Enhanced volatile emissions and anti-herbivore functions mediated by the synergism between jasmonic acid and salicylic acid pathways in tea plants

Abstract

The interaction between jasmonic acid (JA) and salicylic acid (SA) pathways, which affects plant stress resistance, is mainly considered to be antagonistic. Using an established theoretical model, we investigated how tea plant (Camellia sinensis) volatiles induced by exogenous elicitors of JA and SA pathways are affected by the sequence of the elicitor application, the elicitor identity, and the applied concentrations. We also examined the effects of the volatiles mediated by the JA–SA synergistic interaction on the behaviors of a tea leaf-chewing herbivore (Ectropis grisescens) and its parasitic wasp (Apanteles sp.). The JA and SA pathway interactions were almost always reciprocally synergistic when the two pathways were elicited at different times, except at high JA elicitor concentrations. However, the JA pathway antagonized the SA pathway when they were elicited simultaneously. The elicitor identity affected the degree of the JA–SA interaction. The volatiles induced by the JA pathway in the JA–SA reciprocal synergism treatments included up to 11 additional compounds and the total amount of volatiles was up to 7.9-fold higher. Similarly, the amount of emitted volatiles induced by the SA pathway in the reciprocal synergism treatments increased by up to 4.2-fold. Compared with the volatiles induced by either pathway, the enriched volatiles induced by the JA–SA reciprocal synergism similarly repelled E. grisescens, but attracted Apanteles sp. more strongly. Thus, non-simultaneous activation is important for optimizing the JA–SA reciprocal synergism. This reciprocal synergism enables plants to induce multifarious responses, leading to increased biotic stress resistance.

Chromatin accessibility mediated transcriptome changes contribute to flavor substance alterations and jasmonic acid hyperaccumulation during oolong tea withering process

“…In addition, several studies have shown that external application of JA can affect terpenoid synthesis efficiency (Ayala-Zavala et al, 2005;Kim et al, 2006). Similarly, the release of volatile terpenoids was significantly increased by external application of JAs to tea leaves (Jiao et al, 2022). However, this causal linkage between JA and terpene synthesis and the involved key TFs in tea plant remain to be further explored in future.…”

Induced resistance to herbivory and the intelligent plant

“… 42 In contrast, when caterpillars of the specialist tobacco hornworm, Manduca sexta , attacks N. attenuata plants, the simultaneous activation of JA and ethylene signaling pathways results in the attenuation of insecticidal nicotine production, indicating an antagonistic interaction of jasmonate and ethyl signaling. 43 These seemingly opposing outcomes of the crosstalk between the JA and ethylene endogenous signaling suggest that the interaction between two different signaling pathways can be realized at different points in the induction process (from the perception of an environmental cue to the expression of resistance mediating metabolism) and that this can be mediated by differential activation of phytohormone-regulated promoters. It also serves to highlight the point that crosstalk between phytohormonal signaling pathways and their differential outcomes can be evolutionarily adapted and behaviorally adjusted to fine-tune plant metabolism to meet the challenges of the current environmental contexts.…”

Recent Advances in the Specialized Metabolites Mediating Resistance to Insect Pests and Pathogens in Tea Plants (Camellia sinensis)

“…Additionally, exogenous application of JA enhanced the resistance of tea plants to E. grisescens by activating defense characteristics, including defense gene expression and the accumulation of defensive proteins and metabolites. For instance, pretreatment with MeJA increased PPO activity by activating the transcripts of CsPPO2 and CsPPO4 [ 40 ] and induced the biosynthesis of defensive catechins and volatiles [ 38 , 42 ]. In the tea diseases, C. camelliae infection significantly increased JA and OPDA content, and E. vexans infection increased the endogenous levels of JA and SA as well as the expression of synthesis-related genes [ 43 , 44 ] ( Table 1 ).…”