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Temperature responses of Rubisco from Paniceae grasses provide opportunities for improving C3 photosynthesis

Abstract

Enhancing the catalytic properties of the CO2-fixing enzyme Rubisco is a target for improving agricultural crop productivity. Here, we reveal extensive diversity in the kinetic response between 10 and 37 °C by Rubisco from C3 and C4 species within the grass tribe Paniceae. The CO2 fixation rate ( k cat c ) for Rubisco from the C4 grasses with nicotinamide adenine dinucleotide (NAD) phosphate malic enzyme (NADP-ME) and phosphoenolpyruvate carboxykinase (PCK) photosynthetic pathways was twofold greater than the k cat c of Rubisco from NAD-ME species across all temperatures. The declining response of CO2/O2 specificity with increasing temperature was less pronounced for PCK and NADP-ME Rubisco, which would be advantageous in warmer climates relative to the NAD-ME grasses. Modelled variation in the temperature kinetics of Paniceae C3 Rubisco and PCK Rubisco differentially stimulated C3 photosynthesis relative to tobacco above and below 25 °C under current and elevated CO2. Amino acid substitutions in the large subunit that could account for the catalytic variation among Paniceae Rubisco are identified; however, incompatibilities with Paniceae Rubisco biogenesis in tobacco hindered their mutagenic testing by chloroplast transformation. Circumventing these bioengineering limitations is critical to tailoring the properties of crop Rubisco to suit future climates.

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Figure 1: The diversity in the catalytic properties of Rubisco at 25 °C across C3 and C4 grasses within Paniceae.
Figure 2: Variation among the Paniceae Rubisco kinetics differentially affect simulated rates of C3 photosynthesis at 25 °C.
Figure 3: Divergence in the catalytic properties of Paniceae and tobacco Rubisco in response to temperature.
Figure 4: The potential for improving the thermal response of C3 photosynthesis.
Figure 5: Approaches to decipher possible catalytic switches in the L-subunit of Paniceae Rubisco.

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Acknowledgements

We thank A. Cousins for supplying their S. viridis Rubisco kinetic data for analysis. This research was funded by the following grants from the Australian Research Council: DE130101760 (R.E.S.), DP120101603 (O.G., S.M.W.) and CE140100015 (O.G., S.M.W.).

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R.E.S., O.G. and S.M.W. designed the study and undertook the experimental work. M.V.K. undertook the phylogenetic analysis and L.H.G. the structural analysis. All authors contributed to drafting the paper.

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Correspondence to Spencer M. Whitney.

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The authors declare no competing financial interests.

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Supplementary Figures 1-7, Supplementary Tables 1-5, Supplementary References. (PDF 2566 kb)

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Sharwood, R., Ghannoum, O., Kapralov, M. et al. Temperature responses of Rubisco from Paniceae grasses provide opportunities for improving C3 photosynthesis. Nature Plants 2, 16186 (2016). https://doi.org/10.1038/nplants.2016.186

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