Comparative Genomics of Host-Specific Virulence in Pseudomonas syringae

Abstract

While much study has gone into characterizing virulence factors that play a general role in disease, less work has been directed at identifying pathogen factors that act in a host-specific manner. Understanding these factors will help reveal the variety of mechanisms used by pathogens to suppress or avoid host defenses. We identified candidate Pseudomonas syringae host-specific virulence genes by searching for genes whose distribution among natural P. syringae isolates was statistically associated with hosts of isolation. We analyzed 91 strains isolated from 39 plant hosts by DNA microarray-based comparative genomic hybridization against an array containing 353 virulence-associated (VA) genes, including 53 type III secretion system effectors (T3SEs). We identified individual genes and gene profiles that were significantly associated with strains isolated from cauliflower, Chinese cabbage, soybean, rice, and tomato. We also identified specific horizontal gene acquisition events associated with host shifts by mapping the array data onto the core genome phylogeny of the species. This study provides the largest suite of candidate hostspecificity factors from any pathogen, suggests that there are multiple ways in which P. syringae isolates can adapt to the same host, and provides insight into the evolutionary mechanisms underlying host adaptation. P ATHOGENS cannot cause disease indiscriminately, but are generally capable of avoiding or suppressing defenses in only a relatively small set of hosts. Both pathogen factors and host factors govern these interactions, and which of these two is dominant likely depends on the specific interaction. Nevertheless, there is a growing body of data that clearly demonstrates that pathogens have evolved compatibility factors that facilitate the disease process in a host-specific manner. (Cornelis 2002;Abramovitch and Martin 2004;Alfano and Collmer 2004;Espinosa and Alfano 2004;Nomura et al. 2005). However, there are several key issues about pathogen host-specificity factors that are still unknown. For example, the general relationship between virulence factors and host-specificity factors is unclear, although it is likely that the latter are a subset of the former required only on select hosts. It is also not known if the factors that are responsible for pathogen compatibility on different host species are fundamentally different from the factors that determine compatibility among different cultivars of the same host species. We do not even know at what level host specificity acts most strongly. For example, hostspecificity factors may play important roles during initial colonization, during pathogen migration to the appropriate tissue or cell type, during the initiation of cellular interactions, during the maintenance of these interactions, or even at the point where the pathogen disperses to a new host (Levin 1996).To address these questions, we first must have a way of identifying host-specific virulence factors. A reasonable hypothesis is that strains that are able to in...

Comparative Large-Scale Analysis of Interactions between Several Crop Species and the Effector Repertoires from Multiple Pathovars of Pseudomonas and Ralstonia

“…This could be due to either host-specific virulence activities or the detection of effectors by the plant and elicitation of the resistance response. A previous study failed to identify host-specific virulence determinants (Sarkar et al, 2006). In our study, nonhosts responded to more effectors than hosts.…”

“…Because of the selective advantage conferred by such genes, there has been extensive horizontal transfer among microbial pathogens of genes that encode effectors (Lindgren et al, 1988;Hueck, 1998;Deng et al, 2003;Rohmer et al, 2004;Ma et al, 2006;Lindeberg et al, 2008). As a result, diverse pathogens express overlapping sets of effectors (Lindeberg et al, 2006;Sarkar et al, 2006;Stavrinides et al, 2006). On the plant side, R genes, particularly those encoding NBS-LRR proteins and receptor-like kinases, are among the largest and most diverse classes of plant proteins (Clark et al, 2007).…”

Natural Variation in the Pto Disease Resistance Gene Within Species of Wild Tomato (Lycopersicon). II. Population Genetics of Pto

“…In cultivated tomatoes, infestation by this pathogen can lead to yield losses, as both fruit and leaves are attacked. Different races of this pathovar are found worldwide and these races differ in the expression of well-characterized avirulence factors (Sakar et al 2006). For example, two avirulence factors found in race 0, but not in race 1, are AvrPto and AvrPtoB.…”

Diversification of a Type III Effector Family via both Pathoadaptation and Horizontal Transfer in Response to a Coevolutionary Arms Race

“…It is particularly noteworthy that these alternative allelic forms have evolved both through pathoadaptive change via the mutational process, as well as through horizontal transfer. Horizontal gene transfer and gene loss are well-known and accepted mechanisms for modifying T3SE-mediated hostspecific interactions [11,27,28,33,46], yet pathoadaptation in this context is less well-understood. While pathoadaptation is well-established in other virulence-associated systems such as the Escherichia coli fimH loci [29,30], it has not yet been shown to influence T3SE-host interactions.…”

“…Most of this work has implicated horizontal gene transfer and the resulting acquisition and loss of T3SE as an important arms race strategy [27,28]. The alternative to modulating virulence via horizontal gene transfer is pathoadaptation, in which increased virulence is achieved through relatively minor mutations (e.g., point mutations) in preexisting genes [29][30][31][32].…”