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Sensitivity of photosynthesis in a C4 plant, maize, to heat stress - PubMed

Sensitivity of photosynthesis in a C4 plant, maize, to heat stress

Steven J Crafts-Brandner et al. Plant Physiol. 2002 Aug.

Abstract

Our objective was to determine the sensitivity of components of the photosynthetic apparatus of maize (Zea mays), a C4 plant, to high temperature stress. Net photosynthesis (Pn) was inhibited at leaf temperatures above 38 degrees C, and the inhibition was much more severe when the temperature was increased rapidly rather than gradually. Transpiration rate increased progressively with leaf temperature, indicating that inhibition was not associated with stomatal closure. Nonphotochemical fluorescence quenching (qN) increased at leaf temperatures above 30 degrees C, indicating increased thylakoid energization even at temperatures that did not inhibit Pn. Compared with CO(2) assimilation, the maximum quantum yield of photosystem II (F(v)/F(m)) was relatively insensitive to leaf temperatures up to 45 degrees C. The activation state of phosphoenolpyruvate carboxylase decreased marginally at leaf temperatures above 40 degrees C, and the activity of pyruvate phosphate dikinase was insensitive to temperature up to 45 degrees C. The activation state of Rubisco decreased at temperatures exceeding 32.5 degrees C, with nearly complete inactivation at 45 degrees C. Levels of 3-phosphoglyceric acid and ribulose-1,5-bisphosphate decreased and increased, respectively, as leaf temperature increased, consistent with the decrease in Rubisco activation. When leaf temperature was increased gradually, Rubisco activation acclimated in a similar manner as Pn, and acclimation was associated with the expression of a new activase polypeptide. Rates of Pn calculated solely from the kinetics of Rubisco were remarkably similar to measured rates if the calculation included adjustment for temperature effects on Rubisco activation. We conclude that inactivation of Rubisco was the primary constraint on the rate of Pn of maize leaves as leaf temperature increased above 30 degrees C.

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Figures

Figure 1
Figure 1

Effect of leaf temperature on Pn and transpiration (inset) of maize leaves. After attaining steady-state net Pn and transpiration at 28°C, leaf temperature was increased rapidly at 1°C min−1 (○) or gradually at 2.5°C h−1 (□). Pn and transpiration were determined after 1 h at the indicated temperature. Different plants were used for each rapid temperature increase treatment, whereas the same leaf was used for the gradual heat stress treatment. Each data point represents the mean ±

se

of three independent measurements.

Figure 2
Figure 2

Effect of leaf temperature on qN of maize leaves. An attached leaf was dark adapted for 1 h at 28°C prior to conducting nonphotochemical quenching analysis. Subsequent measurements were made on the same leaf tissue after increasing the leaf temperature at 1°C min−1 in the dark to 32.5°C for 1 h and then to 37.5°C for 1 h. Each curve represents the mean ±

se

of three independent measurements. At 28°C, qN was the same for plants that were dark adapted for 1 and 3 h (data not shown).

Figure 3
Figure 3

Effect of leaf temperature on the Fv/Fm of maize leaves. Intact leaves were dark adapted for 1 h at 28°C, Fv/Fm was measured, leaf temperature was increased at 1°C min−1 to the indicated temperature, and Fv/Fv was measured again. Different plants were used for each temperature treatment, and the data points represent the mean ±

se

of three independent measurements. The average Fv/Fm for the 28°C treatment was 0.801 ± 0.005.

Figure 4
Figure 4

Effect of leaf temperature on the activation state of Rubisco in maize leaves. Leaves were allowed to attain steady-state Pn (1 h) under high light and ambient CO2 at a given temperature prior to sampling. Leaf temperature was increased rapidly at 1°C min−1 or gradually at 2.5°C h−1, and samples were taken after 1 h at the indicated temperature. Different plants were used for each temperature treatment, and the data points represent the mean ±

se

of three independent measurements.

Figure 5
Figure 5

Western-blot analysis of the effect of heat stress on abundance of Rubisco activase in maize leaves. Controls were treated for two diurnal cycles of 14 h of light at 28°C and 10 h of dark at 24°C, and leaf tissue was sampled at the end of the dark period of the 2nd d (control). Other plants were treated for two diurnal cycles of 14 h of light at 40°C and 10 h of dark at 34°C, and leaf tissue was sampled at the end of the dark period on the 2nd d (48 h heat). In addition, for some plants, the leaf temperature was increased at 2.5°C h−1 in the light until reaching 42.5°C, and after 1.5 h at 42.5°C, leaf tissue was sampled (8 h of heat). Just above the constitutive 42-kD activase polypeptide, the arrow indicates a polypeptide that was immunoreactive to activase antibodies and that contained an N-terminal sequence identical to the constitutive maize activase.

Figure 6
Figure 6

The effect of temperature on the rates of net Pn of maize leaves predicted based on the kinetics of Rubisco. Net Pn at 28°C was assumed to be equal to the maximum activity of Rubisco at 28°C. Net Pn at each temperature was estimated assuming full activation of the enzyme at each temperature (○) or after adjusting the predicted rate for experimentally determined activation state at each temperature (●; from Fig. 4, rapid heat). The adjusted rates of Pn are closely related to the measured rates of Pn for rapid heat stress treatments (see Fig. 1).

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