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JOURNALS - JXB
NETWORKING IS A SECRET TO SUCCESS FOR PLANT MITOCHONDRIA JOURNAL OF EXPERIMENTAL BOTANY BY MAREIKE JEZEK
Joanna M. Chustecki, Ross D. Etherington, Daniel J. Gibbs, Ian G. Johnstone. Altered collective mitochondrial dynamics in the Arabidopsis msh1 mutant compromising organelle DNA maintenance. Journal of Experimental Botany 2022; 73: 5428–5439. https://doi.org/10.1093/jxb/ erac250
The endosymbiosis between an ancient bacterium and its host cell that led to the evolution of mitochondria was one of the most fundamental landmark events in the history of life on Earth. Instead of digesting the engulfed bacteria, the first eukaryotic cells ascertained that interaction and cooperation with the symbionts was of mutual benefit. Equipped with energy-providing internal companions, they were able to gradually evolve into more complex multicelled organisms.
Production of ATP is still the most prominent cellular function of mitochondria, yet they have adopted several other tasks, especially in the plant lineage of eukaryotic life. Here, further endosymbiosis with a cyanobacterium gave rise to an additional energy-transforming organelle, the chloroplast. These organelles are both a blessing and a curse. Chloroplasts enable plants to convert sunlight into chemical energy, but photosynthesis often generates a surplus of reductants, and photorespiration produces harmful byproducts, which can impair photosynthetic performance and lead to oxidative stress. Plant mitochondria are therefore equipped with several mechanisms to balance the cellular redox status and to participate in detoxifying photorespiratory metabolites. They are furthermore essential for the assimilation of inorganic nitrogen, given that the citric acid cycle provides biosynthetic precursors for amino acid synthesis.
Plant and animal mitochondria do not only in their functional repertoire. Unlike in animal cells, where mitochondria often fuse into elongated tube-like structures, plant mitochondria usually retain their individual existence and are akin to their bacterial ancestors in shape and form. The mitochondrial genome in plants is remarkably large, containing long stretches of non-coding elements, and shows a high recombination rate. Because mitochondria are major sites of reactive oxygen species production and replicate frequently, their genome is prone to DNA damage. The very low rate of point mutations found in plant mitochondrial DNA (mtDNA), however, indicates efficient DNA repair, for example, via homologous recombination. For this, an undamaged DNA template is required, which may be provided by another mitochondrion. Mitochondria are not static and the chondriome, the entirety of mitochondria within one cell, resembles a busy beehive with mitochondria swiftly swarming through the cytosol and frequently interacting with one another. However, very little is known about the benefits and orchestration of this energy-consuming movement. Joanna Chustecki from the University of Birmingham and her colleagues from the mitochondrial and chloroplast research project EvoConBiO, led by Iain Johnston at the University of Bergen, want to shed light on the social behaviour of the chondriome, both literally and figuratively. They use single-cell time-lapse microscopy to track the motions of fluorescently labelled mitochondria to reconstruct, quantify and analyse encounter networks of the organelles over time. Their latest findings have been published in the Journal of Experimental Botany (Chustecki et al., 2022) and indicate that mitochondria face a spatial dilemma created by the twin pressures of their genetic integrity and their function within the cell. On the one hand, meeting and interacting with other mitochondria enables exchange of biomolecules, for example mtDNA for homology-based DNA repair. On the other hand, even distribution of mitochondria throughout the cell ensures equal energy supply. Also, prolonged gathering of many mitochondria in the same space could lead to a build-up of harmful substances such as reactive oxygen species, and it reduces their accessibility for other cellular components. Therefore, the authors speculate that mitochondria aim to maximise the number of encounters with others while also remaining evenly spread through the cell – a tension they resolve with their motion. To test this, the authors compared the mitochondrial dynamics between Arabidopsis wildtype plants and msh1 mutants with compromised organelle DNA repair that accumulate increased mtDNA damage. Chustecki and colleagues hypothesised that mitochondria in these mutants would consequently be more ‘social’ and interact more frequently, possibly to exchange undamaged template DNA. The team did indeed measure decreased distance and increased colocalisation time of the mutant mitochondria. The observations in msh1 are similar to mitochondrial dynamics in Arabidopsis-friendly mutants, in which mitochondrial motility is disrupted, leading to increased mitochondria clustering. From this the authors conclude that both genetic and physical challenges alter the chondriome dynamics and increase the mitochondrial network connectivity at the cost of physical spacing.
The American evolutionary biologist Lynn Margulis, one of the earliest and most fervent proponents of the endosymbiotic theory, wrote ‘Life did not take over the globe by combat, but by networking’1 to emphasise the importance of cooperation and communication that ultimately led to the evolution from endosymbiotic bacterium to organellar mitochondrion. Modern-day plant mitochondria seem to stick to this secret to success of their ancestral progenitors, and the work by Chustecki and colleagues brings us one step closer to understanding the underlying mechanisms of the mitochondrial bustling. Their paper in JXB is accompanied by an Insight article in which the connection between mitochondrial interaction and homologous DNA repair is explained and beautifully illustrated.2
Chustecki and colleagues use time-lapse microscopy and computational tracking of fluorescently labelled mitochondria within a single cell (left) to reconstruct and analyse encounter networks (right) Image credit: Joanna Chustecki
Reference:
1. Margulis L, Sagan D. Marvellous microbes. Resurgence 2001; 206: 10–12. 2. Rodriguez M, Martinez-Hottovy A, Christensen AC. Social networks in the single cell. J Exp Bot 2022; 73: 5355–5357.
CHRISTMAS LECTURES 2022
CHRISTMAS LECTURES 2022
LECTURES:
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14 DECEMBER 2022, 2PM – 3PM GMT ONLINE
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15 DECEMBER 2022, 1PM – 2PM GMT, ONLINE
Speaker: Dr Luiza Teixeira-Costa
2022 - 2024 ImpACT Postdoctoral Fellow, Vrije Universiteit Brussel
