Triosephosphate export from chloroplasts regulates flavonoid biosynthesis and permits high light acclimation through the inactivation of SnRK1

Abstract

Plants evolved multiple strategies to cope with rapid changes in the environment. During high light acclimation, biosynthesis of photoprotective flavonoids, such as anthocyanins, is induced. However, the exact nature of the signal and downstream factors for high light induction of flavonoid biosynthesis (FB) are still under debate. Here we show that carbon-fixation in chloroplasts, subsequent export of photosynthates by TRIOSEPHOSPHATE/PHOSPHATE TRANSLOCATOR (TPT), and the rapid increase in cellular sugar contents permit the transcriptional activation of FB during high light acclimation. In combination with genetic and physiological analysis, targeted and whole transcriptome gene expression studies showed that reactive oxygen species and phytohormones play only a minor role for rapid HL-induction of the anthocyanin branch of FB. In addition to FB, sugar-responsive genes were late-repressed or induced in tpt-2 in the course of the high light treatment and a significant overlap with transcripts regulated by SNF1-RELATED PROTEIN KINASE 1 (SnRK1) was found. Analysis of mutants with increased and repressed SnRK1 activity revealed that inactivation of SnRK1 is required for the rapid induction of FB during high light acclimation. Our study underlines the central role of chloroplasts as sensors for environmental changes and emphasizes the vital function of sugar-signalling in plant acclimation, even beyond the regulation of FB.