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First published online February 4, 2009; 10.1104/pp.108.133934 Plant Physiology 149:1860-1871 (2009) © 2009 American Society of Plant Biologists OPEN ACCESS ARTICLE
Inhibition of SNF1-Related Protein Kinase1 Activity and Regulation of Metabolic Pathways by Trehalose-6-Phosphate1,[W],[OA]Plant Science, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, United Kingdom (Y.Z., L.F.P., D.J., P.J.A., R.A.C.M., S.J.P., M.J.P.); Molecular Plant Physiology, Utrecht University, 3584CH Utrecht, The Netherlands (H.S., T.D.); Department of Biomedical Analysis, Utrecht University, 3584CA Utrecht, The Netherlands (T.D.); and Genetics, Evolution, and Environment, University College London, London WC1E 6BT, United Kingdom (A.W.)
Trehalose-6-phosphate (T6P) is a proposed signaling molecule in plants, yet how it signals was not clear. Here, we provide evidence that T6P functions as an inhibitor of SNF1-related protein kinase1 (SnRK1; AKIN10/AKIN11) of the SNF1-related group of protein kinases. T6P, but not other sugars and sugar phosphates, inhibited SnRK1 in Arabidopsis (Arabidopsis thaliana) seedling extracts strongly (50%) at low concentrations (1–20 µM). Inhibition was noncompetitive with respect to ATP. In immunoprecipitation studies using antibodies to AKIN10 and AKIN11, SnRK1 catalytic activity and T6P inhibition were physically separable, with T6P inhibition of SnRK1 dependent on an intermediary factor. In subsequent analysis, T6P inhibited SnRK1 in extracts of all tissues analyzed except those of mature leaves, which did not contain the intermediary factor. To assess the impact of T6P inhibition of SnRK1 in vivo, gene expression was determined in seedlings expressing Escherichia coli otsA encoding T6P synthase to elevate T6P or otsB encoding T6P phosphatase to decrease T6P. SnRK1 target genes showed opposite regulation, consistent with the regulation of SnRK1 by T6P in vivo. Analysis of microarray data showed up-regulation by T6P of genes involved in biosynthetic reactions, such as genes for amino acid, protein, and nucleotide synthesis, the tricarboxylic acid cycle, and mitochondrial electron transport, which are normally down-regulated by SnRK1. In contrast, genes involved in photosynthesis and degradation processes, which are normally up-regulated by SnRK1, were down-regulated by T6P. These experiments provide strong evidence that T6P inhibits SnRK1 to activate biosynthetic processes in growing tissues.
Suc and trehalose are widespread nonreducing disaccharides that function as translocated carbon sources and stress protection compounds. Plants and cyanobacteria are the only organisms in which the pathways of trehalose and Suc synthesis coexist. In the majority of plants, trehalose occurs in trace amounts only, prohibiting a function as a carbon source. This raises the question of the role of the trehalose pathway in plants, given the large number and ubiquity of putative genes encoding enzymes for trehalose synthesis (Avonce et al., 2006  ; Lunn, 2007). Many of these genes are subject to a high level of regulation at the gene (Paul et al., 2008) and posttranslational (Harthill et al., 2006) levels, suggesting an important function. This is confirmed in transgenic and mutant plants with modified trehalose pathway gene expression, which show a range of phenotypes. For example, a trehalose-6-P synthase (TPS1) has been shown to be essential for embryo development (Eastmond et al., 2002) and for normal vegetative growth and the transition to flowering (Van Dijken et al., 2004). Overexpression of TPS from different species, for example, otsA encoding Escherichia coli TPS, produces effects on sugar utilization in seedlings (Schluepmann et al., 2003) and on vegetative and photosynthetic phenotypes (Pellny et al., 2004; Almeida et al., 2007; Stiller et al., 2008), opposite in nature to seedling and photosynthetic phenotypes of plants expressing E. coli otsB encoding trehalose-6-P phosphatase (TPP; Schluepmann et al., 2003; Pellny et al., 2004). The phenotype of the maize (Zea mays) ramosa3 mutant has been attributed to a knockout of a TPP gene normally expressed in discrete domains subtending axillary meristems (Satoh-Nagasawa et al., 2006). This gives rise to an inflorescence architecture that aids the efficient packing and harvesting of seeds. Trehalose-6-P (T6P) has been found to stimulate starch synthesis via redox activation of ADP-Glc pyrophosphorylase (Kolbe et al., 2005), and T6P responds to light and sugar in relation to carbon status (Lunn et al., 2006). This supports a role for T6P in signaling the sugar status of the cytosol to the chloroplast and thereby activating starch synthesis. However, most of the phenotypes produced where the pathway has been genetically modified in mutant and transgenic lines, which also extend to effects on abiotic stress resistance (Garg et al., 2002; Avonce et al., 2004), cell division, cell walls (Gómez et al., 2006), and cell shape (Chary et al., 2008), cannot be explained simply in terms of the effect on starch metabolism but rather support a more central function.
In some fungi, T6P inhibits hexokinase, an enzyme implicated in sugar signaling in plants and other organisms (Moore et al., 2003 Here, we provide evidence for a function of T6P as an inhibitor of SnRK1 activity. First, we show that low micromolar concentrations of T6P inhibit SnRK1 activity in Arabidopsis (Arabidopsis thaliana) seedling extracts and other young plant material, but not in mature leaves. Second, we show that T6P inhibits SnRK1 at a site distinct and separable from the SnRK1 catalytic site via an intermediary factor. This as yet unknown intermediary factor was not found in mature leaves. Third, we establish effects on gene expression in seedlings with elevated T6P consistent with inhibition of SnRK1 in vivo. Overall, the data provide strong evidence for a function of T6P as an inhibitor of SnRK1 to promote biosynthetic reactions in growing tissues.
T6P Inhibits SnRK1 in G-25 Desalted Extracts
SnRK1 activity was measured using desalted tissue extracts with and without T6P in the assay and in comparison with other sugars and sugar phosphates. Inhibition of SnRK1 activity from Arabidopsis seedling extracts by T6P was observed at 1 µM T6P; at 20 µM T6P, SnRK1 activity was inhibited by 50% (Fig. 1A
). In SnRK1 assays of a range of tissues from Arabidopsis (Fig. 1B) and other plant species (Supplemental Fig. S1), T6P inhibited SnRK1 activity in all except fully grown leaves. No inhibition of SnRK1 by T6P was observed from representatives of the nonplant species yeast (Saccharomyces cerevisiae), house fly (Musca domestica), soil nematode (Caenorhabditis elegans), and fresh liver (Supplemental Fig. S1). Arabidopsis seedlings were then focused on as a system in which to study inhibition of SnRK1 by T6P. Minimal effects of 1 mM Glc, Suc, trehalose, Suc-6-P, and Fru-2,6-bisP were observed in comparison with 1 mM T6P (Fig. 1C). Glc-6-P (G6P; 1 mM) inhibited SnRK1 by 15% (Fig. 1C) and 10 mM G6P by 70% (data not shown), as reported previously (Toroser et al., 2000
In Vivo Evidence of Inhibition of SnRK1 by T6P
We then sought evidence for the inhibition of SnRK1 by T6P in vivo, making use of marker gene expression as a footprint of SnRK1 activity. In a recent study using a mesophyll protoplast expression system to transiently overexpress SnRK1 (AKIN10), Baena-González et al. (2007)
We then went on to perform a gene expression profiling experiment using microarrays. otsA and otsB were compared with the wild type, and otsA data were compared with data obtained from overexpression of KIN10 (Baena-González et al., 2007 ). Micoarray data were filtered using a t test with Benjamini and Hochberg multiple test correction (P < 0.05) with a 2-fold change cutoff. Changes in gene expression in otsB were small, with most changes less than 2-fold (Supplemental Table S1) in accordance with Q-RT-PCR data. In otsA, changes in gene expression were far larger. Of the markers repressed by SnRK1 that were established by Baena-González et al. (2007), 296 showed significant induction in otsA and only four showed repression (Fig. 3A
). This would be predicted if T6P inhibited SnRK1 in vivo. Of markers normally induced by SnRK1, 316 showed repression compared with the wild type in otsA (Fig. 3B) and only 12 genes showed a greater than 2-fold change in the opposite direction. These data support an effect in otsA that is consistent with inhibition of SnRK1 by T6P in vivo.
To gain a more complete indication of changes in gene expression in otsA, further analysis was conducted using FatiGO (http://fatigo.bioinfo.cipf.es/; Al-Shahrour et al., 2004 ) to determine overrepresentation or underrepresentation of specific biological processes. In comparison with the wild type, it was found that genes of the "biosynthetic process" category (Supplemental Fig. S3; Supplemental Table S2) were overrepresented among the genes up-regulated in otsA transgenics, whereas genes of the "regulation of biological process" category were underrepresented. These data were compared with those obtained by Baena-González et al. (2007) for KIN10 overexpression in the transient protoplast expression system. The same pattern was found for the genes that are down-regulated by KIN10 (Baena-González et al., 2007), indicating opposite effects of otsA and KIN10 overexpression. Further comparison of otsA and KIN10 transgenics was performed using MapMan analysis to display gene expression data on metabolic pathways (Usadel et al., 2005). Clear effects were observed in plants expressing otsA (Fig. 4A
), including down-regulation of photosynthetic genes (light reactions, Calvin cycle, and photorespiration), starch breakdown, gluconeogenesis/glyoxylate cycle, and an overall induction of genes involved in the tricarboxylic acid (TCA) cycle, mitochondrial electron transport, and nucleotide synthesis. Other effects include the up-regulation of aromatic amino acid and purine synthesis and the down-regulation of branched-chain amino acid degradation. These changes were opposite to the effect of KIN10 overexpression (Fig. 4B). The PageMan program was then employed to display data in terms of functional ontology (Usadel et al., 2006), confirming MapMan analysis showing opposite regulation of genes in photosynthesis, glycolysis, TCA cycle, mitochondrial electron transport, amino acid, protein, and nucleotide metabolism in otsA-expressing and KIN10-overexpressing plants (Fig. 5
). Genes not categorized as SnRK1 markers (Baena-González et al., 2007) were also affected (Supplemental Table S1), particularly genes involved in metabolism, which were induced in otsA transgenics (e.g. UDP-glucoronosyl/UDP-glucosyl transferase, ADP-Glc pyrophosphorylase, Trp synthase), consistent with the induction of biosynthetic reactions in otsA transgenics. DRE2B (At2g38340), a transcription factor gene shown to induce drought tolerance (Wang et al., 2008), was also strongly induced (Supplemental Table S1). Overall, the data strongly support the inhibition of SnRK1 by T6P.
T6P Inhibition of SnRK1 Is Noncompetitive with Respect to ATP at a Site Distinct and Physically Separable from the Catalytic Site
In further analysis of SnRK1 activities in seedlings, effects of ATP concentration were determined and data were fitted to kinetic models (Segel, 1993
SnRK1 was then assayed in supernatant of seedling extracts after immunoprecipitation with antibodies to AKIN10 and AKIN11 of the catalytic component of SnRK1. AKIN10 antibody removed 57.1% of SnRK1 activity, and AKIN11 antibody removed 38.3% of SnRK1 activity (95.4% of total, confirmed when both antibodies were added together; Fig. 7A ). The activities remaining in the supernatant contributed by AKIN10 and AKIN11 were still inhibited by T6P, indicating that T6P inhibits both AKIN10 and AKIN11.
The pellet precipitated by AKIN10 and AKIN11 antibodies from seedling extracts was then resuspended and assayed for SnRK1 activity. SnRK1 activity was recovered (>90%) but was no longer inhibited by T6P (Fig. 7B). To determine whether this was due to a requirement for a factor not precipitated by AKIN10 and AKIN11 antibodies, supernatant from immunoprecipitated extract was added back to resuspended pellet. This restored inhibition by T6P to a large extent (Fig. 7B). Inhibition of SnRK1 by T6P was also lost during anion-exchange chromatographic purification of SnRK1 (Fig. 7C) but could be restored by adding supernatant from immunoprecipitated seedling extracts. Boiled supernatant from seedlings did not restore inhibition by T6P (Fig. 7C). These experiments show that an intermediary factor separable from SnRK1 activity is necessary for inhibition of SnRK1 by T6P.
To establish if the difference in T6P inhibition between seedlings and mature leaves could be attributed to the intermediary factor, experiments were performed using immunoprecipitated SnRK1 and supernatant from seedlings and mature leaves and recombining SnRK1 activity in immunoprecipitate from one with supernatant from the other (Fig. 7D). It was found that mature leaf supernatant could not restore T6P inhibition when added to resuspended immunoprecipitated SnRK1 from seedlings, but seedling supernatant added to resuspended immunoprecipitated SnRK1 from mature leaves did result in inhibition by T6P (Fig. 7D). This shows that an additional factor necessary for T6P inhibition of SnRK1 is present in seedling extracts but not in mature leaf extracts, which can explain the lack of T6P inhibition in mature leaves.
In plants, the pathways for the synthesis of the two widespread nonreducing disaccharides in nature, trehalose and Suc, coexist (Paul et al., 2008 ). While the function of Suc as a carbon source in plants is known, the function of the trehalose pathway has been more enigmatic. Here, we provide evidence that T6P, the precursor of trehalose, functions as an inhibitor of SnRK1 (AKIN10/AKIN11) of the SNF1-related group of protein kinases in plants.
In seedlings and young plant material, SnRK1 activity was inhibited by low micromolar concentrations of T6P. In seedlings, which provided a convenient system to study T6P inhibition of SnRK1 in more detail, activity was inhibited by up to 50% between 1 and 20 µM T6P (Fig. 1A). Inhibition of SnRK1 by 1 and 10 mM G6P by 15% (Fig. 1C) and 70% (data not shown), respectively, was also found. This confirms the findings of Toroser et al. (2000)
SnRK1 was recently shown to affect the transcript abundance of approximately 1,000 genes in Arabidopsis in a central role in the response to starvation (Baena-González et al., 2007
Comparison of microarray data of otsA with cells overexpressing KIN10 (Baena-González et al., 2007
Further analysis of seedling extract SnRK1 activity data obtained at varying T6P and ATP concentrations showed that inhibition of SnRK1 by T6P was noncompetitive with respect to ATP (Fig. 6). Kinetic modeling of these data predicted partial noncompetitive mixed-type inhibition where T6P and ATP interact independently at different sites (Supplemental Fig. S4). This analysis was performed on kinetic data obtained with G-25 desalted extracts to remove small Mr compounds such as T6P. Ideally, kinetic analysis would be performed with a purified SnRK1 complex. However, a SnRK1 complex complete with interacting factors has never been purified or expressed from plants. In further work, it was possible to substantiate and extend the prediction of the kinetic model by showing that the component responsible for T6P inhibition is distinct and physically separable from SnRK1 catalytic activity. This was done by precipitating SnRK1 activity with AKIN10 and AKIN11 antibodies and through partial purification of SnRK1 activity by anion-exchange chromatography. Activities purified in these ways were no longer inhibited by T6P (Fig. 7, B and C). An intermediary factor necessary for T6P inhibition was separated in the supernatant of seedling extracts from SnRK1 activity in the immunoprecipitate. When it was added back to immunoprecipitated SnRK1 and anion-exchange purified SnRK1, T6P inhibition of SnRK1 activity was restored (Fig. 7, B and C). The identity of this intermediary factor has not been established. Being heat labile (Fig. 7C) and not retained on G-25 Sephadex, it is likely to be a protein. It is becoming increasingly clear that the regulation of SnRK1 is particularly complex, involving a growing number of interacting proteins (Polge and Thomas, 2007
T6P inhibition was not found for SnRK1 equivalents of the heterotrophs surveyed (Supplemental Fig. S1). This study was not exhaustive, so it does not rule out the possibility that regulation of a similar nature exists in organisms other than plants. In plants, we provide evidence that an important function of the trehalose pathway is to regulate SnRK1 in growing tissues. Our data do not exclude other functions for T6P, particularly as the TPS and TPP genes for the pathway show expression patterns in a range of tissues, including mature leaves, where T6P regulates starch synthesis via redox activation of AGPase (Kolbe et al., 2005
Overall, our data provide evidence that T6P is another part of the complex network that regulates SnRK1 in plants, where it counters SnRK1 activity in young tissues to promote biosynthetic reactions. In plants, unlike other organisms, trehalose is not a major end product except in a few resurrection species. Hence, T6P is removed from major pathway flux and can fluctuate without compromising other functions, unlike central intermediates (e.g. G6P), which have a limited dynamic range. Suc has been shown to lead to a large (30-fold) and rapid (minutes to hours) increase in T6P levels (Lunn et al., 2006 Through defining a signaling route for T6P, we provide a mechanistic basis for the function and potency of T6P in plants as an inhibitor of the central regulator SnRK1. Further work is necessary to identify and characterize the intermediary factor necessary for T6P inhibition of SnRK1 activity and to determine the cell specificity of the mechanism.
Biological Material
Seeds of Arabidopsis wild type (Arabidopsis thaliana ecotype Col-0) and expressing otsA encoding an Escherichia coli TPS (A19.3) or otsB encoding an E. coli TPP (B12.1; Schluepmann et al., 2003
Plant total soluble protein was extracted in 2 mL (per gram fresh weight tissue) of ice-cold homogenization buffer of 100 mM Tricine-NaOH, pH 8, 25 mM NaF, 5 mM dithiothreitol, 2 mM tetrasodium pyrophosphate, 0.5 mM EDTA, 0.5 mM EGTA, 1 mM benzamidine, 1 mM phenylmethylsulfonyl fluoride, 1 mM protease inhibitor cocktail (Sigma P9599), phosphatase inhibitors (PhosStop; Roche), and insoluble polyvinylpyrrolidone to 2% (w/v). Homogenate was centrifuged at 13,000g at 4°C. Supernatant (200 µL) was spin desalted (2.5-mL Sephadex G-25 medium columns; GE Healthcare) and preequilibrated with homogenization buffer. Eluant was supplemented with protease inhibitor cocktail and okadaic acid to 2.5 µM before freezing in liquid N2. SnRK1 was assayed using the established procedure (Davies et al., 1989
For assays of SNF1, yeast cells were pelleted, washed three times with sterile distilled water, and frozen in liquid N2. For assays of AMPK, adult Musca domestica was snap frozen and a pellet of C. elegans of mixed stages was used for protein extraction. Liver, S. cerevisiae, M. domestica, and C. elegans were extracted as described previously (Davies et al., 1989
Antisera to AKIN10 and AKIN11 peptides raised in rabbits were affinity purified by Eurogentec. AKIN10 peptide was Arg-Ala-Ser-Ser-Gly-Tyr-Leu-Gly-Ala-Glu-Phe-Gln-Glu-Thr-Met, and AKIN11 peptide was Thr-Thr-Asp-Ser-Gly-Ser-Asn-Pro-Met-Arg-Thr-Pro-Glu-Ala-Gly (Zhang et al., 2008
SnRK1 activity was extracted and purified 192-fold relative to crude extract exactly as described by Sugden et al. (1999)
Arabidopsis seedlings were grown as above without Suc under continuous light. Procedures were followed according to the Galbraith protocol using the 29,000-element version 3.0 Arabidopsis Oligonucleotide Microarrays. RNA was extracted using a small-scale phenol-free total RNA isolation kit (Ambion), mRNA amplified using the amino allyl message Amp II aRNA amplification kit (Ambion), labeling using Alexa Fluor 647 (green) and 555 (red) dye (Invitrogen), and microarray immobilization, hybridization, and washing were performed exactly according to the Galbraith protocol (http://ag.arizona.edu/microarray/) using the 29,000-element version 3.0 Arabidopsis Oligonucleotide Microarrays (ATq3.6.2). Slides were scanned using the Gene Pix 4000B scanner. Data were analyzed using GeneSpring GX 7.3.1, normalized per spot and per chip using intensity-dependent (Lowess) normalization, and transformed to ignore low-intensity probes less than 0.01. Dye swaps were performed on each replicate of three biological replicates. otsA and otsB transgenics were compared with the same wild-type sample of three biological replicates. Data were filtered using a t test in combination with Benjamini and Hochberg multiple test correction (P < 0.05). FatiGO (http://fatigo.bioinfo.cipf.es/; Al-Shahrour et al., 2004
Total RNA was isolated from seedlings using the Trizol method (Invitrogen). RNA was quantified on the Nanodrop Spectrophotometer (ND-1000), and its integrity was determined by agarose gel electrophoresis. Genomic DNA was removed with RNase-free DNase using a TURBO DNA-free kit (Ambion catalog no. 1907). cDNA was synthesized by reverse transcribing 2.5 µg of RNA using SuperScript III reverse transcriptase (Invitrogen catalog no. 18080-044) and random synthetic hexamers (Promega C1181). Gene expression was quantified using SYBR Green chemistry on a 7500 real-time PCR system (Applied Biosystems) in 10 µL for each reaction, containing 5 µL of Power SYBR Green Master Mix (Applied Biosystems), 1 µL of cDNA, and 0.25 µM primers. PCR used an initial denaturing stage of 95°C for 5 min followed by 40 cycles of 95°C for 15 s and 60°C for 1 min. PCR was performed with three technical replicates repeated on three biological replicates. Data were normalized using a protein phosphatase 2A subunit (Czechowski et al., 2005
The following materials are available in the online version of this article.
We thank Alfred Keys (Rothamsted Research) and Sjef Smeekens (University of Utrecht) for reading drafts of the manuscript. From Rothamsted Research, we further thank Paul Verrier for checking microarray data, Nigel Halford for discussions, and Rosane Curtis and Kevin Gorman for supplying C. elegans and M. domestica. Received December 16, 2008; accepted February 3, 2009; published February 4, 2009.
1 This work was supported by the Biotechnological and Biological Sciences Research Council (grants to Rothamsted Research and grant nos. BB/C51257X/1, BB/D006112/1, and BB/C512645/1). 
2 These authors contributed equally to the article. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Matthew J. Paul (matthew.paul{at}bbsrc.ac.uk).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.108.133934 * Corresponding author; e-mail matthew.paul{at}bbsrc.ac.uk.
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-subunit and β- and 
-subunits together with a number of additional interacting and regulatory factors (Pierre et al., 2007
