Evolutionary dynamics of retrotransposons following autopolyploidy in the Buckler Mustard species complex

Abstract

Summary Long terminal repeat retrotransposons (LTR-RTs) represent a major fraction of plant genomes, but processes leading to transposition bursts remain elusive. Polyploidy expectedly leads to LTR-RT proliferation, as the merging of divergent diploids provokes a genome shock activating LTR-RTs and/or genetic redundancy supports the accumulation of active LTR-RTs through relaxation of selective constraints. Available evidence supports interspecific hybridization as the main trigger of genome dynamics, but few studies have addressed the consequences of intraspecific polyploidy (i.e. autopolyploidy), where the genome shock is expectedly minimized. The dynamics of LTR-RTs was thus here evaluated through low coverage 454 sequencing of three closely related diploid progenitors and three independent autotetraploids from the young Biscutella laevigata species complex. Genomes from this early diverging Brassicaceae lineage presented a minimum of 40% repeats and a large diversity of transposable elements. Differential abundances and patterns of sequence divergence among genomes for 37 LTR-RT families revealed contrasted dynamics during species diversification. Quiescent LTR-RT families with limited genetic variation among genomes were distinguished from active families (37.8%) having proliferated in specific taxa. Specific families proliferated in autopolyploids only, but most transpositionally active families in polyploids were also differentiated among diploids. Low expression levels of transpositionally active LTR-RT families in autopolyploids further supported that genome shock and redundancy are non-mutually exclusive triggers of LTR-RT proliferation. Although reputed stable, autopolyploid genomes show LTR-RT fractions presenting analogies with polyploids between widely divergent genomes. Significance Statement This genome survey in an early diverging Brassicaceae species highlights the evolution of an ancestral pool of long terminal repeat retrotransposons (LTR-RTs) and further emphasizes astonishing genome dynamics among closely related taxa. Patterns of genetic variation among LTR-RT copies support both intraspecific hybridization and subsequent genome duplication as crucial triggers of LTR-RT proliferation following autopolyploidy.