Arabidopsis RAR1 Exerts Rate-Limiting Control of R Gene–Mediated Defenses against Multiple Pathogens

Abstract

We have identified the Arabidopsis ortholog of barley RAR1 as a component of resistance specified by multiple nucleotide binding/Leu-rich repeat resistance ( R ) genes recognizing different bacterial and oomycete pathogen isolates. Characterization of partially and fully defective rar1 mutations revealed that wild-type RAR1 acts as a rate-limiting regulator of early R gene-triggered defenses, determining the extent of pathogen containment, hypersensitive plant cell death, and an oxidative burst at primary infection sites. We conclude that RAR1 defense signaling function is conserved between plant species that are separated evolutionarily by 150 million years. RAR1 encodes a protein with two zinc binding (CHORD) domains that are highly conserved across eukaryotic phyla, and the single nematode CHORDcontaining homolog, Chp , was found previously to be essential for embryo viability. An absence of obvious developmental defects in null Arabidopsis rar1 mutants favors the notion that, in contrast, RAR1 does not play a fundamental role in plant development. INTRODUCTIONIn countering attack by microbial pathogens or insects, plants have evolved resistance ( R ) genes that specifically recognize corresponding pathogen avirulence ( avr ) genes to trigger plant defenses (Dangl and Jones, 2001). Two plant R gene-encoded proteins, tomato Pto and rice Pi-ta, have been shown to interact physically with their pathogen Avr counterparts, AvrPto and Avr-Pita, respectively, in in vitro assays (Scofield et al., 1996;Tang et al., 1996;Jia et al., 2000). Other plant R proteins may associate with pathogen Avr proteins indirectly within a protein complex . In the absence of a corresponding R gene, the pathogen is able to colonize its host. Some Avr proteins are virulence factors that facilitate pathogen growth or interfere with basal plant defenses (Nimchuk et al., 2000;Staskawicz et al., 2001). R-Avr protein recognition commonly involves localized programmed plant cell death (the hypersensitive response [HR]), an oxidative burst producing reactive oxygen intermediates (ROI), and the accumulation of salicylic acid (SA), a phenolic molecule necessary for the induction of systemic immunity (systemic acquired resistance) (Feys and Parker, 2000).Plant R proteins share a limited repertoire of motifs with animal proteins that control innate immunity (Staskawicz et al., 2001). The most prevalent R gene class encodes predicted cytosolic proteins with a central nucleotide binding (NB) domain and C-terminal Leu-rich repeats (LRRs) (Dangl and Jones, 2001). At least one NB-LRR-type protein, Arabidopsis RPM1, is tethered to the plasma membrane, where it may encounter bacterial Avr proteins that are secreted into the plant cell (Boyes et al., 1998;Nimchuk et al., 2000). NB-LRR proteins fall into two subclasses based on their different N-terminal motifs. One group possesses an N-terminal coiled-coil (CC) domain. The second group has N-terminal similarity to the cytoplasmic Toll Interleukin-1 Receptor (TIR) domains of human and Drosophila Toll-like r...

Specific Arabidopsis HSP90.2 alleles recapitulate RAR1 cochaperone function in plant NB-LRR disease resistance protein regulation

“…S2). The rar1 alleles are consistent with previous mutations: premature stops, splicing defects, and disruption of zinc-coordinating residues (12,13). The allele of hsp90.2 displayed intermediate susceptibility and full penetrance, as previously found for hsp90.2-1 and hsp90.…”

“…From the rar1 suppressor screen, rough mapping was preformed by crossing rsp rar1-21 mutants and the Landsberg erecta rar1-10 mutant (12). F 2 plants were tested for rsp rar1-21-like resistance responses by spray inoculation as described above.…”

Plant disease susceptibility conferred by a “resistance” gene

“…Complete resistance mediated by several R genes requires RAR1, SGT1b, and/or HSP90 to maintain NBS-LRR steadystate levels (25)(26)(27)(28)(29)(30). RAR1 and HSP90 are thought to act as cochaperones that positively regulate NBS-LRR levels (26,(28)(29)(30).…”

Differential Requirement of Oryza sativa RAR1 in Immune Receptor-Mediated Resistance of Rice to Magnaporthe oryzae

“…In Arabidopsis, RAR1 is required for the resistance to P. syringae mediated by the Rpm1, Rps2, and Rps4 genes, and is also required for the resistance to Hyaloperonospora arabidopsidis mediated by Rpp4. In contrast, neither the Rpp2-nor Rpp8-mediated resistance to H. arabidopsidis requires RAR1 Holt et al, 2005;Muskett et al, 2002;Tornero et al, 2002). These findings indicate that RAR1 contributes differentially to NB-LRR-mediated resistance responses.…”