The Activated SA and JA Signaling Pathways Have an Influence on flg22-Triggered Oxidative Burst and Callose Deposition

Abstract

The first line of defense in plants against pathogens is induced by the recognition of microbe-associated molecular patterns (MAMP). Perception of bacterial flagellin (flg22) by the pattern recognition receptor flagellin-sensing 2 (FLS2) is the best characterized MAMP response, although the underlying molecular mechanisms are not fully understood. Here we studied the relationship between salicylic acid (SA) or jasmonic acid (JA) signaling and FLS2-mediated signaling by monitoring flg22-triggered responses in known SA or JA related mutants of Arabidopsis thaliana (L.) Heynh. The sid2 mutant, impaired in SA biosynthesis, had less basal FLS2 mRNA accumulation than the wild type, which correlated with suppression of early flg22 responses such as ROS production and induction of marker genes, WRKY29 and FRK1. The JA-signaling mutants, jar1 and coi1, exhibited an enhanced flg22-triggered oxidative burst and more callose accumulation than the wild type, and pretreatment with SA or coronatine (COR), a structural mimic of JA-isoleucine, altered these flg22-induced responses. Nonexpressor of pathogenesis-related genes 1 (NPR1) acted downstream of SID2 and required SA-dependent priming for the enhanced flg22-triggered oxidative burst and callose deposition. Activation of JA signaling by COR pretreatment suppressed the flg22-triggered oxidative burst and callose accumulation in a coronatine insensitive 1 (COI1) dependent manner. COR had a negative effect on flg22 responses but only the flg22-triggered oxidative burst depended on SA-JA/COR signaling antagonism. Thus the activated SA and JA signaling pathways have an influence on flg22-triggered oxidative burst and callose deposition. These results may explain how SA and JA signaling are cross talked for regulation of flg22-triggered responses.

How does SA signaling link the Flg22 responses?

“…Pretreatment with low concentrations of SA enhanced not only the FLS2 transcript level but also the amplitude of FLS2-mediated flg22 responses, including the oxidative burst and callose deposition, mediated by NPR1. 18 Other reports are consistent with our finding that NPR1 plays a role in SA-mediated priming for enhanced defense responses. 24,25 Although the molecular basis of the SA-mediated priming effect in flg22 responses is unclear, we hypothesize that SA pretreatment act at the post-translational level through protein modification.…”

“…Flg22-dependent induction of WRKY29 and FRK1 genes was reduced by almost 50% in the sid2 mutant compared to WT. 18 These results suggest that basal SA is required to establish sufficient flg22-triggered early responses such as oxidative burst and marker gene induction.…”

“…20 In our system, basal FLS2 mRNA was strongly enhanced in cim6 and suppressed in sid2, compared to the WT. 18 However, this suppression was less in sid2 than in ein2. A possible explanation is that ISOCHOR-ISMATE SYNTHASE2 (ICS2) may have a partially redundant function, by mutation in isochorismate synthase 1 (ICS1) so that SA accumulation is not completely blocked in sid2.…”

“…28,29 In our system, pre-incubation with SA alone promoted FLS2 transcript accumulation compared to the untreated plant. 18 The enhanced level of FLS2 mRNA and free stable NPR1, possibly due to SA pretreatment, might contribute to accelerated FLS2-dependent flg22 responses.…”

“…21 Basal expression of EIN2 mRNA was also suppressed in sid2 compared to WT. 18 It may be that the basal levels of SID2 and SA in the WT plant are required for EIN2 transcript accumulation, a suggestion that implies that SA signaling components are accompanied by other factors, such as EIN2, on regulation of FLS2 gene. Based on our observations, we suggest that SA contributes to early flg22 responses through activating FLS2 mRNA accumulation.…”