Identification of primary and secondary metabolites with phosphorus status‐dependent abundance in <scp><i>A</i></scp><i>rabidopsis</i>, and of the transcription factor <scp>PHR</scp>1 as a major regulator of metabolic changes during phosphorus limitation

<jats:title>Abstract</jats:title><jats:p>Massive changes in gene expression occur when plants are subjected to phosphorus (<jats:styled-content style="fixed-case">P</jats:styled-content>) 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 <jats:styled-content style="fixed-case">P</jats:styled-content>‐replete and <jats:styled-content style="fixed-case">P</jats:styled-content>‐deprived <jats:styled-content style="fixed-case"><jats:italic>A</jats:italic></jats:styled-content><jats:italic>rabidopsis thaliana</jats:italic> wild type and mutants of the central <jats:styled-content style="fixed-case">P</jats:styled-content>‐signalling components <jats:styled-content style="fixed-case">PHR</jats:styled-content>1 and <jats:styled-content style="fixed-case">PHO</jats:styled-content>2, and micro<jats:styled-content style="fixed-case">RNA</jats:styled-content>399 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 <jats:styled-content style="fixed-case">P</jats:styled-content> limitation. Observed changes indicated <jats:styled-content style="fixed-case">P</jats:styled-content>‐saving strategies, increased photorespiration and crosstalk between <jats:styled-content style="fixed-case">P</jats:styled-content> limitation and sulphur and nitrogen metabolism. The <jats:italic>phr1</jats:italic> mutation had a remarkably pronounced effect on the metabolic <jats:styled-content style="fixed-case">P</jats:styled-content>‐limitation response, providing evidence that <jats:styled-content style="fixed-case">PHR</jats:styled-content>1 is a key factor for metabolic reprogramming during <jats:styled-content style="fixed-case">P</jats:styled-content> limitation. The effects of <jats:italic>pho2</jats:italic> or micro<jats:styled-content style="fixed-case">RNA</jats:styled-content>399 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 <jats:styled-content style="fixed-case">P</jats:styled-content> limitation in <jats:styled-content style="fixed-case"><jats:italic>A</jats:italic></jats:styled-content><jats:italic>rabidopsis</jats:italic>.</jats:p>