The energy sensor SnRK1 promotes starvation-induced autophagosome formation by modulating ATG13a phosphorylation in Arabidopsis

Abstract

In eukaryotes, autophagy is an evolutionarily conserved cellular degradation and recycling process that is tightly associated with cellular nutrient status. The energy sensor SNF1-RELATED KINASE 1 (SnRK1) is thought to sense nutrient starvation and induce autophagy, but how it regulates autophagosome formation in plant cells remains largely unknown. Here, we show that the SnRK1 α-catalytic subunit KIN10 regulates autophagosome formation in Arabidopsis (Arabidopsis thaliana) by interacting with and phosphorylating AUTOPHAGY-RELATED PROTEIN 13a (ATG13a), a key component of the ATG1a–ATG13a protein kinase complex involved in autophagy initiation. KIN10 directly phosphorylates ATG13a in vitro and in vivo, inhibiting its ubiquitination and increasing its abundance. Moreover, we identified ten serine residues in ATG13a that are important for KIN10-mediated phosphorylation. Transgenic plants accumulating a nonphosphorylatable ATG13a variant with mutations of these ten residues were less tolerant of starvation than ATG13a-overexpressing plants and displayed accelerated leaf senescence and lower autophagic flux. The KIN10-mediated phosphorylation of ATG13a did not affect ATG1a–ATG13a complex formation; instead, it facilitated ATG1a phosphorylation, thereby promoting autophagosome formation. Therefore, our findings suggest that the KIN10–ATG13a module modulates SnRK1-mediated autophagosome formation, likely representing a key step in integrating energy sensing and autophagy initiation in plant cells.