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. 2016 Sep;67(17):5067-91.
doi: 10.1093/jxb/erw267. Epub 2016 Jul 12.

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

Jeroni Galmés  1 , Carmen Hermida-Carrera  2 , Lauri Laanisto  3 , Ülo Niinemets  4
Affiliations

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

Jeroni Galmés et al. J Exp Bot. 2016 Sep.

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.

Keywords: Activation energy; adaptation; carboxylation; meta-analysis; photosynthesis; temperature dependences..

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Figures

Fig. 1.
Fig. 1.
Values of the Rubisco specificity factor for CO2/O2 (Sc/o) in liquid phase at a range of temperatures in different phylogenetic groups of photosynthetic organisms (A) and in land plants only (B). (A) Open upward triangles and short-dashed line, Proteobacteria; open circles and dash-dotted line, Cyanobacteria; filled circles and long-short-dashed line, Bacillariophyta (diatoms); empty diamond and long-dashed line, Rhodophyta (red algae); filled squares and solid line, Spermatophyta (plants). Sample number n=4 for Bacillariophyta and n=30 for Spermatophyta; no replication was available for Proteobacteria, Cyanobacteria and Rhodophyta. The inset in shows the values of Sc/o for Rhodophyta. (B) Open downward triangles and dotted line, C3 plants from cool habitats (n=8); open upward triangles and long-dashed line, C3 plants from warm habitats (n=16); open circles and solid line, C4 plants (n=6). Different letters denote statistically significant differences by Duncan’s analysis (P<0.05) among plant functional and photosynthetic groups. All data for Sc/o correspond to in vitro measurements at discrete temperatures from data shown in Table 3 after applying Eq. 12, and were standardized to a common set of liquid-phase CO2 and O2 physico-chemical characteristics by Eqs 1–7. For CO2, these equations correct for study-to-study differences in assumed bicarbonate equilibrium as dependent on solution pH, temperature and ionic strength and when pertinent study-to-study differences in the value of Henry’s law constant used. For O2, these equations standardize for differences in the value of Henry’s law constant used. Means and standard errors are provided when n≥2. Table 1 provides Henry’s law constants that can be used to convert the Rubisco kinetic characteristics to gas-phase equivalent values.
Fig. 2.
Fig. 2.
Values of the Rubisco Michaelis–Menten constant for CO2 (Kc) in liquid phase at a range of temperatures in different phylogenetic groups (A) and in land plants only (B). (A) Open circles and dash-dotted line, Cyanobacteria; filled circles and dashed line, Bacillariophyta (diatoms); filled squares and solid line, Spermatophyta (plants). Sample number n=2 for Bacillariophyta and n=17 for Spermatophyta; no replication was available for Cyanobacteria. (B) Open downward triangles and dotted line, C3 plants from cool habitats (n=5); open upward triangles and dashed line, C3 plants from warm habitats (n=7); open circles and dotted line, C4 plants (n=5). Values for Kc correspond to in vitro measurements at discrete temperatures from data shown in Table 3 after applying Eq. 12, and were standardized to a common set of CO2 liquid-phase physico-chemical characteristics as explained in Fig. 1 (Table 1 for Henry’s law constants for CO2 and O2 that can be used to convert the values reported to gas-phase equivalents). Data presentation as in Fig. 1.
Fig. 3.
Fig. 3.
The relationship between the growth temperature (Tgrowth) and the energy of activation (∆Ha) for (A) the Rubisco specificity factor for CO2/O2 (Sc/o) in liquid phase, (B) the Rubisco Michaelis–Menten constant for CO2 (Kc) in liquid phase, and (C) the Rubisco maximum carboxylase turnover rate (kcatc). Each symbol corresponds to individual species (Table 2 for data sources). Open upward triangles, Proteobacteria; open circles, Cyanobacteria; black circles, Bacillariophyta (diatoms); open squares, Chlorophyta (green algae); open diamond, Rhodophyta (red algae); blue squares, C3 plants from cool habitats; red squares, C3 plants from warm habitats; green squares C4 plants. In vitro estimates at discrete temperatures were standardized for study-to-study differences in physico-chemical characteristics for CO2 and O2 used as in Figs 1 and 2 and the temperature responses were fitted by Eq. 12. In (A), the data were fitted by a non-linear equation in the form y=−20.911+0.207x–0.009x2. In (B) and (C), data fits by linear and different monotonic non-linear equations were statistically not significant (best r2 values were 0.090 for (B) and 0.115 for (C), P>0.1 for both).
Fig. 4.
Fig. 4.
The relationship between the energies of activation (∆Ha) for the Rubisco maximum carboxylase turnover rate (kcatc) and the Rubisco specificity factor for CO2/O2 (Sc/o) in liquid phase across domains of life and photosynthetic and ecological groupings of plants (symbols as in Fig. 3). Data were separately fitted by linear regressions across domains of life (all plants averaged; solid line, r2=0.952, P<0.01) and across all groupings (plant functional and photosynthetic groupings, C3 cool and warm and C4, separately considered; dashed line, r2=0.846, P<0.01). In Rhodophyta, the value of ∆Ha for Sc/o is from Galdieria partita, while that of ∆Ha for kcatc is from Cyanidium caldarium. For the other phylogenetic groups, data correspond to averages±SE from different numbers of species (Table 3 for data sources). Data for Thermosynechococcus elongatus (Cyanobacteria) with vastly different Rubisco kinetics (Figs 1 and 2) were not considered in the regression analysis.
Fig. 5.
Fig. 5.
Values of the Rubisco specificity factor for CO2/O2 (Sc/o) (A) and the Michaelis–Menten constants for CO2 (Kc) (B) and O2 (Ko) (C) at a range of temperatures. Values for these parameters were obtained at discrete temperatures from in vivo gas-phase data (shown in Table 4) after applying Eq. 12 and converted to the liquid phase by Eqs 8–10 (Table 1 for corresponding Henry’s law constants to convert between liquid-phase and gas-phase equivalents). For comparative purposes, in vitro C3 average values for Sc/o and Kc have been also included (using data shown in Table 3). In (C), in vitro Ko data for Atriplex glabriuscula (Badger and Collatz 1977, shown in Table 2) that have been widely used to model leaf photosynthesis (see Introduction) have been also included.
Fig. 6.
Fig. 6.
Comparisons between in vitro (filled symbols) and in vivo (open symbols) values of the Rubisco specificity factor for CO2/O2 (Sc/o) (A, B) and the Michaelis–Menten constants for CO2 (Kc) (C, D) and O2 (Ko) (E) at a range of temperatures for species with available data. Equation 12 was used to derive estimates for these parameters at discrete temperatures from data in Tables 2 and 4. The in vitro liquid-phase data were standardized for a common set of physico-chemical characteristics of CO2 and O2 as explained in Figs 1 and 2, while the in vivo gas-phase data were converted to the liquid phase as explained in Fig. 5 (Table 1 for pertinent Henry’s law constant to convert between liquid- and gas-phase equivalents). Sc/o data for Spinacia oleracea are averages for the studies Jordan and Ogren (1984), Uemura et al. (1997), Zhu et al. (1998) and Yamori et al. (2006). Sc/o data for Triticum aestivum are averages for studies Haslam et al. (2005) and Hermida-Carrera et al. (2016).
Fig. 7.
Fig. 7.
Modeling effect of the different temperature responses of Rubisco kinetic parameters from C3 plants from cool habitats (open downward triangles), C3 plants from warm habitats (open upward triangles) and C3 average (open circles) on the Rubisco-limited gross assimilation rate (ARubisco) at chloroplastic CO2 concentrations (Cc) of 120, 200 and 400 μmol mol−1. To model ARubisco at different temperatures, the values for the temperature dependence parameters of Sc/o, Kc and kcatc were taken from Table 3 (see Methods for further details). We simulated gross assimilation here to avoid confounding effects of mitochondrial respiration.
Fig. 8.
Fig. 8.
Comparison of the Rubisco-limited gross photosynthesis (ARubisco) among average of in vitro data reported for C3 plants and three widely cited datasets at chloroplastic CO2 concentrations (Cc) of 120, 200 and 400 μmol mol−1. The temperature dependence parameters of Sc/o, Kc, kcatc and Ko for in vitro average C3 plants (shown in Table 3) were the same as in Fig. 7, while those for in vivo Nicotiana tabacum (Bernacchi et al., 2001; Walker et al., 2013) and in vitro Spinacia oleracea (Jordan and Ogren, 1984) were obtained from the original papers (shown in Tables 2 and 4). Bernacchi et al. (2001), Walker et al. (2013) and Jordan and Ogren (1984) did not report values of the deactivation energy (∆Hd) and the entropy term (∆S) for kcatc, and the simulation assumed identical values to those used for the in vitro average C3 plants (indicated in the Methods). Note that Bernacchi et al. (2001) in vivo values have been derived without considering mesophyll conductance, while mesophyll conductance has been included in the in vivo estimates of Walker et al. (2013).
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