Altered collective mitochondrial dynamics in the Arabidopsismsh1mutant compromising organelle DNA maintenance

Abstract

Mitochondria form highly dynamic populations in the cells of plants (and all eukaryotes). The characteristics and benefits of this collective behaviour, and how it is influenced by nuclear features, remain to be fully elucidated. Here, we use a recently developed quantitative approach to reveal and analyse the physical and collective "social" dynamics of mitochondria in an Arabidopsis msh1 mutant where organelle DNA maintenance machinery is compromised. We use a newly created line combining the msh1 mutant with mitochondrially-targeted GFP, and characterise mitochondrial dynamics with a combination of single-cell timelapse microscopy, computational tracking and network analysis. The collective physical behaviour of msh1 mitochondria is altered from wildtype in several ways: mitochondria become less evenly spread, and networks of inter-mitochondrial encounters become more connected with greater potential efficiency for inter-organelle exchange -- reflecting a potential compensatory mechanism for the genetic challenge to the mtDNA population, supporting more inter-organelle exchange. We find that these changes are similar to those observed in friendly, where mitochondrial dynamics are altered by a physical perturbation, suggesting that this shift to higher connectivity may reflect a general response to mitochondrial challenges, where physical dynamics of mitochondria may be altered to control the genetic structure of the mtDNA population.

Social networks in the single cell

“…Plant mitochondria undergo fission and fusion to form transient networks which could allow the exchange of genetic information. To test this hypothesis, Chustecki et al (2022) used msh1 mutants with defective DNA repair, and showed that mitochondrial interactions increased, revealing a link between the physical and genetic behavior of mitochondria.…”

“…In plants, MSH1, a MutS homolog, is a protein that plays a role in organellar genome maintenance, including homologous recombination ( Abdelnoor et al , 2003 ), and in msh1 mutants the mitochondrial mutations accumulate ( Wu et al , 2020 ). By analyzing mitochondrial dynamics in the msh1 mutant and comparing it with the wild type, Chustecki et al (2022) aimed to answer the question of whether mitochondria interact differently when they have compromised mtDNA integrity. Because mitochondria in msh1 mutants accumulate damage, the authors hypothesized that they would frequently interact with each other, possibly to acquire an intact template for homology-based DNA repair.…”

“…After demonstrating the altered physical behaviors of mitochondria in msh1 mutants, Chustecki et al (2022) also compared mitochondrial behavior in msh1 and friendly mutants. The FRIENDLY protein mediates inter-mitochondrial association, and friendly mutants exhibit a reduction in mitochondrial fusion and increased mitochondrial clustering ( El Zawily et al , 2014 ).…”

“…While Chustecki et al (2022) have answered the question of whether mitochondria physically interact within a cell in response to mtDNA damage, questions remain, and new ones arise. Although they showed that mitochondrial social interactions increase with genetic perturbations, presumably to share contents including DNA repair templates, it still needs to be shown directly that interacting mitochondria are exchanging and replicating DNA.…”

“…Ovules must contain complete and intact copies of the mitochondrial genome—how is this accomplished, and are there checkpoints to signal the nucleus that the mitochondria are ready to be transmitted to progeny? The findings of Chustecki et al (2022) open the door to further understanding of how plants accurately transmit mitochondrial DNA to their progeny.…”