Comparative genome analysis indicates high evolutionary potential of pathogenicity genes in Colletotrichum tanaceti

Colletotrichum tanaceti is an emerging foliar fungal pathogen of commercially grown pyrethrum (Tanacetum cinerariifolium). Despite being reported consistently from field surveys in Australia, the molecular basis of pathogenicity of C. tanaceti on pyrethrum is unknown. Herein, the genome of C. tanace...

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Bibliographic Details
Published in:PloS one 2019-05, Vol.14 (5), p.e0212248-e0212248
Main Authors: Lelwala, Ruvini V, Korhonen, Pasi K, Young, Neil D, Scott, Jason B, Ades, Peter K, Gasser, Robin B, Taylor, Paul W J
Format: Article
Language:English
Subjects:
Biological evolution
Biology and Life Sciences
Chrysanthemum cinerariifolium - microbiology
Clustering
Colletotrichum
Colletotrichum - genetics
Colletotrichum - pathogenicity
Comparative analysis
Disease control
Evolution
Evolution, Molecular
Evolutionary genetics
Genes
Genome, Fungal
Genomes
Genomics
Kinases
Medicine and Health Sciences
Metabolites
Mutation
Pathogenicity
Pathogens
Plant Diseases - microbiology
Secondary metabolites
Species
Transposition
Virulence - genetics
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Summary:Colletotrichum tanaceti is an emerging foliar fungal pathogen of commercially grown pyrethrum (Tanacetum cinerariifolium). Despite being reported consistently from field surveys in Australia, the molecular basis of pathogenicity of C. tanaceti on pyrethrum is unknown. Herein, the genome of C. tanaceti (isolate BRIP57314) was assembled de novo and annotated using transcriptomic evidence. The inferred putative pathogenicity gene suite of C. tanaceti comprised a large array of genes encoding secreted effectors, proteases, CAZymes and secondary metabolites. Comparative analysis of its putative pathogenicity gene profiles with those of closely related species suggested that C. tanaceti likely has additional hosts to pyrethrum. The genome of C. tanaceti had a high repeat content and repetitive elements were located significantly closer to genes inferred to influence pathogenicity than other genes. These repeats are likely to have accelerated mutational and transposition rates in the genome, resulting in a rapid evolution of certain CAZyme families in this species. The C. tanaceti genome showed strong signals of Repeat Induced Point (RIP) mutation which likely caused its bipartite nature consisting of distinct gene-sparse, repeat and A-T rich regions. Pathogenicity genes within these RIP affected regions were likely to have a higher evolutionary rate than the rest of the genome. This "two-speed" genome phenomenon in certain Colletotrichum spp. was hypothesized to have caused the clustering of species based on the pathogenicity genes, to deviate from taxonomic relationships. The large repertoire of pathogenicity factors that potentially evolve rapidly due to the plasticity of the genome, indicated that C. tanaceti has a high evolutionary potential. Therefore, C. tanaceti poses a high-risk to the pyrethrum industry. Knowledge of the evolution and diversity of the putative pathogenicity genes will facilitate future research in disease management of C. tanaceti and other Colletotrichum spp.
ISSN:1932-6203
1932-6203
DOI:10.1371/journal.pone.0212248