Genome reorganization in F ₁ hybrids uncovers the role of retrotransposons in reproductive isolation

Abstract

Interspecific hybridization leads to new interactions among divergent genomes, revealing the nature of genetic incompatibilities having accumulated during and after the origin of species. Conflicts associated with misregulation of transposable elements (TEs) in hybrids expectedly result in their activation and genome-wide changes that may be key to species boundaries. Repetitive genomes of wild wheats have diverged under differential dynamics of specific long terminal repeat retrotransposons (LTR-RTs), offering unparalleled opportunities to address the underpinnings of plant genome reorganization by selfish sequences. Using reciprocal F 1 hybrids between three Aegilops species, restructuring and epigenetic repatterning was assessed at random and LTR-RT sequences with amplified fragment length polymorphism and sequencespecific amplified polymorphisms as well as their methylation-sensitive counterparts, respectively. Asymmetrical reorganization of LTR-RT families predicted to cause conflicting interactions matched differential survival of F 1 hybrids. Consistent with the genome shock model, increasing divergence of merged LTR-RTs yielded higher levels of changes in corresponding genome fractions and lead to repeated reorganization of LTR-RT sequences in F 1 hybrids. Such non-random reorganization of hybrid genomes is coherent with the necessary repression of incompatible TE loci in support of hybrid viability and indicates that TE-driven genomic conflicts may represent an overlooked factor supporting reproductive isolation.

Differential introgression and reorganization of retrotransposons in hybrid zones between wild wheats

“…A similar pattern was previously reported in experimental F1 hybrids (Senerchia et al . ) and is here congruent with the silencing of incompatible LTR‐RT loci through deletion and/or transgressive segregation in natural hybrids (Rieseberg ; Tayale & Parisod ).…”

“…before any recombination of genomes occurred), demonstrating that A. triuncialis cytoplasms tolerate the introgression of LTR‐RT insertions from A. geniculata , whereas introgression of active LTR‐RTs from A. triuncialis into A. geniculata is prevented due to cytoplasmic incompatibility (Senerchia et al . ). In consequence, later‐generation hybrids show asymmetrical specific admixtures, indicating the establishment of active insertions dependent on cytoplasmic context.…”

“…Such evidence matches observations of Senerchia et al . () that nucleo‐cytoplasmic incompatibilities related to conflicting interactions between LTR‐RTs can be a cause of reproductive isolation between these species.…”

“…This is particularly well illustrated by Sabine that was massively eliminated from the A. geniculata genome (Senerchia et al . , ) and was thus predicted to induce strong conflicts in hybrids containing A. geniculata cytoplasm. Accordingly, Sabine exhibited a negative presence in introgressants towards A. geniculata , indicating limited introgression of A. triuncialis insertions in this background, but a strong presence in hybrids towards A. triuncialis , highlighting introgression from A. geniculata .…”

Creating Order from Chaos: Epigenome Dynamics in Plants with Complex Genomes

“…However, it also appears that TE amplification can occur in the absence of horizontal transfer (Piegu et al, 2006;Ungerer et al, 2006;Deininger, 2011;Estep et al, 2013) and horizontal transfer can occur without subsequent TE amplification (Diao et al, 2006). It has also been suggested that wide hybridization and subsequent WGD may play a role in TE amplification (Ungerer et al, 2006;Petit et al, 2010;Madlung and Wendel, 2013;Senerchia et al, 2015). Other potentially important factors include abiotic stresses (Kalendar et al, 2000;Ito et al, 2011;Grandbastien, 2015), viral infection (Wieczorek and Obrę palska-Stę plowska, 2015), and chromosomal breaks (McClintock, 1950).…”