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...
Systemic acquired resistance is a pathogen-inducible defense mechanism in plants. The resistant state is dependent on endogenous accumulation of salicylic acid (SA) and is characterized by the activation of genes encoding pathogenesisrelated (PR) proteins. Recently, selected nonpathogenic, root-colonizing biocontrol bacteria have been shown to trigger a systemic resistance response as well. To study the molecular basis underlying this type of systemic resistance, we developed an Arabidopsis-based model system using Fusarium oxysporum f sp raphani and Pseudomonas syringae pv tomato as challenging pathogens. Colonization of the rhizosphere by the biological control strain WCS417r of R fluorescens resulted in a plant-mediated resistance response that significantly reduced symptoms elicited by both challenging pathogens; Moreover, growth of R syringae in infected leaves was strongly inhibited in R fluorescens WCS417r-treated plants. Transgenic Arabidopsis NahG plants, unable to accumulate SA, and wild-type plants were equally responsive to R fluorescens WCS417r-mediated induction of resistance. Furthermore, R fluorescens WCS417r-mediated systemic resistance did not coincide with the accumulation of PR mRNAs before challenge inoculation. These results indicate that R fluorescens WCS417r induces a pathway different from the one that controls classic systemic acquired resistance and that this pathway leads to a form of systemic resistance independent of SA accumulation and PR gene expression.
SummaryIn plants carrying the NahG transgene, salicylate hydroxylase converts salicylic acid (SA) to catechol. Arabidopsis NahG plants are defective in non-host resistance to Pseudomonas syringae pv. phaseolicola strain 3121 (Psp), suggesting that resistance requires SA signaling. However, several mutants with defects in SA signaling, including eds1, pad4, eds5, sid2, and npr1, remain resistant to Psp, demonstrating that susceptibility of NahG plants is not due to absence of SA. SA synthesis is blocked in sid2NahG double mutants, but resistance to Psp is retained. Therefore, it must be the degradative action of NAHG on SA that causes the loss of resistance of NahG to Psp. Treatment of plants with catechol compromised Psp resistance suggesting that the effect of NahG on resistance results from catechol production. Application of catalase to NahG or catechol-treated wild-type plants partially restored resistance to Psp, suggesting that the deleterious effect of catechol results from inappropriate production of hydrogen peroxide. These results indicate that conclusions about SA requirements based solely on phenotypes of NahG plants should be reevaluated.
The phytohormone jasmonic acid (JA) is a critical regulator of plant growth and defense. To significantly advance our understanding of the architecture and dynamics of the JA gene regulatory network, we performed high-resolution RNA-Seq time series analyses of methyl JAtreated Arabidopsis thaliana. Computational analysis unraveled in detail the chronology of events that occur during the early and later phases of the JA response. Several transcription factors, including ERF16 and bHLH27, were uncovered as early components of the JA gene regulatory network with a role in pathogen and insect resistance. Moreover, analysis of subnetworks surrounding the JA-induced transcription factors ORA47, RAP2.6L, and ANAC055 provided novel insights into their regulatory role of defined JA network modules. Collectively, our work illuminates the complexity of the JA gene regulatory network, pinpoints to novel regulators, and provides a valuable resource for future studies on the function of JA signaling components in plant defense and development.
Background Since the 1980s, numerous mutualistic Pseudomonas spp. strains have been used in studies on the biology of plant growth-promoting rhizobacteria (PGPR) and their interactions with host plants. In 1988, a strain from the Pseudomonas fluorescens group, WCS417, was isolated from lesions of wheat roots growing in a take-all disease-suppressive soil. In subsequent trials, WCS417 limited the build-up of take-all disease in field-grown wheat and significantly increased wheat yield. In 1991, WCS417 was featured in one of the first landmark studies on rhizobacteria-induced systemic resistance (ISR), in which it was shown to confer systemic immunity in carnation (Dianthus caryophyllus) against Fusarium wilt. The discovery that WCS417 conferred systemic immunity in the model plant species Arabidopsis thaliana in 1996 incited intensive research on the molecular mechanisms by which PGPR promote plant growth and induce broad-spectrum disease resistance in plants. Since then, the strain name appeared in over 750 studies on beneficial plant-microbe interactions. Scope In this review, we will highlight key discoveries in plant-microbe interactions research that have emerged from over 30 years of research featuring WCS417 as a model rhizobacterial strain. WCS417 was instrumental in improving our understanding of the microbial determinants that are involved in root colonization and the establishment of mutually beneficial interactions with the host plant. The model strain also provided novel insight into the molecular mechanisms of plant growth promotion and the onset and expression of rhizobacteria-ISR. More recently, WCS417 has been featured in studies on host immune evasion during root colonization, and chemical communication in the rhizosphere during root microbiome assembly. Conclusions Numerous studies on the modes of action of WCS417 have provided major conceptual advances in our understanding of how free-living mutualists colonize the rhizosphere, modulate plant immunity, and promote plant growth. The concepts may prove useful in our understanding of the molecular mechanisms involved in other binary plant-beneficial microbe interactions, and in more complex microbial community contexts, such as the root microbiome.
The phytohormone jasmonic acid (JA) is vital in plant defense and development. Although biosynthesis of JA and activation of JA-responsive gene expression by the bioactive form JAisoleucine (JA-Ile) have been well-studied, knowledge on JA metabolism is incomplete. In particular, the enzyme that hydroxylates JA to 12-OH-JA, an inactive form of JA that accumulates after wounding and pathogen attack, is unknown. Here, we report the identification of four paralogous 2-oxoglutarate/Fe(II)-dependent oxygenases in Arabidopsis thaliana as JA hydroxylases and show that they down-regulate JA-dependent responses. As they are induced by JA we named them JASMONATE-INDUCED OXYGENASEs (JOXs). Concurrent mutation of the four genes in a quadruple Arabidopsis mutant resulted in increased defense gene expression and increased resistance to the necrotrophic fungus Botrytis cinerea and the caterpillar Mamestra brassicae. In addition, root and shoot growth of the plants was inhibited. Metabolite analysis of leaves showed that loss of function of the four JOX enzymes resulted in over-accumulation of JA and in reduced turnover of JA into 12-OH-JA. Transformation of the quadruple mutant with each JOX gene strongly reduced JA levels, demonstrating that all four JOXs inactivate JA in plants. The in vitro catalysis of 12-OH-JA from JA by recombinant enzyme could be confirmed for three JOXs. The identification of the enzymes responsible for hydroxylation of JA reveals a missing step in JA metabolism, which is important for the inactivation of the hormone and subsequent down-regulation of JA-dependent defenses. SIGNIFICANCE STATEMENTIn plants, the hormone jasmonic acid (JA) is synthesized in response to attack by pathogens and herbivores, leading to activation of defense responses. Rapidly following JA accumulation, the hormone is metabolized, presumably to prevent inhibitive effects of high JA levels on growth and development. The enzymes that directly inactivate JA were so far unknown. Here, we identify four jasmonate-induced oxygenases (JOXs) in Arabidopsis that hydroxylate jasmonic acid to form inactive 12-OH-JA. A mutant that no longer produces the four enzymes hyperaccumulates JA, exhibits reduced growth, and is highly resistant to attackers that are sensitive to JA-dependent defense. The JOX enzymes thus play an important role in determining the amplitude and duration of JA responses to balance the growth-defense tradeoff.peer-reviewed)
Plants detect neighboring competitors through a decrease in the ratio between red and far-red light (R:FR). This decreased R:FR is perceived by phytochrome photoreceptors and triggers shade avoidance responses such as shoot elongation and upward leaf movement (hyponasty). In addition to promoting elongation growth, low R:FR perception enhances plant susceptibility to pathogens: the growth-defense trade-off. Although increased susceptibility in low R:FR has been studied for over a decade, the associated timing of molecular events is still unknown. Here, we studied the chronology of FR-induced susceptibility events in tomato (Solanum lycopersicum) plants pre-exposed to either white light (WL) or WL supplemented with FR light (WL+FR) prior to inoculation with the necrotrophic fungus Botrytis cinerea (B.c.). We monitored the leaf transcriptional changes over a 30-hr time course upon infection and followed up with functional studies to identify mechanisms. We found that FR-induced susceptibility in tomato is linked to a general dampening of B.c.-responsive gene expression, and a delay in both pathogen recognition and jasmonic acid-mediated defense gene expression. In addition, we found that the supplemental FR-induced ethylene emissions affected plant immune responses under the WL+FR condition. This study improves our understanding of the growth–immunity trade-off, while simultaneously providing leads to improve tomato resistance against pathogens in dense cropping systems.
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