The Crosstalks Between Jasmonic Acid and Other Plant Hormone Signaling Highlight the Involvement of Jasmonic Acid as a Core Component in Plant Response to Biotic and Abiotic Stresses

Abstract

Plant hormones play central roles in plant growth, developmental processes, and plant response to biotic and abiotic stresses. On the one hand, plant hormones may allocate limited resources to the most serious stresses; on the other hand, the crosstalks among multiple plant hormone signaling regulate the balance between plant growth and defense. Many studies have reported the mechanism of crosstalks between jasmonic acid (JA) and other plant hormones in plant growth and stress responses. Based on these studies, this paper mainly reviews the crosstalks between JA and other plant hormone signaling in regulating the balance between plant growth and defense response. The suppressor proteins JASMONATE ZIM DOMAIN PROTEIN (JAZ) and MYC2 as the key components in the crosstalks are also highlighted in the review. We conclude that JA interacts with other hormone signaling pathways [such as auxin, ethylene (ET), abscisic acid (ABA), salicylic acid (SA), brassinosteroids (BRs), and gibberellin (GA)] to regulate plant growth, abiotic stress tolerance, and defense resistance against hemibiotrophic pathogens such as Magnaporthe oryzae and Pseudomonas syringae. Notably, JA may act as a core signal in the phytohormone signaling network.

Keywords: crosstalk; defense response; environmental stress; jasmonic acid; plant hormone.

Figure 1

The core components of the jasmonic acid (JA) signaling pathway in rice, tobacco, and Arabidopsis. CORONATINE INSENSITIVE 1 (COI1) protein, JASMONATE ZIM DOMAIN PROTEIN (JAZ), and MYC constitute the core signal transduction mechanism of JA signaling. Under control conditions, the endogenous level of JA–isoleucine (Ile) is very low plants. JAZ repressors bind to MYC2 to inhibit its transcriptional activation on downstream genes. Under stress conditions, the endogenous level of JA–Ile is largely activated, which is perceived by JA receptor COI1. Then SKP1/CULLIN/F-box (SCF)^COI1 binds to JAZs for ubiquitination and degradation through the 26S proteasome pathway, resulting in the release of the downstream transcription factors (TFs) such as MYCs and the activation of JA responses.

Figure 2

JASMONATE ZIM DOMAIN PROTEIN (JAZ)-mediated crosstalks among jasmonic acid (JA) hormone signaling pathways in plant growth and stress responses. (A) The complex crosstalk between JA and auxin signaling pathways. JA and auxin signaling pathways coordinately regulate flower development through modulation of JA, while JA and auxin antagonize root growth through JAZs-MYC2. (B) The complex crosstalk between JA and ethylene (ET) signaling pathways. JA and ET coordinately regulate plant stress responses through JAZs-MYC2 and EIN3/EIL1, especially in resisting necrotrophic or hemibiotrophic pathogens. (C) The complex crosstalk between JA and abscisic acid (ABA) signaling pathways. The crosstalk between PYRABACTIN RESISTANCE1-Like protein (PYL) and JAZ–MYC2 coordinates the balance between plant growth and defense resistance. (D) The complex crosstalk between JA and SA signaling pathways. SA initiates early defense-related gene expression in pathogen-infected plants, while JA induces late defense-related gene expression in pathogen-infected plants, mainly in the necrotrophic stage of necrotrophic or hemibiotrophic pathogens. (E) The complex crosstalk between JA and brassinosteroids (BR) signaling pathways. The crosstalk between JA and BR biosynthesis may be involved in the balance between plant growth and defense resistance. (F) The complex crosstalk between JA and GA signaling pathways. The JAZ-MYC2-DELLA-PIF signaling module being involved in the crosstalk between JA and GA signaling can be elucidated. In addition, many transcription factors (TFs) such as MYC3, MYC4, MYB21, and MYB24 can also interact with DELLAs, so there may be synergistic effect between JA and GA signaling.

Figure 3

JA-mediated cold and freezing stress responses in plants. Under control conditions, JAZ1 and JAZ4 interact with ICE1 and ICE2 to inhibit the ICE–CBF signaling pathway. Under low-temperature conditions, bioactive JA–Ile and ICE–CBF pathways are activated, and the expressions of cold-regulated genes are induced to improve plant cold tolerance. CBF, C repeat binding factor; ICE, INDUCER OF CBF EXPRESSION; Ile, isoleucine; JA, jasmonic acid; JAZ, JASMONATE ZIM DOMAIN PROTEIN.

Figure 4

Jasmonic acid (JA)-mediated drought stress response in plants. In response to drought stress, the JA signaling pathway is activated; OsbHLH148 interacts with OsJAZ1 to activate the expression of OsDREB1, together with JA-mediated root hydraulic conductivity and stomatal closure, thereby improving drought tolerance in rice.

Figure 5

(A) Jasmonic acid (JA)-mediated disease resistance against Magnaporthe oryzae in rice. When rice blast fungus is compatible with rice, rice blast fungus secretes antibiotic biosynthetic monooxygenase (Abm) and inhibits JA activity and immune response. When rice blast fungus and rice are incompatible, Abm secreted by rice blast fungus is degraded, resulting in the accumulation of methyl jasmonate (MeJA) and the activation of JA downstream response as well as immune response. (B) JA-mediated disease resistance against Pseudomonas syringae in Arabidopsis. HopZ1a directly interacts with JASMONATE ZIM DOMAIN PROTEIN (JAZ) proteins and induces the acetylation of JAZ proteins, thereby activating the JA signaling pathway (Jiang et al., 2013). As one kind of functional JA analog, coronatine (COR) can induce CORONATINE INSENSITIVE 1 (COI1) to bind to JAZ proteins, thereby activating JA downstream response and plant immune response (Zhang F et al., 2015).