Novel application of cyclo(-Phe-Pro) in mitigating aluminum toxicity through oxidative stress alleviation in wheat roots

Environ Pollut. 2024 Dec 15;363(Pt 2):125241. doi: 10.1016/j.envpol.2024.125241. Epub 2024 Nov 4.

Abstract

Microbial secondary metabolites are crucial in plant-microorganism interactions, regulating plant growth and stress responses. In this study, we found that cyclo(-Phe-Pro), a proline-based cyclic dipeptide secreted by many microorganisms, alleviated aluminum toxicity in wheat roots by increasing root growth, decreasing callose deposition, and decreasing Al accumulation. Cyclo(-Phe-Pro) also significantly reduced Al-induced reactive oxygen species (ROS) with H2O2, O2•-, and •OH levels decreasing by 19.1%, 42.8%, and 17.9% in root tips, thus protecting the plasma membrane from oxidative damage. Although Al stress increased the activities of superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), and ascorbate peroxidase (APX) in wheat roots, cyclo(-Phe-Pro) application reduced these enzyme activities. However, compared to the Al treatment, cyclo(-Phe-Pro) application increased DPPH and FRAP activities by 16.8% and 14.9%, indicating increased non-enzymatic antioxidant capacity in wheat roots. We observed that Al caused the oxidation of ascorbate (AsA) and glutathione (GSH) to dehydroascorbate (DHA) and glutathione disulfide (GSSG), respectively. Under Al stress, cyclo(-Phe-Pro) treatment maintained reduced AsA and GSH levels, as well as high AsA/DHA and GSH/GSSG redox pair ratios in wheat roots. High AsA/DHA and GSH/GSSG ratios can reduce Al toxicity by neutralizing free radicals and restoring redox homeostasis via antioxidant properties. These results suggest that cyclo(-Phe-Pro) maintains ASA- and GSH-dependent redox homeostasis to alleviate oxidative and Al stress in wheat roots. Findings of this study establishes a theoretical foundation for using microbial metabolites to mitigate Al toxicity in acidic soils, highlighting their potential in sustainable agriculture.

Keywords: Aluminum stress; Antioxidant capacity; Cyclic dipeptides; Cyclo(-Phe-Pro); Wheat roots.

MeSH terms

  • Aluminum* / toxicity
  • Antioxidants / metabolism
  • Ascorbate Peroxidases / metabolism
  • Ascorbic Acid / metabolism
  • Catalase / metabolism
  • Dipeptides
  • Glutathione / metabolism
  • Hydrogen Peroxide / metabolism
  • Oxidative Stress* / drug effects
  • Plant Roots* / drug effects
  • Plant Roots* / metabolism
  • Reactive Oxygen Species / metabolism
  • Soil Pollutants / toxicity
  • Superoxide Dismutase / metabolism
  • Triticum* / drug effects
  • Triticum* / growth & development
  • Triticum* / metabolism

Substances

  • Aluminum
  • Reactive Oxygen Species
  • Antioxidants
  • Dipeptides
  • Superoxide Dismutase
  • Catalase
  • Glutathione
  • Soil Pollutants
  • Hydrogen Peroxide
  • Ascorbate Peroxidases
  • Ascorbic Acid