Rubisco and Rubisco Activase Play an Important Role in the Biochemical Limitations of Photosynthesis in Rice, Wheat, and Maize under High Temperature and Water Deficit

Abstract

To understand the effect of heat and drought on three major cereal crops, the physiological and biochemical (i.e., metabolic) factors affecting photosynthesis were examined in rice, wheat, and maize plants grown under long-term water deficit (WD), high temperature (HT) and the combination of both stresses (HT-WD). Diffusional limitations to photosynthesis prevailed under WD for the C₃ species, rice and wheat. Conversely, biochemical limitations prevailed under WD for the C₄ species, maize, under HT for all three species, and under HT-WD in rice and maize. These biochemical limitations to photosynthesis were associated with Rubisco activity that was highly impaired at HT and under HT-WD in the three species. Decreases in Rubisco activation were unrelated to the amount of Rubisco and Rubisco activase (Rca), but were probably caused by inhibition of Rca activity, as suggested by the mutual decrease and positive correlation between Rubisco activation state and the rate of electron transport. Decreased Rubisco activation at HT was associated with biochemical limitation of net CO₂ assimilation rate (A_N). Overall, the results highlight the importance of Rubisco as a target for improving the photosynthetic performance of these C₃ (wheat and rice) and C₄ (maize) cereal crops under increasingly variable and warmer climates.

Keywords: Rubisco; Rubisco activase; crops; photosynthesis; temperature; water deficit.

FIGURE 1

The diffusive (D_L) and biochemical limitations (B_L) to CO₂ assimilation in rice (A), wheat (B), and maize (C) plants grown under water deficit (WD), high temperature (HT) and a combination of HT and water deficit (HT-WD). Values represent means ± SE (n = 4–5). Different letters denote statistically significant differences by Duncan analysis (P < 0.05) between types of limitation within each species and treatment.

FIGURE 2

The relationship between the Rubisco activation state and the net CO₂ assimilation rate (A_N) in well-watered plants of rice (A), wheat (B), and maize (C) grown at 25°C (control) or 38°C (HT) and measured at 25°C. Each symbol corresponds to one independent sample.

FIGURE 3

Rubisco amount (A), initial (B) and total (C) activities at 25°C measured in plants of rice, wheat, and maize grown at control, WD, HT and a combination of HT and water deficit (HT-WD) conditions. To unify scales among the different species, values are means ± SE (n = 4–5) of each parameter expressed relative to control plants. Different letters denote statistically significant differences by Duncan analysis (P < 0.05) among treatments within each species. The control values for rice, wheat, and maize of Rubisco amount were, respectively, 0.49 ± 0.03, 0.34 ± 0.04, 0.15 ± 0.05 mg Rubisco mg^-1 TSP; Rubisco initial activity 0.31 ± 0.02, 0.19 ± 0.04, 0.08 ± 0.01 μmol CO₂ mg^-1 TSP min^-1; and Rubisco total activity 0.36 ± 0.01, 0.44 ± 0.05, 0.13 ± 0.02 μmol CO₂ mg^-1 TSP min^-1.

FIGURE 4

Total Rubisco activase (Rca) amount (A), Rca large isoform amount (B) and Rca small isoform amount (C) in plants of rice, wheat, and maize grown at control, WD, HT and a combination of HT and water deficit (HT-WD) conditions. Values represent means ± SE (n = 4) of amounts expressed relative to control plants. Different letters denote statistically significant differences by Duncan analysis (P < 0.05) among treatments within each species.

FIGURE 5

Rubisco activation state in relation to the ratio of Rubisco activase (Rca) to Rubisco amounts (Rca/Rubisco; A,C,E), the CO₂ concentration in the mesophyll chloroplasts (C_c; B,D) or the bundle sheath (C_s; F) in rice (A,B), wheat (C,D), and maize (E,F). Values represent means ± SE (n = 4–5).

FIGURE 6

The relationship between the CO₂ concentration in the mesophyll chloroplasts (C_c) in rice (A) and wheat (B) and the CO₂ concentration in the bundle sheath chloroplasts (C_s) in maize (C) and the ratio of Rubisco activase (Rca) to Rubisco amounts (Rca/Rubisco). Values represent means ± SE (n = 4–5).

FIGURE 7

The relationship between the Rubisco activation state and the electron transport rate (J) in rice (A), wheat (B), and maize (C).