Theoretical and Applied Genetics

, Volume 127, Issue 1, pp 43–50 | Cite as

Inheritance of soybean aphid resistance in 21 soybean plant introductions

  • Carolyn M. FoxEmail author
  • Ki-Seung Kim
  • Perry B. Cregan
  • Curtis B. Hill
  • Glen L. Hartman
  • Brian W. Diers
Original Paper


Key Message

The Rag2 region was frequently identified among 21 F 2 populations evaluated for soybean aphid resistance, and dominant gene action and single-gene resistance were also commonly identified.


The soybean aphid [Aphis glycines Matsumura (Hemiptera: Aphididae)] is one of the most important insect pests of soybean [Glycine max (L.) Merr] in the northern USA and southern Canada, and four resistance loci (Rag1rag4) have been discovered since the pest was identified in the USA in 2000. The objective of this research was to determine whether resistance expression in recently identified soybean aphid-resistant plant introductions (PIs) was associated with the four Rag loci using a collection of 21 F2 populations. The F2 populations were phenotyped with soybean aphid biotype 1, which is avirulent on plants having any of the currently identified Rag genes, using choice tests in the greenhouse and were tested with genetic markers linked to the four Rag loci. The phenotyping results indicate that soybean aphid resistance is controlled by a single dominant gene in 14 PIs, by two genes in three PIs, and four PIs had no clear Mendelian inheritance patterns. Genetic markers flanking Rag2 were significantly associated with aphid resistance in 20 PIs, the Rag1 region was significantly identified in five PIs, and the Rag3 region was identified in one PI. These results show that single dominant gene action at the Rag2 region may be a major source for aphid resistance in the USDA soybean germplasm collection.


Simple Sequence Repeat Marker Single Nucleotide Polymorphism Marker Plant Introduction Single Dominant Gene Aphid Resistance 
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.



Bulked segregant analysis


Maturity group


Polymerase chain reaction


Plant introduction


Single nucleotide polymorphism


Simple sequence repeats



This work was supported by soybean check-off funding from the Illinois Soybean Association to B.D. and funding from the United Soybean Board to C.F. We also thank Laura Crull and Sarah Schultz for experiment assistance and support.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

The authors state that the experiments comply with the current laws of the country in which they were performed (USA).


  1. Beckendorf EA, Catangui MA, Riedell WE (2008) Soybean aphid feeding injury and soybean yield, yield components, and seed composition. Agron J 100:237–246CrossRefGoogle Scholar
  2. Brace RC, Fehr WR (2012) Impact of combining the Rag1 and Rag2 alleles for aphid resistance on agronomic and seed traits of soybean. Crop Sci 52:2070–2074CrossRefGoogle Scholar
  3. Carena M, Glogoza P (2004) Resistance of maize to the corn leaf aphid: a review. Maydica 49:241–254Google Scholar
  4. Cregan PB, Quigley CV (1997) Simple sequence repeat DNA marker analysis. In: Caetano-Anolles G, Gresshoff PM (eds) DNA markers: protocols, applications and overview. Wiley, New York, pp 173–185Google Scholar
  5. Diaz-Montano J, Reese JC, Schapaugh WT, Campbell LR (2006) Characterization of antibiosis and antixenosis to the soybean aphid (Hemiptera: Aphididae) in several soybean genotypes. J Econ Entomol 99:1884–1889PubMedCrossRefGoogle Scholar
  6. Dong H, Quick J (1995) Inheritance and allelism of resistances to the Russian wheat aphid in 7 wheat lines. Euphytica 81:299–303CrossRefGoogle Scholar
  7. Ellis P, Pink D, Ramsey A (1994) Inheritance of resistance to lettuce root aphid in the lettuce cultivars Avoncrisp and Lakeland. Ann Appl Biol 124:141–151CrossRefGoogle Scholar
  8. Fehr WR, Caviness CE (1977) Stages of soybean development. Cooperative Extension Service, Agriculture and Home Economics Experiment Station, Iowa State University, AmesGoogle Scholar
  9. Gao L, Klingler JP, Anderson JP, Edwards OR, Singh KB (2008) Characterization of pea aphid resistance in Medicago truncatula. Plant Physiol 146:996–1009PubMedCentralPubMedCrossRefGoogle Scholar
  10. Hartman GL, Domier LL, Wax LM, Helm CG, Onstad DW, Shaw JT, Solter LF, Voegtlin DJ, D’Arcy CJ, Gray ME, Steffey KL, Isard SA, Orwick PL (2001) Occurrence and distribution of Aphis glycines on soybeans in Illinois in 2000 and its potential control. Plant Health Progess. doi: 10.1094/PHP-2001-0205-01-HN Google Scholar
  11. Hesler LS, Dashiell KE (2008) Identification and characterization of new sources of resistance to Aphis glycines Matsumura (Hemiptera: Aphididae) in soybean lines. Appl Entomol Zool 43:197–206CrossRefGoogle Scholar
  12. Hill CB, Li Y, Hartman GL (2004) Resistance to the soybean aphid in soybean germplasm. Crop Sci 44:98–106CrossRefGoogle Scholar
  13. Hill CB, Li Y, Hartman GL (2006a) A single dominant gene for resistance to the soybean aphid in the soybean cultivar Dowling. Crop Sci 46:1601–1605CrossRefGoogle Scholar
  14. Hill CB, Li Y, Hartman GL (2006b) Soybean aphid resistance in soybean Jackson is controlled by a single dominant gene. Crop Sci 46:1606–1608CrossRefGoogle Scholar
  15. Hill CB, Kim K, Crull L, Diers BW, Hartman GL (2009) Inheritance of resistance to the soybean aphid in soybean PI 200538. Crop Sci 49:1193–1200CrossRefGoogle Scholar
  16. Hill CB, Crull L, Herman TK, Voegtlin DJ, Hartman GL (2010) A new soybean aphid (Hemiptera: Aphididae) biotype identified. J Econ Entomol 103:509–515PubMedCrossRefGoogle Scholar
  17. Hill CB, Chirumamilla A, Hartman GL (2012) Resistance and virulence in the soybean–Aphis glycines interaction. Euphytica 186:635–646CrossRefGoogle Scholar
  18. Hyten DL, Song Q, Choi I, Yoon M, Specht JE, Matukumalli LK, Nelson RL, Shoemaker RC, Young ND, Cregan PB (2008) High-throughput genotyping with the GoldenGate assay in the complex genome of soybean. Theor Appl Genet 116:945–952PubMedCrossRefGoogle Scholar
  19. Hyten DL, Choi I, Song Q, Specht JE, Carter TE Jr, Shoemaker RC, Hwang E, Matukumalli LK, Cregan PB (2010) A high density integrated genetic linkage map of soybean and the development of a 1536 universal soy linkage panel for quantitative trait locus mapping. Crop Sci 50:960–968CrossRefGoogle Scholar
  20. Jun T, Rouf Mian MA, Michel AP (2012) Genetic mapping revealed two loci for soybean aphid resistance in PI 567301B. Theor Appl Genet 124:13–22PubMedCrossRefGoogle Scholar
  21. Kaczorowski KA, Kim K, Diers BW, Hudson ME (2008) Microarray-based genetic mapping using soybean near-isogenic lines and generation of SNP markers in the Rag1 aphid-resistance interval. Plant Gen 1:89–98CrossRefGoogle Scholar
  22. Kang S, Mian MAR, Hammond RB (2008) Soybean aphid resistance in PI 243540 is controlled by a single dominant gene. Crop Sci 48:1744–1748CrossRefGoogle Scholar
  23. Keim P, Shoemaker RC (1988) A rapid protocol for isolating soybean DNA. Soybean Genet Newsl 15:150–152Google Scholar
  24. Kim KS, Diers BW (2009) The associated effects of the soybean aphid resistance locus Rag1 on soybean yield and other agronomic traits. Crop Sci 49:1726–1732CrossRefGoogle Scholar
  25. Kim KS, Diers BW (2013) The associated effects of the soybean aphid resistance gene Rag2 from PI 200538 on agronomic traits in soybean. Crop Sci 53:1326–1334CrossRefGoogle Scholar
  26. Kim KS, Hill CB, Hartman GL, Mian MAR, Diers BW (2008) Discovery of soybean aphid biotypes. Crop Sci 48:923–928CrossRefGoogle Scholar
  27. Kim K, Bellendir S, Hudson KA, Hill CB, Hartman GL, Hyten DL, Hudson ME, Diers BW (2010a) Fine mapping the soybean aphid resistance gene Rag1 in soybean. Theor Appl Genet 120:1063–1071PubMedCrossRefGoogle Scholar
  28. Kim KS, Hill CB, Hartman GL, Hyten DL, Hudson ME, Diers BW (2010b) Fine mapping of the soybean aphid-resistance gene Rag2 in soybean PI 200538. Theor Appl Genet 121:599–610PubMedCrossRefGoogle Scholar
  29. Klingler J, Kovalski I, Silberstein L, Thompson G, Perl-Treves R (2001) Mapping of cotton-melon aphid resistance in melon. J Am Soc Hortic Sci 126:56–63Google Scholar
  30. Li Y, Hill CB, Carlson SR, Diers BW, Hartman GL (2007) Soybean aphid resistance genes in the soybean cultivars Dowling and Jackson map to linkage group M. Mol Breed 19:25–34CrossRefGoogle Scholar
  31. Macedo TB, Bastos CS, Higley LG, Ostlie KR, Madhavan S (2003) Photosynthetic responses of soybean to soybean aphid (Homoptera: Aphididae) injury. J Econ Entomol 96:188–193PubMedCrossRefGoogle Scholar
  32. Mardorf JL, Fehr WR, O’Neal ME (2010) Agronomic and seed traits of soybean lines with the Rag1 gene for aphid resistance. Crop Sci 50:1891–1895CrossRefGoogle Scholar
  33. Mensah C, DiFonzo C, Nelson RL, Wang DC (2005) Resistance to soybean aphid in early maturing soybean germplasm. Crop Sci 45:2228–2233CrossRefGoogle Scholar
  34. Mensah C, DiFonzo C, Wang D (2008) Inheritance of soybean aphid resistance in PI 567541B and PI 567598B. Crop Sci 48:1759–1763CrossRefGoogle Scholar
  35. Mian MAR, Hammond RB, Martin SKS (2008a) New plant introductions with resistance to the soybean aphid. Crop Sci 48:1055–1061CrossRefGoogle Scholar
  36. Mian MAR, Kang S, Beil SE, Hammond RB (2008b) Genetic linkage mapping of the soybean aphid resistance gene in PI 243540. Theor Appl Genet 117:955–962CrossRefGoogle Scholar
  37. 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 88:9828–9832PubMedCrossRefGoogle Scholar
  38. Nurden Av, Scott RA, Hesler L, Tilmon K, Glover K, Carter C (2010) Inheritance of soybean aphid resistance from PI 71506. J Crop Improv 24:400–416CrossRefGoogle Scholar
  39. Ostlie K (2002) Managing soybean aphid, University of Minnesota Extension Service, St Paul. Accessed on 09 April 2013
  40. Ragsdale DW, Landis DA, Brodeur J, Heimpel GE, Desneux N (2011) Ecology and management of the soybean aphid in North America. Annu Rev Entomol 56:375–399PubMedCrossRefGoogle Scholar
  41. SAS Institute (2008) The SAS system for Microsoft Windows. Release 9.2. SAS Inst., Cary, NCGoogle Scholar
  42. Smith CM, Boyko EV (2007) The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomol Exp Appl 122:1–16CrossRefGoogle Scholar
  43. Stokes ME, Davis CS, Koch GG (2000) Categorical data analysis using the SAS system, 2nd edn. SAS Institute Inc, CaryGoogle Scholar
  44. 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
  45. Wu ZS, Schenk-Hamlin D, Zhan WY, Ragsdale DW, Heimpel GE (2004) The soybean aphid in China: a historical review. Ann Entomol Soc Am 97:209–218CrossRefGoogle Scholar
  46. Zhang G, Gu C, Wang D (2009) Molecular mapping of soybean aphid resistance genes in PI 567541B. Theor Appl Genet 118:473–482PubMedCrossRefGoogle Scholar
  47. Zhang G, Gu C, Wang D (2010) A novel locus for soybean aphid resistance. Theor Appl Genet 120:1183–1191PubMedCrossRefGoogle Scholar
  48. Zhang G, Gu C, Wang D (2013) Mapping and validation of a gene for soybean aphid resistance in PI 567537. Mol Bio. doi: 10.1007/s11032-013-9857-5 Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Carolyn M. Fox
    • 1
    Email author
  • Ki-Seung Kim
    • 1
    • 4
  • Perry B. Cregan
    • 3
  • Curtis B. Hill
    • 1
  • Glen L. Hartman
    • 1
    • 2
  • Brian W. Diers
    • 1
  1. 1.Department of Crop SciencesUniversity of IllinoisUrbanaUSA
  2. 2.USDA-ARSUrbanaUSA
  3. 3.Soybean Genomics and Improvement LaboratoryUSDA-ARSBeltsvilleUSA
  4. 4.The Samuel Roberts Noble FoundationArdmoreUSA

Personalised recommendations