Molecular Mechanism of Oxidation of P700 and Suppression of ROS Production in Photosystem I in Response to Electron-Sink Limitations in C3 Plants

Abstract

Photosynthesis fixes CO2 and converts it to sugar, using chemical-energy compounds of both NADPH and ATP, which are produced in the photosynthetic electron transport system. The photosynthetic electron transport system absorbs photon energy to drive electron flow from Photosystem II (PSII) to Photosystem I (PSI). That is, both PSII and PSI are full of electrons. O2 is easily reduced to a superoxide radical (O2−) at the reducing side, i.e., the acceptor side, of PSI, which is the main production site of reactive oxygen species (ROS) in photosynthetic organisms. ROS-dependent inactivation of PSI in vivo has been reported, where the electrons are accumulated at the acceptor side of PSI by artificial treatments: exposure to low temperature and repetitive short-pulse (rSP) illumination treatment, and the accumulated electrons flow to O2, producing ROS. Recently, my group found that the redox state of the reaction center of chlorophyll P700 in PSI regulates the production of ROS: P700 oxidation suppresses the production of O2− and prevents PSI inactivation. This is why P700 in PSI is oxidized upon the exposure of photosynthesis organisms to higher light intensity and/or low CO2 conditions, where photosynthesis efficiency decreases. In this study, I introduce a new molecular mechanism for the oxidation of P700 in PSI and suppression of ROS production from the robust relationship between the light and dark reactions of photosynthesis. The accumulated protons in the lumenal space of the thylakoid membrane and the accumulated electrons in the plastoquinone (PQ) pool drive the rate-determining step of the P700 photo-oxidation reduction cycle in PSI from the photo-excited P700 oxidation to the reduction of the oxidized P700, thereby enhancing P700 oxidation.

Intrinsic Fluctuations in Transpiration Induce Photorespiration to Oxidize P700 in Photosystem I

“…Both compounds are used for the regeneration of ribulose 1,5-bisphophate (RuBP), which is one of the substrates of RuBP carboxylase/oxygenase (Rubisco). The electron flux in the linear electron flow of the light reaction is almost equal to the flux of electrons consumed in the CBB cycle [ 2 , 3 , 4 ].…”

“…The coupling between the light reaction and the CBB cycle requires an interaction between their systems to suppress the production of reactive oxygen species (ROS) in PSI [ 2 ]. For example, saturated pulse illumination (5,000–20,000 µmol photons m −2 s −1 of light intensity, 300–800 ms duration) in the dark causes the rapid accumulation of electrons at the acceptor side of PSI [ 12 , 13 ].…”

“…Thus, the production of ROS is regulated by the redox state of P700: if P700* oxidation is rate-limited, electrons accumulate at the acceptor-side of PSI and flow toward ROS production. Conversely, if P700 + reduction is rate limited, O 2 reduction is suppressed and electron accumulation at the acceptor-side of PSI is relieved [ 2 , 24 ]. When the efficiency of CO 2 assimilation is reduced, such as under high light intensity, low CO 2 concentrations, drought, or extreme temperatures, all oxygenic photosynthetic organisms can oxidize P700 and suppress ROS production [ 13 , 25 , 26 , 27 ].…”

“…All oxygenic photosynthetic organisms have evolved P700 oxidation systems [ 2 , 13 ]. As mentioned above, the transition of the rate-determining steps in the P700 photo-oxidation/reduction cycle is key to maintaining P700 in the oxidized state.…”

Oxidative Stress in Plants

“…The review by Dr. Petřivalský’s group [ 10 ] provided the present knowledge about the compartment-specific pathways of reactive oxygen species generation and decomposition in plant cells, and the mechanisms that controlling their homeostasis in cell compartments. Likewise, with a particular example at the chloroplastic level, in an in-depth review Miyake [ 11 ] summarised the current research concerning the molecular mechanisms of ROS formation and suppression in photosystem I. He established a novel molecular mechanism for the oxidation of the P700 oxidation system in photosystem I and the elimination of ROS formation from the strong relationship between the light and dark reactions of photosynthesis.…”