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 (c(cat)(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(cat)(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.

Rubisco Catalytic Properties and Temperature Response in Crops

“…This finding contrasts with previous evidence suggesting that the temperature sensitivity of Rubisco kinetic properties has evolved to improve the enzyme's performance according to the prevailing thermal environment to which each species is adapted (Sage, 2002;Galmés et al, 2005Galmés et al, , 2015.…”

“…In particular, Rubisco catalytic parameters are highly sensitive to changes in temperature. For instance, the maximum carboxylase turnover rate (k cat c ) increases exponentially with temperature (Sage, 2002;Galmés et al, 2015). However, at temperatures higher than the photosynthetic thermal optimum, the increases in k cat c are not translated into increased CO 2 assimilation because of the decreased affinity of Rubisco for CO 2 (i.e.…”

Temperature response of C4 photosynthesis: Biochemical analysis of Rubisco, Phosphoenolpyruvate Carboxylase and Carbonic Anhydrase in Setaria viridis.

“…However, there is less support in the literature for differences in the temperature response between C 3 and C 4 Rubisco (Jordan and Ogren, 1984;Sage, 2002;Galmés et al, 2015;Perdomo et al, 2015). The Rubisco temperature responses of S. viridis presented here are similar to the available temperature responses of C 3 species, suggesting a generally conserved variation in kinetic parameters.…”

“…These C 3 temperature responses are typically applied to C 4 Rubisco 25°C values, with the assumption that the temperature response is similar between these two photosynthetic functional types (Berry and Farquhar, 1978). However, this assumption has not been tested for the Rubisco parameters used in the C 4 model of photosynthesis, and the previous comparisons of C 3 and C 4 Rubisco temperature responses have been limited to k catCO2 and S C/O (Björkman and Pearcy, 1970;Jordan and Ogren, 1984;Sage, 2002;Galmés et al, 2015) and a recent investigation comparing k catCO2 , K C , and S C/O between C 3 , C 4 , and intermediate species within the Flaveria lineage (Perdomo et al, 2015). However, these studies lack comparisons of the oxygenation parameters k catO2 and K O needed to accurately predict the temperature response of carboxylation and oxygenation.…”

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

“…Furthermore, at any given [CO 2 ], Rubisco catalysis is also strongly affected by temperature. In particular, the maximum carboxylase turnover rate ($k_{\text{cat}}^{\text{c}}$) of Rubisco increases up to 50–55 ºC or even higher for some organisms from extreme environments (Galmés et al , 2015 for a review), while the Rubisco specificity factor ( S c/o ) decreases and the Michaelis–Menten constants for CO 2 ( K c ) and O 2 ( K o ) increase (Bernacchi et al , 2001). Although the basic patterns of temperature-dependent variation in key Rubisco kinetic characteristics are well known and measured in a number of studies, there is surprisingly limited comparative information of the variability of temperature responses of Rubisco across different photosynthetic groups that evolved at different periods of time, as well as among photosynthetic organisms adapted to different environmental conditions.…”