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Combining field epidemiological information and genetic data to comprehensively reconstruct the invasion history and the microevolution of the sudden oak death agent Phytophthora ramorum (Stramenopila: Oomycetes) in California.

ABSTRACT: Understanding the migration patterns of invasive organisms is of paramount importance to predict and prevent their further spread. Previous attempts at reconstructing the entire history of the sudden oak death (SOD) epidemic in California were limited by: (1) incomplete sampling; (2) the inability to include infestations caused by a single genotype of the pathogen; (3) collapsing of non-spatially contiguous yet genetically similar samples into large meta-samples that confounded the coalescent analyses. Here, we employ an intensive sampling coverage of 832 isolates of Phytopthora ramorum (the causative agent of SOD) from 60 California forests, genotyped at nine microsatellite loci, to reconstruct its invasion. By using age of infestation as a constraint on coalescent analyses, by dividing genetically indistinguishable meta-populations into highly-resolved sets of spatially contiguous populations, and by using Bruvo genetic distances for most analyses, we reconstruct the entire history of the epidemic and convincingly show infected nursery plants are the original source for the entire California epidemic. Results indicate that multiple human-mediated introductions occurred in most counties and that further disease sources were represented by large wild infestations. The study also identifies minor introductions, some of them relatively recent, linked to infected ornamental plants. Finally, using archival isolates collected soon after the discovery of the pathogen in California, we corroborate that the epidemic is likely to have resulted form 3 to 4 core founder individuals evolved from a single genotype. This is probably the most complete reconstruction ever completed for an invasion by an exotic forest pathogen, and the approach here described may be useful for the reconstruction of invasions by any clonally reproducing organism with a relatively limited natural dispersal range.

SUBMITTER: Croucher PJ

PROVIDER: S-EPMC3782357 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Aneuploidy can result in significant phenotypic changes, which can sometimes be selectively advantageous. For example, aneuploidy confers resistance to antifungal drugs in human pathogenic fungi. Aneuploidy has also been observed in invasive fungal and oomycete plant pathogens in the field. Environments conducive to the generation of aneuploids, the underlying genetic mechanisms, and the contribution of aneuploidy to invasiveness are underexplored. We studied phenotypic diversification and associated genome changes in Phytophthora ramorum, a highly destructive oomycete pathogen with a wide host-range that causes Sudden Oak Death in western North America and Sudden Larch Death in the UK. Introduced populations of the pathogen are exclusively clonal. In California, oak (Quercus spp.) isolates obtained from trunk cankers frequently exhibit host-dependent, atypical phenotypes called non-wild type (nwt), apparently without any host-associated population differentiation. Based on a large survey of genotypes from different hosts, we previously hypothesized that the environment in oak cankers may be responsible for the observed phenotypic diversification in P. ramorum.We show that both normal wild type (wt) and nwt phenotypes were obtained when wt P. ramorum isolates from the foliar host California bay (Umbellularia californica) were re-isolated from cankers of artificially-inoculated canyon live oak (Q. chrysolepis). We also found comparable nwt phenotypes in P. ramorum isolates from a bark canker of Lawson cypress (Chamaecyparis lawsoniana) in the UK; previously nwt was not known to occur in this pathogen population. High-throughput sequencing-based analyses identified major genomic alterations including partial aneuploidy and copy-neutral loss of heterozygosity predominantly in nwt isolates. Chromosomal breakpoints were located at or near transposons.This work demonstrates that major genome alterations of a pathogen can be induced by its host species. This is an undocumented type of plant-microbe interaction, and its contribution to pathogen evolution is yet to be investigated, but one of the potential collateral effects of nwt phenotypes may be host survival.

Dataset Information

Combining field epidemiological information and genetic data to comprehensively reconstruct the invasion history and the microevolution of the sudden oak death agent Phytophthora ramorum (Stramenopila: Oomycetes) in California.

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