Abstract

BackgroundPrevious studies have shown that plant mitochondrial movements are myosin-based along actin filaments, which undergo continuous turnover by the exchange of actin subunits from existing filaments. Although earlier studies revealed that actin filament dynamics are essential for many functions of the actin cytoskeleton, there are little data connecting actin dynamics and mitochondrial movements.Methodology/Principal FindingsWe addressed the role of actin filament dynamics in the control of mitochondrial movements by treating cells with various pharmaceuticals that affect actin filament assembly and disassembly. Confocal microscopy of Arabidopsis thaliana root hairs expressing GFP-FABD2 as an actin filament reporter showed that mitochondrial distribution was in agreement with the arrangement of actin filaments in root hairs at different developmental stages. Analyses of mitochondrial trajectories and instantaneous velocities immediately following pharmacological perturbation of the cytoskeleton using variable-angle evanescent wave microscopy and/or spinning disk confocal microscopy revealed that mitochondrial velocities were regulated by myosin activity and actin filament dynamics. Furthermore, simultaneous visualization of mitochondria and actin filaments suggested that mitochondrial positioning might involve depolymerization of actin filaments on the surface of mitochondria.Conclusions/SignificanceBase on these results we propose a mechanism for the regulation of mitochondrial speed of movements, positioning, and direction of movements that combines the coordinated activity of myosin and the rate of actin turnover, together with microtubule dynamics, which directs the positioning of actin polymerization events.

Highlights

  • Mitochondria serve as energy-producing organelles in plants and other eukaryotes, and they are known to associate with energy-consuming organelles and structures, such as the nucleus, rough endoplasmic reticulum, and plasma membrane [1]

  • Conclusions/Significance: Base on these results we propose a mechanism for the regulation of mitochondrial speed of movements, positioning, and direction of movements that combines the coordinated activity of myosin and the rate of actin turnover, together with microtubule dynamics, which directs the positioning of actin polymerization events

  • When trichoblast cells formed bulges, mitochondria aggregated within the bulge (Fig. 1C), the average thickness of actin bundles were reduced to 0.4160.10 mm (n = 14 cells), and fine actin filaments were present at the site of bulge outgrowth (Fig. 1D)

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Summary

Introduction

Mitochondria serve as energy-producing organelles in plants and other eukaryotes, and they are known to associate with energy-consuming organelles and structures, such as the nucleus, rough endoplasmic reticulum, and plasma membrane [1]. Active mitochondrial movements involve a close interaction with the cytoskeleton, in particular, with actin filaments or with microtubules. A number of studies have shown that both microfilaments and microtubules function in mitochondrial movements, the contribution of each cytoskeletal element varied considerably depending on specific cell types and organisms. Studies in neuronal axons [13,14] and in insect cells [15] revealed that actin filaments could serve as tracks for mitochondrial transport. In higher plants it has been shown that mitochondria are closely associated with microfilaments and mitochondrial translocation is mainly dependent on intact microfilaments, in contrast to studies using yeast or animal cells [16,17,18,19]. Earlier studies revealed that actin filament dynamics are essential for many functions of the actin cytoskeleton, there are little data connecting actin dynamics and mitochondrial movements

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