Collective mitochondrial dynamics resolve conflicting cellular tensions: From plants to general principles

Chustecki, Joanna M.; Johnston, Iain G.

doi:10.1016/j.semcdb.2023.09.005

Cited by 4 publications

(4 citation statements)

References 172 publications

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“…Chen & Liu, 2014;Havey, 2004). Although hard to precisely quantify, CMS is involved in a substantial proportion, or majority, of the global production of many tabletop crop species (Chustecki & Johnston, 2024;Havey, 2004). In this sense, dysfunctional mtDNA genuinely helps feed the world.…”

Section: How Do Organisms Maintain the Function Of The Genes They Ret...mentioning

confidence: 99%

“…Famous examples in the Silene genus involve the mtDNA genome partitioned into dozens of chromosomes, some of which contain no functional content (Sloan et al, 2012;. These subgenomic molecules interact through recombination in a dynamic population (Albert et al, 1996;Atlan & Couvet, 1993;Johnston, 2019a), and individual mitochondria share mtDNA and its products through exchange on dynamic "social networks" in the cell (Arimura, 2018;Arimura et al, 2004;Chustecki et al, 2021;Chustecki & Johnston, 2024;Logan, 2010). When msh1, responsible for organelle DNA maintenance, is perturbed, the dynamics of this social exchange are altered to support more mtDNA sharing (Chustecki et al, 2022).…”

Section: Specific Strategies Across Eukaryotesmentioning

confidence: 99%

“…Chen et al, 2017). While detrimental to natural plants, CMS is of great use in agriculture, where sterile males support highyielding hybrid production (Bohra et al, 2016;Chustecki & Johnston, 2024;Havey, 2004).…”

Section: Specific Strategies Across Eukaryotesmentioning

confidence: 99%

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Evolution and maintenance of mtDNA gene content across eukaryotes

Veeraragavan,

Johansen,

Johnston

2024

Preprint

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

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Section: How Do Organisms Maintain the Function Of The Genes They Ret...mentioning

confidence: 99%

Section: Specific Strategies Across Eukaryotesmentioning

confidence: 99%

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Evolution and maintenance of mtDNA gene content across eukaryotes

Veeraragavan,

Johansen,

Johnston

2024

Preprint

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“…Across eukaryotes, gene content in mitochondrial DNA (mtDNA), and plastid DNA (ptDNA) have been dramatically reduced since the endosymbiotic events that created the organelles and now varies dramatically across species ( Keeling 2010 ; Smith and Keeling 2015 ; Johnston and Williams 2016 ; Janouškovec et al 2017 ; Roger et al 2017 ; Johnston and Burgstaller 2019 ; Mohanta et al 2020 ; Giannakis et al 2022 ). The genes retained in oDNA are of central importance in bioenergetics and metabolism, with impact from human diseases ( Taylor and Turnbull 2005 ; Wallace and Chalkia 2013 ; Stewart and Chinnery 2015 ) to crop production ( Havey 2004 ; Mackenzie 2010 ; Chen and Liu 2014 ; Chustecki and Johnston 2024 ). The question of why particular genes are retained across species has been studied for some time: hypotheses include the favoring of genes encoding products that are hard to import to the organelle after expression outside it ( von Heijne 1986 ; Björkholm et al 2015 ), genes that allow direct local control of organelle function ( Allen 2015 ; Allen and Martin 2016 ), are energetically favorable to retain ( Kelly 2021 ), and many more, reviewed and quantitatively compared in ( Johnston and Williams 2016 ; Giannakis et al 2022 ).…”

mentioning

confidence: 99%

Ecological Predictors of Organelle Genome Evolution: Phylogenetic Correlations with Taxonomically Broad, Sparse, Unsystematized Data

Giannakis,

Richards,

Johnston

2024

Systematic Biology

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Comparative analysis of variables across phylogenetically linked observations can reveal mechanisms and insights in evolutionary biology. As the taxonomic breadth of the sample of interest increases, challenges of data sparsity, poor phylogenetic resolution, and complicated evolutionary dynamics emerge. Here, we investigate a cross-eukaryotic question where all these problems exist: which organismal ecology features are correlated with gene retention in mitochondrial and chloroplast DNA (organelle DNA or oDNA). Through a wide palette of synthetic control studies, we first characterize the specificity and sensitivity of a collection of parametric and non-parametric phylogenetic comparative approaches to identify relationships in the face of such sparse and awkward datasets. This analysis is not directly focused on oDNA, and so provides generalizable insights into comparative approaches with challenging data. We then combine and curate ecological data coupled to oDNA genome information across eukaryotes, including a new semi-automated approach for gathering data on organismal traits from less systematized open-access resources including encyclopedia articles on species and taxa. The curation process also involved resolving several issues with existing datasets, including enforcing clade-specificity of several ecological features and fixing incorrect annotations. Combining this unique dataset with our benchmarked comparative approaches, we confirm support for several known links between organismal ecology and organelle gene retention, identify several previously unidentified relationships constituting possible ecological contributors to oDNA genome evolution, and provide support for a recently hypothesized link between environmental demand and oDNA retention. We, with caution, discuss the implications of these findings for organelle evolution and of this pipeline for broad comparative analyses in other fields.

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