Mitotic recombination and a two-speed genome shape the evolution of asexual lineages of the sudden oak death pathogen Phytophthora ramorum

Authors: DALE, A - University Of British Columbia; FEAU, N - University Of British Columbia; EVERHART, S - University Of Nebraska; DHILLON, B - University Of British Columbia; WONG, B - University Of British Columbia; SHEPPARD, J - University Of British Columbia; BILODEAU, G - Canadian Food Inspection Agency; BRAR, A - Canadian Food Inspection Agency; TABIMA, J - Oregon State University; BRASIER, C - Forestry Commission; Grunwald, Niklaus - Nik; HAMELIN, R - University Of British Columbia

Submitted to: mBio
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/29/2019
Publication Date: 3/12/2019
Citation: Dale, A.L., Feau, N., Everhart, S.E., Dhillon, B., Wong, B., Sheppard, J., Bilodeau, G.J., Brar, A., Tabima, J.F., Brasier, C.M., Grunwald, N.J., Hamelin, R.C. 2019. Mitotic recombination and a two-speed genome shape the evolution of asexual lineages of the sudden oak death pathogen Phytophthora ramorum. mBio. 10(2):e02452-18. https://doi.org/10.1128/mBio.02452-18.
DOI: https://doi.org/10.1128/mBio.02452-18

Interpretive Summary: Invasive alien species often have reduced genetic diversity and face the challenge of adapting to new hosts and environments. Given the success of a large number of invasive alien species this has been called the genetic paradox of invasion. Phytophthora ramorum, an invasive alien pathogen responsible for sudden oak death and sudden larch death, reproduces asexually in North America and Europe. We sequenced the genomes of 107 individuals of the four known clonal lineages of P. ramorum to compare genome diversity and evolutionary patterns and to gain insight into the paradox of invasion. Evolution of the asexual lineages of the invasive P. ramorum appears to be accelerated by both genetic recombination that increases genotypic diversity and rapid turnover of effectors and other genes involved in pathogenicity in regions enriched for repetitive elements. This work provides novel insights into mechanisms whereby microorganisms evolve in the absence of sex and sheds new light on patterns of emergence of the sudden oak death pathogen.

Technical Abstract: Invasive alien species often have reduced genetic diversity and face the challenge of adapting to new hosts and environments. Given the success of a large number of invasive alien species this has been called the genetic paradox of invasion. Phytophthora ramorum, an invasive alien pathogen responsible for sudden oak death and sudden larch death reproduces asexually in North America and Europe. We sequenced the genomes of 107 individuals of the four known clonal lineages of P. ramorum to compare genome diversity and evolutionary patterns and to gain insight into the paradox of invasion. We estimate that these lineages diverged approximately 0.75 million years ago for the split between EU1 and NA1 and 1.3 MYA for the split between EU2 and the other lineages. We discovered extensive mitotic recombination that generates genetic diversity in all lineages by producing runs of homozygosity (ROH). Mitotic recombination breakpoints were associated with transposons in regions with low gene density. One ROH region fixed in all NA1 individuals sequenced was enriched in putative pathogenicity genes and in transposons, suggesting a selective sweep. Remarkably, an ROH resulting in the opposite haplotype in that region was present in eight EU1 individuals, suggesting an independent event and a mitotic recombination hotspot. There was a large core genome (>98%) shared by all lineages; however there were also non-core genomic regions and lineage specific regions. The non-core regions were enriched in putative pathogenicity genes and transposons. Non-core regions appeared to be shaped by a genome defense mechanism producing distinct characteristics than the core genome. A striking pattern of gene loss was observed in the non-core genome of the EU2 lineage including loss of all pathogenicity effectors. Evolution of the asexual lineages of the invasive P. ramorum appears to be accelerated by both mitotic recombination that increases genotypic diversity and a two-speed genome that allows for rapid turnover of effectors and other genes involved in pathogenicity.