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A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity

Abstract

Many bacterial pathogens of plants and animals use a type III secretion system to deliver diverse virulence-associated ‘effector’ proteins into the host cell1. The mechanisms by which these effectors act are mostly unknown; however, they often promote disease by suppressing host immunity2. One type III effector, AvrPtoB, expressed by the plant pathogen Pseudomonas syringae pv. tomato, has a carboxy-terminal domain that is an E3 ubiquitin ligase3. Deletion of this domain allows an amino-terminal region of AvrPtoB (AvrPtoB1–387) to be detected by certain tomato varieties leading to immunity-associated programmed cell death4. Here we show that a host kinase, Fen, physically interacts with AvrPtoB1–387 and is responsible for activating the plant immune response. The AvrPtoB E3 ligase specifically ubiquitinates Fen and promotes its degradation in a proteasome-dependent manner. This degradation leads to disease susceptibility in Fen-expressing tomato lines. Various wild species of tomato were found to exhibit immunity in response to AvrPtoB1–387 and not to full-length AvrPtoB. Thus, by acquiring an E3 ligase domain, AvrPtoB has thwarted a highly conserved host resistance mechanism.

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Figure 1: The Fen kinase is responsible for the Rsb phenotype.
Figure 2: Fen is ubiquitinated in the presence of AvrPtoB.
Figure 3: In the presence of AvrPtoB, Fen is degraded in a proteasome-dependent manner.
Figure 4: Rsb is present in many cultivated and wild species of tomato.

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Acknowledgements

We thank K. Munkvold and X. Tang for critical review of the manuscript; B. Randall for assistance with plant inoculations; J. Cohn and P. Pascuzzi for generation and characterization of the RG-PtoR(hpPto) line; J. Li and X. Tang for unpublished data; S. Collier for technical assistance; and our greenhouse staff for plant care. This work was supported, in part, by the NIH, the NSF and the Triad Foundation (G.B.M.).

Author Contributions T.R.R. and G.B.M. conceived, designed, and analysed the experiments. T.R.R. performed all of the experiments with the exceptions noted below. L.Z. performed the experiment shown in Figure 2b and Supplementary Fig. 5b. J.J.B. performed the experiments shown in Figure 1c and Supplementary Fig. 2. R.B.A. and F.X. provided technical assistance and unpublished clones. T.R.R. and G.B.M. wrote the manuscript. All authors contributed comments that were incorporated into the final version.

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Correspondence to Gregory B. Martin.

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Rosebrock, T., Zeng, L., Brady, J. et al. A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 448, 370–374 (2007). https://doi.org/10.1038/nature05966

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