A positive feedback regulation of SnRK1 signaling by autophagy in plants
A positive feedback regulation of SnRK1 signaling by autophagy in plants
复制标题
植物中自噬对 SnRK1 信号的正反馈调节
DOI：
10.1016/j.molp.2023.07.001
复制
发表时间：
2023
期刊：
影响因子：
27.5
通讯作者：
Bai, Mingyi
中科院分区：
文献类型：
--
作者：
Yang, Chao;Li, Xibao;Yang, Lianming;Chen, Shunquan;Liao, Jun;Li, Kailin;Zhou, Jun;Shen, Wenjin;Zhuang, Xiaohong;Bai, Mingyi
SnRK1 是一种进化上保守的异三聚体激酶复合物，作为维持植物能量稳态的关键代谢传感器，是自噬的重要上游激活剂，可作为植物健康生长的细胞降解机制。然而，自噬途径是否以及如何参与调节 SnRK1 活性仍不清楚。在这项研究中，我们鉴定了植物特异性和线粒体定位的 FCS 样锌指 (FLZ) 蛋白的进化枝，作为目前未知的 ATG8 相互作用伙伴，它们通过抑制 SnRK1 催化 α 亚基的 T 环磷酸化来主动抑制 SnRK1 信号传导，从而负向调节自噬和植物对长期碳饥饿引起的能量匮乏的耐受性。有趣的是，这些AtFLZ在低能应激下受到转录抑制，AtFLZ蛋白经历选择性自噬依赖性途径被递送至液泡进行降解，从而构成正反馈调节以缓解其对SnRK1信号传导的抑制。生物信息学分析表明，ATG8-FLZ-SnRK1 调控轴首先出现在裸子植物中，并且在种子植物的进化过程中似乎高度保守。与此一致的是，ATG8 相互作用的 ZmFLZ14 的耗尽会增强玉米的耐受性，而 ZmFLZ14 的过度表达会导致玉米对能量剥夺的耐受性降低。总的来说，我们的研究揭示了一种以前未知的机制，通过该机制，自噬有助于 SnRK1 信号的正反馈调节，从而使植物能够更好地适应压力环境。
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 catalytic α subunits of SnRK1, thereby negatively modulating autophagy and plant tolerance to energy deprivation caused by long-term carbon starvation. Interestingly, theseAtFLZsare 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.