HY5-HDA9 Module Transcriptionally Regulates Plant Autophagy in Response to Light-to-dark Conversion and Nitrogen Starvation

Light is arguably one of the most important environmental factors that determines virtually all aspects of plant growth and development, but the molecular link between light signaling and the autophagy pathway has not been elucidated in plants. In this study, we demonstrate that autophagy is activated during light-to-dark conversion though transcriptional upregulation of autophagy-related genes (ATGs). We showed that depletion of the ELONGATED HYPOCOTYL 5 (HY5), a key component of light signaling, leads to enhanced autophagy activity and resistance to extended darkness and nitrogen starvation treatments, contributing to higher expression of ATGs. HY5 interacts with and recruits HISTONE DEACETYLASE 9 (HDA9) to ATG5 and ATG8e loci to repress their expression by deacetylation of the Lys9 and Lys27 of histone 3. Furthermore, we found that both darkness and nitrogen depletion induce the degradation of HY5 via 26S proteasome and the concomitant disassociation of HDA9 from ATG5 and ATG8e loci, leading to their depression and thereby activated autophagy. Genetic analysis further confirmed that HY5 and HDA9 act synergistically and function upstream of the autophagy pathway. Collectively, our study unveils a previously unknown transcriptional and epigenetic network that regulates autophagy in response to light-to-dark conversion and nitrogen starvation in plants.