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Artificial remodelling of alternative electron flow by flavodiiron proteins in Arabidopsis


In photosynthesis, linear electron transport from water to nicotinamide adenine dinucleotide phosphate (NADP+) cannot satisfy the ATP/NADPH production stoichiometry required by the Calvin–Benson cycle. Cyclic electron transport (CET) around photosystem I (PSI) and pseudocyclic electron transport (pseudoCET) can produce ATP without the accumulation of NADPH. Flavodiiron proteins (Flv) are the main mediator of pseudoCET in photosynthetic organisms, spanning cyanobacteria to gymnosperms. However, their genes are not conserved in angiosperms. Here we explore the possibility of complementing CET with Flv-dependent pseudoCET in the angiosperm Arabidopsis thaliana. We introduced FlvA and FlvB genes from the moss Physcomitrella patens into both wild-type (WT) Arabidopsis and the proton gradient regulation 5 (pgr5) mutant, which is defective in the main pathway of CET. We measured rates of pseudoCET using membrane inlet mass spectrometry, along with several photosynthetic parameters. Flv expression significantly increased rates of pseudoCET in the mutant plants, particularly at high light intensities, and partially restored the photosynthetic phenotype. In WT plants, Flv did not compete with PGR5-dependent CET during steady-state photosynthesis, but did form a large electron sink in fluctuating light. We conclude that flavodiiron proteins can help to protect the photosystems in Arabidopsis under fluctuating light, even in the presence of CET.

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Figure 1: A schematic representation of alternative electron transport pathways.
Figure 2: Expression of P. patens Flv in Arabidopsis.
Figure 3: Flv-dependent O2 uptake in the MIMS conditions.
Figure 4: Impact of the Flv accumulation on electron transport in ambient air.
Figure 5: Flv-dependent pseudoCET protects photosystems from photodamage under fluctuating light.

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We thank A. Tahara (Kyoto University) and P. Kell (Australian National University) for skilled technical support and A. Makino (Tohoku University), T. Hase (Osaka University), H. Mi (Shanghai Institutes for Biological Sciences, Chinese Academy of Science) for their gifts of antibodies. The information about nucleotide sequences of M. polymorpha Flvs was kindly provided by T. Kohchi (Kyoto University). This work was supported by grants from the Japan Science and Technology Agency (CREST program), the Ministry of Agriculture, Forestry and Fisheries (GPN0008), and the Japanese Society for the Promotion of Science (25251032) and the project Network of Centers of Carbon Dioxide Resource Studies in Plants.

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H.Y. and T.S. designed the research; H.Y. produced transgenic plants; H.Y. and S.T. analysed the plants. All authors designed the experiments, interpreted results and wrote the manuscript.

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Correspondence to Hiroshi Yamamoto or Toshiharu Shikanai.

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The authors declare no competing financial interests.

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Yamamoto, H., Takahashi, S., Badger, M. et al. Artificial remodelling of alternative electron flow by flavodiiron proteins in Arabidopsis. Nature Plants 2, 16012 (2016).

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