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.
Highlights
We try to answer the following questions in this review: “Is the excess accumulation of electrons in Photosystem I (PSI) truly harmful to photosynthetic organisms?” and “Does reactive oxygen species (ROS) production occur in vivo?” Driever and Baker [30,31] and Ruuska et al [30,31] reported that the in vivo activity of the Mehler reaction is too small compared to the electron flux in photosynthesis
We asked “How do photosynthetic organisms manage to escape from the accumulation of electrons in PSI?” We developed a method for suppressing photosynthesis and imitating the accumulation of electrons in PSI
The atmospheric repetitive short-pulse (rSP) illumination treatment produces a superoxide radical (O2 − ) in PSI [32,40,41,42,43]. These results suggest that the electrons accumulated on the PSI acceptor side during one light pulse are used for O2 reduction, which triggers the O2 − production reflected as P700* accumulation
Summary
Numerous researchers have shown that, in photosynthetic organisms, oxidative damage due to enhanced production of reactive oxygen species (ROS) occurs when environmental stress (e.g., extreme low/high temperatures, high salinity, and oligotrophic inorganic components) decreases the photosynthetic efficiency [1,2,3,4,5,6,7,8,9,10,11,12,13,14,15,16,17,18,19,20,21]. P700+ rapidly decreases during the light pulse, which is due to the occupation of P700* in the photo-oxidation reduction cycle of P700, indicating the accumulation of electrons at the acceptor side of PSI. The atmospheric rSP illumination treatment produces a superoxide radical (O2 − ) in PSI [32,40,41,42,43] These results suggest that the electrons accumulated on the PSI acceptor side during one light pulse are used for O2 reduction, which triggers the O2 − production reflected as P700* accumulation.
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