Cyclic Electron Flow around Photosystem I in C3 Plants. 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...

Enhanced rates of P700 + dark-reduction in leaves of Cucumis sativus L. photoinhibited at chilling temperature

“…7), the electron donation to oxidized P700 via the Ndh complex involving PQ is independent of cyclic electron pathways. The above is in agreement with the association of nonphotochemical reduction of PQ with an enhanced electron flow to P700 + in the dark (Joe¨t et al 2002). Hence, the Ndh complex was proposed to control the redox poise of the intersystem electron transport chain in intact leaves (Joe¨t et al 2002) while the reduced state of PQ and pyridine nucleotides may regulate the interactions between photosynthetic electron flow and chloroplast respiration .…”

“…The above is in agreement with the association of nonphotochemical reduction of PQ with an enhanced electron flow to P700 + in the dark (Joe¨t et al 2002). Hence, the Ndh complex was proposed to control the redox poise of the intersystem electron transport chain in intact leaves (Joe¨t et al 2002) while the reduced state of PQ and pyridine nucleotides may regulate the interactions between photosynthetic electron flow and chloroplast respiration . However, these considerations have the important implication that the reduction state of the PQ pool plays a key role in the photoinhibition-induced enhancement of electron donation to P700 + in the dark.…”

“…Numbers adjacent to curves indicate the relative magnitudes of the fast and slow components of dark decay. In each panel, the magnitude of absorbance changes was normalized to their maximum magnitude component in P700 + reduction in the dark with halftimes of about 500, 1,000, and 1,200 ms for potato, cucumber, and tobacco leaves, respectively (Havaux 1996;Kim et al 2001;Joe¨t et al 2002). Figure 4 provides strong evidence for the operation of two reactions in the reduction of P700 + from a source(s) alternative to PSII, as shown in intact barley leaves that experienced heat stress (Bukhov et al 2002).…”

“…Considering the above, it is likely that the slower P700 + reduction in the dark is restricted by the availability of stromal donors. This argument is sustained by the fact that P700 + reduction in darkness is not only governed by the size of the stromal pool of reductants (Bukhov et al 2002) but also by the kinetics of electron transfer from such stromal donors to the intersystem chain (Joe¨t et al 2002). In this context, it should be mentioned that the kinetics of P700 + re-reduction mediated by linear electron transport with the participation of both PSII and PSI (in the absence of diuron and MV) is much faster in leaves kept under steady-state photosynthesis (Bukhov et al 2002) in comparison with PSII-independent electron flow mediated by stromal reductants.…”

“…The major electron acceptor of the Ndh complex seems to be the PQ pool. Recently, it was proposed that the Ndh complex also acts as a redox poise regulator (Joe¨t et al 2002).…”