Growth Arrest by Trehalose-6-Phosphate: An Astonishing Case of Primary Metabolite Control over Growth by Way of the SnRK1 Signaling Pathway      

Abstract

The strong regulation of plant carbon allocation and growth by trehalose metabolism is important for our understanding of the mechanisms that determine growth and yield, with obvious applications in crop improvement. To gain further insight on the growth arrest by trehalose feeding, we first established that starch-deficient seedlings of the plastidic phosphoglucomutase1 mutant were similarly affected as the wild type on trehalose. Starch accumulation in the source cotyledons, therefore, did not cause starvation and consequent growth arrest in the growing zones. We then screened the FOX collection of Arabidopsis (Arabidopsis thaliana) expressing full-length cDNAs for seedling resistance to 100 mM trehalose. Three independent transgenic lines were identified with dominant segregation of the trehalose resistance trait that overexpress the bZIP11 (for basic region/ leucine zipper motif) transcription factor. The resistance of these lines to trehalose could not be explained simply through enhanced trehalase activity or through inhibition of bZIP11 translation. Instead, trehalose-6-phosphate (T6P) accumulation was much increased in bZIP11-overexpressing lines, suggesting that these lines may be insensitive to the effects of T6P. T6P is known to inhibit the central stress-integrating kinase SnRK1 (KIN10) activity. We confirmed that this holds true in extracts from seedlings grown on trehalose, then showed that two independent transgenic lines overexpressing KIN10 were insensitive to trehalose. Moreover, the expression of marker genes known to be jointly controlled by SnRK1 activity and bZIP11 was consistent with low SnRK1 or bZIP11 activity in seedlings on trehalose. These results reveal an astonishing case of primary metabolite control over growth by way of the SnRK1 signaling pathway involving T6P, SnRK1, and bZIP11.

Acclimation of metabolism to light in Arabidopsis thaliana: the glucose 6‐phosphate/phosphate translocator GPT2 directs metabolic acclimation

“…T6P has previously been suggested to play a role in regulating photosynthetic capacity (Delatte et al . 2011). The concentration of shikimate was also found to be substantially higher in gpt2.2 leaves than in Ws‐4 wild type under all treatments, while the concentration of succinate was lower.…”

“…2009; Delatte et al . 2011; Nunes et al . 2013); however, our data show that there is no simple causal relationship between T6P and photosynthetic capacity.…”

Overexpression of the Trehalase Gene AtTRE1 Leads to Increased Drought Stress Tolerance in Arabidopsis and Is Involved in Abscisic Acid-Induced Stomatal Closure

“…T6P promotes biosynthetic processes in growing tissues in response to high Suc (Delatte et al, 2011b) and induces starch synthesis in the plastids via thioredoxin-mediated activation of AGPase (Kolbe et al, 2005). In developing tissues of Arabidopsis, T6P inhibits the activity of the SNF1-related kinase1 (SnRK1; Zhang et al, 2009), which is known to repress plant growth and to promote survival under stress (Baena-González et al, 2007).…”

“…In developing tissues of Arabidopsis, T6P inhibits the activity of the SNF1-related kinase1 (SnRK1; Zhang et al, 2009), which is known to repress plant growth and to promote survival under stress (Baena-González et al, 2007). T6P, SnRK1, and the sugar-regulated transcription factor basic region leucine zipper transcription factor11 (bZIP11) have been postulated to be part of a regulatory loop, controlling Suc availability and utilization in plants (Delatte et al, 2011b). Furthermore, a strong correlation between T6P levels and abscisic acid (ABA) sensitivity has recently been proposed .…”

The Energy-Signaling Hub SnRK1 Is Important for Sucrose-Induced Hypocotyl Elongation

“…SnRK1 controls metabolic enzymes directly by protein phosphorylation (Baena-González and Sheen, 2008). It also regulates greater than 1000 transcripts in response to carbohydrate availability, for example by adjusting bZIP transcription factor activity (Baena-González et al, 2007;Smeekens et al, 2010;Delatte et al, 2011;Matiolli et al, 2011;Mair et al, 2015). Both SnRK1-and hexokinasemediated sugar signaling involve specific sugars functioning as signaling molecules that provide cellular information concerning sugar availability.…”