Experimentally heat‐induced transposition increases drought tolerance in Arabidopsis thaliana

Abstract

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.

Regulatory mechanism of a heat-activated retrotransposon by DDR complex in Arabidopsis thaliana

“…When plants are exposed to the external environment, especially to adverse conditions such as high temperature, salt stress, low temperature, etc., the retrotransposons are activated; they insert into the target genes and simultaneously affect the expression of the surrounding genes ( Lisch, 2013 ; Ito, 2022 ; Thieme et al., 2022 ). Since the transcription of retrotransposons affects the stability of plant genomes, almost all transposons are silenced by epigenetic modifications, such as DNA methylation and histone modifications ( Zilberman et al., 2007 ; Zhang et al., 2010 ).…”

Phenotypic diversity influenced by a transposable element increases productivity and resistance to competitors in plant populations

“…Interestingly, ONSEN transposition shows a pronounced preference for exons and regions rich in the histone variant H2A.Z (Quadrana et al, 2019; Roquis et al, 2021), an attribute anticipated to yield significant phenotypic implications. Additionally, several studies underscore ONSEN's direct role in generating transcriptomic and phenotypic variation in A. thaliana (Baduel et al, 2021; Ito et al, 2011, 2016; Quadrana et al, 2019; Roquis et al, 2021; Thieme et al, 2017, 2022). Given these findings, we deduce that the ONSEN effect, inclusive of its influence on epigenetic variation, was likely the central driver in generating functional diversity in our experimental populations.…”

Potential and limits of (mal)adaptive mutation rate plasticity in plants

“…A screening of experimental A. thaliana lines that accumulated transposition mutation from heat‐induced ONSEN transposable elements found that five out of 23 exhibited elevated drought tolerance. The causal mutation in one line was shown to be loss‐of‐function resulting from an exonic transposon insertion in a ribose‐5‐phosphate‐isomerase 2 gene that led to reduced water loss (Thieme et al ., 2022). The extent to which these observations reflect a generalizable bias in the dynamics of transposable elements is unclear.…”