Sugar-mediated control of ATG101 modulates carbon deficiency-induced autophagy in Arabidopsis

Autophagy is a major eukaryotic degradation and recycling pathway, which eliminates damaged cellular components and provides energy and building blocks especially under adverse environmental conditions. While the core autophagy machinery has been extensively studied, autophagy initiation and regulation remain less understood. In this study, we show that genes encoding the core autophagy initiation complex, ATG1, ATG11, ATG13, and ATG101, are transcriptionally regulated by sugars. To analyze the expression of these genes, we took advantage of Arabidopsis thaliana accessions, which display strong variations in their responses to darkness-induced fixed carbon deprivation. One of the components of the initiation complex, ATG101, has multiple sugar-related elements, and was repressed by sugar. Moreover, ATG101 was induced stronger upon starvation in carbon starvation-resistant accessions when compared to carbon starvation-sensitive accessions. We identified three single nucleotide polymorphisms in the genomic region of ATG101 which are associated with the carbon-starvation phenotype. Further analyses through complementation of the atg101 mutant with different variants of ATG101 demonstrated that the single nucleotide polymorphism alleles contribute differently to ATG101 expression regulation, response to sugar, and phenotype recovery. Taken together, our data suggest that modulation of ATG101 by sugar is part of a multi-layered mechanism regulating the sensitivity to carbon starvation in Arabidopsis.