Mitochondrial function relies on the precise spatial coordination of protein synthesis and import. Most mitochondrial proteins are nuclear-encoded and must be supplied across varying intracellular distances. In highly polarized cells such as fungal hyphae and neurons, active long distance mRNA transport is thought to sustain distal mitochondrial function, but its mechanistic coupling to protein import and organelle physiology is unclear. Here, we demonstrate that endosomal transport of mRNAs encoding mitochondrial proteins orchestrates local bioenergetics in infectious hyphae of Ustilago maydis. Using the subunit Atp3 of electron transport chain Complex V as a model, we uncover that the endosomal mRNA transporter Rrm4 is required for efficient mitochondrial protein import, particularly at growth poles. Loss of Rrm4 leads to defects in mitochondrial import, resulting in altered physiology. We propose that endosome-coupled mRNA transport constitutes a fundamental layer of subcellular mitochondrial homeostasis, with implications extending from fungal pathogenicity to neuronal disease.
Postma, J., Kuenzel, P., Wegmann, S. U., Muentjes, K., Devan, S. K., Sankaranarayanan, S., Krueger, S., Westhoff, P., Wierckx, N., Wijlick, L. v., Feldbruegge, M.
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