Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis

Abstract

Jasmonate (JA) and ethylene (ET) are two major plant hormones that synergistically regulate plant development and tolerance to necrotrophic fungi. Both JA and ET induce the expression of several pathogenesis-related genes, while blocking either signaling pathway abolishes the induction of these genes by JA and ET alone or in combination. However, the molecular basis of JA/ET coaction and signaling interdependency is largely unknown. Here, we report that two Arabidopsis ET-stabilized transcription factors (EIN3 and EIL1) integrate ET and JA signaling in the regulation of gene expression, root development, and necrotrophic pathogen defense. Further studies reveal that JA enhances the transcriptional activity of EIN3/EIL1 by removal of JA-Zim domain (JAZ) proteins, which physically interact with and repress EIN3/EIL1. In addition, we find that JAZ proteins recruit an RPD3-type histone deacetylase (HDA6) as a corepressor that modulates histone acetylation, represses EIN3/EIL1-dependent transcription, and inhibits JA signaling. Our studies identify EIN3/EIL1 as a key integration node whose activation requires both JA and ET signaling, and illustrate transcriptional derepression as a common mechanism to integrate diverse signaling pathways in the regulation of plant development and defense.root hair | Botrytis cinerea P lants are sessile organisms and face different environmental changes during their lifespan. To survive various abiotic and biotic stresses, plants synthesize a number of small molecules functioning as phytohormones to elaborately regulate their growth, development, and defense. Two types of phytohormonesethylene (ET) and jasmonate (JA)-are crucial for plant development and defense against necrotrophic fungi infections (1-3). Complicated modes of interaction between ET and JA have been documented in different processes. For example, ET strongly suppresses JA-induced wounding-responsive gene expression, but JA suppresses ET-induced apical hook formation (4, 5), indicative of their antagonisms. Upon necrotrophic fungi infections, plants can quickly produce ET and JA and induce the expression of downstream defense genes (like ERF1, ORA59, and PDF1.2) that help plants tolerate or fight against the fungal pathogens (1). Plants treated with exogenous JA or ET express high levels of defense genes (6, 7), and simultaneous treatment with JA and ET results in the highest expression (8). Nevertheless, in the ET or JA insensitive mutant (ein2 or coi1, respectively), JA and ET alone or in combination fail to induce the expression of those defense genes (8, 9), indicating that the two hormone-signaling pathways are required concomitantly for the activation of plant-defense response. These results suggest that JA and ET act synergistically and mutually dependently in regulating necrotrophic pathogen responses. However, the molecular details underlying such hormone synergy and signaling interdependency are currently unknown.ET is a gaseous hormone, which is perceived by its receptors and represses a Raf-like kinase CON...

The Arabidopsis Mediator subunit MED16 regulates iron homeostasis by associating with EIN3/EIL1 through subunit MED25

“…B€ ackstr€ om et al (2007) proposed that Mediator recruits and works with species-specific transcription factors through either newly evolved subunits or subunits with one conserved Mediator-interacting domain and one species-specific regulator-interacting domain. This proposal is supported by recent research that the ACID domain of MED25 interacts with many transcription factors in Arabidopsis (Elfving et al, 2011;Ou et al, 2011;Zhu et al, 2011;C ßevik et al, 2012) and our results that MED25 interacts with YID1/MED16 through its conserved N-terminal vWF-A domain. We noticed, however, that neither YID1/MED16 nor MED25 was induced by iron deficiency ( Figure S6), which raised the question of how the Mediator complex was assembled under iron-deficient conditions.…”

“…Furthermore, EIN3 and EIL1 are linked to ethylene signaling in the jasmonic acid (JA) signaling pathways. EIN3 and EIL1 interact with JAZ proteins that are associated with NINJA protein, recruiting TOP-LESS to induce gene expression in the JA signaling pathway (Pauwels et al, 2010;Zhu et al, 2011).…”

Interaction between MYC2 and ETHYLENE INSENSITIVE3 Modulates Antagonism between Jasmonate and Ethylene Signaling inArabidopsis

“…double mutant displayed susceptibility, as indicated by the larger lesion size compared with the wild type ( Figures 7A and 7B), confirming that EIN3 and EIL1 are required for resistance against B. cinerea (Alonso et al, 2003;Zhu et al, 2011). Similar to ein3 eil1, the myc2 ein3 eil1 triple mutant also exhibited larger lesion size ( Figures 7A and 7B), demonstrating that ein3 eil1 blocked the elevated resistance against B. cinerea in myc2.…”

“…JA and ET act synergistically to defend against necrotrophic pathogen infection and to promote root hair development (Penninckx et al, 1996;Zhu et al, 2006) via a synergistic regulatory model in which JA induces degradation of JAZ proteins and derepresses ET-stabilized EIN3 and EIL1, which interact with JAZs (Zhu et al, 2011). However, such a synergistic regulatory model is inconsistent with the antagonistic roles of JA and ET signaling in many important processes.…”

“…It is so far reported that such JA-ET signaling synergy is mediated by derepression of ET-stabilized EIN3 and EIL1: JAZ proteins directly interact with and repress EIN3/EIL1, while JA induces JAZ degradation to derepress EIN3 and EIL1 (Zhu et al, 2011). JAinduced EIN3 and EIL1 activation (Zhu et al, 2011) and ETinduced EIN3 and EIL1 stabilization (Guo and Ecker, 2003;Potuschak et al, 2003;Gagne et al, 2004) mediate JA and ET signaling synergy in the regulation of root hair development and resistance against necrotrophic fungal infection.…”