Skip to main content
SpringerLink
Log in

Characterization and genetics of multiple soybean aphid biotype resistance in five soybean plant introductions

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

Five soybean plant introductions expressed antibiosis resistance to multiple soybean aphid biotypes. Two introductions had resistance genes located in the Rag1, Rag2, and Rag3 regions; one introduction had resistance genes located in the Rag1, Rag2, and rag4 regions; one introduction had resistance genes located in the Rag1 and Rag2 regions; and one introduction had a resistance gene located in the Rag2 region.

Abstract

Soybean aphid (Aphis glycines Matsumura) is the most important soybean [Glycine max (L.) Merr.] insect pest in the USA. The objectives of this study were to characterize the resistance expressed in five plant introductions (PIs) to four soybean aphid biotypes, determine the mode of resistance inheritance, and identify markers associated with genes controlling resistance in these accessions. Five soybean PIs, from an initial set of 3000 PIs, were tested for resistance against soybean aphid biotypes 1, 2, 3, and 4 in choice and no-choice tests. Of these five PIs, PI 587663, PI 587677, and PI 587685 expressed antibiosis against all four biotypes, while PI 587972 and PI 594592 expressed antibiosis against biotypes 1, 2, and 3. F2 populations derived from PI 587663 and PI 587972 were evaluated for resistance against soybean aphid biotype 1, and populations derived from PIs 587677, 587685, and 594592 were tested against biotype 3. In addition, F2:3 plants were tested against biotypes 2 and 3. Genomic DNA from F2 plants was screened with markers linked to Rag1, Rag2, Rag3, and rag4 soybean aphid-resistance genes. Results showed that PI 587663 and PI 594592 each had three genes with variable gene action located in the Rag1, Rag2, and Rag3 regions. PI 587677 had three genes with variable gene action located in the Rag1, Rag2 and rag4 regions. PI 587685 had one dominant gene located in the Rag1 region and an additive gene in the Rag2 region. PI 587972 had one dominant gene located in the Rag2 region controlling antixenosis- or antibiosis-type resistance to soybean aphid biotypes 1, 2, or 3. PIs 587663, 587677, and 587685 also showed antibiosis-type resistance against biotype 4. Information on multi-biotype aphid resistance and resistance gene markers will be useful for improving soybean aphid resistance in commercial soybean cultivars.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Abbreviations

PCR:

Polymerase chain reaction

SNP:

Single nucleotide polymorphisms

SSR:

Simple sequence repeat

References

  • Ajayi-Oyetunde OO, Diers BW, Lagos-Kutz DM, Hill CB, Hartman GL, Reuter-Carlson U, Bradley CA (2016) Differential reactions of soybean isolines with combinations of aphid resistance genes Rag1, Rag2, and Rag3 to four soybean aphid biotypes. J Econ Entomol 109:1431–1437

    Article  Google Scholar 

  • Alt J, Ryan-Mahmutagic M (2013) Soybean aphid biotype 4 identified. Crop Sci 53:1491–1495

    Article  Google Scholar 

  • Bales C, Zhang G, Liu M, Mensah C, Gu C, Song Q, Hyten D, Cregan P, Wang D (2013) Mapping soybean aphid resistance genes in PI 567598B. Theor Appl Genet 126:2081–2091

    Article  CAS  PubMed  Google Scholar 

  • Bansal R, Mian M, Michel AP (2013) Identification of novel sources of host plant resistance to known soybean aphid biotypes. J Econ Entomol 106:1479–1485

    Article  PubMed  Google Scholar 

  • 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 

  • Bhusal SJ, Jiang G-L, Tilmon KJ, Hesler LS (2013) Identification of soybean aphid resistance in early maturing genotypes of soybean. Crop Sci 53:491–499

    Article  Google Scholar 

  • Bhusal SJ, Jiang G-L, Hesler LS, Orf JH (2014) Soybean aphid resistance in soybean germplasm accessions of maturity group I. Crop Sci 54:2093–2098

    Article  Google Scholar 

  • Chen Y, Mensah C, DiFonzo C, Wang D (2006) Identification of QTLs underlying soybean aphid resistance in PI 567541B. The ASA-CSSA-SSSA International Annual Meetings

  • Chirumamilla A, Hill CB, Hartman GL (2014) Stability of soybean aphid resistance in soybean across different temperatures. Crop Sci 54:2557–2563

    Article  Google Scholar 

  • Cregan P, Quigley C (1997) Simple sequence repeat DNA marker analysis. In: Caetano-Anolles G, Gresshoff P (eds) DNA markers: protocols, applications and overview. Wiley, New York, pp 173–185

    Google Scholar 

  • Crossley MS, Hogg DB (2015) Rag virulence among soybean aphids (Hemiptera: Aphididae) in Wisconsin. J Econ Entomol 108:326–338

    Article  PubMed  Google Scholar 

  • Crute IR, Pink D (1996) Genetics and utilization of pathogen resistance in plants. The Plant Cell 8:1747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Djian-Caporalino C, Palloix A, Fazari A, Marteu N, Barbary A, Abad P, Sage-Palloix A-M, Mateille T, Risso S, Lanza R (2014) Pyramiding, alternating or mixing: comparative performances of deployment strategies of nematode resistance genes to promote plant resistance efficiency and durability. BMC Plant Biol 14:53. http://www.biomedcentral.com/1471-2229/14/53

  • Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Sci 11:929–931

    Article  Google Scholar 

  • Fernandez-Cornejo J, Nehring R, Osteen C, Wechsler S, Martin A, Vialou A (2014) Pesticide Use in US Agriculture: 21 Selected Crops, 1960–2008. United States Department of Agriculture, Economic Research Service

  • Fox CM, Kim K-S, Cregan PB, Hill CB, Hartman GL, Diers BW (2014) Inheritance of soybean aphid resistance in 21 soybean plant introductions. Theor Appl Genet 127:43–50

    Article  CAS  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. Online Plant Health Progress doi:101094/PHP-2001-0205-01-HN. Plant Health Progress

  • Hesler LS, Prischmann DA, Dashiell KE (2012) Field and laboratory evaluations of soybean lines against soybean aphid (Hemiptera: Aphididae). J Econ Entomol 105:608–615

    Article  PubMed  Google Scholar 

  • Hesler LS, Chiozza MV, O’Neal ME, MacIntosh GC, Tilmon KJ, Chandrasena DI, Tinsley NA, Cianzio SR, Costamagna AC, Cullen EM (2013) Performance and prospects of Rag genes for management of soybean aphid. Entomol Exp Appl 147:201–216

    Article  CAS  Google Scholar 

  • Hill JH, Alleman R, Hogg DB, Grau CR (2001) First report of transmission of Soybean mosaic virus and Alfalfa mosaic virus by Aphis glycines in the New World. Plant Dis 85:561

    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-S, 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 C, Chirumamilla A, Hartman G (2012) Resistance and virulence in the soybean-Aphis glycines interaction. Euphytica 186:635–646

    Article  CAS  Google Scholar 

  • Hyten DL, Song Q, Choi I-Y, Yoon M-S, 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-Y, Song Q, Specht JE, Carter TE, Shoemaker RC, Hwang E-Y, 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-H, Mian MR, 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-S, 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 

  • Keim P, Shoemaker RC (1988) Construction of a random recombinant DNA library that is primarily single copy sequence. Soybean Genet Newsl 15:147–148

    Google Scholar 

  • Kim C, Schaible G, Garrett L, Lubowski R, Lee D (2008a) Economic impacts of the US soybean aphid infestation: a multi-regional competitive dynamic analysis. Agr Resource Econ Rev 37:227–242

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Kim K-S, Chirumamilla A, Hill CB, Hartman GL, Diers BW (2014) Identification and molecular mapping of two soybean aphid resistance genes in soybean PI 587732. Theor Appl Genet 127:1251–1259

    Article  CAS  PubMed  Google Scholar 

  • Lehman A, O’Rourke N, Hatcher L, Stepanski E (2013) JMP for basic univariate and multivariate statistics: methods for researchers and social scientists. SAS Institute

  • Li Y, Hill CB, Carlson SR, Diers BW, Hartman GL (2007) Soybean aphid resistance in the soybean cultivars Dowling and Jackson map to linkage group M. Mol Breed 19:25–34

    Article  CAS  Google Scholar 

  • Liang X, Biao W, Tianlong W (2013) Identification of Two Soybean Aphid Biotypes. Crops 4:033

    Google Scholar 

  • Little TM, Hills FJ (1978) Agricultural Experimentation: Design and Analysis. John Wiley and Sons, New York

    Google Scholar 

  • Liu G, Xing H, Diao Y, Yang X, Sun D, Wang Q, Qi N, Lin H (2014) Identification of resistance to soybean aphids in early germplasm. Crop Sci 54:2707–2712

    Article  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 

  • McCarville MT, O’Neal ME, Potter B, Tilmon KJ, Cullen EM, McCornack BP, Tooker JF, Prischmann-Voldseth D (2014) One gene versus two: a regional study on the efficacy of single gene versus pyramided resistance for soybean aphid management. J Econ Entomol 107:1680–1687

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Mian MAR, Kang ST, Beil SE, Hammond RB (2008) 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 R (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  PubMed Central  Google Scholar 

  • Mundt C (1991) Probability of mutation of multiple virulence and durability of resistance gene pyramids: Further comments. Phytopathology 81:240–242

    Article  Google Scholar 

  • NASS (2015) National Agricultural Statistics Service. United States

  • Pawlowski M, Hill CB, Voegtlin DJ, Hartman GL (2014) Soybean aphid intrabiotype variability based on colonization of specific soybean genotypes. Insect Sci. doi:10.1111/1744-7917.12169

    PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Riedell W, Catangui M (2006) Greenhouse studies of soybean aphid (Hemiptera: Aphididae) effects on plant growth, seed yield and composition. J Agric Urban Entomol 23:225–235

    Google Scholar 

  • Tilmon K, Hodgson E, O’Neal M, Ragsdale D (2011) Biology of the soybean aphid, Aphis glycines (Hemiptera: Aphididae) in the United States. JIPM 2:A1–A7

    Article  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 

  • Wiarda SL, Fehr WR, O’Neal ME (2012) Soybean aphid (Hemiptera: Aphididae) development on soybean with Rag1 alone, Rag2 alone, and both genes combined. J Econ Entomol 105:252–258

    Article  CAS  PubMed  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 

  • Zhong YP, Xiao L, Wang B, Jiang YN, Yan JH, Cheng LJ, Wu TL (2014) Biotypic variation among soybean aphid isolates from four provinces in China. Crop Sci 54:2023–2029

    Article  Google Scholar 

Download references

Acknowledgements

We thank the United Soybean Board for partial funding for this research. We also thank Brian Diers for critically reviewing this manuscript.

Author information

Author notes

  1. Curtis B. Hill

    Present address: Agricen Sciences LLC, Pilot Point, TX, 76258, USA

Authors and Affiliations

  1. Department of Crop Sciences, University of Illinois, National Soybean Research Center, 1101 W. Peabody Dr., Urbana, IL, 61801, USA

    Curtis B. Hill, Derek Shiao, Carolyn M. Fox & Glen L. Hartman

  2. Indigo Agriculture, Urbana, IL, 61801, USA

    Derek Shiao

  3. USDA-ARS, Raleigh, NC, 27607, USA

    Carolyn M. Fox

  4. USDA-ARS, Urbana, IL, 61801, USA

    Glen L. Hartman

Authors
  1. Curtis B. Hill
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Derek Shiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carolyn M. Fox
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Glen L. Hartman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Glen L. Hartman.

Ethics declarations

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).

Additional information

Communicated by Henry T. Nguyen.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hill, C.B., Shiao, D., Fox, C.M. et al. Characterization and genetics of multiple soybean aphid biotype resistance in five soybean plant introductions. Theor Appl Genet 130, 1335–1348 (2017). https://doi.org/10.1007/s00122-017-2891-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-017-2891-7

Keywords

Search

Navigation