Molecular Genetics and Genomics

, Volume 280, Issue 3, pp 187–198 | Cite as

Recent duplications dominate NBS-encoding gene expansion in two woody species

  • Sihai Yang
  • Xiaohui Zhang
  • Jia-Xing Yue
  • Dacheng TianEmail author
  • Jian-Qun ChenEmail author
Original Paper


Most disease resistance genes in plants encode NBS-LRR proteins. However, in woody species, little is known about the evolutionary history of these genes. Here, we identified 459 and 330 respective NBS-LRRs in grapevine and poplar genomes. We subsequently investigated protein motif composition, phylogenetic relationships and physical locations. We found significant excesses of recent duplications in perennial species, compared with those of annuals, represented by rice and Arabidopsis. Consequently, we observed higher nucleotide identity among paralogs and a higher percentage of NBS-encoding genes positioned in numerous clusters in the grapevine and poplar. These results suggested that recent tandem duplication played a major role in NBS-encoding gene expansion in perennial species. These duplication events, together with a higher probability of recombination revealed in this study, could compensate for the longer generation time in woody perennial species e.g. duplication and recombination could serve to generate novel resistance specificities. In addition, we observed extensive species-specific expansion in TIR-NBS-encoding genes. Non-TIR-NBS-encoding genes were poly- or paraphyletic, i.e. genes from three or more plant species were nested in different clades, suggesting different evolutionary patterns between these two gene types.


NBS-LRR genes Disease resistance genes Evolution Grapevine Poplar 



This work was supported by the National Natural Science Foundation of China (30570987 and 30470122), Pre-program for NBRPC (2005CCA02100) and 111 project to D. T., or J-Q. C.

Supplementary material

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  1. Ameline-Torregrosa C, Wang BB, O’Bleness MS, Deshpande S, Zhu H, Roe B, Young ND, Cannon SB (2008) Identification and characterization of NBS-LRR genes in the model plant medicago truncatula. Plant Physiol 146:5–21PubMedCrossRefGoogle Scholar
  2. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefGoogle Scholar
  3. Bai J, Pennill LA, Ning J, Lee SW, Ramalingam J, Webb CA, Zhao B, Sun Q, Nelson JC, Leach JE, Hulbert SH (2002) Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res 12:1871–1884PubMedCrossRefGoogle Scholar
  4. Bailey TL, Elkan C (2005) The value of prior knowledge in discovering motifs with MEME. Proc Int Conf Intell Syst Mol Biol 3:21–29Google Scholar
  5. Bent AF, Mackey D (2007) Elicitors, effectors, and R-genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol 45:399–436PubMedCrossRefGoogle Scholar
  6. Cannon SB, Zhu H, Baumgarten AM, Spangler R, May G, Cook DR, Young ND (2002) Diversity, distribution, and ancient taxonomic relationships within the TIR and non-TIR NBS-LRR resistance gene subfamilies. J Mol Evol 54:548–562PubMedCrossRefGoogle Scholar
  7. Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833PubMedCrossRefGoogle Scholar
  8. Ding J, Araki H, Wang Q, Zhang P, Yang S, Chen JQ, Tian D (2007a) Highly asymmetric rice genomes. BMC Genomics 8:154PubMedCrossRefGoogle Scholar
  9. Ding J, Zhang W, Jing Z, Chen JQ, Tian D (2007b) Unique pattern of R-gene variation within populations in Arabidopsis. Mol Genet Genomics 277:619–629PubMedCrossRefGoogle Scholar
  10. Holub EB (2001) The arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Genet 2:516–527PubMedCrossRefGoogle Scholar
  11. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800CrossRefGoogle Scholar
  12. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467PubMedCrossRefGoogle Scholar
  13. Jiang H, Wang C, Ping L, Tian D, Yang S (2007) Pattern of LRR nucleotide variation in plant resistance genes. Plant Sci 173:253–261CrossRefGoogle Scholar
  14. Leister D (2004) Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance genes. Trends Genet 20:116–122PubMedCrossRefGoogle Scholar
  15. Lupas A, Van Dyke M, Stock J (1991) Predicting coiled coils from protein sequences. Science 252:1162–1164CrossRefGoogle Scholar
  16. Lynch M, Crease TJ (1990) The analysis of population survey data on DNA sequence variation. Mol Biol Evol 7:377–394PubMedGoogle Scholar
  17. McHale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212PubMedCrossRefGoogle Scholar
  18. Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, Young ND (1999) Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J 20:317–332PubMedCrossRefGoogle Scholar
  19. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834PubMedCrossRefGoogle Scholar
  20. Meyers BC, Morgante M, Michelmore RW (2002) TIR-X and TIR-NBS proteins: two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes. Plant J 32:77–92PubMedCrossRefGoogle Scholar
  21. Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8:1113–1130PubMedGoogle Scholar
  22. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426PubMedGoogle Scholar
  23. Nobuta K, Ashfield T, Kim S, Innes RW (2005) Diversification of non-TIR class NB-LRR genes in relation to whole-genome duplication events in Arabidopsis. Mol Plant Microbe Interact 18:103–109PubMedCrossRefGoogle Scholar
  24. 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 91:821–832PubMedCrossRefGoogle Scholar
  25. Rice Chromosomes 11 and 12 Sequencing Consortia (2005) The sequence of rice chromosomes 11 and 12, rich in disease resistance genes and recent gene duplications. BMC Biol 3:20CrossRefGoogle Scholar
  26. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  27. Shen J, Araki H, Chen L, Chen JQ, Tian D (2006) Unique evolutionary mechanism in R-genes under the presence/absence polymorphism in Arabidopsis thaliana. Genetics 172:1243–1250PubMedCrossRefGoogle Scholar
  28. Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, Li WH (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220–1234PubMedCrossRefGoogle Scholar
  29. Xiao S, Ellwood S, Calis O, Patrick E, Li T et al (2001) Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 291:118–120PubMedCrossRefGoogle Scholar
  30. Xiao S, Emerson B, Ratanasut K, Patrick E, O’Neill C et al (2004) Origin and maintenance of a broad-spectrum disease resistance locus in Arabidopsis. Mol Biol Evol 21:1661–1672PubMedCrossRefGoogle Scholar
  31. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  32. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  33. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I et al (2006) The genome of black cottonwood, Populus trichocarpa (torr. & gray). Science 313:1596–1604PubMedCrossRefGoogle Scholar
  34. van Ooijen G, van den Burg HA, Cornelissen BJ, Takken FL (2007) Structure and function of resistance proteins in solanaceous plants. Annu Rev Phytopathol 45:43–72PubMedCrossRefGoogle Scholar
  35. Yang S, Feng Z, Zhang X, Jiang K, Jin X, Hang Y, Chen JQ, Tian D (2006) Genome-wide investigation on the genetic variations of rice disease resistance genes. Plant Mol Biol 62:181–193PubMedCrossRefGoogle Scholar
  36. Yang S, Jiang K, Araki H, Ding J, Yang YH, Tian D (2007) A molecular isolation mechanism associated with high intra-specific diversity in rice. Gene 394:87–95PubMedCrossRefGoogle Scholar
  37. Yu J, Wang J, Lin W, Li S, Li H et al (2005) The Genomes of Oryza sativa: a history of duplications. PLoS Biol 3:e38PubMedCrossRefGoogle Scholar
  38. Zhang P, Gu Z, Li WH (2003) Different evolutionary patterns between young duplicate genes in the human genome. Genome Biol 4:R56PubMedCrossRefGoogle Scholar
  39. Zhou T, Wang Y, Chen JQ, Araki H, Jing Z, 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 Genomics 271:402–415PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.State Key Laboratory of Pharmaceutical Biotechnology, Department of BiologyNanjing UniversityNanjingChina

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