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...

Genetic mapping of rust resistance genes in confection sunflower line HA-R6 and oilseed line RHA 397

“…The sunflower rust R-gene cluster in LG13 is similar to the multi-gene clusters in other crops (Islam and Shepherd 1991;Meyers et al 1998Meyers et al , 2003Hulbert et al 2001;Richly et al 2002;Wei et al 1999Wei et al , 2002Baumgarten et al 2003). This region encompasses four rust R-genes (R 4 , R adv , R 11 , and R 13 ), and three downy mildew R-genes (Pl 5 , Pl 8 , and Pl 21 ) (Lawson et al 1998;Bert et al 2001;Yu et al 2003;Radwan et al 2003Radwan et al , 2008Qi et al 2011b;Vincourt et al 2012).…”

Resistance gene analogues of chickpea (Cicer arietinum L.): isolation, genetic mapping and association with a Fusarium resistance gene cluster

“…However, genetic clustering of these RGAs can either result from physical clustering with multiple homologous sequences in close vicinity or be the result of suppressed recombination in this genomic region. Such clusters with reduced recombination rates were in fact identified in other crops such as soybean and lettuce (Kanazin et al 1996;Meyers et al 1998). Genetic mapping of Cicer RGAs in other inter-specific crosses will be useful to clarify their genomic organisation.…”

Recombination between diverged clusters of the tomato Cf-9 plant disease resistance gene family

“…The composition and size of these clusters exhibited strong intra-and interspecific variation, suggesting rapid reorganization (22). Similar ectopic events might have been involved in the generation of the Dm3 complex of lettuce, in which diverged R gene homologues are dispersed over several Mb (13,23). The L and M loci in flax are composed of members of the same gene family which suggests a common progenitor; however, the loci reside on different chromosomes (4).…”