Journal of Plant Biology

, Volume 48, Issue 2, pp 220–228 | Cite as

Expression ofMbR4, a TIR-NBS type of appleR Gene, confers resistance to bacterial spot disease inArabidopsis



A single disease resistance gene candidate,MbR4, was isolated from the wild-type apple speciesMalus baccta. This gene was predicted to encode motifs characteristic of the Toll Interleukin 1 Receptor (TIR) — Nucleotide Binding Site (NBS) of theR gene. Starting with an isolated cDNA clone, genomic clones were obtained via inverse polymerase chain reaction (IPCR). TheMbR4 gene has a single open reading frame (ORF) of 2178 nucleotides, a 41-b untranslated 5’ region, a 21-b untranslated 3’ region, and a predicted protein of 726 amino acids (82 kDa). Its deduced amino acid sequence resembles the N protein of tobacco and the NL25 protein of potato. Ectopic expression ofMbR4 induced enhanced resistance in transgenicArabidopsis plants against the virulent pathogen,Pseudomonas syringae pv.tomato DC3000. Microarray analysis confirmed the induction of defense-related gene expression in pathogen-free 35S::MbR4 heterologousArabidopsis plants, thereby indicating that theMbR4 gene likely activates a pathogen-independent resistance pathway, rather than a gene-for-gene pathway. Our results suggest thatMbR4 plays a role in theR gene, and may be a source of resistance for cultivated apple species.


apple disease resistance gene TIR-NBS (Toll Interleukin 1 Receptor-Nucleotide Binding Site) 


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Literature Cited

  1. Aarts MG, Hekkert B, Holub EB, Beynon JL, Stiekema WJ, Pereira A (1998) Identification of R-gene homologous DNA fragments genetically linked to disease resistance loci inArabidopsis thaliana. Mol Plant Microbe Interact 11: 251–258PubMedCrossRefGoogle Scholar
  2. Baldi P, Patocchi A, Zini E, Toller C, Velasco R, Komjanc M (2004) Cloning and linkage mapping of resistance gene homologous in apple. Theor Appl Genet 109: 231–239PubMedCrossRefGoogle Scholar
  3. Bendahmane A, Querci M, Kanyuka K, Baulcombe DC (2000)Agrobacterium transient expression system as a tool for the isolation of disease resistance genes: Application to the Rx2locus in potato. Plant J 21: 73–81PubMedCrossRefGoogle Scholar
  4. Bent AF (1996) Plant disease resistance gene: Function meets structure. Plant Cell 8: 1757–1771PubMedCrossRefGoogle Scholar
  5. Bergey DR, Orozco-Cardenas M, de Moura DS, Ryan CA (1999) A wound-and systemin-inducible polygalacturonase in tomato leaves. Proc Natl Acad Sci USA 96: 1756–1760PubMedCrossRefGoogle Scholar
  6. Crandall CS (1926) Apple breeding at the University of Illinois. III. Agric Exp Sm Bull 275: 341–600Google Scholar
  7. Dayton DF, Mowry JB, Hought LF, Bailey CH, Williams EB, Janick J, Emerson FH (1970) Prima: An early fall red apple with resistance to apple scab. Fruit Var Hort Dig 24: 20–22Google Scholar
  8. Dellagi A, Helibronn J, Avrova AO, Montesano M, Palva ET, Stewart HE, Toth IK, Cooke DE, Lyon GD, Birch PR (2000) A potato gene encoding a WRKY-like transcription factor is induced in interactions withErwinia carotovora subsp.atroseptica and Phytophthora infestans and is coregulated with class I endochitinase expression. Mol Plant Microbe Interact 13: 1092–1101PubMedCrossRefGoogle Scholar
  9. Dicko MH, Searle-van Leeuwen MJ, Traore AS, Hilhorst R, Beldman G (2001) Polysaccharide hydrolases from leaves ofBoscia senegalensis: Properties of endo-(1-3)-beta-D-glucanase. Appl Biochem Biotechnol 94: 225–241PubMedCrossRefGoogle Scholar
  10. Dinesh-Kumar SP, Baker BJ (2000) Alternatively splicedN resistance gene transcripts: Their possible role in tobacco mosaic virus resistance. Proc Natl Acad Sci USA 5:199Google Scholar
  11. Ding CK, Wang CY, Gross KC, Smith DL (2002) Jasmonate and salicylate induce the expression of pathogenesis-related-protein genes and increase resistance to chilling injury in tomato fruit. Planta 214: 895–901PubMedCrossRefGoogle Scholar
  12. Hehl R, Faurie E, Hesselbach J, Salamini F (1999) TMV resistance gene N homologues are linked toSyn-chytrium endobioticum resistance in potato. Theor Appl Genet 98: 379–386CrossRefGoogle Scholar
  13. Jirage D, Tootle TL, Reuber TL, Frost LN, Feys BJ, Parker JE, Ausubel FM, Glazebrook J (1999)Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc Natl Acad Sci USA 96: 13583–13588PubMedCrossRefGoogle Scholar
  14. Kachroo P, Shanklin J, Shah J, Whittle EJ, Klessig DF (2001) A fatty acid desaturase modulates the activation of defense signaling pathways in plants. Proc Natl Acad Sci USA 98: 9448–9453PubMedCrossRefGoogle Scholar
  15. Lee SY, Seo JS, Rodriguez-Lanetty M, Lee DH (2003) Comparative analysis of superfamilies of NBS-encoding disease resistance gene analogs in cultivated and wild apple species. Mol Genet Genom 269: 101–108Google Scholar
  16. Leister D, Ballvora A, Salamini F, Gebhardt C (1996) A PCR-based approach for isolating pathogen resistance genes from potato with potential for wide application in plants. Nat Genet 14: 421–429PubMedCrossRefGoogle Scholar
  17. Li J, Shan L, Zhou JM, Tang X (2002) Overexpression ofPto induces a salicylate-independent cell death but inhibits necrotic lesions caused by salicylate-deficiency in tomato plants. Mol Plant Microbe Interact 15: 654–661PubMedCrossRefGoogle Scholar
  18. Luck JE, Lawrence GJ, Dodds PN, Shepherd KW, Ellis JG (2000) Regions outside of the leucine-rich repeats of flax rust resistance proteins play a role in specificity determination. Plant Cell 12: 1367–1377PubMedCrossRefGoogle Scholar
  19. 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: 1817–1832PubMedCrossRefGoogle Scholar
  20. Simpson CL, Giffard PM, Jacques NA (1993) A method for the isolation of RNA fromStreptococcus salivarius and its application to the transcriptional analysis of the gtfJK locus. FEMS Microbiol Lett 108: 93–97PubMedCrossRefGoogle Scholar
  21. Tai TH, Dahlbeck D, Clark ET, Gajiwala P, Pasion R, Whalen MC, Stall RE, Staskawicz BJ (1999) Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proc Natl Acad Sci USA 96: 14153–14158PubMedCrossRefGoogle Scholar
  22. Tang X, Xie M, Kim YJ, Zhou J, Klessig DF, Martin GB (1999) Overexpression of Pto activates defense responses and confers broad resistance. Plant Cell 11: 15–29PubMedCrossRefGoogle Scholar
  23. Vinatzer BA, Patocchi A, Gianfranceschi L, Tartarini S, Zhang HB, Gessler C, Sansavini S (2001) Apple contains receptor-like genes homologous to theCladospo-rium fulvum resistance gene family of tomato with a cluster of genes cosegregating with Vf apple scab resistance. Mol Plant Microbe Interact 14: 508–515PubMedCrossRefGoogle Scholar
  24. Whalen MC, Innes RW, Bent AF, Staskawicz BJ (1991) Identification ofPseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining aviru-lence on bothArabidopsis and soybean. Plant Cell 3: 49–59PubMedCrossRefGoogle Scholar
  25. Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr D, Baker B (1994) The product of the tobacco mosaic virus resistance geneN: Similarity to toll and the inter-leukin-1 receptor. Cell 78: 1101PubMedCrossRefGoogle Scholar
  26. Xiao F, Tang X, Zhou JM (2001) Expression of 35S: Pto globally activates defense-related genes in tomato plants. Plant Physiol 126: 1637–1645PubMedCrossRefGoogle Scholar
  27. Xiao F, Lu M, Li J, Zhao T, Yi SY, Thara VK, Tang X, Zhou JM (2003) Pto mutants differentially activate Prf-depen-dent, avrPto-independent resistance and gene-for-gene resistance. Plant Physiol 131: 1239–1249PubMedCrossRefGoogle Scholar
  28. Yu YG, Buss GR, Maroof MA (1996) Isolation of a super-family of candidate disease-resistance genes in soybean based on a conserved nucleotide-binding site. Proc Natl Acad Sci USA 93: 11751–11756PubMedCrossRefGoogle Scholar
  29. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X (1997) Apaf-1, a human protein homologous to C.elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90: 405–413PubMedCrossRefGoogle Scholar

Copyright information

© The Botanical Society of Korea 2005

Authors and Affiliations

  1. 1.Department of Life SciencesEwha Womans UniversitySeoulKorea

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