Skip to main content
Log in

Inheritance of soybean aphid resistance in 21 soybean plant introductions

Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

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.

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

BSA:

Bulked segregant analysis

MG:

Maturity group

PCR:

Polymerase chain reaction

PI:

Plant introduction

SNP:

Single nucleotide polymorphism

SSR:

Simple sequence repeats

References

  • Beckendorf EA, Catangui MA, Riedell WE (2008) Soybean aphid feeding injury and soybean yield, yield components, and seed composition. Agron J 100:237–246

    Article  Google Scholar 

  • 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 52:2070–2074

    Article  Google Scholar 

  • Carena M, Glogoza P (2004) Resistance of maize to the corn leaf aphid: a review. Maydica 49:241–254

    Google Scholar 

  • 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 173–185

    Google Scholar 

  • 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 99:1884–1889

    Article  PubMed  Google Scholar 

  • Dong H, Quick J (1995) Inheritance and allelism of resistances to the Russian wheat aphid in 7 wheat lines. Euphytica 81:299–303

    Article  Google Scholar 

  • Ellis P, Pink D, Ramsey A (1994) Inheritance of resistance to lettuce root aphid in the lettuce cultivars Avoncrisp and Lakeland. Ann Appl Biol 124:141–151

    Article  Google Scholar 

  • Fehr WR, Caviness CE (1977) Stages of soybean development. Cooperative Extension Service, Agriculture and Home Economics Experiment Station, Iowa State University, Ames

    Google Scholar 

  • Gao L, Klingler JP, Anderson JP, Edwards OR, Singh KB (2008) Characterization of pea aphid resistance in Medicago truncatula. Plant Physiol 146:996–1009

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 

  • 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 43:197–206

    Article  Google Scholar 

  • Hill CB, Li Y, Hartman GL (2004) Resistance to the soybean aphid in soybean germplasm. Crop Sci 44:98–106

    Article  Google Scholar 

  • Hill CB, Li Y, Hartman GL (2006a) A single dominant gene for resistance to the soybean aphid in the soybean cultivar Dowling. Crop Sci 46:1601–1605

    Article  Google Scholar 

  • Hill CB, Li Y, Hartman GL (2006b) Soybean aphid resistance in soybean Jackson is controlled by a single dominant gene. Crop Sci 46:1606–1608

    Article  CAS  Google Scholar 

  • Hill CB, Kim K, Crull L, Diers BW, Hartman GL (2009) Inheritance of resistance to the soybean aphid in soybean PI 200538. Crop Sci 49:1193–1200

    Article  CAS  Google Scholar 

  • Hill CB, Crull L, Herman TK, Voegtlin DJ, Hartman GL (2010) A new soybean aphid (Hemiptera: Aphididae) biotype identified. J Econ Entomol 103:509–515

    Article  CAS  PubMed  Google Scholar 

  • Hill CB, Chirumamilla A, Hartman GL (2012) Resistance and virulence in the soybean–Aphis glycines interaction. Euphytica 186:635–646

    Article  CAS  Google Scholar 

  • 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 116:945–952

    Article  CAS  PubMed  Google Scholar 

  • 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 50:960–968

    Article  CAS  Google Scholar 

  • Jun T, Rouf Mian MA, Michel AP (2012) Genetic mapping revealed two loci for soybean aphid resistance in PI 567301B. Theor Appl Genet 124:13–22

    Article  CAS  PubMed  Google Scholar 

  • 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 1:89–98

    Article  CAS  Google Scholar 

  • Kang S, Mian MAR, Hammond RB (2008) Soybean aphid resistance in PI 243540 is controlled by a single dominant gene. Crop Sci 48:1744–1748

    Article  CAS  Google Scholar 

  • Keim P, Shoemaker RC (1988) A rapid protocol for isolating soybean DNA. Soybean Genet Newsl 15:150–152

    Google Scholar 

  • Kim KS, Diers BW (2009) The associated effects of the soybean aphid resistance locus Rag1 on soybean yield and other agronomic traits. Crop Sci 49:1726–1732

    Article  CAS  Google Scholar 

  • 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 53:1326–1334

    Article  CAS  Google Scholar 

  • Kim KS, Hill CB, Hartman GL, Mian MAR, Diers BW (2008) Discovery of soybean aphid biotypes. Crop Sci 48:923–928

    Article  Google Scholar 

  • 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 120:1063–1071

    Article  CAS  PubMed  Google Scholar 

  • 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 121:599–610

    Article  CAS  PubMed  Google Scholar 

  • 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 126:56–63

    CAS  Google Scholar 

  • 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 19:25–34

    Article  CAS  Google Scholar 

  • Macedo TB, Bastos CS, Higley LG, Ostlie KR, Madhavan S (2003) Photosynthetic responses of soybean to soybean aphid (Homoptera: Aphididae) injury. J Econ Entomol 96:188–193

    Article  CAS  PubMed  Google Scholar 

  • Mardorf JL, Fehr WR, O’Neal ME (2010) Agronomic and seed traits of soybean lines with the Rag1 gene for aphid resistance. Crop Sci 50:1891–1895

    Article  CAS  Google Scholar 

  • Mensah C, DiFonzo C, Nelson RL, Wang DC (2005) Resistance to soybean aphid in early maturing soybean germplasm. Crop Sci 45:2228–2233

    Article  Google Scholar 

  • Mensah C, DiFonzo C, Wang D (2008) Inheritance of soybean aphid resistance in PI 567541B and PI 567598B. Crop Sci 48:1759–1763

    Article  Google Scholar 

  • Mian MAR, Hammond RB, Martin SKS (2008a) New plant introductions with resistance to the soybean aphid. Crop Sci 48:1055–1061

    Article  Google Scholar 

  • Mian MAR, Kang S, Beil SE, Hammond RB (2008b) Genetic linkage mapping of the soybean aphid resistance gene in PI 243540. Theor Appl Genet 117:955–962

    Article  Google Scholar 

  • 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 88:9828–9832

    Article  CAS  PubMed  Google Scholar 

  • Nurden Av, Scott RA, Hesler L, Tilmon K, Glover K, Carter C (2010) Inheritance of soybean aphid resistance from PI 71506. J Crop Improv 24:400–416

    Article  Google Scholar 

  • Ostlie K (2002) Managing soybean aphid, University of Minnesota Extension Service, St Paul. http://www.soybeans.umn.edu/crop/insects/aphid/aphid_publication_managingsba.htm. Accessed on 09 April 2013

  • Ragsdale DW, Landis DA, Brodeur J, Heimpel GE, Desneux N (2011) Ecology and management of the soybean aphid in North America. Annu Rev Entomol 56:375–399

    Article  CAS  PubMed  Google Scholar 

  • SAS Institute (2008) The SAS system for Microsoft Windows. Release 9.2. SAS Inst., Cary, NC

  • Smith CM, Boyko EV (2007) The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomol Exp Appl 122:1–16

    Article  CAS  Google Scholar 

  • Stokes ME, Davis CS, Koch GG (2000) Categorical data analysis using the SAS system, 2nd edn. SAS Institute Inc, Cary

    Google Scholar 

  • 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 43:1828–1832

    Article  CAS  Google Scholar 

  • Wu ZS, Schenk-Hamlin D, Zhan WY, Ragsdale DW, Heimpel GE (2004) The soybean aphid in China: a historical review. Ann Entomol Soc Am 97:209–218

    Article  Google Scholar 

  • Zhang G, Gu C, Wang D (2009) Molecular mapping of soybean aphid resistance genes in PI 567541B. Theor Appl Genet 118:473–482

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Gu C, Wang D (2010) A novel locus for soybean aphid resistance. Theor Appl Genet 120:1183–1191

    Article  CAS  PubMed  Google Scholar 

  • 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 

Download references

Acknowledgments

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Carolyn M. Fox.

Additional information

Communicated by A. H. Schulman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fox, C.M., Kim, KS., Cregan, P.B. et al. Inheritance of soybean aphid resistance in 21 soybean plant introductions. Theor Appl Genet 127, 43–50 (2014). https://doi.org/10.1007/s00122-013-2199-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-013-2199-1

Keywords

Navigation