Herbivore-Induced Resistance against Microbial Pathogens in Arabidopsis

Abstract

Caterpillars of the herbivore Pieris rapae stimulate the production of jasmonic acid (JA) and ethylene (ET) in Arabidopsis (Arabidopsis thaliana) and trigger a defense response that affects insect performance on systemic tissues. To investigate the spectrum of effectiveness of P. rapae-induced resistance, we examined the level of resistance against different pathogens. Although the necrotrophic fungus Alternaria brassicicola is sensitive to JA-dependent defenses, herbivore-induced resistance was not effective against this pathogen. By contrast, caterpillar feeding significantly reduced disease caused by the bacterial pathogens Pseudomonas syringae pv tomato and Xanthomonas campestris pv armoraciae. However, this effect was apparent only locally in caterpillar-damaged tissue. Arabidopsis mutants jar1, coi1, ein2, sid2, eds5, and npr1 showed wild-type levels of P. rapae-induced protection against P. syringae pv tomato, suggesting that this local, herbivore-induced defense response does not depend exclusively on either JA, ET, or salicylic acid (SA). Resistance against the biotroph Turnip crinkle virus (TCV) requires SA, but not JA and ET. Nevertheless, herbivore feeding strongly affected TCV multiplication and TCV lesion formation, also in systemic tissues. Wounding alone was not effective, but application of P. rapae regurgitate onto the wounds induced a similar level of protection. Analysis of SA-induced PATHOGENESIS RELATED-1 (PR-1) expression revealed that P. rapae grazing primed Arabidopsis leaves for augmented expression of SA-dependent defenses. Pharmacological experiments showed that ET acts synergistically on SA-induced PR-1, suggesting that the increased production of ET upon herbivore feeding sensitizes the tissue to respond faster to SA, thereby contributing to an enhanced defensive capacity toward pathogens, such as TCV, that trigger SA-dependent defenses upon infection.

Induction of Resistance against the Leafminer,Liriomyza trifolii, by Jasmonic Acid in Sweet Pepper

“…23) Salicylate and JA were also accumulated by attacking spider mites, Tetranychus urticae, in lima bean leaves, 24) and these signaling compounds accumulated by the action of an attacking herbivore could induce resistance against insects or pathogens. It is not known whether or not oviposition of the fly would induce JA in a plant as far as we know, and the cotyledon of sweet pepper did not show any resistance to L. trifolii attack, so the induced amount of JA would have been negligable or nothing.…”

Cross Talk in Defense Signaling

“…For instance, ET produced by Arabidopsis upon herbivory by P. rapae was demonstrated to prime the plant for enhanced SA-mediated defenses that are activated upon infection by Turnip crinkle virus, resulting in enhanced resistance against this biotrophic pathogen (De Vos et al, 2006). Furthermore, transcription factors MYC2 and ETHYLENE RESPONSE FACTOR1 (ERF1) were found to function as important signaling nodes that integrate signals from the JA, ABA, and ET pathways (Anderson et al, 2004;Lorenzo et al, 2004).…”

The Mechanistic Underpinnings of anago1-Mediated, Environmentally Dependent, and Stochastic Phenotype

“…In plant defense, ET potentiates some branches of SA-responsive gene expression (De Vos et al, 2006) but globally represses SA-responsive genes (Chen et al, 2009). ET and JA synergistically promote defense against necrotrophic fungal pathogens through ethylene-responsive transcription factors (ERFs; Lorenzo et al, 2003).…”