Genetics, Vol. 163, 735-746, February 2003, Copyright © 2003

Natural Selection for Polymorphism in the Disease Resistance Gene Rps2 of Arabidopsis thaliana

Rodney Mauricioa,b, Eli A. Stahla,c, Tonia Korvesa, Dacheng Tiana, Martin Kreitmana,c, and Joy Bergelsona,c
a Department of Ecology and Evolution, University of Chicago, Chicago, Illinois 60637,
b Department of Genetics, University of Georgia, Athens, Georgia 30602-7223
c Committee on Genetics, University of Chicago, Chicago, Illinois 60637

Corresponding author: Joy Bergelson, 1101 E. 57th St., Chicago, IL 60637., jbergels{at}midway.uchicago.edu (E-mail)

Communicating editor: M. AGUADÉ

Pathogen resistance is an ecologically important phenotype increasingly well understood at the molecular genetic level. In this article, we examine levels of avrRpt2-dependent resistance and Rps2 locus DNA sequence variability in a worldwide sample of 27 accessions of Arabidopsis thaliana. The rooted parsimony tree of Rps2 sequences drawn from a diverse set of ecotypes includes a deep bifurcation separating major resistance and susceptibility clades of alleles. We find evidence for selection maintaining these alleles and identify the N-terminal part of the leucine-rich repeat region as a probable target of selection. Additional protein variants are found within the two major clades and correlate well with measurable differences among ecotypes in resistance to the avirulence gene avrRpt2 of the pathogen Pseudomonas syringae. Long-lived polymorphisms have been observed for other resistance genes of A. thaliana; the Rps2 data suggest that the long-term maintenance of phenotypic variation in resistance genes may be a general phenomenon and are consistent with diversifying selection acting in concert with selection to maintain variation.





This article has been cited by other articles:


Home page
GeneticsHome page
I. Ashikawa, N. Hayashi, H. Yamane, H. Kanamori, J. Wu, T. Matsumoto, K. Ono, and M. Yano
Two Adjacent Nucleotide-Binding Site-Leucine-Rich Repeat Class Genes Are Required to Confer Pikm-Specific Rice Blast Resistance
Genetics, December 1, 2008; 180(4): 2267 - 2276.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Bot.Home page
A. L. Caicedo
Geographic diversity cline of R gene homologs in wild populations of Solanum pimpinellifolium (Solanaceae)
Am. J. Botany, March 1, 2008; 95(3): 393 - 398.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
H. Kuang, H. J. van Eck, D. Sicard, R. Michelmore, and E. Nevo
Evolution and Genetic Population Structure of Prickly Lettuce (Lactuca serriola) and Its RGC2 Resistance Gene Cluster
Genetics, March 1, 2008; 178(3): 1547 - 1558.
[Abstract] [Full Text] [PDF]


Home page
Plant CellHome page
R. M.P. Van Poecke, M. Sato, L. Lenarz-Wyatt, S. Weisberg, and F. Katagiri
Natural Variation in RPS2-Mediated Resistance among Arabidopsis Accessions: Correlation between Gene Expression Profiles and Phenotypic Responses
PLANT CELL, December 1, 2007; 19(12): 4046 - 4060.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
U. Orgil, H. Araki, S. Tangchaiburana, R. Berkey, and S. Xiao
Intraspecific Genetic Variations, Fitness Cost and Benefit of RPW8, A Disease Resistance Locus in Arabidopsis thaliana
Genetics, August 1, 2007; 176(4): 2317 - 2333.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
J. O. Borevitz, S. P. Hazen, T. P. Michael, G. P. Morris, I. R. Baxter, T. T. Hu, H. Chen, J. D. Werner, M. Nordborg, D. E. Salt, et al.
Genome-wide patterns of single-feature polymorphism in Arabidopsis thaliana
PNAS, July 17, 2007; 104(29): 12057 - 12062.
[Abstract] [Full Text] [PDF]


Home page
Nucleic Acids ResHome page
A. Boyko, P. Kathiria, F. J. Zemp, Y. Yao, I. Pogribny, and I. Kovalchuk
Transgenerational changes in the genome stability and methylation in pathogen-infected plants: (Virus-induced plant genome instability)
Nucleic Acids Res., March 12, 2007; 35(5): 1714 - 1725.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
L. E. Rose, R. W. Michelmore, and C. H. Langley
Natural Variation in the Pto Disease Resistance Gene Within Species of Wild Tomato (Lycopersicon). II. Population Genetics of Pto
Genetics, March 1, 2007; 175(3): 1307 - 1319.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
D. S. Guttman, S. J. Gropp, R. L. Morgan, and P. W. Wang
Diversifying Selection Drives the Evolution of the Type III Secretion System Pilus of Pseudomonas syringae
Mol. Biol. Evol., December 1, 2006; 23(12): 2342 - 2354.
[Abstract] [Full Text] [PDF]


Home page
Plant CellHome page
E. G. Bakker, C. Toomajian, M. Kreitman, and J. Bergelson
A Genome-Wide Survey of R Gene Polymorphisms in Arabidopsis
PLANT CELL, August 1, 2006; 18(8): 1803 - 1818.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Bot.Home page
I. M. Ehrenreich and M. D. Purugganan
The molecular genetic basis of plant adaptation
Am. J. Botany, July 1, 2006; 93(7): 953 - 962.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
P. N. Dodds, G. J. Lawrence, A.-M. Catanzariti, T. Teh, C.-I. A. Wang, M. A. Ayliffe, B. Kobe, and J. G. Ellis
From the Cover: Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes
PNAS, June 6, 2006; 103(23): 8888 - 8893.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
D. J. Kliebenstein, M. A. L. West, H. van Leeuwen, K. Kim, R. W. Doerge, R. W. Michelmore, and D. A. St. Clair
Genomic Survey of Gene Expression Diversity in Arabidopsis thaliana
Genetics, February 1, 2006; 172(2): 1179 - 1189.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
J. Shen, H. Araki, L. Chen, J.-Q. Chen, and D. Tian
Unique Evolutionary Mechanism in R-Genes Under the Presence/Absence Polymorphism in Arabidopsis thaliana
Genetics, February 1, 2006; 172(2): 1243 - 1250.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
D. A. Moeller and P. Tiffin
Genetic Diversity and the Evolutionary History of Plant Immunity Genes in Two Species of Zea
Mol. Biol. Evol., December 1, 2005; 22(12): 2480 - 2490.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
L. E. Rose, C. H. Langley, A. J. Bernal, and R. W. Michelmore
Natural Variation in the Pto Pathogen Resistance Gene Within Species of Wild Tomato (Lycopersicon). I. Functional Analysis of Pto Alleles
Genetics, September 1, 2005; 171(1): 345 - 357.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
J. M. Cork and M. D. Purugganan
High-Diversity Genes in the Arabidopsis Genome
Genetics, August 1, 2005; 170(4): 1897 - 1911.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
A. Takahashi and T. Takano-Shimizu
A High-Frequency Null Mutant of an Odorant-Binding Protein Gene, Obp57e, in Drosophila melanogaster
Genetics, June 1, 2005; 170(2): 709 - 718.
[Abstract] [Full Text] [PDF]


Home page
Appl. Environ. Microbiol.Home page
G. Wichmann, D. Ritchie, C. S. Kousik, and J. Bergelson
Reduced Genetic Variation Occurs among Genes of the Highly Clonal Plant Pathogen Xanthomonas axonopodis pv. vesicatoria, Including the Effector Gene avrBs2
Appl. Envir. Microbiol., May 1, 2005; 71(5): 2418 - 2432.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
K. J. Schmid, S. Ramos-Onsins, H. Ringys-Beckstein, B. Weisshaar, and T. Mitchell-Olds
A Multilocus Sequence Survey in Arabidopsis thaliana Reveals a Genome-Wide Departure From a Neutral Model of DNA Sequence Polymorphism
Genetics, March 1, 2005; 169(3): 1601 - 1615.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
S. I. Wright and B. S. Gaut
Molecular Population Genetics and the Search for Adaptive Evolution in Plants
Mol. Biol. Evol., March 1, 2005; 22(3): 506 - 519.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
J. G. Bishop, D. R. Ripoll, S. Bashir, C. M. B. Damasceno, J. D. Seeds, and J. K. C. Rose
Selection on Glycine {beta}-1,3-Endoglucanase Genes Differentially Inhibited by a Phytophthora Glucanase Inhibitor Protein
Genetics, February 1, 2005; 169(2): 1009 - 1019.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
E. M. Goss, M. Kreitman, and J. Bergelson
Genetic Diversity, Recombination and Cryptic Clades in Pseudomonas viridiflava Infecting Natural Populations of Arabidopsis thaliana
Genetics, January 1, 2005; 169(1): 21 - 35.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
A. L. Caicedo and B. A. Schaal
Heterogeneous evolutionary processes affect R gene diversity in natural populations of Solanum pimpinellifolium
PNAS, December 14, 2004; 101(50): 17444 - 17449.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
P. Tiffin, R. Hacker, and B. S. Gaut
Population Genetic Evidence for Rapid Changes in Intraspecific Diversity and Allelic Cycling of a Specialist Defense Gene in Zea
Genetics, September 1, 2004; 168(1): 425 - 434.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
P. Tiffin
Comparative Evolutionary Histories of Chitinase Genes in the Genus Zea and Family Poaceae
Genetics, July 1, 2004; 167(3): 1331 - 1340.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
M. J. Clauss and T. Mitchell-Olds
Functional Divergence in Tandemly Duplicated Arabidopsis thaliana Trypsin Inhibitor Genes
Genetics, March 1, 2004; 166(3): 1419 - 1436.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
L. E. Rose, P. D. Bittner-Eddy, C. H. Langley, E. B. Holub, R. W. Michelmore, and J. L. Beynon
The Maintenance of Extreme Amino Acid Diversity at the Disease Resistance Gene, RPP13, in Arabidopsis thaliana
Genetics, March 1, 2004; 166(3): 1517 - 1527.
[Abstract] [Full Text] [PDF]