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Title: Phenotypic diversification is associated with host-induced transposon derepression in the Sudden Oak Death pathogen Phytophthora ramorum

Author
item Kasuga, Takao
item KOZANITAS, MELINA - University Of California
item Bui, Mai
item HUBERLI, DANIEL - Department Of Food And Agriculture Western Australia
item RIZZO, DAVID - University Of California
item GARBELOTTO, MATTEO - University Of California

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/26/2012
Publication Date: 4/18/2012
Citation: Kasuga, T., Kozanitas, M., Bui, M.Q., Huberli, D., Rizzo, D., Garbelotto, M. 2012. Phenotypic diversification is associated with host-induced transposon derepression in the Sudden Oak Death pathogen Phytophthora ramorum. PLoS One. 7:e34728.

Interpretive Summary: Forestry, agriculture and native ecosystems face ever-increasing threats to invasive pathogens. Due to severe population bottlenecks, invasive microbes typically have a limited genetic variation and often propagate clonally, yet they can display diverse phenotypic variation. This attribute may be responsible for the tenacity and adaptability of the pathogens in non-native environments. The invasive oomycete pathogen, Phytophthora ramorum is a causal agent of sudden oak death in North America and sudden larch death in plantation forests in Europe. A clonal lineage of P. ramorum in California is known to display wide range of virulence and colony morphology. We found variation in gene expression as well as aforementioned phenotypes, associated with originating host species; isolates obtained from coast live oak and those from California Bay laurel displayed distinctive phenotypic differences despite a lack of detectable genetic variation between the two groups.

Technical Abstract: The oomycete pathogen Phytophthora ramorum is responsible for sudden oak death (SOD) in California coastal forests. P. ramorum is a generalist pathogen with over 100 known host species. Three or four closely related genotypes of P. ramorum (from a single lineage) were originally introduced in California forests and the pathogen reproduces clonally. Because of this the genetic diversity of P. ramorum is extremely low in Californian forests. However, P. ramorum shows diverse phenotypic variation in colony morphology, colony senescence, and virulence. In this study, we show that phenotypic variation among isolates is associated with the host species from which the microbe was originally cultured. Microarray global mRNA profiling detected derepression of transposable elements (TEs) and down-regulation of crinkler effector homologs (CRNs) in the majority of isolates originating from coast live oak (Quercus agrifolia), but this expression pattern was not observed in isolates from California bay laurel (Umbellularia californica). In some instances, oak and bay laurel isolates originating from the same geographic location had identical genotypes based on multilocus simples sequence repeat (SSR) marker analysis but had different phenotypes. Expression levels of the two marker genes analyzed by quantitative reverse transcription PCR were correlated with originating host species, but not with multilocus genotypes. Because oak is a non-transmissive dead-end host for P. ramorum, our observations are congruent with an epi-transposon hypothesis; i.e., physiological stress is triggered on P. ramorum while colonizing oak stems and disrupts epigenetic silencing of TEs. This then results in TE reactivation and possibly genome diversification without significant epidemiological consequences. We propose the P. ramorum-oak host system in California forests as an ad hoc model for epi-transposon mediated diversification.