, 215:4 | Cite as

Genome-wide association study for an efficient selection of Fusarium head blight resistance in winter triticale

  • Ana L. Galiano-Carneiro
  • Philipp H. G. Boeven
  • Hans Peter Maurer
  • Tobias Würschum
  • Thomas MiedanerEmail author


Fusarium head blight (FHB) is one of the most serious diseases in small-grain cereals including triticale (× Triticosecale Wittmack). The disease reduces yield and accumulates mycotoxins which are harmful to human and animal health. Triticale grain is almost exclusively used on-farm in feed formulations for swine and other animals, and swine is the most susceptible farm animal to Fusarium mycotoxins. In order to evaluate the potential of genomics-assisted breeding to FHB, we performed the first genome-wide association study for FHB resistance in triticale. QTL for FHB resistance were identified on chromosomes 2A, 2B, 5B and 3R with an explained genotypic variance ranging from 0.28 to 30.23% and a total explained genetic variance of 56.64%. A QTL on chromosome 3R that explained 15.38% of the genotypic variance was identified for the first time. Association mapping was complemented by genome-wide prediction, which yielded a high prediction accuracy of 0.78 for FHB resistance when weighted genomic selection was performed. Collectively our findings highlight the potential of genomics-assisted approaches to improve Fusarium resistance in triticale in early generations.


Fusarium head blight (FHB) Genome-wide association (GWA) Genomics-assisted breeding (GAB) Genomic selection (GS) Triticale 



Best linear unbiased estimators




Fusarium head blight


Flowering time


Genomic estimated breeding value


Genomic selection


Genome-wide association




Minor allele frequency


Marker-assisted selection




Principal component analysis


Plant height


Quantitative trait loci


Ridge-regression BLUP


Weighted ridge-regression BLUP





The molecular marker data was funded by the Federal Ministry of Food and Agriculture (BMEL) through its project management body Fachagentur für Nachwachsende Rohstoffe e.V. (FNR) (Grants: 22406112, 22406212, 22406312, and 22406412). We thank the Federal Ministry of Food and Agriculture (BMEL) based on a decision of the Parliament of the Federal Republic of Germany via the Federal Office for Agriculture and Food (BLE) under the innovation support program within the PRIMA cooperative project (Grant No. 2818202815) for financially supporting the first author of this project. The authors also would like to thank Tizian Zollinger for the collection of phenotypic data within his master thesis and Dr. S. Weissmann, HegeSaat GmbH & Co. KG, Singen, for providing genotypes. We highly appreciate the excellent technical support of the teams at Hohenheim and Oberer Lindenhof.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standard

The authors declare that the experiments comply with the current laws of Germany.

Supplementary material

10681_2018_2327_MOESM1_ESM.pdf (111 kb)
Supplementary material 1 (PDF 111 kb)


  1. Audenaert K, Vanheule A, Höfte M, Haesaert G (2013) Deoxynivalenol: a major player in the multifaceted response of Fusarium to its environment. Toxins 6:1–19. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aulchenko YS, Ripke S, Isaacs A, van Duijn CM (2007) GenABEL: an R library for genome-wide association analysis. Bioinformatics 23:1294–1296. CrossRefPubMedGoogle Scholar
  3. Bassi FM, Bentley AR, Charmet G et al (2016) Breeding schemes for the implementation of genomic selection in wheat (Triticum spp.). Plant Sci 242:23–36. CrossRefPubMedGoogle Scholar
  4. Becher R, Miedaner T, Wirsel SGR (2013) Biology, diversity, and management of FHB-causing Fusarium species in small-grain cereals. In: Kempken F (ed) Agricultural applications. 2nd Edition. The Mycota XI. Springer, Berlin, pp 199–241CrossRefGoogle Scholar
  5. Bennett JW, Klich M (2003) Mycotoxins. Clin Microbiol Rev 16:497–516. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bird SH, Rowe JB, Choct M et al (1999) In vitro fermentation of grain and enzymatic digestion of cereal starch. Recent Adv Anim Nutr Aust 12:53–62Google Scholar
  7. Boeven PHG, Longin CFH, Leiser WL et al (2016a) Genetic architecture of male floral traits required for hybrid wheat breeding. Theor Appl Genet 129:2343–2357. CrossRefPubMedGoogle Scholar
  8. Boeven PHG, Würschum T, Weissmann S et al (2016b) Prediction of hybrid performance for Fusarium head blight resistance in triticale (× Triticosecale Wittmack). Euphytica 207:475–490. CrossRefGoogle Scholar
  9. Bolduan C, Miedaner T, Schipprack W et al (2009) Genetic variation for resistance to ear rots and mycotoxins contamination in early European maize inbred lines. Crop Sci 49:2019–2028. CrossRefGoogle Scholar
  10. Buerstmayr H, Steiner B, Lemmens M, Ruckenbauer P (2000) Resistance to Fusarium head blight in winter wheat: heritability and trait associations. Crop Sci 40:1012–1018. CrossRefGoogle Scholar
  11. Bundessortenamt (2014) Beschreibende Sortenliste: Getreide, Mais, Öl- und Faserpflanzen, Leguminosen, Rüben, Zwischenfrüchte. Accessed 9th Aug 2018
  12. Čonková E, Laciaková A, Kováč G, Seidel H (2003) Fusarial toxins and their role in animal diseases. Vet J 165:214–220. CrossRefPubMedGoogle Scholar
  13. Dhariwal R, Fedak G, Dion Y et al (2018) High density single nucleotide polymorphism (SNP) mapping and quantitative trait loci (QTL) analysis in a biparental spring triticale population localized major and minor effect Fusarium head blight resistance and associated traits QTL. Genes 9:1–26. CrossRefGoogle Scholar
  14. EFSA (2004) Opinion of the scientific panel on contaminants in the food chain on a request from the commission related to deoxynivalenol (DON) as undesirable substance in animal feed. EFSA J 73:1–41Google Scholar
  15. Emrich K, Wilde F, Miedaner T, Piepho HP (2008) REML approach for adjusting the Fusarium head blight rating to a phenological date in inoculated selection experiments of wheat. Theor Appl Genet 117:65–73. CrossRefPubMedGoogle Scholar
  16. Endelman JB (2011) Ridge regression and other kernels for genomic selection with R package rrBLUP. Plant Genome J 4:250–255. CrossRefGoogle Scholar
  17. Endelman JB, Jannink J (2012) Shrinkage estimation of the realized relationship matrix. G3 Genes Genomes Genet 2:1405–1413. CrossRefGoogle Scholar
  18. European Commission (2006) Commission Recommendation (EC) No 576/2006 on the presence of deoxynivalenol, zearalenone, ochratoxin A, T-2 and HT-2 and fumonisins in products intended for animal feeding. = OJ:L:2006:229:0007:0009:EN:PDF. Accessed on 23rd March 2015
  19. FAOSTAT (2018) Statistical databases and datasets of the food and agriculture organization of the United Nations. Accessed 5th Feb 2018
  20. Fisher RA (1921) On the “probable error” of a coefficient of correlation deduced from a small sample. Metron 1:3–32Google Scholar
  21. Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2009) ASReml user guide release 3.0. VSN International Ltd, Hemel Hempstead, p 275Google Scholar
  22. Gowda M, Hahn V, Reif JC et al (2011) Potential for simultaneous improvement of grain and biomass yield in Central European winter triticale germplasm. Field Crops Res 121:153–157. CrossRefGoogle Scholar
  23. Gowda M, Zhao Y, Würschum T, Longin CF et al (2014) Relatedness severely impacts accuracy of marker-assisted selection for disease resistance in hybrid wheat. Heredity 112:552–561. CrossRefPubMedGoogle Scholar
  24. Hackauf B, Haffke S, Fromme FJ et al (2017) QTL mapping and comparative genome analysis of agronomic traits including grain yield in winter rye. Theor Appl Genet 130:1801–1817. CrossRefPubMedGoogle Scholar
  25. Hallauer AR, Carena MJ, Filho J (2010) Quantitative genetics in maize breeding, 3rd edn. Handbook of plant breeding. Springer, New YorkGoogle Scholar
  26. Heffner EL, Lorenz AJ, Jannink JL, Sorrells ME (2010) Plant breeding with Genomic selection: gain per unit time and cost. Crop Sci 50:1681–1690. CrossRefGoogle Scholar
  27. Jiang Y, Schulthess AW, Rodemann B et al (2017) Validating the prediction accuracies of marker-assisted and genomic selection of Fusarium head blight resistance in wheat using an independent sample. Theor Appl Genet 130:471–482. CrossRefPubMedGoogle Scholar
  28. Kalih R, Maurer HP, Hackauf B, Miedaner T (2014) Effect of a rye dwarfing gene on plant height, heading stage, and Fusarium head blight in triticale (× Triticosecale Wittmack). Theor Appl Genet 127:1527–1536. CrossRefPubMedGoogle Scholar
  29. Kalih R, Maurer HP, Miedaner T (2015) Genetic architecture of fusarium head blight resistance in four winter triticale populations. Phytopathology 105:334–341. CrossRefPubMedGoogle Scholar
  30. Lander ES, Schork NJ (1994) Genetic dissection of complex traits. Science 265:2037–2048CrossRefGoogle Scholar
  31. Liu W, Leiser WL, Maurer HP et al (2015) Evaluation of genomic approaches for marker-based improvement of lodging tolerance in triticale. Plant Breed 134:416–422CrossRefGoogle Scholar
  32. Löffler M, Schön CC, Miedaner T (2009) Revealing the genetic architecture of FHB resistance in hexaploid wheat (Triticum aestivum L.) by QTL meta-analysis. Mol Breed 23:473–488. CrossRefGoogle Scholar
  33. Losert D, Maurer HP, Leiser WL, Würschum T (2017a) Defeating the Warrior: genetic architecture of triticale resistance against a novel aggressive yellow rust race. Theor Appl Genet 130:685–696. CrossRefPubMedGoogle Scholar
  34. Losert D, Maurer HP, Marulanda JJ, Würschum T (2017b) Phenotypic and genotypic analyses of diversity and breeding progress in European triticale (× Triticosecale Wittmack). Plant Breed 136:18–27. CrossRefGoogle Scholar
  35. Martin M, Dhillon BS, Miedaner T, Melchinger AE (2012) Inheritance of resistance to Gibberella ear rot and deoxynivalenol contamination in five flint maize crosses. Plant Breed 131:28–32. CrossRefGoogle Scholar
  36. McGill R, Tukey JW, Larsen WA (1978) Variations of box plots. Am Stat 32(1):12–16Google Scholar
  37. Mergoum M, Singh PK, Peña RJ et al (2009) Triticale: a ‘new’ crop with old challenges. In: Carena MJ (ed) Cereals. Handbook of plant breeding, vol 3. Springer, New York, NY, pp 267–287. CrossRefGoogle Scholar
  38. Mesterházy A (1995) Types and components of resistance to Fusarium head blight of wheat. Plant Breed 114:377–386. CrossRefGoogle Scholar
  39. Miedaner T (1997) Breeding wheat and rye for resistance to Fusarium diseases. Plant Breed 116:201–220. CrossRefGoogle Scholar
  40. Miedaner T, Voss HH (2008) Effect of dwarfing Rht genes on fusarium head blight resistance in two sets of near-isogenic lines of wheat and check cultivars. Crop Sci 48:2115–2122. CrossRefGoogle Scholar
  41. Miedaner T, Heinrich N, Schneider B et al (2004) Estimation of deoxynivalenol (DON) content by symptom rating and exoantigen content for resistance selection in wheat and triticale. Euphytica 139:123–132. CrossRefGoogle Scholar
  42. Miedaner T, Caixeta F, Talas F (2013) Head-blighting populations of Fusarium culmorum from Germany, Russia, and Syria analyzed by microsatellite markers show a recombining structure. Eur J Plant Pathol 137:743–752. CrossRefGoogle Scholar
  43. Miedaner T, Kalih R, Großmann MS, Maurer HP (2016) Correlation between Fusarium head blight severity and DON content in triticale as revealed by phenotypic and molecular data. Plant Breed 135:31–37. CrossRefGoogle Scholar
  44. Miedaner T, Sieber AN, Desaint H et al (2017) The potential of genomic-assisted breeding to improve Fusarium head blight resistance in winter durum wheat. Plant Breed 136:610–619. CrossRefGoogle Scholar
  45. Mirdita V, He S, Zhao Y, Korzun V et al (2015) Potential and limits of whole genome prediction of resistance to Fusarium head blight and Septoria tritici blotch in a vast Central European elite winter wheat population. Theor Appl Genet 128:2471–2481. CrossRefPubMedGoogle Scholar
  46. Money D, Gardner K, Migicovsky Z et al (2015) LinkImpute: fast and accurate genotype imputation for nonmodel organisms. Genes Genomes Genet 5:2383–2390. CrossRefGoogle Scholar
  47. Oettler G (2005) The fortune of a botanical curiosity—triticale: past, present and future. J Agric Sci 143:329–346. CrossRefGoogle Scholar
  48. Oettler G, Wahle G (2001) Genotypic and environmental variation of resistance to head blight in triticale inoculated with Fusarium culmorum. Plant Breed 120:297–300. CrossRefGoogle Scholar
  49. Oettler G, Heinrich N, Miedaner T (2004) Estimates of additive and dominance effects for Fusarium head blight resistance of winter triticale. Plant Breed 123:525–530CrossRefGoogle Scholar
  50. Passioura JB (1996) Drought and drought tolerance. Plant Growth Regul 20:79–83. CrossRefGoogle Scholar
  51. Piepho HP, Williams ER, Fleck M (2006) A note on the analysis of designed experiments with complex treatment structure. HortScience 41:446–452Google Scholar
  52. Pronyk C, Mazza G (2011) Optimization of processing conditions for the fractionation of triticale straw using pressurized low polarity water. Biores Technol 102:2016–2025. CrossRefGoogle Scholar
  53. Scherm B, Balmas V, Spanu F et al (2013) Fusarium culmorum: causal agent of foot and root rot and head blight on wheat. Mol Plant Pathol 14:323–341. CrossRefPubMedGoogle Scholar
  54. Schmolke M, Zimmermann G, Buerstmayr H et al (2005) Molecular mapping of Fusarium head blight resistance in the winter wheat population Dream/Lynx. Theor Appl Genet 111:747–756. CrossRefPubMedGoogle Scholar
  55. Slafer GA, Whitechurch EM (2001) Manipulating wheat development to improve adaptation and to search for alternative opportunities to increase yield potential. In: Reynolds MP, Ortiz-Monasterio JI, McNab A (eds) Application of physiology in wheat breeding. CIMMYT, Mexico, pp 160–170Google Scholar
  56. Spindel JE, Begum H, Akdemir D et al (2016) Genome-wide prediction models that incorporate de novo GWA are a powerful new tool for tropical rice improvement. Heredity 116:395–408. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Sugita-Konishi Y, Kubosaki A, Takahashi M et al (2008) Nivalenol and the targeting of the female reproductive system as well as haematopoietic and immune systems in rats after 90-day exposure through the diet. Food Addit Contam Part A Chem Anal Control Exposure Risk Assess 25:1118–1127. CrossRefGoogle Scholar
  58. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical ComputingGoogle Scholar
  59. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  60. van Inghelandt D, Reif JC, Dhillon BS et al (2011) Extent and genome-wide distribution of linkage disequilibrium in commercial maize germplasm. Theor Appl Genet 123:11–20. CrossRefPubMedGoogle Scholar
  61. Whittaker JC, Thompson R, Denham MC (2000) Marker-assisted selection using ridge regression. Genet Res 75:249–252CrossRefGoogle Scholar
  62. Würschum T (2012) Mapping QTL for agronomic traits in breeding populations. Theor Appl Genet 125:201–210. CrossRefPubMedGoogle Scholar
  63. Würschum T, Langer SM, Longin CFH (2015) Genetic control of plant height in European winter wheat cultivars. Theor Appl Genet 128:865–874. CrossRefPubMedGoogle Scholar
  64. Würschum T, Maurer HP, Weissmann S et al (2017) Accuracy of within- and among-family genomic prediction in triticale. Plant Breed 136:230–236. CrossRefGoogle Scholar
  65. Yu J, Pressoir G, Briggs WH et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208. CrossRefPubMedGoogle Scholar
  66. Zhao Y, Mette MF, Gowda M et al (2014) Bridging the gap between marker-assisted and genomic selection of heading time and plant height in hybrid wheat. Heredity 112:638–645. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.State Plant Breeding InstituteUniversity of HohenheimStuttgartGermany
  2. 2.Limagrain GmbHPeine-RosenthalGermany

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