Retrotransposon-driven environmental regulation of FLC leads to adaptive response to herbicide

Abstract

The mobilization of transposable elements is a potent source of mutations. In plants, several stransposable elements respond to external cues, fuelling the hypothesis that natural transposition can create environmentally sensitive alleles for adaptation. Here we report on the detailed characterization of a retrotransposon insertion within the first intron of the Arabidopsis floral-repressor gene FLOWERING LOCUS C (FLC) and the discovery of its role for adaptation. The insertion mutation augments the environmental sensitivity of FLC by affecting the balance between coding and non-coding transcripts in response to stress, thus expediting flowering. This balance is modulated by DNA methylation and orchestrated by IBM2, a factor involved in the processing of intronic heterochromatic sequences. The stress-sensitive allele of FLC has spread across populations subjected to recurrent chemical weeding, and we show that retrotransposon-driven acceleration of the life cycle represents a rapid response to herbicide application. Our work provides a compelling example of a transposable element-driven environmentally sensitive allele that confers an adaptive response in nature. This study reports the discovery of a retrotransposon insertion in the FLC gene conferring an environmentally dependent control mechanism mediated by DNA methylation that drives the adaptation of natural Arabidopsis populations to herbicide exposure.