Dataset Information

Asexual Evolution and Forest Conditions Drive Genetic Parallelism in Phytophthora ramorum.

ABSTRACT: It is commonly assumed that asexual lineages are short-lived evolutionarily, yet many asexual organisms can generate genetic and phenotypic variation, providing an avenue for further evolution. Previous work on the asexual plant pathogen Phytophthora ramorum NA1 revealed considerable genetic variation in the form of Structural Variants (SVs). To better understand how SVs arise and their significance to the California NA1 population, we studied the evolutionary histories of SVs and the forest conditions associated with their emergence. Ancestral state reconstruction suggests that SVs arose by somatic mutations among multiple independent lineages, rather than by recombination. We asked if this unusual phenomenon of parallel evolution between isolated populations is transmitted to extant lineages and found that SVs persist longer in a population if their genetic background had a lower mutation load. Genetic parallelism was also found in geographically distant demes where forest conditions such as host density, solar radiation, and temperature, were similar. Parallel SVs overlap with genes involved in pathogenicity such as RXLRs and have the potential to change the course of an epidemic. By combining genomics and environmental data, we identified an unexpected pattern of repeated evolution in an asexual population and identified environmental factors potentially driving this phenomenon.

SUBMITTER: Yuzon JD

PROVIDER: S-EPMC7357085 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Asexual Evolution and Forest Conditions Drive Genetic Parallelism in <i>Phytophthora ramorum</i>.

Yuzon Jennifer David JD Travadon Renaud R Malar C Mathu M Tripathy Sucheta S Rank Nathan N Mehl Heather K HK Rizzo David M DM Cobb Richard R Small Corinn C Tang Tiffany T McCown Haley E HE Garbelotto Matteo M Kasuga Takao T

Microorganisms 20200622 6

It is commonly assumed that asexual lineages are short-lived evolutionarily, yet many asexual organisms can generate genetic and phenotypic variation, providing an avenue for further evolution. Previous work on the asexual plant pathogen <i>Phytophthora ramorum</i> NA1 revealed considerable genetic variation in the form of Structural Variants (SVs). To better understand how SVs arise and their significance to the California NA1 population, we studied the evolutionary histories of SVs and the for ...[more]

PMID: 32580470

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Project description:Invasive alien species often have reduced genetic diversity and must adapt to new environments. Given the success of many invasions, this is sometimes called the genetic paradox of invasion. Phytophthora ramorum is invasive, limited to asexual reproduction within four lineages, and presumed clonal. It is responsible for sudden oak death in the United States, sudden larch death in Europe, and ramorum blight in North America and Europe. We sequenced the genomes of 107 isolates to determine how this pathogen can overcome the invasion paradox. Mitotic recombination (MR) associated with transposons and low gene density has generated runs of homozygosity (ROH) affecting 2,698 genes, resulting in novel genotypic diversity within the lineages. One ROH enriched in effectors was fixed in the NA1 lineage. An independent ROH affected the same scaffold in the EU1 lineage, suggesting an MR hot spot and a selection target. Differences in host infection between EU1 isolates with and without the ROH suggest that they may differ in aggressiveness. Non-core regions (not shared by all lineages) had signatures of accelerated evolution and were enriched in putative pathogenicity genes and transposons. There was a striking pattern of gene loss, including all effectors, in the non-core EU2 genome. Positive selection was observed in 8.0% of RxLR and 18.8% of Crinkler effector genes compared with 0.9% of the core eukaryotic gene set. We conclude that the P. ramorum lineages are diverging via a rapidly evolving non-core genome and that the invasive asexual lineages are not clonal, but display genotypic diversity caused by MR.IMPORTANCE Alien species are often successful invaders in new environments, despite the introduction of a few isolates with a reduced genetic pool. This is called the genetic paradox of invasion. We found two mechanisms by which the invasive forest pathogen causing sudden oak and sudden larch death can evolve. Extensive mitotic recombination producing runs of homozygosity generates genotypic diversity even in the absence of sexual reproduction, and rapid turnover of genes in the non-core, or nonessential portion of genome not shared by all isolates, allows pathogenicity genes to evolve rapidly or be eliminated while retaining essential genes. Mitotic recombination events occur in genomic hot spots, resulting in similar ROH patterns in different isolates or groups; one ROH, independently generated in two different groups, was enriched in pathogenicity genes and may be a target for selection. This provides important insights into the evolution of invasive alien pathogens and their potential for adaptation and future persistence.

Project description:Recently introduced, exotic plant pathogens may exhibit low genetic diversity and be limited to clonal reproduction. However, rapidly mutating molecular markers such as microsatellites can reveal genetic variation within these populations and be used to model putative migration patterns. Phytophthora ramorum is the exotic pathogen, discovered in the late 1990s, that is responsible for sudden oak death in California forests and ramorum blight of common ornamentals. The nursery trade has moved this pathogen from source populations on the West Coast to locations across the United States, thus risking introduction to other native forests. We examined the genetic diversity of P. ramorum in United States nurseries by microsatellite genotyping 279 isolates collected from 19 states between 2004 and 2007. Of the three known P. ramorum clonal lineages, the most common and genetically diverse lineage in the sample was NA1. Two eastward migration pathways were revealed in the clustering of NA1 isolates into two groups, one containing isolates from Connecticut, Oregon, and Washington and the other isolates from California and the remaining states. This finding is consistent with trace forward analyses conducted by the US Department of Agriculture's Animal and Plant Health Inspection Service. At the same time, genetic diversities in several states equaled those observed in California, Oregon, and Washington and two-thirds of multilocus genotypes exhibited limited geographic distributions, indicating that mutation was common during or subsequent to migration. Together, these data suggest that migration, rapid mutation, and genetic drift all play a role in structuring the genetic diversity of P. ramorum in US nurseries. This work demonstrates that fast-evolving genetic markers can be used to examine the evolutionary processes acting on recently introduced pathogens and to infer their putative migration patterns, thus showing promise for the application of forensics to plant pathogens.

Dataset Information

Asexual Evolution and Forest Conditions Drive Genetic Parallelism in Phytophthora ramorum.

Publications

Asexual Evolution and Forest Conditions Drive Genetic Parallelism in <i>Phytophthora ramorum</i>.

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