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Analysis of donors of electrons to photosystem I and cyclic electron flow by redox kinetics of P700 in chloroplasts of isolated bundle sheath strands of maize

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Abstract

Bundle sheath chloroplasts of NADP-malic enzyme (NADP-ME) type C4 species have a high demand for ATP, while being deficient in linear electron flow and oxidation of water by photosystem II (PSII). To evaluate electron donors to photosystem I (PSI) and possible pathways of cyclic electron flow (CEF1) in isolated bundle sheath strands of maize (Zea mays L.), an NADP-ME species, light-induced redox kinetics of the reaction center chlorophyll of PSI (P700) were followed under aerobic conditions. Donors of electrons to CEF1 are needed to compensate for electrons lost from the cycle. When stromal electron donors to CEF1 are generated during pre-illumination with actinic light (AL), they retard the subsequent rate of oxidation of P700 by far-red light. Ascorbate was more effective than malate in generating stromal electron donors by AL. The generation of stromal donors by ascorbate was inhibited by DCMU, showing ascorbate donates electrons to the oxidizing side of PSII. The inhibitors of NADPH dehydrogenase (NDH), amytal and rotenone, accelerated the oxidation rate of P700 by far-red light after AL, indicating donation of electrons to the intersystem from stromal donors via NDH. These inhibitors, however, did not affect the steady-state level of P700+ under AL, which represents a balance of input and output of electrons in P700. In contrast, antimycin A, the inhibitor of the ferredoxin-plastoquinone reductase-dependent CEF1, substantially lowered the level of P700+ under AL. Thus, the primary pathway of ATP generation by CEF1 may be through ferredoxin-plastoquinone, while function of CEF1 via NDH may be restricted by low levels of ferredoxin-NADP reductase. NDH may contribute to redox poising of CEF1, or function to generate ATP in linear electron flow to O2 via PSI, utilizing NADPH generated from malate by chloroplastic NADP-ME.

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Abbreviations

AA:

Antimycin A

AL:

Actinic light

Asc:

Ascorbate

BS:

Bundle sheath

BSS:

Bundle sheath strands

CEF1:

Cyclic electron flow around photosystem I

Chl:

Chlorophyll

DCMU:

3-(3,4-Dichlorophenyl)-1,1-dimethylurea

Fd:

Ferredoxin

Fdrd :

Reduced ferredoxin

FR:

Far-red light

Mal:

Malate

Mv:

Methyl viologen

NADP-ME:

NADP-malic enzyme

NDH:

NADPH dehydrogenase

Nig:

Nigericin

PQ:

Plastoquinone

PSI:

Photosystem I

PSII:

Photosystem II

P700, P700+ :

Reduced and oxidized forms of reaction center chlorophyll of PSI

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Acknowledgments

This work was supported by Grant 05-04-48629 from the Russian Foundation for Basic Research, U.S. Department of Energy Grant DE-FG02-04ER15559, NSF Grants IBN-0131098 and IBN 0236959, and by the Fellowship Programs for Research in Japan from the Japan Society for Promotion of Science. The authors are grateful to Drs. J. Mano, S. Khorobrykh, and R. Bassi for valuable discussions.

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Authors and Affiliations

  1. Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, 142290, Russia

    Boris Ivanov

  2. Faculty of Biotechnology and Life Science, Fukuyama University, Gakuen-cho 1, Fukuyama, 729-0292, Japan

    Kozi Asada

  3. School of Biological Sciences, Washington State University, Pullman, WA, 99164-4236, USA

    Gerald E. Edwards

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  1. Boris Ivanov
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  2. Kozi Asada
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  3. Gerald E. Edwards
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Correspondence to Gerald E. Edwards.

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Ivanov, B., Asada, K. & Edwards, G.E. Analysis of donors of electrons to photosystem I and cyclic electron flow by redox kinetics of P700 in chloroplasts of isolated bundle sheath strands of maize. Photosynth Res 92, 65–74 (2007). https://doi.org/10.1007/s11120-007-9166-0

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