Abstract
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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- BLUEs:
-
Best linear unbiased estimators
- DON:
-
Deoxynivalenol
- FHB:
-
Fusarium head blight
- FT:
-
Flowering time
- GEBV:
-
Genomic estimated breeding value
- GS:
-
Genomic selection
- GWA:
-
Genome-wide association
- K:
-
Kinship
- MAF:
-
Minor allele frequency
- MAS:
-
Marker-assisted selection
- NIV:
-
Nivalenol
- PCA:
-
Principal component analysis
- PH:
-
Plant height
- QTL:
-
Quantitative trait loci
- RR-BLUP:
-
Ridge-regression BLUP
- wRR-BLUP:
-
Weighted ridge-regression BLUP
- ZON:
-
Zearalenone
References
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. https://doi.org/10.3390/toxins6010001
Aulchenko YS, Ripke S, Isaacs A, van Duijn CM (2007) GenABEL: an R library for genome-wide association analysis. Bioinformatics 23:1294–1296. https://doi.org/10.1093/bioinformatics/btm108
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. https://doi.org/10.1016/j.plantsci.2015.08.021
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 199–241
Bennett JW, Klich M (2003) Mycotoxins. Clin Microbiol Rev 16:497–516. https://doi.org/10.1128/CMR.16.3.497
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 12:53–62
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. https://doi.org/10.1007/s00122-016-2771-6
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. https://doi.org/10.1007/s10681-015-1498-9
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. https://doi.org/10.2135/cropsci2008.12.0701
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. https://doi.org/10.2135/cropsci2000.4041012x
Bundessortenamt (2014) Beschreibende Sortenliste: Getreide, Mais, Öl- und Faserpflanzen, Leguminosen, Rüben, Zwischenfrüchte. http://www.bundessortenamt.de/internet30/file%0Aadmin/Files/PDF/bsl_getreide_2014.pdf%0A. Accessed 9th Aug 2018
Čonková E, Laciaková A, Kováč G, Seidel H (2003) Fusarial toxins and their role in animal diseases. Vet J 165:214–220. https://doi.org/10.1016/S1090-0233(02)00127-2
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. https://doi.org/10.3390/genes9010019
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 73:1–41
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. https://doi.org/10.1007/s00122-008-0753-z
Endelman JB (2011) Ridge regression and other kernels for genomic selection with R package rrBLUP. Plant Genome J 4:250–255. https://doi.org/10.3835/plantgenome2011.08.0024
Endelman JB, Jannink J (2012) Shrinkage estimation of the realized relationship matrix. G3 Genes Genomes Genet 2:1405–1413. https://doi.org/10.1534/g3.112.004259
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. http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri = OJ:L:2006:229:0007:0009:EN:PDF. Accessed on 23rd March 2015
FAOSTAT (2018) Statistical databases and datasets of the food and agriculture organization of the United Nations. http://www.fao.org/faostat/en/#data/QC. Accessed 5th Feb 2018
Fisher RA (1921) On the “probable error” of a coefficient of correlation deduced from a small sample. Metron 1:3–32
Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2009) ASReml user guide release 3.0. VSN International Ltd, Hemel Hempstead, p 275
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. https://doi.org/10.1016/j.fcr.2010.12.003
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. https://doi.org/10.1038/hdy.2013.139
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. https://doi.org/10.1007/s00122-017-2926-0
Hallauer AR, Carena MJ, Filho J (2010) Quantitative genetics in maize breeding, 3rd edn. Handbook of plant breeding. Springer, New York
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. https://doi.org/10.2135/cropsci2009.11.0662
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. https://doi.org/10.1007/s00122-016-2827-7
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. https://doi.org/10.1007/s00122-014-2316-9
Kalih R, Maurer HP, Miedaner T (2015) Genetic architecture of fusarium head blight resistance in four winter triticale populations. Phytopathology 105:334–341. https://doi.org/10.1094/PHYTO-04-14-0124-R
Lander ES, Schork NJ (1994) Genetic dissection of complex traits. Science 265:2037–2048
Liu W, Leiser WL, Maurer HP et al (2015) Evaluation of genomic approaches for marker-based improvement of lodging tolerance in triticale. Plant Breed 134:416–422
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. https://doi.org/10.1007/s11032-008-9250-y
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. https://doi.org/10.1007/s00122-016-2843-7
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. https://doi.org/10.1111/pbr.12433
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. https://doi.org/10.1111/j.1439-0523.2011.01908.x
McGill R, Tukey JW, Larsen WA (1978) Variations of box plots. Am Stat 32(1):12–16
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. https://doi.org/10.1007/978-0-387-72297-9_9
Mesterházy A (1995) Types and components of resistance to Fusarium head blight of wheat. Plant Breed 114:377–386. https://doi.org/10.1111/j.1439-0523.1995.tb00816.x
Miedaner T (1997) Breeding wheat and rye for resistance to Fusarium diseases. Plant Breed 116:201–220. https://doi.org/10.1111/j.1439-0523.1997.tb00985.x
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. https://doi.org/10.2135/cropsci2008.02.0107
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. https://doi.org/10.1007/s10681-004-2489-4
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. https://doi.org/10.1007/s10658-013-0284-6
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. https://doi.org/10.1111/pbr.12327
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. https://doi.org/10.1111/pbr.12515
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. https://doi.org/10.1007/s00122-015-2602-1
Money D, Gardner K, Migicovsky Z et al (2015) LinkImpute: fast and accurate genotype imputation for nonmodel organisms. Genes Genomes Genet 5:2383–2390. https://doi.org/10.1534/g3.115.021667
Oettler G (2005) The fortune of a botanical curiosity—triticale: past, present and future. J Agric Sci 143:329–346. https://doi.org/10.1017/S0021859605005290
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. https://doi.org/10.1046/j.1439-0523.2001.00611.x
Oettler G, Heinrich N, Miedaner T (2004) Estimates of additive and dominance effects for Fusarium head blight resistance of winter triticale. Plant Breed 123:525–530
Passioura JB (1996) Drought and drought tolerance. Plant Growth Regul 20:79–83. https://doi.org/10.1007/978-94-017-1299-6_1
Piepho HP, Williams ER, Fleck M (2006) A note on the analysis of designed experiments with complex treatment structure. HortScience 41:446–452
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. https://doi.org/10.1016/j.biortech.2010.09.064
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. https://doi.org/10.1111/mpp.12011
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. https://doi.org/10.1007/s00122-005-2060-2
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 160–170
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. https://doi.org/10.1038/hdy.2015.113
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. https://doi.org/10.1080/02652030802093892
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing
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. https://doi.org/10.2307/1403680
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. https://doi.org/10.1007/s00122-011-1562-3
Whittaker JC, Thompson R, Denham MC (2000) Marker-assisted selection using ridge regression. Genet Res 75:249–252
Würschum T (2012) Mapping QTL for agronomic traits in breeding populations. Theor Appl Genet 125:201–210. https://doi.org/10.1007/s00122-012-1887-6
Würschum T, Langer SM, Longin CFH (2015) Genetic control of plant height in European winter wheat cultivars. Theor Appl Genet 128:865–874. https://doi.org/10.1007/s00122-015-2476-2
Würschum T, Maurer HP, Weissmann S et al (2017) Accuracy of within- and among-family genomic prediction in triticale. Plant Breed 136:230–236. https://doi.org/10.1111/pbr.12465
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. https://doi.org/10.1038/ng1702
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. https://doi.org/10.1038/hdy.2014.1
Acknowledgements
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
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.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Galiano-Carneiro, A.L., Boeven, P.H.G., Maurer, H.P. et al. Genome-wide association study for an efficient selection of Fusarium head blight resistance in winter triticale. Euphytica 215, 4 (2019). https://doi.org/10.1007/s10681-018-2327-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10681-018-2327-8