Metabolite Profiling Reveals Distinct Changes in Carbon and Nitrogen Metabolism in Phosphate-Deficient Barley Plants (Hordeum vulgare L.)

Abstract

Plants modify metabolic processes for adaptation to low phosphate (P) conditions. Whilst transcriptomic analyses show that P deficiency changes hundreds of genes related to various metabolic processes, there is limited information available for global metabolite changes of P-deficient plants, especially for cereals. As changes in metabolites are the ultimate 'readout' of changes in gene expression, we profiled polar metabolites from both shoots and roots of P-deficient barley (Hordeum vulgare) using gas chromatography-mass spectrometry (GC-MS). The results showed that mildly P-deficient plants accumulated di- and trisaccharides (sucrose, maltose, raffinose and 6-kestose), especially in shoots. Severe P deficiency increased the levels of metabolites related to ammonium metabolism in addition to di- and trisaccharides, but reduced the levels of phosphorylated intermediates (glucose-6-P, fructose-6-P, inositol-1-P and glycerol-3-P) and organic acids (alpha-ketoglutarate, succinate, fumarate and malate). The results revealed that P-deficient plants modify carbohydrate metabolism initially to reduce P consumption, and salvage P from small P-containing metabolites when P deficiency is severe, which consequently reduced levels of organic acids in the tricarboxylic acid (TCA) cycle. The extent of the effect of severe P deficiency on ammonium metabolism was also revealed by liquid chromatography-mass spectrometry (LC-MS) quantitative analysis of free amino acids. A sharp increase in the concentrations of glutamine and asparagine was observed in both shoots and roots of severely P-deficient plants. Based on these data, a strategy for improving the ability of cereals to adapt to low P environments is proposed that involves alteration in partitioning of carbohydrates into organic acids and amino acids to enable more efficient utilization of carbon in P-deficient plants.

Phosphate Utilization Efficiency Correlates with Expression of Low-Affinity Phosphate Transporters and Noncoding RNA, IPS1, in Barley

“…It is expressed in both shoots and roots (Huang et al, 2008) and especially in phloem tissues of the leaf (Rae et al, 2003), suggesting that HvPHT1;6 plays a role in Pi remobilization in the whole plant. The protein sequence of HvPHT1;3 is more similar to HvPHT1;6 than to the HvPHT1;1 paralogs.…”

“…PAE is considered to be a major component of overall P efficiency (Ozturk et al, 2005;Ismail et al, 2007;Ramaekers et al, 2010), but PUE can influence PAE. P supply to plants is often fluctuating; therefore, P remobilization within the plant is critical for plant survival (Drew and Saker, 1984;Marschner and Cakmak, 1986;Jeschke et al, 1997;Vance et al, 2003;Huang et al, 2008). Remobilization and translocation of P from shoots to roots can lead to a larger root system, and hence greater exploitation of limited soil P resources for more P. However, the effect of PUE and simultaneous carbohydrate partitioning on PAE (Hermans et al, 2006;Liao et al, 2008) is not clear (Manske et al, 2001;Wang et al, 2010).…”

“…Recently, it was confirmed that HvPHT1;1 is a high-affinity Pi transporter with a K m of 1.9 mM when expressed in Xenopus laevis oocytes (Preuss et al, 2011), suggesting that HvPHT1;1 is involved in Pi acquisition. HvPHT1;6 is expressed in both shoots and roots (Huang et al, 2008) and localized in the leaf phloem tissue (Rae et al, 2003). It displays unsaturated uptake in a millimolar range of Pi concentrations when expressed in oocytes (Preuss et al, 2010), suggesting that HvPHT1;6 is involved in Pi retranslocation.…”

Genetic approaches to enhancing phosphorus-use efficiency (PUE) in crops: challenges and directions

“…HvPHT1;6 is highly expressed in old leaves, and its transcript is abundant in phloem tissue (Rae et al 2003). The expression of HvPHT1;6 in both shoots and roots is upregulated by P deficiency (Huang et al 2008;Huang et al 2011). These data suggest that HvPHT1;6 plays a major role in Pi remobilisation.…”

Plant and microbe genomics and beyond: potential for developing a novel molecular plant nutrition approach

“…Various research groups worldwide have analyzed global changes in plants in response to P, either through transcriptomic studies (Wasaki et al 2006), metabolomic studies (Huang et al 2008) or integrated ones [transcriptomics, proteomics and metabolomics; (Morcuende et al 2007)]. Phosphorus deficiency quickly causes the induction of high-affinity P transporters and acidic phosphatases, as well as glycolysis, possibly as a mechanism to produce organic acids which allow the recycling of P from phosphorylated intermediate compounds.…”