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

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) (ΦPSII), and the regulated heat loss at PSII (ΦNPQ) decreased locally at the feeding zones, accompanied by increased non-regulated energy losses (ΦNO) that indicated increased singlet oxygen (1O2) formation. In contrast, in zones neighboring the feeding zones and in the rest of the leaf, ΦPSII increased due to a decreased ΦNPQ. This suggests that leaf areas not directly affected by herbivory compensate for the photosynthetic losses by increasing the fraction of open PSII reaction centers (qp) 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.

Root-Associated Entomopathogenic Fungi Modulate Their Host Plant’s Photosystem II Photochemistry and Response to Herbivorous Insects

“…The compensatory reaction to herbivory can minimize a reduction in growth or reproduction of the plant after herbivore attack, improving fitness of plants growing in environments with a high herbivory level [ 74 ]. The compensatory capability differs, varying with the plant species, the extent of the leaf area lost, the timing of the herbivory, the environmental conditions, and the mode of herbivore injury [ 44 , 74 ]. Such a compensatory is rationalized by a higher requirement of the remaining leaf area for a higher fraction of the absorbed light energy for photochemistry to fix larger amounts of carbon [ 44 , 74 ].…”

“…The compensatory capability differs, varying with the plant species, the extent of the leaf area lost, the timing of the herbivory, the environmental conditions, and the mode of herbivore injury [ 44 , 74 ]. Such a compensatory is rationalized by a higher requirement of the remaining leaf area for a higher fraction of the absorbed light energy for photochemistry to fix larger amounts of carbon [ 44 , 74 ]. The light reactions of photosynthesis feed the energy supply required for the production of compounds used in defense, such as hormones, and other defense-related metabolites [ 26 , 75 ].…”

“…Spodoptera exigua larvae were cultured from eggs (Entocare Wageningen, Netherlands) on an artificial diet [ 44 ] prior to experiments and kept under controlled conditions at 21 ± 1 °C day/night temperature, with a 12-h light cycle and 38 ± 5% relative humidity. The larvae used in the experiments were L2 instar larvae, which were starved for 24 h before exposing them to the tomato leaflets, assuring a faster consumption.…”

“…In a previous study [ 44 ], we showed that photosynthetic efficiency of tomato leaves increased in response to biting by Spodoptera exigua larvae (Hűbner; beet armyworm) in neighboring leaf parts, suggesting a compensatory response. Tomato, Solanum lycopersicum , is one of the commonly cultivated horticultural crops [ 45 , 46 ] that is susceptible to a variety of insect pests [ 3 , 47 , 48 ].…”

Leaf Age-Dependent Photosystem II Photochemistry and Oxidative Stress Responses to Drought Stress in Arabidopsis thaliana Are Modulated by Flavonoid Accumulation

“…Chlorophyll fluorescence analysis has been widely used to acquire knowledge about the function of the photosynthetic machinery and for the assessment of photosynthetic tolerance mechanisms to biotic [ 66 , 86 , 101 , 102 ] and abiotic stresses [ 103 , 104 , 105 , 106 , 107 , 108 ], including drought stress [ 21 , 22 , 96 , 108 , 109 , 110 ]. However, DS may not affect a plant leaf uniformly [ 97 ], thus photosynthetic performance may be extremely heterogeneous at the leaf surface, denoting conventional chlorophyll fluorescence measurements non-characteristic of the physiological status of the entire leaf [ 111 , 112 , 113 ].…”