Evolutionary Dynamics of Plant R-Genes
Abstract
Plant R-genes involved in gene-for-gene interactions with pathogens are expected to undergo coevolutionary arms races in which plant specificity and pathogen virulence continually adapt in response to each other. Lending support to this idea, the solvent-exposed amino acid residues of leucine-rich repeats, a region of R-genes involved in recognizing pathogens, often evolve at unusually fast rates. But within-species polymorphism is also common in R-genes, implying that the adaptive substitution process is not simply one of successive selective sweeps. Here we document these features in available data and discuss them in light of the evolutionary dynamics they likely reflect.
Get full access to this article
View all available purchase options and get full access to this article.
REFERENCES AND NOTES
1
Lawlor D. A., Ward F. E., Ennis P. D., Jackson A. P., Parham P., Nature 335, 268 (1988).
2
W. E. Mayer et al., EMBO J.7, 2765 (1988).
3
Stahl E. A., Dwyer G., Mauricio R., Kreitman M., Bergelson J., Nature 400, 667 (1999).
4
Clark A. G., Wang L., Genetics 147, 713 (1997).
5
Young N. D., Curr. Opin. Plant Biol. 3, 285 (2000).
6
Van Valen L., Evol. Theory 1, 1 (1971).
7
Clay K., Kover P. X., Annu. Rev. Phytopathol. 34, 29 (1996).
8
M. Parniske et al., Cell91, 821 (1997).
9
M. A. Botella et al., Plant Cell 10, 1847 (1998).
10
J. M. McDowell et al., Plant Cell 10, 1861 (1998).
11
Meyers B. C., Shen K. A., Rohani R., Gaut B. S., Michelmore R. W., Plant Cell 10, 1833 (1998).
12
L. Noel et al., Plant Cell11, 2099 (1999).
13
Flor H. H., Adv. Genet. 8, 29 (1956).
14
Hughes A. L., Nei M., Nature 335, 167 (1988).
15
___, Proc. Natl. Acad. Sci. U.S.A. 86, 958 (1989).
16
Ellis J., Dodds P., Pryor T., Curr. Opin. Plant Biol. 3, 278 (2000).
17
Jones D. A., Jones J. D. G., Adv. Bot. Res. Adv. Plant Pathol. 24, 89 (1997).
18
Leister R. T., Katagiri F., Plant J. 22, 345 (2000).
19
Bittner-Eddy P. D., Crute I. R., Holub E. B., Beynon J. L., Plant J. 21, 177 (2000).
20
Ellis J. G., Lawrence G. J., Luck J. E., Dodds P. N., Plant Cell 11, 495 (1999).
21
Luck J. E., Lawrence G. J., Dodds P. N., Shepherd K. W., Ellis J. G., Plant Cell 12, 1367 (2000).
22
Banerjee D., Zhang X., Bent A. F., Genetics 158, 439 (2001).
23
G. L. Wang et al., Plant Cell10, 765 (1998).
24
Sudupak M. A., Bennetzen J. L., Hulbert S. H., Genetics 133, 119 (1993).
25
Hulbert S. H., Annu. Rev. Phytopathol. 35, 293 (1997).
26
Stahl E. A., Bishop J. G., Curr. Opin. Plant Biol. 3, 299 (2000).
27
The Arabidopsis Genome Initiative, Nature408, 796 (2000).
28
We analyzed the 182 A. thaliana NBS-containing R-gene homologs in the NIBLRRS database and defined clusters of evolutionarily related R-genes on the basis of position and local DNA sequence similarity (fasta expectation < 0.1). Cluster sizes (frequencies) are 2 (13), 3 (6), 4 (4), 5 (1), 6 (1), 7 (2), 8 (2), 9 (1), 11 (1), and 12 (1). Of these complex clusters, 20 had at least 50% nucleotide similarity and were thus sufficiently related for statistically reliable DNA sequence analysis. Four sets of single R-genes also met the criterion of 50% nucleotide similarity and were more closely related to each other than to any clusteredR-genes. HMMer Pfam analyses defined LRR regions and LRR domains (see Table 2) in 15 of the complex R-loci and 2 of the single R-gene sets. Supplemental information is available at Science Online (38).
29
Michelmore R. W., Meyers B. C., Genome Res. 8, 1113 (1998).
30
Hudson R. R., Kaplan N. L., Genetics 120, 831 (1988).
31
Caicedo A. L., Schaal B. A., Kunkel B. N., Proc. Natl. Acad. Sci. U.S.A. 96, 302 (1999).
32
M. R. Grant et al., Proc. Natl. Acad. Sci. U.S.A. 95, 15843 (1998).
33
Unpublished data of authors (39), comparing about 2 kb of flanking sequence in 23 A. thaliana accessions.
34
To calculate changes in codons with more than one position substituted, current algorithms for calculat ing Ks and Ka assume equal rates of synonymous and replacement changes. This assumption leads to the overestimation of synonymous changes and underestimation of replacement changes when the replacement rate actually exceeds the synonymous rate (J. Comeron, M. Kreitman, unpublished results).
35
W.-H. Li, Molecular Evolution (Sinauer Associates, Sunderland, MA, 1997).
36
Abbott R. J., Gomes M. F., Heredity 62, 411 (1989).
37
May R. M., Anderson R. M., Proc. R. Soc. London B 219, 281 (1983).
38
Supplemental material is available on Science Online at www.sciencemag.org/cgi/content/full/292/5525/2281/DC1.
39
J. Bergelson, M. Kreitman, E. A. Stahl, D. Tian, unpublished data.
40
R. Mauricio, unpublished data.
41
We gratefully acknowledge support from the NIH to J.B. and M.K., a Packard Fellowship to J.B., and a Sloan/Department of Energy fellowship to E.A.S. K. Thornton provided computer programs.
42
{newshr}Review
(0)eLetters
eLetters is a forum for ongoing peer review. eLetters are not edited, proofread, or indexed, but they are screened. eLetters should provide substantive and scholarly commentary on the article. Embedded figures cannot be submitted, and we discourage the use of figures within eLetters in general. If a figure is essential, please include a link to the figure within the text of the eLetter. Please read our Terms of Service before submitting an eLetter.
Log In to Submit a ResponseNo eLetters have been published for this article yet.
Information & Authors
Information
Published In
Science
Volume 292 | Issue 5525
22 June 2001
22 June 2001
Submission history
Published in print: 22 June 2001
Authors
Metrics & Citations
Metrics
Article Usage
Altmetrics
Citations
Cite as
- Joy Bergelson et al.
Export citation
Select the format you want to export the citation of this publication.
Cited by
- Real-Time Evolution of New Genes by Innovation, Amplification, and Divergence, Science, 338, 6105, (384-387), (2021)./doi/10.1126/science.1226521
- Natural Enemies Drive Geographic Variation in Plant Defenses, Science, 338, 6103, (116-119), (2021)./doi/10.1126/science.1226397
- Genetic Loci Affecting Resistance to Human Malaria Parasites in a West African Mosquito Vector Population, Science, 298, 5591, (213-216), (2021)./doi/10.1126/science.1073420
Loading...
View Options
Check Access
Log in to view the full text
AAAS login provides access to Science for AAAS Members, and access to other journals in the Science family to users who have purchased individual subscriptions.
- Become a AAAS Member
- Activate your AAAS ID
- Purchase Access to Other Journals in the Science Family
- Account Help
Log in via OpenAthens.
Log in via Shibboleth.
More options
Purchase digital access to this article
Download and print this article for your personal scholarly, research, and educational use.
Buy a single issue of Science for just $15 USD.