Jasmonate-triggered plant immunity

Abstract

The plant hormone jasmonate (JA) exerts direct control over the production of chemical defense compounds that confer resistance to a remarkable spectrum of plant-associated organisms, ranging from microbial pathogens to vertebrate herbivores. The underlying mechanism of JA-triggered immunity (JATI) can be conceptualized as a multi-stage signal transduction cascade involving: i) pattern recognition receptors (PRRs) that couple the perception of danger signals to rapid synthesis of bioactive JA; ii) an evolutionarily conserved JA signaling module that links fluctuating JA levels to changes in the abundance of transcriptional repressor proteins; and iii) activation (de-repression) of transcription factors that orchestrate the expression of myriad chemical and morphological defense traits. Multiple negative feedback loops act in concert to restrain the duration and amplitude of defense responses, presumably to mitigate potential fitness costs of JATI. The convergence of diverse plant- and non-plant-derived signals on the core JA module indicates that JATI is a general response to perceived danger. However, the modular structure of JATI may accommodate attacker-specific defense responses through evolutionary innovation of PRRs (inputs) and defense traits (outputs). The efficacy of JATI as a defense strategy is highlighted by its capacity to shape natural populations of plant attackers, as well as the propensity of plant-associated organisms to subvert or otherwise manipulate JA signaling. As both a cellular hub for integrating informational cues from the environment and a common target of pathogen effectors, the core JA module provides a focal point for understanding immune system networks and the evolution of chemical diversity in the plant kingdom.

Fig. 1

Jasmonate perception by the COI1 receptor system is essential for resistance of cultivated tomato to the oomycete pathogen Pythium. Wild-type (cv Castlemart) and jai1 mutant plants grown for three weeks in a growth chamber without visible signs of disease were transplanted to a field plot at Michigan State University, East Lansing, MI. Two weeks after transplanting, all jai1 plants (N = 30) died from a disease that was diagnosed as Pythium stem/root rot by the MSU Diagnostics Lab. Sequencing of PCR products derived from 5.8S ribosomal gene and internal transcribed spacer region in infected tomato tissue confirmed the presence of Pythium ultimum. Of several hundred wild-type (Jai1/Jai1) plants grown side-by-side at the same field site, none showed symptoms of the disease. The figure shows photographs of representative wild-type (A and B) and jai1 mutant (C and D) plants two weeks after transplantation. Identical results were obtained in three independent trails performed at the same site.

Fig. 2

Model of jasmonate-triggered plant immunity (JATI). Danger signals (MAMPs/HAMPs) derived from attacking organisms and damaged plant cells (DAMPs) are recognized by pattern recognition receptors (PRRs) at the cell surface. PRR activation is coupled to intracellular signaling systems involving MAP kinase pathways, calcium ion-sensing proteins, and reactive oxygen species (ROS), among others. How these signaling events are connected to activation of the core JA signal module, which includes JA biosynthesis from its precursor linolenic acid (LA), is largely unknown (?). Plastidic and peroxisomal enzymes convert LA to jasmonic acid (JA), which is the substrate for synthesis of JA-Ile in the cytosol. Within the nucleus, JA-Ile promotes JAZ-COI1 interaction and targets JAZs for proteolytic degradation by the ubiquitin-proteasome system. Removal of JAZ alleviates TFs from repression, thereby activating the expression of JA-responsive genes and the expression of chemical and morphological defense traits (Defense). Several mechanisms to attenuate signaling through the core module have been elucidated, including catabolism of JA-Ile via ω-oxidation and hydrolysis, de novo synthesis of JAZ repressors that are stable in the presence of JA-Ile, and accumulation of JAM TFs that negatively regulate transcription. Pathogen-derived effectors target the core JA signal module to disrupt hormonal balance and induced immune responses. Abbreviations: Microbe-associated molecular patterns (MAMPs); Herbivore-associated molecular patterns (HAMPs); Damage-associated molecular patterns (DAMPs), Mitogen-activated protein kinase (MAPK); 12-oxo-phytodienoic acid (OPDA), β-oxidation (β-ox), jasmonoyl-L-isoleucine (JA-Ile), JASMONATE-ZIM domain (JAZ), JA-related transcription factor (TF), JASMONATE-ASSOCIATED MYC2-LIKE (JAM), 12-carboxy-JA-Ile (12COOH-JA-Ile).