Mitochondrial fusion, division and positioning in plants

Abstract

Mitochondria are involved in many fundamental processes underpinning plant growth, development and death. Owing to their multiple roles, as the sites of the tricarboxylic acid cycle and oxidative phosphorylation, as harbourers of their own genomes and as sensors of cell redox status, amongst others, mitochondria are in a unique position to act as sentinels of cell physiology. The plant chondriome is typically organized as a population of physically discrete organelles, but visualization of mitochondria in living tissues has shown that the mitochondrial population is highly interactive. Mitochondria are highly motile and movement on the cytoskeleton ensures that the physically discrete organelles come into contact with one another, which allows transient fusion, followed by division of the mitochondrial membranes. This article serves to review our current knowledge of mitochondrial fusion and division, and link this to recent discoveries regarding a putative mitochondrial 'health-check' and repair process, whereby non-repairable dysfunctional mitochondria can be removed from the chondriome. It is proposed that the unequal distribution of the multipartite plant mitochondrial genome between discrete organelles provides the driver for transient mitochondrial fusion that, in turn, is dependent on mitochondrial motility, and that both fusion and motility are necessary to maintain a healthy functional chondriome.

FRIENDLY Regulates Mitochondrial Distribution, Fusion, and Quality Control in Arabidopsis

“…Regulation of mitochondrial movement and position within the cytosol has been demonstrated to be essential for correct mitochondrial and cellular function (Boldogh and Pon, 2007;Frederick and Shaw, 2007;Logan, 2010b;Shutt and McBride, 2013). Moreover, mitochondria display altered motility and distribution under stress conditions, or when their function is impaired, in a variety of cell types across diverse eukaryote lineages (Chen and Chan, 2009;Nunnari and Suomalainen, 2012).…”

“…This heterogeneity led to the plant chondriome being termed a dynamic syncytium (Lonsdale et al, 1988) or a discontinuous whole (Logan, 2006) to describe the functional interdependence of the physically discrete organelles. This interdependence has been suggested to drive a need to meet, such that there is a requirement for mitochondria to be mobile so that they can associate with and then fuse with one another to enable the transfer of mtDNA (Logan, 2010b).…”

“…The fundamental differences in the structure of plant and nonplant chondriomes and the lack of conservation of genes, identified to date, as involved in mitochondrial fusion (Logan, 2003(Logan, , 2010b led one of us to perform a microscopy-based screen to identify Arabidopsis (Arabidopsis thaliana) mutants with disrupted chondriome structure with the goal of discovering genes involved in plant mitochondrial fusion and plant-specific genes involved in plant mitochondrial fission . One of the mutants, called friendly (or friendly mitochondria), was identified due to the presence of large clusters of mitochondria rather than the homogenous distribution of mitochondria in the wild type .…”

Cell-to-cell movement of mitochondria in plants

“…Reconstruction of events that leads to formation of chimeric mitochondrial genomes in cells adjacent to graft junctions is complicated by the propensity of mitochondria for fusion (16,23,24). The mtDNA may move as naked DNA, or inside an organelle, but when heterologous mitochondrial genomes are present in a mixed cytoplasm, the mtDNA recombines (25)(26)(27).…”

“…For chromosomes 8, 12, 14, and 16, the PCR program of 94°C for 5 min; 37 cycles of 94°C for 20 s, 54°C for 20 s, 72°C for 1 min; 72°C for 10 min was used. The PCR products were ran on a 2.5% (wt/vol) TAE agarose gel for chromosomes 8,14,[16][17][18], and 20 and on a 5% (wt/vol) MetaPhor agarose (Lonza) gel for chromosomes 1-7, 9-13, 15, 19, and 21-24.…”