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A novel methyltransferase from the intracellular pathogen Plasmodiophora brassicae methylates salicylic acid.

ABSTRACT: The obligate biotrophic pathogen Plasmodiophora brassicae causes clubroot disease in Arabidopsis thaliana, which is characterized by large root galls. Salicylic acid (SA) production is a defence response in plants, and its methyl ester is involved in systemic signalling. Plasmodiophora brassicae seems to suppress plant defence reactions, but information on how this is achieved is scarce. Here, we profile the changes in SA metabolism during Arabidopsis clubroot disease. The accumulation of SA and the emission of methylated SA (methyl salicylate, MeSA) were observed in P.?brassicae-infected Arabidopsis 28 days after inoculation. There is evidence that MeSA is transported from infected roots to the upper plant. Analysis of the mutant Atbsmt1, deficient in the methylation of SA, indicated that the Arabidopsis SA methyltransferase was not responsible for alterations in clubroot symptoms. We found that P.?brassicae possesses a methyltransferase (PbBSMT) with homology to plant methyltransferases. The PbBSMT gene is maximally transcribed when SA production is highest. By heterologous expression and enzymatic analyses, we showed that PbBSMT can methylate SA, benzoic and anthranilic acids.

SUBMITTER: Ludwig-Muller J

PROVIDER: S-EPMC6638400 | biostudies-literature | 2015 May

REPOSITORIES: biostudies-literature

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A novel methyltransferase from the intracellular pathogen Plasmodiophora brassicae methylates salicylic acid.

Ludwig-Müller Jutta J Jülke Sabine S Geiß Kathleen K Richter Franziska F Mithöfer Axel A Šola Ivana I Rusak Gordana G Keenan Sandi S Bulman Simon S

Molecular plant pathology 20140925 4

The obligate biotrophic pathogen Plasmodiophora brassicae causes clubroot disease in Arabidopsis thaliana, which is characterized by large root galls. Salicylic acid (SA) production is a defence response in plants, and its methyl ester is involved in systemic signalling. Plasmodiophora brassicae seems to suppress plant defence reactions, but information on how this is achieved is scarce. Here, we profile the changes in SA metabolism during Arabidopsis clubroot disease. The accumulation of SA and ...[more]

PMID: 25135243

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Project description:BackgroundPlasmodiophora brassicae is the causal agent of clubroot disease of cruciferous plants and one of the biggest threats to the rapeseed (Brassica napus) and brassica vegetable industry worldwide.Disease symptomsIn the advanced stages of clubroot disease wilting, stunting, yellowing, and redness are visible in the shoots. However, the typical symptoms of the disease are the presence of club-shaped galls in the roots of susceptible hosts that block the absorption of water and nutrients.Host rangeMembers of the family Brassicaceae are the primary host of the pathogen, although some members of the family, such as Bunias orientalis, Coronopus squamatus, and Raphanus sativus, have been identified as being consistently resistant to P. brassicae isolates with variable virulence profile.TaxonomyClass: Phytomyxea; Order: Plasmodiophorales; Family: Plasmodiophoraceae; Genus: Plasmodiophora; Species: Plasmodiophora brassicae (Woronin, 1877).DistributionClubroot disease is spread worldwide, with reports from all continents except Antarctica. To date, clubroot disease has been reported in more than 80 countries.PathotypingBased on its virulence on different hosts, P. brassicae is classified into pathotypes or races. Five main pathotyping systems have been developed to understand the relationship between P. brassicae and its hosts. Nowadays, the Canadian clubroot differential is extensively used in Canada and has so far identified 36 different pathotypes based on the response of a set of 13 hosts.Effectors and resistanceAfter the identification and characterization of the clubroot pathogen SABATH-type methyltransferase PbBSMT, several other effectors have been characterized. However, no avirulence gene is known, hindering the functional characterization of the five intercellular nucleotide-binding (NB) site leucine-rich-repeat (LRR) receptors (NLRs) clubroot resistance genes validated to date.Important linkCanola Council of Canada is constantly updating information about clubroot and P. brassicae as part of their Canola Encyclopedia: https://www.canolacouncil.org/canola-encyclopedia/diseases/clubroot/.Phytosanitary categorizationPLADBR: EPPO A2 list; Annex designation 9E.

Project description:Clubroot, caused by the obligate parasite Plasmodiophora brassicae, is an important disease of the Brassicaceae and poses a significant threat to the $26.7 billion canola/oilseed rape (Brassica napus) industry in western Canada. While clubroot is managed most effectively by planting resistant host varieties, new pathotypes of P. brassicae have emerged recently that can overcome this resistance. Whole genome analyses provide both a toolbox and a systemic view of molecular mechanisms in host-pathogen interactions, which can be used to design new breeding strategies to increase P. brassicae resistance. We used RNA-seq to evaluate differential gene expression at 7, 14 and 21 days after inoculation (dai) of two B. napus genotypes with differential responses to P. brassicae pathotype 5X. Gall development was evident at 14 dai in the susceptible genotype (the oilseed rape 'Brutor'), while gall development in the resistant genotype (the rutabaga (B. napus) 'Laurentian') was limited and not visible until 21 dai. Immune responses were better sustained through the time-course in 'Laurentian', and numerous genes from immune-related functional categories were associated with salicylic acid (SA)-mediated responses. Jasmonic acid (JA)-mediated responses seemed to be mostly inhibited, especially in the resistant genotype. The upregulation of standard defense-related proteins, like chitinases and thaumatins, was evident in 'Laurentian'. The enrichment, in both host genotypes, of functional categories for syncytium formation and response to nematodes indicated that cell enlargement during P. brassicae infection, and the metabolic processes therein, share similarities with the response to infection by nematodes that produce similar anatomical symptoms. An analysis of shared genes between the two genotypes at different time-points, confirmed that the nematode-like responses occurred earlier for 'Brutor', along with cell metabolism and growth changes. Additionally, the susceptible cultivar turned off defense mechanisms earlier than 'Laurentian'. Collectively, this study showed the importance of SA in triggering immune responses and suggested some key resistance and susceptibility factors that can be used in future studies for resistance breeding through gene-editing approaches.

Project description:BackgroundThe protist Plasmodiophora brassicae is a soil-borne pathogen of cruciferous species and the causal agent of clubroot disease of Brassicas including agriculturally important crops such as canola/rapeseed (Brassica napus). P. brassicae has remained an enigmatic plant pathogen and is a rare example of an obligate biotroph that resides entirely inside the host plant cell. The pathogen is the cause of severe yield losses and can render infested fields unsuitable for Brassica crop growth due to the persistence of resting spores in the soil for up to 20 years.ResultsTo provide insight into the biology of the pathogen and its interaction with its primary host B. napus, we produced a draft genome of P. brassicae pathotypes 3 and 6 (Pb3 and Pb6) that differ in their host range. Pb3 is highly virulent on B. napus (but also infects other Brassica species) while Pb6 infects only vegetable Brassica crops. Both the Pb3 and Pb6 genomes are highly compact, each with a total size of 24.2 Mb, and contain less than 2 % repetitive DNA. Clustering of genome-wide single nucleotide polymorphisms (SNP) of Pb3, Pb6 and three additional re-sequenced pathotypes (Pb2, Pb5 and Pb8) shows a high degree of correlation of cluster grouping with host range. The Pb3 genome features significant reduction of intergenic space with multiple examples of overlapping untranslated regions (UTRs). Dependency on the host for essential nutrients is evident from the loss of genes for the biosynthesis of thiamine and some amino acids and the presence of a wide range of transport proteins, including some unique to P. brassicae. The annotated genes of Pb3 include those with a potential role in the regulation of the plant growth hormones cytokinin and auxin. The expression profile of Pb3 genes, including putative effectors, during infection and their potential role in manipulation of host defence is discussed.ConclusionThe P. brassicae genome sequence reveals a compact genome, a dependency of the pathogen on its host for some essential nutrients and a potential role in the regulation of host plant cytokinin and auxin. Genome annotation supported by RNA sequencing reveals significant reduction in intergenic space which, in addition to low repeat content, has likely contributed to the P. brassicae compact genome.

Dataset Information

A novel methyltransferase from the intracellular pathogen Plasmodiophora brassicae methylates salicylic acid.

Publications

A novel methyltransferase from the intracellular pathogen Plasmodiophora brassicae methylates salicylic acid.

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