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The genomic architecture of disease resistance in lettuce


Genbank and The Compositae Genome Project database, containing over 42,000 lettuce unigenes from Lactuca sativa cv. Salinas and L. serriola accession UC96US23 were mined to identify 702 candidate genes involved in pathogen recognition (RGCs), resistance signal transduction, defense responses, and disease susceptibility. In addition, to identify sequences representing additional sub-families of nucleotide binding site (NBS)-leucine-rich repeat encoding genes; the major classes of resistance genes (R-genes), NBS-encoding sequences were amplified by PCR using degenerate oligonucleotides designed to NBS sub-families specific to the subclass Asteridae, which includes the Compositae family. These products were cloned and sequenced resulting in 18 novel NBS sequences from cv. Salinas and 15 novel NBS sequences from UC96US23. Using a variety of marker technologies, 294 of the 735 candidate disease resistance genes were mapped in our primary mapping population, which consisted of 119 F7 recombinant inbred lines derived from an interspecific cross between cv. Salinas and UC96US23. Using markers shared across multiple genetic maps, 36 resistance phenotypic loci, including two new loci for resistance to downy mildew and two quantitative trait loci for resistance to anthracnose were positioned onto the reference map to provide a global view of the genomic architecture of disease resistance in lettuce and to identify candidate genes for resistance phenotypes. The majority but not all of the resistance phenotypes were genetically associated with RGCs.

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  1. Albar L, Bangratz-Reyser M, Hebrard E, Ndjiondjop MN, Jones M, Ghesquiere A (2006) Mutations in the eIF(iso)4G translation initiation factor confer high resistance of rice to rice yellow mottle virus. Plant J 47:417–426

  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

  3. Anonymous (2007) Crop values, 2006 summary. National Agricultural Statistics Service, USDA.

  4. Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer EL (2002) The Pfam protein families’ database. Nucleic Acids Res 30:276–280

  5. Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, Leung J, Staskawicz BJ (1994) RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265:1856–1860

  6. Belkhadir Y, Subramaniam R, Dangl JL (2004) Plant disease resistance protein signaling NBS-LRR proteins and their partners. Curr Opin Plant Biol 7:391–399

  7. Berardini TZ, Mundodi S, Reiser L, Huala E, Garcia-Hernandez M, Zhang P, Mueller LA, Yoon J, Doyle A, Lander G, Moseyko N, Yoo D, Xu I, Zoeckler B, Montoya M, Miller N, Weems D, Rhee SY (2004) Functional annotation of the Arabidopsis genome using controlled vocabularies. Plant Physiol 135:745–755

  8. Bernatsky R, Tanksley SD (1986) Genetics of actin-related sequences in tomato. Theor Appl Genet 72:314–321

  9. Bhattacharyya MK, Narayanan NN, Gao H, Santra DK, Salimath SS, Kasuga T, Liu Y, Espinosa B, Ellison L, Marek L, Shoemaker R, Gijzen M, Buzzell RI (2005) Identification of a large cluster of coiled coil-nucleotide binding site-leucine rich repeat-type genes from the Rps1 region containing Phytophthora resistance genes in soybean. Theor Appl Genet 111:75–86

  10. Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, Dangl JL, Weigel D (2007) Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLoS Biol 5:e236

  11. Burlat V, Kwon M, Davin LB, Lewis NG (2001) Dirigent proteins and dirigent sites in lignifying tissues. Phytochemistry 57:883–897

  12. Buschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Diergaarde P, Groenendijk J, Topsch S, Vos P, Salamini F, Schulze-Lefert P (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695–705

  13. Büttner M, Singh KB (1997) Arabidopsis thaliana ethylene-responsive element binding protein (AtEBP), an ethylene-inducible, GCC box DNA-binding protein interacts with an ocs element binding protein. Proc Natl Acad Sci USA 94:5961–5966

  14. Calenge F, Van der Linden CG, Van de Weg E, Schouten HJ, Van Arkel G, Denancé C, Durel CE (2005) Resistance gene analogues identified through the NBS-profiling method map close to major genes and QTL for disease resistance in apple. Theor Appl Genet 110:660–668

  15. Chin DB, Arroyo-Garcia R, Ochoa OE, Kesseli RV, Lavelle DO, Michelmore RW (2001) Recombination and spontaneous mutation at the major cluster of resistance genes in lettuce (Lactuca sativa). Genetics 157:831–849

  16. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

  17. Crute IR, Pink D (1996) Genetics and utilization of pathogen resistance in plants. Plant Cell 8:1747–1755

  18. Datta K, Baisakh N, Thet KM, Tu J, Datta SK (2002) Pyramiding transgenes for multiple resistance in rice against bacterial blight, yellow stem borer and sheath blight. Theor Appl Genet 106:1–8

  19. Davis RM, Subbarao KV, Raid RN, Kurtz EA (1997) Compendium of lettuce diseases. APS Press, St Paul

  20. Deslandes L, Olivier J, Theulieres F, Hirsch J, Feng DX, Bittner-Eddy P, Beynon J, Marco Y (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 99:2404–2409

  21. Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, Boucher C, Somssich I, Genin S, Marco Y (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 100:8024–8029

  22. Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CI, Ayliffe MA, Kobe B, Ellis JG (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 103:8888–8893

  23. Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763

  24. Felsenstein J (2004) PHYLIP (Phylogeny Inference Package) version 3.6 distributed by the author. Department of Genome Sciences. University of Washington, Seattle

  25. Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis-2001 status. Curr Opin Plant Biol 4:301–308

  26. Godiard L, Sauviac L, Torii KU, Grenon O, Mangin B, Grimsley NH, Marco Y (2003) ERECTA, an LRR receptor-like kinase protein controlling development pleitropically affects resistance to bacterial wilt. Plant J 36:353–365

  27. Gomi K, Yamamato H, Akimitsu K (2003) Epoxide hydrolase: a mRNA induced by the fungal pathogen Alternaria alternata on rough lemon (Citrus jambhiri Lush). Plant Mol Biol 53:189–199

  28. Grant SR, Fisher EJ, Chang JH, Mole BM, Dangl JL (2006) Subterfuge and manipulation: type III effector proteins of phytopathogenic bacteria. Annu Rev Microbiol 60:425–429

  29. Grube RC, Radwanski ER, Jahn M (2000) Comparative genetics of disease resistance within the solanaceae. Genetics 155:873–887

  30. Grube RC, Wintermantel WM, Hand P, Aburomia R, Pink DA, Ryder EJ (2005) Genetic analysis and mapping of resistance to lettuce dieback: a soilborne disease caused by tombusviruses. Theor Appl Genet 110:259–268

  31. Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877

  32. Hulbert SH, Michelmore RW (1985) Linkage analysis of genes for resistance to downy mildew (Bremia lactucae) in lettuce (Lactuca sativa). Theor Appl Genet 70:520–528

  33. Iyer-Pascuzzi AS, McCouch SR (2007) Recessive resistance genes and the Oryza sativaXanthomonas oryzae pv. oryzae pathosystem. Mol Plant Microbe Interact 20:731–739

  34. Jain A, Ariyadasa R, Kumar A, Srivastava MN, Mohan M, Nair S (2004) Tagging and mapping of a rice gall midge resistance gene, Gm8, and development of SCARs for use in marker-aided selection and gene pyramiding. Theor Appl Genet 109:1377–1384

  35. Jeuken MJ, Lindhout P (2002) Lactuca saligna, a non-host for lettuce downy mildew (Bremia lactucae), harbors a new race-specific Dm gene and three QTLs for resistance. Theor Appl Genet 105:384–391

  36. 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

  37. Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

  38. 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 266:789–793

  39. Kanazin V, Marek LF, Shoemaker RC (1996) Resistance gene analogs are conserved and clustered in soybean. Proc Natl Acad Sci USA 93:11746–11750

  40. Kesseli RV, Witsenboer H, Stanghellini M, Vandermark G, Michelmore RW (1993) Recessive resistance to Plasmopara lactucae-radicis is mapped by bulked segregant analysis to a cluster of dominant disease resistance genes in lettuce. Mol Plant Microbe Interact 6:722–728

  41. Kesseli RV, Paran I, Michelmore RW (1994) Analysis of a detailed genetic linkage map of Lactuca sativa (lettuce) constructed from RFLP and RAPD markers. Genetics 136:1435–1446

  42. Kuang H, van Eck HJ, Sicard D, Michelmore RW, Nevo E (2008) Evolution and genetic population structure of prickly lettuce (Lactuca serriola) and its RGC2 resistance gene cluster. Genetics 178:1547–1558

  43. Lalli DA, Decroocq V, Blenda AV, Schurdi-Levraud V, Garay L, Le Gall O, Damsteegt V, Reighard GL, Abbott AG (2005) Identification and mapping of resistance gene analogs (RGAs) in Prunus: a resistance map for Prunus. Theor Appl Genet 111:1504–1513

  44. Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

  45. Landry BS, Kesseli RV, Farrara B, Michelmore RW (1987) A genetic map of lettuce (Lactuca sativa L.) with restriction fragment length polymorphism, isozyme, disease resistance and morphological markers. Genetics 116:331–337

  46. Lein JC, Asbach K, Tian Y, Schulte D, Li C, Koch G, Jung C, Cai D (2007) Resistance gene analogues are clustered on chromosome 3 of sugar beet and cosegregate with QTL for rhizomania resistance. Genome 50:61–71

  47. 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 Genomics 34:765–776

  48. Lopez CE, Zuluaga AP, Cooke R, Delseny M, Tohme J, Verdier V (2003) Isolation of resistance gene candidates (RGCs) and characterization of an RGCs cluster in cassava. Mol Genet Genomics 269:658–671

  49. Llorente F, Alonso-Blanco C, Sánchez-Rodriguez C, Jorda L, Molina A (2005) ERECTA receptor-like kinase and heterotrimeric G protein from Arabidopsis are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina. Plant J 43:165–180

  50. 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 108:743–754

  51. Maisonneuve B, Bellec Y, Anderson P, Michelmore RW (1994) Rapid mapping of two genes for resistance to downy mildew from Lactuca serriola to existing cluster of resistance genes. Theor Appl Genet 89:96–104

  52. Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earle ED, Tanksley SD (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–1436

  53. McHale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212

  54. 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

  55. 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

  56. 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

  57. Michelmore RW (1995) Molecular approaches to manipulation of disease resistance genes. Ann Rev Phytopathol 15:393–427

  58. Michelmore RW (2003) The impact zone: genomics and breeding for durable disease resistance. Curr Opin Plant Biol 6:397–404

  59. Montesclaros L, Nicol N, Ubalijora E, Leclerc-Potvin C, Ganivet L, Laliberte JF, Fortin MG (1997) Response to potyvirus infection and genetic mapping of resistance loci to potyvirus infection in Lactucae. Theor Appl Genet 94:941–946

  60. Moreno-Vazquez S, Ochoa OE, Faber N, Chao S, Jacobs JM, Maisonneuve B, Kesseli RV, Michelmore RW (2003) SNP-based codominant markers for a recessive gene conferring resistance to corky root rot (Rhizomonas suberifaciens) in lettuce (Lactuca sativa). Genome 46:1059–1069

  61. Naik S, Hampson C, Gasic K, Bakkeren G, Korban SS (2006) Development and linkage mapping of E-STS and RGA markers for functional gene homologues in apple. Genome 49:959–968

  62. Nicaise V, German-Retana S, Sanjuan R, Dubrana MP, Mazier M, Maisonneuve B, Candresse T, Caranta C, LeGall O (2003) The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the potyvirus lettuce mosaic virus. Plant Physiol 132:1272–1282

  63. Nieto C, Morales M, Orjeda G, Clepet C, Monfort A, Sturbois B, Puigdomenech P, Pitrat M, Caboche M, Dogimont C, Garcia-Mas J, Aranda MA, Bendahmane A (2006) An eIF4E allele confers resistance to an uncapped and non-polyadenylated RNA virus in melon. Plant J 48:452–462

  64. Ochoa O, Delp B, Michelmore RW (1987) Resistance in Lactuca spp. to Microdochium panattoniana (lettuce anthracnose). Euphytica 36:609–614

  65. Overmyer K, Tuominen H, Kettunen R, Betz C, Langebartels C, Sandermann H Jr, Kangasjärvi J (2000) Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell 12:1849–1862

  66. Paal J, Henselewski H, Muth J, Meksem K, Menendez CM, Salamini F, Ballvora A, Gebhardt C (2004) Molecular cloning of the potato Gro1-4 gene conferring resistance to pathotype Ro1 of the root cyst nematode Globodera rostochiensis, based on a candidate gene approach. Plant J 38:285–297

  67. Pan Q, Liu Y-S, Budai-Hadrian O, Sela M, Carmel-Goren L, Zamir D, Fluhr R (2000) Comparative genetics of nucleotide binding site-leucine rich repeat resistance gene homologues in the genomes of two dicotyledons: tomato and Arabidopsis. Genetics 155:309–322

  68. Panstruga R (2005) Serpentine plant MLO proteins as entry portals for powdery mildew fungi. Biochem Soc Trans 33:389–392

  69. Paran I, Kesseli R, Michelmore R (1991) Identification of restriction fragment length polymorphism and random amplified polymorphic DNA markers linked to downy mildew resistance genes in lettuce, using near-isogenic lines. Genome 34:1021–1027

  70. Plocik A, Layden J, Kesseli R (2004) Comparative analysis of NBS domain sequences of NBS-LRR disease resistance genes from sunflower, lettuce, and chicory. Mol Phylogenet Evol 31:153–163

  71. Radwan O, Gandhi S, Heesacker A, Whitaker B, Taylor C, Plocik A, Kesseli R, Kozik A, Michelmore RW, Knapp SJ (2008) Genetic diversity and genomic distribution of homologs encoding NBS-LRR disease resistance proteins in sunflower. Mol Genet Genomics. Epub ahead of print

  72. Ramalingam J, Vera Cruz CM, Kukreja K, Chittoor JM, Wu JL, Lee SW, Baraoidan M, George ML, Cohen MB, Hulbert SH, Leach JE, Leung H (2003) Candidate defense genes from rice, barley, and maize and their association with qualitative and quantitative resistance in rice. Mol Plant Microbe Interact 16:14–24

  73. Ren C, Pan J, Peng W, Genschik P, Hobbie L, Hellmann H, Estelle M, Gao B, Peng J, Sun C, Xie D (2005) Point mutations in Arabidopsis Cullin1 reveal its essential role in jasmonate response. Plant J 42:514–524

  74. Robaglia C, Caranta C (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11:40–45

  75. Ronald PC, Albano B, Tabien R, Abenes L, Wu KS, McCouch S, Tanksley SD (1992) Genetic and physical analysis of the rice bacterial blight disease resistance locus, Xa21. Mol Gen Genet 236:113–120

  76. Rooney HC, Van’t Klooster JW, van der Hoorn RA, Joosten MH, Jones JD, de Wit PJ (2005) Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308:1783–1786

  77. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386

  78. Ruffel S, Gallois JL, Moury B, Robaglia C, Palloix A, Caranta C (2006) Simultaneous mutations in translation initiation factors eIF4E and eIF(iso)4E are required to prevent pepper veinal mottle virus infection of pepper. J Gen Virol 87:2089–2098

  79. Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW (2003) Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301:1230–1233

  80. Shen KA, Meyers BC, Islam-Faridi MN, Chin DB, Stelly DM, Michelmore RW (1998) Resistance gene candidates identified using PCR with degenerate primers map to resistance genes clusters in lettuce. Mol Plant Microbe Interact 11:815–823

  81. Shen KA, Chin DB, Arroyo-Garcia R, Ochoa OE, Lavelle DO, Wroblewski T, Meyers BC, Michelmore RW (2002) Dm3 is one member of a large constitutively expressed family of nucleotide binding site-leucine-rich repeat encoding genes. Mol Plant Microbe Interact 15:251–261

  82. Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806

  83. Stam P, Van Ooijen JW (1995) Joinmap version 2.0: software for the calculation of genetic linkage maps. Plant Res Int

  84. Tan X, Meyers BC, Kozik A, West MA, Morgante M, St Clair DA, Bent AF, Michelmore RW (2007) Global expression analysis of nucleotide binding site-leucine rich repeat-encoding and related genes in Arabidopsis. BMC Plant Biol 7:56

  85. Thomas CM, Dixon MS, Parniske M, Golstein C, Jones JD (1998) Genetic and molecular analysis of tomato Cf genes for resistance to Cladosporium fulvum. Philos Trans R Soc Lond B Biol Sci 353:1413–1424

  86. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

  87. Timms L, Jimenez R, Chase M, Lavelle D, McHale L, Kozik A, Lai Z, Heesacker A, Knapp S, Rieseberg L, Michelmore R, Kesseli R (2006) Analyses of synteny between Arabidopsis thaliana and species in the Asteraceae reveal a complex network of small syntenic segments and major chromosomal rearrangements. Genetics 173:2227–2235

  88. Truco MJ, Antonise R, Lavelle D, Ochoa O, Kozik A, Witsenboer H, Fort SB, Jeuken MJ, Kesseli RV, Lindhout P, Michelmore RW, Peleman J (2007) A high-density, integrated genetic linkage map of lettuce (Lactuca spp.). Theor Appl Genet 115:735–746

  89. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

  90. Wang S, Basten CJ, Zeng ZB (2005) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh.

  91. Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B (1994) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78:1101–1115

  92. Wroblewski T, Tomczak A, Michelmore RW (2005) Optimization of Agrobacterium-mediated transient assays of gene expression in lettuce, tomato and Arabidopsis. Plant Biotechnol J 3:259–273

  93. Wroblewski T, Piskurewicz U, Tomczak A, Ochoa O, Michelmore R (2007) Silencing of the major family of NBS-LRR-encoding genes in lettuce results in the loss of multiple resistance specificities. Plant J 51:803–818

  94. Zhang LP, Khan A, Nino-Liu D, Foolad MR (2002) A molecular linkage map of tomato displaying chromosomal locations of resistance gene analogs based on a Lycopersicon esculentum × Lycopersicon hirsutum cross. Genome 45:133–146

  95. Zhang Z, Ober JA, Kliebenstein DJ (2006) The gene controlling the quantitative trait locus EPITHIOSPECIFIER MODIFIER1 alters glucosinolate hydrolysis and insect resistance in Arabidopsis. Plant Cell 18:1524–1536

  96. 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 15:529–539

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We thank Dean Lavelle, Robert Kays, and Amy Turnquist for technical assistance. This research was supported by Grant no. 04-35300-14601 from the National Research Initiative (NRI) Plant Genome Program of the USDA Cooperative State Research, Education and Extension Service (CSREES) and by awards DBI0421630 and DBI0211923 from the Plant Genome Program of the National Science Foundation.

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Correspondence to Richard W. Michelmore.

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An erratum to this article can be found at

Communicated by M. Xu.

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McHale, L.K., Truco, M.J., Kozik, A. et al. The genomic architecture of disease resistance in lettuce. Theor Appl Genet 118, 565–580 (2009).

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  • Downy Mildew
  • Resistance Phenotype
  • Nucleotide Binding Site
  • Downy Mildew Resistance
  • Recessive Resistance