Default Activation and Nuclear Translocation of the Plant Cellular Energy Sensor SnRK1 Regulate Metabolic Stress Responses and Development

Abstract

Energy homeostasis is vital to all living organisms. In eukaryotes, this process is controlled by fuel gauging protein kinases: AMP-activated kinase in mammals, Sucrose Non-Fermenting1 (SNF1) in yeast (Saccharomyces cerevisiae), and SNF1-related kinase1 (SnRK1) in plants. These kinases are highly conserved in structure and function and (according to this paradigm) operate as heterotrimeric complexes of catalytic-a and regulatory band g-subunits, responding to low cellular nucleotide charge. Here, we determined that the Arabidopsis (Arabidopsis thaliana) SnRK1 catalytic a-subunit has regulatory subunitindependent activity, which is consistent with default activation (and thus controlled repression), a strategy more generally used by plants. Low energy stress (caused by darkness, inhibited photosynthesis, or hypoxia) also triggers SnRK1a nuclear translocation, thereby controlling induced but not repressed target gene expression to replenish cellular energy for plant survival. The myristoylated and membrane-associated regulatory b-subunits restrict nuclear localization and inhibit target gene induction. Transgenic plants with forced SnRK1a-subunit localization consistently were affected in metabolic stress responses, but their analysis also revealed key roles for nuclear SnRK1 in leaf and root growth and development. Our findings suggest that plants have modified the ancient, highly conserved eukaryotic energy sensor to better fit their unique lifestyle and to more effectively cope with changing environmental conditions.

An abscisic acid-responsive protein interaction network for sucrose non-fermenting related kinase1 in abiotic stress response

“…This is in agreement with previous high-throughput verifications rates using an independent assay 5,48 and confirms that our curated Y2H interactions are of high quality. Additionally, these interactions occur in the nucleus, consistent with recent studies which have shown that SnRK1 relocates to the nucleus in response to stress 13,49 .…”

Protein Phosphorylation Dynamics Under Carbon/Nitrogen-Nutrient Stress and Identification of a Cell Death-Related Receptor-Like Kinase in Arabidopsis

“…In addition, SnRK1 affects plant developmental processes and regulates agedependent and dark-induced senescence progressions (Baena-González et al, 2007;Cho et al, 2012;Mair et al, 2015;Baena-González and Hanson, 2017;Pedrotti et al, 2018). The proteins SNF1, AMPK, and SnRK1 kinases form heterotrimeric holoenzymes containing a catalytic α-subunit and non-catalytic βand γ-subunits (the latter being replaced by a hybrid bg subunit in SnRK1) (Emanuelle et al, 2016;Ramon et al, 2019). In Arabidopsis, the AKIN10 (SnRK1α1) and AKIN11 (SnRK1α2) genes encode the catalytic α-subunits, and plants with double knockdown of AKIN10 and AKIN11 showed accelerated senescence (Baena-González et al, 2007).…”

A negative feedback loop of the TOR signaling moderates growth and enables rapid sensing of stress signals in plants

“…SnRK1 promotes the expression of Dark Induced 6 (DIN6) by phosphorylating bZIP63 53 , and Dark Induced 10 (DIN10) 4 . The expression of DIN6 and DIN10 is positively correlated with SnRK1 activity and thus widely used as SnRK1 signaling readout 4,[53][54][55] . In line with the reduced SnRK1 activity in the flz8 mutants, we found a significant downregulation of DIN6 and DIN10 transcript levels in the mutants (Fig.…”

“…To test these predictions, we first studied how SnRK1 signaling is regulated to sudden exposure to osmotic and salt stress. We estimated DIN6 expression as it is widely used to monitor transient and physiologically relevant SnRK1 signaling 4,[53][54][55] . Osmotic and salt stress treatments led to rapid induction of DIN6 expression at 1h which was downregulated at 3h indicating a rapid activation of SnRK1 signaling under stress.…”