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 ...

Genome organization in dicots: Genome duplication in Arabidopsis and synteny between soybean and Arabidopsis

“…RPP5 and RPP8 (arabIV and arabV, respectively) both confer resistance to Peronospora parasitica (downy mildew). RPP5 is a member of the TIR-NBS-LRR R-gene subclass whereas RPP8 is an example of the LZ-NBS-LRR subclass (22,23). RPS5 (arabI) conditions resistance to Pseudomonas syringae and is also a member of the LZ-NBS-LRR R-gene subclass (24).…”

Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement

“…Regions of elevated Tajima's D encompass 4.8% of the genome, yet contain 12% of the anchored NBS-LRR disease resistance genes. NBS-LRR genes are known to be targets of diversifying selection 24 ; however, the identity of possible pathogen targets in chickpea remains uncertain. Among the 0.7% of the genome with Tajima's D < −2 is a region of Ca4 that contains a tandem array of three co-orthologs of the MATE family transporter TT12.…”

Evolution of plant resistance at the molecular level: ecological context of species interactions

“…Adaptive evolution resulting from mutations on the solvent-exposed residues of leucine-rich repeats (LRR) has been shown, presumably enabling detection of variable pathogen-related ligands (Parniske et al, 1997;Meyers et al, 1998;Noel et al, 1999;Dixon et al, 2000;Sun et al, 2001). In addition, recombination plays an important role in generating new LRR configurations (McDowell et al, 1998;Luck et al, 2000) and new paralogues at complex loci (Parniske et al, 1997;Meyers et al, 1998;Sun et al, 2001). However, mutation and recombination seem to differentially affect R-gene families, which vary in their density and positioning along the chromosome (Parniske et al, 1997;Meyers et al, 1998), in their copy numbers Noel et al, 1999), in the proportion of nonfunctional genes (Parniske et al, 1997;Noel et al, 1999;Sun et al, 2001), in divergence levels among paralogues (Wei et al, 1999;Sun et al, 2001), and in relative rates of recombination (Wei et al, 1999;Sun et al, 2001).…”