Oxidative Pentose Phosphate Pathway-Dependent Sugar Sensing as a Mechanism for Regulation of Root Ion Transporters by Photosynthesis  

Abstract

Root ion transport systems are regulated by light and/or sugars, but the signaling mechanisms are unknown. We showed previously that induction of the NRT2.1 NO 3 2 transporter gene by sugars was dependent on carbon metabolism downstream hexokinase (HXK) in glycolysis. To gain further insights on this signaling pathway and to explore more systematically the mechanisms coordinating root nutrient uptake with photosynthesis, we studied the regulation of 19 light-/sugar-induced ion transporter genes. A combination of sugar, sugar analogs, light, and CO 2 treatments provided evidence that these genes are not regulated by a common mechanism and unraveled at least four different signaling pathways involved: regulation by light per se, by HXK-dependent sugar sensing, and by sugar sensing upstream or downstream HXK, respectively. More specific investigation of sugar-sensing downstream HXK, using NRT2.1 and NRT1.1 NO 3 2 transporter genes as models, highlighted a correlation between expression of these genes and the concentration of glucose-6-P in the roots. Furthermore, the phosphogluconate dehydrogenase inhibitor 6-aminonicotinamide almost completely prevented induction of NRT2.1 and NRT1.1 by sucrose, indicating that glucose-6-P metabolization within the oxidative pentose phosphate pathway is required for generating the sugar signal. Out of the 19 genes investigated, most of those belonging to the NO 3 2 , NH 4 1 , and SO 4 22 transporter families were regulated like NRT2.1 and NRT1.1. These data suggest that a yet-unidentified oxidative pentose phosphate pathwaydependent sugar-sensing pathway governs the regulation of root nitrogen and sulfur acquisition by the carbon status of the plant to coordinate the availability of these three elements for amino acid synthesis.

mRNA-Seq Reveals a Comprehensive Transcriptome Profile of Rice under Phosphate Stress

“…This finding suggests that Pht1;4 can easily adjust to the cellular Pi condition. In Arabidopsis, it has been reported that AtPHT1;4 was induced by sucrose and is thought to be upstream of the hexokinase sugar-sensing pathways (Lejay et al 2008). Thus, morphological changes for adaptation in rice due to changes in Pi concentration may be controlled by local and systemic gene expression.…”

Glucose Elevates NITRATE TRANSPORTER2.1 Protein Levels and Nitrate Transport Activity Independently of Its HEXOKINASE1-Mediated Stimulation of NITRATE TRANSPORTER2.1 Expression

“…Furthermore, reduction of HEXOKINASE1 (HXK1) gene expression by antisense RNA reduced the expression of NRT2.1 (Lejay et al, 2003), indicating that the synthesis of Glc-6-P for the OPPP is required for the sugar-mediated expression of NRT2.1. This suggested that OPPP metabolism may influence nitrate uptake by transcriptional control of nitrate transporter genes (Lejay et al, 2008). Recently, it was shown that the pgl3-1 mutant, which reduces the expression of the plastidial 6-phosphogluconolactonase gene PGL3, had reduced expression of nitrate assimilatory genes in response to Suc (Bussell et al, 2013).…”

“…Sugars also induce the expression of genes involved in the transport of nitrate, phosphate, and sulfate (Lejay et al, 2003;Li et al, 2006), revealing an intimate connection between photosynthesis, carbon metabolism, and nutrient uptake. An inhibitor of phosphogluconate dehydrogenase activity in the OPPP (Kruger and von Schaewen, 2003) reduced Glc-mediated induction of NRT2.1, NRT1.1, NRT1.5, PEPTIDE TRANSPORTER, AMMONIUM TRANSPORTER1.3 (AMT1.3), SULFATE TRANSPORTER1.1 (SULTR1.1), and SULTR3.5 (Lejay et al, 2008), implicating OPPP metabolism in these sugar-mediated responses. Furthermore, reduction of HEXOKINASE1 (HXK1) gene expression by antisense RNA reduced the expression of NRT2.1 (Lejay et al, 2003), indicating that the synthesis of Glc-6-P for the OPPP is required for the sugar-mediated expression of NRT2.1.…”

“…We further show that increased Glc levels rapidly stimulate NRT2.1 protein accumulation and high-affinity nitrate uptake independently of NRT2.1 expression, possibly through posttranscriptional mechanisms. Blocking the OPPP by inhibition of phosphogluconate dehydrogenase activity reduced NRT2.1 expression in response to Suc (Lejay et al, 2008). To assess this genetically, we analyzed the expression of NRT2.1 and five other transporter genes in response to Glc in the HXK1 mutant gin2-1 (Moore et al, 2003).…”

“…We wished to further explore the influence of HXK1 on the expression of NRT2.1 and on nitrate-responsive growth in order to determine if the proposed role of the OPPP in NRT2.1 expression (Lejay et al, 2008) occurs through a novel mechanism or whether the OPPP functions through an existing NRT2.1 regulatory signaling pathway. We confirmed that Glc-induced NRT2.1 expression is highly dependent on HXK1 catalytic activity and show that OPPP intermediates and downstream metabolites rescue the impaired response of NRT2.1 to Glc in gin2-1 mutants, providing genetic and further biochemical evidence to support the conclusions of Lejay et al (2008) and confirming the role of OPPP metabolism in nitrate assimilation and growth (Bussell et al, 2013). Nitrate-mediated changes in NRT2.1 expression were unchanged in gin2-1, indicating that nitrate and Glc influence NRT2.1 expression independently.…”