The Compensatory Response of Photosystem II Photochemistry to Short-Term Insect Herbivory Is Suppressed Under Water Deficit

Abstract

Photosystem II (PSII) is very sensitive to both biotic and abiotic stress conditions, mirroring global climate changes. Crop production worldwide faces rising hazards from the increased duration, frequency, and intensity of drought stress episodes as a result of climate change, and its effects, when combined with biotic stress, are becoming more noticeable. In the present work, we examined PSII responses of well-watered (WW) tomato plants or mildly drought-stressed (MDS) plants to 20 min of Tuta absoluta larvae feeding. The effective quantum yield of PSII photochemistry (Φ_PSII) of the whole leaf in WW plants, after 20 min of larvae feeding, compensated for the reduction in Φ_PSII observed at the feeding area. In contrast, the reduced Φ_PSII at the feeding areas of MDS plants, after 20 min of larvae feeding, was not compensated at the whole-leaf level because of the drought stress. The increased Φ_PSII and electron transport rate (ETR) at the whole-leaf level in WW plants was attributed to the increased fraction of open PSII reaction centers (qp), since there was no difference in the efficiency of the open PSII reaction centers (Fv'/Fm') before and after feeding. Therefore, the response of PSII photochemistry in WW plants to short-term biotic stress resulted in an overcompensation reaction, which developed a whole-leaf photosynthetic enhancement. However, short-term biotic stress in combination with mild abiotic stress resulted in decreased PSII photochemistry. It is concluded that increased crop damage is likely to occur due to the global climate-change-induced drought episodes, influencing insect herbivory.

Keywords: Solanum lycopersicum; Tuta absoluta; compensatory photosynthesis; drought stress; effective quantum yield of PSII (ΦPSII); electron transport rate (ETR); excitation pressure; herbivory; hormesis; non-photochemical quenching (NPQ).

Figure 1

The maximum efficiency of PSII photochemistry (Fv/Fm) (a), and the efficiency of the oxygen-evolving complex (Fv/Fo) (b) before and after 20 min of larvae feeding, in well-watered (WW, control) or mildly drought-stressed (MDS) tomatoes. Standard deviations (SD) are shown by bars. Different lower-case letters reveal significant differences at p < 0.05 (n = 6).

Figure 2

The effective quantum yield of PSII photochemistry (Φ_PSII) at actinic light (AL) of 250 μmol photons m⁻² s⁻¹, corresponding to the growth light intensity (GLI) (a), and at actinic light (AL) of 1000 μmol photons m⁻² s⁻¹, corresponding to a high light intensity (HLI) (b), measured before and after 20 min of larvae feeding, in well-watered (WW, control) or mildly drought-stressed (MDS) tomatoes. Standard deviations (SD) are shown by bars. Different lower-case letters reveal significant differences at p < 0.05 (n = 6).

Figure 3

Τhe quantum yield of regulated non-photochemical energy loss in PSII (Φ_NPQ) at 250 μmol photons m⁻² s⁻¹ AL (a) and at 1000 μmol photons m⁻² s⁻¹ AL (b), before and after 20 min of larvae feeding, in well-watered (WW, control) or mildly drought-stressed (MDS) tomatoes. Standard deviations (SD) are shown by bars. Different lower-case letters reveal significant differences at p < 0.05 (n = 6).

Figure 4

The quantum yield of non-regulated energy loss in PSII (Φ_NO) at 250 μmol photons m⁻² s⁻¹ AL (a) and at 1000 μmol photons m⁻² s⁻¹ AL (b), before and after 20 min of larvae feeding, in well-watered (WW, control) or mildly drought-stressed (MDS) tomatoes. Standard deviations (SD) are shown by bars. Different lower-case letters reveal significant differences at p < 0.05 (n = 6).

Figure 5

The electron transport rate (ETR) at 250 μmol photons m⁻² s⁻¹ AL (a) and at 1000 μmol photons m⁻² s⁻¹ AL (b), before and after 20 min of larvae feeding, in well-watered (WW, control) or mildly drought-stressed (MDS) tomatoes. Standard deviations (SD) are shown by bars. Different lower-case letters reveal significant differences at p < 0.05 (n = 6).

Figure 6

The non-photochemical quenching (NPQ) at 250 μmol photons m⁻² s⁻¹ AL (a) and at 1000 μmol photons m⁻² s⁻¹ AL (b), before and after 20 min of larvae feeding, in well-watered (WW, control) or mildly drought-stressed (MDS) tomatoes. Standard deviations (SD) are shown by bars. Different lower-case letters reveal significant differences at p < 0.05 (n = 6).

Figure 7

The portion of open PSII rection centers (RCs) (qp) that reveal the redox state of quinone A (Q_A), at 250 μmol photons m⁻² s⁻¹ AL (a) and at 1000 μmol photons m⁻² s⁻¹ AL (b), before and after 20 min of larvae feeding, in well-watered (WW, control) or mildly drought-stressed (MDS) tomatoes. Standard deviations (SD) are shown by bars. Different lower-case letters reveal significant differences at p < 0.05 (n = 6).

Figure 8

The efficiency of the open PSII RCs (Fv′/Fm′) at 250 μmol photons m⁻² s⁻¹ AL (a) and at 1000 μmol photons m⁻² s⁻¹ AL (b), before and after 20 min of larvae feeding, in well-watered (WW, control) or mildly drought-stressed (MDS) tomatoes. Standard deviations (SD) are shown by bars. Different lower-case letters reveal significant differences at p < 0.05 (n = 6).

Figure 9

The excess excitation energy at PSII (EXC) at 250 μmol photons m⁻² s⁻¹ AL (a) and at 1000 μmol photons m⁻² s⁻¹ AL (b), before and after 20 min of larvae feeding, in well-watered (WW, control) or mildly drought-stressed (MDS) tomatoes. Standard deviations (SD) are shown by bars. Different lower-case letters reveal significant differences at p < 0.05 (n = 6).

Figure 10

The excitation pressure at PSII (1-qL) at 250 μmol photons m⁻² s⁻¹ AL (a) and at 1000 μmol photons m⁻² s⁻¹ AL (b), before and after 20 min of larvae feeding, in well-watered (WW, control) or mildly drought-stressed (MDS) tomatoes. Standard deviations (SD) are shown by bars. Different lower-case letters reveal significant differences at p < 0.05 (n = 6).

Figure 11

The relationship of the maximum efficiency of PSII photochemistry (Fv/Fm) with the efficiency of the oxygen-evolving complex (Fv/Fo), before and after 20 min of larvae feeding, in well-watered (WW, control) or mildly drought-stressed (MDS) tomatoes, based on the data of Figure 1a,b. Blue dots represent the paired measurements of the variables while the red line is the regression line that illustrates the relationship between the two variables.

Figure 12

The relationship between the excess excitation energy (EXC) and the effective quantum yield of PSII photochemistry (Φ_PSII) at 250 μmol photons m⁻² s⁻¹ (a) and at 1000 μmol photons m⁻² s⁻¹ AL (b), before and after 20 min of larvae feeding, in well-watered (control) or mildly drought-stressed tomatoes, based on the data of Figure 2a,b and Figure 9a,b. Blue dots represent the paired measurements of the variables while the red line is the regression line that illustrates the relationship between the two variables.

Figure 13

The relationship between the redox state of quinone A (Q_A) and the effective quantum yield of PSII photochemistry (Φ_PSII) at 250 μmol photons m⁻² s⁻¹ (a) and at 1000 μmol photons m⁻² s⁻¹ AL (b), before and after 20 min of larvae feeding, in well-watered (control) or mildly drought-stressed tomatoes, based on the data of Figure 2a,b and Figure 7a,b. Blue dots represent the paired measurements of the variables while the red line is the regression line that illustrates the relationship between the two variables.

Figure 14

Representative color-coded images of the light energy partitioning at PSII, to photochemistry (Φ_PSII), heat dissipation (Φ_NPQ), or nonregulatory lost (Φ_NO), and the respective color-coded images of the portion of open PSII rection centers (RCs) (qp), before and after 20 min of larvae feeding, in well-watered (WW, control) or mildly drought-stressed (MDS) tomatoes. The areas of interest (AOIs) measured at the leaf surface are shown by circles, while the whole leaflet (average) value is given in white. White arrows point out the feeding areas. The color code on the bottom of the images shows pixel values ranging from 0.0 to 1.0.