Abstract
Simple sugars, like glucose (Glc) and sucrose (Suc), act as signals to modulate the expression of hundreds of genes in plants. Frequently, however, it remains unclear whether this regulation is induced by the sugars themselves or by their derivatives generated in the course of carbohydrate (CH) metabolism. In the present study, we tested the relevance of different CH metabolism and allocation pathways affecting expression patterns of five selected sugar-responsive genes (bZIP63, At5g22920, BT2, MGD2, and TPS9) in Arabidopsis thaliana. In general, the expression followed diurnal changes in the overall sugar availability. However, under steady growth conditions, this response was hardly impaired in the mutants for CH metabolizing/ transporting proteins (adg1, sex1, sus1-4, sus5/6, and tpt2), including also hexokinase1 (HXK1) loss- and gain-of-function plants—gin2.1 and oe3.2, respectively. In addition, transgenic plants carrying pbZIP63::GUS showed no changes in reporter-gene-expression when grown on sugar under steady-state conditions. In contrast, short-term treatments of agar-grown seedlings with 1% Glc or Suc induced pbZIP63::GUS repression, which became even more apparent in seedlings grown in liquid media. Subsequent analyses of liquid-grown gin2.1 and oe3.2 seedlings revealed that Glc -dependent regulation of the five selected genes was not affected in gin2.1, whereas it was enhanced in oe3.2 plants for bZIP63, At5g22920, and BT2. The sugar treatments had no effect on ATP/ADP ratio, suggesting that changes in gene expression were not linked to cellular energy status. Overall, the data suggest that HXK1 does not act as Glc sensor controlling bZIP63, At5g22920, and BT2 expression, but it is nevertheless required for the production of a downstream metabolic signal regulating their expression.
Highlights
Within plant cells, carbohydrates (CH) undergo a constant production, transport and metabolization, including inter-conversion, polymerization and degradation
Examples of such proteins include: (i) triose-phosphate-transporter (TPT; corresponding mutant tpt2), involved in carbon export from chloroplasts to the cytosol; (ii) hexokinase (HXK1; gin2.1, oe3.2), catalyzing the phosphorylation of Glc and Fru to provide substrate for glycolysis as well as Suc and starch synthesis (Granot et al, 2013); (iii) Suc synthase (SUS; sus1-4, sus5/6), catalyzing the breakdown of Suc to Fru and UDP-Glc, the latter being an essential precursor for oligo- and polysaccharides (Kleczkowski et al, 2010); as well as (iv) ADP-Glc-phyrophosphorylase (AGPase, adg1) and (v) glucan-water-dikinase (GWD, sex1) which are essential for synthesis and breakdown of starch, the pivotal CH/energy reserve (Caspar et al, 1991)
Growth Conditions In order to investigate the relevance of distinct CH-metabolism pathways for the production of sugar signal(s), we analyzed mutants impaired in Suc metabolism, triose-P transport, and starch biosynthesis and degradation to assess their impact on sugar-responsive gene expression
Summary
Carbohydrates (CH) undergo a constant production, transport and metabolization, including inter-conversion, polymerization and degradation. Mutants impaired in the activity of one of these proteins (or several isozymes as in multiple sus mutants) have frequently exhibited unaffected growth phenotypes and minor changes in the overall internal content of soluble sugars under standard diurnal conditions (12/12 or 16/8 h light/dark photoperiod; light intensity ∼150 μE) (Caspar et al, 1991; Moore et al, 2003; Barratt et al, 2009; Schmitz et al, 2012) This suggests that the affected pathway is likely compensated for by other convergent metabolic pathways, as suggested for SUS isozymes and cytosolic invertases (Barratt et al, 2009). Assuming that such a compensation might result in changes in the size and turnover of specific sugar-pools and lead to differential expression of certain sugar-responsive genes, these mutants represent a valuable tool to assess the relevance of the respective pathway in generation of the signaling molecule
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