Mitochondrial movement during its association with chloroplasts in Arabidopsis thaliana

Kazusato Oikawa,Kiminori Toyooka,Keiji Numata,Yutaka Kodama,Chonprakun Thagun,Kazuya Ishikawa,Takuto Imai,Takeshi Yoshizumi

doi:10.1038/s42003-021-01833-8

Abstract

Plant mitochondria move dynamically inside cells and this movement is classified into two types: directional movement, in which mitochondria travel long distances, and wiggling, in which mitochondria travel short distances. However, the underlying mechanisms and roles of both types of mitochondrial movement, especially wiggling, remain to be determined. Here, we used confocal laser-scanning microscopy to quantitatively characterize mitochondrial movement (rate and trajectory) in Arabidopsis thaliana mesophyll cells. Directional movement leading to long-distance migration occurred at high speed with a low angle-change rate, whereas wiggling leading to short-distance migration occurred at low speed with a high angle-change rate. The mean square displacement (MSD) analysis could separate these two movements. Directional movement was dependent on filamentous actin (F-actin), whereas mitochondrial wiggling was not, but slightly influenced by F-actin. In mesophyll cells, mitochondria could migrate by wiggling, and most of these mitochondria associated with chloroplasts. Thus, mitochondria migrate via F-actin-independent wiggling under the influence of F-actin during their association with chloroplasts in Arabidopsis.

Highlights

Plant mitochondria move dynamically inside cells and this movement is classified into two types: directional movement, in which mitochondria travel long distances, and wiggling, in which mitochondria travel short distances
To evaluate mitochondrial motility in single plant cells, we examined protoplasts isolated from the mesophyll cells of transgenic plant leaves
Many studies have reported that mitochondria cease their directional movement when treated with filamentous actin (F-actin)-disrupting drugs[12,13,14,15], but they continue to exhibit wiggling in various cell types in several plant species[12,13,14]

Summary

Introduction

Plant mitochondria move dynamically inside cells and this movement is classified into two types: directional movement, in which mitochondria travel long distances, and wiggling, in which mitochondria travel short distances. Mitochondria migrate via F-actin-independent wiggling under the influence of F-actin during their association with chloroplasts in Arabidopsis. During treatment with F-actin-disrupting drugs, F-actin-independent wiggling of mitochondria was observed[12,13] This wiggling has been referred to as “Brownian movement” or “Brownian motion” in previous reports[14,15]. Mitochondrial wiggling has been observed in many previous studies, the characteristics of this wiggling remain to be described in detail Mitochondria lose their motility under long-term illumination with weak blue light at levels that activate chloroplast metabolism, suggesting that mitochondrial motility is reduced through their association with chloroplasts whose metabolism is activated[16]. We quantitatively characterized two types of mitochondrial movement, directional movement and wiggling of mitochondria, using time-lapse video recording of over 1000 mitochondria in transgenic A. thaliana protoplasts and leaf palisade mesophyll cells. Frequency analysis indicated that the mitochondria moved at various speeds from 0.05 to 1.00 μm s−1 (Fig. 1d)

Methods

Results

Conclusion