Molecular Genetics and Genomics

, Volume 280, Issue 2, pp 111–125

Genetic diversity and genomic distribution of homologs encoding NBS-LRR disease resistance proteins in sunflower

  • Osman Radwan
  • Sonali Gandhi
  • Adam Heesacker
  • Brett Whitaker
  • Chris Taylor
  • Alex Plocik
  • Richard Kesseli
  • Alexander Kozik
  • Richard W. Michelmore
  • Steven J. Knapp
Original Paper


Three-fourths of the recognition-dependent disease resistance genes (R-genes) identified in plants encode nucleotide binding site (NBS) leucine-rich repeat (LRR) proteins. NBS-LRR homologs have only been isolated on a limited scale from sunflower (Helianthus annuus L.), and most of the previously identified homologs are members of two large NBS-LRR clusters harboring downy mildew R-genes. We mined the sunflower EST database and used comparative genomics approaches to develop a deeper understanding of the diversity and distribution of NBS-LRR homologs in the sunflower genome. Collectively, 630 NBS-LRR homologs were identified, 88 by mining a database of 284,241 sunflower ESTs and 542 by sequencing 1,248 genomic DNA amplicons isolated from common and wild sunflower species. DNA markers were developed from 196 unique NBS-LRR sequences and facilitated genetic mapping of 167 NBS-LRR loci. The latter were distributed throughout the sunflower genome in 44 clusters or singletons. Wild species ESTs were a particularly rich source of novel NBS-LRR homologs, many of which were tightly linked to previously mapped downy mildew, rust, and broomrape R-genes. The DNA sequence and mapping resources described here should facilitate the discovery and isolation of recognition-dependent R-genes guarding sunflower from a broad spectrum of economically important diseases.


Helianthus Lactuca Compositae Resistance genes 


  1. Altschul SF, Madden TL, Schaffer AA, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  2. Ameline-Torregrosa C, Wang BB, O’Bleness MS, Deshpande S, Zhu H, Roe B, Young ND, Cannon SB (2007) Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula. Plant Physiol 146:5–21PubMedCrossRefGoogle Scholar
  3. Ashfield T, Ong LE, Nobuta K, Schneider CM, Innes R (2004) Convergent evolution of disease resistance gene specificity in two flowering plant families. Plant Cell 16:309–318PubMedCrossRefGoogle Scholar
  4. Baack EJ, Whitney KD, Rieseberg LH (2005) Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species. New Phytol 167:623–630PubMedCrossRefGoogle Scholar
  5. Bai J, Pennill LA, Ning J, Lee SW, Ramalingam J, Webb CA, Zhao B, Sun Q, Nelson JC, Leach JE, Hulbert SH (2002) Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res 12:1871–1884PubMedCrossRefGoogle Scholar
  6. Bassam BJ, Caetano-Anollés G, Gresshoff PM (1991) Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal Biochem 196:80–83PubMedCrossRefGoogle Scholar
  7. Bent AF (1996) Plant disease resistance genes: function meets structure. Plant Cell 8:1757–1771PubMedCrossRefGoogle Scholar
  8. Bert PF, Labrouhe DTD, Philippon J, Mouzeyar S, Jouan I, Nicolas P, Vear F (2001) Identification of a second linkage group carrying genes controlling resistance to downy mildew (Plasmopara halstedii) in sunflower (Helianthus annuus L.). Theor Appl Genet 103:992–997CrossRefGoogle Scholar
  9. Bouzidi MF, Badaoui S, Cambon F, Vear F, De Labrouhe DT, Nicolas P, Mouzeyar S (2002) Molecular analysis of a major locus for resistance to downy mildew in sunflower with specific PCR-based markers. Theor Appl Genet 104:592–600PubMedCrossRefGoogle Scholar
  10. Cannon SB, Shu 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 54:548–562PubMedCrossRefGoogle Scholar
  11. 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 157:831–849PubMedGoogle Scholar
  12. Clamp M, Cuff J, Searle SM, Barton GJ (2004) The Jalview Java alignment editor. Bioinformatics 20:426–427PubMedCrossRefGoogle Scholar
  13. Collins NC, Webb CA, Seah S, Ellis JG, Hulbert SH, Pryor A (1998) The isolation and mapping of disease resistance gene analogs in maize. Mol Plant Microbe Interact 11:968–978PubMedCrossRefGoogle Scholar
  14. Dangl JL, Jones JDG (2001) Plant pathogens and integrated defense responses to infection. Nature 411:826–833PubMedCrossRefGoogle Scholar
  15. Degener J, Melchinger AE, Hahn V (1999) Interspecific hybrids as source of resistance to Sclerotinia and Phomopsis in sunflower breeding. Helia 22:49–60Google Scholar
  16. Don RH, Cox PT, Wainwright BJ, Baker K, Mattick JS (1991) ‘Touchdown’ PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res 19:4008PubMedCrossRefGoogle Scholar
  17. Dußle CM, Hahn V, Knapp SJ, Bauer E (2004) Pl Arg from Helianthus argophyllus is unlinked to other known downy mildew resistance genes in sunflower. Theor Appl Genet 109:1083–1086PubMedCrossRefGoogle Scholar
  18. Ellis J, Dodds P, Pryor T (2000) The generation of plant disease resistance gene specificities. Trends Plant Sci 5:373–379PubMedCrossRefGoogle Scholar
  19. Gandhi SD, Heesacker AF, Freeman CA, Argyris J, Bradford K, Knapp SJ (2005) The self-incompatibility locus (S) and quantitative trait loci for self-pollination and seed dormancy in sunflower. Theor Appl Genet 111:619–629PubMedCrossRefGoogle Scholar
  20. Gedil MA, Slabaugh MB, Berry S, Johnson R, Michelmore R, Miller J, Gulya T, Knapp SJ (2001) Candidate disease resistance genes in sunflower cloned using conserved nucleotide-binding site motifs: genetic mapping and linkage to the downy mildew resistance gene Pl1. Genome 44:205–212PubMedCrossRefGoogle Scholar
  21. Gentzbittel L, Mouzeyar S, Badaoui S, Mestries E, Vear F, Tourvieille de Labrouhe D, Nicolas P (1998) Cloning of molecular markers for disease resistance in sunflower, Helianthus annuus L. Theor Appl Genet 96:519–525CrossRefGoogle Scholar
  22. Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:79–92CrossRefGoogle Scholar
  23. Gonzales MD, Archuleta E, Farmer A, Gajendran K, Grant D, Shoemaker R, Beavis WD, Waugh ME (2005) The Legume Information System (LIS): an integrated information resource for comparative legume biology. Nucleic Acids Res 33:D660–D665PubMedCrossRefGoogle Scholar
  24. Hammond-Kosack KE, Jones JDG (1997) Plant disease resistance genes. Ann Rev Plant Phys Plant Mol Biol 48:575–607CrossRefGoogle Scholar
  25. He L, Du C, Covaleda L, Xu Z, Robinson AF, Yu JZ, Kohel RJ, Zhang HB (2004) Cloning, characterization, and evolution of the NBS-LRR-encoding resistance gene analogue family in polyploid cotton (Gossypium hirsutum L.). Mol Plant Microbe Interact 17:1234–1241PubMedCrossRefGoogle Scholar
  26. Hecker KH, Roux KH (1996) High and low annealing temperatures increase both specificity and yield in touchdown and stepdown PCR. Biotechniques 20:478–485PubMedGoogle Scholar
  27. Holt BF, Hubert DA, Dangl JL (2003) Resistance gene signaling in plants: complex similarities to animal innate immunity. Curr Opin Immunol 15:20–25PubMedCrossRefGoogle Scholar
  28. Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes: evolution and utilization. Ann Rev Phytopathol 39:285–312CrossRefGoogle Scholar
  29. Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedCrossRefGoogle Scholar
  30. Kanazin V, Marek LF, Shoemaker RC (1996) Resistance gene analogs are conserved and clustered in soybean. Proc Natl Acad Sci USA 93:11746–11750PubMedCrossRefGoogle Scholar
  31. Kohler A, Rinaldi C, Duplessis S, Baucher M, Geelen D, Duchaussoy F, Meyers BC, Boerjan W, Martin F (2008) Genome-wide identification of NBS resistance genes in Populus trichocarpa. Plant Mol Biol 66:619–636PubMedCrossRefGoogle Scholar
  32. 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
  33. Kukita Y, Tahira T, Sommer SS, Hayashi K (1997) SSCP analysis of long DNA fragments in low pH gel. Hum Mutat 10:400–407PubMedCrossRefGoogle Scholar
  34. 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 25:511–557Google Scholar
  35. Langar K, Griveau Y, Kaan F, Serieys H, Varès D, Bervillé A (2002) Evaluation of parameters accounting for Phomopsis resistance using natural infection and artificial inoculation on recombinant inbred lines from a cross between susceptible and resistant sunflower. Eur J Plant Path 108:307–315CrossRefGoogle Scholar
  36. Larsen LA, Christiansen M, Vuust J, Andersen PS (1999) High-throughput single-strand conformation polymorphism analysis by automated capillary electrophoresis: robust multiplex analysis and pattern-based identification of allelic variants. Hum Mutat 13:318–327PubMedCrossRefGoogle Scholar
  37. Larsen LA, Jespersgaard C, Andersen PS (2007) Single-strand conformation polymorphism analysis using capillary array electrophoresis for large-scale mutation detection. Nat Protoc 2:1458–1466PubMedCrossRefGoogle Scholar
  38. 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
  39. Lawson RR, Goulter KC, Henry RJ, Kong GA, Kochman JK (1998) Marker-assisted selection for two rust resistance genes in sunflower. Mol Breed 4:227–234CrossRefGoogle Scholar
  40. Lee SY, Seo JS, Rodriguez-Lanetty M (2003) Comprative analysis of superfamilies of NBS-encoding disease resistance gene analogs in cultivated and wild apple species. Mol Gen Genomics 269:101–108Google Scholar
  41. 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
  42. Leister D, Kurth J, Laurie DA, Yano M, Sasaki T, Devos K, Graner A, Schulze-Lefert P (1998) Rapid reorganization of resistance gene homologues in cereal genomes. Proc Natl Acad Sci USA 95:370–375PubMedCrossRefGoogle Scholar
  43. Lenardon SL, Bazzalo ME, Abratti G, Cimmino CJ, Galella MT, Grondona M, Giolitti F, Leon AJ (2005) Screening sunflower for resistance to sunflower chlorotic mottle virus and mapping the Rcmo-1 resistance gene. Crop Sci 45:735–739Google Scholar
  44. Lincoln SE, Lander ES (1992) Systematic detection of errors in genetic linkage data. Genomics 14:604–610PubMedCrossRefGoogle Scholar
  45. Madsen LH, Collins NC, Rakwalska M, Backes G, Sandal N, Krusell L, Jensen J, Waterman EH, Jahoor A, Ayliffe M, Pryor AJ, Langridge P, Schulze-Lefert P, Stougaard J (2003) Barley disease resistance gene analogs of the NBS-LRR class: identification and mapping. Mol Genet Genomics 269:150–161PubMedGoogle Scholar
  46. McDowell JM, Dhandaydham M, Long TA, Aarts MG, Goff S, Holub EB, Dangl JL (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
  47. McHale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212PubMedCrossRefGoogle Scholar
  48. Meyers BC, Shen KA, Rohani P, Gaut BS, Michelmore RW (1998a) Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell 10:1833–1846PubMedCrossRefGoogle Scholar
  49. Meyers BC, Chin DB, Shen KA, Sivaramakrishnan S, Lavelle DO, Zhang Z, Michelmore RW (1998b) The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell 10:1817–1832PubMedCrossRefGoogle Scholar
  50. 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 20:317–332PubMedCrossRefGoogle Scholar
  51. 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
  52. Meyers BC, Kozik A, Griego A, Kuang H, Michelomore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834PubMedCrossRefGoogle Scholar
  53. Michelmore RW (2003) The impact zone: genomics and breeding for durable disease resistance. Curr Opin Plant Biol 6:397–404PubMedCrossRefGoogle Scholar
  54. 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
  55. Miller JF, Gulya TJ (1988) Registration of six downy mildew resistant sunflower germplasm lines. Crop Sci 28:1040–1041Google Scholar
  56. Miller JF, Gulya TJ (1991) Inheritance of resistance to race 4 of downy mildew derived from interspecific cross in sunflower. Crop Sci 31:40–43Google Scholar
  57. Miller JF, Gulya TJ, Seiler GJ (2002) Registration of five fertility restorer sunflower germplasms. Crop Sci 42:989Google Scholar
  58. Murray MG, Thompson WR (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325PubMedCrossRefGoogle Scholar
  59. Noel L, Moores TL, van Der Biezen EA, Parniske M, Daniels MJ, Parker JE, Jones JD (1999) Pronounced intraspecific haplotype divergence at RPP5 complex disease resistance locus of Arabidopsis. Plant Cell 11:2099–2112PubMedCrossRefGoogle Scholar
  60. Noir S, Combes MC, Anthony F, Lashermes P (2001) Origin, diversity and evolution of NBS-type disease-resistance gene homologues in coffee trees (Coffea L.). Mol Gent Genomics 265:654–662CrossRefGoogle Scholar
  61. Orita M, Iwahana H, Kanazawa H, Hayashi K, Sekiya T (1989) Detection of polymorphisms of human DNA by gel electrophoresis as single-strand conformation polymorphisms. Proc Natl Acad Sci USA 86:2766–2770PubMedCrossRefGoogle Scholar
  62. Pan Q, Liu YS, 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 155:309–222PubMedGoogle Scholar
  63. Parker C, Riches CR (1993) Parasitic weeds of the world: biology and control. CAB Int, WallingfordGoogle Scholar
  64. 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 91:821–832PubMedCrossRefGoogle Scholar
  65. Pérez-Vich B, Akhtouch B, Knapp SJ, Leon AJ, Velasco L, Fernández-Martínez JM, Berry ST (2004) Quantitative trait loci for broomrape (Orobanche cumana Wallr.) resistance in sunflower. Theor Appl Genet 109:92–102PubMedCrossRefGoogle Scholar
  66. 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 Phylogen Evol 31:153–163CrossRefGoogle Scholar
  67. Pustovoit GV, Kroknin EY (1978) Inheritance of resistance in interspecific hybrids of sunflower to downy mildew. Rev Plant Pathol 57:209Google Scholar
  68. Quresh Z, Jan CC, Gulya TJ (1993) Resistance of sunflower rust and its inheritance in wild sunflower species. Plant Breed 110:297–306CrossRefGoogle Scholar
  69. Radwan O, Bouzidi MF, Vear F, Philippon J, Tourvieille de Labrouhe D, Nicolas P, Mouzeyar S (2003) Identification of non-TIR-NBS-LRR markers linked to PL5/PL8 locus for resistance to downy mildew in sunflower. Theor Appl Genet 106:1438–1446PubMedGoogle Scholar
  70. Radwan O, Bouzidi MF, Nicolas P, Mouzeyar S (2004) Development of PCR markers for the Pl5/ Pl8 locus for resistance to Plasmopara halstedii in sunflower, Helianthus annuus L. from complete CC-NBS-LRR sequences. Theor Appl Genet 109:176–185PubMedCrossRefGoogle Scholar
  71. 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
  72. Rossi M, Araujo PG, Paulet F, Garsmeur O, Dias VM, Chen H, Van Sluys MA, D’Hont A (2003) Genomic distribution and characterization of EST-derived resistance gene analogs (RGAs) in sugarcane. Mol Genet Genomics 269:406–419PubMedCrossRefGoogle Scholar
  73. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  74. Seiler GJ (1991a) Registration of 15 interspecific sunflower germplasm lines derived from wild annual species. Crop Sci 31:1389–1390Google Scholar
  75. Seiler GJ (1991b) Registration of 13 downy mildew tolerant interspecific sunflower germplasm lines derived from wild annual species. Crop Sci 31:1714–1716Google Scholar
  76. Shen KA, Keyers BC, Islam-Faridi MN, Chin DB, Stelly DM, Michelmore RW (1998) Resistance gene candidate identified by PCR with degenerate oligonucleotide primers map to clusters of resistance genes in lettuce. Mol Plant Microbe Interact 11:815–823PubMedCrossRefGoogle Scholar
  77. Škoric D (1985) Sunflower breeding for resistance to Diaporthe/Phomopsis helianthi. Helia 8:21–23Google Scholar
  78. Slabaugh MB, Yu JK, Tang S, Heesacker A, Hu X, Lu G, Han F, Bidney D, Knapp SJ (2003) Haplotyping and mapping a large cluster of resistance gene candidates in sunflower using multilocus intron fragment length polymorphisms. Plant Biotech J 1:167–185CrossRefGoogle Scholar
  79. Sun Q, Collins NC, Ayliffe M, Smith SM, Drake J, Pryor T, Hulbert SH (2001) Recombination between paralogues at the Rp1 rust resistance locus in maize. Genetics 158:423–438PubMedGoogle Scholar
  80. Tan AS, Jan CC, Gulya TJ (1992) Inheritance of resistance to race 4 of sunflower downy mildew in wild sunflower accessions. Crop Sci 32:949–952Google Scholar
  81. Tang S, Yu JK, Slabaugh MB, Shintani DK, Knapp SJ (2002) Simple sequence repeat map of the sunflower genome. Theor Appl Genet 105:1124–1136PubMedCrossRefGoogle Scholar
  82. Tang S, Heesacker A, Kishore VK, Fernandez A, Sadik E, Cole G, Knapp SJ (2003) Genetic mapping of the Or5 gene for resistance to Orobanche race E in sunflower. Crop Sci 43:1021–1028Google Scholar
  83. Tanksley SD, McCouch S (1997) Seed banks and molecular maps: unlocking the genetic potential from the wild. Science 277:1063–1066PubMedCrossRefGoogle Scholar
  84. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgens DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  85. Vear F, De Labrouhe DT, Miller JF (2003) Inheritance of the wide-range downy mildew resistance in the sunflower line RHA 419. Helia 26:19–24CrossRefGoogle Scholar
  86. Vranceanu AV, Tudor VA, Stoenescu FM, Pirvu N (1980) Virulence groups of Orobanche cumana Wallr., different hosts and resistance sources and genes in sunflower. In: Proceedings of the 9th International Sunflower Conference, Torremolinos, Spain, pp 74–82Google Scholar
  87. Viguié A, Labrouhe DTD, Vear F (2000) Inheritance of several sources of resistance to Phomopsis stem canker (Diaporthe helianthi Munt.-Cvet.) in sunflower (Helianthus annuus L.). Euphytica 116:167–179CrossRefGoogle Scholar
  88. Wang Z, Taramino G, Yang D, Liu G, Tingey SV, Miao GH, Wang GL (2001) Rice ESTs with disease-resistance gene or defense-response gene-like sequences mapped to regions containing major resistance genes or QTLs. Mol Gen Genet 265:302–310Google Scholar
  89. Wei FS, Wong RA, Wise RP (2002) Genome dynamics and evolution of the Mla (powdery mildew) resistance locus in barley. Plant Cell 14:1903–1917PubMedCrossRefGoogle Scholar
  90. Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B (1994) The product of tobacco mosaic virus resistance gene N: similarity to Toll and interleukin-1 receptor. Cell 78:1101–1115PubMedCrossRefGoogle Scholar
  91. Yu T, Buss GR, Saghai-Maroof MA (1996) Isolation of the 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
  92. Yu JK, Tang S, Slabaugh MB, Heesacker AF, Cole G, Herring M, Soper J, Han F, Chu WC, Webb DM, Thompson L, Edwards KJ, Berry ST, León AJ, Olungu C, Maes N, Knapp SJ (2003) Towards a saturated molecular genetic linkage map for cultivated sunflower. Crop Sci 43:367–387Google Scholar
  93. 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 15:529–539PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Osman Radwan
    • 1
    • 2
  • Sonali Gandhi
    • 3
  • Adam Heesacker
    • 1
  • Brett Whitaker
    • 1
  • Chris Taylor
    • 1
  • Alex Plocik
    • 4
  • Richard Kesseli
    • 4
  • Alexander Kozik
    • 5
  • Richard W. Michelmore
    • 5
  • Steven J. Knapp
    • 1
  1. 1.Center for Applied Genetic TechnologiesThe University of GeorgiaAthensUSA
  2. 2.Plant Production Department, Efficient Productivity InstituteUniversity of ZagazigSharkiaEgypt
  3. 3.Department of Crop and Soil ScienceOregon State UniversityCorvallisUSA
  4. 4.Department of BiologyUniversity of MassachusettsBostonUSA
  5. 5.Department of Plant Sciences and the Genome CenterUniversity of CaliforniaDavisUSA

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