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The evolutionary and molecular features of the broad-host-range plant pathogen Sclerotinia sclerotiorum.

ABSTRACT: Sclerotinia sclerotiorum is a pathogenic fungus that infects hundreds of plant species, including many of the world's most important crops. Key features of S. sclerotiorum include its extraordinary host range, preference for dicotyledonous plants, relatively slow evolution, and production of protein effectors that are active in multiple host species. Plant resistance to this pathogen is highly complex, typically involving numerous polymorphisms with infinitesimally small effects, which makes resistance breeding a major challenge. Due to its economic significance, S. sclerotiorum has been subjected to a large amount of molecular and evolutionary research. In this updated pathogen profile, we review the evolutionary and molecular features of S. sclerotiorum and discuss avenues for future research into this important species.

SUBMITTER: Derbyshire MC

PROVIDER: S-EPMC9276942 | biostudies-literature | 2022 Aug

REPOSITORIES: biostudies-literature

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The evolutionary and molecular features of the broad-host-range plant pathogen Sclerotinia sclerotiorum.

Derbyshire Mark C MC Newman Toby E TE Khentry Yuphin Y Owolabi Taiwo Akeem A

Molecular plant pathology 20220411 8

Sclerotinia sclerotiorum is a pathogenic fungus that infects hundreds of plant species, including many of the world's most important crops. Key features of S. sclerotiorum include its extraordinary host range, preference for dicotyledonous plants, relatively slow evolution, and production of protein effectors that are active in multiple host species. Plant resistance to this pathogen is highly complex, typically involving numerous polymorphisms with infinitesimally small effects, which makes res ...[more]

PMID: 35411696

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Project description:BackgroundThe broad host range pathogen Sclerotinia sclerotiorum infects over 400 plant species and causes substantial yield losses in crops worldwide. Secondary metabolites are known to play important roles in the virulence of plant pathogens, but little is known about the secondary metabolite repertoire of S. sclerotiorum. In this study, we predicted secondary metabolite biosynthetic gene clusters in the genome of S. sclerotiorum and analysed their expression during infection of Brassica napus using an existing transcriptome data set. We also investigated their sequence diversity among a panel of 25 previously published S. sclerotiorum isolate genomes.ResultsWe identified 80 putative secondary metabolite clusters. Over half of the clusters contained at least three transcriptionally coregulated genes. Comparative genomics revealed clusters homologous to clusters in the closely related plant pathogen Botrytis cinerea for production of carotenoids, hydroxamate siderophores, DHN melanin and botcinic acid. We also identified putative phytotoxin clusters that can potentially produce the polyketide sclerin and an epipolythiodioxopiperazine. Secondary metabolite clusters were enriched in subtelomeric genomic regions, and those containing paralogues showed a particularly strong association with repeats. The positional bias we identified was borne out by intraspecific comparisons that revealed putative secondary metabolite genes suffered more presence / absence polymorphisms and exhibited a significantly higher sequence diversity than other genes.ConclusionsThese data suggest that S. sclerotiorum produces numerous secondary metabolites during plant infection and that their gene clusters undergo enhanced rates of mutation, duplication and recombination in subtelomeric regions. The microevolutionary regimes leading to S. sclerotiorum secondary metabolite diversity have yet to be elucidated. Several potential phytotoxins documented in this study provide the basis for future functional analyses.

Project description:White mold commonly known as Sclerotinia sclerotiorum causes stem rot disease and has emerged as one of the major fungal pathogens of oilseed Brassica across the world. In the present study, consistently virulent S. sclerotiorum isolate "ESR-01" was sequenced and an assembly size of ~ 41 Mb with 328 scaffolds having N50 of 447,128 was obtained. Additionally, 27,450 single nucleotide polymorphisms (SNPs) were identified from 155 scaffolds against S. sclerotiorum 1980 isolate, with an average SNP density of ~ 1.5 per kb genome. 667 repetitive elements were identified and approximately comprised 7% of the total annotated genes. The DDE_1 with 454 in numbers was found to be the most abundant and accounts for 68% of the total predicted repetitive elements. In total, 3844 simple sequence repeats are identified in the 328 scaffolds. A total of 9469 protein-coding genes were predicted from the whole genome assembly with an average gene length of 1587 bp and their distribution as 230.95 genes per Mb in the genome. Out of 9469 predicted protein-coding genes, 529 genes were observed encoding the CAZymes (Carbohydrate-Active enzymes) capable of degradation of the complex polysaccharides. Glycosyltransferase (GT) families were most abundant (49.71%) among the predicted CAZymes and GT2 (23%), GT4 (20%), and glycoside hydrolase (GH) 23% with GH18 (11%) were the prominent cell wall degrading enzyme families in the ESR-01 secretome. Besides this, 156 genes essential for the pathogen-host interactions were also identified. The effector analysis in the whole genome proteomics dataset revealed a total of 57 effector candidates (ECs) and 27 of them were having their analogs whereas the remaining 30 were novel ones. Eleven selected ECs were validated experimentally by analyzing the expression profile of the ESR-01 isolate of S. sclerotiorum. Together, the present investigation offers a better understanding of the S. sclerotiorum genome, secretome, and its effector repertoire which will help in refining the present knowledge on S. sclerotiorum-Brassica interactions and necrotrophic lifestyle of the phytopathogen in general.

Project description:The pathogenic fungus Sclerotinia sclerotiorum infects over 600 species of plant. It is present in numerous environments throughout the world and causes significant damage to many agricultural crops. Fragmentation and lack of gene flow between populations may lead to population sub-structure. Within discrete recombining populations, positive selection may lead to a 'selective sweep'. This is characterised by an increase in frequency of a favourable allele leading to reduction in genotypic diversity in a localised genomic region due to the phenomenon of genetic hitchhiking. We aimed to assess whether isolates of S. sclerotiorum from around the world formed genotypic clusters associated with geographical origin and to determine whether signatures of population-specific positive selection could be detected. To do this, we sequenced the genomes of 25 isolates of S. sclerotiorum collected from four different continents-Australia, Africa (north and south), Europe and North America (Canada and the northen United States) and conducted SNP based analyses of population structure and selective sweeps. Among the 25 isolates, there was evidence for two major population clusters. One of these consisted of 11 isolates from Canada, the USA and France (population 1), and the other consisted of nine isolates from Australia and one from Morocco (population 2). The rest of the isolates were genotypic outliers. We found that there was evidence of outcrossing in these two populations based on linkage disequilibrium decay. However, only a single candidate selective sweep was observed, and it was present in population 2. This sweep was close to a Major Facilitator Superfamily transporter gene, and we speculate that this gene may have a role in nutrient uptake from the host. The low abundance of selective sweeps in the S. sclerotiorum genome contrasts the numerous examples in the genomes of other fungal pathogens. This may be a result of its slow rate of evolution and low effective recombination rate due to self-fertilisation and vegetative reproduction.

Project description:Pathogen exposure to sublethal doses of fungicides may result in mutations that may represent an important and largely overlooked mechanism of introducing new genetic variation into strictly clonal populations, including acquisition of fungicide resistance. We tested this hypothesis using the clonal plant pathogen, Sclerotinia sclerotiorum. Nine susceptible isolates were exposed independently to five commercial fungicides with different modes of action: boscalid (respiration inhibitor), iprodione (unclear mode of action), thiophanate methyl (inhibition of microtubulin synthesis) and azoxystrobin and pyraclostrobin (quinone outside inhibitors). Mycelium of each isolate was inoculated onto a fungicide gradient and sub-cultured from the 50-100% inhibition zone for 12 generations and experiment repeated. Mutational changes were assessed for all isolates at six neutral microsatellite (SSR) loci and for a subset of isolates using amplified fragment length polymorphisms (AFLPs). SSR analysis showed 12 of 85 fungicide-exposed isolates had a total of 127 stepwise mutations with 42 insertions and 85 deletions. Most stepwise deletions were in iprodione- and azoxystrobin-exposed isolates (n = 40/85 each). Estimated mutation rates were 1.7 to 60-fold higher for mutated loci compared to that expected under neutral conditions. AFLP genotyping of 33 isolates (16 non-exposed control and 17 fungicide exposed) generated 602 polymorphic alleles. Cluster analysis with principal coordinate analysis (PCoA) and discriminant analysis of principal components (DAPC) identified fungicide-exposed isolates as a distinct group from non-exposed control isolates (PhiPT = 0.15, P = 0.001). Dendrograms based on neighbor-joining also supported allelic variation associated with fungicide-exposure. Fungicide sensitivity of isolates measured throughout both experiments did not show consistent trends. For example, eight isolates exposed to boscalid had higher EC50 values at the end of the experiment, and when repeated, only one isolate had higher EC50 while most isolates showed no difference. Results of this support the hypothesis that sublethal fungicide stress increases mutation rates in a largely clonal plant pathogen under in vitro conditions. Collectively, this work will aid our understanding how non-lethal fungicide exposure may affect genomic variation, which may be an important mechanism of novel trait emergence, adaptation, and evolution for clonal organisms.

Dataset Information

The evolutionary and molecular features of the broad-host-range plant pathogen Sclerotinia sclerotiorum.

Publications

The evolutionary and molecular features of the broad-host-range plant pathogen Sclerotinia sclerotiorum.

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