Theoretical and Applied Genetics

, Volume 125, Issue 6, pp 1339–1352 | Cite as

Molecular mapping of soybean rust resistance in soybean accession PI 561356 and SNP haplotype analysis of the Rpp1 region in diverse germplasm

  • Ki-Seung Kim
  • Jair R. Unfried
  • David L. Hyten
  • Reid D. Frederick
  • Glen L. Hartman
  • Randall L. Nelson
  • Qijian Song
  • Brian W. Diers
Original Paper


Soybean rust (SBR), caused by Phakopsora pachyrhizi Sydow, is one of the most economically important and destructive diseases of soybean [Glycine max (L.) Merr.] and the discovery of novel SBR resistance genes is needed because of virulence diversity in the pathogen. The objectives of this research were to map SBR resistance in plant introduction (PI) 561356 and to identify single nucleotide polymorphism (SNP) haplotypes within the region on soybean chromosome 18 where the SBR resistance gene Rpp1 maps. One-hundred F2:3 lines derived from a cross between PI 561356 and the susceptible experimental line LD02-4485 were genotyped with genetic markers and phenotyped for resistance to P. pachyrhizi isolate ZM01-1. The segregation ratio of reddish brown versus tan lesion type in the population supported that resistance was controlled by a single dominant gene. The gene was mapped to a 1-cM region on soybean chromosome 18 corresponding to the same interval as Rpp1. A haplotype analysis of diverse germplasm across a 213-kb interval that included Rpp1 revealed 21 distinct haplotypes of which 4 were present among 5 SBR resistance sources that have a resistance gene in the Rpp1 region. Four major North American soybean ancestors belong to the same SNP haplotype as PI 561356 and seven belong to the same haplotype as PI 594538A, the Rpp1-b source. There were no North American soybean ancestors belonging to the SNP haplotypes found in PI 200492, the source of Rpp1, or PI 587886 and PI 587880A, additional sources with SBR resistance mapping to the Rpp1 region.


Simple Sequence Repeat Marker Single Nucleotide Polymorphism Marker Plant Introduction Resistance Source Wild Soybean 
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.



This research was supported by funding from the United Soybean Board.


  1. Born H, Diver S (2005) Asian soybean rust: notes and organic control options for farmers.
  2. Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of genetic linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet 32:314–331PubMedGoogle Scholar
  3. Bromfield KR (1984) Soybean rust. Monograph no. 11. American Phytopathological Society, St. PaulGoogle Scholar
  4. Caldwell P, McLaren NW (2004) Soybean rust research in South Africa. In: Proc. VII world soybean res. conf. IV int. soybean processing and utilization conference, III Brazilian soybean congress, Foz do Iguassu, PR, Brazil, pp 354–360Google Scholar
  5. Chakraborty N, Curley J, Frederick RD, Hyten DL, Nelson RL, Hartman GL, Diers BW (2009) Mapping and confirmation of a new allele at Rpp 1 from soybean PI 594538A conferring RB lesion-type resistance to soybean rust. Crop Sci 49:783–790CrossRefGoogle Scholar
  6. Fan JB, Chee MS, Gunderson KL (2006) Highly parallel genomic assays. Nat Rev Genet 7:632–644PubMedCrossRefGoogle Scholar
  7. Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Sci 11:929–931CrossRefGoogle Scholar
  8. Garcia A, Calvo ES, Kiihl RS, Harada A, Hiromoto DM, Vieira LGE (2008) Molecular mapping of soybean rust (Phakopsora pachyrhizi) resistance genes: discovery of a novel locus and alleles. Theor Appl Genet 117:545–553PubMedCrossRefGoogle Scholar
  9. Gizlice Z, Carter TE, Burton JW (1994) Genetic base for North American public soybean cultivars released between 1947 and 1988. Crop Sci 34:1143–1151CrossRefGoogle Scholar
  10. Gore MA, Chia JM, Elshire RJ, Sun Q, Ersoz ES, Hurwitz BL, Peiffer JA, McMullen MD, Grills GS, Ross-Ibarra J, Ware DH, Buckler ES (2009) A first-generation haplotype map of maize. Science 326:1115–1117PubMedCrossRefGoogle Scholar
  11. Hartman GL, Wang TC, Tschanz AT (1991) Soybean rust development and the quantitative relationship between rust severity and soybean yield. Plant Dis 75:596–600CrossRefGoogle Scholar
  12. Hartman GL, Miles MR, Frederick RD (2005) Breeding for resistance to soybean rust. Plant Dis 89:664–666CrossRefGoogle Scholar
  13. Hartman GL, Hill CB, Twizeyimana M, Miles MR, Bandyopadhyay R (2011) Interaction of soybean and Phakopsora pachyrhizi, the cause of soybean rust. CAB Rev Perspect Agric Vet Sci Nutr Nat Resour 6. doi: 10.1079/PAVSNNR20116025
  14. Hennings VP (1903) A few new Japanese Uredinaceae. Hedwigia 42:S107–S108Google Scholar
  15. Hershman D, Sikora E, Giesler L (2011) Soybean rust PIPE: Past, present, and future. J Integr Pest Manag 2. doi:10.1603/IPM11001
  16. Hyten DL, Song Q, Zhu Y, Choi IY, Nelson RL, Costa JM, Specht JE, Shoemaker RC, Cregan PB (2006) Impacts of genetic bottlenecks on soybean genome diversity. Proc Natl Acad Sci USA 103:16666–16671PubMedCrossRefGoogle Scholar
  17. Hyten DL, Hartman GL, Nelson RL, Frederick RD, Concibido VC, Narvel JM, Cregan PB (2007) Map location of the Rpp 1 locus that confers resistance to soybean rust in soybean. Crop Sci 47:837–840CrossRefGoogle Scholar
  18. Hyten DL, Smith JR, Frederick RD, Tuker ML, Song Q, Cregan PB (2009) Bulk segregate analysis using the GoldenGate assay to locate the Rpp 3 locus that confers resistance to Phakopsora pachyrhizi (soybean rust) in soybean. Crop Sci 49:265–271CrossRefGoogle Scholar
  19. Isard SA, Gage SH, Comtois P, Russo JM (2005) Principles of the atmospheric pathway for invasive species applied to soybean rust. Bioscience 55:851–862CrossRefGoogle Scholar
  20. Johnson GC, Esposito L, Barratt BJ, Smith AN, Heward J, Genova GD, Ueda H, Cordell HJ, Eaves IA, Dudbridge F, Twells RC, Payne F, Hughes W, Nutland S, Stevens H, Carr P, Tuomilehto-Wolf E, Tuomilehto J, Gough SC, Clayton DG, Todd JA (2001) Haplotype tagging for the identification of common disease genes. Nat Genet 29:233–237PubMedCrossRefGoogle Scholar
  21. Keim P, Olson T, Shoemaker RC (1988) A rapid protocol for isolating soybean DNA. Soybean Genet Newsl 15:150–152Google Scholar
  22. Killgore E, Heu R (1994) First report of soybean rust in Hawaii. Plant Dis 78:1216CrossRefGoogle Scholar
  23. Lam HM, Xu X, Liu X, Chen W, Yang G, Wong FL, Li MW, He W, Qin N, Wang B, Li J, Jian M, Wang J, Shao G, Wang J, Sun SS, Zhang G (2010) Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet 42:1053–1059PubMedCrossRefGoogle Scholar
  24. Li S, Smith JR, Ray JD, Frederick RD (2012) Identification of a new soybean rust resistance genes in PI 567102B. Theor Appl Genet 125:133–142PubMedCrossRefGoogle Scholar
  25. Melching JS, Bromfield KR, Kingsolver CH (1983) The plant pathogen containment facility at Frederick, Maryland. Plant Dis 67:717–722CrossRefGoogle Scholar
  26. Meyer JDF, Silva DCG, Yang C, Pedley KF, Zhang C, van de Mortel M, Hill JH, Shoemaker RC, Abdelnoor RV, Whitham SA, Graham MA (2009) Identification and analyses of candidate genes for Rpp 4-mediated resistance to Asian soybean rust in soybean (Glycine max (L.) Merr.). Plant Physiol 150:295–307PubMedCrossRefGoogle Scholar
  27. Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832PubMedCrossRefGoogle Scholar
  28. Miles MR, Frederick RD, Hartman GL (2003) Soybean rust: is the U.S. soybean crop at risk? APS Net Plant Pathol. doi: 10.1094/APSnetFeature-2003-060 Google Scholar
  29. Miles MR, Frederick RD, Hartman GL (2006) Evaluation of soybean germplasm for resistance to Phakopsora pachyrhizi. Plant Health Prog. doi: 10.1094/PHP-2006-0104-01-RS Google Scholar
  30. Miles MR, Bonde MR, Nester SE, Berner DK, Frederick RD, Hartman GL (2011) Characterizing resistance to Phakopsora pachyrhizi in soybean. Plant Dis 95:577–581CrossRefGoogle Scholar
  31. Monteros MJ, Missaoui AM, Phillips DV, Walker DR, Boerma HR (2007) Mapping and confirmation of the ‘Hyuuga’ red-brown lesion resistance gene for Asian soybean rust. Crop Sci 47:829–836CrossRefGoogle Scholar
  32. Monteros MJ, Ha BK, Phillips DV, Boerma HR (2010) SNP assay to detect the ‘Hyuuga’ red-brown lesion resistance gene for Asian soybean rust. Theor Appl Genet 121:1023–1032PubMedCrossRefGoogle Scholar
  33. Mueller TA, Miles MR, Morel W, Marios JJ, Wright DL, Kemerait RC, Levy C, Hartman GL (2009) Effect of fungicide and timing of application on soybean rust severity and yield. Plant Dis 93:243–248CrossRefGoogle Scholar
  34. Pathan MS, Sleper DA (2008) Advances in soybean breeding. In: Stacey G (ed) Genetics and genomics of soybean. Springer, NYGoogle Scholar
  35. Pham TA, Miles MR, Frederick RD, Hill CB, Hartman GL (2009) Differential responses of resistant soybean entries to isolates of Phakopsora pachyrhizi. Plant Dis 93:224–228CrossRefGoogle Scholar
  36. Rafalski A (2002) Applications of single nucleotide polymorphisms in crop genetics. Curr Opin Plant Biol 5:94–100PubMedCrossRefGoogle Scholar
  37. Ray JD, Morel W, Smith JR, Frederick RD, Miles MR (2009) Genetics and mapping of adult plant rust resistance in soybean PI 587886 and PI 587880A. Theor Appl Genet 119:271–280PubMedCrossRefGoogle Scholar
  38. Ribeiro AS, Ubirajara J, Moreira V, Pierozzi EB, Rachid BF, Toledo JFF, Arias CAA, Soares RM, Godoy CV (2007) Genetic control of Asian rust in soybean. Euphytica 157:15–25CrossRefGoogle Scholar
  39. SAS Institute (2002) The SAS system for Windows. Release 9.2. SAS Institute, CaryGoogle Scholar
  40. Schmutz J, Cannon S, Schlueter J, Ma J, Mitros T, Nelson W, Hyten D, Song Q, Thelen J, Cheng J, Xu D, Hellsten U, May G, Yu Y, Sakurai T, Umezawa T, Bhattacharyya M, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang X, Shinozaki K, Nguyen H, Wing R, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker R, Jackson S (2010) Genome sequence of the paleopolyploid soybean. Nature 463:178–183PubMedCrossRefGoogle Scholar
  41. Schneider RW, Hollier CA, Whitman HK, Palm ME, McKenny JM, Hernández JR, Levy L, Devries-Paterson R (2005) First report of soybean rust caused by Phakopsora pachyrhizi in the continental United States. Plant Dis 89:774CrossRefGoogle Scholar
  42. Shastry BS (2004) Role of SNP/haplotype map in gene discovery and drug development: an overview. Drug Dev Res 62:143–150CrossRefGoogle Scholar
  43. Silva DCG, Yamanaka N, Brogin RL, Arias CAA, Nepomuceno AL, Di Mauro AO, Pereira SS, Nogueira LM, Passianotto ALL, Abdelnoor RV (2008) Molecular mapping of two loci that confer resistance to Asian rust in soybean. Theor Appl Genet 117:57–63PubMedCrossRefGoogle Scholar
  44. Song QJ, Jia GF, Zhu YL, Grant D, Nelson RT, Hwang EY, Hyten DL, Cregan PB (2010) Abundance of SSR motifs and development of candidate polymorphic SSR markers (BARCSOYSSR_1.0) in soybean. Crop Sci 50:1950–1960CrossRefGoogle Scholar
  45. Song QJ, Hyten DL, Jia GF, Quigley C, Fickus E, Cregan PB (2012) Development and Evaluation of a high-density Illumina Infinium iSelect Beadchip SoySNP50K. In: Plant and animal genome conference XX. San Diego, CA, USA.
  46. Tamura K, Dudley J, Ne Mi, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24(8):1596–1599Google Scholar
  47. USDA-ARS (2012) National Genetic Resources Program. Germplasm Resources Information Network—(GRIN). (Online Database) National Germplasm Resources Laboratory, Beltsville, Maryland. Retrieved from
  48. Utomo HS, Linscombe SD (2009) Current patents and future development underlying marker-assisted breeding in major grain crops. Rec Pat DNA Gene Seq 3:53–62CrossRefGoogle Scholar
  49. Van Ooijen JW, Voorrips RW (2001) Joinmap 3.0. Software for the calculation of genetic linkage maps. Plant Research International, WageningenGoogle Scholar
  50. Van Ooijen JW, Boer MP, Jansen RC, Maliepaard C (2002) MapQTL 4.0. Software for the calculation of QTL positions on genetic maps. Plant Research International, WageningenGoogle Scholar
  51. Wang D, Shi J, Carlson SR, Cregan PB, Ward RW, Diers BW (2003) A low-cost, high-throughput polyacrylamide gel electrophoresis system for genotyping with microsatellite DNA markers. Crop Sci 43:1828–1832CrossRefGoogle Scholar
  52. Yorinori JT, Paiva WM, Frederick RD, Costamilan LM, Bertagnoli PF, Hartman GL, Godoy CV, Nunes JJ (2005) Epidemics of soybean rust (Phakopsora pachyrhizi) in Brazil and Paraguay from 2001 to 2003. Plant Dis 89:675–677CrossRefGoogle Scholar
  53. Zhu YL, Song QJ, Hyten DL, Van Tassell CP, Matukumalli LK, Grimm DR, Hyatt SM, Fickus EW, Young ND, Cregan PB (2003) Single-nucleotide polymorphisms in soybean. Genetics 163:1123–1134PubMedGoogle Scholar
  54. Zhu Q, Zheng X, Luo J, Gaut BS, Ge S (2007) Multilocus analysis of nucleotide variation of Oryza sativa and its wild relatives: severe bottleneck during domestication of rice. Mol Biol Evol 24:875–888PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Ki-Seung Kim
    • 1
  • Jair R. Unfried
    • 2
  • David L. Hyten
    • 3
    • 4
  • Reid D. Frederick
    • 5
  • Glen L. Hartman
    • 6
  • Randall L. Nelson
    • 6
  • Qijian Song
    • 7
  • Brian W. Diers
    • 1
  1. 1.Department of Crop ScienceUniversity of IllinoisUrbanaUSA
  2. 2.TMG-Tropical Melhoramento & GenéticaCambéBrazil
  3. 3.Soybean Genomics and Improvement LaboratoryUSDA-ARSBeltsvilleUSA
  4. 4.Pioneer Hi-BredJohnstonUSA
  5. 5.Foreign Disease-Weed Science Research UnitUSDA-ARSFort DetrickUSA
  6. 6.Soybean/Maize Germplasm, Pathology, and Genetics Research Unit, Department of Crop SciencesUniversity of Illinois, USDA-ARSUrbanaUSA
  7. 7.Soybean Genomics and Improvement Laboratory, Beltsville Agricultural Research CenterUSDA-ARSBeltsvilleUSA

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