Summary Eukaryotic genomes contain a vast diversity of transposable elements (TEs). Formerly often described as selfish and parasitic DNA sequences, TEs are now recognised as a source of genetic diversity and powerful drivers of evolution. However, because their mobility is tightly controlled by the host, studies experimentally assessing how fast TEs may mediate the emergence of adaptive traits are scarce. We exposed Arabidopsis thaliana high‐copy TE lines (hcLines) with up to c. eight‐fold increased copy numbers of the heat‐responsive ONSEN TE to drought as a straightforward and ecologically highly relevant selection pressure. We provide evidence for increased drought tolerance in five out of the 23 tested hcLines and further pinpoint one of the causative mutations to an exonic insertion of ONSEN in the ribose‐5‐phosphate‐isomerase 2 gene. The resulting loss‐of‐function mutation caused a decreased rate of photosynthesis, plant size and water consumption. Overall, we show that the heat‐induced transposition of a low‐copy TE increases phenotypic diversity and leads to the emergence of drought‐tolerant individuals in A. thaliana. This is one of the rare empirical examples substantiating the adaptive potential of mobilised stress‐responsive TEs in eukaryotes. Our work demonstrates the potential of TE‐mediated loss‐of‐function mutations in stress adaptation.
Plant genomes comprise a vast diversity of transposable elements (TEs) (Tenaillon et al. 2010). While their uncontrolled proliferation can have fatal consequences for their host, there is strong evidence for their importance in fueling genetic diversity and plant evolution (Baduel et al. 2021). However, the number of studies addressing the role of TEs in this process is limited. Here we show that the heat-induced burst of a low-copy TE increases phenotypic diversity and leads to the rapid emergence of more drought-resistant individuals of Arabidopsis thaliana. We exposed TE-high-copy-(hc)lines (Thieme et al. 2017) with up to ~8 fold increased copy numbers of the heat-responsive ONSEN-TE (AtCOPIA78) (Ito et al. 2011; Cavrak et al. 2014; Tittel-Elmer et al. 2010) in the wild type background to desiccation as a straightforward and highly relevant selection pressure. We found evidence for a drastic increase of drought resistance in five out of the 23 tested hc-lines and further pinpoint one of the causative mutations to an exonic ONSEN-insertion in the ribose-5-phosphate-isomerase 2 gene. This loss-of-function mutation resulted in a decreased rate of photosynthesis and water consumption. This is one of the rare examples (Esnault et al. 2019) experimentally demonstrating the adaptive potential of mobilized stress-responsive TEs in eukaryotes. Our results further shed light on the complex relationship between mobile elements and their hosts and substantiate the importance of TE-mediated loss-of-function mutations in stress adaptation, particularly with respect to global warming.
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