Zinc regulation of chlorophyll fluorescence and carbohydrate metabolism in saline-sodic stressed rice seedlings

Abstract

Saline-sodic stress can limit the absorption of available zinc in rice, subsequently impacting the normal photosynthesis and carbohydrate metabolism of rice plants. To investigate the impact of exogenous zinc application on photosynthesis and carbohydrate metabolism in rice grown in saline-sodic soil, this study simulated saline-sodic stress conditions using two rice varieties, 'Changbai 9' and 'Tonghe 899', as experimental materials. Rice seedlings at 4 weeks of age underwent various treatments including control (CT), 2 μmol·L^-1 zinc treatment alone (Z), 50 mmol·L^-1 saline-sodic treatment (S), and 50 mmol·L^-1 saline-sodic treatment with 2 μmol·L^-1 zinc (Z + S). We utilized JIP-test to analyze the variations in excitation fluorescence and MR820 signal in rice leaves resulting from zinc supplementation under saline-sodic stress, and examined the impact of zinc supplementation on carbohydrate metabolism in both rice leaves and roots under saline-sodic stress. Research shows that zinc increased the chloroplast pigment content, specific energy flow, quantum yield, and performance of active PSII reaction centers (PI_ABS), as well as the oxidation (V_OX) and reduction rate (V_red) of PSI in rice leaves under saline-sodic stress. Additionally, it decreased the relative variable fluorescence (W_K and V_J) and quantum energy dissipation yield (φ_DO) of the rice. Meanwhile, zinc application can reduce the content of soluble sugars and starch in rice leaves and increasing the starch content in the roots. Therefore, the addition of zinc promotes electron and energy transfer in the rice photosystem under saline-sodic stress. It enhances rice carbohydrate metabolism, improving the rice plants' ability to withstand saline-sodic stress and ultimately promoting rice growth and development.

Keywords: Carbohydrate metabolism; Chlorophyll fluorescence; Rice; Saline-sodic stress; Zinc.

Fig. 1

Effect of zinc on dry weight of leaves (A) and roots (B) and relative water content of leaves (C) of rice seedlings under saline-sodic stress. Different letters represent the significant differences between treatments at p ≤ 0.05. Values are mean ± SE (n = 3). CT: no saline-sodic and no zinc treatment; Z: zinc treatment; S: saline-sodic treatment; Z + S: saline-sodic and zinc treatment. CB: Changbai 9; TH: Tonghe 899

Fig. 2

Effect of zinc on chlorophyll a (A), chlorophyll b (B), and carotenoid (C) contents, as well as on the net photosynthetic rate (D), intercellular carbon dioxide concentration (E), and stomatal conductance (F) of rice leaves under conditions of saline-sodic stress. Different letters represent the significant differences between treatments at p ≤ 0.05. Values are mean ± SE (n = 3). CT: no saline-sodic and no zinc treatment; Z: zinc treatment; S: saline-sodic treatment; Z + S: saline-sodic and zinc treatment. CB: Changbai 9; TH: Tonghe 899

Fig. 3

Effect of zinc on the V_t (A, D), O-J (B, E), and O-I (C, F) phases of variable chlorophyll a fluorescence in two rice varieties 'Changbai 9' (A, B, C) and 'Tonghe 899' (D, E, F) under saline-sodic stress. Values are mean ± SE (n = 9). CT: no saline-sodic and no zinc treatment; Z: zinc treatment; S: saline-sodic treatment; Z + S: saline-sodic and zinc treatment

Fig. 4

Effects of zinc on quantum yield and specific energy flux of PSII reaction center of two rice varieties 'Changbai 9' (A) and 'Tonghe 899' (B), and energy conservation performance index (C, D) of PSII in two rice varieties (Changbai 9, Tonghe 899) under saline-sodic stress. Fig. E presents the correlation analysis of PI_ABS, V_J, W_K, φ_Do, φ_Po, ψ_Eo, φ_Eo, φ_Ro, δ_Ro, ABS/RC, DI₀/RC and TR₀/RC. * indicates significant correlation at P < 0.05, ** indicates significant correlation at P < 0.01. φ_Po, maximum quantum yield for primary photochemistry; ψ_Eo, probability that an electron moves further than Q_A; φ_Eo, quantum yield for electron transport (ET); φ_Do, quantum yield (at t = 0) of energy dissipation; φ_Do, quantum yield (at t = 0) of energy dissipation; φ_Ro, quantum yield for reduction of the end electron acceptors at the PSI acceptor side (RE); δ_Ro, probability that an electron is transported from the reduced intersystem electron acceptors to the final electron acceptors of PSI (RE); ABS/RC, Absorbed photon flux per active PSII; TR₀/RC, Trapped energy flux per active PSII; DI₀/RC, Dissipated energy (as heat and fluorescence) flux per active PSII; ET₀/RC, Electron flux from Q_A^‒ to the PQ pool per active PSII; RE₀/RC, Electron flux from Q_A^‒ to the final electron acceptors of PSI per active PSII. Values are mean ± SE (n = 9). CT: no saline-sodic and no zinc treatment; Z: zinc treatment; S: saline-sodic treatment; Z + S: saline-sodic and zinc treatment

Fig. 5

Normalized modulated 820 nm reflectance kinetics (MR₀ = MR_0.7 ms) of zinc on 'Changbai 9' rice variety(A, B) and 'Tonghe 899' rice variety(D, E) under saline-sodic stress. (B, E) the amplitudes of the fast phase (ΔMR_fast/MR₀) and the slow phase (ΔMR_slow/MR₀). (C, F) Vox, the slope of the fast descending phase (MR₀ to MR_min) and Vred, the slope of the slow ascending phase (MR_min to MR_max). Values are mean ± SE (n = 9). CT: no saline-sodic and no zinc treatment; Z: zinc treatment; S: saline-sodic treatment; Z + S: saline-sodic and zinc treatment. CB: Changbai 9; TH: Tonghe 899

Fig. 6

Effects of zinc on sucrose (A, D), fructose (B, E) and starch contents (C, F) and ratio of sucrose to starch contents (c, f) in rice leaves (A, B, C, c) and roots (D, E, F, f) under saline-sodic stress. Different letters represent the significant differences between treatments at p ≤ 0.05. Values are mean ± SE (n = 3). CT: no saline-sodic and no zinc treatment; Z: zinc treatment; S: saline-sodic treatment; Z + S: saline-sodic and zinc treatment. CB: Changbai 9; TH: Tonghe 899

Fig. 7

Effect of zinc on carbohydrate metabolism enzyme activity of rice leaves (A) and roots (B) under saline-sodic stress. Different letters represent the significant differences between treatments at p ≤ 0.05. Values are mean ± SE (n = 3). CT: no saline-sodic and no zinc treatment; Z: zinc treatment; S: saline-sodic treatment; Z + S: saline-sodic and zinc treatment. CB: Changbai 9; TH: Tonghe 899

Fig. 8

Schematic diagram illustrating the composition of Z-shaped electron transport membrane proteins in the photosynthetic electron transport chain. The protein complex includes PSII, cytochrome b6f complex, PSI, and ATP synthase. Electrons are initially released from water by the oxygen-releasing complex (OEC), then transferred to quinone molecules Q_A and Q_B, and further to PSI via quinone and cyanin. Ultimately, these electrons are utilized for ATP synthesis facilitated by ATP synthase. Under saline-sodic stress, the OEC is significantly impaired, leading to inhibition of the electron acceptor and electron donor of PSII and PSI. Nonetheless, the addition of zinc supplement mitigates the saline-sodic stress, diminishes the damage to the OEC, enhances the electron acceptor and electron donor of PSII and PSI, and facilitates electron transfer. Consequently, the photosynthetic efficiency of rice leaves in saline-sodic soil is enhanced. Fdx, Ferredoxin. FNR, Ferredoxin NADP⁺ reductase

Fig. 9

Correlation between sucrose content in rice leaves and roots and sucrose phosphate synthase activity.**is significantly correlated with P < 0.01

Fig. 10

Zinc regulation of rice seedling growth under saline-sodic stress. Black upward and downward arrows indicate the increase and decrease in each indicator