Dissecting photosynthetic electron transport and photosystems performance in Jerusalem artichoke (Helianthus tuberosus L.) under salt stress

Abstract

Jerusalem artichoke (Helianthus tuberosus L.), a vegetable with medical applications, has a strong adaptability to marginal barren land, but the suitability as planting material in saline land remains to be evaluated. This study was envisaged to examine salt tolerance in Jerusalem artichoke from the angle of photosynthetic apparatus stability by dissecting the photosynthetic electron transport process. Potted plants were exposed to salt stress by watering with a nutrient solution supplemented with NaCl. Photosystem I (PSI) and photosystem II (PSII) photoinhibition appeared under salt stress, according to the significant decrease in the maximal photochemical efficiency of PSI (△MR/MR₀) and PSII. Consistently, leaf hydrogen peroxide (H₂O₂) concentration and lipid peroxidation were remarkably elevated after 8 days of salt stress, confirming salt-induced oxidative stress. Besides photoinhibition of the PSII reaction center, the PSII donor side was also impaired under salt stress, as a K step emerged in the prompt chlorophyll transient, but the PSII acceptor side was more vulnerable, considering the decreased probability of an electron movement beyond the primary quinone (ETo/TRo) upon depressed upstream electron donation. The declined performance of entire PSII components inhibited electron inflow to PSI, but severe PSI photoinhibition was not averted. Notably, PSI photoinhibition elevated the excitation pressure of PSII (1-qP) by inhibiting the PSII acceptor side due to the negative and positive correlation of △MR/MR₀ with 1-qP and ETo/TRo, respectively. Furthermore, excessive reduction of PSII acceptors side due to PSI photoinhibition was simulated by applying a specific inhibitor blocking electron transport beyond primary quinone, demonstrating that PSII photoinhibition was actually accelerated by PSI photoinhibition under salt stress. In conclusion, PSII and PSI vulnerabilities were proven in Jerusalem artichoke under salt stress, and PSII inactivation, which was a passive consequence of PSI photoinhibition, hardly helped protect PSI. As a salt-sensitive species, Jerusalem artichoke was recommended to be planted in non-saline marginal land or mild saline land with soil desalination measures.

Keywords: chlorophyll fluorescence; delayed chlorophyll fluorescence; malondialdehyde; modulated 820 nm reflection; photoinhibition.

FIGURE 1

Changes in leaf H₂O₂ (A), malondialdehyde (MDA) (B), Na⁺ (C), and relative water (D) contents in Jerusalem artichoke after 8 days of 100 and 200 mM NaCl stress. Data in the figure are the average value of five replicates (±SD), and the different letters on error bars indicate remarkable differences among salt treatments at P < 0.05. CP, T1, and T2 indicate control plants, plants exposed to 100 and 200 mM NaCl, respectively, and these symbols are also used in the following figures.

FIGURE 2

Changes in photosynthetic rate (Pn) (A), stomatal conductance (g_s) (B), actual photochemical efficiency of photosystem II (PSII) (ΦPSII) (C), and PSII excitation pressure (1-qP) (D) in Jerusalem artichoke under 100 and 200 mM NaCl stress. Data in the figure are the average value of five replicates (±SD), and the different letters on error bars indicate remarkable differences among salt treatments at P < 0.05.

FIGURE 3

Transients of prompt chlorophyll fluorescence (A), delayed chlorophyll fluorescence (B), modulated 820 nm reflection (C), and photosystem I (PSI) oxidation and re-reduction amplitude (D) in Jerusalem artichoke after 8 days of 100 and 200 mM NaCl stress. The specific steps in chlorophyll fluorescence transient are O, K, J, I, and P. The value of modulated 820 nm at the onset of red light illumination [0.7 ms, the first reliable modulated reflection (MR) measurement] is MR₀. PSI oxidation and re-reduction amplitude were represented by MR₀–MR_min and MR_max–MR_min, respectively. Data of MR₀–MR_min and MR_max–MR_min indicate the average value of five replicates (±SD), and the different letters on error bars indicate significant differences at P < 0.05. In delayed chlorophyll fluorescence curves, D0, I1, I2, and D2 are the initial point, the first (7 ms) and second (50 ms) maximal peaks, and the minimum point. The initial microsecond delayed fluorescence signal at 0.3 ms is indicated by DF₀._{3 ms}. The signals were plotted on a logarithmic timescale, and each curve is the mean of five replicate plants.

FIGURE 4

Changes in the maximal photochemical efficiency of photosystem II (PSII) (Fv/Fm) (A), photosystem I (PSI) (△MR/MR₀) (B), variable fluorescence intensity at K step (V_k) (C), primary quinone reducing reaction centers per PSII antenna chlorophyll (RC/ABS) (D), probability that an electron moves beyond primary quinone (ETo/TRo) (E), and probability with which an electron from the intersystem electron carriers is transferred to reduce end electron acceptors at the PSI acceptor side (REo/ETo) (F) in Jerusalem artichoke under 100 and 200 mM NaCl stress. Data in the figure are the average value of five replicates (±SD), and the different letters on error bars indicate remarkable differences among salt treatments at P < 0.05.

FIGURE 5

Regression of the maximal photochemical efficiency of photosystem II (PSI) (△MR/MR₀) with PSII excitation pressure (1-qP) (A) and probability that an electron moves beyond primary quinone (ETo/TRo) (C) in Jerusalem artichoke. The significant correlation at P < 0.05 was indicated by #. Effects of applying DCMU on the maximal photochemical efficiency of PSII (Fv/Fm) (B) and ETo/TRo (D) in Jerusalem artichoke after 8 days of 100 and 200 mM NaCl stress. For reagent treatment, the leaves after 5 days of 100 and 200 mM NaCl stress were immersed in 0 or 70 μM DCMU for 3 h in the dark. Data of Fv/Fm and ETo/TRo indicate the average value of five replicates (±SD), and the different letters on error bars indicate remarkable differences between the leaves with and without DCMU treatment at P < 0.05.