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Giannakis, K.

Publications and source records attributed to Giannakis, K..

5 recordsLinked to original sources

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

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.

evolutionary biology↗

Ecological predictors of organelle genome evolution: Phylogenetic correlations with taxonomically broad, sparse, unsystematized data

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 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. We 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. 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.

evolutionary biology↗

Avoiding misleading estimates using mtDNA heteroplasmy statistics to study bottleneck size and selection

Mitochondrial DNA (mtDNA) heteroplasmy samples can shed light on vital developmental and genetic processes shaping mtDNA populations. The sample mean and sample variance of a set of heteroplasmy observations are typically used both to estimate bottleneck sizes and to perform fits to the theoretical "Kimura" distribution in seeking evidence for mtDNA selection. However, each of these applications raises problems. Sample statistics do not generally provide optimal fits to the Kimura distribution and so can give misleading results in hypothesis testing, including false positive signals of selection. Using sample variance can give misleading results for bottleneck size estimates, particularly for small samples. These issues can and do lead to false positive results for mtDNA mechanisms - all published experimental datasets we re-analysed, reported as displaying departures from the Kimura model, do not in fact give evidence for such departures. Here we outline a maximum likelihood approach that is simple to implement computationally and addresses all of these issues. We advocate the use of maximum likelihood fits and explicit hypothesis tests, not fits and Kolmogorov-Smirnov tests via summary statistics, for ongoing work with mtDNA heteroplasmy.

genetics↗

Universal features shaping organelle gene retention

Mitochondria and plastids power complex life, and retain their own organelle DNA (oDNA) genomes, with highly reduced gene contents compared to their endosymbiont ancestors. Why some protein-coding genes are retained in oDNA and some lost remains a debated question. Here we harness over 15k oDNA sequences and over 300 whole genome sequences with tools from structural biology, bioinformatics, machine learning, and Bayesian model selection to reveal the properties of genes, and associated underlying mechanisms, that shape oDNA evolution. Striking symmetry exists between the two organelle types: gene retention patterns in both are predicted by the hydrophobicity of a protein product and its energetic centrality within its protein complex, with additional influences of nucleic acid and amino acid biochemistry. Remarkably, retention principles from one organelle type successfully and quantitatively predict retention in the other, supporting this universality; these principles also distinguish gene profiles in independent endosymbiotic relationships. The identification of these features shaping organelle gene retention both provides quantitative support for several existing evolutionary hypotheses, and suggests new biochemical and biophysical mechanisms influencing organelle genome evolution.

evolutionary biology↗

Encounter networks from collective mitochondrial dynamics support the emergence of effective mtDNA genomes in plant cells

Mitochondria in plant cells form strikingly dynamic populations of largely individual organelles. Each mitochondrion contains on average less than a full copy of the mitochondrial DNA (mtDNA) genome. Here, we asked whether mitochondrial dynamics may allow individual mitochondria to collect a full copy of the mtDNA genome over time, by facilitating exchange between individuals. Akin to trade on a social network, exchange of mtDNA fragments across organelles may lead to the emergence of full effective genomes in individuals over time. We characterise the collective dynamics of mitochondria in Arabidopsis thaliana hypocotyl cells using a recent approach combining single-cell timelapse microscopy, video analysis, and network science. We then use a quantitative model to predict the capacity for the sharing and accumulation of genetic information through the networks of encounters between mitochondria. We find that biological encounter networks are strikingly well predisposed to support the collection of full genomes over time, outperforming a range of other networks generated from theory and simulation. Using results from the coupon collectors problem, we show that the upper tail of the degree distribution is a key determinant of an encounter networks performance at this task and discuss how features of mitochondrial dynamics observed in biology facilitate the emergence of full effective genomes.

plant biology↗