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QTL, additive and epistatic effects for SCN resistance in PI 437654

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Abstract

PI 437654 is a unique accession because of its resistance to nearly all HG types (races) of soybean cyst nematode (Heterodera glycines Ichinohe; SCN). Objectives of this study were to confirm and refine the locations and gene action associated with SCN resistance previously discovered in PI 437654, and to identify new QTLs that may have been missed because of low coverage with genetic markers used in previous studies. Using 205 F7:9 RILs and 276 SSR and AFLP molecular markers covering 2,406.5 cM of 20 linkage groups (LGs), we confirmed and refined the locations of major SCN resistance QTLs on LG-A2, -B1, and -G previously identified in PI 437654 or other resistant sources. We found that these major QTLs have epistatic effects among them or with other loci for SCN resistance. We also detected some new QTLs with additive or epistatic effects for SCN resistance to different HG types (races) on all LGs except LGs-B2 and -D1b. The QTL on LG-G was associated with resistance to HG types 2.5.7, 1.2.5.7, 0, and 2.7 (races 1, 2, 3, and 5), and it contributed a large proportion of the additive effects. The QTL on LG-A2 was associated with resistance to HG types 2.5.7 and 0 (races 1 and 3). The QTL on LG-B1, associated with resistance to HG types 2.5.7, 0, 2.7 (races 1, 3, and 5), was the similar QTL found in PI 90763 and PI 404198B. In addition to QTL on LGs-A2, -B1 and -G, a novel additive QTL associated with SCN resistance to HG types 0, 2.7, and 1.3.5.6.7 (race 3, 5, and 14) was identified on LG-I flanked by Sat_299 and Sat_189. Several minor QTLs on LGs-C1, D1a, H, and K were also found to be associated with SCN resistance. Confirmation of the new resistance QTL is underway by evaluating another RIL population with a different genetic background.

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References

  • Anand SC, Gallo KM, Baker IA, Hartwig EE (1988) Soybean plant introductions with resistance to races 4 or 5 of soybean cyst nematode. Crop Sci 28:563–564

    Google Scholar 

  • Arelli PR, Wilcox JA, Jr Myers, Gibson PT (1997) Soybean germplasm resistant to races 1 and 2 of Heterodera glycines. Crop Sci 37:1367–1369

    Google Scholar 

  • Arelli PR, Sleper DA, Yue P, Wilcox JA (2000) Soybean reaction to races 1 and 2 Heterodera glycines. Crop Sci 40:824–826

    Google Scholar 

  • Caldwell BE, Brim CA, Ross JP (1960) Inheritance of resistance of soybeans to the cyst nematode, Heterodera glycines. Agron J 52:635–636

    Google Scholar 

  • Carlborg O, Haley CS (2004) Epistasis: too often neglected in complex trait studies? Nat Rev Genet 5:618–624

    Article  PubMed  CAS  Google Scholar 

  • Carlborg O, Brockmann GA, Haley CS (2005) Simultaneous mapping of epistatic QTL in DU6i x DBA/2 mice. Mamm Genome 16:481–494

    Article  PubMed  CAS  Google Scholar 

  • Chang SJC, Doubler TW, Kilo VY, Abu-Thredeih J, Prabhu R, Freire V, Suttner R, Klein J, Schmidt ME, Gibson PT, Lightfoot DA (1997) Association of loci underlying field resistance to soybean sudden death syndrome (SDS) and cyst nematode (SCN) race 3. Crop Sci 37:965–971

    CAS  Google Scholar 

  • Chen Y, Wang D, Arelli P, Ebrahimi M, Nelson RL (2006) Molecular marker diversity of SCN-resistant sources in soybean. Genome 49:938–949

    Article  PubMed  CAS  Google Scholar 

  • Choi IY, Hyten DL, Matukumalli LK, Song Q, Chaky JM, Quigley CV, Chase K, Lark KG, Reiter RS, Yoon MS, Hwang EY, Yi SI, Young ND, Shoemaker RC, van Tassell CP, Specht JE, Cregan PB (2007) A soybean transcript map: gene distribution, haplotype and single-nucleotide polymorphism analysis. Genetics 176:685–696

    Article  PubMed  CAS  Google Scholar 

  • Concibido VC, Young ND, Lange DA, Denny RL, Orf JH (1996) RFLP mapping and marker-assisted selection of soybean cyst nematode resistance in PI 209332. Crop Sci 36:1643–1650

    Article  CAS  Google Scholar 

  • Concibido VC, Lange D, Denny RL, Orf J, Young N (1997) Genome mapping on soybean cyst nematode resistance genes in ‘Peking’, PI 90763, and PI 88788 using DNA markers. Crop Sci 37:258–264

    CAS  Google Scholar 

  • Concibido VC, Diers BW, Arelli PR (2004) A decade of QTL mapping for cyst nematode resistance in soybean. Crop Sci 44:1121–1131

    CAS  Google Scholar 

  • Cregan PB, Mudge J, Fickus EW, Danesh D, Denny R, Young ND (1999) Two simple sequence repeat markers to select for soybean cyst nematode resistance conditioned by the rhg1 locus. Theor Appl Genet 99:811–818

    Article  CAS  Google Scholar 

  • Diers BW, Arelli PR (1999) Management of parasitic nematodes of soybean through genetic resistance. In: Kauffman HE (ed) Proceedings of World soybean resistance conference, 6th. Chicago, IL, 4–7 August 1999. Superior Printing, Champaign, IL, pp 300–306

  • Diers BW, Skorupska HT, Rao-Arelli AP, Cianzio SR (1997) Genetic relationships among soybean plant introductions with resistance to soybean cyst nematode. Crop Sci 37:1966–1972

    Article  Google Scholar 

  • Fehr WR (1987) Heritability. In: Fehr WR (ed) Principles of cultivar development: theory and technique, vol I. Macmillan, New York, pp 95–105

    Google Scholar 

  • Glover KD, Wang D, Arelli PR, Carlson SR, Cianzio SR, Diers BW (2004) Near isogenic lines confirm a soybean cyst nematode resistance gene from PI 88788 on linkage group J. Crop Sci 44:936–941

    Google Scholar 

  • Golden AM, Epps JM, Riggs RD, Duclos LA, Fox JA, Bernard RL (1970) Terminology and identity of intraspecific forms of the soybean cyst nematode (Heterodera glycines). Plant Dis Rep 54:544–546

    Google Scholar 

  • Guo B, Sleper DA, Arelli PR, Shannon JG, Nguyen HT (2005) Identification of QTLs associated with resistance to soybean cyst nematode races 2, 3 and 5 in soybean PI 90763. Theor Appl Genet 111:965–971

    Article  PubMed  CAS  Google Scholar 

  • Guo B, Sleper DA, Nguyen HT, Arelli PR, Shannon JG (2006) Quantitative trait loci underlying resistance to three soybean cyst nematode populations in soybean PI 404198A. Crop Sci 46:224–233

    Article  CAS  Google Scholar 

  • Ha BK, Bennett JB, Hussey RS, Finnerty SL, Boerma HR (2007) SSR mapping and confirmation of soybean QTL from PI 437654 conditioning resistance to reniform nematode. Crop Sci 44:758–763

    Article  Google Scholar 

  • Heer JA, Knap HT, Mahalingam R, Shipe ER, Arelli PR, Matthews BF (1998) Molecular markers for resistance to Heterodera glycines in advanced soybean germplasm. Mol Breed 4:359–367

    Article  CAS  Google Scholar 

  • Jannink JL, Moreau L, Charmet G, Charcosset A (2008) Overview of QTL detection in plants and tests for synergistic epistatic interactions. Genetica. Aug 10. 10.1007/s10709-008-9306-2

  • Jansen RC, Stam P (1994) High resolution of quantitative traits into multiple loci via interval mapping. Genetics 136:1447–1455

    PubMed  CAS  Google Scholar 

  • Kassem MA, Meksem K, Wood AJ, Lightfoot DA (2007) Loci underlying SDS and SCN resistance mapped in the ‘Essex’ by ‘Forrest’ soybean recombinant inbred lines. Rev Biol Biotech 6:2–10

    Google Scholar 

  • Keim P, Olsen TC, Shoemaker RC (1988) A rapid protocol for isolating soybean DNA. Soybean Genet Newslett 15:147–148

    Google Scholar 

  • Lee GJ, Wu XL, Shannon JG, Sleper DA, Nguyen HT (2007) Oilseeds–Soybean. In: Kole C (ed) Genome mapping and molecular breeding in plants, vol 2. Springer, Heidelberg, pp 1–53

    Google Scholar 

  • Lewers K, Heinz R, Beard H, Marek L, Matthews B (2002) A physical map of a gene-dense region in soybean linkage group A2 near the black seed coat and Rhg (4) loci. Theor Appl Genet 104:254–260

    Article  PubMed  CAS  Google Scholar 

  • Liu P, Zhu J, Lu Y (2004) Marker-assisted selection in segregating generations of self-fertilizing crops. Theor Appl Genet 109:370–376

    PubMed  CAS  Google Scholar 

  • Liu G, Yang J, Xu H, Zhu J (2007) Influence of epistasis and QTL x environment interaction on heading date of rice (Oryza sativa L.). J Genet Genomics 34:608–615

    Article  PubMed  Google Scholar 

  • Lu P, Shannon JG, Sleper DA, Nguyen HT, Cianzio SR, Arelli PR (2006) Genetics of cyst nematode resistance in soybean PIs 467312 and 507354. Euphytica 149:259–265

    Article  Google Scholar 

  • Malmberg RL, Held S, Waits A, Mauricio R (2005) Epistasis for fitness-related quantitative traits in Arabidopsis thaliana grown in the field and in the greenhouse. Genetics 171:2013–2027

    Article  PubMed  CAS  Google Scholar 

  • Mansur LM, Carriquiry AL, Rao-Arelli AP (1993) Generation mean analysis of resistance to race-3 of soybean cyst-nematode. Crop Sci 33:1249–1253

    Google Scholar 

  • Matson AL, Williams LF (1965) Evidence of a fourth gene for resistance to the soybean cyst nematode. Crop Sci 5:477

    Article  Google Scholar 

  • Meksem K, Doubler TW, Chancharoenchai K, Njiti VN, Chang SJC, Arelli PR, Cregan PE, Gray LE, Gibson PT, Lightfoot DA (1999) Clustering among loci underlying soybean resistance to Fusarium solani, SDS and SCN in near-isogenic lines. Theor Appl Genet 99:1131–1142

    Article  CAS  Google Scholar 

  • Meksem K, Pangiotis P, Hyten D, Njiti V, Lightfoot DA, Arelli P (2001) Forrest resistance to soybean cyst nematode is bi-genic: saturation mapping of the rhg1 and Rhg4 loci. Theor Appl Genet 103:710–717

    Article  CAS  Google Scholar 

  • Mudge J, Cregan PB, Kenworthy JP, Kenworthy WJ, Orf JH, Young ND (1997) Two microsatellite markers that flank the major soybean cyst nematode resistance locus. Crop Sci 37:1611–1615

    Article  CAS  Google Scholar 

  • Myers GO, Anand SC (1991) Inheritance of resistance and genetic relationships among soybean plant introductions to races of soybean cyst nematode. Euphytica 55:197–201

    Article  Google Scholar 

  • Niblack TL, Arelli PR, Noel GR, Opperman CH, Orf J, Schmitt DP, Shannon JG, Tylka GL (2002) A revised classification scheme for genetically diverse populations of Heterodera glycines. J Nematol 34:279–288

    PubMed  CAS  Google Scholar 

  • Ohno Y, Tanase H, Nabika T, Otsuda K, Sasaki T, Suzawa T, Korii T, Yamori Y, Saruta T (2000) Selective genotyping with epistasis can be utilized for a major quantitative trait locus mapping in hypertension in rats. Genetics 155:785–792

    PubMed  CAS  Google Scholar 

  • Podlich DW, Winkler CR, Cooper M (2004) Mapping as you go: an effective approach for marker-assisted selection of complex traits. Crop Sci 44:1560–1571

    Google Scholar 

  • Prabhu RR, Njiti VN, Johnson BB, Johnson JE, Schmidt ME, Klein JH, Lightfoot DA (1999) Selecting soybean cultivars for dual resistance to soybean cyst nematode and sudden death syndrome using two DNA markers. Crop Sci 39:982–987

    Article  CAS  Google Scholar 

  • Purcell S, Sham PC (2004) Epistasis in quantitative trait locus linkage analysis: interaction or main effect? Behav Genet 34:143–152

    Article  PubMed  Google Scholar 

  • Qiu BX, Arelli PR, Sleper DA (1999) RFLP markers associated with soybean cyst nematode resistance and seed composition in a ‘Peking’ × ‘Essex’ population. Theor Appl Genet 98:356–364

    Article  CAS  Google Scholar 

  • Rao-Arelli AP (1994) Inheritance of resistance to Heterodera glycines race 3 in soybean accessions. Plant Dis 78:898–900

    Google Scholar 

  • Rinehart TA (2004) AFLP analysis using GeneMapper® software and an Excel® macro that aligns and converts output to binary. BioTechniques 37:186–188

    PubMed  CAS  Google Scholar 

  • Ruben E, Jamai A, Afzal J, Njiti VN, Triwitayakorn K, Iqbal MJ, Yaegashi S, Bashir R, Kazi S, Arelli P, Town CD, Ishihara H, Meksem K, Lightfoot DA (2006) Genomic analysis of the rhg1 locus: candidate genes that underlie soybean resistance to the cyst nematode. Mol Genet Genomics 276:503–516

    Article  PubMed  CAS  Google Scholar 

  • Schuster I, Abdelnoor RV, Marin SRR, Carvalho VP, Kiihl RAS, Silva JFV, Sediyama CS, Barros EG, Moreira MA (2001) Identification of a new major QTL associated with resistance to soybean cyst nematode (Heterodera glycines). Theor Appl Genet 102:91–96

    Article  CAS  Google Scholar 

  • Song QJ, Marek LF, Shoemaker RC, Lark KG, Concibido VC, Delannay X, Specht JE, Cregan PB (2004) A new integrated genetic linkage map of the soybean. Theor Appl Genet 109:122–128

    Article  PubMed  CAS  Google Scholar 

  • Van Ooijen JW, Voorrips RE (2001) JoinMap 3.0 software for the calculation of genetic linkage maps. Plant Research Internation, Wageningen

    Google Scholar 

  • Vierling RA, Faghihi J, Ferris VR, Ferris JM. (Inventors), Purdue Research Foundation (assignee) (2000) Methods for conferring broad-based soybean cyst nematode resistance to a soybean line. US patent 6,096,944, 1 Aug 2000

  • Vierling RA, Faghihi J, Ferris VR, Ferris JM (1996) Association of RFLP markers conferring broad-based resistance to the soybean cyst nematode (Heterodera glycines). Theor Appl Genet 92:83–86

    Article  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4417

    Article  PubMed  CAS  Google Scholar 

  • Webb DM, inventor; Pioneer Hi-Bred International Inc., assignee (2003) Quantitative trait loci associated with cyst nematode resistance and uses thereof. US patent 6,538,175, 25 Mar 2003

  • Webb DM, Baltazar BM, Rao-Arelli PA, Schupp J, Clayton K, Keim P, Beavis WD (1995) Genetic mapping of soybean cyst nematode race-3 resistance loci in soybean PI 437654. Theor Appl Genet 91:574–581

    Article  CAS  Google Scholar 

  • Weismann JM, Matthews BF, Devine TE (1992) Molecular markers located proximal to the soybean cyst nematode resistance gene, Rhg4. Theor Appl Genet 85:136–138

    Google Scholar 

  • Wilfert L, Schmid-Hempel P (2008) The genetic architecture of susceptibility to parasites. BMC Evol Biol 8:187

    Article  PubMed  CAS  Google Scholar 

  • Winter SMJ, Shelp BJ, Anderson TR, Welacky TW, Rajcan I (2006) QTL associated with horizontal resistance to soybean cyst nematode in Glycine soja PI 464925B. Theor Appl Genet 114:461–472

    Article  PubMed  Google Scholar 

  • Wrather JA, Koenning SR (2006) Estimates of disease effects on soybean yields in the United States 2003 to 2005. J Nematol 38:173–180

    PubMed  Google Scholar 

  • Wrather JA, Anderson TR, Arsyad DM, Tan Y, Ploper LD, Porta-Puglia A, Ram HH, Yorinori JT (2001) Soybean disease loss estimates for the top ten soybean producing countries in 1998. Can J Plant Pathol 23:115–121

    Google Scholar 

  • Wu X, Larson SR, Hu Z, Palazzo AJ, Jones TA, Wang RR, Jensen KB, Chatterton NJ (2003) Molecular genetic linkage maps for allotetraploid Leymus wildryes (Gramineae: Triticeae). Genome 46:627–646

    Article  PubMed  CAS  Google Scholar 

  • Wu XL, Zhong G, Findley SD, Cregan P, Stacey G, Nguyen HT (2008) Genetic marker anchoring by six-dimensional pools for development of a soybean physical map. BMC Genomics 9:28

    Article  PubMed  CAS  Google Scholar 

  • Yang J, Zhu J (2005) Methods for predicting superior genotypes under multiple environments based on QTL effects. Theor Appl Genet 110:1268–1274

    Article  PubMed  Google Scholar 

  • Yang J, Zhu J, Williams RW (2007) Mapping the genetic architecture of complex traits in experimental populations. Bioinformatics 23:1527–1536

    Article  PubMed  CAS  Google Scholar 

  • Yue P, Arelli PR, Sleper DA (2001a) Molecular characterization of resistance to Heterodera glycines in soybean PI 438489B. Theor Appl Genet 102:921–928

    Article  CAS  Google Scholar 

  • Yue P, Sleper DA, Arelli PR (2001b) Mapping resistance to multiple races of Heterodera glycines in soybean PI 89772. Crop Sci 41:1589–1595

    Article  CAS  Google Scholar 

  • Zeng Z-B (1993) Theoretical basis of separation of multiple linked gene effects on mapping quantitative trait loci. Proc Natl Acad Sci USA 90:10972–10976

    Article  PubMed  CAS  Google Scholar 

  • Zeng Z-B (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468

    PubMed  CAS  Google Scholar 

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Acknowledgments

This research was supported by the National Center for Soybean Biotechnology and the Missouri Soybean Merchandising Council. We thank John A. Wilcox for assistance in phenotyping RILs for SCN resistance to the various HG types and Kerry M. Clark for increasing seed of genotypes used in this study.

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Authors and Affiliations

  1. Division of Plant Sciences and National Center for Soybean Biotechnology, University of Missouri-Columbia, Columbia, MO, 65211, USA

    Xiaolei Wu, Sean Blake, David A. Sleper & Henry T. Nguyen

  2. University of Missouri, Delta Center, P.O. Box 160, Portageville, MO, 63873, USA

    J. Grover Shannon

  3. Soybean Genomics and Improvement Laboratory, USDA-ARS, Beltsville, MD, 20705, USA

    Perry Cregan

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  1. Xiaolei Wu
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  2. Sean Blake
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  3. David A. Sleper
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  6. Henry T. Nguyen
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Correspondence to Xiaolei Wu or Henry T. Nguyen.

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Communicated by D. A. Lightfoot.

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Wu, X., Blake, S., Sleper, D.A. et al. QTL, additive and epistatic effects for SCN resistance in PI 437654. Theor Appl Genet 118, 1093–1105 (2009). https://doi.org/10.1007/s00122-009-0965-x

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