Emergence of new virulent populations of apple scab from nonagricultural disease reservoirs

Lemaire, Christophe; Gracia, Marie de; Leroy, Thibault; Michalecka, Monika; Lindhard-Pedersen, Hanne; Guérin, Fabien; Gladieux, Pierre; Cam, Bruno Le

doi:10.1111/nph.13658

Cited by 42 publications

(54 citation statements)

References 75 publications

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“…Many of the grass or cereal species that are hosts to M. oryzae are widely cultivated as staple crops or widely distributed as pasture or weeds, including "universal suscepts" such as barley, Italian ryegrass, tall fescue, and weeping lovegrass (40), increasing the chance for encounters and mating between isolates with overlapping host ranges. These shared hosts may act as a platform facilitating encounters and mating between fertile and compatible isolates from different lineages, thereby enabling interlineage gene flow (51). Plant health vigilance is therefore warranted for disease emergence via recombination in regions where multiple lineages are in contact and shared hosts are present.…”

Section: Discussionmentioning

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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186

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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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Section: Discussionmentioning

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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186

206

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“…From such studies, we know that some important crop pathogens have emerged from pathogen populations initially found on wild hosts, e.g. the septoria tritici leaf blotch pathogen Z. tritici [7,29], the rice blast pathogen P. oryzae [26] and the apple scab pathogen V. inaequalis [30]. The domesticated crop-infecting rstb.royalsocietypublishing.org Phil.…”

Section: Introductionmentioning

confidence: 99%

Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security

McDonald

Stukenbrock

2016

Phil. Trans. R. Soc. B

282

199

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Agricultural ecosystems are composed of genetically depauperate populations of crop plants grown at a high density and over large spatial scales, with the regional composition of crop species changing little from year to year. These environments are highly conducive for the emergence and dissemination of pathogens. The uniform host populations facilitate the specialization of pathogens to particular crop cultivars and allow the build-up of large population sizes. Population genetic and genomic studies have shed light on the evolutionary mechanisms underlying speciation processes, adaptive evolution and long-distance dispersal of highly damaging pathogens in agro-ecosystems. These studies document the speed with which pathogens evolve to overcome crop resistance genes and pesticides. They also show that crop pathogens can be disseminated very quickly across and among continents through human activities. In this review, we discuss how the peculiar architecture of agro-ecosystems facilitates pathogen emergence, evolution and dispersal. We present four example pathosystems that illustrate both pathogen specialization and pathogen speciation, including different time frames for emergence and different mechanisms underlying the emergence process. Lastly, we argue for a re-design of agro-ecosystems that embraces the concept of dynamic diversity to improve their resilience to pathogens. This article is part of the themed issue ‘Tackling emerging fungal threats to animal health, food security and ecosystem resilience’.

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“…The virulent Rvi6 strains can thus infect the non‐ Rvi6 hosts, come into contact with the other strains, and mate, allowing introgression to occur. As Rvi6 resistance gene is nowadays overcome in many dessert apple orchards in Europe where hybridization events were becoming common (Lemaire et al ., ), evolutionary and epidemiologic changes are probably ongoing in apple scab. At site 2, habitat alteration associated with planting numerous Rvi6 hosts into closer proximity of susceptible hosts in the orchard has probably speeded up the process of introgression by allowing invasion of the non‐ Rvi6 hosts by the virulent Rvi6 strains.…”

Section: Discussionmentioning

confidence: 99%

When virulence originates from nonagricultural hosts: evolutionary and epidemiological consequences of introgressions following secondary contacts inVenturia inaequalis

et al. 2016

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SummaryIn pathogens, introgressions through secondary contacts between divergent populations from agricultural and nonagricultural disease reservoirs are expected to have crucial evolutionary and epidemiological implications. Despite the importance of this question for disease management, experimental demonstrations of these implications remain scarce.Recently, we identified a virulent population of the apple scab pathogen Venturia inaequalis that migrated from nonagricultural hosts to European domestic apple orchards. Here, we investigated the occurrence of gene flow between agricultural and nonagricultural populations sampled in two orchards, and thereafter its consequences on the pathogenicity of hybrids.Population genetic structure and demographic inferences based on the genotypes of 104 strains revealed a high amount of gene flow between the two populations in one orchard. In this site, mating between populations was made possible by the presence of a common host. Our results revealed an invasion of the virulent trait in the agricultural population; a main direction of introgression in hybrids from the agricultural to nonagricultural genetic backgrounds; and a population of hybrids with transgressive traits.We demonstrate a secondary contact with gene flow between divergent populations of pathogens. Our findings highlight evolutionary and epidemiological changes in pathogens and have concrete implications for sustainable disease management.

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Emergence of new virulent populations of apple scab from nonagricultural disease reservoirs

Cited by 42 publications

References 75 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

Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security

When virulence originates from nonagricultural hosts: evolutionary and epidemiological consequences of introgressions following secondary contacts inVenturia inaequalis

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