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. 2012 Oct;13(10):811-23.
doi: 10.1631/jzus.B1200130.

Hydrogen peroxide functions as a secondary messenger for brassinosteroids-induced CO2 assimilation and carbohydrate metabolism in Cucumis sativus

Yu-ping Jiang  1 , Fei Cheng, Yan-hong Zhou, Xiao-jian Xia, Wei-hua Mao, Kai Shi, Zhi-xiang Chen, Jing-quan Yu
Affiliations

Hydrogen peroxide functions as a secondary messenger for brassinosteroids-induced CO2 assimilation and carbohydrate metabolism in Cucumis sativus

Yu-ping Jiang et al. J Zhejiang Univ Sci B. 2012 Oct.

Abstract

Brassinosteroids (BRs) are potent regulators of photosynthesis and crop yield in agricultural crops; however, the mechanism by which BRs increase photosynthesis is not fully understood. Here, we show that foliar application of 24-epibrassinolide (EBR) resulted in increases in CO(2) assimilation, hydrogen peroxide (H(2)O(2)) accumulation, and leaf area in cucumber. H(2)O(2) treatment induced increases in CO(2) assimilation whilst inhibition of the H(2)O(2) accumulation by its generation inhibitor or scavenger completely abolished EBR-induced CO(2) assimilation. Increases of light harvesting due to larger leaf areas in EBR- and H(2)O(2)-treated plants were accompanied by increases in the photochemical efficiency of photosystem II (Φ(PSII)) and photochemical quenching coefficient (q(P)). EBR and H(2)O(2) both activated carboxylation efficiency of ribulose-1,5-bisphosphate oxygenase/carboxylase (Rubisco) from analysis of CO(2) response curve and in vitro measurement of Rubisco activities. Moreover, EBR and H(2)O(2) increased contents of total soluble sugar, sucrose, hexose, and starch, followed by enhanced activities of sugar metabolism such as sucrose phosphate synthase, sucrose synthase, and invertase. Interestingly, expression of transcripts of enzymes involved in starch and sugar utilization were inhibited by EBR and H(2)O(2). However, the effects of EBR on carbohydrate metabolisms were reversed by the H(2)O(2) generation inhibitor diphenyleneodonium (DPI) or scavenger dimethylthiourea (DMTU) pretreatment. All of these results indicate that H(2)O(2) functions as a secondary messenger for EBR-induced CO(2) assimilation and carbohydrate metabolism in cucumber plants. Our study confirms that H(2)O(2) mediates the regulation of photosynthesis by BRs and suggests that EBR and H(2)O(2) regulate Calvin cycle and sugar metabolism via redox signaling and thus increase the photosynthetic potential and yield of crops.

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Figures

Fig. 1
Fig. 1
Time course responses of A sat and content of H2O2 to EBR Four-week-old cucumber plants were treated with distilled water or EBR at 0.1 μmol/L at 9 am. CO2 assimilation rate at saturated light (A sat) was determined at 1 000 μmol/(m2·s) light intensity and 25 °C. Measurements were taken at 1, 2, 3, 6, 9, 24, and 72 h after EBR treatment. Data are expressed as mean±standard deviation (SD) (n=4). FW: fresh weight
Fig. 2
Fig. 2
Changes in maximum carboxylation rate of Rubisco (V c,max) (a), maximum RuBP regeneration rates (J max) (b), stomatal limitation (l) (c), photochemical efficiency of photosystem II (ΦPSII) (d), photochemical quenching coefficient (q P) (e), and the efficiency of excitation capture by open PSII centers (Fv′/Fm′) (f) for control, EBR-treated, and H2O2-treated plants Measurements were taken at 1, 2, 3, 6, 9, 24, and 72 h after treatment with 0.1 μmol/L EBR or 5 mmol/L H2O2, respectively. Data are expressed as mean±SD (n=4)
Fig. 3
Fig. 3
Effects of EBR and H2O2 and pretreatments with DPI and DMTU on the A max of CO2 A max was determined at saturating PPFD of 1 500 μmol/(m2·s) and CO2 of 2 000 μmol/mol. Measurements were taken at 24 h after treatment with EBR at 0.1 μmol/L or H2O2 at 5 mmol/L, respectively. DPI at 100 μmol/L and DMTU at 5 mmol/L were used, respectively. Values are expressed as mean±SD (n=4). Means denoted with different letters showed statistically significant difference (P<0.05) according to Tukey’s test
Fig. 4
Fig. 4
Effects of EBR and H2O2 and pretreatments with DPI and DMTU on transcripts of BAM (β-amylolytic enzyme), SUS (sucrose synthase), invertase, and UGDH (UDP-glucose 6-dehydrogenase) in cucumber leaves Leaf samples were taken at 24 h after treatment with EBR at 0.1 μmol/L or H2O2 at 5 mmol/L, respectively. DPI at 100 μmol/L and DMTU at 5 mmol/L were used respectively. Data are expressed as mean±SD (n=4). Means denoted with different letters showed statistically significant difference (P<0.05) according to Tukey’s test
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