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

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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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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Armet, an aphid effector protein, induces pathogen resistance in plants by promoting the accumulation of salicylic acid

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2018.0314 ◽

2019 ◽

Vol 374 (1767) ◽

pp. 20180314 ◽

Cited By ~ 12

Author(s):

Na Cui ◽

Hong Lu ◽

Tianzuo Wang ◽

Wenhao Zhang ◽

Le Kang ◽

...

Keyword(s):

Salicylic Acid ◽

Pseudomonas Syringae ◽

Plant Pathogen ◽

Bacterial Pathogen ◽

Pathogen Resistance ◽

Effector Proteins ◽

Mitogen Activated Protein Kinase ◽

Effector Protein ◽

Plant Interactions ◽

Fourfold Increase

Effector proteins present in aphid saliva are thought to modulate aphid–plant interactions. Armet, an effector protein, is found in the phloem sap of pea-aphid-infested plants and is indispensable for the survival of aphids on plants. However, its function in plants has not been investigated. Here, we explored the functions of Armet after delivery into plants. Examination of the transcriptomes of Nicotiana benthamiana and Medicago truncatula following transgenic expression of Armet or infiltration of the protein showed that Armet activated pathways associated with plant–pathogen interactions, mitogen-activated protein kinase and salicylic acid (SA). Armet induced a fourfold increase in SA accumulation by regulating the expression of SAMT and SABP2 , two genes associated with SA metabolism, in Armet-infiltrated tobacco. The increase in SA enhanced the plants' resistance to bacterial pathogen Pseudomonas syringae but had no detectable adverse effects on aphid survival or reproduction. Similar molecular responses and a chlorosis phenotype were induced in tobacco by Armet from two aphid species but not by locust Armet, suggesting that the effector function of Armet may be specific for aphids. The results suggest that Armet causes plants to make a pathogen-resistance decision and reflect a novel tripartite insect–plant–pathogen interaction. This article is part of the theme issue ‘Biotic signalling sheds light on smart pest management’.

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Identification of Arabidopsis Mutants Exhibiting an Altered Hypersensitive Response in Gene-for-Gene Disease Resistance

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi.2000.13.3.277 ◽

2000 ◽

Vol 13 (3) ◽

pp. 277-286 ◽

Cited By ~ 37

Author(s):

I-ching Yu ◽

Kevin A. Fengler ◽

Steven J. Clough ◽

Andrew F. Bent

Keyword(s):

Salicylic Acid ◽

Disease Resistance ◽

Pseudomonas Syringae ◽

Hypersensitive Response ◽

Growth Defects ◽

Lesion Mimic ◽

Pathogenesis Related ◽

Lesion Mimic Mutant ◽

Mutant Phenotypes ◽

Temporally Correlated

A mutational study was carried out to isolate Arabidopsis thaliana plants that exhibit full or partial disruption of the RPS2-mediated hypersensitive response (HR) to Pseudomonas syringae that express avrRpt2. Five classes of mutants were identified including mutations at RPS2, dnd mutations causing a “defense, no death” loss-of-HR phenotype, a lesion-mimic mutant that also exhibited an HR¯phenotype, and a number of intermediate or partial-loss-of-HR mutants. Surprisingly, many of these mutants displayed elevated resistance to virulent P. syringae and, in some cases, to Peronospora parasitica. Constitutively elevated levels of pathogenesis-related (PR) gene expression and salicylic acid were also observed. In the lesion-mimic mutant, appearance of elevated resistance was temporally correlated with appearance of lesions. For one of the intermediate lines, resistance was shown to be dependent on elevated levels of salicylic acid. A new locus was identified and named IHR1, after the mutant phenotype of “intermediate HR.” Genetic analysis of the intermediate-HR plant lines was difficult due to uncertainties in distinguishing the partial/intermediate mutant phenotypes from wild type. Despite this difficulty, the intermediate-HR mutants remain of interest because they reveal potential new defense-related loci and because many of these lines exhibit partially elevated disease resistance without dwarfing or other apparent growth defects.

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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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WRKY55 transcription factor positively regulates leaf senescence and the defense response by modulating the transcription of genes implicated in the biosynthesis of reactive oxygen species and salicylic acid in Arabidopsis

Development ◽

10.1242/dev.189647 ◽

2020 ◽

Vol 147 (16) ◽

pp. dev189647

Author(s):

Yiqiao Wang ◽

Xing Cui ◽

Bo Yang ◽

Shutao Xu ◽

Xiangyan Wei ◽

...

Keyword(s):

Reactive Oxygen Species ◽

Transcription Factor ◽

Salicylic Acid ◽

Pseudomonas Syringae ◽

Leaf Senescence ◽

Single Gene ◽

Bacterial Pathogen ◽

Reactive Oxygen ◽

Pathogen Resistance ◽

Oxygen Species

ABSTRACTReactive oxygen species (ROS) and salicylic acid (SA) are two factors regulating leaf senescence and defense against pathogens. However, how a single gene integrates both ROS and SA pathways remains poorly understood. Here, we show that Arabidopsis WRKY55 transcription factor positively regulates ROS and SA accumulation, and thus leaf senescence and resistance against the bacterial pathogen Pseudomonas syringae. WRKY55 is predominantly expressed in senescent leaves and encodes a transcriptional activator localized to nuclei. Both inducible and constitutive overexpression of WRKY55 accelerates leaf senescence, whereas mutants delay it. Transcriptomic sequencing identified 1448 differentially expressed genes, of which 1157 genes are upregulated by WRKY55 expression. Accordingly, the ROS and SA contents in WRKY55-overexpressing plants are higher than those in control plants, whereas the opposite occurs in mutants. Moreover, WRKY55 positively regulates defense against P. syringae. Finally, we show that WRKY55 activates the expression of RbohD, ICS1, PBS3 and SAG13 by binding directly to the W-box-containing fragments. Taken together, our work has identified a new WRKY transcription factor that integrates both ROS and SA pathways to regulate leaf senescence and pathogen resistance.

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Salicylic acid biosynthesis is enhanced and contributes to increased biotrophic pathogen resistance in Arabidopsis hybrids

Nature Communications ◽

10.1038/ncomms8309 ◽

2015 ◽

Vol 6 (1) ◽

Cited By ~ 35

Author(s):

Li Yang ◽

Bosheng Li ◽

Xiao-yu Zheng ◽

Jigang Li ◽

Mei Yang ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Salicylic Acid ◽

Pseudomonas Syringae ◽

Histone H3 ◽

Bacterial Pathogen ◽

Pathogen Resistance ◽

Biosynthesis Pathway ◽

Acid Biosynthesis ◽

Histone H3 Acetylation ◽

H3 Acetylation

Abstract Heterosis, the phenotypic superiority of a hybrid over its parents, has been demonstrated for many traits in Arabidopsis thaliana, but its effect on defence remains largely unexplored. Here, we show that hybrids between some A. thaliana accessions show increased resistance to the biotrophic bacterial pathogen Pseudomonas syringae pv. tomato (Pst) DC3000. Comparisons of transcriptomes between these hybrids and their parents after inoculation reveal that several key salicylic acid (SA) biosynthesis genes are significantly upregulated in hybrids. Moreover, SA levels are higher in hybrids than in either parent. Increased resistance to Pst DC3000 is significantly compromised in hybrids of pad4 mutants in which the SA biosynthesis pathway is blocked. Finally, increased histone H3 acetylation of key SA biosynthesis genes correlates with their upregulation in infected hybrids. Our data demonstrate that enhanced activation of SA biosynthesis in A. thaliana hybrids may contribute to their increased resistance to a biotrophic bacterial pathogen.

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Salicylic Acid Accumulation Controlled by LSD1 Is Essential in Triggering Cell Death in Response to Abiotic Stress

Cells ◽

10.3390/cells10040962 ◽

2021 ◽

Vol 10 (4) ◽

pp. 962

Author(s):

Maciej Jerzy Bernacki ◽

Anna Rusaczonek ◽

Weronika Czarnocka ◽

Stanisław Karpiński

Keyword(s):

Cell Death ◽

Salicylic Acid ◽

Abiotic Stress ◽

Wild Type ◽

Pr Genes ◽

Genes Expression ◽

Salicylic Acid Accumulation ◽

Cell Death Phenotype ◽

Insight Into

Salicylic acid (SA) is well known hormonal molecule involved in cell death regulation. In response to a broad range of environmental factors (e.g., high light, UV, pathogens attack), plants accumulate SA, which participates in cell death induction and spread in some foliar cells. LESION SIMULATING DISEASE 1 (LSD1) is one of the best-known cell death regulators in Arabidopsis thaliana. The lsd1 mutant, lacking functional LSD1 protein, accumulates SA and is conditionally susceptible to many biotic and abiotic stresses. In order to get more insight into the role of LSD1-dependent regulation of SA accumulation during cell death, we crossed the lsd1 with the sid2 mutant, caring mutation in ISOCHORISMATE SYNTHASE 1(ICS1) gene and having deregulated SA synthesis, and with plants expressing the bacterial nahG gene and thus decomposing SA to catechol. In response to UV A+B irradiation, the lsd1 mutant exhibited clear cell death phenotype, which was reversed in lsd1/sid2 and lsd1/NahG plants. The expression of PR-genes and the H2O2 content in UV-treated lsd1 were significantly higher when compared with the wild type. In contrast, lsd1/sid2 and lsd1/NahG plants demonstrated comparability with the wild-type level of PR-genes expression and H2O2. Our results demonstrate that SA accumulation is crucial for triggering cell death in lsd1, while the reduction of excessive SA accumulation may lead to a greater tolerance toward abiotic stress.

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Systemic Acquired Resistance in Canola Is Linked with Pathogenesis-Related Gene Expression and Requires Salicylic Acid

Phytopathology ◽

10.1094/phyto-97-7-0794 ◽

2007 ◽

Vol 97 (7) ◽

pp. 794-802 ◽

Cited By ~ 29

Author(s):

Shobha D. Potlakayala ◽

Darwin W. Reed ◽

Patrick S. Covello ◽

Pierre R. Fobert

Keyword(s):

Salicylic Acid ◽

Pseudomonas Syringae ◽

Systemic Acquired Resistance ◽

Induced Defense ◽

Acquired Resistance ◽

Microbial Pathogens ◽

Broad Host Range ◽

Avirulent Strain ◽

Enhanced Resistance ◽

Pathogenesis Related

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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A 2′-O-Methyltransferase Responsible for Transfer RNA Anticodon Modification Is Pivotal for Resistance to Pseudomonas syringae DC3000 in Arabidopsis

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-06-18-0148-r ◽

2018 ◽

Vol 31 (12) ◽

pp. 1323-1336 ◽

Cited By ~ 2

Author(s):

Vicente Ramírez ◽

Beatriz González ◽

Ana López ◽

Maria Jose Castelló ◽

Maria José Gil ◽

...

Keyword(s):

Disease Resistance ◽

Pseudomonas Syringae ◽

Bacterial Pathogen ◽

Transfer Rna ◽

Resistance Response ◽

Chemical Structures ◽

Trna Modifications ◽

Trna Species ◽

Living Organisms ◽

And Function

Transfer RNA (tRNA) is the most highly modified class of RNA species in all living organisms. Recent discoveries have revealed unprecedented complexity in the tRNA chemical structures, modification patterns, regulation, and function, suggesting that each modified nucleoside in tRNA may have its own specific function. However, in plants, our knowledge of the role of individual tRNA modifications and how they are regulated is very limited. In a genetic screen designed to identify factors regulating disease resistance in Arabidopsis, we identified SUPPRESSOR OF CSB3 9 (SCS9). Our results reveal SCS9 encodes a tRNA methyltransferase that mediates the 2′-O-ribose methylation of selected tRNA species in the anticodon loop. These SCS9-mediated tRNA modifications enhance susceptibility during infection with the virulent bacterial pathogen Pseudomonas syringae DC3000. Lack of such tRNA modification, as observed in scs9 mutants, specifically dampens plant resistance against DC3000 without compromising the activation of the salicylic acid signaling pathway or the resistance to other biotrophic pathogens. Our results support a model that gives importance to the control of certain tRNA modifications for mounting an effective disease resistance in Arabidopsis toward DC3000 and, therefore, expands the repertoire of molecular components essential for an efficient disease resistance response.

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The Arabidopsis Hypoxia Inducible AtR8 Long Non-Coding RNA also Contributes to Plant Defense and Root Elongation Coordinating with WRKY Genes under Low Levels of Salicylic Acid

Non-Coding RNA ◽

10.3390/ncrna6010008 ◽

2020 ◽

Vol 6 (1) ◽

pp. 8

Author(s):

Shuang Li ◽

Saraswati Nayar ◽

HuiYuan Jia ◽

Sanjay Kapoor ◽

Juan Wu ◽

...

Keyword(s):

Salicylic Acid ◽

Pseudomonas Syringae ◽

Root Elongation ◽

Early Stage ◽

Flowering Plant ◽

Stage Of Development ◽

Non Coding Rna ◽

Pathogenesis Related ◽

Low Levels ◽

Long Non Coding Rna

AtR8 lncRNA was previously identified in the flowering plant Arabidopsis thaliana as an abundant Pol III-transcribed long non-coding RNA (lncRNA) of approximately 260 nt. AtR8 lncRNA accumulation is responsive to hypoxic stress and salicylic acid (SA) treatment in roots, but its function has not yet been identified. In this study, microarray analysis of an atr8 mutant and wild-type Arabidopsis indicated a strong association of AtR8 lncRNA with the defense response. AtR8 accumulation exhibited an inverse correlation with an accumulation of two WRKY genes (WRKY53/WRKY70) when plants were exposed to exogenous low SA concentrations (20 µM), infected with Pseudomonas syringae, or in the early stage of development. The highest AtR8 accumulation was observed 5 days after germination, at which time no WRKY53 or WRKY70 mRNA was detectable. The presence of low levels of SA resulted in a significant reduction of root length in atr8 seedlings, whereas wrky53 and wrky70 mutants exhibited the opposite phenotype. Taken together, AtR8 lncRNA participates in Pathogenesis-Related Proteins 1 (PR-1)-independent defense and root elongation, which are related to the SA response. The mutual regulation of AtR8 lncRNA and WRKY53/WRKY70 is mediated by Nonexpressor of Pathogenesis-Related Gene 1 (NPR1).

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