Temporal and Spatial Genetic Population Structure of <i>Cryphonectria parasitica</i> and Its Associated Hypovirus Across an Invasive Range of Chestnut Blight in Europe

Ježić, Marin; Schwarz, Janine Melanie; Prospero, Simone; Sotirovski, Kiril; Risteski, Mihajlo; Ćurković‐Perica, Mirna; Nuskern, Lucija; Krstin, Ljiljana; Katanić, Zorana; Maleničić, Ema; Poljak, Igor; Idžojtić, Marilena; Rigling, Daniel

doi:10.1094/phyto-09-20-0405-r

Cited by 11 publications

(23 citation statements)

References 69 publications

(74 reference statements)

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“…Both in the 1990s and in 2019, Ticino populations were largely dominated by vc types EU‐01, EU‐02 and EU‐05 (and partially EU‐06), which are the most frequent vc types in central Europe (Robin & Heiniger, 2001). A relative stability of vc type diversity over time was also recently reported by Ježić et al (2021) for other C. parasitica populations in Switzerland, Croatia and North Macedonia. These results of retained low vc type diversity in the presence of a deleterious mycovirus are in striking contrast to findings on the invasive forest pathogen Ophiostoma novo ‐ ulmi , the causal agent of Dutch elm disease.…”

Section: Discussionsupporting

confidence: 81%

Temporal changes in pathogen diversity in a perennial plant–pathogen–hyperparasite system

2022

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Hyperparasites can affect the evolution of pathosystems by influencing the stability of both pathogen and host populations. However, how pathogens of perennial hosts evolve in the presence of a hyperparasite has rarely been studied. Here, we investigated temporal changes in genetic diversity of the invasive chestnut blight pathogen Cryphonectria parasitica in the presence of its parasitic mycovirus Cryphonectria hypovirus 1 (CHV1). The virus reduces fungal virulence and represents an effective natural biocontrol agent against chestnut blight in Europe. We analysed genome‐wide diversity and CHV1 prevalence in C. parasitica populations in southern Switzerland that were sampled twice at an interval of about 30 years. Overall, we found that both pathogen population structure and CHV1 prevalence were retained over time. The results suggest that recent bottlenecks have influenced the structure of C. parasitica populations in southern Switzerland. Strong balancing selection signals were found at a single vegetative incompatibility (vic) locus, consistent with negative frequency‐dependent selection imposed by the vegetative incompatibility system. High levels of mating among related individuals (i.e., inbreeding) and genetic drift are probably at the origin of imbalanced allele ratios at vic loci and subsequently low vc type diversity. Virus infection rates were stable at ~30% over the study period and we found no significant impact of the virus on fungal population diversity. Consequently, the efficacy of CHV1‐mediated biocontrol was probably retained.

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Section: Discussionsupporting

confidence: 81%

Temporal changes in pathogen diversity in a perennial plant–pathogen–hyperparasite system

2022

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“…Reduced landscape connectivity between the sites in Croatia is supported by previous studies, which showed a reduced diversity of the fungal host in Kast relative to other Croatian sites ( Ježić et al. 2018 , 2021 ).…”

Section: Discussionsupporting

confidence: 74%

“…Historically, characterizing intra-host virus populations was limited by sequencing capabilities that constrained researchers to host-level virus consensus sequences (often at small amplicons e.g.< 600 base pairs ‘bp’, Kinoti et al. 2017 ; Ježić et al. 2021 ) or a small number of intra-host haplotypes obtained through cloning and Sanger sequencing (e.g.…”

Section: Introductionmentioning

confidence: 99%

Long-read sequencing reveals the evolutionary drivers of intra-host diversity across natural RNA mycovirus infections

et al. 2021

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Intra-host dynamics are a core component of virus evolution but most intra-host data comes from a narrow range of hosts or experimental infections. Gaining broader information on the intra-host diversity and dynamics of naturally occurring virus infections is essential to our understanding of evolution across the virosphere. Here we used PacBio long read HiFi sequencing to characterize the intra-host populations of natural infections of the RNA mycovirus Cryphonectria hypovirus 1 (CHV1). CHV1 is a biocontrol agent for the chestnut blight fungus (Cryphonectria parasitica), which co-invaded Europe alongside the fungus. We characterized the mutational and haplotypic intra-host virus diversity of 38 natural CHV1 infections spread across four locations in Croatia and Switzerland. Intra-host CHV1 diversity values were shaped by purifying selection and accumulation of mutations over time, as well as epistatic interactions within the host genome at defense loci. Geographical landscape features impacted CHV1 inter-host relationships through restricting dispersal and causing founder effects. Interestingly, a small number of intra-host viral haplotypes showed high sequence similarity across large geographical distances unlikely to be linked by dispersal.

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“…The most remarkable result from our data is the presence of 51 different microsatellite haplotypes of C. parasitica in a geographic region as small as South Tyrol. This diversity is considerably higher than in many other European populations, for example, 57 haplotypes were found collectively in Switzerland, Croatia and Macedonia [33]. In addition, we found three genetic clusters in the region, whereas two different clusters were found in a multinational study; one in Switzerland and Croatia and another in Macedonia [33].…”

Section: Discussioncontrasting

confidence: 60%

“…A close relationship between the genotypes found in South Tyrol and those found in neighboring regions, such as northern Italy and Switzerland, was depicted in the PCoA, which also indicates that the direct introduction of genotypes to South Tyrol from China or Japan is unlikely as both clusters were clearly separated. A recent study also found that most of the central-western European populations of C. parasitica could be related to the first introduction event to Italy in the 1930s [33]. The high VC-type and microsatellite haplotype diversity in the region led us to hypothesize that the neighboring populations may have actively played a role in increasing local genetic diversity through natural dissemination or human-mediated transmission.…”

Section: Discussionmentioning

confidence: 91%

Microsatellite Analysis Revealing High Genetic Diversity of the Chestnut Blight Fungus in South Tyrol (Northern Italy)

Ahmad

Baric

2022

Forests

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Cryphonectria parasitica, which causes chestnut blight, is one of the most important pathogens of forest trees. In Europe, mycovirus-mediated biocontrol is the most efficient method to control the disease but can be impeded by the lack of information about the population structure of the fungus within a region. In particular, sexual reproduction and the new introduction of the pathogen can complicate biocontrol strategies. For this reason, this study aimed to determine the population structure of C. parasitica, which causes chestnut blight, in the northern Italian region of South Tyrol, using eleven multilocus microsatellite markers. Fifty-one haplotypes were found across South Tyrol, belonging to three divergent clusters. Recombinant genotypes demonstrated that sexual reproduction occurs across the different clusters. The most dominant genotypes in the region were also the most dominant in neighboring areas, such as Switzerland, northern Italy and France. All of the clusters from South Tyrol were related to the Italian genotype pool and are thought to have been introduced from northern Italian and other European populations due to naturally occurring gene flow or human-mediated introduction. At least three separate introduction events of C. parasitica might have happened in South Tyrol that could be separated by time. This study demonstrated a high genetic diversity of C. parasitica in South Tyrol and helped to shed light on the sexual reproduction and introduction events in the local populations.

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Temporal and Spatial Genetic Population Structure of Cryphonectria parasitica and Its Associated Hypovirus Across an Invasive Range of Chestnut Blight in Europe

Cited by 11 publications

References 69 publications

Temporal changes in pathogen diversity in a perennial plant–pathogen–hyperparasite system

Temporal changes in pathogen diversity in a perennial plant–pathogen–hyperparasite system

Long-read sequencing reveals the evolutionary drivers of intra-host diversity across natural RNA mycovirus infections

Microsatellite Analysis Revealing High Genetic Diversity of the Chestnut Blight Fungus in South Tyrol (Northern Italy)

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