Fast co-evolution of anti-silencing systems shapes the invasiveness of Mu-like DNA transposons in eudicots.

Transposable elements (TEs) constitute a major threat to genome stability and are therefore typically silenced by epigenetic mechanisms. In response, some TEs have evolved counteracting systems to suppress epigenetic silencing. In the model plant Arabidopsis thaliana, two such anti-silencing systems have been identified and found to be mediated by the VANC DNA-binding proteins encoded by VANDAL transposons. Here, we show that anti-silencing systems have rapidly diversified since their origin in eudicots by gaining and losing VANC-containing domains, such as DUF1985, DUF287, and Ulp1, as well as target sequence motifs. We further demonstrate that these motifs determine anti-silencing specificity by sequence, density, and helical periodicity. Moreover, such rapid diversification yielded at least 10 distinct VANC-induced anti-silencing systems in Arabidopsis. Strikingly, anti-silencing of non-autonomous VANDALs, which can act as reservoirs of 24-nt small RNAs, is critical to prevent the demise of cognate autonomous TEs and to ensure their propagation. Our findings illustrate how complex co-evolutionary dynamics between TEs and host suppression pathways have shaped the emergence of new epigenetic control mechanisms.

Genetic basis and evolution of rapid cycling in railway populations of tetraploid Arabidopsis arenosa.

Spatially structured plant populations with diverse adaptations provide powerful models to investigate evolution. Human-generated ruderal habitats are abundant and low-competition, but are challenging for plants not adapted to them. Ruderal habitats also sometimes form networked corridors (e.g. roadsides and railways) that allow rapid long-distance spread of successfully adapted variants. Here we use transcriptomic and genomic analyses, coupled with genetic mapping and transgenic follow-up, to understand the evolution of rapid cycling during adaptation to railway sites in autotetraploid Arabidopsis arenosa. We focus mostly on a hybrid population that is likely a secondary colonist of a railway site. These mountain railway plants are phenotypically similar to their cosmopolitan cousins. We thus hypothesized that colonization primarily involved the flow of adaptive alleles from the cosmopolitan railway variant. But our data shows that it is not that simple: while there is evidence of selection having acted on introgressed alleles, selection also acted on rare standing variation, and new mutations may also contribute. Among the genes we show have allelic divergence with functional relevance to flowering time are known regulators of flowering, including FLC and CONSTANS. Prior implications of these genes in weediness and rapid cycling supports the idea that these are "evolutionary hotspots" for these traits. We also find that one of two alleles of CONSTANS under selection in the secondary colonist was selected from rare standing variation in mountain populations, while the other was introgressed from the cosmopolitan railway populations. The latter allele likely arose in diploid populations over 700km away, highlighting how ruderal populations could act as allele conduits and thus influence local adaptation.

Habitat-Associated Life History and Stress-Tolerance Variation in Arabidopsis arenosa.

Weediness in ephemeral plants is commonly characterized by rapid cycling, prolific all-in flowering, and loss of perenniality. Many species made transitions to weediness of this sort, which can be advantageous in high-disturbance or human-associated habitats. The molecular basis of this shift, however, remains mostly mysterious. Here, we use transcriptome sequencing, genome resequencing scans for selection, and stress tolerance assays to study a weedy population of the otherwise nonweedy Arabidopsis arenosa, an obligately outbreeding relative of Arabidopsis thaliana Although weedy A. arenosa is widespread, a single genetic lineage colonized railways throughout central and northern Europe. We show that railway plants, in contrast to plants from sheltered outcrops in hill/mountain regions, are rapid cycling, have lost the vernalization requirement, show prolific flowering, and do not return to vegetative growth. Comparing transcriptomes of railway and mountain plants across time courses with and without vernalization, we found that railway plants have sharply abrogated vernalization responsiveness and high constitutive expression of heat- and cold-responsive genes. Railway plants also have strong constitutive heat shock and freezing tolerance compared with mountain plants, where tolerance must be induced. We found 20 genes with good evidence of selection in the railway population. One of these, LATE ELONGATED HYPOCOTYL, is known in A. thaliana to regulate many stress-response genes that we found to be differentially regulated among the distinct habitats. Our data suggest that, beyond life history regulation, other traits like basal stress tolerance also are associated with the evolution of weediness in A. arenosa.

Population structure and coalescence in pedigrees: Comparisons to the structured coalescent and a framework for inference.

Contrary to what is often assumed in population genetics, independently segregating loci do not have completely independent ancestries, since all loci are inherited through a single, shared population pedigree. Previous work has shown that the non-independence between gene genealogies of independently segregating loci created by the population pedigree is weak in panmictic populations, and predictions made from standard coalescent theory are accurate for populations that are at least moderately sized. Here, we investigate patterns of coalescence in pedigrees of structured populations. We find that the pedigree creates deviations away from the predictions of the structured coalescent that persist on a longer timescale than in the case of panmictic populations. Nevertheless, we find that the structured coalescent provides a reasonable approximation for the coalescent process in structured population pedigrees so long as migration events are moderately frequent and there are no migration events in the recent pedigree of the sample. When there are migration events in the recent sample pedigree, we find that distributions of coalescence in the sample can be modeled as a mixture of distributions from different initial sample configurations. We use this observation to motivate a maximum-likelihood approach for inferring migration rates and mutation rates jointly with features of the pedigree such as recent migrant ancestry and recent relatedness. Using simulation, we show that our inference framework accurately recovers long-term migration rates in the presence of recent migration events in the sample pedigree.

The genetic basis of epigenetic variation and its consequences for adaptation.

Recent population genomic studies in plants have shed new light on natural epigenetic variation by identifying key genetic determinants, "trans modifiers," that influence epigenetic states genome-wide and their interplay with environmental factors. Here, we review this progress by focusing on the epigenetic control of transposition and life-cycle transitions to highlight the ecological consequences of this genetic architecture and its evolutionary significance. This knowledge provides new opportunities to address long-standing questions about the establishment of environment-associated epigenetic variation and its relevance in adaptation.

The epiallelic potential of transposable elements and its evolutionary significance in plants.

DNA provides the fundamental framework for heritability, yet heritable trait variation need not be completely 'hard-wired' into the DNA sequence. In plants, the epigenetic machinery that controls transposable element (TE) activity, and which includes DNA methylation, underpins most known cases of inherited trait variants that are independent of DNA sequence changes. Here, we review our current knowledge of the extent, mechanisms and potential adaptive contribution of epiallelic variation at TE-containing alleles in this group of species. For the purpose of this review, we focus mainly on DNA methylation, as it provides an easily quantifiable readout of such variation. The picture that emerges is complex. On the one hand, pronounced differences in DNA methylation at TE sequences can either occur spontaneously or be induced experimentally en masse across the genome through genetic means. Many of these epivariants are stably inherited over multiple sexual generations, thus leading to transgenerational epigenetic inheritance. Functional consequences can be significant, yet they are typically of limited magnitude and although the same epivariants can be found in nature, the factors involved in their generation in this setting remain to be determined. On the other hand, moderate DNA methylation variation at TE-containing alleles can be reproducibly induced by the environment, again usually with mild effects, and most of this variation tends to be lost across generations. Based on these considerations, we argue that TE-containing alleles, rather than their inherited epiallelic variants, are the main targets of natural selection. Thus, we propose that the adaptive contribution of TE-associated epivariation, whether stable or not, lies predominantly in its capacity to modulate TE mobilization in response to the environment, hence providing hard-wired opportunities for the flexible exploration of the phenotypic space. This article is part of the theme issue 'How does epigenetics influence the course of evolution?'

Jumpstarting evolution: How transposition can facilitate adaptation to rapid environmental changes.

Because of their ability to replicate across genomes, transposable elements (TEs) represent major generators of large-effect mutations. As a result, chromatin-based mechanisms have evolved to control the mutational potential of TEs at multiple levels, from the epigenetic silencing of TE sequences, through the modulation of their integration space, up to the alleviation of the impact of new insertions. Although most TE insertions are highly deleterious, some can provide key adaptive variation. Together with their remarkable sensitivity to the environment and precise integration preferences, the unique characteristics of TEs place them as potent genomic engines of adaptive innovation. Herein, we review recent works exploring the regulation and impact of transposition in nature and discuss their implications for the evolutionary response of species to drastic environmental changes.

Efficient Detection of Transposable Element Insertion Polymorphisms Between Genomes Using Short-Read Sequencing Data.

Transposable elements (TEs) are powerful generators of major-effect mutations, most of which are deleterious at the species level and maintained at very low frequencies within populations. As reference genomes can only capture a minor fraction of such variants, methods were developed to detect TE insertion polymorphisms (TIPs) in non-reference genomes from the short-read sequencing data that are becoming increasingly available. We present here a bioinformatic framework combining an improved version of the SPLITREADER and TEPID pipelines to detect non-reference TE presence and reference TE absence variants, respectively. We benchmark our method on ten non-reference Arabidopsis thaliana genomes and demonstrate its high specificity and sensitivity in the detection of TIPs between genomes.

Genetic and environmental modulation of transposition shapes the evolutionary potential of Arabidopsis thaliana.

BACKGROUND: How species can adapt to abrupt environmental changes, particularly in the absence of standing genetic variation, is poorly understood and a pressing question in the face of ongoing climate change. Here we leverage publicly available multi-omic and bio-climatic data for more than 1000 wild Arabidopsis thaliana accessions to determine the rate of transposable element (TE) mobilization and its potential to create adaptive variation in natural settings. RESULTS: We demonstrate that TE insertions arise at almost the same rate as base substitutions. Mobilization activity of individual TE families varies greatly between accessions, in association with genetic and environmental factors as well as through complex gene-environment interactions. Although the distribution of TE insertions across the genome is ultimately shaped by purifying selection, reflecting their typically strong deleterious effects when located near or within genes, numerous recent TE-containing alleles show signatures of positive selection. Moreover, high rates of transposition appear positively selected at the edge of the species' ecological niche. Based on these findings, we predict through mathematical modeling higher transposition activity in Mediterranean regions within the next decades in response to global warming, which in turn should accelerate the creation of large-effect alleles. CONCLUSIONS: Our study reveals that TE mobilization is a major generator of genetic variation in A. thaliana that is finely modulated by genetic and environmental factors. These findings and modeling indicate that TEs may be essential genomic players in the demise or rescue of native populations in times of climate crises.

Relaxed purifying selection in autopolyploids drives transposable element over-accumulation which provides variants for local adaptation.

Polyploidization is frequently associated with increased transposable element (TE) content. However, what drives TE dynamics following whole genome duplication (WGD) and the evolutionary implications remain unclear. Here, we leverage whole-genome resequencing data available for ~300 individuals of Arabidopsis arenosa, a well characterized natural diploid-autotetraploid plant species, to address these questions. Based on 43,176 TE insertions we detect in these genomes, we demonstrate that relaxed purifying selection rather than transposition bursts is the main driver of TE over-accumulation after WGD. Furthermore, the increased pool of TE insertions in tetraploids is especially enriched within or near environmentally responsive genes. Notably, we show that the major flowering-time repressor gene FLC is disrupted by a TE insertion specifically in the rapid-cycling tetraploid lineage that colonized mainland railways. Together, our findings indicate that tetrasomy leads to an enhanced accumulation of genic TE insertions, some of which likely contribute to local adaptation.

Pervasive population genomic consequences of genome duplication in Arabidopsis arenosa.

Ploidy-variable species allow direct inference of the effects of chromosome copy number on fundamental evolutionary processes. While an abundance of theoretical work suggests polyploidy should leave distinct population genomic signatures, empirical data remains sparse. We sequenced ~300 individuals from 39 populations of Arabidopsis arenosa, a naturally diploid-autotetraploid species. We find that the impacts of polyploidy on population genomic processes are subtle yet pervasive, such as reduced efficiency of purifying selection, differences in linked selection and rampant gene flow from diploids. Initial masking of deleterious mutations, faster rates of nucleotide substitution and interploidy introgression likely conspire to shape the evolutionary potential of polyploids.