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High ammonium supply impairs photosynthetic efficiency in rice exposed to excess light

Abstract

Mechanisms involving ammonium toxicity, excess light, and photosynthesis are scarcely known in plants. We tested the hypothesis that high NH4+ supply in presence of high light decreases photosynthetic efficiency of rice plants, an allegedly tolerant species. Mature rice plants were previously supplied with 10 mM NH4+ or 10 mM NO3− and subsequently exposed to 400 µmol m−2 s−1 (moderate light—ML) or 2000 µmol m−2 s−1 (high light—HL) for 8 h. HL greatly stimulated NH4+ accumulation in roots and in a minor extent in leaves. These plants displayed significant delay in D1 protein recovery in the dark, compared to nitrate-supplied plants. These responses were related to reduction of both PSII and PSI quantum efficiencies and induction of non-photochemical quenching. These changes were also associated with higher limitation in the donor side and lower restriction in the acceptor side of PSI. This later response was closely related to prominent decrease in stomatal conductance and net CO2 assimilation that could have strongly affected the energy balance in chloroplast, favoring ATP accumulation and NPQ induction. In parallel, NH4+ induced a strong increase in the electron flux to photorespiration and, inversely, it decreased the flux to Rubisco carboxylation. Overall, ammonium supply negatively interacts with excess light, possibly by enhancing ammonium transport towards leaves, causing negative effects on some photosynthetic steps. We propose that high ammonium supply to rice combined with excess light is capable to induce strong delay in D1 protein turnover and restriction in stomatal conductance, which might have contributed to generalized disturbances on photosynthetic efficiency.

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Abbreviations

Amax :

Maximum net CO2 assimilation rate

Ci:

Intercellular CO2 partial concentration

ETRI:

Electron transport rate at PSI

ETRII:

Electron transport rate at PSII

Fm:

Dark maximum fluorescence

Fm′:

Light maximum fluorescence

Fo:

Dark minimum fluorescence

Fo′:

Light minimum fluorescence after the far-red illumination

Fs:

Light steady-state fluorescence

Fv/Fm:

Maximum quantum efficiency of PSII

Jc:

Electron flux to Rubisco carboxylation

Jmax:

Maximum electron transport rate

Jo:

Electron flux to Rubisco oxygenation

NPQ:

Non-photochemical quenching

OEC:

Oxygen evolving complex

PPFD:

Photosynthetic photon flux density

Vcmax:

Maximum Rubisco carboxylation rate

Φ(NA):

Acceptor side limitation of PSI

Φ(ND):

Donor side limitation of PSI

PETC:

Photosynthetic electron transport chain

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Acknowledgements

The authors are grateful to Prof. Danilo M. Daloso for the manuscript revision and important suggestions. Authors also acknowledge to Coordination for the Improvement of Higher Education Personnel (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—CAPES), National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq), INCT Plant Stress Biotech (Conselho de Desenvolvimento Científico e Tecnológico) Proc. 465480/2014-4 and Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP) for funding. FELC is supported by FUNCAP/CAPES (Bolsista CAPES/BRASIL—Proc. 88887.162856/2018-00). AKML is supported by CNPq (Proc. 154471/2018-6).

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Correspondence to J. A. G. Silveira.

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Alencar, V.T.C.B., Lobo, A.K.M., Carvalho, F.E.L. et al. High ammonium supply impairs photosynthetic efficiency in rice exposed to excess light. Photosynth Res 140, 321–335 (2019). https://doi.org/10.1007/s11120-019-00614-z

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  • DOI: https://doi.org/10.1007/s11120-019-00614-z

Keywords

  • Ammonia toxicity
  • D1 turnover
  • Photosynthesis
  • Photoinhibition
  • Photosystems
  • Oryza sativa