Transposable elements (TEs) are predominant in most plant genomes but their ongoing activity and diversity in plant populations has been mostly characterized in annual species. Beech trees (Fagus sylvatica) make up most of European forests and are highly threatened by drought and climate change. We sought to investigate the genomic diversity caused by TEs and their adaptive potential in this long-living species. We characterized TE insertion polymorphism (TIPs) in a single population of 150 common beech trees from the preserved Massane forest, a UNESCO world heritage site located near Perpignan, France. Using 672 and 558 LTR (Long Terminal Repeats) retrotransposon and MITE (Miniature Inverted- repeat Transposable Element) families, respectively, we show that the majority of TIPs are highly polymorphic and mostly privately shared within the population. We conducted a Genome-Wide Association Study (GWAS) using these TIPs as markers and identified several candidate TIPs associated with bud burst date, implying their potential involvement in regulating this important phenotypic trait. TIPs distribution revealed several hotspots near stress responsive genes. Bud burst date being an adaptive trait, our results could open new perspectives for the selection of best adapted trees.

Furthermore, given this high level of recent TE activity in common beech, we investigated ongoing TE mobility using extrachromosomal circular DNA (eccDNA) sequencing or mobilome-seq. We detected several active TEs in different beech trees from the Massane and Verzy French forests. Notably, we identified an highly active MITE family, responsible for somatic mutations. We further found several other active MITEs producing abundant eccDNA suggesting that MITEs could play a role in genome dynamics in this species. All together, our study sheds lights on how TEs impact genome evolution and adaptation in a non model perennial species. This could help us gain insights on TE dynamics and amplification in natura.