Constitutive Activation of Jasmonate Signaling in an Arabidopsis Mutant Correlates with Enhanced Resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae

In Arabidopsis spp., the jasmonate (JA) response pathway generally is required for defenses against necrotrophic pathogens and chewing insects, while the salicylic acid (SA) response pathway is generally required for specific, resistance (R) gene-mediated defenses against both biotrophic and necrotrophic pathogens. For example, SA-dependent defenses are required for resistance to the biotrophic fungal pathogen Erysiphe cichoracearum UCSC1 and the bacterial pathogen Pseudomonas syringae pv. maculicola, and also are expressed during response to the green peach aphid Myzus persicae. However, recent evidence indicates that the expression of JA-dependent defenses also may confer resistance to E. cichoracearum. To confirm and to extend this observation, we have compared the disease and pest resistance of wild-type Arabidopsis plants with that of the mutants coi1, which is insensitive to JA, and cev1, which has constitutive JA signaling. Measurements of the colonization of these plants by E. cichoracearum, P. syringae pv. maculicola, and M. persicae indicated that activation of the JA signal pathway enhanced resistance, and was associated with the activation of JA-dependent defense genes and the suppression of SA-dependent defense genes. We conclude that JA and SA induce alternative defense pathways that can confer resistance to the same pathogens and pests.

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Uncoupling Salicylic Acid-Dependent Cell Death and Defense-Related Responses From Disease Resistance in the Arabidopsis Mutant acd5

Genetics ◽

10.1093/genetics/156.1.341 ◽

2000 ◽

Vol 156 (1) ◽

pp. 341-350

Author(s):

Jean T Greenberg ◽

F Paul Silverman ◽

Hua Liang

Keyword(s):

Cell Death ◽

Salicylic Acid ◽

Disease Resistance ◽

Pseudomonas Syringae ◽

Higher Plants ◽

Ethylene Signaling ◽

Symptom Development ◽

Wild Type ◽

Dependent Cell ◽

Arabidopsis Mutant

Abstract Salicylic acid (SA) is required for resistance to many diseases in higher plants. SA-dependent cell death and defense-related responses have been correlated with disease resistance. The accelerated cell death 5 mutant of Arabidopsis provides additional genetic evidence that SA regulates cell death and defense-related responses. However, in acd5, these events are uncoupled from disease resistance. acd5 plants are more susceptible to Pseudomonas syringae early in development and show spontaneous SA accumulation, cell death, and defense-related markers later in development. In acd5 plants, cell death and defense-related responses are SA dependent but they do not confer disease resistance. Double mutants with acd5 and nonexpressor of PR1, in which SA signaling is partially blocked, show greatly attenuated cell death, indicating a role for NPR1 in controlling cell death. The hormone ethylene potentiates the effects of SA and is important for disease symptom development in Arabidopsis. Double mutants of acd5 and ethylene insensitive 2, in which ethylene signaling is blocked, show decreased cell death, supporting a role for ethylene in cell death control. We propose that acd5 plants mimic P. syringae-infected wild-type plants and that both SA and ethylene are normally involved in regulating cell death during some susceptible pathogen infections.

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The overexpression of OsACBP5 protects transgenic rice against necrotrophic, hemibiotrophic and biotrophic pathogens

Scientific Reports ◽

10.1038/s41598-020-71851-9 ◽

2020 ◽

Vol 10 (1) ◽

Author(s):

Saritha Panthapulakkal Narayanan ◽

Shiu-Cheung Lung ◽

Pan Liao ◽

Clive Lo ◽

Mee-Len Chye

Keyword(s):

Pseudomonas Syringae ◽

Rice Blast ◽

Transgenic Arabidopsis ◽

Sheath Blight ◽

Xanthomonas Oryzae ◽

Deficient Mutant ◽

Class Iii ◽

Wild Type ◽

Enhanced Resistance ◽

Biotrophic Pathogens

Abstract The most devastating diseases in rice (Oryza sativa) are sheath blight caused by the fungal necrotroph Rhizoctonia solani, rice blast by hemibiotrophic fungus Magnaporthe oryzae, and leaf blight by bacterial biotroph Xanthomonas oryzae (Xoo). It has been reported that the Class III acyl-CoA-binding proteins (ACBPs) such as those from dicots (Arabidopsis and grapevine) play a role in defence against biotrophic pathogens. Of the six Arabidopsis (Arabidopsis thaliana) ACBPs, AtACBP3 conferred protection in transgenic Arabidopsis against Pseudomonas syringae, but not the necrotrophic fungus, Botrytis cinerea. Similar to Arabidopsis, rice possesses six ACBPs, designated OsACBPs. The aims of this study were to test whether OsACBP5, the homologue of AtACBP3, can confer resistance against representative necrotrophic, hemibiotrophic and biotrophic phytopathogens and to understand the mechanisms in protection. Herein, when OsACBP5 was overexpressed in rice, the OsACBP5-overexpressing (OsACBP5-OE) lines exhibited enhanced disease resistance against representative necrotrophic (R. solani & Cercospora oryzae), hemibiotrophic (M. oryzae & Fusarium graminearum) and biotrophic (Xoo) phytopathogens. Progeny from a cross between OsACBP5-OE9 and the jasmonate (JA)-signalling deficient mutant were more susceptible than the wild type to infection by the necrotroph R. solani. In contrast, progeny from a cross between OsACBP5-OE9 and the salicylic acid (SA)-signalling deficient mutant was more susceptible to infection by the hemibiotroph M. oryzae and biotroph Xoo. Hence, enhanced resistance of OsACBP5-OEs against representative necrotrophs appears to be JA-dependent whilst that to (hemi)biotrophs is SA-mediated.

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Characterization of a Novel, Defense-Related Arabidopsis Mutant, cir1, Isolated By Luciferase Imaging

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi.2002.15.6.557 ◽

2002 ◽

Vol 15 (6) ◽

pp. 557-566 ◽

Cited By ~ 32

Author(s):

Shane L. Murray ◽

Catherine Thomson ◽

Andrea Chini ◽

Nick D. Read ◽

Gary J. Loake

Keyword(s):

Signaling Pathways ◽

Pseudomonas Syringae ◽

Constitutive Expression ◽

Bacterial Pathogen ◽

Negative Regulator ◽

Reactive Oxygen Intermediate ◽

Peronospora Parasitica ◽

Tomato Dc3000 ◽

Pathogen Invasion ◽

Arabidopsis Mutant

In order to identify components of the defense signaling network engaged following attempted pathogen invasion, we generated a novel PR-1∷luciferase (LUC) transgenic line that was deployed in an imaging-based screen to uncover defense-related mutants. The recessive mutant designated cir1 exhibited constitutive expression of salicylic acid (SA), jasmonic acid (JA)/ethylene, and reactive oxygen intermediate-dependent genes. Moreover, this mutation conferred resistance against the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 and a virulent oomycete pathogen Peronospora parasitica Noco2. Epistasis analyses were undertaken between cir1 and mutants that disrupt the SA (npr1, nahG), JA (jar1), and ethylene (ET) (ein2) signaling pathways. While resistance against both P. syringae pv. tomato DC3000 and Peronospora parasitica Noco2 was partially reduced by npr1, resistance against both of these pathogens was lost in an nahG genetic background. Hence, cir1-mediated resistance is established via NPR1-dependent and -independent signaling pathways and SA accumulation is essential for the function of both pathways. While jar1 and ein2 reduced resistance against P. syringae pv. tomato DC3000, these mutations appeared not to impact cir1-mediated resistance against Peronospora parasitica Noco2. Thus, JA and ET sensitivity are required for cir1-mediated resistance against P. syringae pv. tomato DC3000 but not Peronospora parasitica Noco2. Therefore, the cir1 mutation may define a negative regulator of disease resistance that operates upstream of SA, JA, and ET accumulation.

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Analyses of wrky18 wrky40 Plants Reveal Critical Roles of SA/EDS1 Signaling and Indole-Glucosinolate Biosynthesis for Golovinomyces orontii Resistance and a Loss-of Resistance Towards Pseudomonas syringae pv. tomato AvrRPS4

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-11-12-0265-r ◽

2013 ◽

Vol 26 (7) ◽

pp. 758-767 ◽

Cited By ~ 58

Author(s):

Moritz Schön ◽

Armin Töller ◽

Celia Diezel ◽

Charlotte Roth ◽

Lore Westphal ◽

...

Keyword(s):

Pseudomonas Syringae ◽

Double Mutant ◽

Bacterial Pathogen ◽

Wild Type ◽

Powdery Mildew Fungus ◽

Golovinomyces Orontii ◽

Transcriptional Reprogramming ◽

Essential Components ◽

Effector Triggered Immunity ◽

Indole Glucosinolate

Simultaneous mutation of two WRKY-type transcription factors, WRKY18 and WRKY40, renders otherwise susceptible wild-type Arabidopsis plants resistant towards the biotrophic powdery mildew fungus Golovinomyces orontii. Resistance in wrky18 wrky40 double mutant plants is accompanied by massive transcriptional reprogramming, imbalance in salicylic acid (SA) and jasmonic acid (JA) signaling, altered ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1) expression, and accumulation of the phytoalexin camalexin. Genetic analyses identified SA biosynthesis and EDS1 signaling as well as biosynthesis of the indole-glucosinolate 4MI3G as essential components required for loss-of-WRKY18 WRKY40–mediated resistance towards G. orontii. The analysis of wrky18 wrky40 pad3 mutant plants impaired in camalexin biosynthesis revealed an uncoupling of pre- from postinvasive resistance against G. orontii. Comprehensive infection studies demonstrated the specificity of wrky18 wrky40–mediated G. orontii resistance. Interestingly, WRKY18 and WRKY40 act as positive regulators in effector-triggered immunity, as the wrky18 wrky40 double mutant was found to be strongly susceptible towards the bacterial pathogen Pseudomonas syringae DC3000 expressing the effector AvrRPS4 but not against other tested Pseudomonas strains. We hypothesize that G. orontii depends on the function of WRKY18 and WRKY40 to successfully infect Arabidopsis wild-type plants while, in the interaction with P. syringae AvrRPS4, they are required to mediate effector-triggered immunity.

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Pseudomonas syringae Elicits Emission of the Terpenoid (E,E)-4,8,12-Trimethyl-1,3,7,11-Tridecatetraene in Arabidopsis Leaves Via Jasmonate Signaling and Expression of the Terpene Synthase TPS4

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-21-11-1482 ◽

2008 ◽

Vol 21 (11) ◽

pp. 1482-1497 ◽

Cited By ~ 21

Author(s):

Elham Attaran ◽

Michael Rostás ◽

Jürgen Zeier

Keyword(s):

Pseudomonas Syringae ◽

Systemic Acquired Resistance ◽

Induced Defense ◽

Acquired Resistance ◽

Bacterial Pathogen ◽

Microbial Pathogens ◽

Terpene Synthase ◽

Knockout Mutant ◽

Direct Role ◽

Ja Signaling

Volatile, low–molecular weight terpenoids have been implicated in plant defenses, but their direct role in resistance against microbial pathogens is not clearly defined. We have examined a possible role of terpenoid metabolism in the induced defense of Arabidopsis thaliana plants against leaf infection with the bacterial pathogen Pseudomonas syringae. Inoculation of plants with virulent or avirulent P. syringae strains induces the emission of the terpenoids (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene (TMTT), β-ionone and α-farnesene. While the most abundant volatile, the C16-homoterpene TMTT, is produced relatively early in compatible and incompatible interactions, emission of both β-ionone and α-farnesene only increases in later stages of the compatible interaction. Pathogen-induced synthesis of TMTT is controlled through jasmonic acid (JA)-dependent signaling but is independent of a functional salicylic acid (SA) pathway. We have identified Arabidopsis T-DNA insertion lines with defects in the terpene synthase gene TPS4, which is expressed in response to P. syringae inoculation. The tps4 knockout mutant completely lacks induced emission of TMTT but is capable of β-ionone and α-farnesene production, demonstrating that TPS4 is specifically involved in TMTT formation. The tps4 plants display at least wild type–like resistance against P. syringae, indicating that TMTT per se does not protect against the bacterial pathogen in Arabidopsis leaves. Similarly, the ability to mount SA-dependent defenses and systemic acquired resistance (SAR) is barely affected in tps4, which excludes a signaling function of TMTT during SAR. Besides P. syringae challenge, intoxication of Arabidopsis leaves with copper sulfate, a treatment that strongly activates JA biosynthesis, triggers production of TMTT, β-ionone, and α-farnesene. Taken together, our data suggest that induced TMTT production in Arabidopsis is a by-product of activated JA signaling, rather than an effective defense response that contributes to resistance against P. syringae.

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Pathogen exploitation of an abscisic acid- and jasmonate-inducible MAPK phosphatase and its interception by Arabidopsis immunity

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1702613114 ◽

2017 ◽

Vol 114 (28) ◽

pp. 7456-7461 ◽

Cited By ~ 42

Author(s):

Akira Mine ◽

Matthias L. Berens ◽

Tatsuya Nobori ◽

Shajahan Anver ◽

Kaori Fukumoto ◽

...

Keyword(s):

Abscisic Acid ◽

Signaling Pathways ◽

Pseudomonas Syringae ◽

Map Kinases ◽

Bacterial Pathogen ◽

Expression Of Genes ◽

Genes Encoding ◽

Signaling Activation ◽

Ja Signaling

Phytopathogens promote virulence by, for example, exploiting signaling pathways mediated by phytohormones such as abscisic acid (ABA) and jasmonate (JA). Some plants can counteract pathogen virulence by invoking a potent form of immunity called effector-triggered immunity (ETI). Here, we report that ABA and JA mediate inactivation of the immune-associated MAP kinases (MAPKs), MPK3 and MPK6, in Arabidopsis thaliana. ABA induced expression of genes encoding the protein phosphatases 2C (PP2Cs), HAI1, HAI2, and HAI3 through ABF/AREB transcription factors. These three HAI PP2Cs interacted with MPK3 and MPK6 and were required for ABA-mediated MPK3/MPK6 inactivation and immune suppression. The bacterial pathogen Pseudomonas syringae pv. tomato (Pto) DC3000 activates ABA signaling and produces a JA-mimicking phytotoxin, coronatine (COR), that promotes virulence. We found that Pto DC3000 induces HAI1 through COR-mediated activation of MYC2, a master transcription factor in JA signaling. HAI1 dephosphorylated MPK3 and MPK6 in vitro and was necessary for COR-mediated suppression of MPK3/MPK6 activation and immunity. Intriguingly, upon ETI activation, A. thaliana plants overcame the HAI1-dependent virulence of COR by blocking JA signaling. Finally, we showed conservation of induction of HAI PP2Cs by ABA and JA in other Brassicaceae species. Taken together, these results suggest that ABA and JA signaling pathways, which are hijacked by the bacterial pathogen, converge on the HAI PP2Cs that suppress activation of the immune-associated MAPKs. Also, our data unveil interception of JA-signaling activation as a host counterstrategy against the bacterial suppression of MAPKs during ETI.

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Ascorbic Acid Deficiency in Arabidopsis Induces Constitutive Priming That is Dependent on Hydrogen Peroxide, Salicylic Acid, and the NPR1 Gene

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-23-3-0340 ◽

2010 ◽

Vol 23 (3) ◽

pp. 340-351 ◽

Cited By ~ 67

Author(s):

Madhumati Mukherjee ◽

Katherine E. Larrimore ◽

Naushin J. Ahmed ◽

Tyler S. Bedick ◽

Nadia T. Barghouthi ◽

...

Keyword(s):

Ascorbic Acid ◽

Salicylic Acid ◽

Disease Resistance ◽

Pseudomonas Syringae ◽

Messenger Rna ◽

Bacterial Pathogen ◽

Pathogen Resistance ◽

Wild Type ◽

Pr Genes ◽

Pathogenesis Related

The ascorbic acid (AA)-deficient Arabidopsis thaliana vtc1-1 mutant exhibits increased resistance to the virulent bacterial pathogen Pseudomonas syringae. This response correlates with heightened levels of salicylic acid (SA), which induces antimicrobial pathogenesis-related (PR) proteins. To determine if SA-mediated, enhanced disease resistance is a general phenomenon of AA deficiency, to elucidate the signal that stimulates SA synthesis, and to identify the biosynthetic pathway through which SA accumulates, we studied the four AA-deficient vtc1-1, vtc2-1, vtc3-1, and vtc4-1 mutants. We also studied double mutants defective in the AA-biosynthetic gene VTC1 and the SA signaling pathway genes PAD4, EDS5, and NPR1, respectively. All vtc mutants were more resistant to P. syringae than the wild type. With the exception of vtc4-1, this correlated with constitutively upregulated H2O2, SA, and messenger RNA levels of PR genes. Double mutants exhibited decreased SA levels and enhanced susceptibility to P. syringae compared with the wild type, suggesting that vtc1-1 requires functional PAD4, EDS5, and NPR1 for SA biosynthesis and pathogen resistance. We suggest that AA deficiency causes constitutive priming through a buildup of H2O2 that stimulates SA accumulation, conferring enhanced disease resistance in vtc1-1, vtc2-1, and vtc3-1, whereas vtc4-1 might be sensitized to H2O2 and SA production after infection.

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Host target modification as a strategy to counter pathogen hijacking of the jasmonate hormone receptor

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1510745112 ◽

2015 ◽

Vol 112 (46) ◽

pp. 14354-14359 ◽

Cited By ~ 34

Author(s):

Li Zhang ◽

Jian Yao ◽

John Withers ◽

Xiu-Fang Xin ◽

Rahul Banerjee ◽

...

Keyword(s):

Pseudomonas Syringae ◽

Virulence Factors ◽

Disease Susceptibility ◽

Bacterial Pathogen ◽

New Approach ◽

Insect Defense ◽

High Level ◽

Ja Signaling ◽

Host Target ◽

Highly Evolved

In the past decade, characterization of the host targets of pathogen virulence factors took a center stage in the study of pathogenesis and disease susceptibility in plants and humans. However, the impressive knowledge of host targets has not been broadly exploited to inhibit pathogen infection. Here, we show that host target modification could be a promising new approach to “protect” the disease-vulnerable components of plants. In particular, recent studies have identified the plant hormone jasmonate (JA) receptor as one of the common targets of virulence factors from highly evolved biotrophic/hemibiotrophic pathogens. Strains of the bacterial pathogenPseudomonas syringae, for example, produce proteinaceous effectors, as well as a JA-mimicking toxin, coronatine (COR), to activate JA signaling as a mechanism to promote disease susceptibility. Guided by the crystal structure of the JA receptor and evolutionary clues, we succeeded in modifying the JA receptor to allow for sufficient endogenous JA signaling but greatly reduced sensitivity to COR. TransgenicArabidopsisexpressing this modified receptor not only are fertile and maintain a high level of insect defense, but also gain the ability to resist COR-producing pathogensPseudomonas syringaepv.tomatoandP. syringaepv.maculicola. Our results provide a proof-of-concept demonstration that host target modification can be a promising new approach to prevent the virulence action of highly evolved pathogens.

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Ectomycorrhizal fungi induce systemic resistance against insects on a non-mycorrhizal plant in a CERK1-dependent manner

10.1101/852640 ◽

2019 ◽

Author(s):

Kishore Vishwanathan ◽

Krzysztof Zienkiewicz ◽

Yang Liu ◽

Dennis Janz ◽

Ivo Feussner ◽

...

Keyword(s):

Pseudomonas Syringae ◽

Trichoplusia Ni ◽

Bacterial Pathogen ◽

Systemic Resistance ◽

Dependent Manner ◽

Induce Systemic Resistance ◽

Mycorrhizal Plant ◽

Plant Host ◽

Mediated Effects ◽

Ja Signaling

ABSTRACTBelow-ground microbes can induce systemic resistance (ISR) against foliar pests and pathogens on diverse plant hosts. The prevalence of ISR among plant-microbe-pest systems raises the question of host specificity in microbial induction of ISR. To test whether ISR is limited by plant host range, we tested the ISR-inducing ectomycorrhizal (ECM) fungus Laccaria bicolor on the non-mycorrhizal plant Arabidopsis. We found that root inoculation with L. bicolor triggered ISR against the insect herbivore Trichoplusia ni and induced systemic susceptibility (ISS) against the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 (Pto). We found that L. bicolor-triggered ISR against T. ni was dependent on jasmonic acid (JA) signaling and salicylic acid (SA) biosynthesis and signaling. We found that heat killed L. bicolor and chitin are sufficient to trigger ISR against T. ni and ISS against Pto and that the chitin receptor CERK1 is necessary for L. bicolor-mediated effects on systemic immunity. Collectively our findings suggest that some ISR responses might not require intimate co-evolution of host and microbe, but rather might be the result of root perception of conserved microbial signals.

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Two Chloroplast-Localized Proteins: AtNHR2A and AtNHR2B, Contribute to Callose Deposition During Nonhost Disease Resistance in Arabidopsis

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-04-18-0094-r ◽

2018 ◽

Vol 31 (12) ◽

pp. 1280-1290 ◽

Cited By ~ 5

Author(s):

Raksha Singh ◽

Seonghee Lee ◽

Laura Ortega ◽

Vemanna S. Ramu ◽

Muthappa Senthil-Kumar ◽

...

Keyword(s):

Disease Resistance ◽

Pseudomonas Syringae ◽

Fluorescent Protein ◽

Bacterial Pathogen ◽

Virus Induced Gene Silencing ◽

Wild Type ◽

Orthologous Genes ◽

Callose Deposition ◽

Complex Process ◽

Physical And Chemical

Plants are naturally resistant to most pathogens through a broad and durable defense response called nonhost disease resistance. Nonhost disease resistance is a complex process that includes preformed physical and chemical barriers and induced responses. In spite of its importance, many components of nonhost disease resistance remain to be identified and characterized. Using virus-induced gene silencing in Nicotiana benthamiana, we discovered a novel gene that we named NbNHR2 (N. benthamiana nonhost resistance 2). NbNHR2-silenced plants were susceptible to the nonadapted pathogen Pseudomonas syringae pv. tomato T1, which does not cause disease in wild-type or nonsilenced N. benthamiana plants. We found two orthologous genes in Arabidopsis thaliana: AtNHR2A and AtNHR2B. Similar to the results obtained in N. benthamiana, Atnhr2a and Atnhr2b mutants were susceptible to the nonadapted bacterial pathogen of A. thaliana, P. syringae pv. tabaci. We further found that these mutants were also defective in callose deposition. AtNHR2A and AtNHR2B fluorescent protein fusions transiently expressed in N. benthamiana localized predominantly to chloroplasts and a few unidentified dynamic puncta. RFP-AtNHR2A and AtNHR2B-GFP displayed overlapping signals in chloroplasts, indicating that the two proteins could interact, an idea supported by coimmunoprecipitation studies. We propose that AtNHR2A and AtNHR2B are new components of a chloroplast-signaling pathway that activates callose deposition to the cell wall in response to bacterial pathogens.

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