Phenotypic Diversification is Associated with Host-Induced Transposon Derepression in the Sudden Oak Death Pathogen Phytophthora ramorum.

Author , , , , ,
Date 2012.
Publication PLoS ONE 7(4): e34728.
Key Words
AbstractThe 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 deadend 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. Significance: This study found that the virulence of plant-borne diseases depends not only on the particular strain of a pathogen, but on where the pathogen has been before landing on its host. It demonstrated that the pattern of gene regulation—how a cell determines which genes it will express and how it will express them—rather than gene make-up alone affects how aggressively a microbe will behave in a plant host. The pattern of gene regulation is formed by past environments or by an original host plant from which the pathogen is transmitted. In the study, researchers showed that genetically identical strains of P. ramorum isolated from different plant hosts were strikingly different in their virulence and their ability to proliferate, and showed that these traits were maintained long after they had been isolated from their hosts. The implications for disease control are significant, as researchers say that it may not be enough to know what strain of pathogens they are dealing with in order to make treatment decisions, it also may be necessary to know how the pathogen’s genes are being regulated. Also identified were two groups of genes that are capable of affecting virulence and whose expression patterns are indicative of the previous host species they inhabited. Over-expression of transposons—mobile genetic elements—combined with under-expression of crinkler genes—genes involved in host-pathogen interactions—is consistently associated with lowered fitness of the pathogen. Understanding the regulation of these genes may provide scientists with some future approaches to control the disease, such as manipulating the gene expression to artificially reduce the aggressiveness of plant pathogens.
Full Citation Kasuga, T.; Kozanitas, M.; Bui, M.; Hüberli, D.; Rizzo, D.M.; and Garbelotto, M. 2012. Phenotypic Diversification is Associated with Host-Induced Transposon Derepression in the Sudden Oak Death Pathogen Phytophthora ramorum. PLoS ONE 7(4): e34728. DOI: 10.1371/journal.pone.0034728.