Circadian Network Interactions with Jasmonate Signaling and Defense

Abstract

Plants experience specific stresses at particular, but predictable, times of the day. The circadian clock is a molecular oscillator that increases plant survival by timing internal processes to optimally match these environmental challenges. Clock regulation of jasmonic acid (JA) action is important for effective defenses against fungal pathogens and generalist herbivores in multiple plant species. Endogenous JA levels are rhythmic and under clock control with peak JA abundance during the day, a time when plants are more likely to experience certain types of biotic stresses. The expression of many JA biosynthesis, signaling, and response genes is transcriptionally controlled by the clock and timed through direct connections with core clock proteins. For example, the promoter of Arabidopsis transcription factor MYC2, a master regulator for JA signaling, is directly bound by the clock evening complex (EC) to negatively affect JA processes, including leaf senescence, at the end of the day. Also, tobacco ZEITLUPE, a circadian photoreceptor, binds directly to JAZ proteins and stimulates their degradation with resulting effects on JA root-based defenses. Collectively, a model where JA processes are embedded within the circadian network at multiple levels is emerging, and these connections to the circadian network suggest multiple avenues for future research.

Keywords: circadian clock; defense; jasmonic acid; signaling.

Figure 1

Progression of a simplified oscillator and JA processes over the 24-h day. Core oscillator components that are directly relevant to JA processes are shown (top) where proteins (ovals) appear at the time of their peak activity between dawn (left) and night (right). Transcriptional regulation events are depicted by red lines and post-translational regulation events are shown with black lines. The clock proteins shown at each phase, in general, suppress activities at other parts of the day. Morning proteins (CCA1/LHY) repress PRR genes, including TOC1, and themselves. PRR activity (grouped in box) is sequential throughout the day; PRRs repress previous PRR genes and CCA1/LHY. The evening complex (EC) represses TOC1, GI, and itself. F-box protein ZTL is stabilized by GI in blue light, but targets (without GI) PRR5, TOC1, and CHE for ubiquitylation and degradation in the dark. Proteins depicted here are relevant to the discussion of JA processes; other clock proteins exist with both repression and activation roles. JA biosynthesis genes, JA levels, and many JA response genes cycle over the course of 24 h and thus time many aspects of JA action to midday (bottom).

Figure 2

Gating of JA responses through gene expression control and by TIC. COI1-JAZ-MYC signaling complex positive components (green) and negative components (red) are shown in the morning (left) or evening (right); more intense coloring and darker border indicate higher protein abundance. Throughout the night and at dawn, the clock protein TIC reduces MYC2 protein abundance likely through direct interaction, and it therefore restricts MYC2-dependent actions (right side) [76]. Positive factors of the COI1-JAZ-MYC2 complex (COI1, MYC2) are more abundant at dawn and during the daytime due to transcriptional or post-translational control, and this is one mechanism that gates JA responsiveness to this time of the day. JA early genes (i.e., JAZ5) are most inducible by JA treatment at dawn [76]. The JA mimic coronatine (COR) produced by Pseudomonas syringae (Pst DC3000) hyper-activates the JA pathway and suppresses SA-dependent and independent host defenses against biotrophic pathogens [77,78]. Treatment of plants at dawn with Pst DC3000 results in leaves that support more pathogen proliferation compared to treatment at dusk, although clock-timing of stomata closure that is independent of JA signaling could play an important role too (bottom) [76,79].

Figure 3

The clock protein ZTL directly regulates JA signaling and nicotine biosynthesis in Nicotiana attenuata roots. Nicotine is a neurotoxin produced in Nicotiana species that is synthesized in roots and transported to shoots where it accumulates and acts as a feeding deterrent (left side) [81]. Some underlying genes in nicotine biosynthesis are rhythmically expressed and/or are directly controlled by master regulator MYC2 homologs in Nicotiana species [80,82]. N. attenuata plants with reduced abundance of clock protein ZTL through expression of an inverted repeat construct (referred to ir-ztl) have defective rhythms, due to the role of ZTL in the clock [80,83] (right side). Both basal and induced JA levels are not substantially different between wild type and ir-ztl plants [80]. However, plants with reduced ZTL expression have reduced nicotine levels and diminished resistance to the generalist herbivore Spodoptera littoralis (Egyptian cotton leafworm) as measured by worm biomass, a defect that is rescued by exogenous application of nicotine [80]. Nicotine biosynthesis genes in ir-ztl plants are expressed at lower levels and with dampened rhythms [80]. ZTL physically interacts with the JAZb repressor protein with a resulting decrease in JAZb abundance (left) [80]; more intense coloring and darker border indicate higher protein abundance. Loss of ZTL function in ir-ztl plants likely increases JAZ presence and decreases N. attenuata MYC2a action in nicotine biosynthesis, among other processes (right). ZTL therefore contributes to herbivore resistance in Nicotiana by enabling MYC2 gene expression capabilities through JAZ destabilization that may depend on the time of day.