The AMP-Activated Protein Kinase KIN10 Is Involved in the Regulation of Autophagy in Arabidopsis

Abstract

Autophagy is a highly conserved system in eukaryotes for the bulk degradation and recycling of intracellular components. Autophagy is involved in many physiological processes including development, senescence, and responses to abiotic and biotic stress. The adenosine 5’-monophosphate (AMP)-activated protein kinase AMPK positively regulates autophagy in mammals; however, the potential function of AMPK in plant autophagy remains largely unknown. Here, we identified KIN10, a plant ortholog of the mammalian AMPK, as a positive regulator of plant autophagy and showed that it acts by affecting the phosphorylation of ATG1 (AUTOPHAGY-RELATED GENE 1) proteins in Arabidopsis. Transgenic Arabidopsis lines overexpressing KIN10 (KIN10-OE) showed delays in leaf senescence, and increased tolerance to nutrient starvation, these phenotypes required a functional autophagy pathway. Consistent with KIN10 having a potential role in autophagy, the nutrient starvation-induced formation of autophagosomes and cleavage of GFP-ATG8e were accelerated in the KIN10-OE lines compared to the wild type. Moreover, the KIN10-OE lines were less sensitive to drought and hypoxia treatments, compared with wild type. Carbon starvation enhanced the level of phosphorylated YFP-ATG1a in the KIN10-OE lines compared to that of wild type. Together, these findings suggest that KIN10 is involved in positive regulation of autophagy, possibly by affecting the phosphorylation of ATG1s in Arabidopsis.

The SnRK1 Kinase as Central Mediator of Energy Signaling between Different Organelles

“…Plant leaf senescence involves autophagy (Liu and Bassham, 2012), and recently, AKIN10 was identified as a positive regulator of plant autophagy. Transgenic Arabidopsis lines overexpressing AKIN10 show delayed leaf senescence and increased tolerance to nutrient starvation and abiotic stresses, and a functional autophagy pathway was found to require AKIN10 activity (Baena-González et al, 2007;Chen et al, 2017;Soto-Burgos and Bassham, 2017). Moreover, phosphorylation of ATG1 (AUTOPHAGY RELATED GENE1), the plant ortholog of mammalian ULK1, was enhanced when AKIN10 was overexpressed, indicating that the mechanism of autophagy activation is conserved between plants and animals .…”

Group VII Ethylene Response Factors in Arabidopsis: Regulation and Physiological Roles

“…These proteins modulate the autophagy pathway and thereby enhance Arabidopsis tolerance to nutrient starvation (Qi et al, 2017). In fact, autophagy responses are also activated during hypoxia and contribute to plant submergence tolerance (Chen et al, 2015(Chen et al, , 2017a(Chen et al, and 2017b. This evidence suggests that an additional tier of regulation might connect the ERF-VIIs to submergence responses, through the SINAT factors.…”

Dynamics of Autophagosome Formation

“…KIN10 overexpression led to increased phosphorylation of ATG1 during Suc starvation, suggesting that KIN10 regulates autophagy by affecting the phosphorylation of ATG1 (Chen et al, 2017), as in mammals and yeast. Autophagy is activated during a wide range of abiotic stresses, and a kin10 knockout mutant failed to activate autophagy during most of these stresses (Soto-Burgos and Bassham, 2017).…”

“…Overexpression of the KIN10 gene in Arabidopsis leads to constitutive activation of autophagy (Chen et al, 2017;Soto-Burgos and Bassham, 2017), suggesting a positive role in the regulation of autophagy. KIN10 overexpression led to increased phosphorylation of ATG1 during Suc starvation, suggesting that KIN10 regulates autophagy by affecting the phosphorylation of ATG1 (Chen et al, 2017), as in mammals and yeast.…”

“…In mammals, AMPK promotes autophagy by phosphorylating Ulk1 (ATG1 homolog) upon Glc starvation (Kim et al, 2011). In Arabidopsis, KIN10 overexpression results in an increase in ATG1 phosphorylation, suggesting that this mode of regulation is conserved (Chen et al, 2017). In yeast, TOR phosphorylates ATG13 in nutrient-rich conditions, causing a decrease in its affinity for ATG1, preventing their association and therefore repressing autophagy.…”