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Characterization of photosynthetic electron transport in bundle sheath cells of maize. I. Ascorbate effectively stimulates cyclic electron flow around PSI

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Abstract

Redox changes of the reaction-center chlorophyll of photosystem I (P700) and chlorophyll fluorescence yield were measured in bundle sheath strands (BSS) isolated from maize (Zea mays L.) leaves. Oxidation of P700 in BSS by actinic light was suppressed by nigericin, indicating the generation of a proton gradient across the thylakoid membranes of BSS chloroplasts. Methyl viologen, which transfers electrons from photosystem I (PSI) to O2, caused a considerable decrease in the reduction rate of P700+ in BSS after turning off actinic light, showing that electron flow from the acceptor side of PSI to stromal components is critical for this reduction. Ascorbate (Asc), and to a lesser extent malate (Mal), caused a lower level of P700+ in BSS under aerobic conditions in far-red light, implying electron donation from these substances to the intersystem carriers. When Asc or Mal was added to BSS during pre-illumination under anaerobic conditions in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethyl urea (DCMU), the far-red-induced level of P700+ was lowered. The results suggest Asc and Mal can cause reduction of stromal donors, which in turn establishes conditions for rapid PSI-driven P700+ reduction. Addition of these metabolites also strongly stimulated the development of a proton gradient in thylakoids under aerobic conditions in the absence of DCMU, i.e. under conditions analogous to those in vivo. Ascorbate was a much more effective electron donor than Mal, suggesting it has a physiological role in activation of cyclic electron flow around PSI.

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Abbreviations

Asc :

Ascorbate

BS :

Bundle sheath

BSS :

Bundle sheath strands

Chl :

Chlorophyll

CEF1 :

Cyclic electron flow around PSI

DBMIB :

2,5-Dibromo-3-methyl-6-isopropyl-p-benzoquinone

DCMU :

3-(3,4-dichlorophenyl)-1,1-dimethyl urea

FR :

Far-red light

Mal :

Malate

MV :

Methyl viologen (paraquat)

NADP-ME :

NADP-malic enzyme

NDH :

NAD(P)H dehydrogenase

PSI, PSII:

Photosystem I, II

P700, P700+:

Reduced and oxidized forms of reaction center chlorophyll of PSI

pmf :

Proton-motive force

ΔpH :

pH difference between the lumen and stroma

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Acknowledgements

This work was supported by Grant 02-04-49285 from the Russian Foundation for Basic Research, the U.S. Department of Energy Grant DE-FG02-04ER15559, NSF Grant IBN-0131098 and the fellowship programs for research in Japan to B.I. from the Japan Society for Promotion of Science.

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Authors and Affiliations

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

    Gerald Edwards

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

    Boris Ivanov

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

    Kozi Asada

  4. Institute of Biological Chemistry, Washington State University, Pullman, WA 99164-6340, USA

    David M. Kramer

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  1. Boris Ivanov
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  2. Kozi Asada
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  3. David M. Kramer
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  4. Gerald Edwards
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Correspondence to Gerald Edwards.

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Ivanov, B., Asada, K., Kramer, D.M. et al. Characterization of photosynthetic electron transport in bundle sheath cells of maize. I. Ascorbate effectively stimulates cyclic electron flow around PSI. Planta 220, 572–581 (2005). https://doi.org/10.1007/s00425-004-1367-6

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  • DOI: https://doi.org/10.1007/s00425-004-1367-6

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