Identification of primary and secondary metabolites with phosphorus status-dependent abundance in Arabidopsis, and of the transcription factor PHR1 as a major regulator of metabolic changes during phosphorus limitation

Massive changes in gene expression occur when plants are subjected to phosphorus (P) limitation, but the breadth of metabolic changes in these conditions and their regulation is barely investigated. Nearly 350 primary and secondary metabolites were profiled in shoots and roots of P-replete and P-deprived Arabidopsis thaliana wild type and mutants of the central P-signalling components PHR1 and PHO2, and microRNA399 overexpresser. In the wild type, the levels of 87 primary metabolites, including phosphorylated metabolites but not 3-phosphoglycerate, decreased, whereas the concentrations of most organic acids, amino acids, nitrogenous compounds, polyhydroxy acids and sugars increased. Furthermore, the levels of 35 secondary metabolites, including glucosinolates, benzoides, phenylpropanoids and flavonoids, were altered during P limitation. Observed changes indicated P-saving strategies, increased photorespiration and crosstalk between P limitation and sulphur and nitrogen metabolism. The phr1 mutation had a remarkably pronounced effect on the metabolic P-limitation response, providing evidence that PHR1 is a key factor for metabolic reprogramming during P limitation. The effects of pho2 or microRNA399 overexpression were comparatively minor. In addition, positive correlations between metabolites and gene transcripts encoding pathway enzymes were revealed. This study provides an unprecedented metabolic phenotype during P limitation in Arabidopsis. Unlike transcript data, large-scale metabolite data for P-limited plants are still missing. Current metabolite profiling technologies were used to determine the abundance of nearly 350 primary and secondary metabolites in roots and shoots of P-limited and P-replete Arabidopsis wildtype plants and mutants in P-signaling. Besides determining a large number of metabolites with P-status dependent abundance, the transcription factor PHR1 was found to be important for metabolic reprogramming during P-limitation.