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 nontransmissive dead-end host for P. ramorum, our observations are congruent with an epi-transposon hypothesis; that is, 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.
Highlights
The growing number of sequenced genomes reveals that a large fraction of plant pathogenic fungal genomes are composed of transposable elements (TEs) [1,2,3,4]
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)
As described by Brasier and coworkers [33], Californian NA1 isolates of P. ramorum show a large variation in growth rate and colony morphology (Fig. S1) including a majority of ‘wild type’ isolates and a minority of ‘non-wild type’ isolates characterized by irregular growth patterns
Summary
The growing number of sequenced genomes reveals that a large fraction of plant pathogenic fungal (including oomycetes) genomes are composed of transposable elements (TEs) [1,2,3,4]. TEs are often not distributed evenly along chromosomes, but rather form clusters with fast evolving genes that are likely involved in host-pathogen interactions. [1,2], and effector genes in Phytophthora infestans [3,4] In these examples, TEs are postulated to be involved in host-specialization and speciation of pathogens. The expansion of TEs and genome size detected in B. graminis is thought to coincide with evolution to obligate biotrophy. In both examples, TEs are associated with the emergence of evolutionarily novel lineages characterized either by a host switch or by a change in trophic behavior
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