, Volume 146, Issue 6, pp 517–528 | Cite as

Genetic signatures of plant resistance genes with known function within and between species

  • Dan Wang
  • Yan ShaEmail author
  • Junfeng Hu
  • Ting Yang
  • Xue Piao
  • Xiaohui Zhang
Original Paper


Plant disease resistance (R) genes have undergone significant evolutionary divergence to cope with rapid changes in pathogens. These highly variable evolutionary patterns may have contributed to diversity in R gene protein families or structures. Here, the evolutionary patterns of 76 identified R genes and their homologs were investigated within and between plant species. Results demonstrated that nucleotide binding sites and leucine-rich-repeat genes located in loci with complex evolutionary histories tended to evolve rapidly, have high variation in copy numbers, exhibit high levels of nucleotide variation and frequent gene conversion events, and also exhibit high non-synonymous to synonymous substitution ratios in LRR regions. However, non-NBS-LRR R genes are relatively well conserved with constrained variation and are more likely to participate in the basic defense system of hosts. In addition, both conserved and highly divergent evolutionary patterns were observed for the same R genes and were consistent with inter- and intra-specific distributions of some R genes. These results thus indicate either continuous or altered evolutionary patterns between and within species. The present investigation is the first attempt to investigate evolutionary patterns among all clearly functional R genes. The results reported here thus provide a foundation for future plant disease studies.


Disease resistance gene Plants Genetic variation 



This work was funded by Jiangsu Planned Projects for Postdoctoral Research Funds (1601080C), the Jiangsu University Natural Science Foundation Funded Project (17KJB310015), and the Research Foundation for Talented Scholars at Xuzhou Medical University (D2015001, D2017020).

Compliance with ethical standards

Conflict of interest

All authors declare that they no conflict of interest.

Supplementary material

10709_2018_44_MOESM1_ESM.rar (464 kb)
Supplementary material 1 (RAR 464 KB)


  1. And HK, Jones JDG (2003) Plant disease resistance genes. Annurevplant Physiolplant Molbiol 48:575Google Scholar
  2. Bittnereddy PD, Crute IR, 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 21:177CrossRefGoogle Scholar
  3. Cao J, Schneeberger K, Ossowski S, Günther T, Bender S, Fitz J et al (2011) Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet 43:956–963CrossRefGoogle Scholar
  4. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant. Immune Response Cell 124:803–814PubMedGoogle Scholar
  5. Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833CrossRefGoogle Scholar
  6. Ding J, Araki H, Wang Q, Zhang P, Yang S, Chen JQ, Tian D (2007a) Highly asymmetric rice genomes. BMC Genomics 8:154CrossRefGoogle Scholar
  7. Ding J, Cheng H, Jin X, Araki H, Yang Y, Tian D (2007b) Contrasting patterns of evolution between allelic groups at a single locus in Arabidopsis. Genetica 129:235–242CrossRefGoogle Scholar
  8. Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011CrossRefGoogle Scholar
  9. Hulbert SH, Webb CA, And SMS, Sun Q (2003) Resistance gene complexes: evolution and utilization. Ann Rev Phytopathol 39:285CrossRefGoogle Scholar
  10. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329CrossRefGoogle Scholar
  11. Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ (1994) Isolation of the tomato Cf-9 Gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789–793CrossRefGoogle Scholar
  12. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K et al (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci USA 103:11086–11091CrossRefGoogle Scholar
  13. 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 16:2870CrossRefGoogle Scholar
  14. Kuang H, Caldwell KS, Meyers BC, Michelmore RW (2008) Frequent sequence exchanges between homologs of RPP8 in Arabidopsis are not necessarily associated with genomic proximity. Plant J 54:69–80CrossRefGoogle Scholar
  15. Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16:3496–3507CrossRefGoogle Scholar
  16. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of. DNA polymorphism data. Bioinformatics 25:1451CrossRefGoogle Scholar
  17. Liu J, Liu X, Dai L, Wang G (2007) Recent progress in elucidating the structure, function and evolution of disease resistance genes in plants. J Genet Genom 34:765–776CrossRefGoogle Scholar
  18. Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Ann Rev Plant Biol 54:23CrossRefGoogle 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 15:809–834CrossRefGoogle Scholar
  20. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418PubMedGoogle Scholar
  21. Norusis M, Spss I (2010) IBM SPSS statistics 19 statistical procedures companion. Proc Cambridge Philos Soc 45:354–359Google Scholar
  22. Sanseverino W, Roma G, De Simone M, Faino L, Melito S, Stupka E et al (2010) PRGdb: a bioinformatics platform for plant resistance gene analysis. Nucl Acids Res 38:D814CrossRefGoogle Scholar
  23. Shiu SH, Bleecker AB (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132:530–543CrossRefGoogle Scholar
  24. Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T et al (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806CrossRefGoogle Scholar
  25. Stahl EA, Dwyer G, Mauricio R, Kreitman M, Bergelson J (1999) Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400:667–671CrossRefGoogle Scholar
  26. Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG, Jones JD (1995) Molecular genetics of plant disease resistance. Science 268:661–667CrossRefGoogle Scholar
  27. Sun X, Cao Y, Yang Z, Xu C, Li X, Wang S, Zhang Q (2004) Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. Plant J 37:517–527CrossRefGoogle Scholar
  28. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731CrossRefGoogle Scholar
  29. Thomma BPHJ, Nürnberger T, Joosten MHAJ (2011) Of PAMPs and Effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4CrossRefGoogle Scholar
  30. Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74–77CrossRefGoogle Scholar
  31. Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY et al (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20:471–481CrossRefGoogle Scholar
  32. Wang J, Tan S, Zhang L, Li P, Tian D (2011a) Co-variation among major classes of LRR-encoding genes in two pairs of plant species. J Mol Evol 72:498–509CrossRefGoogle Scholar
  33. Wang J, Zhang L, Li J, Lawtonrauh A, Tian D (2011b) Unusual signatures of highly adaptable R-loci in closely-related Arabidopsis species. Gene 482:24CrossRefGoogle Scholar
  34. Wu K, Xu T, Guo C, Zhang X, Yang S (2012) Heterogeneous evolutionary rates of Pi2/9 homologs in rice. BMC Genet 13:1–12Google Scholar
  35. Xiao S, Ellwood S, Calis O, Patrick E, Li T, Coleman M, Turner JG (2001) Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW. Science 291(8):118–120CrossRefGoogle Scholar
  36. Yang S, Feng Z, Zhang X, Jiang K, Jin X, Hang Y et al (2006) Genome-wide investigation on the genetic variations of rice disease resistance genes. Plant Mol Biol 62:181–193CrossRefGoogle Scholar
  37. Yang S, Yuan Y, Wang L, Li J, Wang W, Liu H et al (2012) Great majority of recombination events in Arabidopsis are gene conversion events. Proc Natl Acad Sci USA 109:20992–20997CrossRefGoogle Scholar
  38. Yang S, Li J, Zhang X, Zhang Q, Huang J, Chen JQ et al (2013) Rapidly evolving R genes in diverse grass species confer resistance to rice blast disease. Proc Natl Acad Sci USA 110:18572–18577CrossRefGoogle Scholar
  39. Zhang X, Yang S, Wang J, Jia Y, Huang J, Tan S et al (2015) A genome-wide survey reveals abundant rice blast R genes in resistant cultivars. Plant J 84:20–28CrossRefGoogle Scholar
  40. Zhou T, Wang Y, Chen JQ, Araki H, Jing Z, Jiang K et al (2004) Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol Genet Genom 271:402–415CrossRefGoogle Scholar
  41. Zipfel C (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20:10CrossRefGoogle Scholar
  42. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.School of Medical InformaticsXuzhou Medical UniversityXuzhouP.R. China
  2. 2.State Key Laboratory of Pharmaceutical Biotechnology, School of Life SciencesNanjing UniversityNanjingP.R. China

Personalised recommendations