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SYSTEMS BIOLOGY, MOLECULAR BIOLOGY, AND GENE REGULATION

Inhibition of SNF1-Related Protein Kinase1 Activity and Regulation of Metabolic Pathways by Trehalose-6-Phosphate^1,[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.

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.

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www.plantphysiol.org/cgi/doi/10.1104/pp.108.133934

^* Corresponding author; e-mail matthew.paul{at}bbsrc.ac.uk.

Received December 16, 2008; accepted February 3, 2009; published February 4, 2009.

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