The Genomic Shock Hypothesis: Genetic and Epigenetic Alterations of Transposable Elements after Interspecific Hybridization in Plants

Abstract

Transposable elements (TEs) are major components of plant genomes with the ability to change their position in the genome or to create new copies of themselves in other positions in the genome. These can cause gene disruption and large-scale genomic alterations, including inversions, deletions, and duplications. Host organisms have evolved a set of mechanisms to suppress TE activity and counter the threat that they pose to genome integrity. These includes the epigenetic silencing of TEs mediated by a process of RNA-directed DNA methylation (RdDM). In most cases, the silencing machinery is very efficient for the vast majority of TEs. However, there are specific circumstances in which TEs can evade such silencing mechanisms, for example, a variety of biotic and abiotic stresses or in vitro culture. Hybridization is also proposed as an inductor of TE proliferation. In fact, the discoverer of the transposons, Barbara McClintock, first hypothesized that interspecific hybridization provides a “genomic shock” that inhibits the TE control mechanisms leading to the mobilization of TEs. However, the studies carried out on this topic have yielded diverse results, showing in some cases a total absence of mobilization or being limited to only some TE families. Here, we review the current knowledge about the impact of interspecific hybridization on TEs in plants and the possible implications of changes in the epigenetic mechanisms.

Genome Variability in Artificial Allopolyploid Hybrids of Avena sativa L. and Avena macrostachya Balansa ex Coss. et Durieu Based on Marker Sequences of Satellite DNA and the ITS1–5.8S rDNA Region

“…Hybridization plays a fundamental role in plant evolution and breeding, as it can result in phenotypic changes, sexual isolation, and the appearance of new species [56]. In spontaneous and artificial hybridization, the merging of two or more different genomes can often be accompanied by a phenomenon called a 'genomic shock', which leads to a wide genetic and epigenetic changes in a hybrid [57,58]. Interspecific hybridization is widely used in crop breeding since it expands the species variability that is necessary for emergence of new polyploid hybrids with improved characteristics compared to their parental species [59,60].…”

Ancient hybridization and repetitive element proliferation in the evolutionary history of the monocot genus Amomum (Zingiberaceae)

“…Genomic shock occurs when a significant portion of the repeatome is reactivated or activated anew following hybridization. This phenomenon is often triggered by the merging of sub-genomes, leading to DNA demethylation and the activation of previously silenced repeats (Michalak, 2009;de Tomaś and Vicient, 2024). Reactivation of a broad spectrum of repeats post-hybridization typically arises from the breakdown or malfunction of regulatory mechanisms (e.g., Shan et al, 2005;Ungerer et al, 2006;Wei et al, 2021), conferring potential benefits in terms of adaptability (Schrader and Schmitz, 2019).…”