Metabolic alterations provide insights into Stylosanthes roots responding to phosphorus deficiency

Abstract Background: Phosphorus (P) deficiency is one of the major constraints limiting plant growth, especially in acid soils. Stylosanthes (stylo) is a pioneer tropical legume with excellent adaptability to low P stress, but its underlying mechanisms remain largely unknown. Results: In this study, the physiological, molecular and metabolic changes in stylo responding to phosphate (Pi) starvation were investigated. Under low P condition, the root growth in stylo was significantly enhanced, which was accompanied with up-regulation of expansin genes participating in cell wall loosening. Metabolic profiling analysis showed that a total of 256 metabolites with differential accumulation were identified in stylo roots responding to P deficiency, which mainly include flavonoids, sugars, nucleotides, amino acids, phenylpropanoids and phenylamides. P deficiency led to significant reduction in the accumulation of phosphorylated metabolites (e.g., P-containing sugars, nucleotides and cholines), suggesting that internal P utilization was enhanced in stylo roots. However, flavonoid metabolites, such as kaempferol, daidzein and their glycoside derivatives, were significantly increased in P-deficient stylo roots. Furthermore, the transcripts of various genes involved in flavonoids synthesis were found to be up-regulated by Pi starvation in stylo roots. In addition, the abundance of phenolic acids and phenylamides was significantly increased in stylo roots during P deficiency. The enhanced accumulation of the metabolites in stylo roots, such as flavonoids, phenolic acids and phenylamides, might facilitate P solubilization and cooperate with beneficial microorganisms in rhizosphere, and thus contributing to P acquisition and utilization in stylo. Conclusions: These results suggest that stylo plants cope with P deficiency by modulating root morphology, scavenging internal Pi from phosphorylated metabolites and enhancing accumulation of flavonoids, phenolic acids and phenylamides. This study provides valuable insights into the complex responses and adaptive mechanisms of stylo to P deficiency.