WRR4 Encodes a TIR-NB-LRR Protein That Confers Broad-Spectrum White Rust Resistance in Arabidopsis thaliana to Four Physiological Races of Albugo candida

Abstract

White blister rust in the Brassicaceae is emerging as a superb model for exploring how plant biodiversity has channeled speciation of biotrophic parasites. The causal agents of white rust across a wide breadth of cruciferous hosts currently are named as variants of a single oomycete species, Albugo candida. The most notable examples include a major group of physiological races that each are economically destructive in a different vegetable or oilseed crop of Brassica juncea (A. candida race 2), B. rapa (race 7), or B. oleracea (race 9); or parasitic on wild crucifers such as Capsella bursa-pastoris (race 4). Arabidopsis thaliana is innately immune to these races of A. candida under natural conditions; however, it commonly hosts its own molecularly distinct subspecies of A. candida (A. candida subsp. arabidopsis). In the laboratory, we have identified several accessions of Arabidopsis thaliana (e.g.,. Ws-3) that can permit varying degrees of rust development following inoculation with A. candida races 2, 4, and 7, whereas race 9 is universally incompatible in Arabidopsis thaliana and nonrusting resistance is the most prevalent outcome of interactions with the other races. Subtle variation in resistance phenotypes is evident, observed initially with an isolate of A. candida race 4, indicating additional genetic variation. Therefore, we used the race 4 isolate for map-based cloning of the first of many expected white rust resistance (WRR) genes. This gene was designated WRR4 and encodes a cytoplasmic toll-interleukin receptor-like nucleotide-binding leucine-rich repeat receptor-like protein that confers a dominant, broad-spectrum white rust resistance in the Arabidopsis thaliana accession Columbia to representative isolates of A. candida races 2, 4, 7, and 9, as verified by transgenic expression of the Columbia allele in Ws-3. The WRR4 protein requires functional expression of the lipase-like protein EDS1 but not the paralogous protein PAD4, and confers full immunity that masks an underlying nonhypersensitive incompatibility in Columbia to A. candida race 4. This residual incompatibility is independent of functional EDS1.

Natural history of Arabidopsis thaliana and oomycete symbioses

“…As a consequence, this pathosystem remains undeveloped as a potentially excellent model for investigating such topics as species-level characteristics including host determinants of parasite speciation involving pathogen receptor-like genes ( Fig. 1a; Rehmany et al 2000;Borhan et al 2008), and important aspects of compatible interactions including induced accessibility (pathogen-activated defence suppression) and source-sink dynamics affecting carbohydrate metabolism (Chou et al 2000;Holub and Cooper 2004;Tang et al 1996). Only two UK isolates of AcA have thus far been named including the type isolate Acem1 from East Malling, Kent and Acks1 from Keswick, Cumbria (Borhan et al 2004;Holub et al 1995).…”

The Molecular Basis of Host Specialization in Bean Pathovars of Pseudomonas syringae

“…However, plants can also contain receptors that mediate ETI to nonadapted pathogens, such as RPS4 and RPS5 proteins that could potentially protect Arabidopsis thaliana against legume pathovars of P. syringae in natural populations (Gassmann et al 1999;Warren et al 1999). Additionally, ETI-mediating receptors can provide an effective barrier of broad-spectrum resistance to a pathogen species (Borhan et al 2008;Song et al 2003;Tai et al 1999;Vera Cruz et al 2000), particularly if disruption or loss of the recognized effector significantly affects pathogen fitness on susceptible hosts. Both PTI and ETI can limit the growth of P. syringae across a wide variety of hosts (Ferrante et al 2009;Ham et al 2007;Li et al 2005;Lin and Martin 2007;Perchepied et al 2006;Takeuchi et al 2003;Wen et al 2010;Wroblewski et al 2009).…”

Genome-wide survey of Arabidopsis natural variation in downy mildew resistance using combined association and linkage mapping

“…Among them, 20 have been assigned a function. They include R genes mediating specific recognition of bacteria such as RPM1, RPS2, RPS4, RPS5, and RRS1 or oomycetes such as RAC1, WRR4, RPP1, RPP2, RPP5, RPP7, RPP8, and RPP13 (3,(6)(7)(8)(9)(10)(11)(12). RLM1 and RLM3 encode broad fungal resistance against ascomycete parasites (13,14).…”