Mitochondrial genomes reveal recombination in the presumed asexual Fusarium oxysporum species complex

Delineating species and epidemic lineages in fungal plant pathogens is critical to our understanding of disease emergence and the structure of fungal biodiversity and also informs international regulatory decisions. Pyricularia oryzae (syn. Magnaporthe oryzae) is a multihost pathogen that infects multiple grasses and cereals, is responsible for the most damaging rice disease (rice blast), and is of growing concern due to the recent introduction of wheat blast to Bangladesh from South America. However, the genetic structure and evolutionary history of M. oryzae, including the possible existence of cryptic phylogenetic species, remain poorly defined. Here, we use whole-genome sequence information for 76 M. oryzae isolates sampled from 12 grass and cereal genera to infer the population structure of M. oryzae and to reassess the species status of wheat-infecting populations of the fungus. Species recognition based on genealogical concordance, using published data or extracting previously used loci from genome assemblies, failed to confirm a prior assignment of wheat blast isolates to a new species (Pyricularia graminis-tritici). Inference of population subdivisions revealed multiple divergent lineages within M. oryzae, each preferentially associated with one host genus, suggesting incipient speciation following host shift or host range expansion. Analyses of gene flow, taking into account the possibility of incomplete lineage sorting, revealed that genetic exchanges have contributed to the makeup of multiple lineages within M. oryzae. These findings provide greater understanding of the ecoevolutionary factors that underlie the diversification of M. oryzae and highlight the practicality of genomic data for epidemiological surveillance in this important multihost pathogen.IMPORTANCE Infection of novel hosts is a major route for disease emergence by pathogenic microorganisms. Understanding the evolutionary history of multihost pathogens is therefore important to better predict the likely spread and emergence of new diseases. Magnaporthe oryzae is a multihost fungus that causes serious cereal diseases, including the devastating rice blast disease and wheat blast, a cause of growing concern due to its recent spread from South America to Asia. Using wholegenome analysis of 76 fungal strains from different hosts, we have documented the divergence of M. oryzae into numerous lineages, each infecting a limited number of host species. Our analyses provide evidence that interlineage gene flow has contrib-

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“…We used an implementation of the GCPSR scalable to genomic data (https://github.com/b-brankovics/GCPSR) (69). The method works in two steps.…”

Section: Methodsmentioning

confidence: 99%

Gene Flow between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus Magnaporthe oryzae

Gladieux

Condon

Ravel

et al. 2018

mBio

175

206

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“…The mitochondrial genome consists of two regions, a conserved region with relatively low levels of sequence variation and the large variable region (LV) [22] containing numerous sequence variations [23]. Sequence variations in this region are due to recombination events caused by parasexualism and this has resulted in three variant type sequences within the mitochondrial genome in FOSC [23]. Mt genome sequences have been used in molecular systematics and biodiversity studies of fungi at various taxonomic levels [24].…”

Section: Introductionmentioning

confidence: 99%

“…Mt genome sequences have been used in molecular systematics and biodiversity studies of fungi at various taxonomic levels [24]. Three clades were identified in a phylogenetic analysis of the FOSC using the conserved region of the mt genome in combination with nine nuclear protein coding genes [23].…”

Section: Introductionmentioning

confidence: 99%

Phylogenetic relationship between Australian Fusarium oxysporum isolates and resolving the species complex using the multispecies coalescent model

et al. 2020

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Background: The Fusarium oxysporum species complex (FOSC) is a ubiquitous group of fungal species readily isolated from agroecosystem and natural ecosystem soils which includes important plant and human pathogens. Genetic relatedness within the complex has been studied by sequencing either the genes or the barcoding gene regions within those genes. Phylogenetic analyses have demonstrated a great deal of diversity which is reflected in the differing number of clades identified: three, five and eight. Genetic limitation within the species in the complex has been studied through Genealogical Concordance Phylogenetic Species Recognition (GCPSR) analyses with varying number of phylogenetic 'species' identified ranging from two to 21. Such differing views have continued to confuse users of these taxonomies. Results: The phylogenetic relationships between Australian F. oxysporum isolates from both natural and agricultural ecosystems were determined using three datasets: whole genome, nuclear genes, and mitochondrial genome sequences. The phylogenies were concordant except for three isolates. There were three concordant clades from all the phylogenies suggesting similar evolutionary history for mitochondrial genome and nuclear genes for the isolates in these three clades. Applying a multispecies coalescent (MSC) model on the eight single copy nuclear protein coding genes from the nuclear gene dataset concluded that the three concordant clades correspond to three phylogenetic species within the FOSC. There was 100% posterior probability support for the formation of three species within the FOSC. This is the first report of using the MSC model to estimate species within the F. oxysporum species complex. The findings from this study were compared with previously published phylogenetics and species delimitation studies. Conclusion: Phylogenetic analyses using three different gene datasets from Australian F. oxysporum isolates have all supported the formation of three major clades which delineated into three species. Species 2 (Clade 3) may be called F. oxysporum as it contains the neotype for F. oxysporum.

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“…Fusarium oxysporum is an ascomycete, soilborne, and pathogenic fungus (Alabouvette and Couteaudier 1992;Fravel et al 2003). Owing to next generation sequencing technologies, more than 60 fungal mitogenomes have been assembled (Pantou et al 2008;Fourie et al 2013;Brankovics et al 2017;Park et al, in preparation). These mitogenomes cover only nine out of around 120 formae speciales, suggesting mitogenomes of more formae speciales should be investigated to understand their genetic diversities as well as host-specificity.…”

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confidence: 99%

“…Geneious R11 11.0.5 (Biomatters Ltd, Auckland, New Zealand) was used to annotate its mitochondrial genome by comparing with that of F. oxysporum f. sp. cucumerinum (LT906315; Brankovics et al 2017).…”

mentioning

confidence: 99%

Complete mitochondrial genome sequence of lettuce pathogenic fungus, Fusarium oxysporum f. sp. lactucae 16-086

Kwon¹,

Park²,

Kim

et al. 2019

Mitochondrial DNA Part B

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Fusarium oxysporum f. sp. lactucae 016-086 is a plant pathogenic filamentous fungus isolated from wilted lettuce in Korea. We reported complete mitochondrial genome sequence of F. oxysporum f. sp. lactucae 016-086. Total length of this mitogenome is 41,826 bp and it encoded 42 genes (14 proteincoding genes, 2 rRNAs, and 26 tRNAs). Nucleotide sequence of coding region takes over 30.6%, and overall GC content is 32.5%. Phylogenetic tree of Fusarium mitochondrial genomes presented distinct clades along with nine formae speciales. This mitogenome will contribute distinguishing formae speciales of F. oxysoporum claearly with additional mitogenomes sequenced in the near future. ARTICLE HISTORY

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Mitochondrial genomes reveal recombination in the presumed asexual Fusarium oxysporum species complex

Cited by 60 publications

References 40 publications

Gene Flow between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus Magnaporthe oryzae

Gene Flow between Divergent Cereal- and Grass-Specific Lineages of the Rice Blast Fungus Magnaporthe oryzae

Phylogenetic relationship between Australian Fusarium oxysporum isolates and resolving the species complex using the multispecies coalescent model

Complete mitochondrial genome sequence of lettuce pathogenic fungus, Fusarium oxysporum f. sp. lactucae 16-086

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