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Transposable element and genome evolution following hybridization in wild wheats

2014, Senerchia, Natacha, Parisod, Christian, Kessler, Félix, Felber, François

Genome dynamics is an essential process of eukaryote genome evolution. Hybridization and inter-species gene flow result in new interactions among divergent genomes and may reveal genetic incompatibilities having accumulated after the origin of species. Being highly mutagenic and repressed by various epigenetic mechanisms, transposable elements (TEs) are postulated to play a central role in fuelling genome reorganization following inter-genomic conflicts after hybridization. However, we are still far from understanding mechanisms and forces of such genome dynamics.
The main aim of this was to test the implication of multiple TE families on genome reorganization, hybridization success and introgression. Four Aegilops allotetraploid species with interconnected genomes belonging to the wheats group, Aegilops crassa (DDMM), Ae. cylindrica (CCDD), Ae. geniculata (MMUU) and Ae. triuncialis (CCUU) that derived from the diploids Ae. caudata (CC), Ae. comosa (MM), Ae. tauschii (DD) and Ae. umbellulata (UU) were used as model. These species have complex genomes with 80% of repetitive elements that have differentially diverged under the influence of TEs and hybridization.
As a first step, the TE composition was assessed using high-throughput sequencing in selected model species and TE families were classified as recently active or quiescent. Based on these results, fingerprint assays were designed and evaluated restructuring in 17 active TE families by comparing genome wide restructuring in diploid and derived tetraploid species and highlighted different TE specific evolutionary trajectories following polyploidy. Restructuring was TE-specific and species-specific, but consistently correlated with TE divergence between progenitors. Using this knowledge, levels of restructuring and methylation changes around insertions of nine TE families were assessed in artificial F1 hybrids between the tetraploid species and, again, correlated with TE divergence between parents. Asymmetrical patterns of genome reorganization paralleling patterns of reproductive isolation among tetraploids, together with nonrandom loss and methylation changes in hybrids suggest that certain events are necessary to produce viable plants. In a last study, hybridization and backcrossing was assessed in natural hybrid zones between the Ae. geniculata and Ae. triuncialis, relating important restructuring of which sequences lost was dominant and that three TE families among the six selected ones were differently exchanged.
Aegilops as model offered unparalleled opportunities to address the evolutionary trajectories of multiples candidate TE families and reported evidence of important genome reorganization following various independent hybridization, with multiple TE families clearly playing a central role in host genome evolution and revealing that the progenitors divergence between TE families impacts on the reorganization level. This work reported potential proximate and ultimate factors of genome reorganization driven by conflicts between intragenomic parasites.