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

Pierre Baduel,Olivier Loudet,Vincent Colot,José Gil,Isabelle Gy,Basile Leduque,Leandro Quadrana,Amandine Ignace

doi:10.1186/s13059-021-02348-5

Abstract

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 wild Arabidopsis thaliana accessions 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 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.

Highlights

How species can adapt to abrupt environmental changes, in the absence of standing genetic variation, is poorly understood and a pressing question in the face of ongoing climate change
TE insertion polymorphisms (TIPs) are broadly distributed across the genome, with the notable exception of those produced by the GYPSY superfamily of long terminal repeats (LTRs) retrotransposons, which are enriched in pericentromeric regions
The site frequency spectrum (SFS) of TIPs, which we calculated using the number of informative genomes at each site, is heavily skewed towards low values compared to biallelic SNPs (Fig. 1c)

Summary

Introduction

How species can adapt to abrupt environmental changes, in the absence of standing genetic variation, is poorly understood and a pressing question in the face of ongoing climate change. Mutations typically arise at low rates and produce neutral variants predominantly This picture ignores sequence alterations generated by the mobilization of transposable elements (TEs), which have many properties that distinguish them from “classical,” smallsize mutations. Eukaryotic TEs belong to two broad classes: DNA transposons, which use a cut and paste mechanism for their mobilization, and retrotransposons, which move through an RNA intermediate [5]. These two classes are further divided into TE superfamilies and families based on particular sequence features, such as the presence or absence of long terminal repeats (LTRs) in the case of retrotransposons [5]

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Conclusion