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

Molecular Genetics and Genomics

Volumn 280, Issue 2, 2008, Pages 111-125

  Radwan, Osman ^a,b   Gandhi, Sonali ^c   Heesacker, Adam ^a   Whitaker, Brett ^a   Taylor, Chris ^a   Plocik, Alex ^d   Kesseli, Richard ^d   Kozik, Alexander ^e   Michelmore, Richard W ^e   Knapp, Steven J ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b ZAGAZIG UNIVERSITY   (Egypt)

^c OREGON STATE UNIVERSITY   (United States)

^d UNIVERSITY OF MASSACHUSETTS BOSTON   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Compositae; Helianthus; Lactuca; Resistance genes

Indexed keywords

DNA MARKER; GENOMIC DNA; LEUCINE; NUCLEOTIDE; PROTEIN;

AMPLICON; ARTICLE; COMPARATIVE STUDY; COMPREHENSION; CONTROLLED STUDY; DATA BASE; DNA SEQUENCE; ECONOMICS; GENE; GENE IDENTIFICATION; GENE LOCUS; GENE MAPPING; GENETIC VARIABILITY; GENOME; GENOMICS; HELIANTHUS ANNUUS; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE BINDING SITE; NUCLEOTIDE SEQUENCE; PLANT; PRIORITY JOURNAL; SPECIES; SUNFLOWER; UNINDEXED SEQUENCE;

AMINO ACID SEQUENCE; BASE SEQUENCE; CHROMOSOME MAPPING; CONSERVED SEQUENCE; DATABASES, NUCLEIC ACID; DNA, PLANT; EXPRESSED SEQUENCE TAGS; FUNGI; GENOME, PLANT; HELIANTHUS; MOLECULAR SEQUENCE DATA; OOMYCETES; PHYLOGENY; PLANT DISEASES; PLANT PROTEINS; VARIATION (GENETICS);

ASTERACEAE; HELIANTHUS; HELIANTHUS ANNUUS; LACTUCA; OROBANCHACEAE; PERONOSPORACEAE;

EID: 48349132316     PISSN: 16174615     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00438-008-0346-1     Document Type: Article

References (93)

1. SF Altschul TL Madden AA Schaffer Z Zhang W Miller DJ Lipman 1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res 25 3389 3402
2. C Ameline-Torregrosa BB Wang MS O'Bleness S Deshpande H Zhu B Roe ND Young SB Cannon 2007 Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula Plant Physiol 146 5 21
3. T Ashfield LE Ong K Nobuta CM Schneider R Innes 2004 Convergent evolution of disease resistance gene specificity in two flowering plant families Plant Cell 16 309 318
4. EJ Baack KD Whitney LH Rieseberg 2005 Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species New Phytol 167 623 630
5. J Bai LA Pennill J Ning SW Lee J Ramalingam CA Webb B Zhao Q Sun JC Nelson JE Leach SH Hulbert 2002 Diversity in nucleotide binding site-leucine-rich repeat genes in cereals Genome Res 12 1871 1884
6. BJ Bassam G Caetano-Anollés PM Gresshoff 1991 Fast and sensitive silver staining of DNA in polyacrylamide gels Anal Biochem 196 80 83
7. AF Bent 1996 Plant disease resistance genes: function meets structure Plant Cell 8 1757 1771
8. PF Bert DTD Labrouhe J Philippon S Mouzeyar I Jouan P Nicolas F Vear 2001 Identification of a second linkage group carrying genes controlling resistance to downy mildew (Plasmopara halstedii) in sunflower (Helianthus annuus L.) Theor Appl Genet 103 992 997
9. MF Bouzidi S Badaoui F Cambon F Vear DT De Labrouhe P Nicolas S Mouzeyar 2002 Molecular analysis of a major locus for resistance to downy mildew in sunflower with specific PCR-based markers Theor Appl Genet 104 592 600
10. SB Cannon H Shu AM Baumgarten R Spangler G May DR Cook ND Young 2002 Diversity, distribution, and ancient taxonomic relationships within the TIR and non-TIR NBS-LRR resistance gene subfamilies J Mol Evol 54 548 562
11. DB Chin R Arroyo-Garcia OE Ochoa RV Kesseli DO Lavelle RW Michelmore 2001 Recombination and spontaneous mutation at the major cluster of resistance genes in lettuce (Lactuca sativa) Genetics 157 831 849
12. M Clamp J Cuff SM Searle GJ Barton 2004 The Jalview Java alignment editor Bioinformatics 20 426 427
13. NC Collins CA Webb S Seah JG Ellis SH Hulbert A Pryor 1998 The isolation and mapping of disease resistance gene analogs in maize Mol Plant Microbe Interact 11 968 978
14. JL Dangl JDG Jones 2001 Plant pathogens and integrated defense responses to infection Nature 411 826 833
15. J Degener AE Melchinger V Hahn 1999 Interspecific hybrids as source of resistance to Sclerotinia and Phomopsis in sunflower breeding Helia 22 49 60
16. RH Don PT Cox BJ Wainwright K Baker JS Mattick 1991 'Touchdown' PCR to circumvent spurious priming during gene amplification Nucleic Acids Res 19 4008
17. Arg from Helianthus argophyllus is unlinked to other known downy mildew resistance genes in sunflower Theor Appl Genet 109 1083 1086
18. J Ellis P Dodds T Pryor 2000 The generation of plant disease resistance gene specificities Trends Plant Sci 5 373 379
19. SD Gandhi AF Heesacker CA Freeman J Argyris K Bradford SJ Knapp 2005 The self-incompatibility locus (S) and quantitative trait loci for self-pollination and seed dormancy in sunflower Theor Appl Genet 111 619 629
20. MA Gedil MB Slabaugh S Berry R Johnson R Michelmore J Miller T Gulya SJ Knapp 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 44 205 212
21. L Gentzbittel S Mouzeyar S Badaoui E Mestries F Vear D Tourvieille de Labrouhe P Nicolas 1998 Cloning of molecular markers for disease resistance in sunflower, Helianthus annuus L. Theor Appl Genet 96 519 525
22. SA Goff D Ricke TH Lan G Presting R Wang M Dunn J Glazebrook A Sessions P Oeller H Varma D Hadley D Hutchison C Martin 2002 A draft sequence of the rice genome (Oryza sativa L. ssp. japonica) Science 296 79 92
23. MD Gonzales E Archuleta A Farmer K Gajendran D Grant R Shoemaker WD Beavis ME Waugh 2005 The Legume Information System (LIS): an integrated information resource for comparative legume biology Nucleic Acids Res 33 D660 D665
24. KE Hammond-Kosack JDG Jones 1997 Plant disease resistance genes Ann Rev Plant Phys Plant Mol Biol 48 575 607
25. L He C Du L Covaleda Z Xu AF Robinson JZ Yu RJ Kohel HB Zhang 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 1241
26. KH Hecker KH Roux 1996 High and low annealing temperatures increase both specificity and yield in touchdown and stepdown PCR Biotechniques 20 478 485
27. BF Holt DA Hubert JL Dangl 2003 Resistance gene signaling in plants: complex similarities to animal innate immunity Curr Opin Immunol 15 20 25
28. SH Hulbert CA Webb SM Smith Q Sun 2001 Resistance gene complexes: evolution and utilization Ann Rev Phytopathol 39 285 312
29. JD Jones JL Dangl 2006 The plant immune system Nature 444 323 329
30. V Kanazin LF Marek RC Shoemaker 1996 Resistance gene analogs are conserved and clustered in soybean Proc Natl Acad Sci USA 93 11746 11750
31. A Kohler C Rinaldi S Duplessis M Baucher D Geelen F Duchaussoy BC Meyers W Boerjan F Martin 2008 Genome-wide identification of NBS resistance genes in Populus trichocarpa Plant Mol Biol 66 619 636
32. H Kuang SS Woo BC Meyers E Nevo RW Michelmore 2004 Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce Plant Cell 16 2870 2894
33. Y Kukita T Tahira SS Sommer K Hayashi 1997 SSCP analysis of long DNA fragments in low pH gel Hum Mutat 10 400 407
34. ES Lander P Green J Abrahamson A Barlow MJ Daly SE Lincoln L Newburg 1987 MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations Genomics 25 511 557
35. K Langar Y Griveau F Kaan H Serieys D Varès A Bervillé 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 108 307 315
36. LA Larsen M Christiansen J Vuust PS Andersen 1999 High-throughput single-strand conformation polymorphism analysis by automated capillary electrophoresis: robust multiplex analysis and pattern-based identification of allelic variants Hum Mutat 13 318 327
37. LA Larsen C Jespersgaard PS Andersen 2007 Single-strand conformation polymorphism analysis using capillary array electrophoresis for large-scale mutation detection Nat Protoc 2 1458 1466
38. GJ Lawrence EJ Finnegan MA Ayliffe JG Ellis 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 1206
39. RR Lawson KC Goulter RJ Henry GA Kong JK Kochman 1998 Marker-assisted selection for two rust resistance genes in sunflower Mol Breed 4 227 234
40. SY Lee JS Seo M Rodriguez-Lanetty 2003 Comprative analysis of superfamilies of NBS-encoding disease resistance gene analogs in cultivated and wild apple species Mol Gen Genomics 269 101 108
41. D Leister A Ballvora F Salamini C Gebhardt 1996 A PCR-based approach for isolating pathogen resistance genes from potato with potential for wide application in plants Nat Genet 14 421 429
42. D Leister J Kurth DA Laurie M Yano T Sasaki K Devos A Graner P Schulze-Lefert 1998 Rapid reorganization of resistance gene homologues in cereal genomes Proc Natl Acad Sci USA 95 370 375
43. SL Lenardon ME Bazzalo G Abratti CJ Cimmino MT Galella M Grondona F Giolitti AJ Leon 2005 Screening sunflower for resistance to sunflower chlorotic mottle virus and mapping the Rcmo-1 resistance gene Crop Sci 45 735 739
44. SE Lincoln ES Lander 1992 Systematic detection of errors in genetic linkage data Genomics 14 604 610
45. LH Madsen NC Collins M Rakwalska G Backes N Sandal L Krusell J Jensen EH Waterman A Jahoor M Ayliffe AJ Pryor P Langridge P Schulze-Lefert J Stougaard 2003 Barley disease resistance gene analogs of the NBS-LRR class: identification and mapping Mol Genet Genomics 269 150 161
46. JM McDowell M Dhandaydham TA Long MG Aarts S Goff EB Holub JL Dangl 1998 Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis Plant Cell 10 1861 1874
47. L McHale X Tan P Koehl RW Michelmore 2006 Plant NBS-LRR proteins: adaptable guards Genome Biol 7 212
48. BC Meyers KA Shen P Rohani BS Gaut RW Michelmore 1998 Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection Plant Cell 10 1833 1846
49. BC Meyers DB Chin KA Shen S Sivaramakrishnan DO Lavelle Z Zhang RW Michelmore 1998 The major resistance gene cluster in lettuce is highly duplicated and spans several megabases Plant Cell 10 1817 1832
50. BC Meyers AW Dickerman RW Michelmore S Sivaramakrishnan BW Sobral ND Young 1999 Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily Plant J 20 317 332
51. BC Meyers M Morgante RW Michelmore 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 92
52. BC Meyers A Kozik A Griego H Kuang RW Michelomore 2003 Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis Plant Cell 15 809 834
53. RW Michelmore 2003 The impact zone: genomics and breeding for durable disease resistance Curr Opin Plant Biol 6 397 404
54. RW Michelmore BC Meyers 1998 Clusters of resistance genes in plants evolve by divergent selection and a birth- and- death process Genome Res 8 1113 1130
55. JF Miller TJ Gulya 1988 Registration of six downy mildew resistant sunflower germplasm lines Crop Sci 28 1040 1041
56. JF Miller TJ Gulya 1991 Inheritance of resistance to race 4 of downy mildew derived from interspecific cross in sunflower Crop Sci 31 40 43
57. JF Miller TJ Gulya GJ Seiler 2002 Registration of five fertility restorer sunflower germplasms Crop Sci 42 989
58. MG Murray WR Thompson 1980 Rapid isolation of high molecular weight plant DNA Nucleic Acids Res 8 4321 4325
59. L Noel TL Moores EA van Der Biezen M Parniske MJ Daniels JE Parker JD Jones 1999 Pronounced intraspecific haplotype divergence at RPP5 complex disease resistance locus of Arabidopsis Plant Cell 11 2099 2112
60. S Noir MC Combes F Anthony P Lashermes 2001 Origin, diversity and evolution of NBS-type disease-resistance gene homologues in coffee trees (Coffea L.) Mol Gent Genomics 265 654 662
61. M Orita H Iwahana H Kanazawa K Hayashi T Sekiya 1989 Detection of polymorphisms of human DNA by gel electrophoresis as single-strand conformation polymorphisms Proc Natl Acad Sci USA 86 2766 2770
62. Q Pan YS Liu O Budai-Hadrian M Sela L Carmel-Goren D Zamir R Fluhr 2000 Comparative genetics of nucleotide binding site-leucine rich repeat resistance gene homologues in the genomes of two dicotyledons: tomato and arabidopsis Genetics 155 309 222
63. Parker C, Riches CR (1993) Parasitic weeds of the world: biology and control. CAB Int, Wallingford
64. M Parniske KE Hammond-Kosack C Golstein CM Thomas DA Jones K Harrison BB Wulff JD Jones 1997 Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato Cell 91 821 832
65. B Pérez-Vich B Akhtouch SJ Knapp AJ Leon L Velasco JM Fernández-Martínez ST Berry 2004 Quantitative trait loci for broomrape (Orobanche cumana Wallr.) resistance in sunflower Theor Appl Genet 109 92 102
66. A Plocik J Layden R Kesseli 2004 Comparative analysis of NBS domain sequences of NBS-LRR disease resistance genes from sunflower, lettuce, and chicory Mol Phylogen Evol 31 153 163
67. GV Pustovoit EY Kroknin 1978 Inheritance of resistance in interspecific hybrids of sunflower to downy mildew Rev Plant Pathol 57 209
68. Z Quresh CC Jan TJ Gulya 1993 Resistance of sunflower rust and its inheritance in wild sunflower species Plant Breed 110 297 306
69. O Radwan MF Bouzidi F Vear J Philippon D Tourvieille de Labrouhe P Nicolas S Mouzeyar 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 1446
70. O Radwan MF Bouzidi P Nicolas S Mouzeyar 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 109 176 185
71. E Richly J Kurth D Leister 2002 Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution Mol Biol Evol 19 76 84
72. M Rossi PG Araujo F Paulet O Garsmeur VM Dias H Chen MA Van Sluys A D'Hont 2003 Genomic distribution and characterization of EST-derived resistance gene analogs (RGAs) in sugarcane Mol Genet Genomics 269 406 419
73. N Saitou M Nei 1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees Mol Biol Evol 4 406 425
74. GJ Seiler 1991 Registration of 15 interspecific sunflower germplasm lines derived from wild annual species Crop Sci 31 1389 1390
75. GJ Seiler 1991 Registration of 13 downy mildew tolerant interspecific sunflower germplasm lines derived from wild annual species Crop Sci 31 1714 1716
76. KA Shen BC Keyers MN Islam-Faridi DB Chin DM Stelly RW Michelmore 1998 Resistance gene candidate identified by PCR with degenerate oligonucleotide primers map to clusters of resistance genes in lettuce Mol Plant Microbe Interact 11 815 823
77. D Škoric 1985 Sunflower breeding for resistance to Diaporthe/Phomopsis helianthi Helia 8 21 23
78. MB Slabaugh JK Yu S Tang A Heesacker X Hu G Lu F Han D Bidney SJ Knapp 2003 Haplotyping and mapping a large cluster of resistance gene candidates in sunflower using multilocus intron fragment length polymorphisms Plant Biotech J 1 167 185
79. Q Sun NC Collins M Ayliffe SM Smith J Drake T Pryor SH Hulbert 2001 Recombination between paralogues at the Rp1 rust resistance locus in maize Genetics 158 423 438
80. AS Tan CC Jan TJ Gulya 1992 Inheritance of resistance to race 4 of sunflower downy mildew in wild sunflower accessions Crop Sci 32 949 952
81. S Tang JK Yu MB Slabaugh DK Shintani SJ Knapp 2002 Simple sequence repeat map of the sunflower genome Theor Appl Genet 105 1124 1136
82. S Tang A Heesacker VK Kishore A Fernandez E Sadik G Cole SJ Knapp 2003 Genetic mapping of the Or5 gene for resistance to Orobanche race E in sunflower Crop Sci 43 1021 1028
83. SD Tanksley S McCouch 1997 Seed banks and molecular maps: unlocking the genetic potential from the wild Science 277 1063 1066
84. JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgens 1997 The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools Nucleic Acids Res 25 4876 4882
85. F Vear DT De Labrouhe JF Miller 2003 Inheritance of the wide-range downy mildew resistance in the sunflower line RHA 419 Helia 26 19 24
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 74-82
87. A Viguié DTD Labrouhe F Vear 2000 Inheritance of several sources of resistance to Phomopsis stem canker (Diaporthe helianthi Munt.-Cvet.) in sunflower (Helianthus annuus L.) Euphytica 116 167 179
88. Z Wang G Taramino D Yang G Liu SV Tingey GH Miao GL Wang 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 265 302 310
89. FS Wei RA Wong RP Wise 2002 Genome dynamics and evolution of the Mla (powdery mildew) resistance locus in barley Plant Cell 14 1903 1917
90. S Whitham SP Dinesh-Kumar D Choi R Hehl C Corr B Baker 1994 The product of tobacco mosaic virus resistance gene N: similarity to Toll and interleukin-1 receptor Cell 78 1101 1115
91. T Yu GR Buss MA Saghai-Maroof 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 11756
92. JK Yu S Tang MB Slabaugh AF Heesacker G Cole M Herring J Soper F Han WC Chu DM Webb L Thompson KJ Edwards ST Berry AJ León C Olungu N Maes SJ Knapp 2003 Towards a saturated molecular genetic linkage map for cultivated sunflower Crop Sci 43 367 387
93. H Zhu SB Cannon ND Young DR Cook 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