The low energy signaling network

Abstract

Stress impacts negatively on plant growth and crop productivity, caicultural production worldwide. Throughout their life, plants are often confronted with multiple types of stress that affect overall cellular energy status and activate energy-saving responses. The resulting low energy syndrome (LES) includes transcriptional, translational, and metabolic reprogramming and is essential for stress adaptation. The conserved kinases sucrose-non-fermenting-1-related protein kinase-1 (SnRK1) and target of rapamycin (TOR) play central roles in the regulation of LES in response to stress conditions, affecting cellular processes and leading to growth arrest and metabolic reprogramming. We review the current understanding of how TOR and SnRK1 are involved in regulating the response of plants to low energy conditions. The central role in the regulation of cellular processes, the reprogramming of metabolism, and the phenotypic consequences of these two kinases will be discussed in light of current knowledge and potential future developments.

Keywords: SnRK1; T6P; TOR; bZIP; energy signaling; metabolism; stress.

FIGURE 1

The low energy syndrome (LES) is a collection of phenotypical consequences of stress condition and drives plant acclimation to environmental changes. The figure aims at depicting all causes and consequences described so far, but LES can be induced by one or multiple stress conditions and the acclimation process can include only a subset of the depicted outcomes.

FIGURE 2

Domain structure and nomenclature of Arabidopsis SnRK1 and TOR subunits. SnRK1 structures include the conserved phosphorylation sites on T-loop of the α-subunit. The α-subunit contains the kinase domain, together with an auto-inhibitory (UBA) domain and a kinase associated (KA1) domain where the interaction with the ß-subunit takes place. The β-subunit (except in SnRK1ß3) contains a starch-binding domain (Ávila-Castañeda et al., 2014) and binds to the γ-subunit at the association with the SNF1 complex (ASC) domain. The plant-specific βγ-subunit might take the place described for the γ-subunit in mammals and yeast, containing multiple cystathionine β-synthase (CBS) domains. TOR contain two FAT domains (FRAP, ATM, and TRAP) probably constituting the active center, a PI3K kinase domain, a FRB domain (FKB12-rapamycin binding) for interaction with the inhibitor FKB12, and a number of HEAT repeats [huntingtin, elongation factor 3 (EF3), protein phosphatase 2A (PP2A), TOR1] for the interaction with RAPTOR. Next to HEAT repeats, RAPTOR contains a RNC domain (raptor N-terminal conserved/putative caspase domain) and a number of WD40 repeat domains (Hay and Sonenberg, 2004). Nomenclature as described before (Robaglia et al., 2012).

FIGURE 3

Simplified summary of SnRK1 effects on cellular processes by direct phosphorylation of target proteins and by alteration of mRNA levels of many genes via transcription factors or the miRNA machinery. Arrows indicate a positive or negative regulatory effect; P denotes phosphorylation. Abbreviations: HMGCoAR, 3-hydroxy-3- methylglutaryl-coenzyme A reductase; SPS, sucrose phosphate synthase; NR, nitrate reductase; TPS, trehalose phosphate synthase; bZIP TF, basic leucine zipper transcription factor; ProDH, proline dehydrogenase; DIN6/ASN1, dark inducible 6/asparagine synthetase 1; TCP2, teosinte branched 1, cycloidea and PCF transcription factor 2; Hsp70–15, heat shock protein 70–15.

FIGURE 4

The low energy syndrome involves processes regulated by TOR and SnRK1 central to the adaptation to energy limitation. The kinases SnRK1 and TOR are affected by energy availability and mediate transcription, translation, enzyme activity, and the accumulation of metabolites in order to drive adaptation to different conditions. Gray arrows indicate processes shut down in response to energy limitation and the dashed arrow denotes a probable interaction between these two signaling pathways. Abbreviations: SnAK, SnRK1-activating kinase; PP2C, type 2C protein phosphatase; TPS, trehalose phosphate synthase; T6P, trehalose 6-phosphate; TPP, trehalose phosphate phosphatase; eIF3h, eukaryotic translation initiation factor 3 subunit H; S6K, ribosomal protein S6 kinase.