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

Abstract 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 autophagy pathway has not been elucidated in plants. Here, we demonstrate that autophagy is activated during light-to-dark conversion though transcriptional upregulation of autophagy-related genes (ATGs). Moreover, depletion of the ELONGATED HYPOCOTYL 5 (HY5), a key component of light signaling, leads to enhanced autophagy activity and resistant to extended darkness and nitrogen starvation treatments attributing 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 find that both darkness and nitrogen depletion can induce the degradation of HY5 via 26S proteasome and the concomitant disassociation of HDA9 from ATG5 and ATG8e loci to relieve their repression, thereby activating autophagy. Genetic analysis further confirm that HY5 and HDA9 act synergistically and function at upstream of 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.