Altered collective mitochondrial dynamics in the Arabidopsis \u3ci\u3emsh1\u3c/i\u3e mutant compromising organelle DNA maintenance

Mitochondria form highly dynamic populations in the cells of plants (and almost 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 the organelle DNA maintenance machinery is compromised. We use a newly created line combining the msh1 mutant with mitochondrially targeted green fluorescent protein (GFP), and characterize mitochondrial dynamics with a combination of single-cell time-lapse microscopy, computational tracking, and network analysis. The collective physical behaviour of msh1 mitochondria is altered from that of the wild type 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 mitochondrial DNA 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

Network analysis of Arabidopsis mitochondrial dynamics reveals a resolved tradeoff between physical distribution and social connectivity

Mitochondria in plant cells exist largely as individual organelles which move, colocalize, and interact, but the cellular priorities addressed by these dynamics remain incompletely understood. Here, we elucidate these principles by studying the dynamic "social networks" of mitochondria in Arabidopsis thaliana wildtype and mutants, describing the colocalization of individuals over time. We combine single-cell live imaging of hypocotyl mitochondrial dynamics with individual-based modeling and network analysis. We identify an inevitable tradeoff between mitochondrial physical priorities (an even cellular distribution of mitochondria) and "social" priorities (individuals interacting, to facilitate the exchange of chemicals and information). This tradeoff results in a tension between maintaining mitochondrial spacing and facilitating colocalization. We find that plant cells resolve this tension to favor efficient networks with high potential for exchanging contents. We suggest that this combination of physical modeling coupled to experimental data through network analysis can shed light on the fundamental principles underlying these complex organelle dynamics. A record of this paper's transparent peer review process is included in the supplemental information. [Abstract copyright: Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.

Evolutionary inference across eukaryotes identifies universal features shaping organelle gene retention

Mitochondria and plastids power complex life. Why some genes and not others are retained in their organelle DNA (oDNA) genomes remains a debated question. Here, we attempt to identify the properties of genes and associated underlying mechanisms that determine oDNA retention. We harness over 15k oDNA sequences and over 300 whole genome sequences across eukaryotes with tools from structural biology, bioinformatics, machine learning, and Bayesian model selection. Previously hypothesized features, including the hydrophobicity of a protein product, and less well-known features, including binding energy centrality within a protein complex, predict oDNA retention across eukaryotes, with additional influences of nucleic acid and amino acid biochemistry. Notably, the same features predict retention in both organelles, and retention models learned from one organelle type quantitatively predict retention in the other, supporting the universality of these features—which also distinguish gene profiles in more recent, independent endosymbiotic relationships. A record of this paper’s transparent peer review process is included in the supplemental information

Network analysis of Arabidopsis mitochondrial dynamics reveals a resolved tradeoff between physical distribution and social connectivity

Mitochondria in plant cells exist largely as individual organelles which move, colocalize, and interact, but the cellular priorities addressed by these dynamics remain incompletely understood. Here, we elucidate these principles by studying the dynamic "social networks" of mitochondria in Arabidopsis thaliana wildtype and mutants, describing the colocalization of individuals over time. We combine single-cell live imaging of hypocotyl mitochondrial dynamics with individual-based modeling and network analysis. We identify an inevitable tradeoff between mitochondrial physical priorities (an even cellular distribution of mitochondria) and “social” priorities (individuals interacting, to facilitate the exchange of chemicals and information). This tradeoff results in a tension between maintaining mitochondrial spacing and facilitating colocalization. We find that plant cells resolve this tension to favor efficient networks with high potential for exchanging contents. We suggest that this combination of physical modeling coupled to experimental data through network analysis can shed light on the fundamental principles underlying these complex organelle dynamics. A record of this paper’s transparent peer review process is included in the supplemental information

Altered collective mitochondrial dynamics in the Arabidopsis msh1 mutant compromising organelle DNA maintenance

Mitochondria form highly dynamic populations in the cells of plants (and almost 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 the organelle DNA maintenance machinery is compromised. We use a newly created line combining the msh1 mutant with mitochondrially targeted green fluorescent protein (GFP), and characterize mitochondrial dynamics with a combination of single-cell time-lapse microscopy, computational tracking, and network analysis. The collective physical behaviour of msh1 mitochondria is altered from that of the wild type 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 mitochondrial DNA 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.publishedVersio