Modulation of Photosystem II Function in Celery via Foliar-Applied Salicylic Acid during Gradual Water Deficit Stress

Abstract

Water deficit is the major stress factor magnified by climate change that causes the most reductions in plant productivity. Knowledge of photosystem II (PSII) response mechanisms underlying crop vulnerability to drought is critical to better understanding the consequences of climate change on crop plants. Salicylic acid (SA) application under drought stress may stimulate PSII function, although the exact mechanism remains essentially unclear. To reveal the PSII response mechanism of celery plants sprayed with water (WA) or SA, we employed chlorophyll fluorescence imaging analysis at 48 h, 96 h, and 192 h after watering. The results showed that up to 96 h after watering, the stroma lamellae of SA-sprayed leaves appeared dilated, and the efficiency of PSII declined, compared to WA-sprayed plants, which displayed a better PSII function. However, 192 h after watering, the stroma lamellae of SA-sprayed leaves was restored, while SA boosted chlorophyll synthesis, and by ameliorating the osmotic potential of celery plants, it resulted in higher relative leaf water content compared to WA-sprayed plants. SA, by acting as an antioxidant under drought stress, suppressed phototoxicity, thereby offering PSII photoprotection, together with enhanced effective quantum yield of PSII photochemistry (Φ_PSII) and decreased quantity of singlet oxygen (¹O₂) generation compared to WA-sprayed plants. The PSII photoprotection mechanism induced by SA under drought stress was triggered by non-photochemical quenching (NPQ), which is a strategy to protect the chloroplast from photo-oxidative damage by dissipating the excess light energy as heat. This photoprotective mechanism, triggered by NPQ under drought stress, was adequate in keeping, especially in high-light conditions, an equal fraction of open PSII reaction centers (qp) as of non-stress conditions. Thus, under water deficit stress, SA activates a regulatory network of stress and light energy partitioning signaling that can mitigate, to an extent, the water deficit stress on PSII functioning.

Keywords: chlorophyll fluorescence imaging; chloroplast ultrastructure; drought; electron transport rate; photochemical quenching; photoprotective heat dissipation; singlet oxygen.

Figure 1

Light energy partitioning at PSII. The effective quantum yield of PSII photochemistry (Φ_PSII) at low light (LL) (a) and at high light (HL) (b); the quantum yield of regulated non-photochemical energy loss in PSII (Φ_NPQ) at LL (c) and at HL (d); and the quantum yield of non-regulated energy loss in PSII (Φ_NO) at LL (e) and at HL (f) of water-sprayed or salicylic acid-sprayed (SA), celery plants at 48 h, 96 h, and 192 h after watering. Standard deviations (SD) are shown as error bars (n = 9, 3 independent experiments with 3 plants for each treatment and time point measurement). Significant differences are expressed by different alphabet letters.

Figure 2

The non-photochemical quenching (NPQ) at low light (LL) (a) and at high light (HL) (b) and the electron transport rate (ETR) at LL (c) and at HL (d) of water-sprayed or salicylic acid-sprayed (SA) celery plants at 48 h, 96 h, and 192 h after watering. Standard deviations (SD) are shown as error bars (n = 9, 3 independent experiments with 3 plants for each treatment and time point measurement). Significant differences are expressed by different alphabet letters.

Figure 3

The photochemical quenching (qp), representing the fraction of open PSII reaction centers (RCs) at low light (LL) (a) and at high light (HL) (b), and the efficiency of the open PSII RCs (Fv′/Fm′) at LL (c) and at HL (d) of water-sprayed or salicylic acid-sprayed (SA) celery plants at 48 h, 96 h, and 192 h after watering. Standard deviations (SD) are shown as error bars (n = 9, 3 independent experiments with 3 plants for each treatment and time point measurement). Significant differences are expressed by different alphabet letters.

Figure 4

The excitation pressure at PSII (1−qL) at low light (LL) (a) and at high light (HL) (b) and the excess excitation energy at PSII (EXC) at LL (c) and at HL (d) of water-sprayed or salicylic acid-sprayed (SA) celery plants at 48 h, 96 h, and 192 h after watering. Standard deviations (SD) are shown as error bars (n = 9, 3 independent experiments with 3 plants for each treatment and time point measurement). Significant differences are expressed by different alphabet letters.

Figure 5

Whole leaf area color-coded pictures of Φ_PSII, Φ_NPQ, Φ_NO, and qp, obtained at 200 μmol photons m⁻² s⁻¹, in water-sprayed and salicylic acid-sprayed (SA) celery plants at 48 h after watering. The average whole leaf value of each chlorophyll parameter is provided. At the bottom, the color code indicates the corresponding parameter value as color with a scale from 0 to 1.

Figure 6

Whole leaf area color-coded pictures of Φ_PSII, Φ_NPQ, Φ_NO, and qp, obtained at 200 μmol photons m⁻² s⁻¹, in water-sprayed and salicylic acid-sprayed (SA) celery plants at 192 h after watering. The average whole leaf value of each chlorophyll parameter is provided. At the bottom, the color code indicates the corresponding parameter value as color with a scale from 0 to 1.

Figure 7

TEM micrographs depicting chloroplast ultrastructure in leaves of WA-sprayed (a,c,e) and SA-sprayed (b,d,f) plants at 48 h (a,b), 96 h (c,d), and 192 h (e,f) after watering. Note the dilated appearance of stroma lamellae in chloroplasts of SA-sprayed plants 48 h and 96 h after watering [arrowheads in (b,d)]. Pg: plastoglobuli, Sg: starch grain, scale bars: 0.2 μm.