Up-regulation of biosynthetic processes associated with growth by trehalose 6-phosphate

Abstract

Trehalose 6-phosphate (T6P), the precursor of trehalose, is a signaling molecule in plants with strong effects on metabolism, growth and development. We recently showed that in growing tissues T6P is an inhibitor of SnRK1 of the SNF1-related group of protein kinases1. SnRK1 acts as transcriptional integrator in response to carbon and energy supply. In microarray experiments on seedlings of transgenic Arabidopsis with elevated T6P content we found that expression of SnRK1 marker genes was affected in a manner to be predicted by inhibition of SnRK1 by T6P in vivo1. A large number of genes involved in reactions that utilize carbon, e.g. UDP-glucose dehydrogenase genes involved in cell wall synthesis, were upregulated. T6P was also found to affect developmental signaling pathways, probably in a SnRK1-independent manner. This includes upregulation of genes encoding UDP-glycosyltransferases that are involved in the glycosylation of hormones. In addition, genes involved in auxin response and light signaling were affected. Many of these genes belong to pathways that link the circadian clock to plant growth and development. The overall pattern of changes in gene expression supports a role for T6P in coordinating carbon supply with biosynthetic process involved in growth and development.

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Acknowledgements

Rothamsted Research receives grant-aided support from the Biotechnological and Biological Sciences Research Council (BBSRC) of the United Kingdom. Research was supported by BBSRC grants BB/C51257X/1, BB/D006112/1 and BB/C512645/1.

Figures and Tables

Figure 1 T6P content in 7-day-old wild-type and otsA-expressing seedlings grown in half-strength MS medium as in1 with 15 mM (□) or 100 mM (▪) sucrose. n = 4 with standard error of the mean.

Figure 2 Synthesis of cell wall precursors from UD P-glucose. Changes in gene expression were analyzed using Mapman9 for Arabidopsis seedlings expressing the E. coli trehalose phosphate synthase gene otsA and containing elevated trehalose 6-phosphate. Blue denotes upregulation, red denotes downregulation.

Figure 3 (A) Fresh weight of seedlings of otsA-expressing plants with increased T6P (▪), wild type (▪) and otsB-expressing plants with decreased T6P (□) grown on 100 mM sucrose. (B) Phenotype of otsA seedlings.

Figure 4 Model for the interactions of light signaling, circadian rhythms and auxin-regulated growth in response to T6P. The circadian clock regulates transcript levels of the growth regulator PIF4, while PIF4 protein is degraded by the 26S proteasome in response to light. Auxin induces the expression of Aux/IAA proteins as well as promoting their degradation by the 26S proteasome in a process gated by the circadian clock. Aux/IAA proteins regulate gene expression by heterodimerizing with auxin response factor (ARF) proteins. DFL1, ENP = MAB4 = NPY1 (At4g31820) and NPY5 are possible downstream targets that are involved in plant development in response to auxin as well as to light. Examples of genes whose expression was affected in otsA-expressing seedlings with increased T6P are listed in blue (upregulated) or red (downregulated). See Table 1 for list of genes.

Table 1 Genes with altered transcript abundance compared to wild type in transgenic arabidopsis seedlings expressing the E. coli trehalose phosphate synthase gene otsA and containing elevated trehalose 6-phosphate

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