Impact of the SnRK1 protein kinase on sucrose homeostasis and the transcriptome during the diel cycle

Abstract

SNF1-Related Kinase 1 (SnRK1) is an evolutionarily conserved protein kinase with key functions in energy management during stress responses in plants. To address a potential role of SnRK1 under favourable conditions, we performed a metabolomic and transcriptomic characterization of rosettes of 20-d-old Arabidopsis (Arabidopsis thaliana) plants of SnRK1 gain- and loss-of-function mutants during the regular diel cycle. Our results show that SnRK1 manipulation alters the sucrose and trehalose 6-phosphate (Tre6P) relationship, influencing how the sucrose content is translated into Tre6P accumulation and modulating the flux of carbon to the tricarboxylic acid cycle downstream of Tre6P signalling. On the other hand, daily cycles of Tre6P accumulation were accompanied by changes in SnRK1 signaling, leading to a maximum in the expression of SnRK1-induced genes at the end of the night, when Tre6P levels are lowest, and to a minimum at the end of the day, when Tre6P levels peak. The expression of SnRK1-induced genes was strongly reduced by transient Tre6P accumulation in an inducible Tre6P synthase (otsA) line, further suggesting the involvement of Tre6P in the diel oscillations in SnRK1 signaling. Transcriptional profiling of wild-type plants and SnRK1 mutants also uncovered defects that are suggestive of an iron sufficiency response and of a matching induction of sulfur acquisition and assimilation when SnRK1 is depleted. In conclusion, under favourable growth conditions, SnRK1 plays a role in sucrose homeostasis and transcriptome remodelling in autotrophic tissues and its activity is influenced by diel fluctuations in Tre6P levels.

Sugars and the speed of life—Metabolic signals that determine plant growth, development and death

“…However, the mechanism underlying this interaction remains unresolved as the abundance of TPS1, the principal catalytically active TPS, was not altered accordingly. This control of sucrose homeostasis in the diel cycle was described for favourable growing conditions (Peixoto et al, 2021), suggesting that SnRK1 also has a function under non-stress conditions. This is in agreement with its role in normal developmental processes, e.g.…”

Triosephosphate export from chloroplasts regulates flavonoid biosynthesis and permits high light acclimation through the inactivation of SnRK1

“…On the other hand, perturbed TOR function leads to starch and sugar accumulation (Caldana et al, 2013, Salem et al, 2018, Zhang et al, 2018). Due to the strong correlation between sugar, mainly sucrose, and T6P contents (Carillo et al, 2013, Yadav et al, 2014, Peixoto et al, 2021), it could be hypothesized that FB is (further) stimulated when TOR activity is suppressed (in HL) because high sugar levels may result in stronger inactivation of SnRK1 (like in the sugar over accumulating starch mutants). The involvement of TOR and its interconnection with SnRK1 in the regulation of FB during HL acclimation should be analyzed in the future using (double) mutants with altered activities of both factors.…”

“…The newly established connection between FB activation in HL and SnRK1 activity gets strong support from previous studies: PAP1 is repressed by overexpressing KIN10 in protoplast assays and excess of KIN10 diminished sucrose-induced activation of FB in planta (Baena-Gonzalez et al, 2007). On the contrary, FB is activated, and pathway genes are de-repressed in partial loss-of-function snrk1α1 − / − snrk1α2 +/ − and snrk1α1-3 amiRNAi KIN11 mutants even under normal growth conditions (Nukarinen et al, 2016, Peixoto et al, 2021, Wang et al, 2021). Overexpression of T6P PHOSPHATASE leading to the activation of SnRK1 in stably transformed lines ( otsB , Zhang et al, 2009) repressed, but increased T6P level in T6P SYNTHASE ( otsA ) overexpressor plants induced FB (Schluepmann et al, 2003, Zhang et al, 2009, Wingler et al, 2012).…”

Turning the Knobs: The Impact of Post-translational Modifications on Carbon Metabolism

“…The increase of AGPase in the monomeric state could be reproduced by sucrose but not glucose, suggesting that the process may obey the sucrose-T6P nexus (Baena-González and Lunn, 2020;Peixoto et al, 2021). The increase in sucrose levels leads to increased T6P accumulation, a process that might be regulated by SnRK1 (Peixoto et al, 2021), which in turn, feedback regulates carbon partitioning between sucrose and starch. Further analysis considering the diel fluctuation in the sink and source tissues on the regulation of SnRK1 and T6P in starch metabolism is needed to clarify this pathway.…”

“…Interestingly, the artificial increase of T6P through the overexpression of TREHALOSE PHOSPHATE SYNTHASE1 (TPS1) also leads to the accumulation of AGPase in a monomeric state (Kolbe et al, 2005). The increase of AGPase in the monomeric state could be reproduced by sucrose but not glucose, suggesting that the process may obey the sucrose-T6P nexus (Baena-González and Lunn, 2020;Peixoto et al, 2021). The increase in sucrose levels leads to increased T6P accumulation, a process that might be regulated by SnRK1 (Peixoto et al, 2021), which in turn, feedback regulates carbon partitioning between sucrose and starch.…”