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Manganese binding to Rubisco could drive a photorespiratory pathway that increases the energy efficiency of photosynthesis

Abstract

Most plants, contrary to popular belief, do not waste over 30% of their photosynthate in a futile cycle called photorespiration. Rather, the photorespiratory pathway generates additional malate in the chloroplast that empowers many energy-intensive chemical reactions, such as those involved in nitrate assimilation. Thus, the balance between carbon fixation and photorespiration determines the plant carbon–nitrogen balance and protein concentrations. Plant protein concentrations, in turn, depend not only on the relative concentrations of carbon dioxide and oxygen in the chloroplast but also on the relative activities of magnesium and manganese, which are metals that associate with several key enzymes in the photorespiratory pathway and alter their function. Understanding the regulation of these processes is critical for sustaining food quality under rising CO2 atmospheres.

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Fig. 1: The proposed photorespiratory pathway within the context of photosynthetic carbon and nitrogen metabolism.
Fig. 2: Mg2+ and Mn2+ activities in chloroplasts and binding of these metals to Rubisco.
Fig. 3: NO3 assimilation.
Fig. 4: Plant responses to CO2 enrichment.
Fig. 5: Possible electron transfers involving manganese during the oxidation of RuBP.

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Acknowledgements

This work was funded by NSF grants IOS-16-55810 and IOS-13-58675, USDA-IWYP-16-06702 and the John B. Orr Endowment. We thank F. Fox for his comments on the manuscript.

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A.J.B. wrote most of the manuscript. K.M.L. contributed the section on the chemistry of Mn2+ electron transfers and helped to edit the entire manuscript.

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Correspondence to Arnold J. Bloom.

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Bloom, A.J., Lancaster, K.M. Manganese binding to Rubisco could drive a photorespiratory pathway that increases the energy efficiency of photosynthesis. Nature Plants 4, 414–422 (2018). https://doi.org/10.1038/s41477-018-0191-0

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