Comparative analysis of centromeres of oat ( Avena sativa ) and its tetraploid and diploid relatives reveals rapid evolution of centromere composition and architecture

Background Recent advances in assemblies of nearly gap-free, high-quality genomes have enabled detailed analysis of centromeres in large and highly repetitive crop genomes. Here, we analyse the hexaploid Avena sativa genome and its tetraploid (A. insularis) and diploid relatives (A. longiglumis, A. atlantica and A. eriantha).

Avena centromeres are largely composed of retrotransposons belonging to three families, RLG_Ava, RLG_Cereba and RLG_Beth. Analysis of retrotransposon populations revealed striking differences in the centromere architecture between the A, C and D genome lineages. We identified distinct profiles of transposable element bursts for these lineages which include the emergence and disappearance of retrotransposon families and subfamilies. We identified multiple centromere shifts which occurred in the C genome lineage within the past ∼ 4 myrs and retraced species divergences and polyploidization events in the Avena genus. Although the studied species are closely related, our data show that their centromeres have rapidly evolved different and distinct centromere architectures, for example through the spread of novel satellite repeats or activity bursts of different retrotransposon families and subfamilies. Additionally, we found that RLG_Ava and RLG_Cereba retrotransposons have been coexisting while simultaneously competing for the centromeric “niche” since the emergence of the Poaceae (grasses).

Our comparative analyses provided detailed insight into centromere evolution across the Avena genus and revealed that composition and architecture of centromeres can vary greatly even between closely related species and different ploidy levels. Our findings emphasize the need for extended analyses of large genome species to improve our understanding of centromere evolution. Competing Interest Statement The authors have declared no competing interest. Abbreviations - AP - Aspartate protease - CDS - Coding sequence - ChiP - Chromatin Immunoprecipitation - CR - Chromodomain - FISH - Fluorescence in-situ Hybridization Assays - INT - Integrase - LTR - Long Terminal Repeats mya Million years ago - myrs - Million years - PCA - Principal component analysis - RH - RNase H - RLG - Retrotransposon LTR Gypsy - RT - Reverse transcriptase - TE - Transposable Element