Induction of a Compensatory Photosynthetic Response Mechanism in Tomato Leaves upon Short Time Feeding by the Chewing Insect Spodoptera exigua

SIMPLE SUMMARY: Insects such as beet armyworm (Spodoptera exigua) can cause extensive damage to tomato plants (Solanum lycopersicum). Tomato photosynthesis was clearly reduced directly at S. exigua feeding spots. However, neighboring zones and the rest of the leaf compensated through increased light energy use in photosystem II, possibly trigged by singlet oxygen from the feeding zone. Three hours after feeding, whole-leaf photosynthetic efficiency was as before feeding, demonstrating the compensatory ability. Thus, chlorophyll fluorescence imaging analysis could contribute to understanding the effects of herbivory on photosynthesis at a detailed spatial and temporal pattern. ABSTRACT: In addition to direct tissue consumption, herbivory may affect other important plant processes. Here, we evaluated the effects of short-time leaf feeding by Spodoptera exigua larvae on the photosynthetic efficiency of tomato plants, using chlorophyll a fluorescence imaging analysis. After 15 min of feeding, the light used for photochemistry at photosystem II (PSII) (Φ(PSII)), and the regulated heat loss at PSII (Φ(NPQ)) decreased locally at the feeding zones, accompanied by increased non-regulated energy losses (Φ(NO)) that indicated increased singlet oxygen ((1)O(2)) formation. In contrast, in zones neighboring the feeding zones and in the rest of the leaf, Φ(PSII) increased due to a decreased Φ(NPQ). This suggests that leaf areas not directly affected by herbivory compensate for the photosynthetic losses by increasing the fraction of open PSII reaction centers (q(p)) and the efficiency of these centers (Fv’/Fm’), because of decreased non-photochemical quenching (NPQ). This compensatory reaction mechanism may be signaled by singlet oxygen formed at the feeding zone. PSII functionality at the feeding zones began to balance with the rest of the leaf 3 h after feeding, in parallel with decreased compensatory responses. Thus, 3 h after feeding, PSII efficiency at the whole-leaf level was the same as before feeding, indicating that the plant managed to overcome the feeding effects with no or minor photosynthetic costs.