Dynamics of organelle DNA segregation inArabidopsisdevelopment and reproduction revealed with tissue-specific heteroplasmy profiling and stochastic modelling DOI Creative Commons
Amanda K. Broz, Daniel B. Sloan, Iain G. Johnston

et al.

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2022, Volume and Issue: unknown

Published: Nov. 8, 2022

Abstract Organelle DNA (oDNA) in mitochondria and plastids is vital for plant (and eukaryotic) life. Selection against damaged oDNA mediated part by segregation – the sorting of different types into cells germline. Plants segregate very rapidly, with recombination protein MutS Homolog 1 (MSH1), a key driver this segregation, but contrast to mammals, we have limited knowledge dynamics within plants between generations. Here, combine stochastic modelling tissue-specific heteroplasmy measurements reveal trajectories Arabidopsis thaliana development reproduction. We obtain use new experimental observations through confirm refine predictions theory inferred from existing measurements. Ongoing proceeds gradually continually during development, more rapid increase inflorescence formation establishment next generation. When MSH1 compromised, show that majority observed could be achieved partitioning at cell divisions. functional, mtDNA far than can divisions; increased gene conversion plausible mechanism quantitatively explaining acceleration. also discuss support models germline provided these observations.

Language: Английский

Subcellular visualization: Organelle-specific targeted drug delivery and discovery DOI
Xintian Shao,

Caicai Meng,

Wenjing Song

et al.

Advanced Drug Delivery Reviews, Journal Year: 2023, Volume and Issue: 199, P. 114977 - 114977

Published: June 28, 2023

Language: Английский

Citations

38

Genome copy number predicts extreme evolutionary rate variation in plant mitochondrial DNA DOI Creative Commons

Kendra D. Maclaine,

Lydia G. Tressel, Zhiqiang Wu

et al.

Proceedings of the National Academy of Sciences, Journal Year: 2024, Volume and Issue: 121(10)

Published: March 1, 2024

Nuclear and organellar genomes can evolve at vastly different rates despite occupying the same cell. In most bilaterian animals, mitochondrial DNA (mtDNA) evolves faster than nuclear DNA, whereas this trend is generally reversed in plants. However, some exceptional angiosperm clades, mtDNA substitution have increased up to 5,000-fold compared with closely related lineages. The mechanisms responsible for acceleration are unknown. Because plants rely on homologous recombination repair damage, we hypothesized that copy numbers may predict evolutionary rates, as lower provide fewer templates such mechanisms. support of hypothesis, found number explains 47% variation synonymous across 60 diverse seed plant species representing ~300 million years evolution. Copy was also negatively correlated mitogenome size, which be a cause or consequence mutation rate variation. Both relationships were unique not observed plastid DNA. These results suggest recombinational plays role driving explain evolution more broadly eukaryotes. Our findings contribute broader questions about between genome selection efficiency, drift-barrier hypothesis.

Language: Английский

Citations

14

Sorting of mitochondrial and plastid heteroplasmy in Arabidopsis is extremely rapid and depends on MSH1 activity DOI Creative Commons
Amanda K. Broz, Alexandra Keene, Matheus Fernandes Gyorfy

et al.

Proceedings of the National Academy of Sciences, Journal Year: 2022, Volume and Issue: 119(34)

Published: Aug. 15, 2022

The fate of new mitochondrial and plastid mutations depends on their ability to persist spread among the numerous organellar genome copies within a cell (heteroplasmy). extent which heteroplasmies are transmitted across generations or eliminated through genetic bottlenecks is not well understood in plants, part because low mutation rates make these variants so infrequent. Disruption MutS Homolog 1 ( MSH1 ), gene involved plant DNA repair, results de novo point mutations, we used quantitatively track inheritance single nucleotide genomes Arabidopsis . We found that heteroplasmic sorting (the fixation loss variant) was rapid for both organelles, greatly exceeding observed animals. In msh1 mutants, sorted faster than those mitochondria were typically fixed lost generation. Effective transmission bottleneck sizes N ) plastids ∼ 4, respectively. Restoring function further increased rate 1.3), potentially its hypothesized role promoting conversion as mechanism expected homogenize cell. Heteroplasmic also favored GC base pairs. Therefore, recombinational repair can accelerate elimination bias outcome this process.

Language: Английский

Citations

33

Exchange on dynamic encounter networks allows plant mitochondria to collect complete sets of mitochondrial DNA products despite their incomplete genomes DOI Creative Commons
Konstantinos Giannakis, Joanna M. Chustecki, Iain G. Johnston

et al.

Quantitative Plant Biology, Journal Year: 2022, Volume and Issue: 3

Published: Jan. 1, 2022

Mitochondria in plant cells usually contain less than a full copy of the mitochondrial DNA (mtDNA) genome. Here, we asked whether dynamics may allow individual mitochondria to 'collect' set mtDNA-encoded gene products over time, by facilitating exchange between individuals akin trade on social network. We characterise collective Arabidopsis hypocotyl using recent approach combining single-cell time-lapse microscopy, video analysis and network science. use quantitative model predict capacity for sharing genetic information through networks encounters mitochondria. find that biological encounter support emergence product sets time more readily range other possible structures. Using results from combinatorics, identify statistics determine this propensity, discuss how features observed biology facilitate collection products.

Language: Английский

Citations

21

Stochastic organelle genome segregation through Arabidopsis development and reproduction DOI Creative Commons
Amanda K. Broz, Daniel B. Sloan, Iain G. Johnston

et al.

New Phytologist, Journal Year: 2023, Volume and Issue: 241(2), P. 896 - 910

Published: Nov. 5, 2023

Summary Organelle DNA (oDNA) in mitochondria and plastids is vital for plant (and eukaryotic) life. Selection against damaged oDNA mediated part by segregation – sorting different types into cells the germline. Plants segregate very rapidly, with recombination protein MSH1 a key driver of this segregation, but we have limited knowledge dynamics within plants between generations. Here, reveal how evolves through Arabidopsis thaliana development reproduction. We combine stochastic modelling, Bayesian inference, model selection new existing tissue‐specific measurements from heteroplasmic lines Segregation proceeds gradually continually during development, more rapid increase inflorescence formation next generation. When compromised, majority observed can be achieved partitioning at cell divisions. functional, mtDNA far rapid; show that increased gene conversion plausible mechanism quantitatively explaining acceleration. These findings quantitative, time‐dependent details Arabidopsis. also discuss support models germline provided these observations.

Language: Английский

Citations

12

Expansion of the MutS gene family in plants DOI
Daniel B. Sloan, Amanda K. Broz, Shady A Kuster

et al.

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: July 20, 2024

The

Language: Английский

Citations

4

Evolution and maintenance of mtDNA gene content across eukaryotes DOI Creative Commons
Shibani Veeraragavan, Maria Vang Johansen, Iain G. Johnston

et al.

Biochemical Journal, Journal Year: 2024, Volume and Issue: 481(15), P. 1015 - 1042

Published: Aug. 5, 2024

Across eukaryotes, most genes required for mitochondrial function have been transferred to, or otherwise acquired by, the nucleus. Encoding in nucleus has many advantages. So why do mitochondria retain any at all? Why does set of mtDNA vary so much across different species? And how species maintain functionality they retain? In this review, we will discuss some possible answers to these questions, attempting a broad perspective eukaryotes. We hope cover interesting features which may be less familiar from particular species, including ubiquity recombination outside bilaterian animals, encrypted chainmail-like mtDNA, single split over multiple chromosomes, triparental inheritance, gene transfer by grafting, gain factors, social networks mitochondria, and role dysfunction feeding world. unifying picture where organismal ecology gene-specific together influence whether organism X retains Y, development determine strategies, importantly recombination, are used that retained.

Language: Английский

Citations

3

Perception and processing of stress signals by plant mitochondria DOI Creative Commons
Jennifer Selinski, Stephanie Frings, Romy Schmidt

et al.

The Plant Journal, Journal Year: 2024, Volume and Issue: unknown

Published: Nov. 11, 2024

In the course of their life, plants continuously experience a wide range unfavourable environmental conditions in form biotic and abiotic stress factors. The perception via various organelles rapid, tailored cellular responses are essential for establishment plant resilience. Mitochondria as biosynthetic sites energy equivalents ATP-provided order to enable multitude biological processes cell-are often directly impacted by external At same time, mitochondrial function may fluctuate tolerable extent without need activate downstream retrograde signalling cascades adaptation. this Focus Review, we summarise current state knowledge on processing signals mitochondria show which layers signalling, that is, those involving transcription factors, metabolites, but also enzymes with moonlighting functions, communication nucleus. Also, light is shed signal integration between chloroplasts part signalling. With aim ways organelle-specific can be further researched collected data used long-term strengthen resilience context climate change.

Language: Английский

Citations

3

Asymmetric partitioning of persistent paternal mitochondria during cell divisions safeguards embryo development and mitochondrial inheritance DOI
Songyun Wang, Ding Xue

Developmental Cell, Journal Year: 2025, Volume and Issue: unknown

Published: Feb. 1, 2025

Language: Английский

Citations

0

Collective mitochondrial dynamics resolve conflicting cellular tensions: From plants to general principles DOI Creative Commons
Joanna M. Chustecki, Iain G. Johnston

Seminars in Cell and Developmental Biology, Journal Year: 2023, Volume and Issue: 156, P. 253 - 265

Published: Nov. 30, 2023

Mitochondria play diverse and essential roles in eukaryotic cells, plants are no exception. Plant mitochondria have several differences from their metazoan fungal cousins: they often exist a fragmented state, move rapidly on actin rather than microtubules, many plant-specific metabolic features roles, usually contain only subset of the complete mtDNA genome, which itself undergoes frequent recombination. This arrangement means that exchange complementation is for plant mitochondria, recent work has begun to reveal how collective dynamics resultant "social networks" encounters support this exchange, connecting time space. review will argue social network perspective can be extended "societal network", where mitochondrial an part interacting cellular society organelles biomolecules. Evidence emerging allow optimal resolutions competing priorities; we survey evidence potential future research directions, highlighting help test principles apply across other kingdoms life. In parallel with fundamental cell biology, also highlight translational "One Health" importance behaviour – exploited production vast amount crops consumed worldwide multi-objective optimisation understand rationally re-engineer evolved these tensions.

Language: Английский

Citations

6