Plant Molecular Biology

, Volume 42, Issue 1, pp 195–204 | Cite as

The evolution of disease resistance genes

  • Todd E. Richter
  • Pamela C. Ronald


Several common themes have shaped the evolution of plant disease resistance genes. These include duplication events of progenitor resistance genes and further expansion to create clustered gene families. Variation can arise from both intragenic and intergenic recombination and gene conversion. Recombination has also been implicated in the generation of novel resistance specificities. Resistance gene clusters appear to evolve more rapidly than other regions of the genome. In addition, domains believed to be involved in recognitional specificity, such as the leucine-rich repeat (LRR), are subject to adaptive selection. Transposable elements have been associated with some resistance gene clusters, and may generate further variation at these complexes.

gene duplication intergenic recombination leucine-rich repeat (LRR) transposable elements Xa21 


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  1. 1.
    Andersson G, Svensson A, Setterblad N, Rask L: Retroelements in the human MHC class II region. Trends Genet 14: 109–114 (1998).Google Scholar
  2. 2.
    Anderson PA, Lawrence GJ, Morrish BC, Ayliffe MA, Finnegan EJ, Ellis JG: Inactivation of the flax rust resistance gene M associated with loss of a repeated unit within the leucine-rich repeat coding region. Plant Cell 9: 641–651 (1997).Google Scholar
  3. 3.
    Baker B, Zambryski P, Staskawicz B, Dinesh-Kumar SP: Signaling in plant-microbe interactions. Science 276: 726–733 (1997).Google Scholar
  4. 4.
    Bennetzen JL, Freeling M: Grasses as a single genetic system: genome composition, collinearity and compatibility. Trends Genet 9: 259–261 (1993).Google Scholar
  5. 5.
    Bennetzen JL, Qin M, Ingels S, Ellingboe: Allele-specific and Mutator-associated instability at the Rp1 disease-resistance locus of maize. Nature 332: 369–370 (1988).Google Scholar
  6. 6.
    Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, Leung J, Staskawicz BJ: RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265: 1856–1859 (1994)Google Scholar
  7. 7.
    Botella MA, Coleman MJ, Hughes DE, Nishimura MT, Jones JD, Somerville SC: Map positions of 47 Arabidopsis sequences with sequence similarity to disease resistance genes. Plant J 12: 1197–1211 (1997).Google Scholar
  8. 8.
    Bureau T, Ronald P, Wessler S: A computer-based systematic survey reveals the predominance of small inverted-repeat el203 ements in wild-type rice genes. Proc Natl Acad Sci USA 93: 8524–8529 (1996).Google Scholar
  9. 9.
    Buschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Groenendijk J, Topsch S, Vos P, Salamini F, Schulze-Lefert P: The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88: 695–705 (1997).Google Scholar
  10. 10.
    Clark SE, Williams RW, Meyerowitz EM: The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89: 575–585 (1997).Google Scholar
  11. 11.
    Crute IR: The genetic basis of relationships between microbial parasites and their hosts. In: Frazer RSS (ed.), Mechanisms of Plant Diseases, pp. 80–142. Martinus Nijhoff/W. Junk, Dordrecht, Netherlands (1985).Google Scholar
  12. 12.
    Dietrich RA, Delaney TP, Uknes SJ, Ward ER, Ryals JA, Dangl JL: Arabidopsis mutants simulating disease resistance response. Cell 77: 565–577 (1994).Google Scholar
  13. 13.
    Dietrich RA, Richberg MH, Schmidt R, Dean C, Dangl JL: A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death. Cell 88: 685–694 (1997).Google Scholar
  14. 14.
    Devos KM, Gale MD: Comparative genetics in the grasses. Plant Mol Biol 35: 3–15 (1997).Google Scholar
  15. 15.
    Dixon MS, Jones DA, Keddie JS, Thomas CM, Harrison K, Jones JD: The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84: 451–459 (1996).Google Scholar
  16. 16.
    Dooner HK, Martinez-Ferez IM: Germinal excisions of the maize transposon activator do not stimulate meiotic recombination or homology-dependent repair at the bz locus. Genetics 147: 1923–1932 (1997).Google Scholar
  17. 17.
    Ellis J, Jones D: Structure and function of proteins controlling strain specific pathogen resistance in plants. Curr Opin Plant Biol 1: 288–293 (1998).Google Scholar
  18. 18.
    Ellis J, Lawrence GJ, Finnegan EJ, Anderson PA: Contrasting complexity of two rust resistance loci in flax. Proc Natl Acad Sci USA 92: 4185–4188 (1995).Google Scholar
  19. 19.
    Endo T, Ikeo K, Gojobori T: Large-scale search for genes on which positive selection may operate. Mol Biol Evol 13: 685–690 (1996).Google Scholar
  20. 20.
    Flor HH: The complementary genic systems in flax and flax rust. Adv Genet 8: 29–54 (1956).Google Scholar
  21. 21.
    Greenberg JT, Guo A, Klessig DF, Ausubel FM: Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell 77: 551–563 (1994).Google Scholar
  22. 22.
    Grant MR, Godiard L, Straube E, Ashfield T, Lewald J, Sattler A, Innes RW, Dangle JL: Structure of the Arabidopsis Rpm1 gene enabling dual specificity disease resistance. Science 269: 843–846 (1995).Google Scholar
  23. 23.
    Hu G. Hulbert SH: Evidence for the involvement of gene conversion in the meiotic instability of the Rp1 rust resistance genes of maize. Genome 37: 742–746 (1994).Google Scholar
  24. 24.
    Hu G, Richter T, Hulbert S, Pryor T: Disease lesion mimicry caused by mutations in the rust resistance gene rp1. Plant Cell 8: 1367–1376 (1996).Google Scholar
  25. 25.
    Hughes AL, Nei M: Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335: 167–170 (1988).Google Scholar
  26. 26.
    Hulbert SH, Bennetzen JL: Recombination at the Rp1 locus of maize. Mol Gen Genet 226: 742–746 (1991).Google Scholar
  27. 27.
    Islam MR, Shepherd KW: Present status of genetics of rust resistance in flax. Euphytica 55: 255–267 (1991).Google Scholar
  28. 28.
    Jiang J, Wang GL, Ronald PC, Gill B, Ward: Metaphase and interphase mapping of the rice genome using bacterial artifi-cial chromosomes. Proc Natl Acad Sci USA 92: 4487–4491 (1995).Google Scholar
  29. 29.
    Johal GS, Briggs SP: Reductase activity encoded by the Hm1 disease resistance gene in maize. Science 258: 985–987 (1992).Google Scholar
  30. 30.
    Jones J, Parniske M, Thomas T, Hammond-Kosack K, Romeis T, Piedras P, Tai T, Torres MA, Hatzixanthis K, Brading P, Wulff BH: Evolution and function of tomato Cf-disease resistance genes. In: Plant Disease Resistance Gene Function. An EMBO Workshop, 18- 20 May 1997 (Moratea, Italy).Google Scholar
  31. 31.
    Kaloshian I, Lange WH, Williamson VM: An aphid-resistance locus is tightly linked to the nematode-resistance gene, Mi, in tomato. Proc Natl Acad Sci USA 92: 622–625 (1995).Google Scholar
  32. 32.
    Kanazin V, Marek LF, Shoemaker RC: Resistance gene analogs are conserved and clustered in soybean. Proc Natl Acad Sci USA 93: 11746–11750 (1996).Google Scholar
  33. 33.
    Kilian A, Chen J, Han F, Steffenson B, Kleinhofs A: Towards map-based cloning of the barley stem rust resistance genes Rpg1 and rpg4 using rice as an intergenomic cloning vehicle. Plant Mol Biol 35: 187–195 (1997).Google Scholar
  34. 34.
    Kimura M: The Neutral Theory of Molecular Evolution, Cambridge University Press, Cambridge, UK (1983).Google Scholar
  35. 35.
    Kobe B, Deisenhofer J. The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 19: 415–420 (1994).Google Scholar
  36. 36.
    Lawrence GJ, Finnegan EJ, Ayliffe MA, Ellis JG: 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: 1195–1206 (1995).Google Scholar
  37. 37.
    Leister D, Kurth J, Laurie DA, Yano M, Sasaki T, Devos K, Graner A, Schulze-Lefert P: Rapid reorganization of resistance gene homologues in cereal genomes. Proc Natl Acad Sci USA 95: 370–375 (1998).Google Scholar
  38. 38.
    Li J, Chory J: A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90: 929–938 (1997).Google Scholar
  39. 39.
    Marionette S, Wessler SR: Retrotransposon insertion into the maize waxy gene results in tissue-specific RNA processing. Plant Cell 9: 967–978 (1997).Google Scholar
  40. 40.
    Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earle ED, Tanksley SD: Mapbased cloning of a protein kinase gene conferring disease resistance in tomato. Science 262: 1432–1436 (1993).Google Scholar
  41. 41.
    Martin GB, Frary A, Wu T, Brommonschenkel SH, Chunwongse J, Earle ED, Tanksley S D: A member of the tomato Pto gene family confers sensitivity to fenthion resulting in rapid cell death. Plant Cell 6: 1543–1552 (1994).Google Scholar
  42. 42.
    Mathern J, Hake S: Mu element-generated gene conversions in maize attenuate the dominant knotted phenotype. Genetics 147: 305–314 (1997).Google Scholar
  43. 43.
    McClintock B: The significance of responses of the genome to challenge. Science 226: 792–801 (1984).Google Scholar
  44. 44.
    McMullen MD, Simcox K: Genomic organization of disease and insect resistance genes in maize. Mol Plant-Microbe Interact 8: 811–815 (1995).Google Scholar
  45. 45.
    McDonald JF: Transposable elements - possible catalysts of organismic evolution. Trends Ecol Evol 10: 123–126 (1995).Google Scholar
  46. 46.
    Messier W, Stewart CB: Episodic adaptive evolution of primate lysozymes. Nature 385: 151–154 (1997).Google Scholar
  47. 47.
    Meyers BC, Shen KA, Rohani P, Gaut B, Michelmore R: Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell 10: 1833–1846 (1998).Google Scholar
  48. 48.
    Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM: The root-knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10: 1307–1319 (1998).Google Scholar
  49. 49.
    Mindrinos M, Katagiri F, Yu GL, Ausubel FM: The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78: 1089–1099 (1994).Google Scholar
  50. 50.
    Multani DS, Meeley RB, Paterson AH, Gray J, Briggs SP, Johal GS: Plant-pathogen microevolution: molecular basis for the origin of a fungal disease in maize. Proc Natl Acad Sci USA 95: 1686–1691 (1998).Google Scholar
  51. 51.
    Ohno S: Evolution by Gene Duplication, Springer-Verlag, Berlin/Vienna/New York(1970).Google Scholar
  52. 52.
    Panstruga R, Buschges R, Freialdenhoven A, Ropenack E, Schulze-Lefert P: Insights into non-race-specific resistance: the mlo-controlled resistance in barley to powdery mildew. In: Plant Disease Resistance Gene Function. An EMBO Workshop, 18–20 May 1997 (Moratea, Italy).Google Scholar
  53. 53.
    Parker JE, Coleman MJ, Szabo V, Frost LN, Schmidt R, van der Biezen EA, Moores T, Dean C, Daniels MJ, Jones JDG: The Arabidopsis downy mildew resistance gene Rpp5 shares similarity to the Toll and Interleukin-1 receptors with N and L6. Plant Cell 9: 879–894 (1997).Google Scholar
  54. 54.
    Parniske M, Hammond-Kosack KE, Golstein C, Thomas CM, Jones DA, Harrison K, Wulff BB, Jones JD: Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 91: 821–832 (1997).Google Scholar
  55. 55.
    Petersen UM, Bjorklund G, Ip YT, Engstrom Y: The dorsalrelated immunity factor, Dif, is a sequence-specific transactivator of Drosophila Cecropin gene expression. EMBO J 14: 3146–3158 (1995).Google Scholar
  56. 56.
    Pouteau S, Boccara M, Grandbastien MA: Microbial elicitors of plant defense responses activate transcription of a retrotranspsoson. Plant J 5: 535–542 (1994).Google Scholar
  57. 57.
    Pryor AJ: The origin and structure of fungal disease resistance genes in plants. Trends Genet 3: 157–161 (1987).Google Scholar
  58. 58.
    Pryor AJ, Ellis J: The genetic complexity of fungal disease resistance genes in plants. Adv Plant Pathol 10: 281–305 (1993).Google Scholar
  59. 59.
    Rathjen JP, Chang JH, Staskawicz BJ, Michelmore RW: Constitutively active Pto induces a Prf-dependent hypersensitive response in the absence of AvrPto. EMBO J, in press (1999).Google Scholar
  60. 60.
    Richter TE, Pryor AJ, Bennetzen JL, Hulbert SH: New rust resistance specificities associated with recombination at the Rp1 complex in maize. Genetics 141: 373–381 (1995).Google Scholar
  61. 61.
    Ronald PC, Albano B, Tabien R, Abenes L, Wu K, McCouch S, Tanksley S: Genetic and physical analysis of the rice bacterial blight resistance locus, Xa21. Mol Gen Genet 236: 113–120 (1992).Google Scholar
  62. 62.
    Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM: The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc Natl Acad Sci USA 95: 9750–9754 (1998).Google Scholar
  63. 63.
    Saxena KMS, Hooker AL: A study on the structure of gene Rp3 for rust resistance in Zea mays. Can J Genet Cytol 16:857–860 (1974).Google Scholar
  64. 64.
    Sanz-Alferez S, Richter TE, Hulbert, SH, and Bennetzen JL: The Rp3 disease resistance gene of maize: mapping and characterization of introgressed alleles. Theor Appl Genet 91: 25–32 (1995).Google Scholar
  65. 65.
    Scofield SR, Tobias CM, Rathjen JP, Chang JH, Lavelle DT, Michelmore RW, Staskawicz BJ: Molecular basis of gene-forgene specificity in bacterial speck disease of tomato. Science 274: 765–768 (1996).Google Scholar
  66. 66.
    Shalev G, Levy AA: The transposable element Ac induces recombination between the donor site and a homologous ectopic sequence. Genetics 146: 1143–1151 (1997).Google Scholar
  67. 67.
    Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Gardner J, Wang B, Holsten T, Zhai WX, Zhu LH, Fauquet C, Ronald PC: A receptor kinase-like protein encoded by the rice disease resistance gene Xa21. Science 270: 1804–1806 (1995).Google Scholar
  68. 68.
    Song W, Pi L, Wang G, Gardner J, Holsten T, Ronald P: Evolution of the rice Xa21 disease resistance gene family. Plant Cell 9: 1279–1287 (1997).Google Scholar
  69. 69.
    Song WY, Pi LY, Bureau T, Ronald PR: Identification and characterization of 14 transposable-like elements in the noncoding regions of the rice Xa21 disease resistance gene family members. Mol Gen Genet 258: 449–456 (1998).Google Scholar
  70. 70.
    Sudupak MA, Bennetzen JL, Hulbert SH: Unequal exchange and meiotic instability of the Rp1 region disease resistance genes in maize. Genetics 133: 119–125 (1993).Google Scholar
  71. 71.
    Thomas CM, Jones DA, Parniske M, Harrison K, Balint-Kurti PJ, Hatzixanthis K, Jones JD: Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell 9: 2209–2224 (1997).Google Scholar
  72. 72.
    Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF, Komeda Y: The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8: 735–746 (1996).Google Scholar
  73. 73.
    Wang G-L, Ruan D-L, Song WY, Sideris S, Chen L-L, Pi LY, Zhang S, Zhang Z, Fauquet C, Gaut B, Ronald P: 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: 1–15 (1998).Google Scholar
  74. 74.
    Wessler S, Bureau TE, White SE: LTR-retrotransposons and MITEs - important players in the evolution of plant genomes. Curr Opin Genet Dev 5: 814–821 (1995).Google Scholar
  75. 75.
    Whitman S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B: The product of the tobacco mosaic virus resistance gene N: similarity to Toll and the interleukin-1 receptor. Cell 78:1101–1115 (1994).Google Scholar
  76. 76.
    Williamson VM: Root-knot nematode resistance genes in tomato and their potential for future use. Annu Rev Phytopathol 36: 277–293 (1998).Google Scholar
  77. 77.
    Wilkinson DR, Hooker AL: Genetics of reaction to Puccinia sorghi in ten corn inbred lines from Africa and Europe. Phytopathology 58: 605–608 (1968).Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Todd E. Richter
    • 1
  • Pamela C. Ronald
    • 1
  1. 1.Center for Engineering Plants for Resistance Against PathogensDavisUSA

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