Originally published as Genetics Published Articles Ahead of Print on May 27, 2009.

Genetics, Vol. 182, 1351-1364, August 2009, Copyright © 2009
doi:10.1534/genetics.109.101022

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

* Department of Plant Breeding and Genetics, Cornell University, Ithaca, New York 14853, {dagger} Boyce Thompson Institute for Plant Research, Ithaca, New York 14853, {ddagger} Department of Plant Sciences, Seoul National University, Seoul 151-921, Korea, § Department of Plant Pathology, University of Minnesota, St. Paul, Minnesota 55108 and ** College of Agriculture and Life Sciences, University of Wisconsin, Madison, Wisconsin 53706

3 Corresponding author: College of Agricultural and Life Sciences, University of Wisconsin, 140 Agricultural Hall, Madison, WI 53706.
E-mail: mjahn{at}cals.wisc.edu

Comparative genomics provides a powerful tool for the identification of genes that encode traits shared between crop plants and model organisms. Pathogen resistance conferred by plant R genes of the nucleotide-binding–leucine-rich-repeat (NB–LRR) class is one such trait with great agricultural importance that occupies a critical position in understanding fundamental processes of pathogen detection and coevolution. The proposed rapid rearrangement of R genes in genome evolution would make comparative approaches tenuous. Here, we test the hypothesis that orthology is predictive of R-gene genomic location in the Solanaceae using the pepper R gene Bs2. Homologs of Bs2 were compared in terms of sequence and gene and protein architecture. Comparative mapping demonstrated that Bs2 shared macrosynteny with R genes that best fit criteria determined to be its orthologs. Analysis of the genomic sequence encompassing solanaceous R genes revealed the magnitude of transposon insertions and local duplications that resulted in the expansion of the Bs2 intron to 27 kb and the frequently detected duplications of the 5'-end of R genes. However, these duplications did not impact protein expression or function in transient assays. Taken together, our results support a conservation of synteny for NB–LRR genes and further show that their distribution in the genome has been consistent with global rearrangements.