Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo

Abstract

CO(2) transfer conductance from the intercellular airspaces of the leaf into the chloroplast, defined as mesophyll conductance (g(m)), is finite. Therefore, it will limit photosynthesis when CO(2) is not saturating, as in C3 leaves in the present atmosphere. Little is known about the processes that determine the magnitude of g(m). The process dominating g(m) is uncertain, though carbonic anhydrase, aquaporins, and the diffusivity of CO(2) in water have all been suggested. The response of g(m) to temperature (10 degrees C-40 degrees C) in mature leaves of tobacco (Nicotiana tabacum L. cv W38) was determined using measurements of leaf carbon dioxide and water vapor exchange, coupled with modulated chlorophyll fluorescence. These measurements revealed a temperature coefficient (Q(10)) of approximately 2.2 for g(m), suggesting control by a protein-facilitated process because the Q(10) for diffusion of CO(2) in water is about 1.25. Further, g(m) values are maximal at 35 degrees C to 37.5 degrees C, again suggesting a protein-facilitated process, but with a lower energy of deactivation than Rubisco. Using the temperature response of g(m) to calculate CO(2) at Rubisco, the kinetic parameters of Rubisco were calculated in vivo from 10 degrees C to 40 degrees C. Using these parameters, we determined the limitation imposed on photosynthesis by g(m). Despite an exponential rise with temperature, g(m) does not keep pace with increased capacity for CO(2) uptake at the site of Rubisco. The fraction of the total limitations to CO(2) uptake within the leaf attributable to g(m) rose from 0.10 at 10 degrees C to 0.22 at 40 degrees C. This shows that transfer of CO(2) from the intercellular air space to Rubisco is a very substantial limitation on photosynthesis, especially at high temperature.

Figure 1

Temperature response of g_m normalized to unity for measurements made by the variable J method at 25°C, determined from simultaneous measurements of gas exchange and chlorophyll fluorescence. g_m was estimated using both the constant J (g_m at 25°C = 0.1075 mol m⁻² s⁻¹ bar⁻¹; white symbols) and variable J methods (g_m at 25°C = 0.095 mol m⁻² s⁻¹ bar⁻¹; black symbols). The continuous line represents the function: fitted to all the illustrated points. Each point is the mean of at least three replicate plants (±1 se).

Figure 2

a, Temperature response of Γ* measured using mass spectrophotometry at the CO₂ compensation point when chloroplast CO₂ concentration (C_c) is equal to intercellular CO₂ concentration (C_i). Values represent the mean of two to nine individual leaves (±1 se of the population mean). b and c, K_c and K_o as a function of temperature and calculated as apparent values based on C_i (solid lines) and actual values based on C_c (broken lines). Points represent K_c and K_o determined previously and independently using similar methods but for a single temperature, 25°C, from von Caemmerer et al. (1994).

Figure 3

Temperature response of the limitation imposed upon photosynthesis by g_m: where A_cc and A_ci are values of A estimated graphically using the actual g_m and infinite g_m, respectively.