Sugars as hydroxyl radical scavengers: proof-of-concept by studying the fate of sucralose in Arabidopsis

Plant J. 2015 Jun;82(5):822-39. doi: 10.1111/tpj.12853.

Abstract

Substantial formation of reactive oxygen species (ROS) is inevitable in aerobic life forms. Due to their extremely high reactivity and short lifetime, hydroxyl radicals are a special case, because cells have not developed enzymes to detoxify these most dangerous ROS. Thus, scavenging of hydroxyl radicals may only occur by accumulation of higher levels of simple organic compounds. Previous studies have demonstrated that plant-derived sugars show hydroxyl radical scavenging capabilities during Fenton reactions with Fe(2+) and hydrogen peroxide in vitro, leading to formation of less detrimental sugar radicals that may be subject of regeneration to non-radical carbohydrates in vivo. Here, we provide further evidence for the occurrence of such radical reactions with sugars in planta, by following the fate of sucralose, an artificial analog of sucrose, in Arabidopsis tissues. The expected sucralose recombination and degradation products were detected in both normal and stressed plant tissues. Oxidation products of endogenous sugars were also assessed in planta for Arabidopsis and barley, and were shown to increase in abundance relative to the non-oxidized precursor during oxidative stress conditions. We concluded that such non-enzymatic reactions with hydroxyl radicals form an integral part of plant antioxidant mechanisms contributing to cellular ROS homeostasis, and may be more important than generally assumed. This is discussed in relation to the recently proposed roles for Fe(2+) and hydrogen peroxide in processes leading to the origin of metabolism and the origin of life.

Keywords: Arabidopsis thaliana; ROS; hydroxyl radical; membrane protection; stress; sucralose; sugar.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / metabolism
  • Free Radical Scavengers / metabolism
  • Hordeum / metabolism
  • Hydroxyl Radical / chemistry*
  • Hydroxyl Radical / metabolism
  • Oxidation-Reduction
  • Oxidative Stress
  • Plant Leaves / metabolism
  • Reactive Oxygen Species / metabolism
  • Sucrose / analogs & derivatives*
  • Sucrose / chemistry
  • Sucrose / metabolism
  • Sucrose / pharmacokinetics
  • Tandem Mass Spectrometry
  • Tissue Distribution

Substances

  • Arabidopsis Proteins
  • Free Radical Scavengers
  • Reactive Oxygen Species
  • Hydroxyl Radical
  • Sucrose
  • trichlorosucrose