Genome - epigenome dynamics and natural variation in Thlaspi arvense

Abstract

Plants play a vital role in sustaining all life on Earth. However, anthropogenic environmental changes are now threatening plant populations. Understanding how plants adapted to environmental changes in the past is key to understanding how they will respond in the future and one way to do this is the study of intraspecific natural variation – the heritable differences occurring in different populations of a species. This natural variation is the result of adaptive processes, and it allows to study phenotypes and their genetic bases, and to discover beneficial alleles with potential applications in breeding. Besides DNA sequence variation, plant populations also harbour extensive epigenetic variation, which can affect phenotypes and be induced by the environment or accumulated in the form of stochastic epimutations. In sexually reproducing species, most but not all heritable epigenetic variation is controlled by genetic variation. In turn, epigenetic changes can affect not only gene expression, but also the silencing of transposable elements, regulating novel genetic variation. To understand these processes and interactions, I worked with Thlaspi arvense, which compared to the model species Arabidopsis thaliana has a more complex genome, rich in transposable elements. This species is also a new biofuel and winter cover crop, and breeding efforts to domesticate it are underway. I surveyed genome-wide genetic and epigenetic natural variation in a large collection of European T. arvense accessions, grown in a common environment. I found extensive genetic and epigenetic variation, and that genetic variants at genes involved in the DNA methylation machinery were associated with variable levels of methylation across the whole genome. However, DNA methylation patterns were also associated with climate of origin. Although the genetic variants explained the majority of the observed Differentially Methylated Regions (DMRs), a fraction of DMRs was more strongly associated with environment than DNA sequence, and this fraction was sequence-context dependent, increasing from CG to CHG to CHH. To understand how short genetic variants and DNA methylation interact with transposable element dynamics, I analysed transposon insertion polymorphisms detected against the reference accession and found several genes associated with the rate of transposition. As DNA methylation is the main mechanism silencing transposons, many of these genes were indeed part of the genomic machinery depositing and maintaining DNA methylation. Nevertheless this was only the case for retrotransposons, whose new insertions became indeed methylated, while DNA transposons, whose new insertions were not methylated, were not associated with DNA methylation machinery genes but with a single gene coding for Heat Shock Protein 19 (HSP19). Since this gene is absent in A. thaliana, this shows how moving away from classical model species can bring new insights into genome dynamics. In this work we also investigated the insertion behaviour of different TE families and identified an Alesia family preferentially inserting into genes and coding sequences. Since there is growing interest in domesticating T. arvense, this TE family could potentially be used to generate new phenotypes of interest. In the final chapter, I recycled sequencing data not belonging to T. arvense to indirectly estimate the abundance of pests and pathogens in my common-environment experiment, and thus natural variation in plant resistance. I found that resistance variation was related to the environment of plant origins, suggesting local adaptation. Moreover, pathogen read-counts allowed me to map genes associated with this resistance variation. Many of these genes were already known to be involved in plant defense and are of potential interest for breeding. Using DNA methylation information I also detected epialleles associated with pathogen presence, located close to genes and transposons. Altogether my thesis provides evidence of strong and complex interactions between the genome, the epigenome and the environment, which are important to understand adaptive processes and predict the effects of climate change on plant populations. My work also brought insights with potential applications for breeding T. arvense as a future crop.