Genome-Level Evolution of Resistance Genes in Arabidopsis thaliana

Corresponding author: Andrew Baumgarten, Evolution and Behavior, 100 Ecology, 1987 Upper Buford Circle, University of Minnesota, St. Paul, MN 55108., baum0217{at}tc.umn.edu (E-mail)

Communicating editor: J. B. WALSH

Pathogen resistance genes represent some of the most abundant and diverse gene families found within plant genomes. However, evolutionary mechanisms generating resistance gene diversity at the genome level are not well understood. We used the complete Arabidopsis thaliana genome sequence to show that most duplication of individual NBS-LRR sequences occurs at close physical proximity to the parent sequence and generates clusters of closely related NBS-LRR sequences. Deploying the statistical strength of phylogeographic approaches and using chromosomal location as a proxy for spatial location, we show that apparent duplication of NBS-LRR genes to ectopic chromosomal locations is largely the consequence of segmental chromosome duplication and rearrangement, rather than the independent duplication of individual sequences. Although accounting for a smaller fraction of NBS-LRR gene duplications, segmental chromosome duplication and rearrangement events have a large impact on the evolution of this multigene family. Intergenic exchange is dramatically lower between NBS-LRR sequences located in different chromosome regions as compared to exchange between sequences within the same chromosome region. Consequently, once translocated to new chromosome locations, NBS-LRR gene copies have a greater likelihood of escaping intergenic exchange and adopting new functions than do gene copies located within the same chromosomal region. We propose an evolutionary model that relates processes of genome evolution to mechanisms of evolution for the large, diverse, NBS-LRR gene family.

This article has been cited by other articles:

				C. Ameline-Torregrosa, B.-B. Wang, M. S. O'Bleness, S. Deshpande, H. Zhu, B. Roe, N. D. Young, and S. B. Cannon Identification and Characterization of Nucleotide-Binding Site-Leucine-Rich Repeat Genes in the Model Plant Medicago truncatula Plant Physiology, January 1, 2008; 146(1): 5 - 21. [Abstract] [Full Text] [PDF]

				N. A. Eckardt Positive and Negative Feedback Coordinate Regulation of Disease Resistance Gene Expression PLANT CELL, September 1, 2007; 19(9): 2700 - 2702. [Full Text] [PDF]

				H. Yi and E. J. Richards A Cluster of Disease Resistance Genes in Arabidopsis Is Coordinately Regulated by Transcriptional Activation and RNA Silencing PLANT CELL, September 1, 2007; 19(9): 2929 - 2939. [Abstract] [Full Text] [PDF]

				E. R. Valdivia, J. Sampedro, J. C. Lamb, S. Chopra, and D. J. Cosgrove Recent Proliferation and Translocation of Pollen Group 1 Allergen Genes in the Maize Genome Plant Physiology, March 1, 2007; 143(3): 1269 - 1281. [Abstract] [Full Text] [PDF]

				J. Hagenblad, J. Bechsgaard, and D. Charlesworth Linkage Disequilibrium Between Incompatibility Locus Region Genes in the Plant Arabidopsis lyrata Genetics, June 1, 2006; 173(2): 1057 - 1073. [Abstract] [Full Text] [PDF]

				C. E. Vallejos, G. Astua-Monge, V. Jones, T. R. Plyler, N. S. Sakiyama, and S. A. Mackenzie Genetic and Molecular Characterization of the I Locus of Phaseolus vulgaris Genetics, February 1, 2006; 172(2): 1229 - 1242. [Abstract] [Full Text] [PDF]

				M. Mondragon-Palomino and B. S. Gaut Gene Conversion and the Evolution of Three Leucine-Rich Repeat Gene Families in Arabidopsis thaliana Mol. Biol. Evol., December 1, 2005; 22(12): 2444 - 2456. [Abstract] [Full Text] [PDF]

				K. A.T. Silverstein, M. A. Graham, T. D. Paape, and K. A. VandenBosch Genome Organization of More Than 300 Defensin-Like Genes in Arabidopsis Plant Physiology, June 1, 2005; 138(2): 600 - 610. [Abstract] [Full Text] [PDF]

				S. Xiao, B. Emerson, K. Ratanasut, E. Patrick, C. O'Neill, I. Bancroft, and J. G. Turner Origin and Maintenance of a Broad-Spectrum Disease Resistance Locus in Arabidopsis Mol. Biol. Evol., September 1, 2004; 21(9): 1661 - 1672. [Abstract] [Full Text] [PDF]

				R. D'Ovidio, A. Raiola, C. Capodicasa, A. Devoto, D. Pontiggia, S. Roberti, R. Galletti, E. Conti, D. O'Sullivan, and G. De Lorenzo Characterization of the Complex Locus of Bean Encoding Polygalacturonase-Inhibiting Proteins Reveals Subfunctionalization for Defense against Fungi and Insects Plant Physiology, August 1, 2004; 135(4): 2424 - 2435. [Abstract] [Full Text] [PDF]

				M. A. Graham, K. A.T. Silverstein, S. B. Cannon, and K. A. VandenBosch Computational Identification and Characterization of Novel Genes from Legumes Plant Physiology, July 1, 2004; 135(3): 1179 - 1197. [Abstract] [Full Text] [PDF]