Accumulation of salicylic acid and PR-1 gene transcripts in relation to the systemic acquired resistance (SAR) response induced by Pseudomonas syringae pv. tomato in Arabidopsis

Systemic acquired resistance (SAR) is an induced defense response that confers long-lasting protection against a broad range of microbial pathogens. Here we show that treatment of Brassica napus plants with the SAR-inducing chemical benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester (BTH) significantly enhanced resistance against virulent strains of the bacterial pathogen Pseudomonas syringae pv. maculicola and the fungal pathogen Leptosphaeria maculans. Localized preinoculation of plants with an avirulent strain of P. syringae pv. maculicola also enhanced resistance to these pathogens but was not as effective as BTH treatment. Single applications of either SAR-inducing pretreatment were effective against P. syringae pv. maculicola, even when given more than 3 weeks prior to the secondary challenge. The pretreatments also led to the accumulation of pathogenesis-related (PR) genes, including BnPR-1 and BnPR-2, with higher levels of transcripts observed in the BTH-treatment material. B. napus plants expressing a bacterial salicylate hydroxylase transgene (NahG) that metabolizes salicylic acid to catechol were substantially compromised in SAR and accumulated reduced levels of PR gene transcripts when compared with untransformed controls. Thus, SAR in B. napus displays many of the hallmarks of classical SAR including long lasting and broad host range resistance, association with PR gene activation, and a requirement for salicylic acid.

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Signaling Crosstalk between Salicylic Acid and Ethylene/Jasmonate in Plant Defense: Do We Understand What They Are Whispering?

International Journal of Molecular Sciences ◽

10.3390/ijms20030671 ◽

2019 ◽

Vol 20 (3) ◽

pp. 671 ◽

Cited By ~ 44

Author(s):

Ning Li ◽

Xiao Han ◽

Dan Feng ◽

Deyi Yuan ◽

Li-Jun Huang

Keyword(s):

Salicylic Acid ◽

Signaling Pathways ◽

Pseudomonas Syringae ◽

Defense Response ◽

Systemic Acquired Resistance ◽

Acquired Resistance ◽

Defense Responses ◽

Host Cells ◽

Defense Gene Expression ◽

Signaling Crosstalk

During their lifetime, plants encounter numerous biotic and abiotic stresses with diverse modes of attack. Phytohormones, including salicylic acid (SA), ethylene (ET), jasmonate (JA), abscisic acid (ABA), auxin (AUX), brassinosteroid (BR), gibberellic acid (GA), cytokinin (CK) and the recently identified strigolactones (SLs), orchestrate effective defense responses by activating defense gene expression. Genetic analysis of the model plant Arabidopsis thaliana has advanced our understanding of the function of these hormones. The SA- and ET/JA-mediated signaling pathways were thought to be the backbone of plant immune responses against biotic invaders, whereas ABA, auxin, BR, GA, CK and SL were considered to be involved in the plant immune response through modulating the SA-ET/JA signaling pathways. In general, the SA-mediated defense response plays a central role in local and systemic-acquired resistance (SAR) against biotrophic pathogens, such as Pseudomonas syringae, which colonize between the host cells by producing nutrient-absorbing structures while keeping the host alive. The ET/JA-mediated response contributes to the defense against necrotrophic pathogens, such as Botrytis cinerea, which invade and kill hosts to extract their nutrients. Increasing evidence indicates that the SA- and ET/JA-mediated defense response pathways are mutually antagonistic.

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Arabidopsis thaliana EDS4 Contributes to Salicylic Acid (SA)-Dependent Expression of Defense Responses: Evidence for Inhibition of Jasmonic Acid Signaling by SA

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi.2000.13.5.503 ◽

2000 ◽

Vol 13 (5) ◽

pp. 503-511 ◽

Cited By ~ 114

Author(s):

Vaijayanti Gupta ◽

Michael G. Willits ◽

Jane Glazebrook

Keyword(s):

Gene Expression ◽

Salicylic Acid ◽

Jasmonic Acid ◽

Pseudomonas Syringae ◽

Systemic Acquired Resistance ◽

Acquired Resistance ◽

Defense Responses ◽

Avirulence Gene ◽

Signal Molecule ◽

Resistance Response

The Arabidopsis enhanced disease susceptibility 4 (eds4) mutation causes enhanced susceptibility to infection by the bacterial pathogen Pseudomonas syringae pv. Maculicola ES4326 (Psm ES4326). Gene-for-gene resistance to bacteria carrying the avirulence gene avrRpt2 is not significantly affected by eds4. Plants homozygous for eds4 exhibit reduced expression of the pathogenesis-related gene PR-1 after infection by Psm ES4326, weakened responses to treatment with the signal molecule salicylic acid (SA), impairment of the systemic acquired resistance response, and reduced accumulation of SA after infection with Psm ES4326. These phenotypes indicate that EDS4 plays a role in SA-dependent signaling. SA has been shown to have a negative effect on activation of gene expression by the signal molecule jasmonic acid (JA). Two mutations that cause reduced SA levels, eds4 and pad4, cause heightened responses to inducers of JA-dependent gene expression, providing genetic evidence to support the idea that SA interferes with JA-dependent signaling. Two possible working models of the role of EDS4 in governing activation of defense responses are presented.

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Altering Expression of Benzoic Acid/Salicylic Acid Carboxyl Methyltransferase 1 Compromises Systemic Acquired Resistance and PAMP-Triggered Immunity in Arabidopsis

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-23-1-0082 ◽

2010 ◽

Vol 23 (1) ◽

pp. 82-90 ◽

Cited By ~ 55

Author(s):

Po-Pu Liu ◽

Yue Yang ◽

Eran Pichersky ◽

Daniel F. Klessig

Keyword(s):

Salicylic Acid ◽

Benzoic Acid ◽

Pseudomonas Syringae ◽

Systemic Acquired Resistance ◽

Transgenic Arabidopsis ◽

Acquired Resistance ◽

Pathogen Infection ◽

Carboxyl Methyltransferase ◽

Effector Triggered Immunity ◽

Methyltransferase 1

Methyl salicylate (MeSA), which is synthesized in plants from salicylic acid (SA) by methyltransferases, has roles in defense against microbial and insect pests. Most of the MeSA that accumulates after pathogen attack is synthesized by benzoic acid/SA carboxyl methyltransferase 1 (AtBSMT1). To investigate the role of AtBSMT1 in plant defense, transgenic Arabidopsis with altered AtBSMT1 function or expression were assessed for their ability to resist pathogen infection. A knockout mutant (Atbsmt1) failed to accumulate MeSA following pathogen infection; these plants also failed to accumulate SA or its glucoside in the uninoculated leaves and did not develop systemic acquired resistance (SAR). However, the Atbsmt1 mutant exhibited normal levels of effector-triggered immunity and pathogen-associated molecular pattern (PAMP)-triggered immunity to Pseudomonas syringae and Hyaloperonospora arabidopsidis. Analyses of transgenic Arabidopsis plants overexpressing AtBSMT1 revealed that they accumulate elevated levels of MeSA in pathogen-infected leaves but fail to develop SAR. Since the levels of SA and its glucoside were reduced in uninoculated systemic leaves of these plants whereas MeSA levels were elevated, AtBSMT1-mediated conversion of SA to MeSA probably compromised SAR development by suppressing SA accumulation in uninoculated leaves. PAMP-triggered immunity also was compromised in the AtBSMT1 overexpressing plants, although effector-triggered immunity was not.

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Role of Salicylic Acid and NIM1/NPR1 in Race-Specific Resistance in Arabidopsis

Genetics ◽

10.1093/genetics/161.2.803 ◽

2002 ◽

Vol 161 (2) ◽

pp. 803-811

Author(s):

Gregory J Rairdan ◽

Terrence P Delaney

Keyword(s):

Salicylic Acid ◽

Pseudomonas Syringae ◽

Leucine Zipper ◽

Systemic Acquired Resistance ◽

Specific Resistance ◽

Strong Dependence ◽

Acquired Resistance ◽

R Genes ◽

Resistance Response

Abstract Salicylic acid (SA) and the NIM1/NPR1 protein have both been demonstrated to be required for systemic acquired resistance (SAR) and implicated in expression of race-specific resistance. In this work, we analyzed the role that each of these molecules play in the resistance response triggered by members of two subclasses of resistance (R) genes, members of which recognize unrelated pathogens. We tested the ability of TIR and coiled-coil-class (also known as leucine-zipper-class) R genes to confer resistance to Pseudomonas syringae pv. tomato or Peronospora parasitica in SA-depleted (NahG) and nim1/npr1 plants. We found that all of the P. syringae pv. tomato-specific R genes tested were dependent upon SA accumulation, while none showed strong dependence upon NIM1/NPR1 activity. A similar SA dependence was observed for the P. parasitica TIR and CC-class R genes RPP5 and RPP8, respectively. However, the P. parasitica-specific R genes differed in their requirement for NIM1/NPR1, with just RPP5 depending upon NIM1/NPR1 activity for effectiveness. These data are consistent with the hypothesis that at least in Arabidopsis, SA accumulation is necessary for the majority of R-gene-triggered resistance, while the role of NIM1/NPR in race-specific resistance is limited to resistance to P. parasitica mediated by TIR-class R genes.

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Disclosure of salicylic acid and jasmonic acid-responsive genes provides a molecular tool for deciphering stress responses in soybean

Scientific Reports ◽

10.1038/s41598-021-00209-6 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Sebastian F. Beyer ◽

Paloma Sánchez Bel ◽

Victor Flors ◽

Holger Schultheiss ◽

Uwe Conrath ◽

...

Keyword(s):

Salicylic Acid ◽

Jasmonic Acid ◽

Stress Responses ◽

Systemic Acquired Resistance ◽

Marker Gene ◽

Acquired Resistance ◽

Wound Response ◽

Marker Genes ◽

Biotrophic Pathogens ◽

Gene Transcripts

AbstractHormones orchestrate the physiology of organisms. Measuring the activity of defense hormone-responsive genes can help understanding immune signaling and facilitate breeding for plant health. However, different from model species like Arabidopsis, genes that respond to defense hormones salicylic acid (SA) and jasmonic acid (JA) have not been disclosed in the soybean crop. We performed global transcriptome analyses to fill this knowledge gap. Upon exogenous application, endogenous levels of SA and JA increased in leaves. SA predominantly activated genes linked to systemic acquired resistance and defense signaling whereas JA mainly activated wound response-associated genes. In general, SA-responsive genes were activated earlier than those responding to JA. Consistent with the paradigm of biotrophic pathogens predominantly activating SA responses, free SA and here identified most robust SA marker genes GmNIMIN1, GmNIMIN1.2 and GmWRK40 were induced upon inoculation with Phakopsora pachyrhizi, whereas JA marker genes did not respond to infection with the biotrophic fungus. Spodoptera exigua larvae caused a strong accumulation of JA-Ile and JA-specific mRNA transcripts of GmBPI1, GmKTI1 and GmAAT whereas neither free SA nor SA-marker gene transcripts accumulated upon insect feeding. Our study provides molecular tools for monitoring the dynamic accumulation of SA and JA, e.g. in a given stress condition.

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Disclosure of Salicylic Acid and Jasmonic Acid-responsive Genes Provides a Molecular Tool for Deciphering Stress Responses in Soybean

10.21203/rs.3.rs-579376/v1 ◽

2021 ◽

Author(s):

Sebastian F. Beyer ◽

Paloma Sánchez Bel ◽

Victor Flors ◽

Holger Schutheiss ◽

Uwe Conrath ◽

...

Keyword(s):

Salicylic Acid ◽

Jasmonic Acid ◽

Stress Responses ◽

Systemic Acquired Resistance ◽

Marker Gene ◽

Acquired Resistance ◽

Wound Response ◽

Marker Genes ◽

Biotrophic Pathogens ◽

Gene Transcripts

Abstract Hormones orchestrate the physiology of organisms. Measuring the activity of defense hormone-responsive genes can help understanding immune signaling and facilitate breeding for plant health. However, different from model species like Arabidopsis, genes that respond to defense hormones salicylic acid (SA) and jasmonic acid (JA) have not been disclosed in the soybean crop. We performed global transcriptome analyses to fill this knowledge gap. Upon exogenous application, endogenous levels of SA and JA increased in leaves. SA predominantly activated genes linked to systemic acquired resistance and defense signaling whereas JA mainly activated wound response-associated genes. In general, SA-responsive genes were activated earlier than those responding to JA. Consistent with the paradigm of biotrophic pathogens predominantly activating SA responses, free SA and here identified most robust SA marker genes GmNIMIN1, GmNIMIN1.2 and GmWRK40 were induced upon inoculation with Phakopsora pachyrhizi, whereas JA marker genes did not respond to infection with the biotrophic fungus. Spodoptera exigua larvae caused a strong accumulation of JA-Ile and JA-specific mRNA transcripts of GmBPI1, GmKTI1 and GmAAT whereas neither free SA nor SA-marker gene transcripts accumulated upon insect feeding. Our study provides molecular tools for monitoring the dynamic accumulation of SA and JA, e.g. in a given stress condition.

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A Key Role for the Arabidopsis WIN3 Protein in Disease Resistance Triggered by Pseudomonas syringae That Secrete AvrRpt2

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-20-10-1192 ◽

2007 ◽

Vol 20 (10) ◽

pp. 1192-1200 ◽

Cited By ~ 44

Author(s):

Min Woo Lee ◽

Hua Lu ◽

Ho Won Jung ◽

Jean T. Greenberg

Keyword(s):

Salicylic Acid ◽

Pseudomonas Syringae ◽

Pathogenic Bacteria ◽

Systemic Acquired Resistance ◽

Acquired Resistance ◽

Coiled Coil ◽

Firefly Luciferase ◽

Effector Proteins ◽

Infection Site ◽

Hypersensitive Cell Death

Effector proteins injected by the pathogenic bacteria Pseudomonas syringae into plants can have profound effects on the pathogen–host interaction due to their efficient recognition by plants and the subsequent triggering of defenses. The AvrRpt2 effector triggers strong local and systemic defense (called systemic acquired resistance [SAR]) responses in Arabidopsis thaliana plants that harbor a functional RPS2 gene that encodes an R protein in the coiled-coil, nucleotide-binding domain, leucine-rich repeat class. The newly identified win3-T mutant shows greatly reduced resistance to P. syringae carrying avrRpt2. In win3-T plants, RIN4 cleavage, an early AvrRpt2-induced event, is normal. However, salicylic acid accumulation is compromised, as is SAR induction and the local hypersensitive cell death response after infection by P. syringae carrying avrRpt2. WIN3 encodes a member of the firefly luciferase protein superfamily. Expression of WIN3 at an infection site partially requires PAD4, a protein known to play a quantitative role in RPS2-mediated signaling. WIN3 expression in tissue distal to an infection site requires multiple salicylic acid regulatory genes. Finally, win3-T plants show modestly increased susceptibility to virulent P. syringae and modestly reduced SAR in response to P. syringae carrying avrRpm1. Thus, WIN3 is a key element of the RPS2 defense response pathway and a basal and systemic defense component.

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Sulfur-Induced Resistance against Pseudomonas syringae pv. actinidiae via Triggering Salicylic Acid Signaling Pathway in Kiwifruit

International Journal of Molecular Sciences ◽

10.3390/ijms222312710 ◽

2021 ◽

Vol 22 (23) ◽

pp. 12710

Author(s):

Zhuzhu Zhang ◽

Youhua Long ◽

Xianhui Yin ◽

Sen Yang

Keyword(s):

Salicylic Acid ◽

Signaling Pathway ◽

Induced Resistance ◽

Pseudomonas Syringae ◽

Plant Disease Resistance ◽

Plant Pathogens ◽

Systemic Acquired Resistance ◽

Lignin Content ◽

Acquired Resistance ◽

Salicylic Acid Signaling

Sulfur has been previously reported to modulate plant growth and exhibit significant anti-microbial activities. However, the mechanism underlying its diverse effects on plant pathogens has not been elucidated completely. The present study conducted the two-year field experiment of sulfur application to control kiwifruit canker from 2017 to 2018. For the first time, our study uncovered activation of plant disease resistance by salicylic acid after sulfur application in kiwifruit. The results indicated that when the sulfur concentration was 1.5–2.0 kg m−3, the induced effect of kiwifruit canker reached more than 70%. Meanwhile, a salicylic acid high lever was accompanied by the decline of jasmonic acid. Further analysis revealed the high expression of the defense gene, especially AcPR-1, which is a marker of the salicylic acid signaling pathway. Additionally, AcICS1, another critical gene of salicylic acid synthesis, was also highly expressed. All contributed to the synthesis of increasing salicylic acid content in kiwifruit leaves. Moreover, the first key lignin biosynthetic AcPAL gene was marked up-regulated. Thereafter, accumulation of lignin content in the kiwifruit stem and the higher deposition of lignin were visible in histochemical analysis. Moreover, the activity of the endochitinase activity of kiwifruit leaves increased significantly. We suggest that the sulfur-induced resistance against Pseudomonas syringae pv. actinidiae via salicylic activates systemic acquired resistance to enhance plant immune response in kiwifruit.

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Arabidopsismlo3mutant plants exhibit spontaneous callose deposition and signs of early leaf senescence

10.1101/558122 ◽

2019 ◽

Cited By ~ 1

Author(s):

Stefan Kusch ◽

Susanne Thiery ◽

Anja Reinstädler ◽

Katrin Gruner ◽

Krzysztof Zienkiewicz ◽

...

Keyword(s):

Salicylic Acid ◽

Powdery Mildew ◽

Pseudomonas Syringae ◽

Systemic Acquired Resistance ◽

Acquired Resistance ◽

Bacterial Pathogen ◽

Resistance Locus ◽

Callose Deposition ◽

Powdery Mildew Fungi ◽

Hyaloperonospora Arabidopsidis

The family of Mildew resistance Locus O (MLO) proteins is best known for its profound effect on the outcome of powdery mildew infections: when the appropriate MLO protein is absent, the plant is fully resistant to otherwise virulent powdery mildew fungi. However, most members of the MLO protein family remain functionally unexplored. Here, we investigateArabidopsis thaliana MLO3, the closest relative ofAtMLO2, AtMLO6andAtMLO12, which are the ArabidopsisMLOgenes implicated in the powdery mildew interaction. The co-expression network ofAtMLO3suggests association of the gene with plant defense-related processes such as salicylic acid homeostasis. Our extensive analysis shows thatmlo3mutants are unaffected regarding their infection phenotype upon challenge with the powdery mildew fungiGolovinomyces orontiiandErysiphe pisi, the oomyceteHyaloperonospora arabidopsidis, and the bacterial pathogenPseudomonas syringae(the latter both in terms of basal and systemic acquired resistance), indicating that the protein does not play a major role in the response to any of these pathogens. However,mlo3genotypes display spontaneous callose deposition as well as signs of early senescence in six-or seven-week-old rosette leaves in the absence of any pathogen challenge, a phenotype that is reminiscent ofmlo2mutant plants. We hypothesize that de-regulated callose deposition inmlo3genotypes is the result of a subtle transient aberration of salicylic acid-jasmonic acid homeostasis during development.

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