Multi-omics-based identification of purple acid phosphatases and metabolites involved in phosphorus recycling in stylo root exudates

Int J Biol Macromol. 2023 Jun 30:241:124569. doi: 10.1016/j.ijbiomac.2023.124569. Epub 2023 Apr 24.

Abstract

Stylo (Stylosanthes guianensis) is a tropical forage and cover crop that possesses low phosphate (Pi) tolerance traits. However, the mechanisms underlying its tolerance to low-Pi stress, particularly the role of root exudates, remain unclear. This study employed an integrated approach using physiological, biochemical, multi-omics, and gene function analyses to investigate the role of stylo root exudates in response to low-Pi stress. Widely targeted metabolomic analysis revealed that eight organic acids and one amino acid (L-cysteine) were significantly increased in the root exudates of Pi-deficient seedlings, among which tartaric acid and L-cysteine had strong abilities to dissolve insoluble-P. Furthermore, flavonoid-targeted metabolomic analysis identified 18 flavonoids that were significantly increased in root exudates under low-Pi conditions, mainly belonging to the isoflavonoid and flavanone subclasses. Additionally, transcriptomic analysis revealed that 15 genes encoding purple acid phosphatases (PAPs) had upregulated expression in roots under low-Pi conditions. Among them, SgPAP10 was characterized as a root-secreted phosphatase, and overexpression of SgPAP10 enhanced organic-P utilization by transgenic Arabidopsis. Overall, these findings provide detailed information regarding the importance of stylo root exudates in adaptation to low-Pi stress, highlighting the plant's ability to release Pi from organic-P and insoluble-P sources through root-secreted organic acids, amino acids, flavonoids, and PAPs.

Keywords: Low phosphate stress; Purple acid phosphatase; Root exudates.

MeSH terms

  • Arabidopsis* / genetics
  • Arabidopsis* / metabolism
  • Cysteine / metabolism
  • Exudates and Transudates
  • Fabaceae* / genetics
  • Multiomics
  • Phosphorus / metabolism
  • Plant Roots / genetics
  • Plant Roots / metabolism

Substances

  • Phosphorus
  • purple acid phosphatase
  • Cysteine