Photosynthetic acclimation under CO2 fertilization: new perspectives from current experiments

Photosynthetic acclimation under CO₂ fertilization is still incompletely understood. Observed reductions in the maximum rate of carboxylation (V_cmax) and electron transport (J_max) under elevated CO₂ (often called ‘down-regulation’) have been explained in various ways, including limited soil nitrogen (N) and phosphorus (P) availability, or a reduced demand for N. However, there remains large variation of the V_cmax decline and some non-sensitive or even positive responses are documented. The least cost hypothesis (Prentice et al., 2014) states that optimal photosynthesis is achieved at balanced unit costs of capacities of carboxylation and transpiration and predicts the acclimation of V_cmax and J_max in response to the environment. Under elevated CO₂, V_cmax is predicted to decline, while the ratio J_max/V_cmax is predicted to increase - independent of N supply from the soil. In contrast, common model parametrisations conceive V_cmax to be controlled by soil N supply.

Here, we analyse a compilation of experimental results in an attempt to better understand photosynthetic acclimation to elevated CO₂ and balance the evidence for contrasting model formulations. Within 38 CO₂ fertilization plots investigated at forest, grassland and cropland,  V_cmax and J_max are shown to decrease in concert, while the ratio J_max/V_cmax increases with higher CO₂ concentration, consistent with predictions from the least cost hypothesis. However, the predicted increase in the J_max/V_cmax ratio is too large and the observed change in V_cmax is correlated with the change in soil inorganic N. Observed leaf N responses are broadly consistent with changes in V_cmax and J_max. These findings support the idea acclimation of photosynthetic traits under enhanced CO₂ is modulated by soil N supply. This can be explained by the direct decline of soil N availability at higher CO₂ concentrations. However, it may also be caused by increase rates of net primary production (NPP) and N uptake that increase N sequestered in biomass under elevated CO₂, in such a way to constrain labile soil N available for leaf-level photosynthesis.

V_cmax and J_max responses to CO₂ were also found to be negatively related to increases of above- and below-ground net primary production (ANPP, BNPP). This pattern might be explained by a ‘dilution effect’, due to a CO₂-induced increase of leaf area index (LAI). However, it might also be due to plants having different stomatal responses to CO₂. According to this hypothesis, at one end of the spectrum, the ratio of leaf intercellular CO₂ (C_i) relative to ambient CO₂ (C_a) remains constant; optimal photosynthesis increases, while optimal V_cmax declines. At the other end of the spectrum, C_i/C_a  decreases enough that C_i remains constant; then there is no increase in optimal photosynthesis, and no change in optimal V_cmax. Testing this hypothesis would require concomitant measurements of all of the relevant quantities (LAI, NPP, C_i/C_a) in multiple experiments.