Sugar-responsive regulation of an autophagy initiation factor shapes carbon-starvation sensitivity in Arabidopsis

Autophagy is a conserved degradation and recycling pathway that sustains cellular homeostasis and provides energy and building blocks under adverse conditions. Despite detailed core machinery knowledge, transcriptional regulation of autophagy initiation in response to carbon status remains incompletely understood. Here, we combine scalable phenotyping of natural variation with molecular and functional analyses to dissect genotype-dependent autophagy responses to fixed-carbon deprivation in Arabidopsis thaliana. We show that transcription of genes encoding the autophagy initiation complex (ATG1, ATG11, ATG13, and ATG101) is repressed by soluble sugars, and that ATG101 displays the strongest enrichment of sugar-related cis-regulatory elements. Guided by this sugar-regulation framework, we phenotyped 181 accessions under prolonged darkness-induced carbon deprivation and quantified responses using chlorophyll retention (dark/light chlorophyll ratio) as a proxy trait, revealing natural variation in tolerance. ATG101 is induced more strongly upon deprivation in carbon starvation-resistant accessions. Association analysis identifies three SNPs in the ATG101 locus linked to the proxy phenotype, and we demonstrate that these polymorphisms differentially affect ATG101 sugar responsiveness and expression during carbon deprivation. Together, our results link natural variation in carbon-deprivation tolerance to regulatory polymorphisms at ATG101, supporting a model in which sugar-responsive control of autophagy initiation shapes genotype-specific sensitivity to carbon starvation in Arabidopsis.