Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate Carboxylase/Oxygenase

Abstract

Increasing the leaf temperature of intact cotton (Gossypium hirsutum L.) and wheat (Triticum aestivum L.) plants caused a progressive decline in the light-saturated CO2-exchange rate (CER). CER was more sensitive to increased leaf temperature in wheat than in cotton, and both species demonstrated photosynthetic acclimation when leaf temperature was increased gradually. Inhibition of CER was not a consequence of stomatal closure, as indicated by a positive relationship between leaf temperature and transpiration. The activation state of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), which is regulated by Rubisco activase, was closely correlated with temperature-induced changes in CER. Nonphotochemical chlorophyll fluorescence quenching increased with leaf temperature in a manner consistent with inhibited CER and Rubisco activation. Both nonphotochemical fluorescence quenching and Rubisco activation were more sensitive to heat stress than the maximum quantum yield of photochemistry of photosystem II. Heat stress led to decreased 3-phosphoglyceric acid content and increased ribulose-1, 5-bisphosphate content, which is indicative of inhibited metabolite flow through Rubisco. We conclude that heat stress inhibited CER primarily by decreasing the activation state of Rubisco via inhibition of Rubisco activase. Although Rubisco activation was more closely correlated with CER than the maximum quantum yield of photochemistry of photosystem II, both processes could be acclimated to heat stress by gradually increasing the leaf temperature.

Figure 1

The effect of rapid and gradual increases in leaf temperature on CER of cotton and wheat leaves. Values are reported relative to the CER of the control, which was set at 100%. Each point is the mean ± se of two independent experiments in which three measurements were made for each temperature treatment. CER for the controls averaged 32.3 ± 1.8 and 26.2 ± 1.9 μmol CO₂ m⁻² s⁻¹ for cotton and wheat, respectively.

Figure 2

The effect of gradual increases in leaf temperature on the transpiration rate of cotton and wheat leaves. Each point is the mean ± se of two independent experiments in which three measurements were made for each temperature treatment.

Figure 3

The effect of rapid and gradual increases in leaf temperature on initial Rubisco activity. Values are reported relative to the initial Rubisco activity of the control, which was set at 100%. Each point is the mean ± se of two independent experiments in which three measurements were made for each temperature treatment. Initial Rubisco activity of the controls averaged 0.452 ± 0.016 and 0.433 ± 0.018 μmol CO₂ g⁻¹ fresh weight s⁻¹ for cotton and wheat, respectively.

Figure 4

Correlation between initial Rubisco activity and CER of cotton and wheat leaves. Data points are from Figures 1 and 3. ○, Rapid heat stress; •, gradual heat stress.

Figure 5

The effect of rapid and gradual increases in leaf temperature on steady-state qN of cotton and wheat leaves. Values are reported relative to the qN of the control, which was set at 100%. Each point is the mean ± se of two independent experiments in which three measurements were made for each temperature treatment. Steady-state qN values for control cotton and wheat leaves averaged 0.330 ± 0.028 and 0.322 ± 0.030, respectively. The insets represent the correlation between CER (from data in Fig. 1) and steady-state qN. ○, Rapid heat stress; •, gradual heat stress.

Figure 6

The effect of rapid and gradual increases in leaf temperature on F_v/F_m of cotton and wheat leaves. Values are reported relative to the F_v/F_m of the control, which was set at 100%. Each point is the mean ± se of two independent experiments in which three measurements were made for each temperature treatment. F_v/F_m for control cotton and wheat leaves averaged 0.769 ± 0.073 and 0.766 ± 0.063, respectively.

Figure 7

The effect of rapid increases in leaf temperature on the relaxation kinetics of qN of a cotton and a wheat leaf. Relaxation kinetics were analyzed immediately after quenching analysis, during which steady-state qN had developed in the light. Experiments were conducted first at the control temperatures of 28°C and 25°C for cotton and wheat, respectively, and then again after the leaf temperature was rapidly increased to 40°C and 35°C for cotton and wheat, respectively. The data reported were obtained from one representative leaf.

Figure 8

The effect of rapid increases in leaf temperature on the levels of PGA and RuBP in leaves of cotton and wheat. Each point is the mean ± se of two independent experiments in which three leaves were analyzed for each experiment.