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Type III effector diversification via both pathoadaptation and horizontal transfer in response to a coevolutionary arms race.

Ma W, Dong FF, Stavrinides J, Guttman DS - PLoS Genet. (2006)

Bottom Line: We show how the evolution and function of the HopZ family of type III secreted effector proteins carried by the plant pathogen Pseudomonas syringae are influenced by a coevolutionary arms race between pathogen and host.The introduction of the ancestral hopZ1 allele into strains harboring alternate alleles results in a resistance protein-mediated defense response in their respective hosts, which is not observed with the endogenous allele.This genetic diversity permits the pathogen to avoid host defenses while still maintaining a virulence-associated protease, thereby allowing it to thrive on its current host, while simultaneously impacting its host range.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell and Systems Biology, University of Toronto, Toronto, Ontario, Canada.

ABSTRACT
The concept of the coevolutionary arms race holds a central position in our understanding of pathogen-host interactions. Here we identify the molecular mechanisms and follow the stepwise progression of an arms race in a natural system. We show how the evolution and function of the HopZ family of type III secreted effector proteins carried by the plant pathogen Pseudomonas syringae are influenced by a coevolutionary arms race between pathogen and host. We surveyed 96 isolates of P. syringae and identified three homologs (HopZ1, HopZ2, and HopZ3) distributed among approximately 45% of the strains. All alleles were sequenced and their expression was confirmed. Evolutionary analyses determined that the diverse HopZ1 homologs are ancestral to P. syringae, and have diverged via pathoadaptive mutational changes into three functional and two degenerate forms, while HopZ2 and HopZ3 have been brought into P. syringae via horizontal transfer from other ecologically similar bacteria. A PAML selection analysis revealed that the C terminus of HopZ1 is under strong positive selection. Despite the extensive genetic variation observed in this family, all three homologs have cysteine-protease activity, although their substrate specificity may vary. The introduction of the ancestral hopZ1 allele into strains harboring alternate alleles results in a resistance protein-mediated defense response in their respective hosts, which is not observed with the endogenous allele. These data indicate that the P. syringae HopZ family has undergone allelic diversification via both pathoadaptive mutational changes and horizontal transfer in response to selection imposed by the host defense system. This genetic diversity permits the pathogen to avoid host defenses while still maintaining a virulence-associated protease, thereby allowing it to thrive on its current host, while simultaneously impacting its host range.

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Related in: MedlinePlus

Congruence between the HopZ1 Gene Genealogy and the MLST Core Genome Phylogeny of P. syringaeSee Figures 2 and S1 for details on the phylogenetic methods used. Gray areas labeled g2–g5 in the center of the figure indicate the major phylogroups as determined by MLST. Bootstrap support values (>60%) are indicated above nodes.
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pgen-0020209-g003: Congruence between the HopZ1 Gene Genealogy and the MLST Core Genome Phylogeny of P. syringaeSee Figures 2 and S1 for details on the phylogenetic methods used. Gray areas labeled g2–g5 in the center of the figure indicate the major phylogroups as determined by MLST. Bootstrap support values (>60%) are indicated above nodes.

Mentions: The clustering of alleles in the hopZ1 gene genealogy is consistent with the major clades (phylogroups) seen in the P. syringae MLST core-genome tree (Figure 3). The single large-scale incongruence between the hopZ1 gene tree and the core genome phylogeny is the tight clustering between the hopZ1b alleles from phylogroup 3 strains and the hopZ1c alleles from phylogroup 5 strains. Specifically, it appears as if hopZ1 alleles from phylogroup 5 strains transferred into strains of phylogroup 3. An identical incongruity between the phylogroup 3 and 5 strains was observed for one of the major operons that encodes the T3SS apparatus [42]. These results support a horizontal gene exchange event between phylogroups 3 and 5 that mobilized at least part of the genes encoding the T3SS and some of its effectors. There are also some minor points of incongruence within the major clades of the hopZ1 gene genealogy with respect to the MLST core-genome tree, but none of these are strongly supported by bootstrap analysis in both trees. An SH phylogenetic congruence test [43] for the phylogroup 2, 4, and 5 strains (phylogroup 3 strains were omitted in this analysis for the reason discussed above) also finds that the MLST data is congruent with the HopZ1 tree (unpublished data).


Type III effector diversification via both pathoadaptation and horizontal transfer in response to a coevolutionary arms race.

Ma W, Dong FF, Stavrinides J, Guttman DS - PLoS Genet. (2006)

Congruence between the HopZ1 Gene Genealogy and the MLST Core Genome Phylogeny of P. syringaeSee Figures 2 and S1 for details on the phylogenetic methods used. Gray areas labeled g2–g5 in the center of the figure indicate the major phylogroups as determined by MLST. Bootstrap support values (>60%) are indicated above nodes.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC1713259&req=5

pgen-0020209-g003: Congruence between the HopZ1 Gene Genealogy and the MLST Core Genome Phylogeny of P. syringaeSee Figures 2 and S1 for details on the phylogenetic methods used. Gray areas labeled g2–g5 in the center of the figure indicate the major phylogroups as determined by MLST. Bootstrap support values (>60%) are indicated above nodes.
Mentions: The clustering of alleles in the hopZ1 gene genealogy is consistent with the major clades (phylogroups) seen in the P. syringae MLST core-genome tree (Figure 3). The single large-scale incongruence between the hopZ1 gene tree and the core genome phylogeny is the tight clustering between the hopZ1b alleles from phylogroup 3 strains and the hopZ1c alleles from phylogroup 5 strains. Specifically, it appears as if hopZ1 alleles from phylogroup 5 strains transferred into strains of phylogroup 3. An identical incongruity between the phylogroup 3 and 5 strains was observed for one of the major operons that encodes the T3SS apparatus [42]. These results support a horizontal gene exchange event between phylogroups 3 and 5 that mobilized at least part of the genes encoding the T3SS and some of its effectors. There are also some minor points of incongruence within the major clades of the hopZ1 gene genealogy with respect to the MLST core-genome tree, but none of these are strongly supported by bootstrap analysis in both trees. An SH phylogenetic congruence test [43] for the phylogroup 2, 4, and 5 strains (phylogroup 3 strains were omitted in this analysis for the reason discussed above) also finds that the MLST data is congruent with the HopZ1 tree (unpublished data).

Bottom Line: We show how the evolution and function of the HopZ family of type III secreted effector proteins carried by the plant pathogen Pseudomonas syringae are influenced by a coevolutionary arms race between pathogen and host.The introduction of the ancestral hopZ1 allele into strains harboring alternate alleles results in a resistance protein-mediated defense response in their respective hosts, which is not observed with the endogenous allele.This genetic diversity permits the pathogen to avoid host defenses while still maintaining a virulence-associated protease, thereby allowing it to thrive on its current host, while simultaneously impacting its host range.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell and Systems Biology, University of Toronto, Toronto, Ontario, Canada.

ABSTRACT
The concept of the coevolutionary arms race holds a central position in our understanding of pathogen-host interactions. Here we identify the molecular mechanisms and follow the stepwise progression of an arms race in a natural system. We show how the evolution and function of the HopZ family of type III secreted effector proteins carried by the plant pathogen Pseudomonas syringae are influenced by a coevolutionary arms race between pathogen and host. We surveyed 96 isolates of P. syringae and identified three homologs (HopZ1, HopZ2, and HopZ3) distributed among approximately 45% of the strains. All alleles were sequenced and their expression was confirmed. Evolutionary analyses determined that the diverse HopZ1 homologs are ancestral to P. syringae, and have diverged via pathoadaptive mutational changes into three functional and two degenerate forms, while HopZ2 and HopZ3 have been brought into P. syringae via horizontal transfer from other ecologically similar bacteria. A PAML selection analysis revealed that the C terminus of HopZ1 is under strong positive selection. Despite the extensive genetic variation observed in this family, all three homologs have cysteine-protease activity, although their substrate specificity may vary. The introduction of the ancestral hopZ1 allele into strains harboring alternate alleles results in a resistance protein-mediated defense response in their respective hosts, which is not observed with the endogenous allele. These data indicate that the P. syringae HopZ family has undergone allelic diversification via both pathoadaptive mutational changes and horizontal transfer in response to selection imposed by the host defense system. This genetic diversity permits the pathogen to avoid host defenses while still maintaining a virulence-associated protease, thereby allowing it to thrive on its current host, while simultaneously impacting its host range.

Show MeSH
Related in: MedlinePlus