Ben P Williams | bioRxiv Science

bioRxiv2016

Evolutionary inference across eukaryotes identifies specific pressures favoring mitochondrial gene retention

Since their endosymbiotic origin, mitochondria have lost most of their genes. Despite the central cellular importance of mtDNA, selective mechanisms underlying the evolution of its content across eukaryotes remain contentious, with no data-driven exploration of different hypotheses. We developed HyperTraPS, a powerful methodology coupling stochastic modelling with Bayesian inference to identify the ordering and causes of evolutionary events. Using a large dataset from over 2000 complete mitochondrial genomes, we inferred evolutionary trajectories of mtDNA gene loss across the eukaryotic tree of life. We find that proteins fulfilling central energetic roles in the assembly of mitochondrial complexes are prefentially retained in mitochondria across eukary-otes, biophysically supporting colocalization for redox regulation. We also provide the first quantitative evidence that a combination of GC content and protein hydrophobicity is required to explain mtDNA gene retention, and predicts the success of artificial gene transfer experiments. Our results demonstrate that a combination of these three characteristics explains most mtDNA gene variability, addressing the long-debated question of why particular genes are retained in mitochondrial genomes.

Evolutionary Biology↗

bioRxiv2015

Methylation-sensitive expression of a DNA demethylase gene serves as an epigenetic rheostat

Genomes must balance active suppression of transposable elements (TEs) with the need to maintain gene expression. In Arabidopsis, euchromatic TEs are targeted by RNA-directed DNA methylation (RdDM). Conversely, active DNA demethylation prevents accumulation of methylation at genes proximal to these TEs. It is unknown how a cellular balance between methylation and demethylation activities is achieved. Here we show that both RdDM and DNA demethylation are highly active at a TE proximal to the major DNA demethylase gene ROS1. Unexpectedly, and in contrast to most other genomic targets, expression of ROS1 is promoted by DNA methylation and antagonized by DNA demethylation. We demonstrate that inducing methylation of the ROS1 proximal region is sufficient to restore ROS1 expression in an RdDM mutant. Additionally, methylation-sensitive expression of ROS1 is conserved in other species, suggesting it is adaptive. We propose that the ROS1 locus functions as an epigenetic rheostat, tuning the level of demethylase activity in response to methylation alterations, thus ensuring epigenomic stability.\n\nAuthor SummaryOrganisms must adapt to dynamic and variable internal and external environments. Maintaining homeostasis in core biological processes is crucial to minimizing the deleterious consequences of environmental fluctuations. Genomes are also dynamic and variable, and must be robust against stresses, including the invasion of genomic parasites, such as transposable elements (TEs). In this work we present the discovery of an epigenetic rheostat in plants that maintains homeostasis in levels of DNA methylation. DNA methylation typically silences transcription of TEs. Because there is positive feedback between existing and de novo DNA methylation, it is critical that methylation is not allowed to spread and potentially silence transcription of genes. To maintain homeostasis, methylation promotes the production of a demethylase enzyme that removes methylation from gene-proximal regions. The demethylation of genes is therefore always maintained in concert with the levels of methylation suppressing TEs. In addition, this DNA demethylating enzyme also represses its own production in a negative feedback loop. Together, these feedback mechanisms shed new light into how the conflict between gene expression and genome defense is maintained in homeostasis. The presence of this rheostat in multiple species suggests it is an evolutionary conserved adaptation.

Genetics↗