Plant Cell Advance Online Publication
Published on June 23, 2006; 10.1105/tpc.106.042614
Received March 22, 2006
Returned for revision May 5, 2006
Accepted May 23, 2006
A Genome-Wide Survey of R Gene Polymorphisms in Arabidopsis
Erica G. Bakker 1, Christopher Toomajian 2, Martin Kreitman 1, and Joy Bergelson 1*
1 Department of Ecology and Evolution, University of Chicago, Chicago, Illinois 60637
2 Department of Molecular and Computational Biology, University of Southern California, Los Angeles, California 90089
* To whom correspondence should be addressed. E-mail: jbergels{at}midway.uchicago.edu.
We used polymorphism analysis to study the evolutionary dynamics of 27 disease resistance (R) genes by resequencing the leucine-rich repeat (LRR) region in 96 Arabidopsis thaliana accessions. We compared single nucleotide polymorphisms (SNPs) in these R genes to an empirical distribution of SNP in the same sample based on 876 fragments selected to sample the entire genome. LRR regions are highly polymorphic for protein variants but not for synonymous changes, suggesting that they generate many alleles maintained for short time periods. Recombination is also relatively common and important for generating protein variants. Although none of the genes is nearly as polymorphic as RPP13, a locus previously shown to have strong signatures of balancing selection, seven genes show weaker indications of balancing selection. Five R genes are relatively invariant, indicating young alleles, but all contain segregating protein variants. Polymorphism analysis in neighboring fragments yielded inconclusive evidence for recent selective sweeps at these loci. In addition, few alleles are candidates for rapid increases in frequency expected under directional selection. Haplotype sharing analysis revealed significant underrepresentation of R gene alleles with extended haplotypes compared with 1102 random genomic fragments. Lack of convincing evidence for directional selection or selective sweeps argues against an arms race driving R gene evolution. Instead, the data support transient or frequency-dependent selection maintaining protein variants at a locus for variable time periods.
This article has been cited by other articles:
|
|
|
|
 
S. Lee, S. Costanzo, Y. Jia, K. M. Olsen, and A. L. Caicedo
Evolutionary Dynamics of the Genomic Region Around the Blast Resistance Gene Pi-ta in AA Genome Oryza Species
Genetics,
December 1, 2009;
183(4):
1315 - 1325.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. M. Flowers, Y. Hanzawa, M. C. Hall, R. C. Moore, and M. D. Purugganan
Population Genomics of the Arabidopsis thaliana Flowering Time Gene Network
Mol. Biol. Evol.,
November 1, 2009;
26(11):
2475 - 2486.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. P. Foxe and S. I. Wright
Signature of Diversifying Selection on Members of the Pentatricopeptide Repeat Protein Family in Arabidopsis lyrata
Genetics,
October 1, 2009;
183(2):
663 - 672.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Sterken, R. Kiekens, E. Coppens, I. Vercauteren, M. Zabeau, D. Inze, J. Flowers, and M. Vuylsteke
A Population Genomics Study of the Arabidopsis Core Cell Cycle Genes Shows the Signature of Natural Selection
PLANT CELL,
October 1, 2009;
21(10):
2987 - 2998.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Zamora, Q. Sun, M. T. Hamblin, C. F. Aquadro, and S. Kresovich
Positively Selected Disease Response Orthologous Gene Sets in the Cereals Identified Using Sorghum bicolor L. Moench Expression Profiles and Comparative Genomics
Mol. Biol. Evol.,
September 1, 2009;
26(9):
2015 - 2030.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. L. McNally, K. L. Childs, R. Bohnert, R. M. Davidson, K. Zhao, V. J. Ulat, G. Zeller, R. M. Clark, D. R. Hoen, T. E. Bureau, et al.
Genomewide SNP variation reveals relationships among landraces and modern varieties of rice
PNAS,
July 28, 2009;
106(30):
12273 - 12278.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Miyake, N. Takebayashi, and D. E. Wolf
Possible Diversifying Selection in the Imprinted Gene, MEDEA, in Arabidopsis
Mol. Biol. Evol.,
April 1, 2009;
26(4):
843 - 857.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. S. Caldwell and R. W. Michelmore
Arabidopsis thaliana Genes Encoding Defense Signaling and Recognition Proteins Exhibit Contrasting Evolutionary Dynamics
Genetics,
February 1, 2009;
181(2):
671 - 684.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Schulenburg, J. Kurtz, Y. Moret, and M. T Siva-Jothy
Introduction. Ecological immunology
Phil Trans R Soc B,
January 12, 2009;
364(1513):
3 - 14.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Freeling, E. Lyons, B. Pedersen, M. Alam, R. Ming, and D. Lisch
Many or most genes in Arabidopsis transposed after the origin of the order Brassicales
Genome Res.,
December 1, 2008;
18(12):
1924 - 1937.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. A. Tennessen and M. S. Blouin
Balancing Selection at a Frog Antimicrobial Peptide Locus: Fluctuating Immune Effector Alleles?
Mol. Biol. Evol.,
December 1, 2008;
25(12):
2669 - 2680.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. A.L. van der Hoorn and S. Kamoun
From Guard to Decoy: A New Model for Perception of Plant Pathogen Effectors
PLANT CELL,
August 1, 2008;
20(8):
2009 - 2017.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C.-L. Huang, S.-Y. Hwang, Y.-C. Chiang, and T.-P. Lin
Molecular Evolution of the Pi-ta Gene Resistant to Rice Blast in Wild Rice (Oryza rufipogon)
Genetics,
July 1, 2008;
179(3):
1527 - 1538.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Zeller, R. M. Clark, K. Schneeberger, A. Bohlen, D. Weigel, and G. Ratsch
Detecting polymorphic regions in Arabidopsis thaliana with resequencing microarrays
Genome Res.,
June 1, 2008;
18(6):
918 - 929.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. G. Bakker, M. B. Traw, C. Toomajian, M. Kreitman, and J. Bergelson
Low Levels of Polymorphism in Genes That Control the Activation of Defense Response in Arabidopsis thaliana
Genetics,
April 1, 2008;
178(4):
2031 - 2043.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Q. Xu, X. Wen, and X. Deng
Genomic Organization, Rapid Evolution and Meiotic Instability of Nucleotide-Binding-Site-Encoding Genes in a New Fruit Crop, "Chestnut Rose"
Genetics,
April 1, 2008;
178(4):
2081 - 2091.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
M. C. Rentel, L. Leonelli, D. Dahlbeck, B. Zhao, and B. J. Staskawicz
Recognition of the Hyaloperonospora parasitica effector ATR13 triggers resistance against oomycete, bacterial, and viral pathogens
PNAS,
January 22, 2008;
105(3):
1091 - 1096.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Araki, H. Innan, M. Kreitman, and J. Bergelson
Molecular Evolution of Pathogenicity-Island Genes in Pseudomonas viridiflava
Genetics,
October 1, 2007;
177(2):
1031 - 1041.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
R. M. Clark, G. Schweikert, C. Toomajian, S. Ossowski, G. Zeller, P. Shinn, N. Warthmann, T. T. Hu, G. Fu, D. A. Hinds, et al.
Common Sequence Polymorphisms Shaping Genetic Diversity in Arabidopsis thaliana
Science,
July 20, 2007;
317(5836):
338 - 342.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
C. Shindo, G. Bernasconi, and C. S. Hardtke
Natural Genetic Variation in Arabidopsis: Tools, Traits and Prospects for Evolutionary Ecology
Ann. Bot.,
June 1, 2007;
99(6):
1043 - 1054.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W. E. Durrant, S. Wang, and X. Dong
Arabidopsis SNI1 and RAD51D regulate both gene transcription and DNA recombination during the defense response
PNAS,
March 6, 2007;
104(10):
4223 - 4227.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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]
|
|
|
|
|
