The Major Resistance Gene Cluster in Lettuce Is Highly Duplicated and Spans Several Megabases

Abstract

At least 10 Dm genes conferring resistance to the oomycete downy mildew fungus Bremia lactucae map to the major resistance cluster in lettuce. We investigated the structure of this cluster in the lettuce cultivar Diana, which contains Dm3. A deletion breakpoint map of the chromosomal region flanking Dm3 was saturated with a variety of molecular markers. Several of these markers are components of a family of resistance gene candidates ( RGC2 ) that encode a nucleotide binding site and a leucine-rich repeat region. These motifs are characteristic of plant disease resistance genes. Bacterial artificial chromosome clones were identified by using duplicated restriction fragment length polymorphism markers from the region, including the nucleotide binding site-encoding region of RGC2. Twenty-two distinct members of the RGC2 family were characterized from the bacterial artificial chromosomes; at least two additional family members exist. The RGC2 family is highly divergent; the nucleotide identity was as low as 53% between the most distantly related copies. These RGC2 genes span at least 3.5 Mb. Eighteen members were mapped on the deletion breakpoint map. A comparison between the phylogenetic and physical relationships of these sequences demonstrated that closely related copies are physically separated from one another and indicated that complex rearrangements have shaped this region. Analysis of low-copy genomic sequences detected no genes, including RGC2 , in the Dm3 region, other than sequences related to retrotransposons and transposable elements. The related but divergent family of RGC2 genes may act as a resource for the generation of new resistance phenotypes through infrequent recombination or unequal crossing over. INTRODUCTIONDisease resistance genes frequently occur in tightly linked clusters (Pryor, 1987; Crute and Pink, 1996;Michelmore and Meyers, 1998). Clusters of plant resistance genes were first established by use of classic genetic techniques; detailed molecular analyses are now beginning to unravel the complexity of these loci and the underlying mechanisms determining their structure (Parniske et al., 1997;Song et al., 1997). It is becoming increasingly apparent that such clusters may be both common and complex genomic regions in plants.Clusters of resistance genes have been identified in diverse plant species. More than 30 different resistance specificities to the single fungal pathogen responsible for flax rust disease, Melampsora lini , have been mapped to five linkage groups (Flor, 1971;Islam and Shepherd, 1991). These loci exemplify two possible genetic arrangements that may exist for clusters of resistance genes: the flax L locus contains at least 13 allelic rust resistance specificities, and the more complex M locus exists as a tandem array of at least seven genes (Islam and Shepherd, 1991). In maize, multiple Rp genes, both linked and allelic, have been observed to mediate resistance to the rust fungus Puccinia sorghi ; 16 genetically separable loci were mapped to a single cluster known as th...

The Fractionated Orthology of Bs2 and Rx/Gpa2 Supports Shared Synteny of Disease Resistance in the Solanaceae

“…Chromosomal inversions are indicated with a circular arrow, and chromosomes that are separated by translocations are connected by dotted lines. also may explain the dramatic expansion observed in some R-gene clusters (Meyers et al 1998a). The translocation breakpoint proposed within the Rx/Gpa2 cluster would result in these sequences being dispersed to the centromeric and telomeric regions of the lower arm of P9 (Figure 6).…”

“…R genes often occur in clusters of tandem duplications that can span several megabases and include a multitude of copies of functional R genes, pseudogenes, and other genes within the clusters (Meyers et al 1998a;Kuang et al 2004;Smith et al 2004). Of the various modes of evolution ascribed to these clusters, sequence exchange between R genes within the cluster by unequal crossing over or illegitimate recombination is especially noteworthy (Michelmore and Meyers 1998;Ellis et al 2000;Hulbert et al 2001;McDowell and Simon 2006;Friedman and Baker 2007;Wicker et al 2007).…”

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

“…The major cluster of resistance genes in lettuce is comprised of over 24 R gene candidates (RGCs) spanning several megabases (Meyers et al 1998a). Genetic and mutation data indicate that one RGC2 sequence encodes Dm3.…”

“…The cluster has evolved by a series of ancient duplications and more recent deletions. Unequal crossing-over with exchanges both between and within coding regions has occurred but has been infrequent.The major cluster of resistance genes in lettuce is comprised of over 24 R gene candidates (RGCs) spanning several megabases (Meyers et al 1998a). Genetic and mutation data indicate that one RGC2 sequence encodes Dm3.…”

A high-resolution linkage map of the vicinity of the rice submergence tolerance locus Sub1

“…The approach has been successfully applied in non-model crops, such as wheat (Lagudah et al 1997), barley (Buschges et al 1997;Lahaye et al 1998;Schwarz et al 1999), sugar beet (Cai et al 1997) and lettuce (Meyers et al 1998). Most of the genes cloned in this way confer pest resistance, and the detection of common motifs has allowed additional resistance-gene analogs to be mapped in many species (Kanazin et al 1996;Chen et al 1998;Collins et al 1998;Spielmeyer et al 1998).…”