A photoacoustic study of water infiltrated leaves

Malkin, Shmuel; Charland, Marc; Leblanc, Roger M.

doi:10.1007/bf00032981

“…The existence of cyclic electron transport in vivo in C 3 plants has also been questioned by photoacoustic measurements in far-red light (Herbert et al, 1990), which allow a direct and quantitative measure of energy storage (ES) by cyclic electron flow around PS I (for review, see Malkin and Canaani, 1994). This method has confirmed the existence of cyclic electron transfer reactions in C 4 plants, algae, and cyanobacteria (Herbert et al, 1990), but failed to show significant cyclic activity in C 3 plant leaves (Herbert et al, 1990;Havaux et al, 1991;Malkin et al, 1992).…”

mentioning

confidence: 92%

“…In higher plants, photoacoustic measurements must be conducted on water-or buffer-infiltrated leaves to eliminate the oxygen-evolution-related component of the photoacoustic signal (Malkin et al, 1992). In infiltrated leaves of maize (a C 4 plant), ES in far-red light (approximately 15%) was close to the activity measured in Synechocystis sp.…”

Section: Cyclic Electron Transport Around Ps I In Different Organismsmentioning

confidence: 99%

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

Joët

¹

2002

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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...

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“…This point has been a matter of debate in the last decade given that direct measurements of cyclic electron flow such as those given by photoacoustic experiments failed to detect any significant activity in C 3 plants (Heber and Walker, 1992;Bendall and Manasse, 1995). Using photoacoustic measurements on peas, Malkin et al (1992) measured a weak cyclic activity, saturating at low-light intensity. In the same way, based on measurements of P700 rereduction, chlorophyll fluorescence, and light scattering on spinach, Heber et al (1995a) concluded to low cyclic activity in C 3 plants, mainly restricted to the control of PSII, taking part in the complex machinery that acts to protect the photosynthetic apparatus against photo-inhibition.…”

Section: Involvement Of the Ndh Complex In Cyclic Electron Flow Arounmentioning

confidence: 99%

“…Photoacoustic measurements, which allow a direct and quantitative measurement of energy storage by cyclic electron flow around PSI in vivo, have been used to show the existence of cyclic electron transfer reactions in C 4 plants, algae, and cyanobacteria (Herbert et al, 1990). However, until now, this technique failed to show significant cyclic activity in C 3 plants (Herbert et al, 1990;Malkin et al, 1992). For the unicellular alga Chlamydomonas reinhardtii, Ravenel et al (1994), by studying the effect of antimycin A and of different inhibitors on photoacoustic measurements, proposed that two pathways are operating in vivo around PSI.…”

mentioning

confidence: 99%

Increased Sensitivity of Photosynthesis to Antimycin A Induced by Inactivation of the Chloroplast ndhB Gene. Evidence for a Participation of the NADH-Dehydrogenase Complex to Cyclic Electron Flow around Photosystem I

Joët

¹

,

Cournac

²

,

Horváth

³

et al. 2001

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) were used to study the role of the NADH-dehydrogenase complex (NDH) during photosynthesis and particularly the involvement of this complex in cyclic electron flow around photosystem I (PSI). Photosynthetic activity was determined on leaf discs by measuring CO 2 exchange and chlorophyll fluorescence quenchings during a dark-to-light transition. In the absence of treatment, both non-photochemical and photochemical fluorescence quenchings were similar in ndhB Ϫ and wild type (WT). When leaf discs were treated with 5 m antimycin A, an inhibitor of cyclic electron flow around PSI, both quenchings were strongly affected. At steady state, maximum photosynthetic electron transport activity was inhibited by 20% in WT and by 50% in ndhB Ϫ . Under non-photorespiratory conditions (2% O 2 , 2,500 L L Ϫ1 CO 2 ), antimycin A had no effect on photosynthetic activity of WT, whereas a 30% inhibition was observed both on quantum yield of photosynthesis assayed by chlorophyll fluorescence and on CO 2 assimilation in ndhB Ϫ . The effect of antimycin A on ndhB Ϫ could not be mimicked by myxothiazol, an inhibitor of the mitochondrial cytochrome bc 1 complex, therefore showing that it is not related to an inhibition of the mitochondrial electron transport chain but rather to an inhibition of cyclic electron flow around PSI. We conclude to the existence of two different pathways of cyclic electron flow operating around PSI in higher plant chloroplasts. One of these pathways, sensitive to antimycin A, probably involves ferredoxin plastoquinone reductase, whereas the other involves the NDH complex. The absence of visible phenotype in ndhB Ϫ plants under normal conditions is explained by the complement of these two pathways in the supply of extra-ATP for photosynthesis.During oxygenic photosynthesis of C 3 plants, both photosystem II (PSII) and photosystem I (PSI) cooperate to achieve NADP ϩ reduction using water as an electron donor and generate a trans-membrane proton gradient driving ATP synthesis. Although NADP ϩ reduction is recognized to be dependent on the activity of both photosystems through electron transport reactions of the "Z" scheme (Hill and Bendall, 1960;Redding et al., 1999), it has early been reported from studies on isolated thylakoids that ATP could be produced by the sole PSI through cyclic electron transfer reactions (Arnon, 1959). The cyclic electron flow around PSI has been extensively studied in thylakoids and/or chloroplasts of C 3 plants (for review, see Fork and Herbert, 1993; Bendall and Manasse, 1995). This mechanism has been suggested to provide ATP for a variety of cellular processes, including stress adaptation (Havaux et al., 1991) and CO 2 fixation (Furbank and Horton, 1987; Herbert et al., 1990). During photosynthetic CO 2 fixation, both NADPH and ATP are used to regenerate ribulose-1,5-bisphosphate and allow functioning of the photosynthetic carbon reduction cycle (Calvin cycle). In the absence of Q cycle, when one NADPH is produced by linear electron transport reactions, four H ϩ are released in ...

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“…When the plastic film was not used, leaf discs were soaked for 3 h in an osmoticum buffer (25 mm phosphate buffer, pH 7.0, 200 mm sorbitol, 10 mm KCl, and 2 mm MgCl 2 ) to eliminate the photobaric component of the photoacoustic signal as described by Malkin et al (1992). Synechocystis sp.…”

Section: Photoacoustic Measurements Of Photochemical Esmentioning

confidence: 99%

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

Joët

¹

,

Cournac

²

,

Peltier

³

et al. 2002

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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...

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A photoacoustic study of water infiltrated leaves

Cited by 29 publications

References 29 publications

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

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

Increased Sensitivity of Photosynthesis to Antimycin A Induced by Inactivation of the Chloroplast ndhB Gene. Evidence for a Participation of the NADH-Dehydrogenase Complex to Cyclic Electron Flow around Photosystem I

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

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