Feeding of pea leafminer larvae simultaneously activates jasmonic and salicylic acid pathways in plants to release a terpenoid for indirect defense

Abstract

The pea leafminer, Liriomyza huidobrensis, is an important pest species affecting ornamental crops worldwide. Plant damage consists of oviposition and feeding punctures created by female adult flies as well as larva-bored mines in leaf mesophyll tissues. How plants indirectly defend themselves from these two types of leafminer damage has not been sufficiently investigated. In this study, we compared the indirect defense responses of bean plants infested by either female adults or larvae. Puncturing of leaves by adults released green leaf volatiles and terpenoids, while larval feeding caused plants to additionally emit methyl salicylate and (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene (TMTT). Puncturing of plants by female adults induced increases in jasmonic acid (JA) and JA-related gene expressions but reduced the expressions of salicylic acid (SA)-related genes. In contrast, JA and SA and their-related gene expression levels were increased significantly by larval feeding. The exogenous application of JA+SA significantly triggered TMTT emission, thereby significantly inducing the orientation behavior of parasitoids. Our study has confirmed that larval feeding can trigger TMTT emission through the activation of both JA and SA pathways to attract parasitoids; however, TMTT alone is less attractive than the complete blend of volatiles released by infested plants.

Terpenes from herbivore‐induced tomato plant volatiles attract Nesidiocoris tenuis (Hemiptera: Miridae), a predator of major tomato pests

“…T. absoluta and T. vaporariorum have different feeding modes (leaf mining versus phloem sap sucking), and the variation in volatile signature is consequently attributed to differences in the plant defence pathways induced by these herbivores 47 . Leaf mining or chewing larvae activate the jasmonic acid pathway in host plants and trigger the emission of large amounts of volatiles compared to phloem sap‐sucking whiteflies, which are known to activate the salicylic acid pathway 47,48 …”

“…47 Leaf mining or chewing larvae activate the jasmonic acid pathway in host plants and trigger the emission of large amounts of volatiles compared to phloem sap-sucking whiteflies, which are known to activate the salicylic acid pathway. 47,48 Since N. tenuis preys more on T. absoluta than on whiteflies, 22,23 it is possible that the predator has an innate preference for plant odours induced by its preferred prey species. The generalist anthocorid predator Orius majusculus (Reuter) was reported to be more attracted to volatiles of maize plants infested with its preferred prey, the leafhopper Zyginidia scutellaris (Herrich-Schäffer), than to those of plants infested with Dalbulus maidis (DeLong & Wolcott).…”

Plant Secondary Metabolites as Defense Tools against Herbivores for Sustainable Crop Protection

“…The salicyclic acid pathway is activated in plants in response to piercing and sucking insects [ 73 ]. The puncturing of a leaf by leaf minor adults activates the JA pathway, while larval mining activates both JA and SA defense pathways [ 74 ].…”

“…Ethylene emission and JA accumulation in plants upon feeding herbivory have been reported [ 76 ]. The ethylene pathway does not work in an isolated manner to elicit a defense response but works with a network of plant hormones [ 74 ]. Multiple signaling cascades are involved in the induction of plant defenses by insect feeding.…”

A lncRNA fine-tunes salicylic acid biosynthesis to balance plant immunity and growth

“…SA extraction and measurement were performed as previously described (Yang et al, 2021). Briefly, SA was extracted from 240 mg 2-week-old seedlings of Col-0, sabc1-1, sabc1-2, and nac3-1 plants under neutral-day conditions.…”