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Can phenotypic plasticity in Rubisco performance contribute to photosynthetic acclimation?

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Abstract

Photosynthetic acclimation varies among species, which likely reveals variations at the biochemical level in the pathways that constitute carbon assimilation and energy transfer. Local adaptation and phenotypic plasticity affect the environmental response of photosynthesis. Phenotypic plasticity allows for a wide array of responses from a single individual, encouraging fitness in a broad variety of environments. Rubisco catalyses the first enzymatic step of photosynthesis, and is thus central to life on Earth. The enzyme is well conserved, but there is habitat-dependent variation in kinetic parameters, indicating that local adaptation may occur. Here, we review evidence suggesting that land plants can adjust Rubisco’s intrinsic biochemical characteristics during acclimation. We show that this plasticity can theoretically improve CO2 assimilation; the effect is non-trivial, but small relative to other acclimation responses. We conclude by discussing possible mechanisms that could account for biochemical plasticity in land plant Rubisco.

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Acknowledgments

The authors wish to thank two anonymous reviewers for helpful suggestions on a previous version of this manuscript. This work was supported by a National Science and Engineering Research Council of Canada (NSERC) PGS-D scholarship to APC, and a Discovery Grant (327103-2008) to DSK.

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Correspondence to David S. Kubien.

Appendix

Appendix

The modelling in Fig. 1 reflects the acclimation of Rubisco S c/o reported by Yamori et al. (2006b). The ratio of the two reaction efficiencies describes the relative CO2/O2 specificity of Rubisco (S c/o):

$$ S_{{{{\text{c}} \mathord{\left/ {\vphantom {{\text{c}} {\text{o}}}} \right. \kern-0pt} {\text{o}}}}} = \frac{{{{k_{{{\text{cat-CO}}_{ 2} }} } \mathord{\left/ {\vphantom {{k_{{{\text{cat-CO}}_{ 2} }} } {K_{\text{c}} }}} \right. \kern-0pt} {K_{\text{c}} }}}}{{{{k_{{{\text{cat-O}}_{ 2} }} } \mathord{\left/ {\vphantom {{k_{{{\text{cat-O}}_{ 2} }} } {K_{\text{o}} }}} \right. \kern-0pt} {K_{\text{o}} }}}} = \frac{{k_{{{\text{cat-CO}}_{ 2} }} K_{\text{o}}}}{{k_{{{\text{cat-O}}_{ 2} }} K_{\text{c}} }} $$
(1)

where \( k_{{{\text{cat}} - {\text{CO}}_{ 2} }} \) and \( k_{{{\text{cat-O}}_{ 2} }} \) represent the turnover capacity of carboxylation and oxygenation, respectively, and K c and K o are the Michaelis–Menten constants for CO2 and O2. The photorespiratory CO2 compensation point (Γ*) is:

$$ {{\Upgamma}}^{ *} = \frac{{p{\text{O}}_{ 2} }}{{2{\text{S}}_{\text{c/o}} }} $$
(2)

where pO2 is the partial pressure of O2 in the stroma (21 kPa).

We determined the effect of altered spinach S c/o (Yamori et al. 2006b) on Rubisco-limited A:

$$ A = \left( {1 - \Upgamma^{*} /C} \right)V_{c} - R_{\text{d}} = \left( {1 - \Upgamma^{*} /C} \right)\left( {\frac{{V_{{c_{\hbox{max} } }} C}}{{C + K_{\text{c}} \left( {1 + p{\text{O}}_{2} /K_{\text{o}} } \right)}}} \right) - R_{\text{d}} $$
(3)

where C is the level of CO2; V c is the realized rate of carboxylation; \( V_{{c_{\hbox{max} } }} \) is the maximum rate of carboxylation (\( V_{{c_{\hbox{max} } }} \) = \( k_{{{\text{cat}} - {\text{CO}}_{ 2} }} \) * site concentration * activation state); and R d is the rate of non-photorespiratory mitochondrial respiration in the light. We assumed complete Rubisco activation. To incorporate mesophyll conductance, and hence assess A at stromal CO2 (e.g. C c), we followed the solution of Warren and Dreyer (2006, their equation 6).

We used the cubic equation reported by Yamori et al. (Yamori et al. 2006b, their Fig. 4) to calculate S c/o for HT and LT Rubisco, and assigned this to \( k_{{{\text{cat}} - {\text{CO}}_{ 2} }} \), K c, or K o, by re-arranging Equation 1, keeping the other parameters constant. We assumed that \( k_{{{\text{cat - O}}_{ 2} }} \) = \( k_{{{\text{cat}} - {\text{CO}}_{ 2} }} \)/4 (von Caemmerer 2000, p. 45). The 25 °C values and E a (Table 1) were from Jordan and Ogren (1984), and Kubien et al. (2008). Rubisco site concentration was 20 μmol m−2, giving \( V_{{c_{\hbox{max} } }} \) of 64 μmol m−2 s−1 for the default \( k_{{{\text{cat}} - {\text{CO}}_{ 2} }} \). We also calculated the effect of allowing the different S c/o to affect Γ* only, keeping the other parameters constant for HT and LT leaves.

Table 1 Model parameters and activation energies (E a)

We calculated the effect of Rubisco plasticity only, at C i (e.g. infinite mesophyll conductance) and at C c, with R d = 0 (e.g. gross A). We then calculated a more general acclimation potential, assigning HT and LT values for Rubisco content and R d (Yamori et al. 2005, their Table 1 and Fig. 2), and g m (Yamori et al. 2006a, their Fig. 1) (Fig. 2). We left the site concentration for LT leaves at 20 μmol m−2; adjusting for the HT/LT Rubisco ratio reported by Yamori et al. (2005) gives an HT content of 10.3 μmol m−2, and thus a \( V_{{c_{\hbox{max} } }} \) of 33 μmol m−2 s−1 at 25 °C.

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Cavanagh, A.P., Kubien, D.S. Can phenotypic plasticity in Rubisco performance contribute to photosynthetic acclimation?. Photosynth Res 119, 203–214 (2014). https://doi.org/10.1007/s11120-013-9816-3

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