Skip to main content
Log in

Mapping QTLs with main and epistatic effects underlying grain yield and heading time in soft winter wheat

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

Abstract

There is increasing awareness that epistasis plays a role for the determination of complex traits. This study employed an association mapping approach in a large panel of 455 diverse European elite soft winter wheat lines. The genotypes were evaluated in multi-environment trials and fingerprinted with SSR markers to dissect the underlying genetic architecture of grain yield and heading time. A linear mixed model was applied to assess marker-trait associations incorporating information of covariance among relatives. Our findings indicate that main effects dominate the control of grain yield in wheat. In contrast, the genetic architecture underlying heading time is controlled by main and epistatic effects. Consequently, for heading time it is important to consider epistatic effects towards an increased selection gain in marker-assisted breeding.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allison DB, Fernandez JR, Moonseong H, Shankuan Z, Etzel C, Beasley TM, Amos CI (2002) Bias in estimates of quantitative-trait-locus effect in genome scans: demonstration of the phenomenon and a method-of-moments procedure for reducing bias. Am J Hum Genet 70:575–585

    Article  PubMed  CAS  Google Scholar 

  • Barton NH, Charlesworth B (1998) Why sex and recombination? Science 281:1986–1990

    Article  PubMed  CAS  Google Scholar 

  • Beavis WB (1998) QTL analyses: power, precision, and accuracy. In: Patterson AH (ed) Molecular dissection of complex traits. CRC Press, Boca Raton

    Google Scholar 

  • Bernardo R (1993) Estimation of coefficient of coancestry using molecular markers in maize. Theor Appl Genet 85:1055–1062

    Article  CAS  Google Scholar 

  • Boone C, Bussey H, Andrews BJ (2007) Exploring genetic interactions and networks with yeast. Nat Rev Genet 8:437–449

    Article  PubMed  CAS  Google Scholar 

  • Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177

    Article  PubMed  Google Scholar 

  • Buckler ES, Holland JB, Bradbury PJ, Acharya CB, Brown PJ, Browne C, Ersoz E, Flint-Garcia S et al (2009) The genetic architecture of maize flowering time. Science 325:714–718

    Article  PubMed  CAS  Google Scholar 

  • Campbell BT, Baenzigar PS, Gill KS, Eskridge KM, Budak H, Erayman M, Dweikat I, Yen Y (2003) Identification of QTLs and environmental interactions associated with agronomic traits on chromosome 3A of wheat. Crop Sci 43:1493–1505

    Article  CAS  Google Scholar 

  • Carlborg Ö, Jacobsson L, Ahgren P, Siegel P, Andersson L (2006) Epistasis and the release of genetic variation during long-term selection. Nat Genet 38:418–420

    Article  PubMed  CAS  Google Scholar 

  • Carver BF, Rayburn AL (1994) Comparison of related wheat stocks possessing 1B or 1RS.1BL chromosomes: agronomic performance. Crop Sci 34:1505–1510

    Article  Google Scholar 

  • Chao S, Zhang W, Dubcosky J, Sorrels ME (2007) Evaluation of genetic diversity and genome-wide linkage disequilibrium among US wheat (Triticum aestivum L.) germplasm representing different market classes. Crop Sci 47:1018–1030

    Article  CAS  Google Scholar 

  • Cheverud JM, Routman EJ (1996) Epistasis as a source of increased additive genetic variance at population bottlenecks. Evolution 50:1042–1051

    Article  Google Scholar 

  • Cochran WG, Cox GM (1957) Experimental designs, 2nd edn. John Wiley & Sons, New York

    Google Scholar 

  • Coyne JA (1992) Genetics and speciation. Nature 355:511–515

    Article  PubMed  CAS  Google Scholar 

  • Crossa J, Burgueño J, Dreisigacker S, Vargas M, Herrera-Foessel SA, Morten L, Singh RP, Trethowan R, Warburton M, Franco J, Reynolds M, Crouch JH, Ortiz R (2007) Association analysis of historical bread wheat germplasm using additive genetic covariance of relatives and population structure. Genetics 177:1889–1913

    Article  PubMed  CAS  Google Scholar 

  • Distelfeld A, LI C, Dubcovsky J (2009) Regulation of flowering in temperate cereals. Curr Opin Plant Biol 12:178–184

    Article  PubMed  CAS  Google Scholar 

  • El-Lithy ME, Bentsink L, Hanhart CJ, Ruys GJ, Rovito D, Broekhof JLM, van der Poel HJA, van Eijk MJT, Vreugdenhil D, Koornneef M (2006) New Arabidopsis recombinant inbred line populations genotyped using SNPWave and their use for mapping flowering-time quantitative trait loci. Genetics 172:1867–1876

    Article  PubMed  CAS  Google Scholar 

  • Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374

    Article  PubMed  CAS  Google Scholar 

  • Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2006) ASReml User Guide Release 2.0. VSN International, Hemel Hempstead

    Google Scholar 

  • Goldringer I, Brabant P, Gallais A (1997) Estimation of additive and epistatic genetic variances for agronomic traits in a population of doubled-haploid lines of wheat. Heredity 79:60–71

    Article  Google Scholar 

  • Goodnight CJ (1987) On the effect of founder events on epistatic genetic variance. Evolution 41:80–91

    Article  Google Scholar 

  • Göring HHH, Terwilliger JD, Blangero J (2001) Large upward bias in estimation of locus-specific effects from genome-wide scans. Am J Hum Genet 69:1357–1369

    Article  PubMed  Google Scholar 

  • Gower JC (1966) Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53:325–338

    Google Scholar 

  • Griffiths S, Simmonds J, Leverington M, Wang Y, Fish L, Sayers L, Alibert L, Orford S, Wingen L, Herry L, Faure S, Laurie D, Bilham L, Snape J (2009) Meta-QTL analysis of the genetic control of ear emergence in elite European winter wheat germplasm. Theor Appl Genet 119:383–395

    Article  PubMed  CAS  Google Scholar 

  • Habier D, Totir LR, Fernando RL (2010) A Two-stage approximation for analysis of mixture genetic models in large pedigrees. Genetics 185:655–670

    Article  PubMed  CAS  Google Scholar 

  • Hack H, Bleiholder H, Buhr L, Meier U, Schnock-Fricke U, Weber E, Witzenberger A (1992) Einheitliche Codierung der phänologischen Entwicklungsstadien mono- und dikotyler Pflanzen–Erweiterte BBCH-Skala, Allgemein. Nachrichtenbl Deut Pflanzenschutzd 44:265–270

    Google Scholar 

  • Hallauer AR, Miranda JB (1981) Quantitative genetics in maize breeding. Iowa State University Press, Ames

    Google Scholar 

  • Hanocq E, Niarquin M, Heumez E, Rousset M, Legouis J (2004) Detection and mapping of QTL for earliness components in a bread wheat recombinant inbred lines population. Theor Appl Genet 110:106–115

    Article  PubMed  CAS  Google Scholar 

  • Hanocq E, Laperche A, Jaminon O, Lainé AL, Legouis J (2007) Most significant genome regions involved in the control of earliness traits in bread wheat, as revealed by QTL meta-analysis. Theor Appl Genet 114:569–584

    Article  PubMed  CAS  Google Scholar 

  • Hedrick PW (1987) Gametic disequilibrium measures: proceed with caution. Genetics 117:331–341

    PubMed  CAS  Google Scholar 

  • Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70

    Google Scholar 

  • Kearsey MJ, Jinks JL (1968) A general method of detecting additive, dominance and epistatic variation for metrical traits. I. Theory. Heredity 23:403–409

    Article  PubMed  CAS  Google Scholar 

  • Komeda Y (2004) Genetic regulation of time to flower in Arabidopsis thaliana. Annu Rev Plant Biol 55:521–535

    Article  PubMed  CAS  Google Scholar 

  • Kraakman ATW, Niks RE, Van den Berg PMMM, Stam P, Van Eeuwijk FA (2004) Linkage disequilibrium mapping of yield and yield stability in modern spring barley cultivars. Genetics 168:435–446

    Article  PubMed  CAS  Google Scholar 

  • Kuchel H, Hollamby GJ, Langridge P, Williams KJ, Jefferies SP (2006) Identification of genetic loci associated with ear-emergence in bread wheat. Theor Appl Genet 113:1103–1112

    Article  PubMed  CAS  Google Scholar 

  • Kuchel H, Williams KJ, Langridge P, Eagles HA, Jefferies SP (2007) Genetic dissection of grain yield in bread wheat. I. QTL analysis. Theor Appl Genet 115:1029–1041

    Article  PubMed  CAS  Google Scholar 

  • Kumar N, Kulwal PL, Balyan HS, Gupta PK (2007) QTL mapping for yield and yield contributing traits in two mapping populations of bread wheat. Mol Breed 19:163–177

    Article  Google Scholar 

  • Lamkey KR, Schnicker BJ, Melchinger AE (1995) Epistasis in an elite maize hybrid and choice of generation for inbred line development. Crop Sci 35:1272–1281

    Article  Google Scholar 

  • Law CN, Worland AJ (1997) Genetic analysis of some flowering time and adaptive traits in wheat. New Phytol 137:19–28

    Article  Google Scholar 

  • Le Rouzic A, Alvarez-Castro JM (2008) Estimation of genetic effects and genotype-phenotype maps. Evol Bioinform 4:225–235

    CAS  Google Scholar 

  • Leamy LJ, Workman MS, Routman EJ, Cheverud JM (2005) An epistatic genetic basis for fluctuating asymmetry of tooth size and shape in mice. Heredity 94:316–325

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Pinson SRM, Park WD, Paterson AH, Stansel JW (1997) Epistasis for three grain yield components in rice (Oryza sativa L.). Genetics 145:452–465

    Google Scholar 

  • Li S, Jia J, Wei X, Zhang X, Li L, Chen H, Fan Y, Sun H, Zhao X, Lei T, Xu Y, Jiang F, Wang H, Li L (2007) A intervarietal genetic map and QTL analysis for yield traits in wheat. Mol Breed 20:167–178

    Article  Google Scholar 

  • Maurer HP, Melchinger AE, Frisch M (2008) Population genetic simulation and data analysis with Plabsoft. Euphytica 161:133–139

    Article  Google Scholar 

  • McCarthy MI, Abecasis GR, Cardon LR, Goldstein DB, Little J, Ioannidis JPA, Hirschhorn JN (2008) Genome-wide association studies for complex traits: consensus, uncertainty and challenges. Nat Rev Genet 9:356–369

    Article  PubMed  CAS  Google Scholar 

  • Melchinger AE, Utz HF, Schön CC (1998) Quantitative trait locus (QTL) mapping using different testers and independent population samples in maize reveals low power of QTL detection and larger bias in estimates of QTL effects. Genetics 149:383–403

    PubMed  CAS  Google Scholar 

  • Melchinger AE, Piepho H-P, Utz HF, Muninovic J, Wegenast T, Törjek O, Altmann T, Kusterer B (2007) Genetic basis of heterosis for growth-related traits in Arabidopsis investigated by testcross progenies of near-isogenic lines reveals a significant role of epistasis. Genetics 177:1827–1837

    Article  PubMed  Google Scholar 

  • Montooth KL, Marden JH, Clark AG (2003) Mapping determinants of variation in energy metabolism, respiration and flight in drosophila. Genetics 165:623–635

    PubMed  CAS  Google Scholar 

  • Myles S, Peiffer J, Brown PJ, Ersoz ES, Zhang Z, Costich DE, Buckler ES (2009) Association mapping: critical considerations shift from genotyping to experimental design. Plant Cell 21:2194–2202

    Article  PubMed  CAS  Google Scholar 

  • Nyholt DR, LaForge KS, Kallela M, Alakurtti K, Anttila V, Färkkilä M, Hämaläinen E, Kaprio J, Kaunisto MA et al (2008) A high-density association screen of 155 ion transport genes for involvement with common migraine. Hum Mol Genet 17:3318–3331

    Article  PubMed  CAS  Google Scholar 

  • Phillips PC (2008) Epistasis–the essential role of gene interactions in the structure and evolution of genetic systems. Nat Rev Genet 9:855–867

    Article  PubMed  CAS  Google Scholar 

  • Quarrie SA, Steed A, Calestani C, Semikhodskii A, Lebreton C, Chinoy C, Steele N, Pljevljakusic D, Waterman E, Weyen J, Schondelmaier J, Habash DZ, Farmer P, Saker L, Clarkson DT, Abugalieva A, Yessimbekova M, Turuspekov Y, Abugalieva S, Tuberosa R, Sanguineti M-C, Hollington PA, Aragues R, Royo A, Dodig D (2005) A high density genetic map of hexaploid wheat (Triticum aestivum L.) from the cross Chinese Spring × SQ1 and its use to compare QTLs for grain yield across a range of environments. Theor Appl Genet 110:865–880

    Article  PubMed  CAS  Google Scholar 

  • Quarrie SA, Pekic Quarrie S, Radosevic R, Rancic D, Kaminska A, Barnes JD, Leverington M, Ceoloni C, Dodig D (2006) Dissecting a wheat QTL for yield present in a range of environments: from the QTL to candidate genes. J Exp Bot 57:2627–2637

    Article  PubMed  CAS  Google Scholar 

  • Reif JC, Hallauer AR, Melchinger AE (2005) Heterosis and heterotic patterns in maize. Maydica 50:215–223

    Google Scholar 

  • Scarth R, Law CN (1984) The control of the day-length response in wheat by the group 2 chromosomes. Z. Pflanzenzuechtung 92:140–150

    Google Scholar 

  • Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109:1105–1114

    Article  PubMed  CAS  Google Scholar 

  • Sourdille P, Snape JW, Cadalen T, Charmet G, Nakata N, Bernard S, Bernard M (2000) Detection of QTLs for heading time and photoperiod response in wheat using a doubled-haploid population. Genome 43:487–494

    Article  PubMed  CAS  Google Scholar 

  • Stich B, Melchinger AE, Frisch M, Maurer HP, Heckenberger M, Reif JC (2005) Linkage disequilibrium in European elite maize germplasm investigated with SSRs. Theor Appl Genet 111:723–730

    Article  PubMed  Google Scholar 

  • Stich B, Melchinger AE, Piepho HP, Hamrit S, Schipprack W, Maurer HP, Reif JC (2007) Potential causes of linkage disequilibrium in a European maize breeding program investigated with computer simulations. Theor Appl Genet 115:529–536

    Article  PubMed  Google Scholar 

  • Stich B, Melchinger AE, Heckenberger M, Möhring J, Schechert A, Piepho H-P (2008a) Association mapping in multiple segregating populations of sugar beet (Beta vulgaris L.). Theor Appl Genet 117:1167–1179

    Article  PubMed  Google Scholar 

  • Stich B, Möhring J, Piepho H-P, Heckenberger M, Buckler ES, Melchinger AE (2008b) Comparison of mixed-model approaches for association mapping. Genetics 178:1745–1754

    Article  PubMed  Google Scholar 

  • Trethowan R, Reynolds MP, Ortiz-Monasterio I, Ortiz R (2007) The genetic basis of the green revolution in wheat production. Plant Breed Rev 28:39–58

    Article  CAS  Google Scholar 

  • Utz HF, Melchinger AE, Schön CC (2000) Bias and sampling error of the estimated proportion of genotypic variance explained by quantitative trait loci determined from experimental data in maize using cross validation and validation with independent samples. Genetics 154:1839–1849

    PubMed  Google Scholar 

  • Uwatoko N, Onishi A, Ikeda Y, Kontani M, Sasaki A, Matsubara K, Itoh Y, Sano Y (2008) Epistasis among the three major flowering time genes in rice: coordinate changes of photoperiod sensitivity, basic vegetative growth and optimum photoperiod. Euphytica 163:167–175

    Article  CAS  Google Scholar 

  • Worland AJ, Börner A, Korzun V, Li WM, Petrovic S, Sayers EJ (1998) The influence of photoperiod genes to the adaptability of European winter wheats. Euphytica 100:385–394

    Article  CAS  Google Scholar 

  • Wright S (1978) Evolution and genetics of populations, variability within and among natural populations, 4th edn. The University of Chicago Press, Chicago, p 91

    Google Scholar 

  • Würschum T, Maurer HP, Schulz B, Möhring J, Reif JC (2011) Genome-wide association mapping reveals epistasis and genetic interaction networks in sugar beet. Theor Appl Genet (in press)

  • Xu S, Jia Z (2007) Genome-wide analysis of epistatic effects for quantitative traits in barley. Genetics 175:1955–1963

    Article  PubMed  CAS  Google Scholar 

  • Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley J, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208

    Article  PubMed  CAS  Google Scholar 

  • Zhao K, Aranzana MJ, Kim S, Lister C, Shindo C, Tang C, Toomajian C, Zheng H, Dean C, Marjoram P, Nordborg M (2007) An Arabidopsis example of association mapping in structured samples. PLoS Genet 3:e4

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This research was conducted within the Biometric and Bioinformatic Tools for Genomics based Plant Breeding project supported by the German Federal Ministry of Education and Research (BMBF) within the framework of GABI–FUTURE initiative.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jochen C. Reif.

Additional information

Communicated by X. Xia.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reif, J.C., Maurer, H.P., Korzun, V. et al. Mapping QTLs with main and epistatic effects underlying grain yield and heading time in soft winter wheat. Theor Appl Genet 123, 283–292 (2011). https://doi.org/10.1007/s00122-011-1583-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-011-1583-y

Keywords

Navigation