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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

Phylogenetic Analyses(A) Neighbor-joining tree of YopJ family of T3SEs proteins. Bootstrap support is indicated above each node, with only values >60% being shown. T3SEs from P. syringae are highlighted. Accession numbers for each protein are presented in parentheses following the protein name and species.(B) Neighbor-joining gene genealogy of the hopZ1 T3SEs alleles with bootstrap analysis as above and hopZ2Ppi895A used as an out-group. The genetic organization of the three functional allele classes (hopZ1a, hopZ1b, and hopZ1c) and two degenerate hopZ1 alleles (ψhopZ1a and ψhopZ1b) are presented to the right of the gene genealogy. The large gray rectangle represents the region of shared similarity among the alleles, and corresponds to the coding sequence of hopZ1a. The dark vertical rectangle to the left of each gene represents the T3SS promoter element known as the hrp box. The solid black vertical line represents the stop codon for each allele. Arrows at the 5′ end of the coding sequences indicate which alleles are functional. Triangles above each coding sequence indicate insertions, with the insertion size indicated within. The ψhopZ1a allele has a nonsense mutation at nucleotide 171, and a degenerate hrp box in which the conserved GGAACC sequence has mutated to CCAACC. It is not transcribed under T3SS induction conditions. The ψhopZ1b allele is disrupted by an insertion sequence.
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pgen-0020209-g001: Phylogenetic Analyses(A) Neighbor-joining tree of YopJ family of T3SEs proteins. Bootstrap support is indicated above each node, with only values >60% being shown. T3SEs from P. syringae are highlighted. Accession numbers for each protein are presented in parentheses following the protein name and species.(B) Neighbor-joining gene genealogy of the hopZ1 T3SEs alleles with bootstrap analysis as above and hopZ2Ppi895A used as an out-group. The genetic organization of the three functional allele classes (hopZ1a, hopZ1b, and hopZ1c) and two degenerate hopZ1 alleles (ψhopZ1a and ψhopZ1b) are presented to the right of the gene genealogy. The large gray rectangle represents the region of shared similarity among the alleles, and corresponds to the coding sequence of hopZ1a. The dark vertical rectangle to the left of each gene represents the T3SS promoter element known as the hrp box. The solid black vertical line represents the stop codon for each allele. Arrows at the 5′ end of the coding sequences indicate which alleles are functional. Triangles above each coding sequence indicate insertions, with the insertion size indicated within. The ψhopZ1a allele has a nonsense mutation at nucleotide 171, and a degenerate hrp box in which the conserved GGAACC sequence has mutated to CCAACC. It is not transcribed under T3SS induction conditions. The ψhopZ1b allele is disrupted by an insertion sequence.

Mentions: A phylogenetic analysis of the complete YopJ family places the P. syringae effectors in three distinct clades (Figure 1A). The HopZ1 alleles form a distinct clade restricted to P. syringae. HopZ2 clusters with T3SEs from the tomato and pepper pathogen, Xanthomonas campestris (AvrBsT, AvrRxv, and AvrXv4). HopZ3 is in a distinct clade with the virulence-associated ORFB locus from the Asian pear pathogen, Erwinia pyrifoliae, and the fire blight pathogen, Erwinia amylovora. These phylogenetic relationships suggest that hopZ1 is native to P. syringae, while the clustering of hopZ2 and hopZ3 within clades dominated by Xanthomonas and Erwinia T3SEs, respectively, supports the argument that these T3SEs may be functionally related homologs that were horizontally acquired from ecologically related plant pathogens.


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)

Phylogenetic Analyses(A) Neighbor-joining tree of YopJ family of T3SEs proteins. Bootstrap support is indicated above each node, with only values >60% being shown. T3SEs from P. syringae are highlighted. Accession numbers for each protein are presented in parentheses following the protein name and species.(B) Neighbor-joining gene genealogy of the hopZ1 T3SEs alleles with bootstrap analysis as above and hopZ2Ppi895A used as an out-group. The genetic organization of the three functional allele classes (hopZ1a, hopZ1b, and hopZ1c) and two degenerate hopZ1 alleles (ψhopZ1a and ψhopZ1b) are presented to the right of the gene genealogy. The large gray rectangle represents the region of shared similarity among the alleles, and corresponds to the coding sequence of hopZ1a. The dark vertical rectangle to the left of each gene represents the T3SS promoter element known as the hrp box. The solid black vertical line represents the stop codon for each allele. Arrows at the 5′ end of the coding sequences indicate which alleles are functional. Triangles above each coding sequence indicate insertions, with the insertion size indicated within. The ψhopZ1a allele has a nonsense mutation at nucleotide 171, and a degenerate hrp box in which the conserved GGAACC sequence has mutated to CCAACC. It is not transcribed under T3SS induction conditions. The ψhopZ1b allele is disrupted by an insertion sequence.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC1713259&req=5

pgen-0020209-g001: Phylogenetic Analyses(A) Neighbor-joining tree of YopJ family of T3SEs proteins. Bootstrap support is indicated above each node, with only values >60% being shown. T3SEs from P. syringae are highlighted. Accession numbers for each protein are presented in parentheses following the protein name and species.(B) Neighbor-joining gene genealogy of the hopZ1 T3SEs alleles with bootstrap analysis as above and hopZ2Ppi895A used as an out-group. The genetic organization of the three functional allele classes (hopZ1a, hopZ1b, and hopZ1c) and two degenerate hopZ1 alleles (ψhopZ1a and ψhopZ1b) are presented to the right of the gene genealogy. The large gray rectangle represents the region of shared similarity among the alleles, and corresponds to the coding sequence of hopZ1a. The dark vertical rectangle to the left of each gene represents the T3SS promoter element known as the hrp box. The solid black vertical line represents the stop codon for each allele. Arrows at the 5′ end of the coding sequences indicate which alleles are functional. Triangles above each coding sequence indicate insertions, with the insertion size indicated within. The ψhopZ1a allele has a nonsense mutation at nucleotide 171, and a degenerate hrp box in which the conserved GGAACC sequence has mutated to CCAACC. It is not transcribed under T3SS induction conditions. The ψhopZ1b allele is disrupted by an insertion sequence.
Mentions: A phylogenetic analysis of the complete YopJ family places the P. syringae effectors in three distinct clades (Figure 1A). The HopZ1 alleles form a distinct clade restricted to P. syringae. HopZ2 clusters with T3SEs from the tomato and pepper pathogen, Xanthomonas campestris (AvrBsT, AvrRxv, and AvrXv4). HopZ3 is in a distinct clade with the virulence-associated ORFB locus from the Asian pear pathogen, Erwinia pyrifoliae, and the fire blight pathogen, Erwinia amylovora. These phylogenetic relationships suggest that hopZ1 is native to P. syringae, while the clustering of hopZ2 and hopZ3 within clades dominated by Xanthomonas and Erwinia T3SEs, respectively, supports the argument that these T3SEs may be functionally related homologs that were horizontally acquired from ecologically related plant pathogens.

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