Temperature responses of the Rubisco maximum carboxylase activity across domains of life: Phylogenetic signals, trade-offs, and importance for carbon gain (2024)

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 (kcatc) 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 kcatc 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.

Original languageEnglish
Pages (from-to)183-201
Number of pages19
JournalPhotosynthesis Research
Volume123
Issue number2
DOIs
Publication statusPublished - Feb 2015

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Galmés, J., Kapralov, M. V., Copolovici, L. O., Hermida-Carrera, C., & Niinemets (2015). Temperature responses of the Rubisco maximum carboxylase activity across domains of life: Phylogenetic signals, trade-offs, and importance for carbon gain. Photosynthesis Research, 123(2), 183-201. https://doi.org/10.1007/s11120-014-0067-8

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. In: Photosynthesis Research. 2015 ; Vol. 123, No. 2. pp. 183-201.

@article{3f910e9d16ae435091322d6bc3d22833,

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

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 (kcatc) 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 kcatc 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.",

keywords = "Activation energy, Adaptation, Carboxylation, Evolution, Photosynthesis, Temperature dependencies",

author = "J. Galm{\'e}s and Kapralov, {M. V.} and Copolovici, {L. O.} and C. Hermida-Carrera and Niinemets",

note = "Publisher Copyright: {\textcopyright} 2014 Springer Science+Business Media Dordrecht.",

year = "2015",

month = feb,

doi = "10.1007/s11120-014-0067-8",

language = "English",

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Galmés, J, Kapralov, MV, Copolovici, LO, Hermida-Carrera, C & Niinemets 2015, 'Temperature responses of the Rubisco maximum carboxylase activity across domains of life: Phylogenetic signals, trade-offs, and importance for carbon gain', Photosynthesis Research, vol. 123, no. 2, pp. 183-201. https://doi.org/10.1007/s11120-014-0067-8

Temperature responses of the Rubisco maximum carboxylase activity across domains of life: Phylogenetic signals, trade-offs, and importance for carbon gain. / Galmés, J.; Kapralov, M. V.; Copolovici, L. O. et al.
In: Photosynthesis Research, Vol. 123, No. 2, 02.2015, p. 183-201.

Research output: Contribution to journalArticlepeer-review

TY - JOUR

T1 - Temperature responses of the Rubisco maximum carboxylase activity across domains of life

T2 - Phylogenetic signals, trade-offs, and importance for carbon gain

AU - Galmés, J.

AU - Kapralov, M. V.

AU - Copolovici, L. O.

AU - Hermida-Carrera, C.

AU - Niinemets,

N1 - Publisher Copyright:© 2014 Springer Science+Business Media Dordrecht.

PY - 2015/2

Y1 - 2015/2

N2 - 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 (kcatc) 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 kcatc 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.

AB - 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 (kcatc) 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 kcatc 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.

KW - Activation energy

KW - Adaptation

KW - Carboxylation

KW - Evolution

KW - Photosynthesis

KW - Temperature dependencies

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Galmés J, Kapralov MV, Copolovici LO, Hermida-Carrera C, Niinemets. Temperature responses of the Rubisco maximum carboxylase activity across domains of life: Phylogenetic signals, trade-offs, and importance for carbon gain. Photosynthesis Research. 2015 Feb;123(2):183-201. doi: 10.1007/s11120-014-0067-8

Temperature responses of the Rubisco maximum carboxylase activity across domains of life: Phylogenetic signals, trade-offs, and importance for carbon gain (2024)
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