The plant energy sensor: evolutionary conservation and divergence of SnRK1 structure, regulation, and function

Abstract

The SnRK1 (SNF1-related kinase 1) kinases are the plant cellular fuel gauges, activated in response to energy-depleting stress conditions to maintain energy homeostasis while also gatekeeping important developmental transitions for optimal growth and survival. Similar to their opisthokont counterparts (animal AMP-activated kinase, AMPK, and yeast Sucrose Non-Fermenting 1, SNF), they function as heterotrimeric complexes with a catalytic (kinase) α subunit and regulatory β and γ subunits. Although the overall configuration of the kinase complexes is well conserved, plant-specific structural modifications (including a unique hybrid βγ subunit) and associated differences in regulation reflect evolutionary divergence in response to fundamentally different lifestyles. While AMP is the key metabolic signal activating AMPK in animals, the plant kinases appear to be allosterically inhibited by sugar-phosphates. Their function is further fine-tuned by differential subunit expression, localization, and diverse post-translational modifications. The SnRK1 kinases act by direct phosphorylation of key metabolic enzymes and regulatory proteins, extensive transcriptional regulation (e.g. through bZIP transcription factors), and down-regulation of TOR (target of rapamycin) kinase signaling. Significant progress has been made in recent years. New tools and more directed approaches will help answer important fundamental questions regarding their structure, regulation, and function, as well as explore their potential as targets for selection and modification for improved plant performance in a changing environment.

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

“…This often leads to a stop of plant growth involving a reduction in ribosomal protein synthesis, and in parallel, accumulation of protective metabolites or defense compounds. This switching of cellular energy metabolism is mediated by the activity of the evolutionarily conserved AMPK/ SNF1/SnRK1 kinase complex (Box 1; Crozet et al, 2014;Cutler et al, 2010;Hrabak et al, 2003;Kudla et al, 2010;Baena-González and Sheen, 2008;Broeckx et al, 2016).…”

“…Such a reprogramming of cellular (energy) metabolism by SnRK1 can, in principle, be achieved by two different modes of action: (1) by a direct phosphorylation of metabolic enzymes, resulting in either an altered enzymatic activity or protein stability; or (2) by changing transcript levels of key enzymes for metabolic pathways. In fact, various examples for both possibilities have been reported as recently reviewed by Broeckx et al (2016). Key metabolic enzymes in the cytosol, such as Suc-P synthase, NR, TPS5, and HMG-CoA reductase, have been identified as direct targets of SnRK1 in vitro (Jossier et al, 2009;Robertlee et al, 2017) and in vivo (Nukarinen et al, 2016).…”

Phytohormone ethylene-responsive Arabidopsis organ growth under light is in the fine regulation of Photosystem II deficiency-inducible AKIN10 expression

“…Intracellular energy deprivation is known to activate the two isoforms of the evolutionarily conserved energy sensor Snf1-related protein kinase (SnRK1), namely, ARABIDOPSIS KINASE (AKIN)10 and AKIN11 in Arabidopsis thaliana , that can turn catabolic and anabolic pathways on and off, respectively, in order to sustain cellular viability 17 . The chemical blockade of the photosystem (PS) II pathway with 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU), as well as the intervention condition of mitochondrial aerobic respiration by hypoxia, potently induces energy depletion and readily activates AKIN10 activity in Arabidopsis 18–20 .…”

Recent Discoveries on the Role of TOR (Target of Rapamycin) Signaling in Translation in Plants

“…A similar antagonistic relationship between the AMPK plant ortholog SnRK1 (Suc nonfermenting 1-related Kinase 1) and TOR-related signaling pathways in response to changing nutritional and energy conditions was suggested in Arabidopsis Broeckx et al, 2016;Baena-González and Hanson, 2017). In mammals, being upstream of TOR, SnRK1 may inhibit TOR activity via direct interaction and phosphorylation of upstream components of TOR signaling and Raptor-the regulatory subunit of the TOR complex (Nukarinen et al, 2016)-possibly leading to complex disassembly (Hughes Hallett et al, 2015).…”