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

Abstract

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.

Million years old recombination suppression and balancing selection in a region partially linked to the mating-type locus in the invasive chestnut blight fungal pathogenCryphonectria parasitica

“…Noteworthy, we also found blocks of high LD (r²>0.9) around three vic loci (i.e., vic2, vic6 and vic7 on scaffold_3, scaffold_6, and scaffold_7; Fig S2C), known to be involved in vegetative incompatibility (vic) and under balancing selection in C. parasitica (24,36). These high-LD blocks were smaller than the MAT-proximal region but nevertheless larger than elsewhere in the genome (across more than 100 kb, In agreement with the view of a partial linkage with the mating-type locus, the two genetic clusters in the MAT-proximal region appeared strongly associated with mating types, although the association did not reach 100% (Figs 2A and D; Fig S3 , Table 1).…”

“…A situation that may correspond to this theoretically predicted case has been reported in the invasive chestnut blight fungal pathogen Cryphonectria parasitica, where a large region without recombination was suggested to occur near the mating-type locus, although not completely linked to it (i.e., at 3.9 cM of the mating-type locus), based on segregation of RAPD and RFLP markers in three crosses involving five different parents, from the USA, Japan or Italy (22). Recent genome-wide association studies in a worldwide collection and in local C. parasitica populations in southern Switzerland found significant association of SNPs with the mating-type locus across a large region (>1 Mb), further suggesting the existence of reduced recombination in this region (23,24). This genomic region was enriched in SNPs, transposable elements and copy-number variants, such as deletions, which are consistent with sequence degeneration and a lack of recombination (23), and which prevented its assembly so far.…”

“…In C. parasitica, the mating-type locus displays two alleles (MAT-1 and MAT-2) that are both permanently heterozygous in the diploid and dikaryotic stages (25). Although this ascomycete fungus is mostly found as haploid mycelia, some isolates have been reported to be heterokaryotic at the mating-type locus in several invasive European and North American populations, i.e., carrying different nuclei, of the opposite mating types MAT-1 and MAT-2 (23,24,(26)(27)(28). The theoretical model based on recessive deleterious mutations showed that non-recombining fragments could be selected for even with a substantial fraction of the life cycle being haploid (19).…”

Applying molecular and genetic methods to trees and their fungal communities

“…Among changes in hundreds of other DEGs, cryparin expression is down-regulated by the single-stranded RNA Cryphonectria hypervirus 1 (CHV1) infection (Chun et al 2020 ) which in viral disease reduces the pathogenic potential (hypovirulence), concomitantly with fungal yellow-orange pigmentation and sporulation in wounds of trees, by altering gene expression patterns of its fungal host. Therefore, CHV1 is used as a natural sustainable biocontrol agent to protect chestnuts (Eusebio-Cope et al 2015 ; Rigling and Prospero 2018 ; Stauber et al 2022 ).…”

Stepwise recombination suppression around the mating-type locus in an ascomycete fungus with self-fertile spores

“…There is indeed no recombination suppression around the mating-type locus reported so far in true heterothallic ascomycetes, as seen in available genetic maps [32][33][34][35][36][37][38][39][40][41]. An exception is Cryphonectria parasitica [42], in which dikaryons are nevertheless relatively frequently isolated in nature [43][44][45]. One hypothesis that could account for this association between pseudo-homothallism and recombination suppression around the mating-type locus in ascomycetes is that most strains are heterokaryotic at the mating-type locus for most of their life cycle in pseudo-homothallic ascomycetes, while heterothallic ascomycetes have a dominant haploid (or monokaryotic) phase.…”