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Pervasive Purifying Selection Characterizes the Evolution of I2 Homologs

March 2006 , Volume 19 , Number  3
Pages  288 - 303

Brett C. Couch , Russ Spangler , Christine Ramos , and Georgiana May

Department of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, Minnesota 55108, U.S.A.

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Accepted 17 October 2005.

We sampled 384 sequences related to the Solanum pimpinel-lifolium (=Lycopersicon pimpinellifolium) disease resistance (R) gene I2 from six species, potato, S. demissum, tomato, eggplant, pepper, and tobacco. These species represent increasing phylogenetic distance from potato to tobacco, within the family Solanaceae. Using sequence data from the nucleotide binding site (NBS) region of this gene, we tested models of gene family evolution and inferred patterns of selection acting on the NBS gene region and I2 gene family. We find that the I2 family has diversified within the family Solanaceae for at least 14 million years and evolves through a slow birth-and-death process requiring approximately 12 million years to homogenize gene copies within a species. Analyses of selection resolved a general pattern of strong purifying selection acting on individual codon positions within the NBS and on NBS lineages through time. Surprisingly, we find nine codon positions strongly affected by positive selection and six pairs of codon positions demonstrating correlated amino acid substitutions. Evolutionary analyses serve as bioinformatic tools with which to sort through the vast R gene diversity in plants and find candidates for new resistance specificities or to identify specific amino acid positions important for biochemical function. The slow birth-and-death evolution of I2 genes suggests that some NBS-leucine rich repeat-mediated resistances may not be overcome rapidly by virulence evolution and that the natural diversity of R genes is a potentially valuable source for durable resistance.

Additional keywords: NBS-LRR, bioinformatics.

© 2006 The American Phytopathological Society