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Invasion history and demographic pattern of Cryphonectria hypovirus 1 across European populations of the chestnut blight fungus.

ABSTRACT: We reconstructed the invasion history of the fungal virus Cryphonectria hypovirus 1 (CHV-1) in Europe, which infects the chestnut blight fungus Cryphonectria parasitica. The pattern of virus evolution was inferred based on nucleotide sequence variation from isolates sampled across a wide area in Europe at different points in time. Phylogeny and time estimates suggested that CHV-1 was introduced together with its fungal host to Europe and that it rapidly colonized the central range along the south facing slopes of the Alps and the north-east facing slopes of the Dinaric Alps. These central populations were the source for two waves of simultaneous invasions toward the southern Balkans and Turkey, as indicated by migration rates. Our results showed that the evolutionary scenarios for CHV-1 and C. parasitica were spatially congruent. As infection with CHV-1 reduces the pathogenicity of C. parasitica toward the chestnut tree, CHV-1 invasions of the newly established C. parasitica populations probably prevented the development of devastating chestnut blight epidemics in Europe. We propose that in this, and supposedly in other pathosystems, geographic, vegetation-related, demographic, economic, and political factors may help explain the correlated invasion pattern of a parasite and its host.

SUBMITTER: Bryner SF

PROVIDER: S-EPMC3539014 | biostudies-literature | 2012 Dec

REPOSITORIES: biostudies-literature

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Invasion history and demographic pattern of Cryphonectria hypovirus 1 across European populations of the chestnut blight fungus.

Bryner Sarah F SF Rigling Daniel D Brunner Patrick C PC

Ecology and evolution 20121122 12

We reconstructed the invasion history of the fungal virus Cryphonectria hypovirus 1 (CHV-1) in Europe, which infects the chestnut blight fungus Cryphonectria parasitica. The pattern of virus evolution was inferred based on nucleotide sequence variation from isolates sampled across a wide area in Europe at different points in time. Phylogeny and time estimates suggested that CHV-1 was introduced together with its fungal host to Europe and that it rapidly colonized the central range along the sout ...[more]

PMID: 23301186

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Project description:The ascomycete Cryphonectria parasitica causes destructive chestnut blight. Biological control of the fungus by virus infection (hypovirulence) has been shown to be an effective control strategy against chestnut blight in Europe. To provide biocontrol effects, viruses must be able to induce hypovirulence and spread efficiently in chestnut trees. Field studies using living trees to date have focused on a selected family of viruses called hypoviruses, especially prototypic hypovirus CHV1, but there are now known to be many other viruses that infect C. parasitica Here, we tested seven different viruses for their hypovirulence induction, biocontrol potential, and transmission properties between two vegetatively compatible but molecularly distinguishable fungal strains in trees. The test included cytosolically and mitochondrially replicating viruses with positive-sense single-stranded RNA or double-stranded RNA genomes. The seven viruses showed different in planta behaviors and were classified into four groups. Group I, including CHV1, had great biocontrol potential and could protect trees by efficiently spreading and converting virulent to hypovirulent cankers in the trees. Group II could induce high levels of hypovirulence but showed much smaller biocontrol potential, likely because of inefficient virus transmission. Group III showed poor performance in hypovirulence induction and biocontrol, while efficiently being transmitted in the infected trees. Group IV could induce hypovirulence and spread efficiently but showed poor biocontrol potential. Nuclear and mitochondrial genotyping of fungal isolates obtained from the treated cankers confirmed virus transmission between the two fungal strains in most isolates. These results are discussed in view of dynamic interactions in the tripartite pathosystem.IMPORTANCE The ascomycete Cryphonectria parasitica causes destructive chestnut blight, which is controllable by hypovirulence-conferring viruses infecting the fungus. The tripartite chestnut/C. parasitica/virus pathosystem involves the dynamic interactions of their genetic elements, i.e., virus transmission and lateral transfer of nuclear and mitochondrial genomes between fungal strains via anastomosis occurring in trees. Here, we tested diverse RNA viruses for their hypovirulence induction, biocontrol potential, and transmission properties between two vegetatively compatible but molecularly distinguishable fungal strains in live chestnut trees. The tested viruses, which are different in genome type (single-stranded or double-stranded RNA) and organization, replication site (cytosol or mitochondria), virus form (encapsidated or capsidless) and/or symptomatology, have been unexplored in the aforementioned aspects under controlled conditions. This study showed intriguing different in-tree behaviors of the seven viruses and suggested that to exert significant biocontrol effects, viruses must be able to induce hypovirulence and spread efficiently in the fungus infecting the chestnut trees.

Dataset Information

Invasion history and demographic pattern of Cryphonectria hypovirus 1 across European populations of the chestnut blight fungus.

Publications

Invasion history and demographic pattern of Cryphonectria hypovirus 1 across European populations of the chestnut blight fungus.

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