2016Journal of Experimental BotanyOpen access

A compendium of temperature responses of Rubisco kinetic traits: variability among and within photosynthetic groups and impacts on photosynthesis modeling

Jeroni Galmés, Carmen Hermida‐Carrera, Lauri Laanisto, Ülo Niinemets

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Abstract

The present study provides a synthesis of the in vitro and in vivo temperature responses of Rubisco Michaelis-Menten constants for CO2 (Kc) and O2 (Ko), specificity factor (Sc,o) and maximum carboxylase turnover rate (kcatc) for 49 species from all the main photosynthetic kingdoms of life. Novel correction routines were developed for in vitro data to remove the effects of study-to-study differences in Rubisco assays. The compilation revealed differences in the energy of activation (∆Ha) of Rubisco kinetics between higher plants and other photosynthetic groups, although photosynthetic bacteria and algae were under-represented and very few species have been investigated so far. Within plants, the variation in Rubisco temperature responses was related to species' climate and photosynthetic mechanism, with differences in ∆Ha for kcatc among C3 plants from cool and warm environments, and in ∆Ha for kcatc and Kc among C3 and C4 plants. A negative correlation was observed among ∆Ha for Sc/o and species' growth temperature for all data pooled, supporting the convergent adjustment of the temperature sensitivity of Rubisco kinetics to species' thermal history. Simulations of the influence of varying temperature dependences of Rubisco kinetics on Rubisco-limited photosynthesis suggested improved photosynthetic performance of C3 plants from cool habitats at lower temperatures, and C3 plants from warm habitats at higher temperatures, especially at higher CO2 concentration. Thus, variation in Rubisco kinetics for different groups of photosynthetic organisms might need consideration to improve prediction of photosynthesis in future climates. Comparisons between in vitro and in vivo data revealed common trends, but also highlighted a large variability among both types of Rubisco kinetics currently used to simulate photosynthesis, emphasizing the need for more experimental work to fill in the gaps in Rubisco datasets and improve scaling from enzyme kinetics to realized photosynthesis.

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What this paper is about

The present study provides a synthesis of the in vitro and in vivo temperature responses of Rubisco Michaelis-Menten constants for CO2 (Kc) and O2 (Ko), specificity factor (Sc,o) and maximum carboxylase turnover rate (kcatc) for 49 species from all the main photosynthetic kingdoms of life. Novel correction routines were developed for in vitro data to remove the effects of study-to-study differences in Rubisco assays. The compilation revealed differences in the energy of activation (∆Ha) of Rubisco kinetics between higher plants and other photosynthetic groups, although photosynthetic bacteria and algae were under-represented and very few species have been investigated so far. Within plants, the variation in Rubisco temperature responses was related to species' climate and photosynthetic mechanism, with differences in ∆Ha for kcatc among C3 plants from cool and warm environments, and in ∆Ha for kcatc and Kc among C3 and C4 plants. A negative correlation was observed among ∆Ha for Sc/o and species' growth temperature for all data pooled, supporting the convergent adjustment of the temperature sensitivity of Rubisco kinetics to species' thermal history. Simulations of the influence of varying temperature dependences of Rubisco kinetics on Rubisco-limited photosynthesis suggested improved photosynthetic performance of C3 plants from cool habitats at lower temperatures, and C3 plants from warm habitats at higher temperatures, especially at higher CO2 concentration. Thus, variation in Rubisco kinetics for different groups of photosynthetic organisms might need consideration to improve prediction of photosynthesis in future climates. Comparisons between in vitro and in vivo data revealed common trends, but also highlighted a large variability among both types of Rubisco kinetics currently used to simulate photosynthesis, emphasizing the need for more experimental work to fill in the gaps in Rubisco datasets and improve scaling from enzyme kinetics to realized photosynthesis.

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Available abstract

The present study provides a synthesis of the in vitro and in vivo temperature responses of Rubisco Michaelis-Menten constants for CO2 (Kc) and O2 (Ko), specificity factor (Sc,o) and maximum carboxylase turnover rate (kcatc) for 49 species from all the main photosynthetic kingdoms of life. Novel correction routines were developed for in vitro data to remove the effects of study-to-study differences in Rubisco assays. The compilation revealed differences in the energy of activation (∆Ha) of Rubisco kinetics between higher plants and other photosynthetic groups, although photosynthetic bacteria and algae were under-represented and very few species have been investigated so far. Within plants, the variation in Rubisco temperature responses was related to species' climate and photosynthetic mechanism, with differences in ∆Ha for kcatc among C3 plants from cool and warm environments, and in ∆Ha for kcatc and Kc among C3 and C4 plants. A negative correlation was observed among ∆Ha for Sc/o and species' growth temperature for all data pooled, supporting the convergent adjustment of the temperature sensitivity of Rubisco kinetics to species' thermal history. Simulations of the influence of varying temperature dependences of Rubisco kinetics on Rubisco-limited photosynthesis suggested improved photosynthetic performance of C3 plants from cool habitats at lower temperatures, and C3 plants from warm habitats at higher temperatures, especially at higher CO2 concentration. Thus, variation in Rubisco kinetics for different groups of photosynthetic organisms might need consideration to improve prediction of photosynthesis in future climates. Comparisons between in vitro and in vivo data revealed common trends, but also highlighted a large variability among both types of Rubisco kinetics currently used to simulate photosynthesis, emphasizing the need for more experimental work to fill in the gaps in Rubisco datasets and improve scaling from enzyme kinetics to realized photosynthesis.

Key concepts: RuBisCO, Photosynthesis, Biology, Botany, Pyruvate carboxylase, Carbon fixation, Biochemistry, Enzyme

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