Mode of Amplification and Reorganization of Resistance Genes During Recent Arabidopsis thaliana Evolution

Abstract

The NBS-LRR (nucleotide-binding site plus leucine-rich repeat) genes represent the major class of disease resistance genes in flowering plants and comprise 166 genes in the ecotype Col-0 of Arabidopsis thaliana. NBS-LRR genes are organized in single-gene loci, clusters, and superclusters. Phylogenetic analysis reveals nine monophyletic clades and a few phylogenetic orphans. Most clusters contain only genes from the same phylogenetic lineage, reflecting their origin from the exchange of sequence blocks as a result of intralocus recombination. Multiple duplications increased the number of NBS-LRR genes in the progenitors of Arabidopsis, suggesting that the present complexity in Col-0 may derive from as few as 17 progenitors. The combination of physical and phylogenetic analyses of the NBS-LRR genes makes it possible to detect relatively recent gene rearrangements, which increased the number of NBS-LRR genes by about 50, but which are almost never associated with large segmental duplications. The identification of 10 heterogeneous clusters containing members from different clades demonstrates that sequence sampling between different resistance gene loci and clades has occurred. Such events may have taken place early during flowering plant evolution, but they generated modules that have been duplicated and remobilized also more recently.

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

“…For the Rx/Gpa2 cluster, a chromosome translocation/ inversion breakpoint dispersed the R-gene homologs and associated markers in other genera relative to potato. Others have observed the genomic distribution of R genes as a somewhat random phenomenon (Leister et al 1998;Pan et al 2000a;Richly et al 2002), but it has been since shown in Arabidopsis that R-gene locations are consistent with the rearrangements of their chromosomal context (Baumgarten et al 2003). In the Solanaceae, 22 genome rearrangements distinguish tomato and pepper (Livingstone et al 1999).…”

“…The first predicts rapid rearrangement of R-gene distribution during genome evolution, yielding poor conservation of R-gene locations (Leister et al 1998;Richly et al 2002;Meyers et al 2003). Indeed, in monocots, extensive loss of genomewide R-gene colinearity has been attributed to frequent R-gene duplication and ectopic transposition (Gale and Devos 1998;Paterson et al 2003).…”

The obscure events contributing to the evolution of an incipient sex chromosome in Populus: a retrospective working hypothesis

“…In Populus, these clusters are distributed unevenly over the chromosomes and in clusters of clusters or "superclusters" of which three occur on chromosome XIX. Highly similar sequences in head-to-tail orientation suggest that intralocus recombination gave rise to the translocation of a sequence block (Richy et al 2002). The largest NBS-LRR gene supercluster on Populus chromosome XIX collocates with the resistance loci MER, R1, and RUS, conferring qualitative or quantitative resistance to Melampsora larici-populina (Lescot et al 2004;Jorge et al 2005;Bresson et al 2011).…”

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

“…3). Plant R genes often occur in clusters, and genes within one cluster are mostly derived from a common ancestor (Richly et al 2002). Three distinct CC-NBS-LRR gene families were identified in the Mla locus within a 240-kb region (Wei et al 1999;Wei et al 2002).…”

“…R genes are usually organized in clusters, and genes within one cluster are mostly derived from a common ancestor (Richly et al 2002). The clustering feature can facilitate the expansion of R gene number and the generation of new R gene specificities through recombination and positive selection (Michelmore and Meyers 1998).…”