Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3

Abstract

The Arabidopsis mutant pho3 accumulates sucrose and other carbohydrates to high levels, providing a means of investigating the genomic response to sucrose accumulation using microarray analysis. Wild-type and mutant plants were grown in soil to the mature rosette stage for the analysis of gene expression using the Affymetrix ATH1 chip, containing more than 22,500 probe sets. Small, but significant, decreases were observed in the expression of many genes encoding enzymes and regulatory proteins involved in primary carbon assimilation, suggesting that, in mature leaves of Arabidopsis, there is limited feedback regulation on gene expression by sugars. The study revealed a striking increase in the expression of the plastid glucose 6-phosphate/phosphate translocator, characteristically expressed only in heterotrophic tissues. This indicated a change in the nature of metabolite exchange between the plastid and the cytosol in the pho3 mutant. The expression of enzymes of starch synthesis also increased significantly. Very large increases were observed in the expression of transcription factors and enzymes involved in anthocyanin biosynthesis. This finding reinforces the emerging picture of an important role for primary metabolism in regulating secondary metabolism.

Genetic and Genomic Evidence That Sucrose Is a Global Regulator of Plant Responses to Phosphate Starvation in Arabidopsis

“…In contrast, the APase activity on the root surface is largely reduced in the suc2-5 mutant. The high accumulation of anthocyanin and starch in shoots, and the reduced production of APase in roots, were also observed in pho3, another mutant allele of the SUC2 gene (Zakhleniuk et al, 2001;Lloyd and Zakhleniuk, 2004). Taken together, these results show that the hps1 mutant has enhanced sensitivity in multiple plant responses to Pi starvation, and this is primarily due to increased levels of Suc, which acts as a global regulator of plant responses to Pi starvation.…”

“…The similar effects of photosynthates on Pi starvation-induced cluster root formation in white lupin and the expression of miRNA399 in common bean (Phaseolus vulgaris) have also been observed (Zhou et al, 2008;Liu et al, 2010b). In contrast, the Arabidopsis pho3 mutant carries a defective copy of the SUCROSE TRANSPORTER2 (SUC2) gene, leading to substantially reduced transport of Suc from shoot to root and the suppression of induction and secretion of APase on its root surface (Zakhleniuk et al, 2001;Lloyd and Zakhleniuk, 2004). In addition, earlier studies have revealed that the expression of many genes involved in the synthesis, translocation, and degradation of Suc was altered during Pi starvation (Hammond et al, 2003;Vance et al, 2003;Wu et al, 2003;Misson et al, 2005;Mü ller et al, 2007).…”

Expression of Sucrose Transporter cDNAs Specifically in Companion Cells Enhances Phloem Loading and Long-Distance Transport of Sucrose but Leads to an Inhibition of Growth and the Perception of a Phosphate Limitation

“…There is growing evidence that long-distance Suc transport plays an important role in phosphorous responses (Liu et al, 2005;Karthikeyan et al, 2007;White, 2008, 2011). The pho3 mutation, which was identified in a screen for reduced acid phosphatase activity during P limitations, turned out to be a mutant allele of AtSUC2 (Lloyd and Zakhleniuk, 2004). Both a reduction in photosynthesis and stem girdling, which blocks phloem transport, attenuate P deficiency responses in roots, including a decrease in the expression of many PSI genes (Liu et al, 2005;Karthikeyan et al, 2007).…”

Acclimation of metabolism to light in Arabidopsis thaliana: the glucose 6‐phosphate/phosphate translocator GPT2 directs metabolic acclimation

“…In wild‐type plants, GPT2 expression is induced in imbibed seeds (Finch‐Savage et al . 2007), in response to exogenous and endogenous increases in sucrose (Lloyd & Zakhleniuk 2004; Gonzali et al . 2006), in response to an increase in light intensity (Athanasiou et al .…”