A Mutation within the Leucine-Rich Repeat Domain of the Arabidopsis Disease Resistance Gene RPS5 Partially Suppresses Multiple Bacterial and Downy Mildew Resistance Genes

Abstract

Recognition of pathogens by plants is mediated by several distinct families of functionally variable but structurally related disease resistance ( R ) genes. The largest family is defined by the presence of a putative nucleotide binding domain and 12 to 21 leucine-rich repeats (LRRs). The function of these LRRs has not been defined, but they are speculated to bind pathogen-derived ligands. We have isolated a mutation in the Arabidopsis RPS5 gene that indicates that the LRR region may interact with other plant proteins. The rps5-1 mutation causes a glutamate-to-lysine substitution in the third LRR and partially compromises the function of several R genes that confer bacterial and downy mildew resistance. The third LRR is relatively well conserved, and we speculate that it may interact with a signal transduction component shared by multiple R gene pathways. INTRODUCTIONThe molecular recognition of pathogens by plants is often characterized by a gene-for-gene relationship that requires a specific plant resistance ( R ) gene and a corresponding pathogen avirulence ( avr ) gene (Flor, 1971). Genetic evidence from a wide diversity of plant pathosystems suggests that when an appropriate R-avr gene pair is present, the result is host resistance, whereas absence or inactivation of either member of the gene pair results in susceptibility of the host to the pathogen. A common explanation for the molecular basis of this gene-for-gene relationship is an elicitorreceptor model (Gabriel and Rolfe, 1990). According to this model, avr genes directly or indirectly produce an elicitor that is recognized by the corresponding R gene-encoded receptor. This molecular interaction then triggers downstream signaling events that result in the activation of plant defenses and the limitation of pathogen growth.R genes have been cloned from several plant species (reviewed in Bent, 1996; Baker et al., 1997; Hammond-Kosack and Jones, 1997). These include R genes that mediate resistance to bacterial, fungal, oomycete, viral, and nematode pathogens. Many of these R gene products share structural motifs, which indicates that disease resistance to diverse pathogens may operate through similar pathways. For example, leucine-rich repeats (LRRs) are common to most of the R genes that have been characterized (Bent et al., 1994;Jones et al., 1994;Mindrinos et al., 1994; Whitham et al., 1994; Grant et al., 1995;Lawrence et al., 1995;Song et al., 1995; Dixon et al., 1996; Anderson et al., 1997;Parker et al., 1997). LRRs have been shown to play a role in protein-protein interactions (Kobe and Deisenhofer, 1994). This fact, along with the common occurrence of LRRs in R gene proteins, has led to speculation that LRRs serve as the binding domain for the pathogen-produced elicitor (Bent, 1996; Baker et al., 1997).Despite recent work in this area, it remains to be proven that LRR-containing R gene products function as receptors. In tomato, high-affinity binding sites from intact membranes have been found for an elicitor produced by races of Cladosporium fu...

Structural Determinants at the Interface of the ARC2 and Leucine-Rich Repeat Domains Control the Activation of the Plant Immune Receptors Rx1 and Gpa2

“…This is supported by the observation that the N-terminal end of the LRR in Rx1 and Gpa2 is more conserved than the C-terminal region, consistent with a dual role of this domain in NB-LRR protein functioning. In the conserved N-terminal repeats of the LRR, several autoactivating mutations have been identified in Rx1 (Bendahmane et al, 2002;Farnham and Baulcombe, 2006), and in the resistance protein RPS5, a mutation at this location negatively affected the functioning of RPS5 itself and other resistance proteins (Warren et al, 1998). From the results of the Gpa2/Rx1 sequence exchange study, we conclude that as long as the cooperating N-terminal LRR regions and the ARC2 domains are retained as a compatible unit, the C-terminal region of the LRR responsible for recognition can be exchanged and still yield a functional protein.…”

The Rx Gene from Potato Controls Separate Virus Resistance and Cell Death Responses

“…It is surprising that Rx is similar to the leucine zipper class of NBS-LRR proteins. The other proteins in this class control resistance against bacteria (Mindrinos et al, 1994;Grant et al, 1995;Warren et al, 1998), nematodes (Milligan et al, 1998), and insects (Rossi et al, 1998). The product of N, which is the other known virus R gene, belongs to a separate class of NBS-LRR proteins in which the N-terminal domain has similarity to the Toll protein and the interleukin receptor (Whitham et al, 1994).…”

Plant NBS-LRR proteins in pathogen sensing and host defense

“…In addition, the ability of Rx to respond to the potato virus X coat protein is dependent on the carboxy-terminal portion of the LRR domain, further indicating a positive signaling function for this domain43. Finally, the rps5-2 mutant contains a proline-to-serine substitution in the LRR domain and results in loss of RPS5 function rather than constitutive activity 23 .…”

“…RPS5 is a plant NBS-LRR, whereas PBS1 is a protein kinase with unknown substrates [22][23][24] . Both proteins are required for the recognition of P. syringae strains expressing AvrPphB.…”