Autophagy: An Intracellular Degradation Pathway Regulating Plant Survival and Stress Response

Abstract

Autophagy is an intracellular process that facilitates the bulk degradation of cytoplasmic materials by the vacuole or lysosome in eukaryotes. This conserved process is achieved through the coordination of different autophagy-related genes (ATGs). Autophagy is essential for recycling cytoplasmic material and eliminating damaged or dysfunctional cell constituents, such as proteins, aggregates or even entire organelles. Plant autophagy is necessary for maintaining cellular homeostasis under normal conditions and is upregulated during abiotic and biotic stress to prolong cell life. In this review, we present recent advances on our understanding of the molecular mechanisms of autophagy in plants and how autophagy contributes to plant development and plants' adaptation to the environment.

Keywords: autophagy; plant; receptor; selective autophagy; stress.

Figure 1

Schematic diagram of the autophagy process. ① Autophagy is regulated by TOR kinase. Inhibition of TOR results in activation of constitutive autophagy, while overexpression of TOR blocks autophagy. Autophagy is initiated by the association of ATG13 and ATG1, together with ATG11 and ATG101, into an active complex. ② Autophagosome formation includes membrane delivery, vesicle nucleation and phagophore expansion and closure. ATG9, with ATG2 and ATG18, is involved in the delivery of lipids to the expanding phagophore. The VPS34 lipid kinase complex generates PI3P decoration, which is accompanied by the conjugation of ATG8 to PE. ATG8 firstly is matured by cleavage of its C-terminal by ATG4, and then is conjugated to PE by E2-like ATG3 and the E3-like ATG12-ATG5-ATG16 complex. ATG8-PE localizes to the autophagosomal membrane for phagophore expansion. ③ Selective autophagy is mediated by interaction of ATG8 with specific autophagic receptors through the AIM domain. Different cell components can be recognized by specific autophagic receptors. For instance, the C1 protein is translocated from the nucleus to the cytoplasm and binds to ATG8 for degradation. The whole chloroplast is ubiquitulated by PUB4 and binds to ATG8. The fragments of chloroplasts are recognized by CHMO1 or ATI1/2 for degradation by RCBs or ATI1/2 decorated plastid bodies. In plants, peroxisomes to be degraded are probably recognized by PEX6 or PEX10, and the ubiquitylated proteasome is recognized by RPN10. ④ The mature autophagosome is transported to the vacuole with the help of FYVE and FYCO proteins and fused with the vacuole to be degraded.

Figure 2

Schematic diagram of autophagy regulation under various stresses. KIN10, a catalytic subunit of SnRK1, is activated by stresses to phosphorylate TOR-interacting proteins, in turn inhibiting TOR kinase activity and activating ATG1. Additionally, active KIN10 can phosphorylate ATG6 and activate the PI3K complex to induce autophagy by an ATG1 kinase independent pathway. Under nutrient starvation stress, SnRK2 is activated by ABA to inhibit the activity of the TOR complex, and the expression of ATG genes are induced by the transcription factor ATAF1, resulting in the promotion of autophagy. Nutrient starvation stress can also cause the dissociation of GAPDH and ATG3, thus promoting the binding of ATG8 and ATG3. The expression of ATG genes are induced by WRKY33 and HsfA1a under heat stress to promote the degradation of protein aggregates through autophagy. Autophagy can also be induced by drought stress in an ethylene-dependent manner. Moreover, autophagy is also regulated by ROS levels during drought stress, in which AOX plays an important role.