Clusters of Resistance Genes in Plants Evolve by Divergent Selection and a Birth-and-Death Process

Abstract

Classical genetic and molecular data show that genes determining disease resistance in plants are frequently clustered in the genome. Genes for resistance (R genes) to diverse pathogens cloned from several species encode proteins that have motifs in common. These motifs indicate that R genes are part of signal-transduction systems. Most of these R genes encode a leucine-rich repeat (LRR) region. Sequences encoding putative solvent-exposed residues in this region are hypervariable and have elevated ratios of nonsynonymous to synonymous substitutions; this suggests that they have evolved to detect variation in pathogen-derived ligands. Generation of new resistance specificities previously had been thought to involve frequent unequal crossing-over and gene conversions. However, comparisons between resistance haplotypes reveal that orthologs are more similar than paralogs implying a low rate of sequence homogenization from unequal crossing-over and gene conversion. We propose a new model adapted and expanded from one proposed for the evolution of vertebrate major histocompatibility complex and immunoglobulin gene families. Our model emphasizes divergent selection acting on arrays of solvent-exposed residues in the LRR resulting in evolution of individual R genes within a haplotype. Intergenic unequal crossing-over and gene conversions are important but are not the primary mechanisms generating variation.Plants, like animals, are continually challenged by a myriad of potential pathogens. There is increasing evidence that defense systems of plants are at least as complex as vertebrate defense systems. Unlike animals, however, plants do not have a circulatory system and therefore cannot rely on a specialized, proliferative immune system. Each plant cell has to be capable of defense, even though this defense is coordinated locally and systemically between cells. There are a variety of types of resistance genes and mechanisms, some induced and some constitutive (for review, see Godiard et al. 1994;Michelmore 1995;Hammond-Kosack and Jones 1997). Often, although not always, disease resistance in plants is determined by single, usually dominant, genes. The recent cloning of several such resistance genes (R genes) is providing insight into their function and evolution. The defense system of plants may be ancient and predate the evolution of the immune system; genes similar to plant R genes have been identified in mammals van der Biezen and Jones 1998).In this review we consider what is known about the genomic organization and evolution of disease resistance genes in plants. The picture that is emerging for the organization and evolution of plant R genes is similar to that of the vertebrate major histocompatibility complex (MHC), T-cell receptor (TCR), and immunoglobulin genes. Therefore, although the specific types of genes involved are different, the evolutionary forces shaping the plant and vertebrate defense systems may be similar. We propose a model for the evolution of plant R genes that is adapted and expanded from a m...

Allele mining in Solanum: conserved homologues of Rpi-blb1 are identified in Solanum stoloniferum

“…Genomic organization of the Rpi-blb1 gene cluster Many R genes are present within clusters of tightly linked genes (Michelmore and Meyers 1998;Meyers et al 2003). This is also the case for the Rpi-blb1 gene (van der Vossen et al 2003).…”

Recognition and signal transduction in the expression of Phytophthora resistance in soybean [Glycine max (L) Merr]

“…The amplified regions between the two classes of genes were distinguished by the presence of a 63-nt deletion in the Class I Rps1-k genes. The solvent-exposed residues within the consensus repeat sequence xxLxLxx of the LRR domain have been shown to be highly divergent and under substantial diversifying selection (Meyers et al 1998;Parniske et al 1997). Therefore, it is very unlikely that RT-PCR products originated from transcripts of paralogous Rps1-k sequences rather than from that of the Rps1-k candidate genes; and we conclude that both classes of candidate Rps1-k genes are transcribed at very low levels.…”

“…This clustering feature can facilitate the expansion of R gene numbers and the generation of new R gene specificities through recombination and positive selection (Michelmore and Meyers 1998). Study of multiple, genetically linked R gene families has provided insight into the molecular mechanisms of R gene evolution and the generation of novel recognition specificity.…”

“…The RGC2 (Dm3) family of lettuce spans at least 3.5 Mb. The estimated distance between members of RGC2 family is at least 120 kb (Meyers et al 1998). The tomato Pto locus carries five genes that are evidently not evolved from recent gene duplication.…”

“…The solvent-exposed residues within the consensus repeat sequence xxLxLxx of LRRs have been shown to be highly divergent and under substantial diversifying selection (Meyers et al 1998;Parniske et al 1997 Table 3). This suggested that diversifying selection has been imposed on these solvent-exposed residues.…”