Sustained Elongation of Sperm Tail Promoted by Local Remodeling of Giant Mitochondria in Drosophila

Abstract

Sperm length in Drosophilidae varies from a few hundred microns to 6 cm as a result of evolutionary selection. In postcopulatory competition, longer sperm have an advantage in positioning their head closer to the egg. Sperm cell elongation can proceed in the absence of an axoneme, suggesting that a mechanism besides intraflagellar transport emerged to sustain it. Here we report that sperm elongation in Drosophila melanogaster is driven by the interdependent extension of giant mitochondria and microtubule array that is formed around the mitochondrial surface. In primary cultures of elongating spermatids, we demonstrated that the mitochondrial integrity and local dynamics of microtubules at the tail tip region are essential for uniaxial elongation of the sperm tail. Mitochondria-microtubule linker protein Milton accumulated on mitochondria near the tail tip and is required for the sliding movement of microtubules. Disruption of Milton and its associated protein dMiro, and of potential microtubule crosslinkers Nebbish and Fascetto, caused strong elongation defects, indicating that mitochondria-microtubule association and microtubule crosslinking are required for spermatid tail elongation. Mitochondria play unexpected roles in sperm tail elongation in Drosophila by providing a structural platform for microtubule reorganization to support the robust elongation taking place at the tip of the very long sperm tail. The identification of mitochondria as an organizer of cytoskeletal dynamics extends our understanding of mechanisms of cell morphogenesis.