A Novel Signaling Pathway Controlling Induced Systemic Resistance in Arabidopsis

Abstract

Plants have the ability to acquire an enhanced level of resistance to pathogen attack after being exposed to specific biotic stimuli. In Arabidopsis, nonpathogenic, root-colonizing Pseudomonas fluorescens bacteria trigger an induced systemic resistance (ISR) response against infection by the bacterial leaf pathogen P. syringae pv tomato. In contrast to classic, pathogen-induced systemic acquired resistance (SAR), this rhizobacteria-mediated ISR response is independent of salicylic acid accumulation and pathogenesis-related gene activation. Using the jasmonate response mutant jar1 , the ethylene response mutant etr1 , and the SAR regulatory mutant npr1 , we demonstrate that signal transduction leading to P. fluorescens WCS417r-mediated ISR requires responsiveness to jasmonate and ethylene and is dependent on NPR1. Similar to P. fluorescens WCS417r, methyl jasmonate and the ethylene precursor 1-aminocyclopropane-1-carboxylate were effective in inducing resistance against P. s. tomato in salicylic acid-nonaccumulating NahG plants. Moreover, methyl jasmonate-induced protection was blocked in jar1 , etr1 , and npr1 plants, whereas 1-aminocyclopropane-1-carboxylate-induced protection was affected in etr1 and npr1 plants but not in jar1 plants. Hence, we postulate that rhizobacteria-mediated ISR follows a novel signaling pathway in which components from the jasmonate and ethylene response are engaged successively to trigger a defense reaction that, like SAR, is regulated by NPR1. We provide evidence that the processes downstream of NPR1 in the ISR pathway are divergent from those in the SAR pathway, indicating that NPR1 differentially regulates defense responses, depending on the signals that are elicited during induction of resistance. INTRODUCTIONPlants of which the roots have been colonized by selected strains of nonpathogenic fluorescent Pseudomonas spp develop an enhanced level of protection against pathogen attack (reviewed in van Loon et al., 1998). Strain WCS417r of P. fluorescens is a biological control strain that has been shown to trigger an induced systemic resistance (ISR) response in several plant species, including carnation (van Peer et al., 1991), radish (Leeman et al., 1995), tomato (Duijff et al., 1996), and Arabidopsis (Pieterse et al., 1996). In Arabidopsis, P. fluorescens WCS417r-mediated ISR has been demonstrated against the bacterial leaf pathogen P. syringae pv tomato , the fungal root pathogen Fusarium oxysporum f sp raphani (Pieterse et al., 1996;van Wees et al., 1997), and the fungal leaf pathogen Peronospora parasitica (J. Ton and C.M.J. Pieterse, unpublished data), indicating that this type of biologically induced resistance is effective against different types of pathogens.ISR-inducing rhizobacteria show host specificity in regard to eliciting resistance (Leeman et al., 1995;van Wees et al., 1997), which indicates that specific recognition between protective bacteria and the plant is a prerequisite for the activation of the signaling cascade leading to ISR. The downstream signaling event...

Costs and benefits of priming for defense in Arabidopsis

“…Seedlings were grown in sand for 2 weeks and subsequently transferred to 60-ml pots containing a potting soil-sand (12:5) mixture as described in ref. 13. Plants were cultivated in a growth chamber with a 9-h day (24°C) and 15-h (20°C) night cycle at 60-70% relative humidity.…”

“…Selected strains of nonpathogenic rhizobacteria can also induce systemic resistance, which is referred to as induced systemic resistance (ISR) (12). In Arabidopsis, ISR triggered by Pseudomonas fluorescens WCS417r functions independently of SA but requires NPR1 and responsiveness to JA and ethylene (13). P. fluorescens WCS417r-mediated ISR has a different spectrum of effectiveness than SAR, and is predominantly effective against pathogens that are sensitive to JA-and ethylenedependent basal resistance (11).…”

Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana

“…Recently, Zhang et al (40) provided evidence that, upon induction of SAR, NPR1 activates PR-1 gene expression by physically interacting with a subclass of basic leucine zipper protein transcription factors that bind to promoter sequences required for SA-inducible PR gene expression. Elucidation of the sequence of ISR-signaling events revealed that NPR1 also functions downstream of the JA and ethylene response in the ISR pathway (35). Evidently, NPR1 is not only required for the SA-dependent expression of PR genes that are activated during SAR, but also for the JA-and ethylenedependent activation of so far unidentified defense responses resulting from rhizobacteria-mediated ISR.…”

“…In contrast, WCS417r-mediated ISR functions independently of SA and PR gene activation (30,31) but requires JA and ethylene signaling. The JA response mutant jar1 and the ethylene response mutant etr1, that express normal levels of pathogeninduced SAR (32,34,35), did not express ISR upon treatment with WCS417r, indicating that the ISR-signaling pathway requires components of the JA and ethylene response (35,36).…”

“…Although SAR and ISR follow distinct signaling pathways, they are both blocked in the regulatory mutant npr1 (for nonexpresser of PR genes) of Arabidopsis (35,37). NPR1 (also called NIM1 or SAI1) was originally discovered as a key regulatory protein that functions downstream of SA in the SAR pathway (37)(38)(39).…”