Genetic Analyses of the Arabidopsis ATG1 Kinase Complex Reveal Both Kinase-Dependent and Independent Autophagic Routes during Fixed-Carbon Starvation

Abstract

Under nutrient and energy-limiting conditions, plants up-regulate sophisticated catabolic pathways such as autophagy to remobilize nutrients and restore energy homeostasis. Autophagic flux is tightly regulated under these circumstances through the AuTophaGy-related1 (ATG1) kinase complex, which relays upstream nutrient and energy signals to the downstream components that drive autophagy. Here, we investigated the role(s) of the Arabidopsis (Arabidopsis thaliana) ATG1 kinase during autophagy through an analysis of a quadruple mutant deficient in all four ATG1 isoforms. These isoforms appear to act redundantly, including the plant-specific, truncated ATG1t variant, and like other well-characterized atg mutants, homozygous atg1abct quadruple mutants display early leaf senescence and hypersensitivity to nitrogen and fixed-carbon starvations. Although ATG1 kinase is essential for up-regulating autophagy under nitrogen deprivation and short-term carbon starvation, it did not stimulate autophagy under prolonged carbon starvation. Instead, an ATG1-independent response arose requiring phosphatidylinositol-3-phosphate kinase (PI3K) and SUCROSE NONFERMENTING1-RELATED PROTEIN KINASE1 (SnRK1), possibly through phosphorylation of the ATG6 subunit within the PI3K complex by the catalytic KIN10 subunit of SnRK1. Together, our data connect ATG1 kinase to autophagy and reveal that plants engage multiple pathways to activate autophagy during nutrient stress, which include the ATG1 route as well as an alternative route requiring SnRK1 and ATG6 signaling.

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

“…Thus, during responses to environmental stresses, TOR activity is regulated by SnRKs, subsequently, regulating the autophagy process. Interestingly, under prolonged fixed-carbon starvation, the active KIN10 subunit of SnRK1 phosphorylates ATG6 to activate the PI3K complex, which bypasses the requirement of the ATG1 kinase complex for autophagy initiation (Huang et al, 2019a;Huang et al, 2019b) (Figure 2).…”

Membrane Contact Sites and Organelles Interaction in Plant Autophagy

“…ATG2 and ATG18a function together as a complex in autophagosome expansion and maturation downstream of the initiation of autophagy by ATG11 and ATG9 (Kang et al, 2018). Although the precise functions of ATG2 and ATG18s remain unknown in plants, they may play other roles in addition to mediating the formation of autophagosomal MCS (Kang et al, 2018;Huang et al, 2019).…”

“…This enables it to function as an autophagy cargo receptor mediating the degradation of ubiquitinated cargos. Apart from being the autophagy substrate and the cargo receptor (Svenning et al, 2011;Huang et al, 2019), the function of plant NBR1 homologs in protein quality control and pathogen defense has also been revealed. AtNBR1 may function in the selective autophagy of protein aggregates because of the defect in vacuolar delivery of aggregation-prone GFP-FL2 SP observed in nbr1 mutant (Jung et al, 2019).…”

You Are What You Eat: An ATG1-Independent Path to Autophagy

“…An ATG1-independent pathway (dashed line) was discovered that induces autophagy under longterm carbon starvation, whereby SnRK1 directly stimulates autophagy through the PI3K complex. (Adapted from Huang et al [2019], Figure 11.) [OPEN] Articles can be viewed without a subscription.…”