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...

Salicylic acid-independent plant defence pathways

“…The Arabidopsis jasmonate response mutant jar1 and the ethylene response mutant etr1, which show a normal response to inducers of SAR, are unable to express ISR after root treatment with P. fluorescens WCS417r (Ref. 46), indicating that signal transduction leading to rhizobacteria-mediated ISR requires responsiveness to both jasmonate and ethylene. Although ISR and SAR seem to follow distinct signalling pathways, 55 trends in plant science reviews February 1999, Vol.…”

“…tomato has been investigated by application of methyl jasmonate and the ethylene precursor 1-aminocyclopropane-1-carboxylate (ACC) as inducing agents 46 (Fig. 3), which, like P. fluorescens WCS417r, are effective in inducing resistance against P. syringae pv.…”

“…Whether some of these unknown defensive compounds are also produced upon pathogen attack or wounding needs to be investigated. 46 . This suggests that ISR is associated with an increase in sensitivity to these hormones rather than an increase in their production, which might lead to the activation of a partially different set of defence genes.…”

OsWRKY03, a rice transcriptional activator that functions in defense signaling pathway upstream of OsNPR1

“…For example, induced systemic resistance (ISR), which is triggered by nonpathogenic root-colonizing bacteria, is JA and ethylene dependent [16,17] and is independent of SA and PR-gene activation [18,19]. The JA response mutant jar1 and the ethylene response mutant etr1 lose ISR upon treatment with Pseudomonas fluorescens WCS417r, but remain normal level of pathogen-induced SAR [20,21], indicating that JA and ethylene responses are critical for the ISR-signaling pathway [22,23]. Analysis of signaling molecules involved in rhizobacteria-madiated ISR suggests that ISR might be associated with another pathogen-induced jasmonate and ethylene defense response, in which a subset of PR genes, such as PR3, PR4, and PR12, were co-regulated by jasmonate and ethylene [24,25].…”

Colonization of the Arabidopsis rhizosphere by fluorescent Pseudomonas spp. activates a root-specific, ethylene-responsive PR-5 gene in the vascular bundle

“…Analysis of the jasmonic acid (JA)-response mutant jar1-1, a range of ethylene (ET)-response mutants, and the SAR-compromised mutant npr1-1 revealed that components of the JA-and the ET-response are required for triggering WCS417r-mediated ISR, but that like SAR, this induced resistance response depends on NPR1 (Knoester et al, 1999;Pieterse et al, 1998). However, downstream of NPR1, the ISR and the SAR signaling pathways diverge, because unlike SAR, ISR is not accompanied by the concomitant activation of PR genes (Pieterse et al, 1996;Van Wees et al, 1999;Van Wees et al, 1997).…”