Cooperative pathway of O2 reduction to H2O2 in chloroplast thylakoid membrane: new insight into the Mehler reaction

Abstract

Oxygen reduction in chloroplasts in the light was discovered by (Mehler Arch Biochem Biophys 33:65-77, 1951) as production of hydrogen peroxide. Later, it was shown that the primary product of the oxygen reduction is superoxide radical produced in thylakoids by one-electron transfer from reduced components of photosynthetic electron transport chain to O₂ molecule. For a long time, the formation of hydrogen peroxide was considered to be a result of disproportionation of superoxide radicals in chloroplast stroma. Here, we overview a growing number of evidence indicating on another one, additional to disproportionation, pathway of hydrogen peroxide formation in chloroplasts, namely its formation in thylakoid membrane due to reaction of superoxide radical generated in the membrane with the reduced plastoquinone molecule, plastohydroquinone. Since various components of photosynthetic electron transport chain (primarily photosystem I) can supply superoxide radicals to this reaction, we refer this two-step O₂ photoreduction to H₂O₂ as a cooperative process. The significance of hydrogen peroxide production via this pathway for redox signaling and scavenging of reactive oxygen species is discussed.

Keywords: Chloroplast; Electron transport chain; Hydrogen peroxide; Photosynthesis; Superoxide generation.

Fig. 1

The effect of light intensity on the signal size of the nitroxide radicals produced in the reaction of 4-POBN with H₂O₂-derived hydroxyl radicals in a thylakoid suspension, in the presence and in the absence of cytochrome c (cyt c). Thylakoids (15 µg Chl ml⁻¹) were illuminated with red light (λ > 600 nm) for 3 min in the presence of 1 µM GrD. (A) — 50 μmol quanta m⁻² s⁻¹, (B) — 500 μmol quanta m⁻² s.⁻¹; a — in the absence, and b — in the presence of 40 µM cyt c. The spectra are shown on the same scale. (According to Borisova-Mubarakshina et al. 2012)