An epitranscriptomic mechanism regulating chlorophyll biosynthesis in Arabidopsis

Light modulates expression of nuclear-encoded chloroplast proteins to promote chlorophyll biosynthesis and photosynthesis in plants. Photoregulatory mechanisms regulating transcription and protein stability of nuclear-encoded chloroplast proteins have been extensively studied, but how photoresponsive mRNA metabolism affecting chloroplast proteins remains not well understood. We performed a systematic analysis of the photoresponsive transcriptomes, m6A epitranscriptomes, translatomes, and proteomes in Arabidopsis, leading to a hypothesis that the blue light receptor cryptochromes activate the RNA methyltransferase, FIONA 1 (FIO1), to increase RNA methylation, translation of the nuclear-encoded chlorophyll synthesis enzymes (CSEs), and chlorophyll synthesis. We further demonstrate that the photoresponsive CRY2-interacting protein, SPA1, acts as a chaperone to mediate co-condensation of the CRY2/FIO1 complex, activating the FIO1 methyltransferase activity. This finding demonstrates a previously unknown photoregulatory mechanism controlling chlorophyll biosynthesis in plants.