Plants have evolved sophisticated mechanisms to balance between growth and stress tolerance upon changing environmental conditions. Autophagy is a critical process for recycling of cytoplasmic materials during nutrient remodeling and stress responses. Upon activation, the materials to be degraded are engulfed by a double-membrane vesicle called an autophagosome, which delivers the cargo to the vacuole for degradation and recycling. Studies in plants have revealed genes that are involved in the core machinery of autophagosome formation and delivery, and key regulators of autophagy. However, the upstream regulators of autophagy and the functions of autophagy in balancing growth and stress tolerance remain unclear. This dissertation summarizes my efforts in studying the regulation and functions of autophagy in Arabidopsis thaliana.

Previous studies identified a key regulator of autophagy, target of rapamycin (TOR), being a negative regulator of autophagy, and a positive regulator of plant growth. TOR has been suggested to be a nutrient sensor that activates autophagy during nutrient deficiency. Here we have assessed the extent to which TOR controls autophagy activation under abiotic stress. Through overexpression of TOR and activation of TOR activity by auxin, we have revealed that not only nutrient stress, but also salt and osmotic stresses regulate autophagy through a TOR-dependent pathway. In addition, oxidative stress and ER stress-induced autophagy are independent of TOR. Our results also have shown that auxin negatively regulates autophagy through the TOR-dependent pathway, providing a new mechanism of auxin-regulated stress tolerance in plants.

Another plant hormone that promotes plant growth is brassinosteroids (BRs). Our results identified a new link between the BR and TOR signaling through phosphorylation of TOR by a BR-regulated kinase Brassinazole-Insensitive 2 (BIN2). BRs were also characterized as negative regulators of autophagy, and BR regulates autophagy and plant growth through the interaction with the TOR signaling pathway. This reveals a new mechanism of balancing plant growth and stress response through interaction between hormone signaling and regulation of autophagy.

We have also identified the TOR-independent pathway of autophagy regulation upon ER stress. ER stress is triggered when cells accumulate excessive unfolded and misfolded proteins, which then leads to the unfolded protein response (UPR). IRE1 is a dual-function protein kinase and ribonuclease, and one of the isoform, IRE1b, was shown to be dependent in the activation of autophagy upon ER stress. Here we have shown that the ribonuclease function of IRE1b is responsible for autophagy regulation, and we have identified three genes in the Regulated Ire1-Dependent Decay of Messenger RNA (RIDD) pathway that negatively regulate autophagy induction upon ER stress.

In summary, our results reveal that autophagy induced upon abiotic stresses is regulated through TOR-dependent and –independent pathways, and the TOR signaling pathway interacts with auxin and BR hormone signaling to regulate plant growth and stress responses. ER stress regulates autophagy is dependent of IRE1b ribonuclease function.