First published online September 10, 2004; 10.1105/tpc.104.024117
The Plant Cell 16:2822-2835 (2004)
© 2004 American Society of Plant Biologists
Arabidopsis RIN4 Negatively Regulates Disease Resistance Mediated by RPS2 and RPM1 Downstream or Independent of the NDR1 Signal Modulator and Is Not Required for the Virulence Functions of Bacterial Type III Effectors AvrRpt2 or AvrRpm1
Youssef Belkhadira,
Zachary Nimchuka,
David A. Huberta,
David Mackeya,1 and
Jeffery L. Dangla,b,c,d,2
a Department of Biology, University of North Carolina, Chapel Hill, North Carolina 27599
b Department of Microbiology and Immunology, University of North Carolina, Chapel Hill, North Carolina 27599
c Curriculum in Genetics, University of North Carolina, Chapel Hill, North Carolina 27599
d Carolina Center for Genome Sciences, University of North Carolina, Chapel Hill, North Carolina 27599
2 To whom correspondence should be addressed. E-mail dangl{at}email.unc.edu; fax 919-962-1625.
Bacterial pathogens deliver type III effector proteins into the plant cell during infection. On susceptible (r) hosts, type III effectors can contribute to virulence. Some trigger the action of specific disease resistance (R) gene products. The activation of R proteins can occur indirectly via modification of a host target. Thus, at least some type III effectors are recognized at site(s) where they may act as virulence factors. These data indicate that a type III effector's host target might be required for both initiation of R function in resistant plants and pathogen virulence in susceptible plants. In Arabidopsis thaliana, RPM1-interacting protein 4 (RIN4) associates with both the Resistance to Pseudomonas syringae pv maculicola 1 (RPM1) and Resistance to P. syringae 2 (RPS2) disease resistance proteins. RIN4 is posttranslationally modified after delivery of the P. syringae type III effectors AvrRpm1, AvrB, or AvrRpt2 to plant cells. Thus, RIN4 may be a target for virulence functions of these type III effectors. We demonstrate that RIN4 is not the only host target for AvrRpm1 and AvrRpt2 in susceptible plants because its elimination does not diminish their virulence functions. In fact, RIN4 negatively regulates AvrRpt2 virulence function. RIN4 also negatively regulates inappropriate activation of both RPM1 and RPS2. Inappropriate activation of RPS2 is nonspecific disease resistance 1 (NDR1) independent, in contrast with the established requirement for NDR1 during AvrRpt2-dependent RPS2 activation. Thus, RIN4 acts either cooperatively, downstream, or independently of NDR1 to negatively regulate RPS2 in the absence of pathogen. We propose that many P. syringae type III effectors have more than one target in the host cell. We suggest that a limited set of these targets, perhaps only one, are associated with R proteins. Thus, whereas any pathogen virulence factor may have multiple targets, the perturbation of only one is necessary and sufficient for R activation.
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