Differential LTR-retrotransposon dynamics across polyploidization, speciation, domestication and improvement of cotton (Gossypium)

Background Transposable elements (TEs) are major components of plant genomes and major drivers of plant genome evolution. The cotton genus ( Gossypium ) is an excellent evolutionary model for polyploidization, speciation, domestication and crop improvement. Here, we implement genome and pangenome analyses to study in detail the dynamics of LTR-retrotransposons (LTR-RT) during the cotton evolution. Results We show that some LTR-RT lineages amplified in tetraploid cotton compared to their diploid progenitors, whereas others stayed stable or amplified but were removed through solo-LTR formation. Using species-level pangenomes we show that only a few lineages (CRM, Tekay, Ivana and Tork) remained active after polyploidization and are still transposing. Tekay and CRM elements have re-shaped the centromeric and pericentromeric regions of tetraploid cottons in a subgenome specific manner, through new insertions but also selective eliminations through solo-LTR formation. On the other hand, Ivana and Tork have actively inserted within or close to genes. Finally, population-level analyses using the two pangenomes and data from 283 and 223 varieties of G. hirsutum and G. barbandense reveal changes in Transposon Insertion Polymorphism (TIP) frequencies accompanying domestication and improvement of both species, suggesting the possibility of selection on linked regions. Conclusions Our findings reveal that LTR-RT lineages followed differential dynamics during cotton evolution, displaying differences among species and the two coresident genomes of allopolyploid cotton. A handful of the LTR-RT lineages that expanded after polyploidisation helped shape the genomes of both G. hirstutum and G. barbadense , impacting their centromere and pericentromeric regions as well as protein- coding genes.