Temperature response of bundle-sheath conductance in maize leaves

Abstract

A small bundle-sheath conductance (g bs) is essential for the C4 CO2-concentrating mechanism to suppress photorespiration effectively. To predict the productivity of C4 crops accurately under global warming, it is necessary to examine whether and how g bs responds to temperature. We investigated the temperature response of g bs in maize by fitting a C4 photosynthesis model to combined gas exchange and chlorophyll fluorescence measurements of irradiance and CO2 response curves at 21% and 2% O2 within the range of 13.5-39 °C. The analysis was based on reported kinetic constants of C4 Rubisco and phosphoenolpyruvate carboxylase and temperature responses of C3 mesophyll conductance (g m). The estimates of g bs varied greatly with leaf temperature. The temperature response of g bs was well described by the peaked Arrhenius equation, with the optimum temperature being ~34 °C. The assumed temperature responses of g m had only a slight impact on the temperature response of g bs In contrast, using extreme values of some enzyme kinetic constants changed the shape of the response, from the peaked optimum response to the non-peaked Arrhenius pattern. Further studies are needed to confirm such an Arrhenius response pattern from independent measurement techniques and to assess whether it is common across C4 species.

Keywords: Diffusive resistance; Zea mays.; maximum PEPc activity; maximum Rubisco activity; modelling; warming effect.

Fig. 1.

Net CO₂ assimilation rate A at six leaf temperatures in response to incident irradiance or to intercellular CO₂ levels under 21% (left panels) or 2% (right panels) O₂ conditions. Each symbol represents the mean of four replicated leaves (SEMs are visible in bars if larger than the symbols).(This figure is available in colour at JXB online.)

Fig. 2.

Apparent operating quantum efficiency of photosystem II (PSII) electron transport (Φ₂ or ∆F/F _m′) at six leaf temperatures in response to incident irradiance or to intercellular CO₂ levels under 21% (left panels) or 2% (right panels) O₂ conditions. Each symbol represents the mean of four replicated leaves (SEMs are visible if larger than the symbols). (This figure is available in colour at JXB online.)

Fig. 3.

The relationship between net CO₂ assimilation rate A and the lumped variable I _incΦ₂/3 (mean of four replicates) from irradiance response curves under non-photorespiratory conditions (i.e. at 2% O₂ combined with high CO₂) at six leaf temperatures. Open circles are for I _inc ≤500 μmol m⁻² s⁻¹ and filled triangles come from the three levels of I _inc >500 μmol m⁻² s⁻¹. The lines represent linear regression based on data with I _inc ≤500 μmol m⁻² s⁻¹, in which the slope gives the estimate of calibration factor s′ and the intercept gives the estimate of day respiration R _d (see the text).

Fig. 4.

(a) Temperature response of the estimated calibration factor s′, and (b) temperature response of the estimated day respiration R _d. Values of s′ and R _d were estimated as the slope and the intercept, respectively, of linear regression in Fig. 3. In (b), the curve represents the Arrhenius plot of Equation 3 with estimated parameter values in Table 2. Bars in (a) and (b) represent SEs of the estimates.

Fig. 5.

Temperature response of the initial slope of the A–C _i curve at 2% O₂. The error bar of each point indicates ±SEM of four replicated leaves. The error bar of the last point is smaller than the symbol.

Fig. 6.

Temperature response of estimated bundle-sheath conductance g _bs in maize leaves. The error bar at each point represents ±SE of the estimate. The curve represents the peaked Arrhenius fit of Equation 4 with estimated values of the parameters in Table 2.

Fig. 7.

Sensitivity of bundle-sheath conductance, g _bs, temperature response to changes in 12 input parameters as shown in (a–l). The input parameters and their default values are defined in Table 1. The changes were made to be 0.50 (open squares), 0.75 (open triangles), 1.25 (open circles), and 1.50 (open diamonds) times their default value. The temperature response of g _bs using the default set of input parameter values is given by the solid curve of each panel. One or two types of symbols are missing in (j) and (k) because extreme values of either D _Vpmax or S _Vpmax resulted in a biologically unrealistic negative estimate of g _bs. (This figure is available in colour at JXB online.)

Fig. 8.

Calculated CO₂ leakiness ϕ as a function of irradiance (a) and of intercellular CO₂ level (b) at six temperatures. The values of leakiness ϕ from (a) for three contrasting irradiance levels of 100, 500, and 2000 μmol m⁻² s⁻¹ (open symbols) and the mean ϕ (SEM in bars) across all CO₂ levels from (b) (filled circles) are shown as a function of temperature (c). The O₂ level was at 21%.(This figure is available in colour at JXB online.)

Fig. 9

Calculated V _o:V _c ratios (a, b) and V _c:V _p ratios (c, d) as a function of irradiance (a, c) and of intercellular CO₂ level (b, d) at six temperatures. The mean ratios (SEM in bars if larger than symbols) across all irradiance levels and across CO₂ levels with C _a ≥200 μmol mol⁻¹ against temperature during measurements are shown in the inset of each panel. The O₂ level was 21%.(This figure is available in colour at JXB online.)