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International audience; 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.

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?’

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.

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 short-read sequencing data, which 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.

BackgroundHow 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 wildArabidopsis thalianaaccessions to determine the rate of transposable element (TE) mobilization and its potential to create adaptive variation in natural settings.ResultsWe 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.ConclusionsOur study reveals that TE mobilization is a major generator of genetic variation inA. thalianathat 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.

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 leveraged whole-genome resequencing data of ∼300 individual Arabidopsis arenosa plants, a well characterized natural diploid-autotetraploid species, to address these questions. Based on 43,176 polymorphic TE insertions we detected 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 abiotic and biotic stress response genes. Notably, we uncovered one such insertion in a major flowering-time repressor gene and found that the resulting allele is specific to the rapid-cycling tetraploid lineage that colonized mainland railways. Together, our findings indicate that tetrasomy by itself leads to an enhanced tolerance to accumulating genic TE variants, some of which can potentially contribute to local adaptation.

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.

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., Nature Communications, 10 (1), ISSN:2041-1723

The duplication of an entire genome is no small affair. Whole genome duplication (WGD) is a dramatic mutation with long-lasting effects, yet it occurs repeatedly in all eukaryotic kingdoms. Plants are particularly rich in documented WGDs, with recent and ancient polyploidization events in all major extant lineages. However, challenges immediately following WGD, such as the maintenance of stable chromosome segregation or detrimental ecological interactions with diploid progenitors, commonly do not permit establishment of nascent polyploids. Despite these immediate issues some lineages nevertheless persist and thrive. In fact, ecological modeling commonly supports patterns of adaptive niche differentiation in polyploids, with young polyploids often invading new niches and leaving their diploid progenitors behind. In line with these observations of polyploid evolutionary success, recent work documents instant physiological consequences of WGD associated with increased dehydration stress tolerance in first-generation autotetraploids. Furthermore, population genetic theory predicts both short- and long-term benefits of polyploidy and new empirical data suggests that established polyploids may act as “sponges” accumulating adaptive allelic diversity. In addition to their increased genetic variability, introgression with other tetraploid lineages, diploid progenitors, or even other species, further increases the available pool of genetic variants to polyploids. Despite this, the evolutionary advantages of polyploidy are still questioned, and the debate over the idea of polyploidy as an evolutionary dead-end carries on. Here we broadly synthesize the newest empirical data moving this debate forward. Altogether, evidence suggests that if early barriers are overcome, WGD can offer instantaneous fitness advantages opening the way to a transformed fitness landscape by sampling a higher diversity of alleles, including some already preadapted to their local environment. This occurs in the context of intragenomic, population genomic, and physiological modifications that can, on occasion, offer an evolutionary edge. Yet in the long run, early advantages can turn into long-term hindrances, and without ecological drivers such as novel ecological niche availability or agricultural propagation, a restabilization of the genome via diploidization will begin the cycle anew.

PLoS Genetics, 14 (7), ISSN:1553-7390, ISSN:1553-7404

Human-generated ruderal habitats are abundant, but challenging for plants. Some ruderal habitats, however, provide networked corridors (e.g. roadsides and railways) that can facilitate rapid long-distance spread of successfully adapted variants. Here we use transcriptomic and genomic analyses, coupled with genetic mapping and transgenics to understand adaptation to railways inArabidopsis arenosa. We show normally perennialA.arenosaswitched to rapid cycling, a common adaptation for ruderal plants, at least twice upon railway colonization. We further show substantial gene flow from a widely distributed railway colonist likely contributed to secondary colonization by a non-ruderal type, highlighting how connectivity can affect adaptability. We find loss of expression of the reproductive repressorFLOWERING LOCUS C(FLC) is likely primarily responsible for rapid cycling in the widely distributed railway variant. However, a second railway colonist in the Alps also cycles rapidly, but retains highFLC. Some alleles in this population encode non-functional proteins, suggestingFLChas started to decay, but most are functional. Instead, this population likely circumvents FLC via a derived allele ofCONSTANS (CO), which shows strong evidence of selection in this population. Importantly, we find this CO allele arrived via gene flow from the widespread ruderal, where it was also previously under selection. This suggests ruderal adaptation may have been progressive, perhaps in both cases, with FLC-circumvention arising first, and FLC loss arising later but ultimately obscuring its earlier circumvention. These snapshots of railway adaptation highlight that gene flow from widespread ruderals can provide opportunities for subsequent adaptation by local genotypes.

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.