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ABSTRACT: RPM1-interacting protein 4 (RIN4), a negative regulator of the basal defense response in plants, is targeted by multiple bacterial virulence effectors. We show that RIN4 degradation is induced by the effector AvrPto from Pseudomonas syringae and that this degradation in Solanaceous plants is dependent on the resistance protein, Pto, a protein kinase, and Prf, a nucleotide binding site-leucine-rich repeat protein. Our data demonstrate overlap between two of the best-characterized pathways for recognition of pathogen virulence effectors in plants. RIN4 interacts with multiple plant signaling components and bacterial effectors in yeast and in planta. AvrPto induces an endogenous proteolytic activity in both tomato (Solanum lycopersicum) and Nicotiana benthamiana that degrades RIN4 and requires the consensus site cleaved by the protease effector AvrRpt2. The interaction between AvrPto and Pto, but not the kinase activity of Pto, is required for proteolysis of RIN4. Analysis of many of the effectors comprising the secretome of P. syringae pv tomato DC3000 led to the identification of two additional sequence-unrelated effectors that can also induce degradation of RIN4. Therefore, multiple bacterial effectors besides AvrRpt2 elicit proteolysis of RIN4 in planta.
The Plant Cell 09/2009; 21(8):2458-72. · 8.99 Impact Factor
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Tadeusz Wroblewski, Katherine S Caldwell,
Urszula Piskurewicz,
Keri A Cavanaugh,
Huaqin Xu,
Alexander Kozik,
Oswaldo Ochoa,
Leah K McHale,
Kirsten Lahre,
Joanna Jelenska,
Jose A Castillo,
Daniel Blumenthal,
Boris A Vinatzer,
Jean T Greenberg,
Richard W Michelmore
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ABSTRACT: Bacterial plant pathogens manipulate their hosts by injection of numerous effector proteins into host cells via type III secretion systems. Recognition of these effectors by the host plant leads to the induction of a defense reaction that often culminates in a hypersensitive response manifested as cell death. Genes encoding effector proteins can be exchanged between different strains of bacteria via horizontal transfer, and often individual strains are capable of infecting multiple hosts. Host plant species express diverse repertoires of resistance proteins that mediate direct or indirect recognition of bacterial effectors. As a result, plants and their bacterial pathogens should be considered as two extensive coevolving groups rather than as individual host species coevolving with single pathovars. To dissect the complexity of this coevolution, we cloned 171 effector-encoding genes from several pathovars of Pseudomonas and Ralstonia. We used Agrobacterium tumefaciens-mediated transient assays to test the ability of each effector to induce a necrotic phenotype on 59 plant genotypes belonging to four plant families, including numerous diverse accessions of lettuce (Lactuca sativa) and tomato (Solanum lycopersicum). Known defense-inducing effectors (avirulence factors) and their homologs commonly induced extensive necrosis in many different plant species. Nonhost species reacted to multiple effector proteins from an individual pathovar more frequently and more intensely than host species. Both homologous and sequence-unrelated effectors could elicit necrosis in a similar spectrum of plants, suggesting common effector targets or targeting of the same pathways in the plant cell.
Plant physiology 08/2009; 150(4):1733-49. · 6.53 Impact Factor
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ABSTRACT: The interplay between pathogen effectors, their host targets, and cognate recognition proteins provides various opportunities for antagonistic cycles of selection acting on plant and pathogen to achieve or abrogate resistance, respectively. Selection has previously been shown to maintain diversity in plant proteins involved in pathogen recognition and some of their cognate pathogen effectors. We analyzed the signatures of selection on 10 Arabidopsis thaliana genes encoding defense signal transduction proteins in plants, which are potential targets of pathogen effectors. There was insufficient evidence to reject neutral evolution for 6 genes encoding signaling components consistent with these proteins not being targets of effectors and/or indicative of constraints on their ability to coevolve with pathogen effectors. Functional constraints on effector targets may have provided the driving selective force for the evolution of guard proteins. PBS1, a known target of an effector, showed little variation but is known to be monitored by a variable guard protein. Evidence of selection maintaining diversity was present at NPR1, PAD4, and EDS1. Differences in the signatures of selection observed may reflect the numbers of effectors that target a particular protein, the presence or absence of a cognate guard protein, as well as functional constraints imposed by biochemical activities or interactions with plant proteins.
Genetics 01/2009; 181(2):671-84. · 4.01 Impact Factor
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ABSTRACT: Disease resistance (R) genes are often clustered in plant genomes and may exhibit heterogeneous rates of evolution. Some (type I R genes) have evolved rapidly through frequent sequence exchanges, while others (type II R genes) have evolved independently and tend to be conserved in different genotypes or related species. The RPP8 resistance gene in Arabidopsis thaliana is located at a complex locus that also harbors the sequence-related resistance genes HRT and RCY1 in different ecotypes. We sequenced 98 homologs of RPP8 from A. thaliana, Arabidopsis arenosa and Arabidopsis lyrata. Three lineages of type II and one lineage of type I RPP8 homologs were identified. Two of the three lineages of type II genes are each represented by a single-copy locus on either chromosomes I or V. Chromosome V contains two small clusters of RPP8 paralogs. One cluster contains both type I and type II genes and the other comprises only type I genes. These multi-copy loci have expanded and contracted through unequal crossovers, which have generated chimeric genes as well as variations in copy number. Sequence exchanges, most likely gene conversions, were detected between RPP8 homologs that are spatially separated by 2.2 Mb and 12 cM. The sequence exchanges between type I homologs within a locus have been more frequent than sequence exchanges between homologs from two different loci, indicating the influence of chromosomal position on the evolution of these R genes. However, physical distance was not the only factor determining the frequency of sequence exchange, because some closely linked paralogs exhibited little sequence exchange. At least two distinct lineages of type II RPP8 homologs were identified in different species, with obvious allelic/orthologous relationships within each lineage. Therefore, the differentiation of type I and type II RPP8 homologs seems to have occurred before speciation of A. thaliana, A. arenosa and A. lyrata.
The Plant Journal 05/2008; 54(1):69-80. · 6.16 Impact Factor
