PBS3 and EPS1 complete salicylic acid biosynthesis from isochorismate in Arabidopsis

Abstract

Salicylic acid (SA) is an important phytohormone mediating both local and systemic defense responses in plants. Despite over half a century of research, how plants biosynthesize SA remains unresolved. In Arabidopsis, a major part of SA is derived from isochorismate, a key intermediate produced by the isochorismate synthase (ICS), which is reminiscent of SA biosynthesis in bacteria. Whereas bacteria employ an isochorismate pyruvate lyase (IPL) that catalyzes the turnover of isochorismate to pyruvate and SA, plants do not contain an IPL ortholog and generate SA from isochorismate through an unknown mechanism. Combining genetic and biochemical approaches, we delineated the SA biosynthetic pathway downstream of isochorismate in Arabidopsis. We show that PBS3, a GH3 acyl adenylase-family enzyme important for SA accumulation, catalyzes ATP-and Mg 2+ -dependent conjugation of L-glutamate primarily to the 8-carboxyl of isochorismate and yields the key SA biosynthetic intermediate isochorismoyl-glutamate A. Moreover, EPS1, a BAHD acyltransferase-family protein with previously implicated role in SA accumulation upon pathogen attack, harbors a noncanonical active site and an unprecedented isochorismoyl-glutamate A pyruvoyl-glutamate lyase (IPGL) activity that produces SA from the isochorismoyl-glutamate A substrate. Together, PBS3 and EPS1 form a two-step metabolic pathway to produce SA from isochorismate in Arabidopsis, which is distinct from how SA is biosynthesized in bacteria. This study closes a major knowledge gap in plant SA metabolism and would help develop new strategies for engineering disease resistance in crop plants.

High-resolution Expression Profiling of Selected Gene Sets during Plant Immune Activation

“…Pathogen‐induced SA accumulation is required for plant immunity, and one major pathway of SA biosynthesis is via isochorismate (IC) (Dempsey et al, ). The IC pathway involves several enzymes that are required for the key catalytic steps, and encoded by ICS1 , EDS5 and PBS3 (Rekhter et al, ; Torrens‐Spence et al, ). They are all ERGs and directly regulated by TFs SARD1 and CBP60g (Sohn et al, ; Sun et al, ).…”

Fungal effector Jsi1 hijacks plant JA/ET signaling through Topless

“…Regarding the Go category of SA response genes, 39 out of 40 genes were upregulated, including GRX480, ALD1, WRKY70, and PR1 which have been described as SA-regulated genes (Herrera-Vásquez et al, 2014, Cecchini et al, 2015, Li et al, 2004, Durrant and Dong, 2004 . In addition, we found two genes, EPS1 and PBS3, involved in SA synthesis (Torrens-Spence et al, 2019) and regulators of the SA-induce immune response including NPR3, NPR4, andNIMIN1 (Ding et al, 2018, Weigel et al, 2005) (Fig. S8).…”

“…S5c). The increased SA level could be a consequence of the upregulation of EPS1 and PBS3, which are involved in SA synthesis (Torrens-Spence et al, 2019) . On the other hand, the lack of JA and JA-Ile indicate that the activation of the ERF branch by Jsi1 is independent of the hormone.…”

“…and PBS3, involved in SA synthesis (Torrens-Spence et al, 2019). Activation of SA signaling could have several causes.…”

JMJ14 encoded H3K4 demethylase modulates immune responses by regulating defence gene expression and pipecolic acid levels

“…Conversely, mutants that accumulate high levels of SA often display constitutive defence responses (Clarke et al, 2001;Vlot et al, 2009). Following pathogen inoculation, SA biosynthesis is initiated via the ISOCHORISMATE SYNTHASE 1 (ICS1) catalysed step in chloroplasts (Wildermuth et al, 2001), while the conversion of isochorismate to SA occurs in the cytosol (Rekhter et al, 2019;Torrens-Spence et al, 2019). SA accumulation and signalling also involves additional components including PHYTOALEXIN-DEFICIENT 4 (PAD4) (Jirage et al, 1999), GH3-LIKE DEFENSE GENE 1 (GDG1) (Jagadeeswaran et al, 2007), HOPW1-1 INTERACTING 3 (WIN3) (Lee et al, 2007), NON-EXPRESSOR OF PATHOGENESIS-RELATED GENE 1/3/4 (NPR1/3/4) (Cao et al, 1997;Ding et al, 2018), and several WRKY family transcription factors (Eulgem & Somssich, 2007;Zhang & Li, 2019).…”