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Temperature responses of the Rubisco maximum carboxylase activity across domains of life: phylogenetic signals, trade-offs, and importance for carbon gain

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Abstract

Temperature response of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) catalytic properties directly determines the CO2 assimilation capacity of photosynthetic organisms as well as their survival in environments with different thermal conditions. Despite unquestionable importance of Rubisco, the comprehensive analysis summarizing temperature responses of Rubisco traits across lineages of carbon-fixing organisms is lacking. Here, we present a review of the temperature responses of Rubisco carboxylase specific activity (\(k_{\text{cat}}^{\text{c}}\)) within and across domains of life. In particular, we consider the variability of temperature responses, and their ecological, physiological, and evolutionary controls. We observed over two-fold differences in the energy of activation (ΔH a) among different groups of photosynthetic organisms, and found significant differences between C3 plants from cool habitats, C3 plants from warm habitats and C4 plants. According to phylogenetically independent contrast analysis, ΔH a was not related to the species optimum growth temperature (T growth), but was positively correlated with Rubisco specificity factor (S c/o) across all organisms. However, when only land plants were analyzed, ΔH a was positively correlated with both T growth and S c/o, indicating different trends for these traits in plants versus unicellular aquatic organisms, such as algae and bacteria. The optimum temperature (T opt) for \(k_{\text{cat}}^{\text{c}}\) correlated with S c/o for land plants and for all organisms pooled, but the effect of T growth on T opt was driven by species phylogeny. The overall phylogenetic signal was significant for all analyzed parameters, stressing the importance of considering the evolutionary framework and accounting for shared ancestry when deciphering relationships between Rubisco kinetic parameters. We argue that these findings have important implications for improving global photosynthesis models.

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Acknowledgments

The study was financially supported by the Spanish Ministry of Science and Innovation (AGL2009-07999 and AGL2013-42364), the Estonian Ministry of Science and Education (Institutional Grant IUT-8-3) and the European Commission through the European Regional Fund (The Center of Excellence in Environmental Adaptation). We appreciate the insightful comments and discussions on the manuscript from three anonymous reviewers.

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Authors and Affiliations

  1. Research Group in Plant Biology Under Mediterranean Conditions, Department of Biology, Universitat de les Illes Balears, Carretera de Valldemossa km 7.5, 07122, Palma, Illes Balears, Spain

    J. Galmés & C. Hermida-Carrera

  2. Plant Science Division, Research School of Biology, The Australian National University, Acton, Canberra, ACT, 2601, Australia

    M. V. Kapralov

  3. Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Kreutzwaldi 1, 51014, Tartu, Estonia

    L. O. Copolovici & Ü. Niinemets

  4. Estonian Academy of Sciences, Kohtu 6, 10130, Tallinn, Estonia

    Ü. Niinemets

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  1. J. Galmés
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  2. M. V. Kapralov
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  3. L. O. Copolovici
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  4. C. Hermida-Carrera
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  5. Ü. Niinemets
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Correspondence to J. Galmés.

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Galmés, J., Kapralov, M.V., Copolovici, L.O. et al. Temperature responses of the Rubisco maximum carboxylase activity across domains of life: phylogenetic signals, trade-offs, and importance for carbon gain. Photosynth Res 123, 183–201 (2015). https://doi.org/10.1007/s11120-014-0067-8

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