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Using genomic data to understand anthropogenic influences on Oomycete and Phytophthora communities, and the evolution of an alien invasive species responsible for sudden oak death, Phytophthora ramorum Dale, Angela

Abstract

Emerging Phytophthora pathogens, often introduced, represent a threat to natural ecosystems. Phytophthora species are known for rapid adaptation and hybridization, which may be facilitated by anthropogenic activities. Little is known about natural Phytophthora and oomycete populations, or mechanisms behind rapid adaptation. We surveyed oomycete and Phytophthora communities from southwest B.C. under varying anthropogenic influences (urban, interface, natural) to determine effects on diversity, introductions and migration. We used DNA meta-barcoding to address these questions on oomycetes. We then focused on Phytophthora, adding baiting and culturing methods, and further sub-dividing urban sites into agricultural or residential. Finally, we studied an alien invasive species, Phytophthora ramorum responsible for sudden oak death, and how it overcame the invasion paradox, limited to asexual reproduction and presumed reduced adaptability. Anthropogenic activities increase oomycete and Phytophthora diversity. Putative introduced species and hybrids were more frequent in urban sites. Migration is suggested by shared species between urban and interface sites, and two known invasive species found in natural and interface sites. Different anthropogenic activities influence different communities. Abundance increased for some species in either residential or agricultural sites. Two hybrids appear to be spreading in different agricultural sites. In the invasive Phytophthora ramorum, mitotic recombination drives diversification of the four lineages (NA1, NA2, EU1 and EU2), generating runs of homozygosity. One genome region, enriched in putative plant pathogenicity genes and transposons, was fixed in NA1 and present in eight EU1 individuals, but affecting the opposite alleles. Longer lesions during initial colonization in inoculated larch and Douglas fir logs suggested a fitness advantage in these EU1 individuals. Mitotic recombination breakpoints were associated with transposons and low gene density. Non-core and lineage-specific genomic regions were enriched in putative plant pathogenicity genes and transposons. Gene loss was observed in the EU2 non-core genome affecting all effectors. A two-speed genome, where regions enriched in transposons and plant pathogenicity genes evolve faster, appears to drive non-core genome divergence, and mitotic recombination resulting in population evolution. This may explain invasion success and adaptability in Phytophthora pathogens. These results highlight the importance of anthropogenic activities in the emergence of forest diseases.

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Attribution-NonCommercial-NoDerivatives 4.0 International