Skip to main content
Log in

Motifs specific for the ADR1 NBS–LRR protein family in Arabidopsis are conserved among NBS–LRR sequences from both dicotyledonous and monocotyledonous plants

  • Rapid Communication
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The activated disease resistance (ADR) 1 gene encodes a protein that possesses an N-terminal coiled-coil (CC) motif, nucleotide-binding site (NBS) and C-terminal leucine-rich repeat (LRR) domains. ADR1 belongs to a small, atypical Arabidopsis thaliana sub-class containing four CC–NBS–LRR genes. The NBS region of most NBS–LRR proteins possesses numerous conserved motifs. In contrast, the LRR domain, which is subject to positive selection, is highly variable. Surprisingly, sequence analysis revealed that the LRR domain of the ADR1 sub-class was more conserved than the NBS region. Sequence analysis identified two novel conserved motifs, termed TVS and PKAE, specific for this CC–NBS–LRR sub-class. The TVS motif is adjacent to the P-loop, whereas the PKAE motif corresponded to the inter-domain region termed the NBS–LRR linker, which was conserved within the different CC–NBS–LRR classes but varied among classes. These ADR1-specific motifs were employed to identify putative ADR1 homologs in phylogenetically distant and agronomically important plant species. Putative ADR1 homologs were identified in 11 species including rice and in 3 further Poaceae species. The ADR1 sub-class of CC–NBS–LRR proteins is therefore conserved in both monocotyledonous and dicotyledonous plant species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ashfield T, Ong LE, Nobuta K, Schneider CM, Innes RW (2004) Convergent evolution of disease resistance gene specificity in two flowering plant families. Plant Cell 16:309–318

    Article  CAS  PubMed  Google Scholar 

  • Bailey T L, Elkan C (1995) The value of prior knowledge in discovering motifs with MEME. Proc Int Conf Intell Syst Mol Biol 3:21–29

    PubMed  Google Scholar 

  • Baumgarten A, Cannon S, Spangler R, May G (2003) Genome-level evolution of resistance genes in Arabidopsis thaliana. Genetics 165:309–319

    CAS  PubMed  Google Scholar 

  • Bork P, Brown NP, Hegyi H, Schultz J (1996) The protein phosphatase 2C (PP2C) superfamily: detection of bacterial homologues. Protein Sci 5:1421–1425

    CAS  PubMed  Google Scholar 

  • 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 54:548–562

    Article  CAS  PubMed  Google Scholar 

  • Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497–3500

    Article  CAS  PubMed  Google Scholar 

  • Chini A, Grant JJ, Seki M, Shinozaki K, Loake GJ (2004) Drought tolerance established by enhanced expression of the CC-NBS-LRR gene, ADR1, requires salicylic acid, EDS1 and ABI1. Plant J 38:810–822

    Article  CAS  PubMed  Google Scholar 

  • Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833

    Article  CAS  PubMed  Google Scholar 

  • Ellis RP, Forster BP, Robinson D, Handley LL, Gordon DC, Russell JR, Powell W (2000) Wild barley: a source of genes for crop improvement in the 21st century? J Exp Bot 51:9–17

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1989) PHYLIP—phylogeny inference package, version 3.2. Cladistics 5:164–166

    Google Scholar 

  • Grant JJ, Chini A, Basu D, Loake GJ (2003) Targeted activation tagging of the Arabidopsis NBS-LRR gene, ADR1, conveys resistance to virulent pathogens. Mol Plant Microbe Interact 16:669–680

    CAS  PubMed  Google Scholar 

  • Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B (2000) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. Embo J 19:4004–4014

    Article  CAS  PubMed  Google Scholar 

  • Kobe B, Kajava AV (2001) The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 11:725–732

    Article  CAS  PubMed  Google Scholar 

  • Meyers BC, Chin DB, Shen KA, Sivaramakrishnan S, Lavelle DO, Zhang Z, Michelmore RW (1998) The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell 10:1817–1832

    Article  CAS  PubMed  Google Scholar 

  • 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 20:317–332

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8:1113–1130

    CAS  PubMed  Google Scholar 

  • Mondragon-Palomino M, Meyers BC, Michelmore RW, Gaut BS (2002) Patterns of positive selection in the complete NBS-LRR gene family of Arabidopsis thaliana. Genome Res 12:1305–1315

    Article  CAS  PubMed  Google Scholar 

  • 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 11:2099–2112

    Article  CAS  PubMed  Google Scholar 

  • Pan Q, Wendel J, Fluhr R (2000) Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes. J Mol Evol 50:203–213

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG, Jones JDG (1995) Molecular genetics of plant disease resitance. Science 248:189–194

    Google Scholar 

  • Thomas D, Rozell TG, Liu X, Segaloff DL (1996) Mutational analyses of the extracellular domain of the full-length lutropin/choriogonadotropin receptor suggest leucine-rich repeats 1-6 are involved in hormone binding. Mol Endocrinol 10:760–768

    Article  CAS  PubMed  Google Scholar 

  • Wang GL, Ruan DL, Song WY, Sideris S, Chen L, Pi LY, Zhang S, Zhang Z, Fauquet C, Gaut BS et al. (1998) Xa21D encodes a receptor-like molecule with a leucine-rich repeat domain that determines race-specific recognition and is subject to adaptive evolution. Plant Cell 10:765–779

    Article  CAS  PubMed  Google Scholar 

  • Zhu H, Cannon SB, Young ND, Cook DR (2002) Phylogeny and genomic organization of the TIR and non-tIR NBS-LRR resistance gene family in Medicago truncatula. Mol Plant Microbe Interact 15:529–39

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Dietlind Gerloff for critically reading this manuscript. AC was the recipient of a Darwin Trust Studentship. This work was supported by BBSRC grant P16595 to GJL.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gary J. Loake.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chini, A., Loake, G.J. Motifs specific for the ADR1 NBS–LRR protein family in Arabidopsis are conserved among NBS–LRR sequences from both dicotyledonous and monocotyledonous plants. Planta 221, 597–601 (2005). https://doi.org/10.1007/s00425-005-1499-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-005-1499-3

Keywords

Navigation