Emergence and diversification of a highly invasive chestnut pathogen lineage across south-eastern Europe

Abstract

Invasive microbial species constitute a major threat to biodiversity, agricultural production and human health. Invasions are often dominated by one or a small number of genotypes, yet the underlying factors driving invasions are poorly understood. The chestnut blight fungus Cryphonectria parasitica first decimated the American chestnut and a recent outbreak threatens European chestnut trees. To unravel the mechanisms underpinning the invasion of south-eastern Europe, we sequenced 188 genomes of predominantly European strains. Genotypes outside of the invasion zone showed high levels of diversity with evidence for frequent and ongoing recombination. The invasive lineage emerged from the highly diverse European genotype pool rather than a secondary introduction from Asia. The expansion across south-eastern Europe was mostly clonal and is dominated by a single mating type suggesting a fitness advantage of asexual reproduction. Our findings show how an intermediary, highly diverse bridgehead population gave rise to an invasive, largely clonally expanding pathogen.Data availabilityAll raw sequencing data is available on the NCBI Short Read Archive (BioProject PRJNA604575)

Comparative genomics analyses of lifestyle transitions at the origin of an invasive fungal pathogen in the genusCryphonectria

“…Table 1). All isolates were prepared for sequencing as described in Stauber et al (2020). Sequencing was conducted using the Illumina HiSeq4000 and Illumina NovaSeq platforms (Illumina, San Diego, USA) at the Functional Genomics Center Zurich (FGCZ).…”

“…By choosing the Illumina NovaSeq SP flowcell, NovaSeq reads were compatible with HiSeq4000 reads for downstream analysis. Several samples from Stauber et al (2020) were included in this study. All sample accession numbers for the NCBI Short Read Archive are available in Supplementary Table S1.…”

“…In Europe, chestnut blight was first observed in the 1930s and is nowadays present in all major chestnut growing areas (Rigling and Prospero, 2018). Following the colonization of Europe, C. parasitica has rapidly spread through most of southeastern Europe driven by the emergence of a highly successful lineage (Stauber et al 2020). The invasion success likely stems from the establishment of a highly diverse European bridgehead population and a switch to asexual reproduction (Stauber et al 2020).…”

“…Following the colonization of Europe, C. parasitica has rapidly spread through most of southeastern Europe driven by the emergence of a highly successful lineage (Stauber et al 2020). The invasion success likely stems from the establishment of a highly diverse European bridgehead population and a switch to asexual reproduction (Stauber et al 2020). Besides host species in the genus Castanea, C. parasitica has been occasionally reported on oaks (Quercus spp.…”

Comparative Genomics Analyses of Lifestyle Transitions at the Origin of an Invasive Fungal Pathogen in the GenusCryphonectria

“…In Europe, chestnut blight was first observed in the 1930s and is nowadays present in all major chestnut-growing areas ( 37 ). Following the colonization of Europe, C. parasitica has rapidly spread through most of southeastern Europe, driven by the emergence of a highly successful lineage ( 39 ). The invasion success likely stems from the establishment of a highly diverse European bridgehead population and a switch to asexual reproduction ( 39 ).…”