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...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.展开更多
基金grants from the National Natural Science Foundation of China(32061160467,32270291,31870171)Open Competition Program of Top Ten Critical Priorities of Agricultural Science and Technology Innovation for the 14th Five-Year Plan of Guangdong Province(2022SDZG05)to C.G+6 种基金the Youth Innovation Promotion Association,Chinese Academy of Sciences(2023364)the Guangdong Basic and Applied Basic Research Foundation(2022A1515012319)the Guangzhou Basic and Applied Basic Research Foundation(2023A04J0094)to C.Y.the National Natural Science Foundation of China(32222087)the Research Grants Council of Hong Kong(N_CUHK405/20,24108820,and 14106622)The Chinese University of Hong Kong(CUHK)Research Committee to X.Z.the US National Science Foundation(#MCB-2040582)to D.C.B.
文摘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.
