Abstract
BackgroundAneuploidy 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.ResultsWe 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.ConclusionThis 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2717-z) contains supplementary material, which is available to authorized users.
Highlights
Aneuploidy can result in significant phenotypic changes, which can sometimes be selectively advantageous
We have previously reported that wt and nwt isolates show distinct global mRNA patterns [21], indicating physiological differences associated with the colony types
The Sudden Oak Death pathogen Phytophthora ramorum is exclusively clonal, yet exhibits extensive phenotypic differences when obtained from oak
Summary
Aneuploidy can result in significant phenotypic changes, which can sometimes be selectively advantageous. 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. 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. Aneuploidy is a potentially effective and widespread mechanism for developing novel phenotypic variation in a clonal population [6,7,8]. We employed high throughput sequencing to characterize genomic diversity underlying rapid phenotypic diversification in the clonal organism Phytophthora ramorum. The lineages are believed to have originated from distinct genetically isolated populations in their (presently unknown) region of origin [14]. Disease is caused by lethal trunk cankers, which do not extend below ground [10]
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