Cyclic Electron Flow around Photosystem I in C3Plants. In Vivo Control by the Redox State of Chloroplasts and Involvement of the NADH-Dehydrogenase Complex

Abstract

Cyclic electron flow around photosystem (PS) I has been widely described in vitro in chloroplasts or thylakoids isolated from C 3 plant leaves, but its occurrence in vivo is still a matter of debate. Photoacoustic spectroscopy and kinetic spectrophotometry were used to analyze cyclic PS I activity in tobacco (Nicotiana tabacum cv Petit Havana) leaf discs illuminated with far-red light. Only a very weak activity was measured in air with both techniques. When leaf discs were placed in anaerobiosis, a high and rapid cyclic PS I activity was measured. The maximal energy storage in far-red light increased to 30% to 50%, and the half-time of the P 700 re-reduction in the dark decreased to around 400 ms; these values are comparable with those measured in cyanobacteria and C 4 plant leaves in aerobiosis. The stimulatory effect of anaerobiosis was mimicked by infiltrating leaves with inhibitors of mitochondrial respiration or of the chlororespiratory oxidase, therefore, showing that changes in the redox state of intersystem electron carriers tightly control the rate of PS I-driven cyclic electron flow in vivo. Measurements of energy storage at different modulation frequencies of far-red light showed that anaerobiosis-induced cyclic PS I activity in leaves of a tobacco mutant deficient in the plastid Ndh complex was kinetically different from that of the wild type, the cycle being slower in the former leaves. We conclude that the Ndh complex is required for rapid electron cycling around PS I.During oxygenic photosynthesis, photosystem (PS) II and PS I cooperate to achieve a linear electron flow from H 2 O to NADP ϩ and to generate a transmembrane proton gradient driving ATP synthesis. However, ATP can also be produced by the sole PS I through cyclic electron transfer reactions (Arnon, 1959). This mechanism enables the generation of a proton gradient across the thylakoid membrane without NADP reduction by rerouting electrons of reduced PS I acceptors toward the intersystem carriers. Cyclic and linear electron transfers share a common sequence of electron carriers, namely the plastoquinone (PQ) pool, cytochrome b 6 /f complex, and plastocyanin (for review, see Fork and Herbert, 1993; Bendall and Manasse, 1995). This alternative electron flow has been shown to occur in vivo in cyanobacteria (Carpentier et al., 1984), in algae (Maxwell and Biggins, 1976; Ravenel et al., 1994), and in bundle sheath cells of C 4 plants (Herbert et al., 1990; Asada et al., 1993). In cyanobacteria, cyclic electron flow around PS I has been shown to provide extra ATP for different cellular processes, e.g. adaptation to salt stress conditions (Jeanjean et al., 1993). In the bundle sheath cell chloroplasts of C 4 plants, PS II is low or undetectable (Woo et al., 1970) and ATP supply is totally dependent upon PS I-mediated cyclic electron transport (Leegood et al., 1981).In C 3 plants, PS I-driven cyclic electron flow has been studied mainly in vitro on isolated chloroplasts or thylakoids with addition of artificial cofactors or reduced ferredoxi...

Photosynthesis and State Transitions in Mitochondrial Mutants ofChlamydomonas reinhardtiiAffected in Respiration

“…Significant ES was detected in the wild type, which indicates significant cyclic electron transport upon exclusive PSI excitation in state 1. Its biphasic dependence on the modulation frequency of the exciting light values most probably indicates the occurrence of two different cyclic electron pathways with different kinetics, as suggested by a recent study on tobacco (Nicotiana tabacum) chloroplasts (Joët at al., 2002). Following the interpretation from this study, ES at high frequency (200 Hz or more) is mainly due to NAD(P)Hdependent cyclic electron flow, whereas at low frequency, an additional contribution from cyclic electron flow involving ferredoxin and a putative ferredoxin-PQ oxidoreductase is involved.…”

Chloroplast ribonucleoprotein CP31A is required for editing and stability of specific chloroplast mRNAs

“…As with other ndh mutants described to date, no visible developmental phenotype is observed (29). The function of the NDH complex is still under debate, but roles in cyclical electron transport processes in the thylakoid membrane and in stress tolerance have been postulated (29,31,34,35). Future experiments are required to determine whether cp31A functions in adjusting ndhF expression, and thus the entire NDH complex, under different conditions.…”

Involvement of a Plastid Terminal Oxidase in Plastoquinone Oxidation as Evidenced by Expression of the Arabidopsis thaliana Enzyme in Tobacco

“…It was proposed that the Ndh complex participates in both chlororespiration and cyclic electron transfer around PS I (8 -11). A role of the Ndh complex in cyclic electron flow around PS I was recently confirmed by photoacoustic measurements performed in tobacco ndh mutants (12). It should be noted that alternate activities, such as a putative ferredoxin-PQ reductase (FQR) (13,14) or a Ndh-2 type activity may also be involved in these processes (15,16).…”

“…Overexpression of PTOX, by modifying the redox poise of intersystem electron carriers, may perturb the establishment of cyclic electron transfer reactions. Interestingly enough, a role of chlororespiration in the control of cyclic electron flow around PS I was recently deduced from photoacoustic measurements performed in leaves under low O 2 concentration (12). The fact that chlororespiration and cyclic electron transfer reactions around PS I operate within the same membranes (stroma lamellae, see Ref.…”