Inhibition of SnRK1 by metabolites: Tissue-dependent effects and cooperative inhibition by glucose 1-phosphate in combination with trehalose 6-phosphate

Nunes, Clarice; Primavesi, Lucia F.; Patel, Mitul K.; Martínez‐Barajas, Eleazar; Powers, Stephen J.; Sagar, Ram; Fevereiro, Pedro; Davis, Benjamin G.; Paul, M. J.

doi:10.1016/j.plaphy.2012.11.011

Cited by 147 publications

(177 citation statements)

References 25 publications

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“…2011; Nunes et al . 2013); however, our data show that there is no simple causal relationship between T6P and photosynthetic capacity. HL induces a much larger transient increase in T6P in gpt2.2 than in wild‐type plants, yet no acclimation of P max occurs in the former case.…”

Section: Discussioncontrasting

confidence: 72%

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

Dyson

Allwood

Feil

et al. 2015

Plant Cell & Environment

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Mature leaves of plants transferred from low to high light typically increase their photosynthetic capacity. In A rabidopsis thaliana, this dynamic acclimation requires expression of GPT2, a glucose 6‐phosphate/phosphate translocator. Here, we examine the impact of GPT2 on leaf metabolism and photosynthesis. Plants of wild type and of a GPT2 knockout (gpt2.2) grown under low light achieved the same photosynthetic rate despite having different metabolic and transcriptomic strategies. Immediately upon transfer to high light, gpt2.2 plants showed a higher rate of photosynthesis than wild‐type plants (35%); however, over subsequent days, wild‐type plants acclimated photosynthetic capacity, increasing the photosynthesis rate by 100% after 7 d. Wild‐type plants accumulated more starch than gpt2.2 plants throughout acclimation. We suggest that GPT2 activity results in the net import of glucose 6‐phosphate from cytosol to chloroplast, increasing starch synthesis. There was clear acclimation of metabolism, with short‐term changes typically being reversed as plants acclimated. Distinct responses to light were observed in wild‐type and gpt2.2 leaves. Significantly higher levels of sugar phosphates were observed in gpt2.2. We suggest that GPT2 alters the distribution of metabolites between compartments and that this plays an essential role in allowing the cell to interpret environmental signals.

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Section: Discussioncontrasting

confidence: 72%

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

Dyson

Allwood

Feil

et al. 2015

Plant Cell & Environment

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“…Both SnRK1-and hexokinasemediated sugar signaling involve specific sugars functioning as signaling molecules that provide cellular information concerning sugar availability. For example, SnRK1 activity is thought to be regulated by trehalose-6-P (Tre6P), whose concentration tracks the cellular concentration of Suc (Lunn et al, 2006;Zhang et al, 2009;Nunes et al, 2013aNunes et al, , 2013bYadav et al, 2014). Tre6P is synthesized from UDP Glc and Glc-6-P, which are derived from mobilized and transported Suc, and also directly from photosynthesis.…”

mentioning

confidence: 99%

“…Of 11 TPS homologs encoded by the Arabidopsis genome, TREHALOSE-6-PHOSPHATE SYNTHASE1 (TPS1) synthesizes Tre6P in plants (Gómez et al, 2010;Vandesteene et al, 2010), and TPS2 and TPS4 are catalytically active in yeast complementation assays (Delorge et al, 2015). Tre6P is believed to regulate SnRK1-mediated signaling by suppressing the activity of SNF1-RELATED PRO-TEIN KINASE1.1 (KIN10/AKIN10/SnRK1.1), which is a catalytic subunit of SnRK1 that is fundamental to the signaling role of SnRK1 (Baena-González et al, 2007;Zhang et al, 2009;Nunes et al, 2013aNunes et al, , 2013b.…”

mentioning

confidence: 99%

“…Signaling by Tre6P and KIN10 is also important for the regulation of growth rates. Growth is increased by Suc in the presence of Tre6P (Schluepmann et al, 2003;Paul et al, 2010), but the lack of a quantitative (correlative) relationship between relative growth rates and [Tre6P] suggests that a threshold [Tre6P] is required for growth to occur (Nunes et al, 2013a(Nunes et al, , 2013b. Therefore, it has been suggested that control of KIN10/11 by [Tre6P] may prime the regulation of growth-related genes to capitalize upon increased energy availability, rather than by inducing growth directly (Nunes et al, 2013a(Nunes et al, , 2013b.…”

mentioning

confidence: 99%

“…Growth is increased by Suc in the presence of Tre6P (Schluepmann et al, 2003;Paul et al, 2010), but the lack of a quantitative (correlative) relationship between relative growth rates and [Tre6P] suggests that a threshold [Tre6P] is required for growth to occur (Nunes et al, 2013a(Nunes et al, , 2013b. Therefore, it has been suggested that control of KIN10/11 by [Tre6P] may prime the regulation of growth-related genes to capitalize upon increased energy availability, rather than by inducing growth directly (Nunes et al, 2013a(Nunes et al, , 2013b. Remarkably, the impact of this pathway is sufficiently global that its manipulation can increase maize (Zea mays) yields by almost 50% (Nuccio et al, 2015) and increase the yield and drought tolerance of wheat (Triticum aestivum; Griffiths et al, 2016).…”

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confidence: 99%

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

et al. 2017

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Emerging seedlings respond to environmental conditions such as light and temperature to optimize their establishment. Seedlings grow initially through elongation of the hypocotyl, which is regulated by signaling pathways that integrate environmental information to regulate seedling development. The hypocotyls of Arabidopsis (Arabidopsis thaliana) also elongate in response to sucrose. Here, we investigated the role of cellular sugar-sensing mechanisms in the elongation of hypocotyls in response to Suc. We focused upon the role of SnRK1, which is a sugar-signaling hub that regulates metabolism and transcription in response to cellular energy status. We also investigated the role of TPS1, which synthesizes the signaling sugar trehalose-6-P that is proposed to regulate SnRK1 activity. Under light/dark cycles, we found that Suc-induced hypocotyl elongation did not occur in tps1 mutants and overexpressors of KIN10 (AKIN10/SnRK1.1), a catalytic subunit of SnRK1. We demonstrate that the magnitude of Suc-induced hypocotyl elongation depends on the day length and light intensity. We identified roles for auxin and gibberellin signaling in Suc-induced hypocotyl elongation under short photoperiods. We found that Suc-induced hypocotyl elongation under light/dark cycles does not involve another proposed sugar sensor, HEXOKINASE1, or the circadian oscillator. Our study identifies novel roles for KIN10 and TPS1 in mediating a signal that underlies Suc-induced hypocotyl elongation in light/dark cycles.

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Redox state‐dependent modulation of plant SnRK1 kinase activity differs from AMPK regulation in animals

et al. 2017

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The evolutionarily highly conserved SNF1‐related protein kinase (SnRK1) protein kinase is a metabolic master regulator in plants, balancing the critical energy consumption between growth‐ and stress response‐related metabolic pathways. While the regulation of the mammalian [AMP‐activated protein kinase (AMPK)] and yeast (SNF1) orthologues of SnRK1 is well‐characterised, the regulation of SnRK1 kinase activity in plants is still an open question. Here we report that the activity and T‐loop phosphorylation of AKIN10, the kinase subunit of the SnRK1 complex, is regulated by the redox status. Although this regulation is dependent on a conserved cysteine residue, the underlying mechanism is different to the redox regulation of animal AMPK and has functional implications for the regulation of the kinase complex in plants under stress conditions.

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Inhibition of SnRK1 by metabolites: Tissue-dependent effects and cooperative inhibition by glucose 1-phosphate in combination with trehalose 6-phosphate

Cited by 147 publications

References 25 publications

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

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

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

Redox state‐dependent modulation of plant SnRK1 kinase activity differs from AMPK regulation in animals

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