Ethylene Signaling Renders the Jasmonate Response of Arabidopsis Insensitive to Future Suppression by Salicylic Acid

Abstract

Cross-talk between jasmonate (JA), ethylene (ET), and Salicylic acid (SA) signaling is thought to operate as a mechanism to fine-tune induced defenses that are activated in response to multiple attackers. Here, 43 Arabidopsis genotypes impaired in hormone signaling or defense-related processes were screened for their ability to express SA-mediated suppression of JA-responsive gene expression. Mutant cev1, which displays constitutive expression of JA and ET responses, appeared to be insensitive to SA-mediated suppression of the JA-responsive marker genes PDF1.2 and VSP2. Accordingly, strong activation of JA and ET responses by the necrotrophic pathogens Botrytis cinerea and Alternaria brassicicola prior to SA treatment counteracted the ability of SA to suppress the JA response. Pharmacological assays, mutant analysis, and studies with the ET-signaling inhibitor 1-methylcyclopropene revealed that ET signaling renders the JA response insensitive to subsequent suppression by SA. The APETALA2/ETHYLENE RESPONSE FACTOR transcription factor ORA59, which regulates JA/ET-responsive genes such as PDF1.2, emerged as a potential mediator in this process. Collectively, our results point to a model in which simultaneous induction of the JA and ET pathway renders the plant insensitive to future SA-mediated suppression of JA-dependent defenses, which may prioritize the JA/ET pathway over the SA pathway during multi-attacker interactions.

Salicylic Acid Suppresses Jasmonic Acid Signaling Downstream of SCFCOI1-JAZ by Targeting GCC Promoter Motifs via Transcription Factor ORA59

“…SA to suppress JA-induced gene expression (Leon-Reyes et al, 2010a). In two out of five experiments, we did not detect the negative effect of SA on ORA59-GFP accumulation, suggesting that this effect can be modulated by so far unidentified environmental conditions.…”

“…Despite the fact that SA reduced ORA59 accumulation in 35S: ORA59-GFP plants, PDF1.2 gene expression could not be suppressed by SA in these plants (Figures 6C and 6D; see Supplemental Figure 4B online). Leon-Reyes et al (2010a) reported previously that overexpression of ORA59 negatively affects the ability of SA to suppress PDF1.2 gene expression. This finding highlights the importance of ORA59 in the outcome of the SA/JA antagonism.…”

“…Many reports describe an antagonistic interaction between the SA and JA pathways, but synergistic interactions have been reported as well (Mur et al, 2006). Clearly, the kinetics of hormone production and signaling during the interaction of a plant with its enemies is highly decisive in the final outcome of the defense response (Koornneef et al, 2008b;Leon-Reyes et al, 2010a).…”

“…Several other molecular players in SA/ JA crosstalk have been identified, including the mitogen-activated protein kinase MPK4 (Petersen et al, 2000), the lipase-like proteins ENHANCED DISEASE SUSCEPTIBILITY1 and PHY-TOALEXIN-DEFICIENT4 (Brodersen et al, 2006), the fatty acid desaturase SUPPRESSOR OF SA INSENSITIVITY2 (Kachroo et al, 2003), glutaredoxin GRX480 (Ndamukong et al, 2007;Zander et al, 2010), and class II TGA and WRKY transcription factors (Li et al, 2004;Mao et al, 2007;Ndamukong et al, 2007;Leon-Reyes et al, 2010a;Zander et al, 2010;Gao et al, 2011). Mutation or ectopic expression of the corresponding genes often have contrasting effects on SA and JA signaling and on resistance against biotrophs and necrotrophs, indicating that these proteins are important regulators of SA/JA crosstalk.…”

Not to be suppressed? Rethinking the host response at a root-parasite interface

“…If this pathway is indeed utilised for the development of root-knot nematode infestation sites, how then would it be possible to explain the observations that such treatments resulted in increased host resistance? One possible explanation could come from the understanding that defense-like signaling pathways can have altered outcomes depending on how the network was previously stimulated [13,60,61]. The context of pre-exposure may therefore be critical with a consequence that jasmonate signaling processes normally induced by root-knot nematodes could become diverted into an immune response by such treatments.…”