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Opposite domination of cyclic and pseudocyclic electron flows in short-illuminated dark-adapted leaves of angiosperms and gymnosperms

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Abstract

The present work was aimed to explain the recently reported higher O2-dependent electron flow capacity in gymnosperms than in angiosperms and to search for other differences in the electron transport processes by simultaneous characterization of the relative capacities of pseudocyclic (direct or Flavodiiron proteins (Flv)-mediated O2-reduction, Mehler(-like) reactions) and cyclic electron flows around photosystem I (CEF-PSI). To this end, a comparative multicomponent analysis was performed on the fluorescence decay curves of dark-adapted leaves after illumination with a 1-s saturating light pulse. In both gymnosperms and angiosperms, two or three exponential decay components were resolved: fast (t 1/21 ~ 170–260 ms), middle (~1.0–2.3 s), and slow (>4.2 s). The sensitivity of the decay parameters (amplitudes A1–3, halftimes t 1/2 1–3) to the alternative electron flows was assessed using Arabidopsis pgr5 and ndhM mutants, defective in CEF-PSI, Synechocystis sp. PCC 6803 Δflv1 mutant, defective in Flv-mediated O2-photoreduction, different O2 concentrations, and methyl viologen treatment. A1 reflected the part of electrons involved in linear and O2-photoreduction pathways after PSI. The middle component appeared in pgr5 (but not in ndhM), in gymnosperms under low O2, and in Δflv1, and reflected limitations at the PSI acceptor side. The slow component was sensitive to CEF-PSI. The comparison of decay parameters provided evidence that Flv mediate O2-photoreduction in gymnosperms, which explains their higher O2-dependent electron flow capacity. The concomitant quantification of relative electrons branching in O2-photoreduction and CEF-PSI pathways under the applied non-steady-state photosynthetic conditions reveals that CEF-PSI capacity significantly exceeds that of O2-photoreduction in angiosperms while the opposite occurs in gymnosperms.

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Abbreviations

CEF-PSI:

Cyclic electron flows around photosystem I

Chl:

Chlorophyll

Flv:

Flavodiiron proteins

Fd:

Ferredoxin

FR:

Far-red

IRF:

Instrument response function

LEF:

Linear electron flow

MV:

Methyl viologen

NDH:

NADH dehydrogenase-like complex

PGR5:

Proton gradient regulation 5

PGRL1:

Pgr5-like photosynthetic phenotype 1

PQ:

Plastoquinone

PS:

Photosystem

QA(B) :

The primary (secondary) quinone electron acceptor in PSII

SP:

Saturating pulse

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Acknowledgements

We thank the Kyushu University Forest for collection of the materials. R. V. thanks the Bulgarian Academy of Sciences for their support.

Funding

This work was supported by a grant-in-aid for scientific research from JSPS (No. 26450200) and by the JSPS Invitation Fellowships in Japan (to R. V.).

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Authors and Affiliations

  1. Department of Agriculture, Forest and Forest Products Sciences, Plant Metabolic Physiology, Kyushu University, Fukuoka, 812-8581, Japan

    Mari Noridomi, Shouta Nakamura & Michito Tsuyama

  2. Department of Molecular and Cell Biology, Forestry and Forest Products Research Institute, 1 Matsunosato, Tsukuba, Ibaraki, 305-8687, Japan

    Norihiro Futamura

  3. Institute of Biophysics and Biomedical Engineering, Bulgarian Academy of Sciences, Acad. G. Bonchev St. 21, 1113, Sofia, Bulgaria

    Radka Vladkova

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  1. Mari Noridomi
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  2. Shouta Nakamura
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Correspondence to Michito Tsuyama.

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Noridomi, M., Nakamura, S., Tsuyama, M. et al. Opposite domination of cyclic and pseudocyclic electron flows in short-illuminated dark-adapted leaves of angiosperms and gymnosperms. Photosynth Res 134, 149–164 (2017). https://doi.org/10.1007/s11120-017-0419-2

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