Abstract
Even distribution of peroxisomes (POs) and lipid droplets (LDs) is critical to their role in lipid and reactive oxygen species homeostasis. How even distribution is achieved remains elusive, but diffusive motion and directed motility may play a role. Here we show that in the fungus Ustilago maydis ∼95% of POs and LDs undergo diffusive motions. These movements require ATP and involve bidirectional early endosome motility, indicating that microtubule-associated membrane trafficking enhances diffusion of organelles. When early endosome transport is abolished, POs and LDs drift slowly towards the growing cell end. This pole-ward drift is facilitated by anterograde delivery of secretory cargo to the cell tip by myosin-5. Modelling reveals that microtubule-based directed transport and active diffusion support distribution, mobility and mixing of POs. In mammalian COS-7 cells, microtubules and F-actin also counteract each other to distribute POs. This highlights the importance of opposing cytoskeletal forces in organelle positioning in eukaryotes.
Highlights
Even distribution of peroxisomes (POs) and lipid droplets (LDs) is critical to their role in lipid and reactive oxygen species homeostasis
We show that F-actin and myosin-5 exert a polar drift (PD) force that moves POs and LDs to the growth region when MTs are absent
We show that a similar balance between such cytoskeletal forces distributes POs in mammalian COS-7 cells, suggesting that this may be a general principle for organelle distribution that is conserved from fungi to mammals
Summary
Even distribution of peroxisomes (POs) and lipid droplets (LDs) is critical to their role in lipid and reactive oxygen species homeostasis. We tested this idea by disrupting MTs with benomyl and determining the extent of short-range motion of individual organelles, given as the diffusion coefficient DPO, in the axial and radial direction within hyphal cells.
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