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Title: Host-induced aneuploidy and phenotypic diversification in the Sudden Oak Death pathogen Phytophthora ramorum

item Kasuga, Takao
item Bui, Mai
item BERHARDT, ELIZABETH - Phytosphere Research
item SWIECKI, TEDMUND - Phytosphere Research
item ARAM, KAMYAR - University Of California
item CANO, LILIANA - University Of Florida
item WEBBER, JOAN - Forestry Commission
item BRASIER, CLIVE - Forestry Commission
item Press, Caroline
item Grunwald, Niklaus - Nik
item RIZZO, DAVID - University Of California
item GARBELOTTO, MATTEO - University Of California

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/28/2016
Publication Date: 5/20/2016
Citation: Kasuga, T., Bui, M.Q., Berhardt, E., Swiecki, T., Aram, K., Cano, L.M., Webber, J., Brasier, C., Press, C.M., Grunwald, N.J., Rizzo, D.M., Garbelotto, M. 2016. Host-induced aneuploidy and phenotypic diversification in the Sudden Oak Death pathogen Phytophthora ramorum. BMC Genomics. 17:385. doi: 10.1186/s12864-016-2717-z.

Interpretive Summary: The Sudden Oak Death pathogen Phytophthora ramorum is exclusively clonal, yet exhibits extensive phenotypic differences when obtained from oak. When P. ramorum isolates from the foliar host California bay were inoculated and re-isolated from canyon live oak, a large number of re-isolates displayed morphological phenotypes and mRNA expression profiles only seen in cultures from naturally infected oak. Major genomic alterations in oak isolates including partial aneuploidy and copy-neutral loss of heterozygosity were found to be associated with the observed phenotypic diversification. Comparable phenotypic changes and associated genome alterations were also found in isolates from Lawson cypress in the UK. Chromosomal breakpoints were found to be located at or near transposons, linking transposon de-repression caused by the chemical environment of oak to structural genomic changes.

Technical Abstract: 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.