA tension and rate of SA tension generation. The changes in SA properties and myosin kinetics from the converter exchange caused power generation to drop to 10% of control fiber power when the optimal conditions for control fibers, 1% muscle length (ML) amplitude and 150 Hz oscillation frequency, were applied to fibers expressing the embryonic converter (IFI-EC). Optimizing conditions for IFI-EC fiber power production, doubling ML amplitude and decreasing oscillation frequency by 60%, improved power output to be 60% of optimized control fiber power. IFI-EC flies altered their aerodynamic flight characteristics to better match optimal fiber power generation conditions as wing beat frequency decreased and wing stroke amplitude increased. This enabled flight in spite of the drastic changes to fiber mechanical performance.