Intragenic Recombination and Diversifying Selection Contribute to the Evolution of Downy Mildew Resistance at the RPP8 Locus of Arabidopsis

Abstract

Pathogen resistance ( R ) genes of the NBS-LRR class (for nucleotide binding site and leucine-rich repeat) are found in many plant species and confer resistance to a diverse spectrum of pathogens. Little is known about the mechanisms that drive NBS-LRR gene evolution in the host-pathogen arms race. We cloned the RPP8 gene (for resistance to Peronospora parasitica ) and compared the structure of alleles at this locus in resistant Landsberg erecta (L er -0) and susceptible Columbia (Col-0) accessions. RPP8-L er encodes an NBS-LRR protein with a putative N-terminal leucine zipper and is more closely related to previously cloned R genes that confer resistance to bacterial pathogens than it is to other known RPP genes. The RPP8 haplotype in L er -0 contains the functional RPP8-L er gene and a nonfunctional homolog, RPH8A. In contrast, the rpp8 locus in Col-0 contains a single chimeric gene, which was likely derived from unequal crossing over between RPP8-L er and RPH8A ancestors within a L er -like haplotype. Sequence divergence among RPP8 family members has been accelerated by positive selection on the putative ligand binding region in the LRRs. These observations indicate that NBS-LRR molecular evolution is driven by the same mechanisms that promote rapid sequence diversification among other genes involved in non-self-recognition. INTRODUCTIONA broad range of microorganisms have evolved the ability to use plants as a nutritional resource, and plants in turn have evolved multiple lines of defense against pathogen invasion (Hammond-Kosack and Jones, 1996a). Inducible defenses are mediated through gene-for-gene systems in which the plant carrying a particular resistance ( R ) gene allele responds to pathogens carrying a matching avirulence ( avr ) gene (Flor, 1971). Most plants contain large collections of highly specific R genes, which are thought to encode specialized receptors that recognize avr gene-dependent elicitors (Keen, 1990). If the R gene or the corresponding avr gene is not functional, then recognition does not occur, defenses are not activated, and the plant is susceptible to infection. Thus, pathogens can circumvent gene-for-gene resistance by alteration or loss of avr genes. This places the host under selective pressure to evolve new recognition capabilities. avr gene mutations and deletions occur at high frequency in nature (van Kan et al., 1991;Rohe et al., 1995;Sweigard et al., 1995;Joosten et al., 1997), but the host's response in this evolutionary arms race is not well understood.Two themes have emerged from recent molecular characterization of R genes. R genes are often members of tightly linked multigene families, which can be functionally diversified (Hammond-Kosack and Jones, 1996b). A second, somewhat unexpected generality is that all R genes characterized to date, with one exception (Martin et al., 1993), encode proteins with long stretches of leucine-rich repeats (LRRs) . LRRs are present in a wide variety of proteins and participate in protein-protein interactions and ligand binding (Kobe ...

Molecular Basis for Specific Recognition of Bacterial Ligands by NAIP/NLRC4 Inflammasomes

“…Moreover, we find evidence for positive selection acting on this domain but not on the rest of the protein (Figure 5). This signature of positive selection is consistent with direct contact between this domain and rapidly evolving pathogen ligands, as has been observed in other host-pathogen interactions (Daugherty and Malik, 2012; Mitchell et al, 2012) and even some plant NLRs (McDowell et al, 1998). …”

Signaling Pathways That Regulate the Enhanced Disease Resistance of Arabidopsis “Defense, No Death” Mutants

“…The Landsberg erecta allele of RPP8 confers resistance to Emco5, while Columbia plants are susceptible to Emco5 and carry a non-functional allele of RPP8 (McDowell et al 1998). Columbia dnd1 plants exhibited strong resistance to this virulent isolate of H. parasitica , as expected (Yu et al 1998), although this resistance was not as effective as that conferred by RPP8 (Fig.…”

EDR2 negatively regulates salicylic acid-based defenses and cell death during powdery mildew infections of Arabidopsis thaliana

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