title: Host-induced aneuploidy and phenotypic diversification in the Sudden Oak Death pathogen Phytophthora ramorum.
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.
authors.affiliation: Crops Pathology and Genetics Research Unit, USDA Agricultural Research Service, Davis, California, 95616, USA.
authors.forename: Takao
authors.initials: T
authors.lastname: Kasuga
authors.affiliation: Crops Pathology and Genetics Research Unit, USDA Agricultural Research Service, Davis, California, 95616, USA.
authors.forename: Mai
authors.initials: M
authors.lastname: Bui
authors.affiliation: Phytosphere Research, Vacaville, California, 95687, USA.
authors.forename: Elizabeth
authors.initials: E
authors.lastname: Bernhardt
authors.affiliation: Phytosphere Research, Vacaville, California, 95687, USA.
authors.forename: Tedmund
authors.initials: T
authors.lastname: Swiecki
authors.affiliation: Department of Plant Pathology, University of California, Davis, California, 95616, USA.
authors.forename: Kamyar
authors.initials: K
authors.lastname: Aram
authors.affiliation: Department of Plant Pathology, University of Florida, IFAS, Indian River Research and Education Center, Fort Pierce, Florida, 34945, USA.
authors.forename: Liliana M
authors.initials: LM
authors.lastname: Cano
authors.affiliation: Forest Research, Farnham, Surrey, GU10 4LH, UK.
authors.forename: Joan
authors.initials: J
authors.lastname: Webber
authors.affiliation: Forest Research, Farnham, Surrey, GU10 4LH, UK.
authors.forename: Clive
authors.initials: C
authors.lastname: Brasier
authors.affiliation: Horticultural Crops Research Laboratory, USDA Agricultural Research Service, Corvallis, Oregon, 97330, USA.
authors.forename: Caroline
authors.initials: C
authors.lastname: Press
authors.affiliation: Horticultural Crops Research Laboratory, USDA Agricultural Research Service, Corvallis, Oregon, 97330, USA.
authors.forename: Niklaus J
authors.initials: NJ
authors.lastname: Grünwald
authors.affiliation: Department of Plant Pathology, University of California, Davis, California, 95616, USA.
authors.forename: David M
authors.initials: DM
authors.lastname: Rizzo
authors.affiliation: Department of Environmental Science, Policy, and Management, University of California, Berkeley, California, 947020, USA. matteog@berkeley.edu.
authors.forename: Matteo
authors.initials: M
authors.lastname: Garbelotto
mesh_terms: D000782:Aneuploidy; D002140:California; D056915:DNA Copy Number Variations; D004251:DNA Transposable Elements; D020440:Gene Duplication; D020869:Gene Expression Profiling; D008040:Genetic Linkage; D005838:Genotype; D019656:Loss of Heterozygosity; D010641:Phenotype; D010838:Phytophthora / Q000235:genetics*; D010935:Plant Diseases / Q000382:microbiology; D020641:Polymorphism, Single Nucleotide; D029963:Quercus / Q000382:microbiology; D059467:Transcriptome
chemical_list: D004251:DNA Transposable Elements
keywords: Aneuploidy; Invasive pathogens; Loss of heterozygosity; Transposable elements