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Published on February 4, 2009; 10.1104/pp.108.133934

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Received December 16, 2008
Accepted February 3, 2009

Inhibition of Snf1-related protein kinase (SnRK1) activity and regulation of metabolic pathways by trehalose 6-phosphate

Yuhua Zhang , Lucia F. Primavesi , Deveraj Jhurreea , P. John Andralojc , Rowan A. C. Mitchell , Stephen J. Powers , Henriette Schluepmann , Thierry Delatte , Astrid Wingler , and Matthew J. Paul *

Plant Science, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, United Kingdom; Molecular Plant Physiology, Utrecht University, Padualaan 8, 3584CH Utrecht, The Netherlands; Department of Biomedical Analysis, Utrecht University, PO Box 80082 3584CA Utrecht, The Netherlands; Genetics, Evolution and Environment, Darwin Building, University College London, Gower Street, London, WC1E 6BT, United Kingdom

* Corresponding author; email: matthew.paul{at}bbsrc.ac.uk.

Trehalose 6-phosphate (T6P) is a proposed signalling molecule in plants, yet how it signals was not clear. Here we provide evidence that T6P functions as an inhibitor of SnRK1 (AKIN10/ AKIN11) of the Snf1-related group of protein kinases. T6P, but not other sugars and sugar phosphates inhibited SnRK1 in Arabidopsis seedling extracts strongly (50%) at low concentrations (1-20 µM). Inhibition was non-competitive 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 analysed 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 E. coli otsA encoding T6P synthase to elevate T6P or otsB encoding T6P phosphatase to decrease T6P. SnRK1 target genes showed opposite regulation consistent with 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, TCA 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. The experiments provide strong evidence that T6P inhibits SnRK1 to activate biosynthetic processes in growing tissues.






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