Linking the emergence of fungal plant diseases with ecological speciation

Giraud, Tatiana; Gladieux, Pierre; Gavrilets, Sergey

doi:10.1016/j.tree.2010.03.006

Cited by 295 publications

(320 citation statements)

References 69 publications

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“…However, the long-distance wind dispersal of the sexually produced ascospores of Zymoseptoria species argues against this suggestion. Instead, ecological divergence driven by local adaptation or host specialization, as observed for other plant pathogenic species (21,22), seems a more likely explanation for the isolation and differentiation of lineages within Zymoseptoria. We have not been able to identify the parental species of Z. pseudotritici in our collections of pathogens from the studied region in Iran.…”

Section: Discussionmentioning

confidence: 97%

Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species

Stukenbrock

Christiansen

Hansen

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

178

133

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In a genome alignment of five individuals of the ascomycete fungus Zymoseptoria pseudotritici, a close relative of the wheat pathogen Z. tritici (synonym Mycosphaerella graminicola), we observed peculiar diversity patterns. Long regions up to 100 kb without variation alternate with similarly long regions of high variability. The variable segments in the genome alignment are organized into two main haplotype groups that have diverged ∼3% from each other. The genome patterns in Z. pseudotritici are consistent with a hybrid speciation event resulting from a cross between two divergent haploid individuals. The resulting hybrids formed the new species without backcrossing to the parents. We observe no variation in 54% of the genome in the five individuals and estimate a complete loss of variation for at least 30% of the genome in the entire species. A strong population bottleneck following the hybridization event caused this loss of variation. Variable segments in the Z. pseudotritici genome exhibit the two haplotypes contributed by the parental individuals. From our previously estimated recombination map of Z. tritici and the size distribution of variable chromosome blocks untouched by recombination we estimate that the hybridization occurred ∼380 sexual generations ago. We show that the amount of lost variation is explained by genetic drift during the bottleneck and by natural selection, as evidenced by the correlation of presence/ absence of variation with gene density and recombination rate. The successful spread of this unique reproductively isolated pathogen highlights the strong potential of hybridization in the emergence of pathogen species with sexual reproduction. species dynamics | incipient species | population genomics | genome mosaic | genome scans

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Section: Discussionmentioning

confidence: 97%

Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species

Stukenbrock

Christiansen

Hansen

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

178

133

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“…It also exceeds values used in mathematical models of ecological speciation in which adaptive divergence is sufficient to generate reproductive isolation in discrete habitats (49,50) or along clines (51,52). The long period between when a larva settles and when it becomes a colony that contributes genetically to the next generation thus decreases gene flow between depth-adapted lineages and enhances the opportunity for habitat-specific selection and divergent adaptation.…”

Section: Discussionmentioning

confidence: 99%

Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral

Prada

Hellberg

2013

Proc. Natl. Acad. Sci. U.S.A.

139

192

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Long-lived corals, the foundation of modern reefs, often follow ecological gradients, so that populations or sister species segregate by habitat. Adaptive divergence maintains sympatric congeners after secondary contact or may even generate species by natural selection in the face of gene flow. Such ecological divergence, initially between alternative phenotypes within populations, may be aided by immigrant inviability, especially when a long period separates larval dispersal and the onset of reproduction, during which selection can sort lineages to match different habitats. Here, we evaluate the strength of one ecological factor (depth) to isolate populations by comparing the genes and morphologies of pairs of depth-segregated populations of the candelabrum coral Eunicea flexuosa across the Caribbean. Eunicea is endemic to the Caribbean and all sister species co-occur. Eunicea flexuosa is widespread both geographically and across reef habitats. Our genetic analysis revealed two depth-segregated lineages. Field survivorship data, combined with estimates of selection coefficients based on transplant experiments, suggest that selection is strong enough to segregate these two lineages. Genetic exchange between the Shallow and Deep lineages occurred either immediately after divergence or the two have diverged with gene flow. Migration occurs asymmetrically from the Shallow to Deep lineage. Limited recruitment to reproductive age, even under weak annual selection advantage, is sufficient to generate habitat segregation because of the cumulative prolonged prereproductive selection. Ecological factors associated with depth can act as filters generating strong barriers to gene flow, altering morphologies, and contributing to the potential for speciation in the sea.

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“…Under controlled conditions, most lineages have at least one host in common (40), and strains within one lineage can still cause rare susceptible lesions on naive hosts (21,47). Moreover, a single plant infected by a single genotype can produce large numbers of spores in a single growing season (48), allowing the pathogen to persist on an alternative host even if selection is strong and promoting the rapid and repeated creation of genetic variation (6). Although some of these features appear to be antagonistic to the possibility of divergence by host specialization within M. oryzae, our finding that the different lineages within M. oryzae tend to be sampled on a single host suggests that ecologic barriers alone may in fact contribute to reduce gene flow substantially between host-specific lineages.…”

Section: Discussionmentioning

confidence: 99%

“…Many plant-pathogenic ascomycete fungi are host specific, and some of their life history traits have been shown to be conducive to the emergence of novel pathogen species adapted to new hosts (6,7). Investigating population structure within multihost ascomycetes thus offers a unique opportunity to identify the genomic features associated with recent host range expansions or host shifts.…”

mentioning

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

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192

206

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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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Linking the emergence of fungal plant diseases with ecological speciation

Cited by 295 publications

References 69 publications

Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species

Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species

Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral

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

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