Trehalose 6-phosphate (Tre6P), the intermediate of trehalose biosynthesis, is an essential signal metabolite in plants, linking growth and development to carbon status. The Suc-Tre6P nexus model ...postulates that Tre6P is both a signal and negative feedback regulator of Suc levels, forming part of a mechanism to maintain Suc levels within an optimal range and functionally comparable to the insulin-glucagon system for regulating blood Glc levels in animals. The target range and sensitivity of the Tre6P-Suc feedback control circuit can be adjusted according to the cell type, developmental stage, and environmental conditions. In source leaves, Tre6P modulates Suc levels by affecting Suc synthesis, whereas in sink organs it regulates Suc consumption. In illuminated leaves, Tre6P influences the partitioning of photoassimilates between Suc, organic acids, and amino acids via posttranslational regulation of phosphoenolpyruvate carboxylase and nitrate reductase. At night, Tre6P regulates the remobilization of leaf starch reserves to Suc, potentially linking starch turnover in source leaves to carbon demand from developing sink organs. Use of Suc for growth in developing tissues is strongly influenced by the antagonistic activities of two protein kinases: SUC-NON-FERMENTING-1-RELATED KINASE1 (SnRK1) and TARGET OF RAPAMYCIN (TOR). The relationship between Tre6P and SnRK1 in developing tissues is complex and not yet fully resolved, involving both direct and indirect mechanisms, and positive and negative effects. No direct connection between Tre6P and TOR has yet been described. The roles of Tre6P in abiotic stress tolerance and stomatal regulation are also discussed.
Next generation editors Lunn, John E
Journal of experimental botany,
03/2023, Letnik:
74, Številka:
5
Journal Article
Recenzirano
Odprti dostop
The Journal of Experimental Botany is pleased to announce the appointment of six early career researchers as editorial interns: Francesca Bellinazzo (Wageningen University and Research, the ...Netherlands), Konan Ishida (University of Cambridge, UK), Nishat Shayala Islam (Western University, Ontario, Canada), Chao Su (University of Freiburg, Germany), Catherine Walsh (Lancaster University, UK), and Arpita Yadav (University of Massachusetts Amherst, MA, USA) (Fig. 1). The aim of this programme is to help train the next generation of editors.
WRINKLED1 (WRI1), the transcriptional activator of fatty acid synthesis, was recently identified as a target of KIN10, a catalytic α-subunit of the SUCROSE-NON-FERMENTING1-RELATED PROTEIN KINASE1 ...(SnRK1). We tested the hypothesis that trehalose 6-phosphate (T6P), a signal of cellular sucrose status, can regulate fatty acid synthesis by inhibiting SnRK1. Incubation of
suspension cells in medium containing T6P, or overexpression of the
T6P synthase, OtsA, in
, significantly increased T6P levels, WRI1 levels, and fatty acid synthesis rates. T6P directly bound to purified recombinant KIN10 with an equilibrium dissociation constant (
) of 32 ± 6 μM based on microscale thermophoresis. GEMINIVIRUS REP-INTERACTING KINASE1 (GRIK1) bound to KIN10 (
19 ± 3 μM) and activated it by phosphorylation. In the presence of T6P, the GRIK1-KIN10 association was weakened by more than 3-fold (
68 ± 9.8 μM), which reduced both the phosphorylation of KIN10 and its activity. T6P-dependent inhibition of SnRK1 activity was reduced in extracts of individual
and
mutants relative to the wild type, while SnRK1 activity in
extracts was enhanced by T6P. These results indicate that the T6P sensitivity of SnRK1 in vivo is GRIK1/GRIK2 dependent. Based on our findings, we propose a mechanistic model that links sugar signaling and fatty acid homeostasis.
Abscisic acid (ABA) is a plant hormone that regulates a diverse range of cellular and molecular processes during development and in response to osmotic stress. In Arabidopsis (
), three Suc ...nonfermenting-1-related protein kinase2s (SnRK2s), SRK2D, SRK2E, and SRK2I, are key positive regulators involved in ABA signaling whose substrates have been well studied. Besides reduced drought-stress tolerance, the
mutant shows abnormal growth phenotypes, such as an increased number of leaves, under nonstress conditions. However, it remains unclear whether, and if so how, SnRK2-mediated ABA signaling regulates growth and development. Here, we show that the primary metabolite profile of
grown under nonstress conditions was considerably different from that of wild-type plants. The metabolic changes observed in the
were similar to those in an ABA-biosynthesis mutant,
, and both mutants showed a higher leaf emergence rate than wild type. Consistent with the increased amounts of citrate, isotope-labeling experiments revealed that respiration through the tricarboxylic acid cycle was enhanced in
These results, together with transcriptome data, indicate that the SnRK2s involved in ABA signaling modulate metabolism and leaf growth under nonstress conditions by fine-tuning flux through the tricarboxylic acid cycle.
Summary
Trehalose 6‐phosphate (Tre6P) is a sucrose signalling metabolite that has been implicated in regulation of shoot branching, but its precise role is not understood.
We expressed tagged forms ...of TREHALOSE‐6‐PHOSPHATE SYNTHASE1 (TPS1) to determine where Tre6P is synthesized in arabidopsis (Arabidopsis thaliana), and investigated the impact of localized changes in Tre6P levels, in axillary buds or vascular tissues, on shoot branching in wild‐type and branching mutant backgrounds.
TPS1 is expressed in axillary buds and the subtending vasculature, as well as in the leaf and stem vasculature. Expression of a heterologous Tre6P phosphatase (TPP) to lower Tre6P in axillary buds strongly delayed bud outgrowth in long days and inhibited branching in short days. TPP expression in the vasculature also delayed lateral bud outgrowth and decreased branching. Increased Tre6P in the vasculature enhanced branching and was accompanied by higher expression of FLOWERING LOCUS T (FT) and upregulation of sucrose transporters. Increased vascular Tre6P levels enhanced branching in branched1 but not in ft mutant backgrounds.
These results provide direct genetic evidence of a local role for Tre6P in regulation of axillary bud outgrowth within the buds themselves, and also connect Tre6P with systemic regulation of shoot branching via FT.
Many domesticated crop plants have been bred for increased apical dominance, displaying greatly reduced axillary branching compared to their wild ancestors. In maize, this was achieved through ...selection for a gain-of-function allele of the TCP transcription factor teosinte branched1 (tb1). The mechanism for how a dominant Tb1 allele increased apical dominance, is unknown. Through ChIP seq, RNA seq, hormone and sugar measurements on 1 mm axillary bud tissue, we identify the genetic pathways putatively regulated by TB1. These include pathways regulating phytohormones such as gibberellins, abscisic acid and jasmonic acid, but surprisingly, not auxin. In addition, metabolites involved in sugar sensing such as trehalose 6-phosphate were increased. This suggests that TB1 induces bud suppression through the production of inhibitory phytohormones and by reducing sugar levels and energy balance. Interestingly, TB1 also putatively targets several other domestication loci, including teosinte glume architecture1, prol1.1/grassy tillers1, as well as itself. This places tb1 on top of the domestication hierarchy, demonstrating its critical importance during the domestication of maize from teosinte.
The timing of the induction of flowering determines to a large extent the reproductive success of plants. Plants integrate diverse environmental and endogenous signals to ensure the timely transition ...from vegetative growth to flowering. Carbohydrates are thought to play a crucial role in the regulation of flowering, and trehalose-6-phosphate (T6P) has been suggested to function as a proxy for carbohydrate status in plants. The loss of TREHALOSE-6-PHOSPHATE SYNTHASE 1 (TPS1) causes Arabidopsis thaliana to flower extremely late, even under otherwise inductive environmental conditions. This suggests that TPS1 is required for the timely initiation of flowering. We show that the T6P pathway affects flowering both in the leaves and at the shoot meristem, and integrate TPS1 into the existing genetic framework of flowering-time control.
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