A positive feedback regulation of SnRK1 signaling by autophagy in plants

SnRK1,an evolutionarily conserved heterotrimeric kinase complex that acts as a key metabolic sensor in maintaining energy homeostasis in plants,is an important upstream activator of autophagy that serves as a cellular degradation mechanism for the healthy growth of plants.However,whether and how the autophagy pathway is involved in regulating SnRK1 activity remains unknown.In this study,we identified a clade of plant-specific and mitochondria-localized Fcs-like zinc finger(FLZ)proteins as currently unknown ATG8-interacting partners that actively inhibit SnRK1 signaling by repressing the T-loop phosphorylation of the catalyticαsubunits of SnRK1,thereby negatively modulating autophagy and plant tolerance to energy deprivation caused by long-term carbon starvation.Interestingly,these AtFLZs are transcriptionally repressed by low-energy stress,and AtFLZ proteins undergo a selective autophagy-dependent pathway to be delivered to the vacuole for degradation,thereby constituting a positive feedback regulation to relieve their repression of SnRK1 signaling.Bioinformatic analyses show that the ATG8-FLZ-SnRK1 regulatory axis first appears in gymnosperms and seems to be highly conserved during the evolution of seed plants.Consistent with this,depletion of ATG8-interacting ZmFLZ14 confers enhanced tolerance,whereas overexpression of ZmFLZ14 leads to reduced tolerance to energy deprivation in maize.Collectively,our study reveals a previously unknown mechanism by which autophagy contributes to the positive feedback regulation of SnRK1 signaling,thereby enabling plants to better adapt to stressful environments.