Tocopherol controls D1 amino acid oxidation by oxygen radicals in Photosystem II

Proc Natl Acad Sci U S A. 2021 Jan 26;118(4):e2019246118. doi: 10.1073/pnas.2019246118.

Abstract

Photosystem II (PSII) is an intrinsic membrane protein complex that functions as a light-driven water:plastoquinone oxidoreductase in oxygenic photosynthesis. Electron transport in PSII is associated with formation of reactive oxygen species (ROS) responsible for oxidative modifications of PSII proteins. In this study, oxidative modifications of the D1 and D2 proteins by the superoxide anion (O2•-) and the hydroxyl (HO•) radicals were studied in WT and a tocopherol cyclase (vte1) mutant, which is deficient in the lipid-soluble antioxidant α-tocopherol. In the absence of this antioxidant, high-resolution tandem mass spectrometry was used to identify oxidation of D1:130E to hydroxyglutamic acid by O2•- at the PheoD1 site. Additionally, D1:246Y was modified to either tyrosine hydroperoxide or dihydroxyphenylalanine by O2•- and HO•, respectively, in the vicinity of the nonheme iron. We propose that α-tocopherol is localized near PheoD1 and the nonheme iron, with its chromanol head exposed to the lipid-water interface. This helps to prevent oxidative modification of the amino acid's hydrogen that is bonded to PheoD1 and the nonheme iron (via bicarbonate), and thus protects electron transport in PSII from ROS damage.

Keywords: EPR; mass spectrometry; photosystem II; reactive oxygen species; tocopherol.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Amino Acids / chemistry*
  • Amino Acids / metabolism
  • Arabidopsis / enzymology*
  • Arabidopsis / genetics
  • Arabidopsis / radiation effects
  • Binding Sites
  • Hydroxyl Radical / chemistry
  • Hydroxyl Radical / metabolism
  • Intramolecular Transferases / chemistry
  • Intramolecular Transferases / genetics
  • Intramolecular Transferases / metabolism
  • Iron / chemistry
  • Iron / metabolism
  • Light
  • Models, Molecular
  • Mutation
  • Oxidation-Reduction
  • Oxygen / chemistry
  • Oxygen / metabolism
  • Photosynthesis / physiology
  • Photosynthesis / radiation effects
  • Photosystem II Protein Complex / chemistry*
  • Photosystem II Protein Complex / genetics
  • Photosystem II Protein Complex / metabolism
  • Protein Binding
  • Protein Conformation, alpha-Helical
  • Protein Conformation, beta-Strand
  • Protein Interaction Domains and Motifs
  • Superoxides / chemistry*
  • Superoxides / metabolism
  • Thermodynamics
  • Thermosynechococcus / enzymology
  • Thermosynechococcus / genetics
  • Thermosynechococcus / radiation effects
  • Thylakoids / enzymology*
  • Thylakoids / genetics
  • Thylakoids / radiation effects
  • alpha-Tocopherol / chemistry*
  • alpha-Tocopherol / metabolism

Substances

  • Amino Acids
  • Photosystem II Protein Complex
  • Superoxides
  • Hydroxyl Radical
  • Iron
  • Intramolecular Transferases
  • tocopherol cyclase
  • alpha-Tocopherol
  • Oxygen

Supplementary concepts

  • Thermosynechococcus vulcanus