Rust effector PNPi interacting with wheat TaPR1a attenuates plant defense response

Abstract NPR1 is a key regulator of systemic acquired resistance (SAR) in plant species. In our previous study, we identified a conserved fungal effector PNPi from Puccinia striiformis f. sp. tritici (Pst) that can suppress acquired resistance in local leaf by directly targeting the wheat NPR1 protein. In this investigation, we identified and validated a novel protein interaction between PNPi and wheat pathogenesis-related TaPR1a in the apoplastic space. TaPR1a-overexpressing wheat lines exhibited enhanced resistance to both Pst and Puccinia triticina (Pt). We further determined that exogenous expression of PNPi RNA in transgenic wheat lines reduced the degree of acquired resistance to Magnaporthe oryzae isolate P131 in the region adjacent to Pseudomonas syringae pv. tomato DC3000 infection area. Additionally, when PNPi was overexpressed, the expression levels of two plant defense responsive genes were suppressed upon P. syringae DC3000 infection in the local infiltration region. These findings established the mechanism of a single rust effector that can suppress multiple defense responses in wheat plants by targeting different components.

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A Conserved Puccinia striiformis Protein Interacts with Wheat NPR1 and Reduces Induction of Pathogenesis-Related Genes in Response to Pathogens

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-10-16-0207-r ◽

2016 ◽

Vol 29 (12) ◽

pp. 977-989 ◽

Cited By ~ 25

Author(s):

Xiaodong Wang ◽

Baoju Yang ◽

Kun Li ◽

Zhensheng Kang ◽

Dario Cantu ◽

...

Keyword(s):

Pseudomonas Syringae ◽

Systemic Acquired Resistance ◽

Puccinia Striiformis ◽

Acquired Resistance ◽

Bimolecular Fluorescence Complementation ◽

Pr Genes ◽

Pathogen Challenge ◽

Pathogenesis Related ◽

Transgenic Lines ◽

Wheat Leaves

In Arabidopsis, NPR1 is a key transcriptional coregulator of systemic acquired resistance. Upon pathogen challenge, NPR1 translocates from the cytoplasm to the nucleus, in which it interacts with TGA-bZIP transcription factors to activate the expression of several pathogenesis-related (PR) genes. In a screen of a yeast two-hybrid library from wheat leaves infected with Puccinia striiformis f. sp. tritici, we identified a conserved rust protein that interacts with wheat NPR1 and named it PNPi (for Puccinia NPR1 interactor). PNPi interacts with the NPR1/NIM1-like domain of NPR1 via its C-terminal DPBB_1 domain. Using bimolecular fluorescence complementation assays, we detected the interaction between PNPi and wheat NPR1 in the nucleus of Nicotiana benthamiana protoplasts. A yeast three-hybrid assay showed that PNPi interaction with NPR1 competes with the interaction between wheat NPR1 and TGA2.2. In barley transgenic lines overexpressing PNPi, we observed reduced induction of multiple PR genes in the region adjacent to Pseudomonas syringae pv. tomato DC3000 infection. Based on these results, we hypothesize that PNPi has a role in manipulating wheat defense response via its interactions with NPR1.

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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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The Novel Cerato-Platanin-Like Protein FocCP1 from Fusarium oxysporum Triggers an Immune Response in Plants

International Journal of Molecular Sciences ◽

10.3390/ijms20112849 ◽

2019 ◽

Vol 20 (11) ◽

pp. 2849 ◽

Cited By ~ 6

Author(s):

Songwei Li ◽

Yijie Dong ◽

Lin Li ◽

Yi Zhang ◽

Xiufen Yang ◽

...

Keyword(s):

Fusarium Oxysporum ◽

Pseudomonas Syringae ◽

Systemic Acquired Resistance ◽

Acquired Resistance ◽

Defense Responses ◽

Economic Losses ◽

Seedling Resistance ◽

Ros Formation ◽

Serious Disease ◽

Banana Wilt

Panama disease, or Fusarium wilt, the most serious disease in banana cultivation, is caused by Fusarium oxysporum f. sp. cubense (FOC) and has led to great economic losses worldwide. One effective way to combat this disease is by enhancing host plant resistance. The cerato-platanin protein (CPP) family is a group of small secreted cysteine-rich proteins in filamentous fungi. CPPs as elicitors can trigger the immune system resulting in defense responses in plants. In this study, we characterized a novel cerato-platanin-like protein in the secretome of Fusarium oxysporum f. sp. cubense race 4 (FOC4), named FocCP1. In tobacco, the purified recombinant FocCP1 protein caused accumulation of reactive oxygen species (ROS), formation of necrotic reaction, deposition of callose, expression of defense-related genes, and accumulation of salicylic acid (SA) and jasmonic acid (JA) in tobacco. These results indicated that FocCP1 triggered a hypersensitive response (HR) and systemic acquired resistance (SAR) in tobacco. Furthermore, FocCP1 enhanced resistance tobacco mosaic virus (TMV) disease and Pseudomonas syringae pv. tabaci 6605 (Pst. 6605) infection in tobacco and improved banana seedling resistance to FOC4. All results provide the possibility of further research on immune mechanisms of plant and pathogen interactions, and lay a foundation for a new biological strategy of banana wilt control in the future.

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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 Clade I TGA Transcription Factors Regulate Plant Defenses in an NPR1-Independent Fashion

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-09-11-0256 ◽

2012 ◽

Vol 25 (11) ◽

pp. 1459-1468 ◽

Cited By ~ 32

Author(s):

Heather L. Shearer ◽

Yu Ti Cheng ◽

Lipu Wang ◽

Jinman Liu ◽

Patrick Boyle ◽

...

Keyword(s):

Transcription Factors ◽

Pseudomonas Syringae ◽

Systemic Acquired Resistance ◽

Acquired Resistance ◽

Defense Responses ◽

R Gene ◽

Triple Mutant ◽

Transcriptional Reprogramming ◽

Tga Factors ◽

Hyaloperonospora Arabidopsidis

Transcriptional reprogramming during induction of salicylic acid (SA)-mediated defenses is regulated primarily by NPR1 (NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1), likely through interactions with TGA bZIP transcription factors. To ascertain the contributions of clade I TGA factors (TGA1 and TGA4) to defense responses, a tga1-1 tga4-1 double mutant was constructed and challenged with Pseudomonas syringae and Hyaloperonospora arabidopsidis. Although the mutant displayed enhanced susceptibility to virulent P. syringae, it was not compromised in systemic acquired resistance against this pathogen or resistance against avirulent H. arabidopsidis. Microarray analysis of nonelicited and SA-treated plants indicated that clade I TGA factors regulate fewer genes than NPR1. Approximately half of TGA-dependent genes were regulated by NPR1 but, in all cases, the direction of change was opposite in the two mutants. In support of the microarray data, the NPR1-independent disease resistance observed in the autoimmune resistance (R) gene mutant snc1 is partly compromised by tga1-1 tga4-1 mutations, and a triple mutant of clade I TGA factors with npr1-1 is more susceptible than either parent. These results suggest that clade I TGA factors are required for resistance against virulent pathogens and avirulent pathogens mediated by at least some R gene specificities, acting substantially through NPR1-independent pathways.

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Yeast Increases Resistance in Arabidopsis Against Pseudomonas syringae and Botrytis cinerea by Salicylic Acid-Dependent as Well as -Independent Mechanisms

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-19-1138 ◽

2006 ◽

Vol 19 (10) ◽

pp. 1138-1146 ◽

Cited By ~ 25

Author(s):

Ines C. Raacke ◽

Uta von Rad ◽

Martin J. Mueller ◽

Susanne Berger

Keyword(s):

Cell Wall ◽

Botrytis Cinerea ◽

Pseudomonas Syringae ◽

Mode Of Action ◽

Systemic Acquired Resistance ◽

Virulent Strain ◽

Acquired Resistance ◽

Defense Responses ◽

Symptom Development ◽

Yeast Suspension

Cell-wall and glucopeptide components of yeast have been reported to exhibit elicitor activity. The mode of action of defense activation by yeast is not known so far. In this study, we used the model plant Arabidopsis to investigate the activation of defense responses by yeast, the effect on resistance against different pathogens, and the mode of action. Treatment of Arabidopsis plants with an autoclaved yeast suspension induced the expression of systemic acquired resistance-related genes and accumulation of the phytoalexin camalexin. Symptom development and bacterial growth after infection with a virulent strain of the pathogen Pseudomonas syringae was reduced in yeast-pretreated plants. No protection was detectable in mutants affected in the salicylate pathway, while mutants in the jasmonate or camalexin pathway were protected by yeast, indicating that the salicylate pathway is necessary for the yeast-induced resistance against P. syringae. Yeast also reduced symptom development after challenge with Botrytis cinerea. This protection was detectable in all mutants tested, indicating that it is independent of the salicylate, jasmonate, and camalexin pathway.

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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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Wheat Apoplast-Localized Lipid Transfer Protein TaLTP3 Enhances Defense Responses Against Puccinia triticina

Frontiers in Plant Science ◽

10.3389/fpls.2021.771806 ◽

2021 ◽

Vol 12 ◽

Author(s):

Jiaojie Zhao ◽

Weishuai Bi ◽

Shuqing Zhao ◽

Jun Su ◽

Mengyu Li ◽

...

Keyword(s):

Leaf Rust ◽

Lipid Transfer Protein ◽

Puccinia Triticina ◽

Defense Responses ◽

Transgenic Wheat ◽

Lipid Transfer ◽

Transfer Protein ◽

Pathogenesis Related ◽

Rust Pathogen ◽

Wheat Lines

Plant apoplast serves as the frontier battlefield of plant defense in response to different types of pathogens. Many pathogenesis-related (PR) proteins are accumulated in apoplastic space during the onset of plant–pathogen interaction, where they act to suppress pathogen infection. In this study, we found the expression of Triticum aestivum lipid transfer protein 3 (TaLTP3) gene was unregulated during incompatible interaction mediated by leaf rust resistance genes Lr39/41 at the early infection stage. Stable transgenic wheat lines overexpressing TaLTP3 exhibited enhanced resistance to leaf rust pathogen Puccinia triticina. Transcriptome analysis revealed that overexpression of TaLTP3 specifically activated the transcription of pathogenesis-related protein 1a (TaPR1a) and multiple plant hormone pathways, including salicylic acid (SA), jasmonic acid (JA), and auxin, in response to the infection of the model bacterial pathogen Pseudomonas syringae pv. tomato DC3000. Further investigation indicated that TaLTP3 physically associated with wheat TaPR1a protein in the apoplast. Transgenic wheat lines overexpressing TaLTP3 and TaPR1a showed higher accumulations of reactive oxygen species (ROS) during plant defense responses. All these findings suggested that TaLTP3 is involved in wheat resistance against leaf rust pathogen infection and forming a TaLTP3-TaPR1a complex in apoplast against this pathogen, which provides new insights into the functional roles of PR proteins.

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Arabidopsis UGT76B1 glycosylates N-hydroxy-pipecolic acid and inactivates systemic acquired resistance in tomato

10.1101/2020.07.06.189894 ◽

2020 ◽

Cited By ~ 2

Author(s):

Eric C. Holmes ◽

Yun-Chu Chen ◽

Mary Beth Mudgett ◽

Elizabeth S. Sattely

Keyword(s):

Pseudomonas Syringae ◽

Systemic Acquired Resistance ◽

Acquired Resistance ◽

Bacterial Pathogen ◽

Defense Responses ◽

Pipecolic Acid ◽

Systemic Resistance ◽

Biosynthetic Genes ◽

Solanaceous Plants

AbstractSystemic acquired resistance (SAR) is a mechanism that plants utilize to connect a local pathogen infection to global defense responses. N-hydroxy-pipecolic acid (NHP) and a glycosylated derivative are produced during SAR, yet their individual roles in the response have not yet been elucidated. Here we report that Arabidopsis thaliana UGT76B1 can generate glycosylated NHP (NHP-Glc) in vitro and when transiently expressed alongside Arabidopsis NHP biosynthetic genes in two Solanaceous plants. During infection, Arabidopsis ugt76b1 mutants do not accumulate NHP-Glc and accumulate less glycosylated salicylic acid (SA-Glc) than wild type plants. The metabolic changes in ugt76b1 mutant plants are accompanied by enhanced defense to the bacterial pathogen Pseudomonas syringae, suggesting that glycosylation of SAR molecules NHP and SA by UGT76B1 plays an important role in defense modulation. Transient expression of Arabidopsis UGT76B1 with the Arabidopsis NHP biosynthesis genes ALD1 and FMO1 in tomato increases NHP-Glc production and reduces NHP accumulation in local tissue, and abolishes the systemic resistance seen when expressing NHP-biosynthetic genes alone. These findings reveal that the glycosylation of NHP by UGT76B1 alters defense priming in systemic tissue and provide further evidence for the role of the NHP aglycone as the active metabolite in SAR signaling.

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Differential Induction of Systemic Resistance in Arabidopsis by Biocontrol Bacteria

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi.1997.10.6.716 ◽

1997 ◽

Vol 10 (6) ◽

pp. 716-724 ◽

Cited By ~ 272

Author(s):

Saskia C. M. Van Wees ◽

Corné M. J. Pieterse ◽

Annemiek Trijssenaar ◽

Yvonne A. M. Van 't Westende ◽

Femke Hartog ◽

...

Keyword(s):

Pseudomonas Syringae ◽

Molecular Mechanisms ◽

Systemic Acquired Resistance ◽

Induced Systemic Resistance ◽

Acquired Resistance ◽

Systemic Resistance ◽

Biocontrol Bacteria ◽

Pathogenesis Related ◽

Pathogenesis Related Gene ◽

Related Plant

Selected nonpathogenic, root-colonizing bacteria are able to elicit induced systemic resistance (ISR) in plants. To elucidate the molecular mechanisms underlying this type of systemic resistance, an Arabidopsis-based model system was developed in which Pseudomonas syringae pv. tomato and Fusarium oxysporum f. sp. raphani were used as challenging pathogens. In Arabidopsis thaliana ecotypes Columbia and Landsberg erecta, colonization of the rhizosphere by P. fluorescens strain WCS417r induced systemic resistance against both pathogens. In contrast, ecotype RLD did not respond to WCS417r treatment, whereas all three ecotypes expressed systemic acquired resistance upon treatment with salicylic acid (SA). P. fluorescens strain WCS374r, previously shown to induce ISR in radish, did not elicit ISR in Arabidopsis. The opposite was found for P. putida strain WCS358r, which induced ISR in Arabidopsis but not in radish. These results demonstrate that rhizosphere pseudomonads are differentially active in eliciting ISR in related plant species. The outer membrane lipopolysaccharide (LPS) of WCS417r is the main ISR-inducing determinant in radish and carnation, and LPS-containing cell walls also elicit ISR in Arabidopsis. However, mutant WCS417rOA¯, lacking the O-antigenic side chain of the LPS, induced levels of protection similar to those induced by wild-type WCS417r. This indicates that ISR-inducing bacteria produce more than a single factor that trigger ISR in Arabidopsis. Furthermore, WCS417r and WCS358r induced protection in both wildtype Arabidopsis and SA-nonaccumulating NahG plants without activating pathogenesis-related gene expression. This suggests that elicitation of an SA-independent signaling pathway is a characteristic feature of ISR-inducing biocontrol bacteria.

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