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Repetitive light pulse-induced photoinhibition of photosystem I severely affects CO2 assimilation and photoprotection in wheat leaves

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Abstract

It was previously found that photosystem I (PSI) photoinhibition represents mostly irreversible damage with a slow recovery; however, its physiological significance has not been sufficiently characterized. The aim of the study was to assess the effect of PSI photoinhibition on photosynthesis in vivo. The inactivation of PSI was done by a series of short light saturation pulses applied by fluorimeter in darkness (every 10 s for 15 min), which led to decrease of both PSI (~60 %) and photosystem II (PSII) (~15 %) photochemical activity. No PSI recovery was observed within 2 days, whereas the PSII was fully recovered. Strongly limited PSI electron transport led to an imbalance between PSII and PSI photochemistry, with a high excitation pressure on PSII acceptor side and low oxidation of the PSI donor side. Low and delayed light-induced NPQ and P700+ rise in inactivated samples indicated a decrease in formation of transthylakoid proton gradient (ΔpH), which was confirmed also by analysis of electrochromic bandshift (ECSt) records. In parallel with photochemical parameters, the CO2 assimilation was also strongly inhibited, more in low light (~70 %) than in high light (~45 %); the decrease was not caused by stomatal closure. PSI electron transport limited the CO2 assimilation at low to moderate light intensities, but it seems not to be directly responsible for a low CO2 assimilation at high light. In this regard, the possible effects of PSI photoinhibition on the redox signaling in chloroplast and its role in downregulation of Calvin cycle activity are discussed.

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Abbreviations

\(A_{{{\text{CO}}_{2} }}\) :

CO2 assimilation rate

CET:

Cyclic electron transport

cyt b 6/f :

Cytochrome b 6/f

ECS:

Electrochromic shift

ETR:

Apparent electron transport rate

F 0 :

Minimum fluorescence from dark-adapted leaf (PSII centers open)

\(F_{0}^{\prime}\) :

Minimum fluorescence from light-adapted leaf

F m, \(F_{\rm m}^{\prime}\) :

Maximum fluorescence from dark- or light-adapted leaf respectively (PS II centers closed)

FNR:

Ferredoxin NADP+ oxidoreductase

F v/F m :

Maximum quantum yield of PSII photochemistry

gH+ :

Transthylakoid proton conductivity

LED:

Light emitting diode

LHC:

Light harvesting complex

NPQ:

Non-photochemical quenching

P :

P700 absorbance at given light intensity

P700:

Primary electron donor of PSI (reduced form)

P700+ :

Primary electron donor of PSI (oxidized form)

PAM:

Pulse-amplitude modulated

PAR:

Photosynthetic active radiation

P m, \(P_{\rm m}^{\prime}\) :

Maximum P700 signal in dark- or light-adapted state

Pmf:

Proton motive force

PS I:

Photosystem I

PS II:

Photosystem II

Q A :

Primary PSII acceptor

Q −A /Q A :

Total Redox poise of the primary electron acceptor of PSII (1 − qP)

qE:

PH dependent energy dissipation

qL:

‘Lake’ model photochemical quenching coefficient

qP:

‘Puddle’ model photochemical quenching coefficient

SP:

Saturation light pulse

ΔpH:

Transthylakoid pH gradient

ΔpHpmf :

Osmotic component of proton motive force

Φ NA :

Quantum yield of non-photochemical energy dissipation in PSI due to acceptor side limitation

Φ ND :

Quantum yield of non-photochemical energy dissipation in PSI due to donor side limitation

Φ NO :

Quantum efficiency of non-regulated energy dissipation in PSII

Φ NPQ :

Quantum yield of pH-dependent energy dissipation in PSII

Φ PSI :

Effective quantum yield (efficiency) of PSI photochemistry at given actinic light intensity

Φ PSII :

Actual quantum yield (efficiency) of PSII photochemistry

Δψ :

Transmembrane electric potential

Δψ pmf :

Electric component of proton motive force

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Acknowledgments

This work was supported by the European Community under the project no. 26220220180: “Construction of the “AgroBioTech” Research Centre and  project “Center of Excellence for Agrobiodiversity Conservation and Use, ECOVA”.” SIA was supported by Grants from the Russian Foundation for Basic Research (Nos. 14-04-01549, 14-04-92690), and by Molecular and Cell Biology Programs of the Russian Academy of Sciences.

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Authors and Affiliations

  1. Department of Plant Physiology, Slovak Agricultural University, Tr. A. Hlinku 2, 949 76, Nitra, Slovak Republic

    Marek Zivcak, Marian Brestic, Kristyna Kunderlikova & Oksana Sytar

  2. Department of Plant Physiology and Ecology, Taras Shevchenko National University of Kyiv, Volodymyrska St. 64, Kyiv, 01601, Ukraine

    Oksana Sytar

  3. Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, Moscow, 127276, Russia

    Suleyman I. Allakhverdiev

  4. Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, 142290, Russia

    Suleyman I. Allakhverdiev

  5. Department of Plant Physiology, Faculty of Biology, M.V. Lomonosov Moscow State University, Leninskie Gory 1-12, Moscow, 119991, Russia

    Suleyman I. Allakhverdiev

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  1. Marek Zivcak
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Correspondence to Marian Brestic or Suleyman I. Allakhverdiev.

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Zivcak, M., Brestic, M., Kunderlikova, K. et al. Repetitive light pulse-induced photoinhibition of photosystem I severely affects CO2 assimilation and photoprotection in wheat leaves. Photosynth Res 126, 449–463 (2015). https://doi.org/10.1007/s11120-015-0121-1

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