The Phytotoxin Coronatine Contributes to Pathogen Fitness and Is Required for Suppression of Salicylic Acid Accumulation in Tomato Inoculated with Pseudomonas syringae pv. tomato DC3000

The roles of the phytotoxin coronatine (COR) and salicylic acid (SA)-mediated defenses in the interaction of Pseudomonas syringae pv. tomato DC3000 and tomato (Solanum lycopersicum) were investigated. Unlike findings reported for Arabidopsis thaliana, DC3000 mutants impaired for production of COR or one of its components, coronafacic acid (CFA) or coronamic acid (CMA), induced distinctly different disease lesion phenotypes in tomato. Tomato plants inoculated with the CFA- CMA- mutant DB29 showed elevated transcript levels of SlICS, which encodes isochorismate synthase, an enzyme involved in SA biosynthesis in S. lycopersicum. Furthermore, expression of genes encoding SA-mediated defense proteins were elevated in DB29-inoculated plants compared with plants inoculated with DC3000, suggesting that COR suppresses SlICS-mediated SA responses. Sequence analysis of SlICS revealed that it encodes a protein that is 55 and 59.6% identical to the A. thaliana ICS-encoded proteins AtICS1 and AtICS2, respectively. Tomato plants silenced for SlICS were hypersusceptible to DC3000 and accumulated lower levels of SA after infection with DC3000 compared with inoculated wild-type tomato plants. Unlike what has been shown for A. thaliana, the COR- mutant DB29 was impaired for persistence in SlICS-silenced tomato plants; thus, COR has additional roles in virulence that are SA independent and important in the latter stages of disease development. In summary, the infection assays, metabolic profiling, and gene expression results described in this study indicate that the intact COR molecule is required for both suppression of SA-mediated defense responses and full disease symptom development in tomato.

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CorR Regulates Multiple Components of Virulence in Pseudomonas syringae pv. tomato DC3000

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-19-0768 ◽

2006 ◽

Vol 19 (7) ◽

pp. 768-779 ◽

Cited By ~ 51

Author(s):

Aswathy Sreedharan ◽

Alejandro Penaloza-Vazquez ◽

Barbara N. Kunkel ◽

Carol L. Bender

Keyword(s):

Pseudomonas Syringae ◽

Biosynthetic Pathway ◽

Response Regulator ◽

Tomato Dc3000 ◽

Tomato Plants ◽

Coronafacic Acid ◽

Multiple Components ◽

Expression Of Genes ◽

Genes Encoding ◽

Polymerase Chain

The phytotoxin coronatine (COR) is produced by various pathovars of Pseudomonas syringae, including P. syringae pv. tomato DC3000, which is pathogenic on crucifers and tomato, and P. syringae pv. glycinea PG4180, a soybean pathogen. The COR molecule contains two distinct components, coronafacic acid (CFA) and coronamic acid (CMA), which are intermediates in the COR biosynthetic pathway. In P. syringae pv. tomato DC3000, it is not clear whether corR, which encodes a response regulator, positively regulates CFA and CMA synthesis as it does in P. syringae pv. glycinea PG4180. In this study, a corR mutant of P. syringae pv. tomato DC3000 was constructed and was shown to be defective in the production of COR, CFA, and CMA. Furthermore, disease severity was greatly reduced in tomato plants inoculated with the corR mutant compared with wild-type P. syringae pv. tomato DC3000. We also showed that a mutation in hrpL, which encodes an alternate RNA polymerase sigma factor (σL) required for the expression of genes encoding components of the type III secretion system, abrogated production of COR in P. syringae pv. tomato DC3000. The presence of a potential hrp box, the recognition site for σL, upstream of corR suggested that corR might be regulated by hrpL. This was confirmed in reverse-transcription polymerase chain reaction experiments showing that the upstream effector gene holPtoAA, which was associated with the hrp box, was cotranscribed with corR. Furthermore, studies also were conducted to investigate whether mutations in corR had effects on the expression of hrpL. The corR mutant of P. syringae pv. tomato DC3000 showed both a reduction and delay in the expression of hrpL and was impaired in its ability to elicit a hypersensitive response on Nicotiana benthamiana. A putative CorR-binding site was identified upstream of hrpL, and gel shift studies confirmed the binding of CorR to this region. These results indicate that corR directly impacts the expression of the hrp regulon in P. syringae.

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Chitosan Oligosaccharide Induces Resistance to Pseudomonas syringae pv. tomato DC3000 in Arabidopsis thaliana by Activating Both Salicylic Acid– and Jasmonic Acid–Mediated Pathways

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-03-18-0071-r ◽

2018 ◽

Vol 31 (12) ◽

pp. 1271-1279 ◽

Cited By ~ 21

Author(s):

Xiaochen Jia ◽

Haihong Zeng ◽

Wenxia Wang ◽

Fuyun Zhang ◽

Heng Yin

Keyword(s):

Salicylic Acid ◽

Jasmonic Acid ◽

Induced Resistance ◽

Pseudomonas Syringae ◽

Plant Immunity ◽

Chitosan Oligosaccharide ◽

Induction Effect ◽

Tomato Dc3000 ◽

Expression Of Genes ◽

Underlying Mechanisms

Chitosan oligosaccharide (COS) is an effective plant immunity elicitor; however, its induction mechanism in plants is complex and needs further investigation. In this study, the Arabidopsis–Pseudomonas syringae pv. tomato DC3000 (hereafter called DC3000) interaction was used to investigate the induction effect and the underlying mechanisms of COS. COS is effective in inducing resistance to DC3000 in Arabidopsis, and our results demonstrate that treatment with COS 3 days before DC3000 inoculation provided the most effective resistance. Disease severity in jar1 (jasmonic acid [JA]-deficient mutant), NahG, and sid2 (salicylic acid [SA]-deficient mutants) suggest both the SA and JA pathways are required for the Arabidopsis response to DC3000. COS pretreatment induced resistance in wild type (WT), jar1, and also, although to a lesser degree, in NahG and sid2 plants, implying that the SA and JA pathways play redundant roles in COS-induced resistance to DC3000. In COS-pretreated plants, expression of genes related to the SA pathway (PR1, PR2, and PR5) and SA content increased in both WT and jar1. Moreover, expression of genes related to the JA pathway (PDF1.2 and VSP2) and JA content both increased in WT and NahG. In conclusion, COS induces resistance to DC3000 in Arabidopsis by activating both SA- and JA-mediated pathways, although SA and JA pathways play redundant roles in this COS-induced resistance.

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Differential Expression of Genes Encoding Arabidopsis Phospholipases After Challenge with Virulent or Avirulent Pseudomonas Isolates

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi.2002.15.8.808 ◽

2002 ◽

Vol 15 (8) ◽

pp. 808-816 ◽

Cited By ~ 59

Author(s):

Marta de Torres Zabela ◽

Isabelle Fernandez-Delmond ◽

Totte Niittyla ◽

Pedro Sanchez ◽

Murray Grant

Keyword(s):

Pseudomonas Syringae ◽

Defense Responses ◽

Gene Interactions ◽

Gene Encoding ◽

Cellular Processes ◽

Expression Of Genes ◽

Pathogen Challenge ◽

Genes Encoding ◽

Plant Pathogen Interactions ◽

Gene For Gene

Phospholipase D (PLD; EC 3.1.4.4) has been linked to a number of cellular processes, including Tran membrane signaling and membrane degradation. Four PLD genes (α, β, γ1, and γ2) have been cloned from Arabidopsis thalami. They encode isoforms with distinct regulatory and catalytic properties but little is known about their physiological roles. Using cDNA amplified fragment length polymorphism display and RNA blot analysis, we identified Arabidopsis PLDγ1 and a gene encoding a lysophospholipase (EC 3.1.1.5), lysoPL1, to be differentially expressed during host response to virulent and avirulent pathogen challenge. Examination of the expression pattern of phospholipase genes induced in response to pathogen challenge was undertaken using the lysoPL1 and gene-specific probes corresponding to the PLD isoforms α, β, and γ1. Each mRNA class exhibited different temporal patterns of expression after infiltration of leaves with Pseudomonas syringae pv. tomato with or without avrRpm1. PLDα was rapidly induced and remained constitutively elevated regardless of treatment. PLDβ was transiently induced upon pathogen challenge. However, mRNA for the lysoPL1 and PLDγ1 genes showed enhanced and sustained elevation during an incompatible interaction, in both ndr1 and overexpressing NahG genetic backgrounds. Further evidence for differential engagement of these PLD mRNA during defense responses, other than gene-for-gene interactions, was demonstrated by their response to salicylic acid treatment or wounding. Our results indicate that genes encoding lysoPL1, PLDγ1, and PLDβ are induced during early responses to pathogen challenge and, additionally, PLDγ1 and lysoPL1 are specifically upregulated during gene-for-gene interactions, leading to the hypersensitive response. We discuss the possible role of these genes in plant-pathogen interactions.

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Pseudomonas syringae pv. tomato OxyR Is Required for Virulence in Tomato and Arabidopsis

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-09-15-0204-r ◽

2016 ◽

Vol 29 (2) ◽

pp. 119-131 ◽

Cited By ~ 17

Author(s):

Yasuhiro Ishiga ◽

Yuki Ichinose

Keyword(s):

Oxidative Stress ◽

Pseudomonas Syringae ◽

Molecular Mechanisms ◽

Expression Profiles ◽

High Sensitivity ◽

Defense Responses ◽

Bacterial Populations ◽

Disease Symptoms ◽

Expression Of Genes ◽

Genes Encoding

Reactive oxygen species (ROS) have been shown to have a crucial role in plant defense responses and signaling pathways. In addition, ROS also have direct toxicity against pathogens. However, the molecular mechanisms of plant ROS in the direct effects against pathogens is still unclear. To investigate the function of plant ROS in the interactions of plant and bacterial pathogens, we focused on oxyR, encoding an oxidative stress-regulated transcription factor in Pseudomonas syringae pv. tomato DC3000 (DC3000), and generated an ΔoxyR mutant. The DC3000 ΔoxyR mutant showed high sensitivity to oxidative stress in comparison with wild type and the complemented line. The host plants of DC3000, including tomato and Arabidopsis inoculated with the ΔoxyR mutant, clearly showed reduced disease symptoms as well as reduced bacterial populations. Expression profiles of DC3000 genes revealed that OxyR could regulate the expression of genes encoding ROS-detoxifying enzymes, including catalases (KatB and KatG), in response to ROS. We also demonstrated that the expression of katB could be regulated by OxyR during the infection of DC3000 in Arabidopsis. These results suggest that OxyR has an important role in the virulence of DC3000 by regulating the expression of genes related to oxidative stress.

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The MAP Kinase Kinase MKK2 Affects Disease Resistance in Arabidopsis

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-20-5-0589 ◽

2007 ◽

Vol 20 (5) ◽

pp. 589-596 ◽

Cited By ~ 73

Author(s):

Günter Brader ◽

Armin Djamei ◽

Markus Teige ◽

E. Tapio Palva ◽

Heribert Hirt

Keyword(s):

Disease Resistance ◽

Pseudomonas Syringae ◽

Stress Responses ◽

Plant Disease Resistance ◽

Map Kinases ◽

Defense Responses ◽

Alternaria Brassicicola ◽

Tomato Dc3000 ◽

Altered Expression ◽

Expression Of Genes

The Arabidopsis mitogen-activated protein kinase (MAPK) kinase 2 (MKK2) was shown to mediate cold and salt stress responses through activation of the two MAP kinases MPK4 and MPK6. Transcriptome analysis of plants expressing constitutively active MKK2 (MKK2-EE plants) showed altered expression of genes induced by abiotic stresses but also a significant number of genes involved in defense responses. Both MPK4 and MPK6 became rapidly activated upon Pseudomonas syringae pv. tomato DC3000 infection and MKK2-EE plants showed enhanced levels of MPK4 activation. Although MKK2-EE plants shared enhanced expression of genes encoding enzymes of ethylene (ET) and jasmonic acid (JA) synthesis, ET, JA, and salicylic acid (SA) levels did not differ dramatically from those of wild-type or mkk2-null plants under ambient growth conditions. Upon P. syringae pv. tomato DC3000 infection, however, MKK2-EE plants showed reduced increases of JA and SA levels. These results indicate that MKK2 is involved in regulating hormone levels in response to pathogens. MKK2-EE plants were more resistant to infection by P. syringae pv. tomato DC3000 and Erwinia carotovora subsp. carotovora, but showed enhanced sensitivity to the fungal necrotroph Alternaria brassicicola. Our data indicate that MKK2 plays a role in abiotic stress tolerance and plant disease resistance.

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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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Intercellular salicylic acid accumulation is important for age-related resistance in Arabidopsis to Pseudomonas syringae

Physiological and Molecular Plant Pathology ◽

10.1016/j.pmpp.2005.02.002 ◽

2004 ◽

Vol 65 (4) ◽

pp. 197-209 ◽

Cited By ~ 32

Author(s):

Robin K. Cameron ◽

Kasia Zaton

Keyword(s):

Salicylic Acid ◽

Pseudomonas Syringae ◽

Age Related ◽

Acid Accumulation ◽

Salicylic Acid Accumulation

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Genome-Wide Gene Expression Analysis of Pseudomonas syringae pv. tomato DC3000 Reveals Overlapping and Distinct Pathways Regulated by hrpL and hrpRS

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-19-0976 ◽

2006 ◽

Vol 19 (9) ◽

pp. 976-987 ◽

Cited By ~ 46

Author(s):

Lefu Lan ◽

Xin Deng ◽

Jianmin Zhou ◽

Xiaoyan Tang

Keyword(s):

Pseudomonas Syringae ◽

Housekeeping Genes ◽

The Novel ◽

Tomato Dc3000 ◽

Regulatory Pathways ◽

Genome Wide ◽

Genes Encoding ◽

Substrate Proteins ◽

Genome Wide Gene Expression ◽

Insight Into

Pseudomonas syringae pv. tomato DC3000 is a model pathogen infecting tomato and Arabidopsis plants. Genes encoding the type III secretion system and substrate proteins (collectively called TTSS genes) of this bacterium are induced in plants and in minimal medium (MM). The induction of TTSS genes is mediated by HrpL, an alternative sigma factor recognizing the hrp box in the promoter of TTSS genes. The transcription of hrpL is activated by HrpR and HrpS, two homologous DNA-binding proteins encoded by the hrpRS operon. Microarray analysis was conducted to evaluate the DC3000 genes regulated by hrpL and hrpRS in MM. The analysis identified a number of novel hrpL-activated genes with a putative TTSS-independent function. Genes regulated by hrpL were mostly regulated by hrpRS in the same manner, but a large number of genes regulated by hrpRS were hrpL-independent, indicating that hrpL represents one branch of the regulatory pathways downstream of hrpRS. The induction of the TTSS genes was associated with downregulation of the housekeeping genes, indicating that the activation of the TTSS has a cost on the basic cellular activities. The novel genes and pathways identified by the microarray provide new insight into the bacterial functions coordinating with the TTSS.

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Role of Jasmonic Acid Pathway in Tomato Plant-Pseudomonas syringae Interaction

Plants ◽

10.3390/plants9020136 ◽

2020 ◽

Vol 9 (2) ◽

pp. 136 ◽

Cited By ~ 1

Author(s):

Loredana Scalschi ◽

Eugenio Llorens ◽

Pilar García-Agustín ◽

Begonya Vicedo

Keyword(s):

Gene Expression ◽

Salicylic Acid ◽

Jasmonic Acid ◽

Pseudomonas Syringae ◽

Tomato Plant ◽

Wild Type ◽

Tomato Plants ◽

Bacterial Pathogenicity ◽

Acid Pathway

The jasmonic acid pathway has been considered as the backbone of the response against necrotrophic pathogens. However, a hemi-biotrophic pathogen, such as Pseudomonas syringae, has taken advantage of the crosstalk between the different plant hormones in order to manipulate the responses for its own interest. Despite that, the way in which Pseudomonas syringae releases coronatine to activate jasmonic acid-derived responses and block the activation of salicylic acid-mediated responses is widely known. However, the implication of the jasmonic intermediates in the plant-Pseudomonas interaction is not studied yet. In this work, we analyzed the response of both, plant and bacteria using SiOPR3 tomato plants. Interestingly, SiOPR3 plants are more resistant to infection with Pseudomonas. The gene expression of bacteria showed that, in SiOPR3 plants, the activation of pathogenicity is repressed in comparison to wild type plants, suggesting that the jasmonic acid pathway might play a role in the pathogenicity of the bacteria. Moreover, treatments with JA restore the susceptibility as well as activate the expression of bacterial pathogenicity genes. The observed results suggest that a complete jasmonic acid pathway is necessary for the susceptibility of tomato plants to Pseudomonas syringae.

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