ORA59 and EIN3 interaction couples jasmonate‐ethylene synergistic action to antagonistic salicylic acid regulation of PDF expression

Abstract

Hormonal crosstalk is central for tailoring plant responses to the nature of challenges encountered. The role of antagonism between the two major defense hormones, salicylic acid (SA) and jasmonic acid (JA), and modulation of this interplay by ethylene (ET) in favor of JA signaling pathway in plant stress responses is well recognized, but the underlying mechanism is not fully understood. Here, we show the opposing function of two transcription factors, ethylene insensitive3 (EIN3) and EIN3-Like1 (EIL1), in SA-mediated suppression and JA-mediated activation of PLANT DEFENSIN1.2 (PDF1.2). This functional duality is mediated via their effect on protein, not transcript levels of the PDF1.2 transcriptional activator octadecanoid-responsive arabidopsis59 (ORA59). Specifically, JA induces ORA59 protein levels independently of EIN3/EIL1, whereas SA reduces the protein levels dependently of EIN3/EIL1. Co-infiltration assays revealed nuclear co-localization of ORA59 and EIN3, and split-luciferase together with yeast-two-hybrid assays established their physical interaction. The functional ramification of the physical interaction is EIN3-dependent degradation of ORA59 by the 26S proteasome. These findings allude to SA-responsive reduction of ORA59 levels mediated by EIN3 binding to and targeting of ORA59 for degradation, thus nominating ORA59 pool as a coordination node for the antagonistic function of ET/JA and SA.

AP2/ERF Family Transcription Factors ORA59 and RAP2.3 Interact in the Nucleus and Function Together in Ethylene Responses

“…SA suppressed JA-responsive gene expression by downregulating ORA59 accumulation. In agreement with this, ORA59 overexpression in plants counteracted the SA-mediated antagonistic effect on JA-mediated PDF1.2 expression ( Leon-Reyes et al, 2010 ; Van der Does et al, 2013 ; He et al, 2017 ).…”

“…To date, several transcription factors that interact with ORA59 and RAP2.3 have been reported. He et al (2017) demonstrated that ORA59 interacts with EIN3, and this interaction is required for SA-mediated reduction in ORA59 protein levels. RAP2.3 was associated with DELLA proteins ( Marín-de la Rosa et al, 2014 ).…”

Ethylene signaling in plants

“…EIN3 is the transcription factor with the largest role in ethylene signaling (128,139) and it homodimerizes to interact with its target DNA (141). However, environmental factors such as dark versus light or the presence of other hormones can affect this so that depending on conditions, EIN3 interacts with other transcription factors leading to outputs not predicted by the common ethylene signaling models (179)(180)(181). As an example, ethylene is well known for inhibiting hypocotyl growth in dark-grown eudicot seedlings (36,182) and stimulating hypocotyl growth in the light (183)(184)(185)(186)(187).…”

Jasmonic acid alleviates cadmium toxicity in Arabidopsis via suppression of cadmium uptake and translocation

“…Jasmonic acid (JA), an important phytohormone that participates in many physiological processes and stress responses in plants (Robert‐Seilaniantz et al ; He et al ; Hickman et al ; Sarde et al ; Howe et al ), is also known to be involved in the response to Cd stress, with JA promotion of Cd tolerance being reported. For example, Cd induced the expression of JA synthesis and JA‐response genes (Cabot et al ; Keunen et al ), and a biphasic‐modal accumulation of JA was observed in the mature leaves of Arabidopsis (Maksymiec et al ).…”