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

Abstract

The evolutionarily conserved SNF1-related protein kinase 1 (SnRK1) kinase complex is a key regulator in adjusting cellular metabolism during starvation, stress conditions, and growth-promoting conditions. Over the last two decades, extensive genetic evidence for a widespread SnRK1 signaling network has accumulated. It is now well established that SnRK1 is a central integrator of energy signaling. However, little is known about the connections between the cytoplasmic and nuclear-localized SnRK1 and plastids and mitochondria as the main energy-producing compartments in the cell. Here, we review recent findings indicating how SnRK1 affects metabolic adaptation, including plastidial and mitochondrial functions. Special emphasis is put on identified direct targets of SnRK1, which would eventually enable cross talk with organelles. In this context, a number of transcription factors (TFs) are emerging as mediators of SnRK1 signaling, potentially linking SnRK1 activity to organellar functions. Furthermore, many SnRK1 targets act in various hormonal signaling pathways, which are at least partly localized in plastids. With this review, we summarize the current knowledge on SnRK1 organelle interaction and provide ideas on the potential molecular mechanisms governing these interactions. METABOLIC REPROGRAMMING BY SNRK1 KINASE ACTIVITY UNDER DIFFERENT GROWTH AND STRESS CONDITIONSAlready under optimal growth conditions, plants need to continuously adjust their metabolic balance between autotrophic growth based on photosynthesis during the day and respiration during the night. At daytime, sugars and other metabolites are produced by photosynthesis in chloroplasts and further distributed to be used in other metabolic pathways at different cellular compartments or transported to nonphotosynthetic sink tissues. During the night, starch and sugars supply carbon equivalents for respiration, providing the necessary energy for further growth and metabolic activities. Additionally, metabolic reprogramming is required for plants to adjust their metabolism to diverse biotic and abiotic environmental stimuli. 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.,

Mitochondrial Energy Signaling and Its Role in the Low-Oxygen Stress Response of Plants

“…KIN10 is conserved across plants and has been shown to interact with several transcription factors (Kleinow et al, 2009;Tsai and Gazzarrini, 2012;Zhai et al, 2017). The integrative role of KIN10 is further discussed by Wurzinger et al (2018) as part of this Focus Issue. In the mitochondrial retrograde response, CDKE1 has been proposed to act independently of ABI4 (Blanco et al, 2014).…”

“…Other posttranslational modifications such as protein phosphorylation (e.g. through SnRK1, as discussed by Wurzinger et al [2018] in this Focus Issue) and protein Lys acetylation also critically rely on substrates that can be derived from mitochondrial energy metabolism, i.e. ATP and acetyl-CoA.…”

Molecular signatures of local adaptation to light in Norway Spruce: role of lignin mediated immunity

“…Biotic and abiotic stresses lead to energy deficit in the plant cell that triggers the transcription of genes enabling the plants to withstand and survive under low-energy conditions. The SNF1-RELATED KINASE1 ( SnRK1 ) signalling cascade is activated to combat low-energy often by stopping the plant growth involving a reduction in ribosomal protein synthesis, and a simultaneous accumulation of protective metabolites or defense compounds coupled with tuning of the metabolic processes in response to starvation (Baena-Gonzalez et al , 2007, Wurzinger et al , 2018). SnRK1 signalling cascade involves interaction of FLZ gene family members with the kinase subunits.…”

Retrograde signalling as an informant of circadian timing

“…1). SnRK1 regulates metabolism by phosphorylating metabolic enzymes, with its activity regulated in part through control of the AKIN10 catalytic subunit (Wurzinger et al, 2018). SnRK1 activity is additionally repressed by the accumulation of trehalose-6-phosphate, which serves as a molecular indicator of intracellular sucrose (Figueroa & Lunn, 2016).…”