Nitric Oxide Enhances Photosynthetic Nitrogen and Sulfur-Use Efficiency and Activity of Ascorbate-Glutathione Cycle to Reduce High Temperature Stress-Induced Oxidative Stress in Rice (Oryza sativa L.) Plants

Abstract

The effects of nitric oxide (NO) as 100 µM sodium nitroprusside (SNP, NO donor) on photosynthetic-nitrogen use efficiency (NUE), photosynthetic-sulfur use efficiency (SUE), photosynthesis, growth and agronomic traits of rice (Oryza sativa L.) cultivars, Taipie-309 (high photosynthetic-N and SUE) and Rasi (low photosynthetic-N and SUE) were investigated under high temperature stress (40 °C for 6 h). Plants exposed to high temperature stress caused significant reduction in photosynthetic activity, use efficiency of N and S, and increment in H₂O₂ and thiobarbituric acid reactive substance (TBARS) content. The drastic effects of high temperature stress were more pronounced in cultivar Rasi than Taipie-309. However, foliar spray of SNP decreased the high temperature induced H₂O₂ and TBARS content and increased accumulation of proline and activity of ascorbate-glutathione cycle that collectively improved tolerance to high temperature stress more effectively in Taipie-309. Exogenously applied SNP alleviated the high temperature induced decrease in photosynthesis through maintaining higher photosynthetic-NUE and photosynthetic-SUE, activity of ribulose 1,5 bisphosphate carboxylase/oxygenase (Rubisco), and synthesis of reduced glutathione (GSH). The use of 2-4-carboxyphenyl-4,4,5,5-tetramethylimidazoline-1-oxy-3-oxide (cPTIO, NO scavenger) substantiated the study that in the absence of NO oxidative stress increased, while NO increased photosynthetic-NUE and photosynthetic-SUE, net photosynthesis and plant dry mass. Taken together, the present investigation reveals that NO increased heat stress tolerance and minimized high temperature stress adversaries more effectively in cultivar Taipie-309 than Rasi by enhancing photosynthetic-NUE and SUE and strengthening the antioxidant defense system.

Keywords: Oryza sativa; antioxidants; reactive oxygen species; sodium nitroprusside; stomata.

Figure 1

Leaf H₂O₂ content (A), TBARS content (B), Proline content (C), and NO generation (D) in Taipie-309 and Rasi cultivars of rice (Oryza sativa L.) at 30 days after germination (DAG), plants were grown with/without high temperature stress and treated with foliar 100 µM SNP (NO donor). Data are presented as treatments mean ± SE (n = 4). The values followed by same letters above bars represent that data did not differ significantly by LSD test at p < 0.05. FW, fresh weight; DW, dry weight.

Figure 2

Ascorbate peroxidase (APX, A), glutathione reductase (GR, B), and superoxide dismutase (SOD, C) activities in Taipie-309 and Rasi cultivars of rice (Oryza sativa L.) at 30 days after germination (DAG), plants were grown with/without high temperature stress and treated with foliar 100 µM SNP (NO donor). Data are presented as treatments mean ± SE (n = 4). The values followed by same letters above bars represent that data did not differ significantly by LSD test at p < 0.05.

Figure 3

Net photosynthesis (A), stomatal conductance (B), intercellular CO₂ concentration (C), and chlorophyll content (SPAD value) (D) in Taipie-309 and Rasi cultivars of rice (Oryza sativa L.) at 30 days after germination (DAG), plants were grown with/without high temperature stress and treated with foliar 100 µM SNP (NO donor). Data are presented as treatments mean ± SE (n = 4). The values followed by same letters above bars represent that data did not differ significantly by LSD test at p < 0.05.

Figure 4

Maximal PSII photochemical efficiency (A), Rubisco activity (B), leaf area (C), and plant dry mass (D) in Taipie-309 and Rasi cultivars of rice (Oryza sativa L.) at 30 days after germination (DAG), plants were grown with/without high temperature stress and treated with foliar 100 µM SNP (NO donor). Data are presented as treatments mean ± SE (n = 4). The values followed by same letters above bars represent that data did not differ significantly by LSD test at p < 0.05.

Figure 5

Leaf nitrogen content (A), NR activity (B), and photosynthetic NUE (C) in Taipie-309 and Rasi cultivars of rice (Oryza sativa L.) at 30 days after germination (DAG), plants were grown with/without high temperature stress and treated with foliar 100 µM SNP (NO donor). Data are presented as treatments mean ± SE (n = 4). The values followed by same letters above bars represent that data did not differ significantly by LSD test at p < 0.05. DW, dry weight; FW, fresh weight; NUE, nitrogen use efficiency.

Figure 6

Leaf sulfur content (A), photosynthetic SUE (B), GSH content (C), and Cys content (D) in Taipie-309 and Rasi cultivars of rice (Oryza sativa L.) at 30 days after germination (DAG), plants were grown with/without high temperature stress and treated with foliar 100 µM SNP (NO donor). Data are presented as treatments mean ± SE (n = 4). The values followed by same letters above bars represent that data did not differ significantly by LSD test at p < 0.05. DW, dry weight; FW, fresh weight; SUE, sulfur use efficiency.

Figure 7

Stomatal frequency (A), stomatal aperture length (B), and width (C) in Taipie-309 and Rasi cultivars of rice (Oryza sativa L.) at 30 days after germination (DAG), plants were grown with/without high temperature stress and treated with foliar 100 µM SNP (NO donor). Data are presented as treatments mean ± SE (n = 4). The values followed by same letters above bars represent that data did not differ significantly by LSD test at p < 0.05.