Universal features shaping organelle gene retention

Giannakis, Konstantinos; Arrowsmith, Samuel J.; Richards, Luke; Gasparini, Sara; Chustecki, Joanna M.; Røyrvik, Ellen C.; Johnston, Iain G.

doi:10.1101/2021.10.27.465964

Cited by 7 publications

(11 citation statements)

References 72 publications

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“…In correcting for systematic differences in gene count between deep-branching clades (Giannakis et al 2022;Janouškovec et al 2017) and additionally for the phylogenetic relationship between samples, we have attempted to align with the picture in (Maddison and FitzJohn 2015), of both identifying independent subsets of data and then accounting "internally" for phylogenetic signal. However, how best to account for dependencies across phylogenetically-embedded data is a topic of substantial discussion (Uyeda, Zenil-Ferguson, and Pennell 2018;Losos 2011); even well-principled comparative methods have shortcomings in the face of singular evolutionary events (Uyeda, Zenil-Ferguson, and Pennell 2018) and imperfect phylogenetic estimates (as we have here) and the distinction between pattern and process can challenge the application of these methods (Losos 2011)discussed further in an oDNA context in (Giannakis, Richards, and Johnston 2023). In taking different combinations of clade-based and phylogenetic correction, and considering different subtrees of our data, we have attempted to be robust to particular choices of method.…”

Section: Discussionmentioning

confidence: 98%

“…Following findings in (Giannakis, Richards, and Johnston 2023), aligned with the features that most broadly distinguished entries in our dataset, we tested for differences between organisms with different characteristics: algae, unicellularity, green plants/algae, herbaceousness, annual/perennial lifestyle. For clade-corrected oDNA counts (ΔMT and ΔPT), a linear mixed model with random and gradients assigned to the algal category was slightly favoured by AIC over the fixed linear model (1154.7 vs 1157.5 for the fixed model).…”

Section: Ecological and Species-specific Factorsmentioning

confidence: 99%

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Connecting species-specific extents of genome reduction in mitochondria and plastids

Giannakis,

Richards,

Dauda

et al. 2023

Preprint

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Mitochondria and plastids have both dramatically reduced their genomes since the endosymbiotic events that created them. The similarities and differences in the evolution of the two organelle genome types has been the target of discussion and investigation for decades. Ongoing work has suggested that similar mechanisms may modulate the reductive evolution of the two organelles in a given species, but quantitative data and statistical analyses exploring this picture remain limited outside of some specific cases like parasitism. Here, we use cross-eukaryote organelle genome data to explore evidence for coevolution of mitochondrial and chloroplast genome reduction. Controlling for differences between clades and pseudoreplication due to relatedness, we find that mtDNA and ptDNA gene retention are related across taxa, in a generally positive correlation that appears to differ quantitatively across eukaryotes, for example, between algal and non-algal species. We find limited evidence for coevolution of specific mtDNA and ptDNA gene pairs, suggesting that the similarities between the two organelle types may be due mainly to independent responses to consistent evolutionary drivers.

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Section: Discussionmentioning

confidence: 98%

Section: Ecological and Species-specific Factorsmentioning

confidence: 99%

Connecting species-specific extents of genome reduction in mitochondria and plastids

Giannakis,

Richards,

Dauda

et al. 2023

Preprint

Self Cite

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“…Hence, organisms experiencing highly variable bioenergetic and metabolic demands from their environment would retain more oDNA genes, and those experiencing lower and more stable demands would retain fewer. This picture is supported to some extent by mathematical modeling ( García-Pascual et al 2022 ) and comparative analysis of links between ecological traits and oDNA gene counts ( Giannakis et al 2023 )—although we must point out that this picture does not and probably cannot explain the full diversity of oDNA retention profiles across eukaryotes. Although this theoretical picture predicts that similar factors shape—to some extent—mtDNA and ptDNA evolution, this prediction has to our knowledge yet to be tested with data.…”

Section: Introductionmentioning

confidence: 99%

Connecting Species-Specific Extents of Genome Reduction in Mitochondria and Plastids

Giannakis,

Richards,

Dauda

et al. 2024

Molecular Biology and Evolution

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Mitochondria and plastids have both dramatically reduced their genomes since the endosymbiotic events that created them. The similarities and differences in the evolution of the two organelle genome types has been the target of discussion and investigation for decades. Ongoing work has suggested that similar mechanisms may modulate the reductive evolution of the two organelles in a given species, but quantitative data and statistical analyses exploring this picture remain limited outside of some specific cases like parasitism. Here, we use cross-eukaryote organelle genome data to explore evidence for coevolution of mitochondrial and chloroplast genome reduction. Controlling for differences between clades and pseudoreplication due to relatedness, we find that extents of mtDNA and ptDNA gene retention are related to each other across taxa, in a generally positive correlation that appears to differ quantitatively across eukaryotes, for example, between algal and non-algal species. We find limited evidence for coevolution of specific mtDNA and ptDNA gene pairs, suggesting that the similarities between the two organelle types may be due mainly to independent responses to consistent evolutionary drivers.

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“…Intergenomic coevolution between the nucleus and organelle(s) is a common feature among eukaryotes. Gene loss and transfers to the nucleus have greatly reduced the coding regions of modern mitochondrial and plastid genomes to a limited number of essential genes ( Greiner and Bock 2013 ; Budar and Mireau 2018 ; Giannakis et al 2021 ). Consequently, these organelles must coordinate transcripts and protein products from 2 or more different genomic compartments to carry out essential cellular functions.…”

Section: Introductionmentioning

confidence: 99%

Variation in cytonuclear expression accommodation among allopolyploid plants

et al. 2022

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Cytonuclear coevolution is a common feature among plants, which coordinates gene expression and protein products between the nucleus and organelles. Consequently, lineage-specific differences may result in incompatibilities between the nucleus and cytoplasm in hybrid taxa. Allopolyploidy is also a common phenomenon in plant evolution. The hybrid nature of allopolyploids may result in cytonuclear incompatibilities, but the massive nuclear redundancy created during polyploidy affords additional avenues for resolving cytonuclear conflict (i.e., cytonuclear accommodation). Here we evaluate expression changes in organelle-targeted nuclear genes for six allopolyploid lineages that represent four genera (i.e., Arabidopsis, Arachis, Chenopodium, and Gossypium) and encompass a range in polyploid ages. Because incompatibilities between the nucleus and cytoplasm could potentially result in biases toward the maternal homoeolog and/or maternal expression level, we evaluate patterns of homoeolog usage, expression bias, and expression-level dominance in cytonuclear genes relative to the background of non-cytonuclear expression changes and to the diploid parents. Although we find subsets of cytonuclear genes in most lineages that match our expectations of maternal preference, these observations are not consistent among either allopolyploids or categories of organelle-targeted genes. Our results indicate that cytonuclear expression evolution may be subtle and variable among genera and genes, likely reflecting a diversity of mechanisms to resolve nuclear-cytoplasmic incompatibilities in allopolyploid species.

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Universal features shaping organelle gene retention

Cited by 7 publications

References 72 publications

Connecting species-specific extents of genome reduction in mitochondria and plastids

Connecting species-specific extents of genome reduction in mitochondria and plastids

Connecting Species-Specific Extents of Genome Reduction in Mitochondria and Plastids

Variation in cytonuclear expression accommodation among allopolyploid plants

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