Pathogen‐associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis

Abstract

SummarySystemic acquired resistance (SAR) is usually described as a phenomenon whereby localized inoculation with a necrotizing pathogen renders a plant more resistant to subsequent pathogen infection. Here we show that Pseudomonas syringae strains for which Arabidopsis thaliana represents a non-host plant systemically elevate resistance although the underlying interactions neither trigger a hypersensitive response nor cause necrotic disease symptoms. A similar enhancement of systemic resistance was observed when elicitor-active preparations of two typical bacterial pathogen-associated molecular patterns (PAMPs), flagellin and lipopolysaccharides (LPS), were applied in a localized manner. Several lines of evidence indicate that the observed systemic resistance responses are identical to SAR. Localized applications of non-adapted bacteria, flagellin or LPS elevate levels of the SAR regulatory metabolite salicylic acid (SA) and pathogenesis-related (PR) gene expression not only in treated but also in distant leaves. All treatments also systemically increase expression of the SAR marker gene FLAVIN-DEPENDENT MONOOXYGENASE 1. Further, a whole set of SARdeficient Arabidopsis lines, including mutants in SA biosynthesis and signalling, are impaired in establishing the systemic resistance response triggered by non-host bacteria or PAMPs. We also show that the magnitude of defence reactions such as SA accumulation, PR gene expression or camalexin accumulation induced at sites of virulent or avirulent P. syringae inoculation but not the extent of tissue necrosis during these interactions determines the extent of SAR in distant leaves. Our data indicate that PAMPs significantly contribute to SAR initiation in Arabidopsis and that tissue necroses at inoculation sites are dispensable for SAR activation.

Light Regulation and Daytime Dependency of Inducible Plant Defenses in Arabidopsis: Phytochrome Signaling Controls Systemic Acquired Resistance Rather Than Local Defense

“…(Zeier et al, 2004), we tested whether this light dependency would be mediated by photoreceptors. To examine a potential pathogen-induced enhancement of systemic resistance, three lower rosette leaves (here designated as ''primary leaves'') of a given plant were either infiltrated with 10 mM MgCl 2 in a control treatment, or inoculated with a suspension of Psm (optical density [OD] 0.01) for SAR induction (Mishina and Zeier, 2007). Two days later, three upper, previously nontreated leaves (systemic leaves) were either collected and analyzed for SA content and PR gene expression, or they were subject to a subsequent challenge infection with lower inoculi of Psm (OD 0.002).…”

“…At infection sites, these responses often include rapid production of reactive oxygen species (ROS), biosynthesis of low-molecular-weight defense signals such as salicylic acid (SA) and jasmonic acid (JA), accumulation of phytoalexins, increased expression of pathogenesis-related (PR) proteins, and hypersensitive cell death (hypersensitive response [HR]). A localized contact of leaf tissue with pathogenic or nonpathogenic microbes can further lead to systemic acquired resistance (SAR), a state of enhanced, broadspectrum resistance at the whole plant level that protects against subsequent pathogen attack (Durrant and Dong, 2004;Mishina and Zeier, 2007). Plant SA levels rise systemically during SAR, and this increase is required for induced expression of SA-dependent PR genes and systemic enhancement of disease resistance (Ryals et al, 1996;Métraux, 2002).…”

Methyl Salicylate Production and Jasmonate Signaling Are Not Essential for Systemic Acquired Resistance inArabidopsis

“…During this time period, a marked SAR response develops in Col-0 plants upon inoculation with the used inoculation density of Psm (OD 0.01), which is accompanied with systemic rises of 1 to 2 mg g 21 SA (Mishina and Zeier, 2007;Mishina et al, 2008). With 1.2 ng MeSA g 21 h 21 , Psm-inoculated leaves exhibited a threefold higher exudation of MeSA from petioles than control leaves (see Supplemental Figure 1A online).…”

“…Therein, they are supposed to initiate signaling and amplification processes that lead to an increase of systemic defense responses to boost whole-plant resistance (Mishina and Zeier, 2006). Induction of SAR is not restricted to hypersensitive response (HR)-inducing or necrotizing pathogens but also takes place upon leaf contact with high inoculi of nonpathogenic microbes or after local treatment with bacterial pathogen-associated molecular patterns, such as flagellin or lipopolysaccharides (Mishina and Zeier, 2007). Irrespective of the eliciting stimulus, the molecular events set in motion in inoculated leaves to initiate SAR in distant leaves are only partially understood.…”

Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming

“…When a pathogen or MAMP is recognized in leaves, plants induce systemic acquired resistance (SAR) or MAMP-triggered SAR (mSAR) 6,7 . However, if a first exposure occurs in the roots, usually with a beneficial microbe, plants trigger induced systemic resistance (ISR).…”