Abstract
Heterogeneities in evolutionary pattern among different loci are commonly observed. To see whether the heterogeneity can also be observed among allelic groups in a single locus, we investigated the coding sequence and the flanking regions of Rpp13, a disease resistance gene in up to 60 accession lines from worldwide populations in Arabidopsis thaliana. An extraordinarily high level of polymorphism (π=0.098) and four distinct clades were found in the leucine-rich repeat (LRR) region in this gene. No obvious geographic relationship with the clades was observed, and such clades were not observed in the other regions in and around this gene. The average genetic diversity among the clades ranged from 10 to 14.6% in the LRR. The levels of polymorphism within each clade varied largely, and significant heterogeneity in evolutionary rates among clades was detected. A statistically significant departure from neutrality was also detected by Fu & Li’s tests. These results suggest that both directional and diversifying selection are working on this locus, and that natural selection can cause heterogeneity in evolutionary rate, even among allele groups in a locus.
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Allen RL, Bittner-Eddy P, Grenville-Briggs L, Meitz J, Rehmany AP, Rose LE, Beynon JL (2004) Host–parasite coevolutionary conflict between Arabidopsis and Downy Mildew. Science 306:1957–1960
Bergelson J, Kreitman M, Stahl E, Tian D (2001) Evolutionary dynamics of plant R-genes. Science 292:2281–2285
Bittner-Eddy PD, Crute LR, Holub EB, Beynon JL (2000) RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. Plant J 21:177–188
Botella MA, Parker JE, Frost LN, Bittner-Eddy PD, Beynon JL, Daniels MJ, Holub EB, Jones JD (1998) Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants. Plant Cell 10:1847–1860
Cooley MB, Pathirana S, Wu HJ, Kachroo P, Klessig DF (2000) Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens. Plant Cell 12:663–676
Dodds PN, Lawrence GJ, Ellis JG (2001) Contrasting modes of evolution acting on the complex N locus for rust resistance in flax. Plant J 27:439–453
Ellis JG, Lawrence GJ, Luck JE, Dodds PN (1999) Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 11:495–506
Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296
Gassmann W, Dahlbeck D, Chesnokova O, Minsavage GV, Jones JB, Staskawicz BJ (2000) Molecular evolution of virulence in natural field strains of Xanthomonas campestris pv. vesicatoria. J Bacteriol 182:7053–7059
Hammond-Kosack KE, Jones JD (1997) Plant disease resistance genes. Annu Rev Plant Physiol Plant Mol Biol 48:575–607
Hudson RR, Kaplan NL (1988) The coalescent process in models with selection and recombination. Genetics 120:831–840
Kanazin V, Marek LF, Shoemaker RC (1996) Resistance gene analogs are conserved and clustered in soybean. Proc Natl Acad Sci USA 93:11746–11750
Kreitman M, Rienzo AD (2004) Balancing claims for balancing selection. Trends Genet 20:300–304
Kuang H, Woo SS, Meyers BC, Nevo E, Michelmore RW (2004) Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell 16:2870–2894
McDowell JM, Dhandaydham M, Long TA, Aarts MG, Goff S, Holub EB, Dangl JL (1998) Intragenic recombination and diversifying selection contribute to evolution of Downy Mildew resistance at RPP8 locus of Arabidopsis. Plant Cell 10:1861–1874
Meyers BC, Shen KA, Rohani P, Gaut BS, Michelmore RW (1998) Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell 10:1833–1846
Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS–LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834
Noel L, Moores TL, van der Biezen EA, Parniske M, Daniels MJ, Parker JE, Jones JD (1999) Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell 11:2099–2111
Parniske M, Hammond-Kosack KE, Golstein C, Thomas CM, Jones DA, Harrison K, Wulff BB, Jones JD (1997) Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 91:821–832
Rose LE, Bittner-Eddy PD, Langley CH, Holub EB, Michelmore RW, Beynon JL (2004) Maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana. Genetics 166:1517–1527
Rozas J, Rozas R (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174–175
Stahl EA, Dwyer G, Mauricio R, Kreitman M, Bergelson J (1999) Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 12:667–719
Takahashi H, Miller J, Nozaki Y, Takeda M, Shah J, Hase S, Ikegami M, Ehara Y, Dinesh-Kumar SP, Sukamto (2002) RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. Plant J 35:655–667
Wichmann G, Ritchie D, Kousik CS, Bergelson J (2005) Reduced genetic variation occurs among genes of the highly clonal plant pathogen Xanthomonas axonopodis pv. vesicatoria, including the effector gene avrBs2. Appl Environ Microbiol 71:2418–2432
Zhou T, Wang Y, Chen JQ, Araki H, Jing ZQ, Jiang K, Shen J, Tian D (2004) Genome-wide identification of NBS genes in rice reveals significant expansion of divergent non-TIR NBS Genes. Mol Genet Gen 406:402–415
Acknowledgements
We thank Joy Bergelson for providing DNA of Arabidopsis accessions and allowing D. T. to sequence 22 Arabidopsis accessions and A. lyrata in LRR region in her lab. This study was supported by NSFC (30470924 & 30570987) and by SUR grant from IBM to D. T.
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Ding, J., Cheng, H., Jin, X. et al. Contrasting patterns of evolution between allelic groups at a single locus in Arabidopsis . Genetica 129, 235–242 (2007). https://doi.org/10.1007/s10709-006-0002-9
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DOI: https://doi.org/10.1007/s10709-006-0002-9