Complex formation, promiscuity and multi-functionality: protein interactions in disease-resistance pathways

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Abstract

Accumulating evidence indicates that plant disease-resistance (R) proteins assemble in hetero-multimeric protein complexes in the absence of pathogens. Such complexes might enable the indirect recognition of pathogen effector molecules during attempted pathogen invasion. RAR1 and SGT1 are required for the function of most known R proteins. They interact with each other and with diverse protein complexes, which might explain their multi-functionality. The promiscuous behavior of RAR1 and SGT1 might be crucial for the formation and activation of R protein-containing recognition complexes as well as for regulating downstream signaling processes.

Section snippets

R protein complexes

Although several R-AVR pairs have been isolated, the molecular mechanisms of AVR recognition by R proteins and activation of downstream signaling is poorly understood. The simplest model is that R proteins are receptors for the corresponding AVR molecules. Indeed, rice PI-TA, a CC–NB–LRR protein, directly interacts in vitro with AVR-PITA from Magnaporthe grisea [5]. However, direct interactions between R-AVR partners have rarely been demonstrated, indicating that the receptor-ligand model might

RAR1–SGT1 complex in R gene-triggered resistance

Mutations in barley RAR1 suppress resistance against the powdery mildew fungus specified by the CC–NB–LRR gene MLA12, one of many resistance specificities encoded at the MLA disease-resistance locus [14]. Subsequent work has shown that RAR1 is also essential for the function of a subset of MLA-encoded R specificities and of other unlinked powdery mildew R loci 15, 16. A conserved role of RAR1 in R gene-specified resistance against oomycete, bacterial and viral pathogens is now well documented

Possible operation points of the RAR1–SGT1 complex in disease-resistance pathways

Uncoupling of AVR recognition from RAR1 and SGT1 dependence strongly suggest that RAR1 and SGT1 are not involved in ‘upstream’ events such as processing or transport of AVR effectors (e.g. AVRMLA6). This is further supported by the finding that AvrRpt2-mediated disappearance of RIN4 occurs independently of RAR1 [12]. These data indicate that RAR1 and SGT1 might function in R gene-dependent resistance during: (1) formation of R protein complexes, (2) activation of assembled R protein complexes

Possible biochemical functions of RAR1 and SGT1 complexes

Analysis of SGT1 functions in yeast promises to provide leads for SGT1 functions in plants because either of the two Arabidopsis SGT1 homologs, SGT1a and SGT1b, can complement yeast sgt1 mutant strains [25]. Saccharomyces cerevisiae SGT1 protein was originally shown to associate with SKP1 protein and to be required for assembly of the centromere-binding factor 3 (CBF3) kinetochore complex [23]. SKP1 is also a core component of SCF (SKP1/CULLIN/F-box protein) E3 ubiquitin ligases. SCF complexes

Acknowledgements

We thank Jane Parker, Laurent Noel, and Jack Peart for critical reading of the manuscript. Our research was supported by grants from the BBSRC, the Gatsby Charitable Organization, and the Max Planck Society.

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