Rewiring of the jasmonic acid signaling pathway during insect herbivory on Arabidopsis

Abstract

Plants are attacked by a plethora of potentially devastating pathogens and pests. To protect themselves, plants have evolved a sophisticated immune system in which phytohormones play pivotal regulatory roles. Jasmonic acid (JA) emerged as an important hormonal regulator of defense responses that are triggered by insect herbivores and microbial pathogens with a necrotrophic life style. Although JA accumulates in response to invasion by both types of attackers, JA-dependent defenses against herbivores and necrotrophs are antagonistically regulated by different branches of the JA signaling pathway. This PhD research aimed to gain detailed insight into the molecular mechanisms and biological significance of this differential JA response, with the ultimate goal to understand how plants are able to fine-tune their immune system to survive in continuously changing and hostile environments. In model plant Arabidopsis thaliana (Arabidopsis), MYC2 and ERF-type transcription factors are major players in the differential control of the two distinct branches of the JA pathway. This is nicely exemplified in Arabidopsis plants being attacked by larvae of the insect herbivore Pieris rapae (small cabbage white butterfly). Herbivory activates the MYC2-branch of the JA pathway, leading to concomitant suppression of the ERF-branch. Using Arabidopsis genotypes affected in MYC2- or ERF-TF functioning, we demonstrated that the insect larvae prefer to feed from plant tissues that express the ERF-branch of the JA pathway. Interestingly, factors in oral secretion of the caterpillars were shown to steer the JA pathway towards the insect-preferred ERF-branch. However, during the interaction of the insect with Arabidopsis, the MYC2/ERF balance was rewired towards the MYC2 branch, thereby suppressing the insect-preferred ERF-branch of the JA pathway. This “hide-the-candy” strategy of the plant sheds new light on the mechanisms involved in the evolutionary arms race between plants and their herbivorous enemies. A second hormone, abscisic acid (ABA), appeared to play an important modulating role in the differential JA response. Upon insect feeding, ABA production was significantly increased. Using mutant and pharmacological approaches we demonstrated that ABA is essential for rewiring the JA pathway towards expression of the MYC2-branch, thereby preventing stimulation of the insect-preferred ERF-branch. We also demonstrated that herbivory primed undamaged, systemic tissues for enhanced MYC2-dependent defenses, which potentially protects healthy tissues against future insect attack. In a field study, we investigated the performance of Arabidopsis mutants that are constitutively primed for enhanced defenses. From this study we learned that plants may be primed when grown under natural conditions. Moreover, putting molecular mechanisms to the test in a field setting contributes greatly to our understanding of both the complexity and flexibility of the plant’s immune system. The detailed analysis of molecular mechanisms and biological significance of hormonal regulation of the plant immune signaling network fostered important new insights into how plants selectively adapt to the diverse biotic stresses in nature. This provides a rational basis for developinginnovative approaches to sustainably increase crop production in times of increased demand and ever-growing environmental challenges.