Genome‐wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus

Abstract

Affymetrix ATH1 arrays, large-scale real-time reverse transcription PCR of~2200 transcription factor genes and other gene families, and analyses of metabolites and enzyme activities were used to investigate the response of Arabidopsis to phosphate (Pi) deprivation and re-supply. Transcript data were analysed with MapMan software to identify coordinated, system-wide changes in metabolism and other cellular processes. Phosphorus (P) deprivation led to induction or repression of > 1000 genes involved in many processes. A subset, including the induction of genes involved in P uptake, the mobilization of organic Pi, the conversion of phosphorylated glycolytic intermediates to carbohydrates and organic acids, the replacement of P-containing phospholipids with galactolipids and the repression of genes involved in nucleotide/nucleic acid synthesis, was reversed within 3 h after Pi re-supply. Analyses of 22 enzyme activities revealed that changes in transcript levels often, but not always, led to changes in the activities of the encoded enzymes in P-deprived plants. Analyses of metabolites confirmed that P deprivation leads to a shift towards the accumulation of carbohydrates, organic acids and amino acids, and that Pi re-supply leads to use of the latter. P-deprived plants also showed large changes in the expression of many genes involved in, for example, secondary metabolism and photosynthesis. These changes were not reversed rapidly upon Pi re-supply and were probably secondary in origin. Differentially expressed and highly P-specific putative regulator genes were identified that presumably play central roles in coordinating the complex responses of plants to changes in P nutrition. The specific responses to Pi differ markedly from those found for nitrate, whereas the long-term responses during P and N deprivation share common and non-specific features.

Stress Response Versus Stress Tolerance: A Transcriptome Analysis of Two Rice Lines Contrasting in Tolerance to Phosphorus Deficiency

“…In contrast to the increase in expression of galactolipidsynthesis-related genes, no change was detected for the second alternative lipid biosynthesis pathway. Sulfolipidsynthesis-related genes UDP-sulfoquinovose synthase (SQD1) and UDP-sulfoquinovosyl:DAG sulfoquinovosyltransferase (SQD2) were not affected by G or E, which distinguishes our results from those obtained by others for Arabidopsis (Misson et al 2005;Morcuende et al 2007) or rice (Wang et al 2006).…”

“…P deficiency significantly affected the expression pattern of 88 genes in shoots and 34 genes in roots (Table 4; p≤ 0.001). In shoots, just over 50% of phosphatase genes were upregulated under P deficiency whereas about 80% were upregulated in roots, confirming that members of the phosphatase gene family are typically affected by P deficiency (Misson et al 2005;Morcuende et al 2007). However, our comparison between genotypes did not reveal a pattern that would suggest that phosphatases were associated with tolerance.…”

“…Microarray studies in Arabidopsis thaliana (Hammond et al 2003;Misson et al 2005;Morcuende et al 2007) and rice (Wasaki et al 2003;Wang et al 2006;Wasaki et al 2006) have confirmed the Pi responsiveness of many gene families involved in Pi acquisition and P remobilization and redistribution. Despite the valuable insights gained from these studies, it has so far been difficult to draw practically relevant conclusions because distinguishing stress response mechanisms/genes from those leading to elevated tolerance remains difficult.…”

Role of phosphatidic acid in plant galactolipid synthesis

“…The CDP-DAG pathway is more active in the growth phase but nutrient depletion induces a shift towards the Kennedy pathway [16]. The Kennedy pathway indeed contributes to recycling the polar head of phospholipids such as choline and ethanolamine [20] According to [21] Leaf Root Whole seedling ATS1 Glycerol-3-phosphate acyltransferase through phospholipases D (PLDs) and eventually to remodelling of membranes. The PA phosphatase Pah1p is critical for the shift from the CDP-DAG to the Kennedy pathway because it catalyzes the hydrolysis of PA into DAG, and furthermore because the Pah1p-produced DAG negatively regulates the level of expression of genes encoding the CDP-DAG pathway [16].…”

“…However, it is likely important to distinguish two phases in the lipid response to Pi deprivation. In an early stage, a transient increase of PC precedes the increase of galactolipid synthesis [19] and several phospholipases D and C such as PLDz1, PLDz2, NPC4 and NPC5 are highly overexpressed [20,21]. Therefore, this suggests that, at this stage, the Kennedy pathway actively contributes to remodelling of phospholipids, notably of PE into PC [19].…”