Advertisement

Evolution of Resistance Genes in Plants

  • Shunyuan Xiao
  • Wenming Wang
  • Xiaohua Yang
Part of the Nucleic Acids and Molecular Biology book series (NUCLEIC, volume 21)

Potential pathogens deliver effector proteins into plant cells to suppress microbe-associated molecular pattern (MAMP)-triggered immunity in plants, resulting in host—pathogen coevolution. To counter pathogen suppression, plants evolved disease resistance (R) proteins to detect the presence of the pathogen effectors and trigger R-dependent defenses. Most isolated R genes encode proteins possessing a leucine-rich-repeat (LRR) domain, of which the majority also contain a nucleotidebinding site (NBS) domain. There is structural similarity and/or domain homology between plant R proteins and animal immunity proteins, suggesting a common origin or convergent evolution of the defense proteins. Two basic strategies have evolved for an R protein to recognize a pathogen effector (then called avirulence factor; Avr): direct physical interaction and indirect interaction via association with other host proteins targeted by the Avr factor. Direct R-Avr recognition leads to high genetic diversity at paired R and Avr loci due to diversifying selection, whereas indirect recognition leads to simple and stable polymorphism at the R and Avr loci due to balancing selection. Based on these two patterns of R-Avr coevolution, investigation of the sequence features at paired R and Avr may help infer the R-Avr interaction mechanisms, assess the role and strength of natural selection at the molecular level in host—pathogen interactions and predict the durability of R gene-triggered resistance.

Keywords

Curr Opin Plant Biol Plant Disease Resistance Gene Indirect Recognition Flax Rust Resistance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, et al (1998) Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc Natl Acad Sci USA 95:10306–10311PubMedCrossRefGoogle Scholar
  2. Allen RL, Bittner-Eddy PD, Grenville-Briggs LJ, Meitz JC, Rehmany AP, et al (2004) Host–parasite coevolutionary conflict between Arabidopsis and downy mildew. Science 306:1957–1960PubMedCrossRefGoogle Scholar
  3. Araki H, Tian D, Goss EM, Jakob K, Halldorsdottir SS, et al (2006) Presence/absence polymorphism for alternative pathogenicity islands in Pseudomonas viridiflava, a pathogen of Arabidopsis. Proc Natl Acad Sci USA 103:5887–5892PubMedCrossRefGoogle Scholar
  4. 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 16:309–318PubMedCrossRefGoogle Scholar
  5. Ausubel FM (2005) Are innate immune signaling pathways in plants and animals conserved? Nat Immunol 6:973–979PubMedCrossRefGoogle Scholar
  6. Axtell MJ, Staskawicz BJ (2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112:369–377PubMedCrossRefGoogle Scholar
  7. Bai J, Pennill LA, Ning J, Lee SW, Ramalingam J, et al (2002) Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res 12:1871–1884PubMedCrossRefGoogle Scholar
  8. Bakker EG, Toomajian C, Kreitman M, Bergelson J (2006) A genome-wide survey of r gene polymorphisms in Arabidopsis. Plant Cell 18:1803–1818PubMedCrossRefGoogle Scholar
  9. Baumgarten A, Cannon S, Spangler R, May G (2003) Genome-level evolution of resistance genes in Arabidopsis thaliana. Genetics 165:309–319PubMedGoogle Scholar
  10. Belkhadir Y, Subramaniam R, Dangl JL (2004) Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr Opin Plant Biol 7:391–399PubMedCrossRefGoogle Scholar
  11. Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, et al (1994) RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265:1856–1860PubMedCrossRefGoogle Scholar
  12. Bergelson J, Kreitman M, Stahl EA, Tian D (2001) Evolutionary dynamics of plant R-genes. Science 292:2281–2285PubMedCrossRefGoogle Scholar
  13. Birch PR, Rehmany AP, Pritchard L, Kamoun S, Beynon JL (2006) Trafficking arms: oomycete effectors enter host plant cells. Trends Microbiol 14:8–11PubMedCrossRefGoogle Scholar
  14. Botella MA, Parker JE, Frost LN, Bittner-Eddy PD, Beynon JL, et al (1998) Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants. Plant Cell 10:1847–1860PubMedCrossRefGoogle Scholar
  15. Buschges R, Hollricher K, Panstruga R, Simons G, Wolter M, et al (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695–705PubMedCrossRefGoogle Scholar
  16. Caicedo AL, Schaal BA, Kunkel BN (1999) Diversity and molecular evolution of the RPS2 resistance gene in Arabidopsis thaliana. Proc Natl Acad Sci USA 96:302–306PubMedCrossRefGoogle Scholar
  17. Cannon SB, Zhu H, Baumgarten AM, Spangler R, May G, et al (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
  18. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host–microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814PubMedCrossRefGoogle Scholar
  19. Chu Z, Yuan M, Yao J, Ge X, Yuan B, et al (2006) Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes Dev 20:1250–1255PubMedCrossRefGoogle Scholar
  20. Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833PubMedCrossRefGoogle Scholar
  21. Dangl JL, McDowell JM (2006) Two modes of pathogen recognition by plants. Proc Natl Acad Sci USA 103:8575–8576PubMedCrossRefGoogle Scholar
  22. Deslandes L, Olivier J, Theulieres F, Hirsch J, Feng DX, et al (2002) Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc Natl Acad Sci USA 99:2404–2409PubMedCrossRefGoogle Scholar
  23. Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, et al (2003) Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc Natl Acad Sci USA 100:8024–8029PubMedCrossRefGoogle Scholar
  24. Dodds PN, Lawrence GJ, Catanzariti AM, Ayliffe MA, Ellis JG (2004) The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell 16:755–768PubMedCrossRefGoogle Scholar
  25. Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CI, et al (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci USA 103:8888–8893PubMedCrossRefGoogle Scholar
  26. Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209PubMedCrossRefGoogle Scholar
  27. 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 11:495–506PubMedCrossRefGoogle Scholar
  28. Ellis J, Dodds P, Pryor T (2000) Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol 3:278–284PubMedCrossRefGoogle Scholar
  29. Ellis J, Catanzariti AM, Dodds P (2006) The problem of how fungal and oomycete avirulence proteins enter plant cells. Trends Plant Sci 11:61–63PubMedCrossRefGoogle Scholar
  30. Eulgem T (2005) Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci 10:71–78PubMedCrossRefGoogle Scholar
  31. Flor HH (1956) The complementary genic systems in flax and flax rust. Adv Genet Mol Genet Med 8:29–54Google Scholar
  32. Fluhr R, Kaplan-Levy RN (2002) Plant disease resistance: commonality and novelty in multicellular innate immunity. Curr Top Microbiol Immunol 270:23–46PubMedGoogle Scholar
  33. Goff SA, Ricke D, Lan TH, Presting G, Wang R, et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100PubMedCrossRefGoogle Scholar
  34. Gomez-Gomez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011PubMedCrossRefGoogle Scholar
  35. Grant MR, Godiard L, Straube E, Ashfield T, Lewald J, et al (1995) Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269:843–846PubMedCrossRefGoogle Scholar
  36. Gu K, Yang B, Tian D, Wu L, Wang D, et al (2005) R gene expression induced by a type-III effector triggers disease resistance in rice. Nature 435:1122–1125PubMedCrossRefGoogle Scholar
  37. Halterman DA, Wise RP (2004) A single-amino acid substitution in the sixth leucine-rich repeat of barley MLA6 and MLA13 alleviates dependence on RAR1 for disease resistance signaling. Plant J 38:215–226PubMedCrossRefGoogle Scholar
  38. Hammond-Kosack KE, Jones JD (1997) Plant disease resistance genes. Annu Rev Plant Physiol Plant Mol Biol 48:575–607PubMedCrossRefGoogle Scholar
  39. Hammond-Kosack KE, Parker JE (2003) Deciphering plant–pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotechnol 14:177–193PubMedCrossRefGoogle Scholar
  40. He P, Shan L, Lin NC, Martin GB, Kemmerling B, et al (2006) Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125:563–575PubMedCrossRefGoogle Scholar
  41. Holub EB (2001) The arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Genet 2:516–527PubMedCrossRefGoogle Scholar
  42. Inohara N, Nunez G (2003) NODs: intracellular proteins involved in inflammation and apoptosis. Nat Rev Immunol 3:371–382PubMedCrossRefGoogle Scholar
  43. 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 19:4004–4014PubMedCrossRefGoogle Scholar
  44. Johal GS, Briggs SP (1992) Reductase activity encoded by the HM1 disease resistance gene in maize. Science 258:985–987PubMedCrossRefGoogle Scholar
  45. Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ, Jones JD (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789–793PubMedCrossRefGoogle Scholar
  46. Kim MG, da Cunha L, McFall AJ, Belkhadir Y, DebRoy S, et al (2005) Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell 121:749–759PubMedCrossRefGoogle Scholar
  47. Kim YJ, Lin NC, Martin GB (2002) Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109:589–598PubMedCrossRefGoogle Scholar
  48. 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 16:2870–2894PubMedCrossRefGoogle Scholar
  49. Kuang H, Wei F, Marano MR, Wirtz U, Wang X, et al (2005) The R1 resistance gene cluster contains three groups of independently evolving, type I R1 homologues and shows substantial structural variation among haplotypes of Solanum demissum. Plant J 44:37–51PubMedCrossRefGoogle Scholar
  50. Lawrence GJ, Finnegan EJ, Ayliffe MA, Ellis JG (1995) The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. Plant Cell 7:1195–1206PubMedCrossRefGoogle Scholar
  51. Leach JE, Vera Cruz CM, Bai J, Leung H (2001) Pathogen fitness penalty as a predictor of durability of disease resistance genes. Annu Rev Phytopathol 39:187–224PubMedCrossRefGoogle Scholar
  52. Leipe DD, Koonin EV, Aravind L (2004) STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer. J Mol Biol 343:1–28PubMedCrossRefGoogle Scholar
  53. Leister D (2004) Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. Trends Genet 20:116–122PubMedCrossRefGoogle Scholar
  54. Leister RT, Dahlbeck D, Day B, Li Y, Chesnokova O, et al (2005) Molecular genetic evidence for the role of SGT1 in the intramolecular complementation of Bs2 protein activity in Nicotiana benthamiana. Plant Cell 17:1268–1278PubMedCrossRefGoogle Scholar
  55. 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
  56. Luderer R, Takken FL, de Wit PJ, Joosten MH (2002) Cladosporium fulvum overcomes Cf-2-mediated resistance by producing truncated AVR2 elicitor proteins. Mol Microbiol 45:875–884PubMedCrossRefGoogle Scholar
  57. Mackey D, Holt BF 3rd, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743–754PubMedCrossRefGoogle Scholar
  58. Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:379–389PubMedCrossRefGoogle Scholar
  59. Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, et al (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–1436PubMedCrossRefGoogle Scholar
  60. Mauricio R, Stahl EA, Korves T, Tian D, Kreitman M, et al (2003) Natural selection for polymorphism in the disease resistance gene Rps2 of Arabidopsis thaliana. Genetics 163:735–746PubMedGoogle Scholar
  61. McDowell JM, Dhandaydham M, Long TA, Aarts MG, Goff S, et al (1998) Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell 10:1861–1874PubMedCrossRefGoogle Scholar
  62. McHale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212PubMedCrossRefGoogle Scholar
  63. Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, et al (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
  64. 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
  65. 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
  66. Meyers BC, Kaushik S, Nandety RS (2005) Evolving disease resistance genes. Curr Opin Plant Biol 8:129–134PubMedCrossRefGoogle Scholar
  67. 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
  68. Moffett P, Farnham G, Peart J, Baulcombe DC (2002) Interaction between domains of a plant NBS-LRR protein in disease resistance-related cell death. EMBO J 21:4511–4519PubMedCrossRefGoogle Scholar
  69. Mudgett MB (2005) New insights to the function of phytopathogenic bacterial type III effectors in plants. Annu Rev Plant Biol 56:509–531PubMedCrossRefGoogle Scholar
  70. Muskett P, Parker J (2003) Role of SGT1 in the regulation of plant R gene signalling. Microbes Infect 5:969–976PubMedCrossRefGoogle Scholar
  71. Noel L, Moores TL, Van der Biezen EA, Parniske M, Daniels MJ, et al (1999) Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell 11:2099–2112PubMedCrossRefGoogle Scholar
  72. Nomura K, Debroy S, Lee YH, Pumplin N, Jones J, et al (2006) A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313:220–223PubMedCrossRefGoogle Scholar
  73. Nurnberger T, Brunner F (2002) Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Curr Opin Plant Biol 5:318–324PubMedCrossRefGoogle Scholar
  74. Nurnberger T, Brunner F, Kemmerling B, Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198:249–266PubMedCrossRefGoogle Scholar
  75. O’Neill LA, Fitzgerald KA, Bowie AG (2003) The Toll-IL-1 receptor adaptor family grows to five members. Trends Immunol 24:286–290PubMedCrossRefGoogle Scholar
  76. Orgil U, Araki H, Tangchaiburana S, Berkey R, and Xiao S (2007) Intraspecific Genetic Variations, Fitness Cost and Benefit of RPW8, A Disease Resistance Locus in Arabidopsis thaliana. Genetics 176:2317–2333PubMedCrossRefGoogle Scholar
  77. Parniske M, Hammond-Kosack KE, Golstein C, Thomas CM, Jones DA, et al (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
  78. Peart JR, Mestre P, Lu R, Malcuit I, Baulcombe DC (2005) NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against tobacco mosaic virus. Curr Biol 15:968–973PubMedCrossRefGoogle Scholar
  79. Pitman AR, Jackson RW, Mansfield JW, Kaitell V, Thwaites R, et al (2005) Exposure to host resistance mechanisms drives evolution of bacterial virulence in plants. Curr Biol 15:2230–2235PubMedCrossRefGoogle Scholar
  80. Rairdan GJ, Moffett P (2006) Distinct domains in the ARC region of the potato resistance protein Rx mediate LRR binding and inhibition of activation. Plant Cell 18:2082–2093PubMedCrossRefGoogle Scholar
  81. Rehmany AP, Gordon A, Rose LE, Allen RL, Armstrong MR, et al (2005) Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17:1839–1850PubMedCrossRefGoogle Scholar
  82. Richly E, Kurth J, Leister D (2002) Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution. Mol Biol Evol 19:76–84PubMedGoogle Scholar
  83. Roeder A, Kirschning CJ, Rupec RA, Schaller M, Weindl G, et al (2004) Toll-like receptors as key mediators in innate antifungal immunity. Med Mycol 42:485–498PubMedCrossRefGoogle Scholar
  84. Rohmer L, Guttman DS, Dangl JL (2004) Diverse evolutionary mechanisms shape the type III effector virulence factor repertoire in the plant pathogen Pseudomonas syringae. Genetics 167:1341–1360PubMedCrossRefGoogle Scholar
  85. Rooney HC, Van’t Klooster JW, van der Hoorn RA, Joosten MH, Jones JD, et al (2005) Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308:1783–1786PubMedCrossRefGoogle Scholar
  86. Rose LE, Bittner-Eddy PD, Langley CH, Holub EB, Michelmore RW, et al (2004) The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana. Genetics 166:1517–1527PubMedCrossRefGoogle Scholar
  87. Rose LE, Langley CH, Bernal AJ, Michelmore RW (2005) Natural variation in the Pto pathogen resistance gene within species of wild tomato (Lycopersicon). I. Functional analysis of Pto alleles. Genetics 171:345–357PubMedCrossRefGoogle Scholar
  88. Salmeron JM, Oldroyd GE, Rommens CM, Scofield SR, Kim HS, et al (1996) Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell 86:123–133PubMedCrossRefGoogle Scholar
  89. Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, et al (2003) Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301:1230–1233PubMedCrossRefGoogle Scholar
  90. Song WY, Wang GL, Chen LL, Kim HS, Pi LY, et al (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806PubMedCrossRefGoogle Scholar
  91. Stahl EA, Dwyer G, Mauricio R, Kreitman M, Bergelson J (1999) Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400:667–671PubMedCrossRefGoogle Scholar
  92. Staskawicz BJ, Mudgett MB, Dangl JL, Galan JE (2001) Common and contrasting themes of plant and animal diseases. Science 292:2285–2289PubMedCrossRefGoogle Scholar
  93. Sun X, Cao Y, Yang Z, Xu C, Li X, et al (2004) Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. Plant J 37:517–527PubMedCrossRefGoogle Scholar
  94. Swiderski MR, Innes RW (2001) The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. Plant J 26:101–112PubMedCrossRefGoogle Scholar
  95. Takeda K, Akira S (2004) Microbial recognition by Toll-like receptors. J Dermatol Sci 34:73–82PubMedCrossRefGoogle Scholar
  96. Takken FL, Albrecht M, Tameling WI (2006) Resistance proteins: molecular switches of plant defence. Curr Opin Plant Biol 9:383–390PubMedCrossRefGoogle Scholar
  97. Tameling WI, Vossen JH, Albrecht M, Lengauer T, Berden JA, et al (2006) Mutations in the NB-ARC domain of I-2 that impair ATP hydrolysis cause autoactivation. Plant Physiol 140:1233–1245PubMedCrossRefGoogle Scholar
  98. Tang X, Frederick RD, Zhou J, Halterman DA, Jia Y, et al (1996) Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274:2060–2063PubMedCrossRefGoogle Scholar
  99. Tian D, Araki H, Stahl E, Bergelson J, Kreitman M (2002) Signature of balancing selection in Arabidopsis. Proc Natl Acad Sci USA 99:11525–11530PubMedCrossRefGoogle Scholar
  100. Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74–77PubMedCrossRefGoogle Scholar
  101. Tor M, Brown D, Cooper A, Woods-Tor A, Sjolander K, et al (2004) Arabidopsis downy mildew resistance gene RPP27 encodes a receptor-like protein similar to CLAVATA2 and tomato Cf-9. Plant Physiol 135:1100–1112PubMedCrossRefGoogle Scholar
  102. Van der Biezen EA, Jones JD (1998a) Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem Sci 23:454–456PubMedCrossRefGoogle Scholar
  103. Van der Biezen EA, Jones JD (1998b) The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr Biol 8:R226–227PubMedCrossRefGoogle Scholar
  104. Van der Hoorn RA, Roth R, De Wit PJ (2001) Identification of distinct specificity determinants in resistance protein Cf-4 allows construction of a Cf-9 mutant that confers recognition of avirulence protein Avr4. Plant Cell 13:273–285PubMedCrossRefGoogle Scholar
  105. Van der Hoorn RA, De Wit PJ, Joosten MH (2002) Balancing selection favors guarding resistance proteins. Trends Plant Sci 7:67–71PubMedCrossRefGoogle Scholar
  106. Warren RF, Merritt PM, Holub E, Innes RW (1999) Identification of three putative signal transduction genes involved in R gene-specified disease resistance in Arabidopsis. Genetics 152:401–412PubMedGoogle Scholar
  107. Wei F, Wing RA, Wise RP (2002) Genome dynamics and evolution of the Mla (powdery mildew) resistance locus in barley. Plant Cell 14:1903–1917PubMedCrossRefGoogle Scholar
  108. Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, et al (1994) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78:1101–1115PubMedCrossRefGoogle Scholar
  109. Wiermer M, Feys BJ, Parker JE (2005) Plant immunity: the EDS1 regulatory node. Curr Opin Plant Biol 8:383–389PubMedCrossRefGoogle Scholar
  110. Xiao S (2006) Current perspectives on molecular mechanisms of plant disease resistance. In: Teixeira da Silva JA (ed) Floriculture, ornamental and plant biotechnology: advances and topical issues, vol 3. Global Science Books, London, pp 317–333Google Scholar
  111. 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
  112. 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
  113. Yahiaoui N, Brunner S, Keller B (2006) Rapid generation of new powdery mildew resistance genes after wheat domestication. Plant J 47:85–98PubMedCrossRefGoogle Scholar
  114. Yamamoto M, Takeda K, Akira S (2004) TIR domain-containing adaptors define the specificity of TLR signaling. Mol Immunol 40:861–868PubMedCrossRefGoogle Scholar
  115. Young ND (2000) The genetic architecture of resistance. Curr Opin Plant Biol 3:285–290PubMedCrossRefGoogle Scholar
  116. Zhou T, Wang Y, Chen JQ, Araki H, Jing Z, et al (2004) Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol Genet Genomics 271:402–415PubMedCrossRefGoogle Scholar
  117. Zhu Y, Chen H, Fan J, Wang Y, Li Y, et al (2000) Genetic diversity and disease control in rice. Nature 406:718–722PubMedCrossRefGoogle Scholar
  118. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, et al (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  • Shunyuan Xiao
    • 1
  • Wenming Wang
    • 1
  • Xiaohua Yang
    • 1
  1. 1.Center for Biosystems ResearchUniversity of Maryland Biotechnology InstituteRockvilleUSA

Personalised recommendations