Reactive Oxygen Species Initiate Defence Responses of Potato Photosystem II to Sap-Sucking Insect Feeding

SIMPLE SUMMARY: Potato is one of the most universally cultivated horticultural crops and is vulnerable to a range of herbivorous insects. One of them is the brown marmorated stink bug, an invasive polyphagous sap-sucking agricultural insect pest that penetrates the phloem to sieve elements and removes sap via a specialized mouthpart, the stylet. By using the chlorophyll fluorescence imaging methodology, we examined potato photosystem II (PSII) photochemistry responses in the area of feeding on the whole leaf area. Highly increased reactive oxygen species (ROS) generation was observed as rapidly as 3 min after feeding to initiate defence responses and can be considered the primary plant defence response mechanism against herbivores. Our experimental results confirmed that chlorophyll fluorescence imaging methodology can detect spatial heterogeneity of PSII efficiency at the whole leaf surface and is a promising tool for investigating plant response mechanisms of sap-sucking insect herbivores. We suggest that PSII responses to insect feeding underlie ROS-dependent signalling. We conclude that the potato PSII response mechanism to sap-sucking insect herbivores is described by the induction of the defence response to reduce herbivory damage, instead of induction of tolerance, through a compensatory photosynthetic response mechanism that is observed after chewing insect feeding. ABSTRACT: Potato, Solanum tuberosum L., one of the most commonly cultivated horticultural crops throughout the world, is susceptible to a variety of herbivory insects. In the present study, we evaluated the consequence of feeding by the sap-sucking insect Halyomorpha halys on potato leaf photosynthetic efficiency. By using chlorophyll fluorescence imaging methodology, we examined photosystem II (PSII) photochemistry in terms of feeding and at the whole leaf area. The role of reactive oxygen species (ROS) in potato’s defence response mechanism immediately after feeding was also assessed. Even 3 min after feeding, increased ROS generation was observed to diffuse through the leaf central vein, probably to act as a long-distance signalling molecule. The proportion of absorbed energy being used in photochemistry (Φ(PSII)) at the whole leaf level, after 20 min of feeding, was reduced by 8% compared to before feeding due to the decreased number of open PSII reaction centres (qp). After 90 min of feeding, Φ(PSII) decreased by 46% at the whole leaf level. Meanwhile, at the feeding zones, which were located mainly in the proximity of the leaf midrib, Φ(PSII) was lower than 85%, with a concurrent increase in singlet-excited oxygen ((1)O(2)) generation, which is considered to be harmful. However, the photoprotective mechanism (Φ(NPQ)), which was highly induced 90 min after feeding, was efficient to compensate for the decrease in the quantum yield of PSII photochemistry (Φ(PSII)). Therefore, the quantum yield of non-regulated energy loss in PSII (Φ(NO)), which represents (1)O(2) generation, remained unaffected at the whole leaf level. We suggest that the potato PSII response to sap-sucking insect feeding underlies the ROS-dependent signalling that occurs immediately and initiates a photoprotective PSII defence response to reduce herbivory damage. A controlled ROS burst can be considered the primary plant defence response mechanism to herbivores.