Arabidopsis thaliana EDS4 Contributes to Salicylic Acid (SA)-Dependent Expression of Defense Responses: Evidence for Inhibition of Jasmonic Acid Signaling by SA

Abstract

The Arabidopsis enhanced disease susceptibility 4 (eds4) mutation causes enhanced susceptibility to infection by the bacterial pathogen Pseudomonas syringae pv. maculicola ES4326 (Psm ES4326). Gene-for-gene resistance to bacteria carrying the avirulence gene avrRpt2 is not significantly affected by eds4. Plants homozygous for eds4 exhibit reduced expression of the pathogenesis-related gene PR-1 after infection by Psm ES4326, weakened responses to treatment with the signal molecule salicylic acid (SA), impairment of the systemic acquired resistance response, and reduced accumulation of SA after infection with Psm ES4326. These phenotypes indicate that EDS4 plays a role in SA-dependent signaling. SA has been shown to have a negative effect on activation of gene expression by the signal molecule jasmonic acid (JA). Two mutations that cause reduced SA levels, eds4 and pad4, cause heightened responses to inducers of JA-dependent gene expression, providing genetic evidence to support the idea that SA interferes with JA-dependent signaling. Two possible working models of the role of EDS4 in governing activation of defense responses are presented.

Constitutive disease resistance requires EDS1 in the Arabidopsis mutants cpr1 and cpr6 and is partially EDS1‐dependent in cpr5

“…In contrast, cpr6 eds1 lines exhibited enhanced PDF1.2 expression to levels signi®c-antly higher than those of cpr6 EDS1 lines or cpr6 ( Figure 3a). The increase in PDF1.2 expression in cpr6 eds1 is reminiscent of observations with other mutants disrupting SA-mediated responses that become sensitized for activation of the JA/ET pathway (Clarke et al, 1998;Clarke et al, 2000;Gupta et al, 2000). We examined whether hyperinduction of JA/ET signaling in cpr6 eds1 plants was a direct consequence of depletion of SA by the eds1 mutation.…”

Epigenetic Control of a Transcription Factor at the Cross Section of Two Antagonistic Pathways

“…These findings are important because they confirm the validity of our microarray data and provide biological context for their interpretation. None of the reported genes functioning upstream of WRKY70 in the SA-and the JA-signaling pathways 23,[29][30][31][32][33] were found among the misexpressed gene fraction in atx1 plants. RT-PCR assays with specific primers for the NPR1, TGA2, ERF, EDS3, EDS8, PAD3, PAD4, and COI2 genes failed to indicate significant changes in expression for any one of these genes in the atx1 background (results not shown).…”

“…31,32 The transcriptional factor WRKY70 was positioned at the convergence nod of the SA-and JA-signaling pathways activating the SA-responsive PR1 gene and repressing the JA-inducible genes. 23,24 As revealed by microarrays, 19 similar relationships between the expressions of WRKY70, PR1 and the JA-responsive genes (THI2.1, VSP2, PDF1.2, HEL) were displayed also in a network regulated by ATX1 (see model in Figure 5.…”

Constitutive salicylic acid‐dependent signaling in cpr1 and cpr6 mutants requires PAD4

“…While some genes can be activated by either exogenous SA or exogenous JA (Schenk et al, 2000), other responses activated by SAdependent signaling are inhibited by JA-dependent signaling, and vice versa. Support for the latter idea includes observations that several Arabidopsis mutants with defects in SA-dependent signaling show enhanced inducible expression of PDF1.2: NahG and npr1 plants express PDF1.2 at higher levels than wild-type plants after treatment with rose bengal or infection by Alternaria brassicicola (Clarke et al, 1998;Penninckx et al, 1996); pad4 and eds4 plants (eds4 plants have reduced SA levels after infection) display enhanced PDF1.2 expression in response to treatment with rose bengal or JA (Gupta et al, 2000); sid2 plants fail to accumulate SA and display enhanced PDF1.2 expression in response to Erisyphe orontii infection (Dewdney et al, 2000); JA treatment inhibits SA-dependent cell death in response to ozone exposure (Rao et al, 2000); and, conversely, constitutive expression of PDF1.2 in cpr6 plants is inhibited by treatment with INA, an inducer of SAdependent signaling (Clarke et al, 1998).…”

“…Perturbations in SA-dependent signaling have been reported to affect jasmonic acid (JA)-dependent signaling, including the expression of PDF1.2 (Clarke et al, 1998;Dewdney et al, 2000;Gupta et al, 2000;Penninckx et al, 1996;Penninckx et al, 1998;Rao et al, 2000). We found enormous genotype-speci®c variation in PDF1.2 mRNA levels ( Figure 6c).…”