Abstract
Key message
Predictabilities for wheat hybrids less related to the estimation set were improved by shifting from single- to multiple-trait genomic prediction of Fusarium head blight severity.
Abstract
Breeding for improved Fusarium head blight resistance (FHBr) of wheat is a very laborious and expensive task. FHBr complexity is mainly due to its highly polygenic nature and because FHB severity (FHBs) is greatly influenced by the environment. Associated traits plant height and heading date may provide additional information related to FHBr, but this is ignored in single-trait genomic prediction (STGP). The aim of our study was to explore the benefits in predictabilities of multiple-trait genomic prediction (MTGP) over STGP of target trait FHBs in a population of 1604 wheat hybrids using information on 17,372 single nucleotide polymorphism markers along with indicator traits plant height and heading date. The additive inheritance of FHBs allowed accurate hybrid performance predictions using information on general combining abilities or average performance of both parents without the need of markers. Information on molecular markers and indicator trait(s) improved FHBs predictabilities for hybrids less related to the estimation set. Indicator traits must be observed on the predicted individuals to benefit from MTGP. Magnitudes of genetic and phenotypic correlations along with improvements in predictabilities made plant height a better indicator trait for FHBs than heading date. Thus, MTGP having only plant height as indicator trait already maximized FHBs predictabilities. Provided a good indicator trait was available, MTGP could reduce the impacts of genotype environment \(\times\) interaction on STGP for hybrids less related to the estimation set.
Similar content being viewed by others
Abbreviations
- BLUE(s):
-
Best linear unbiased estimation(s)
- BLUP(s):
-
Best linear unbiased prediction(s)
- FHB(r/s):
-
Fusarium head blight (resistance/severity)
- GCA:
-
General combining ability
- GP:
-
Genomic prediction
- GWAS:
-
Genome-wide association mapping studies
- MT:
-
Multiple trait
- QTL:
-
Quantitative trait loci
- SCA:
-
Specific combining ability
- SNP:
-
Single nucleotide polymorphism
- ST:
-
Single trait
References
Arruda MP, Brown PJ, Lipka AE, Krill AM, Thurber C, Kolb FL (2015) Genomic selection for predicting Fusarium head blight resistance in a wheat breeding program. Plant Genome 8:1–12
Arruda MP, Lipka AE, Brown PJ, Krill AM, Thurber C, Brown-Guedira G, Dong Y, Foresman BJ, Kolb FL (2016) Comparing genomic selection and marker-assisted selection for Fusarium head blight resistance in wheat (Triticum aestivum L.). Mol Breed 36:84. https://doi.org/10.1007/s11032-016-0508-5
Bai G-H, Shaner G, Ohm H (2000) Inheritance of resistance to Fusarium graminearum in wheat. Theor Appl Genet 100:1–8
Bao Y, Kurle JE, Anderson G, Yong ND (2015) Association mapping and genomic prediction for resistance to sudden death syndrome in early maturing soybean germplasm. Mol Breed 35:128. https://doi.org/10.1007/s11032-015-0324-3
Borlaug NE (1968) Wheat breeding and its impact on world food supply. Australian Academy of Science, Australia, pp 1–36
Brancourt-Hulmel M, Doussinault G, Lecomte C, Bérard P, Le Buanec B, Trottet M (2003) Genetic improvement of agronomic traits of winter wheat cultivars released in France from 1946 to 1992. Crop Sci 43:37–45
Buerstmayr H, Ban T, Anderson JA (2009) QTL mapping and marker-assisted selection for Fusarium head blight resistance in wheat: a review. Plant Breed 128:1–26
Busemeyer L, Mentrup D, Möller K, Wunder E, Alheit K, Hahn V, Maurer HP, Reif JC, Würschum T, Müller J, Rahe F, Ruckelshausen A (2013) BreedVision—a multi-sensor platform for non-destructive field-based phenotyping in plant breeding. Sensors 13:2830–2847
Butler DG, Cullis BR, Gilmour AR, Gogel B (2009) ASReml-R reference manual. The State of Queensland, Department of Primary Industries and Fisheries, Brisbane
Calus MPL, Veerkamp RF (2011) Accuracy of multi-trait genomic selection using different methods. Genet Sel Evol 43:26. https://doi.org/10.1186/1297-9686-43-26
Cerón-Rojas JJ, Sahagún-Castellanos J, Castillo-González F, Santacruz-Varela A, Crossa J (2008) A restricted selection index method based on eigenanalysis. J Agric Biol Environ Stat 13:440–457
Cerón-Rojas JJ, Crossa J, Arief VN, Basford K, Rutkoski J, Jarquín D, Alvarado G, Beyene Y, Semagn K, DeLacy I (2015) A genomic selection index applied to simulated and real data. G3 5:2155–2164
Chen Y, Lübberstedt T (2010) Molecular basis of trait correlations. Trends Plant Sci 15:454–461
Chernoff H (1954) On the distribution of the likelihood ratio. Ann Math Stat 25:573–578
Dawson JC, Endelman JB, Heslot N, Crossa J, Poland J, Dreisigacker S, Manès Y, Sorrells ME, Jannink J-L (2013) The use of unbalanced historical data for genomic selection in an international wheat breeding program. Field Crops Res 154:12–22
Dekkers JCM (2007) Prediction of response to marker-assisted and genomic selection using selection index theory. J Anim Breed Genet 124:331–341
Draeger R, Gosman N, Steed A, Chandler E, Srinivasachary MT, Schondelmaier J, Buerstmayr H, Lemmens M, Schmolke M, Mesterházy A, Nicholson P (2007) Identification of QTLs for resistance to Fusarium head blight, DON accumulation and associated traits in the winter wheat variety Arina. Theor Appl Genet 115:617–625
Endelman JB (2011) Ridge regression and other kernels for genomic selection with R package rrBLUP. Plant Genome 4:250–255
Endelman JB, Jannink JL (2012) Shrinkage estimation of the realized relationship matrix. G3 2:1405–1413
Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Ronald Press Company, New York
Gervais L, Dedryver F, Morlais J-Y, Bodusseau V, Negre S, Bilous M, Groos C, Trottet M (2003) Mapping of quantitative trait loci for field resistance to Fusarium head blight in an European winter wheat. Theor Appl Genet 106:961–970
Gosman NS, Steed A, Simmonds J, Leverington-Waite M, Wang Y, Snape J, Nicholson P (2008) Susceptibility to Fusarium head blight is associated with the Rht-D1b semi-dwarfing allele in wheat. Theor Appl Genet 116:1145–1153
Gowda M, Zhao Y, Würschum T, Longin CFH, Miedaner T, Ebmeyer E, Schachschneider R, Kazman E, Schacht J, Mette MF, Reif JC (2014) Relatedness severely impacts accuracy of marker-assisted selection for disease resistance in hybrid wheat. Heredity 112:552–561
Guo G, Zhao F, Wang Y, Zhang Y, Du L, Su G (2014) Comparison of single-trait and multiple-trait genomic prediction models. BMC Genet 15:30. https://doi.org/10.1186/1471-2156-15-30
Häberle J, Schmolke M, Schweizer G, Korzun V, Ebmeyer E, Zimmermann G, Hartl L (2007) Effects of two major Fusarium head blight resistance QTL verified in a winter wheat backcross population. Crop Sci 47:1823–1831
Habier D, Fernando RL, Dekkers JCM (2007) The impact of genetic relationship information on genome-assisted breeding values. Genetics 177:2389–2397
Handa H, Namiki N, Xu D, Ban T (2008) Dissecting of the FHB resistance QTL on the short arm of wheat chromosome 2D using a comparative genomic approach: from QTL to candidate gene. Mol Breed 27:71–84
Hayashi T, Iwata H (2013) A Bayesian method and its variational approximation for prediction of genomic breeding values in multiple traits. BMC Bioinform 14:34. https://doi.org/10.1186/1471-2105-14-34
He S, Schulthess AW, Mirdita V, Zhao Y, Korzun V, Bothe R, Ebmeyer E, Reif JC, Jiang Y (2016) Genomic selection in a commercial winter wheat population. Theor Appl Genet 129:641–651
Henderson CR, Quaas RL (1976) Multiple trait evaluation using relatives’ records. J Anim Sci 43:1188–1197
Hilton AJ, Jenkinson P, Hollins TW, Parry DW (1999) Relationship between cultivar height and severity of Fusarium ear blight in wheat. Plant Pathol 48:202–208
Hori T, Montcho D, Agbangla C, Ebana K, Futakuchi K, Iwata H (2016) Multi-task Gaussian process for imputing missing data in multi-trait and multi-environment trials. Theor Appl Genet 129:2101–2115
Jia Y, Jannink JL (2012) Multiple-trait genomic selection methods increase genetic value prediction accuracy. Genetics 192:1513–1522
Jiang GL, Ward RW (2006) Inheritance of resistance to Fusarium head blight in the wheat lines ‘CJ 9306’ and ‘CJ 9403’. Plant Breed 125:417–423
Jiang C, Zeng ZB (1995) Multiple trait analysis for genetic mapping of quantitative trait loci. Genetics 140:1111–1127
Jiang J, Zhang Q, Ma L, Li J, Wang Z, Liu JF (2015a) Joint prediction of multiple quantitative traits using a Bayesian multivariate antedependence model. Heredity 115:29–36
Jiang Y, Zhao Y, Rodemann B, Plieske J, Kollers S, Korzun V, Ebmeyer E, Argillier O, Hinze M, Ling J, Röder MS, Ganal MW, Mette MF, Reif JC (2015b) Potential and limits to unravel the genetic architecture and predict the variation of Fusarium head blight resistance in European winter wheat (Triticum aestivum L.). Heredity 114:318–326
Kempthorne O, Nordskog AW (1959) Restricted selection indices. Biometrics 15:10–19
Klahr A, Zimmermann J, Wenzel G, Mohler V (2007) Effects of environment, disease progress, plant height and heading date on the detection of QTLs for resistance to Fusarium head blight in an European winter wheat cross. Euphytica 154:17–28
Kollers S, Rodemann B, Ling J, Korzun V, Ebmeyer E, Argillier O, Hinze M, Plieske J, Kulosa D, Ganal MW, Röder MS (2013) Whole genome association mapping of Fusarium head blight resistance in European winter wheat (Triticum aestivum L.). PLoS ONE 8:e57500
Kowalski AM, Gooding M, Ferrante A, Slafer GA, Orford S, Gasperini D, Griffiths S (2016) Agronomic assessment of the wheat semi-dwarfing gene Rht8 in contrasting nitrogen treatments and water regimes. Field Crops Res 191:150–160
Liu S, Hall MD, Griffey CA, McKendry AL (2009) Meta-Analysis of QTL associated with Fusarium head blight resistance in wheat. Crop Sci 49:1955–1968
Liu T, Qu H, Luo C, Li X, Shu D, Lund MS, Su G (2014) Genomic selection for the improvement of antibody response to newcastle disease and avian influenza virus in chickens. PLoS ONE 9:e112685
Liu G, Zhao Y, Gowda M, Longin CFH, Reif JC, Mette MF (2016) Predicting hybrid performances for quality traits through genomic-assisted approaches in Central European wheat. PLoS ONE 11:e0158635
Longin CFH, Gowda M, Mühleisen J, Ebmeyer E, Kazman E, Schachschneider R, Schacht J, Kirchhoff M, Zhao Y, Reif JC (2013) Hybrid wheat: quantitative genetic parameters and consequences for the design of breeding programs. Theor Appl Genet 126:2791–2801
Marchal A, Legarra A, Tisné S, Carasco-Lacombe C, Manez A, Suryana E, Omoré A, Nouy B, Durand-Gasselin T, Sánchez L, Bouvet JM, Cros D (2016) Multivariate genomic model improves analysis of oil palm (Elaeis guineensis Jacq.) progeny tests. Mol Breed 36:2. https://doi.org/10.1007/s11032-015-0423-1
McCartney CA, Somers DJ, Fedak G, DePauw RM, Thomas J, Fox SL, Humphreys DG, Lukow O, Savard ME, McCallum BD, Gilbert J, Cao W (2007) The evaluation of FHB resistance QTLs introgressed into elite Canadian spring wheat germplasm. Mol Breed 20:209–221
Mesterházy A (1995) Types and components of resistance to Fusarium head blight of wheat. Plant Breed 114:377–386
Meuwissen THE, Luo Z (1992) Computing inbreeding coefficients in large populations. Genet Sel Evol 24:305–313
Meuwissen THE, Hayes BJ, Goddard ME (2001) Prediction of total genetic value using genome-wide dense marker maps. Genetics 157:1819–1829
Miedaner T (1997) Breeding wheat and rye for resistance to Fusarium disease. Plant Breed 116:201–220
Miedaner T, Gang G, Geiger HH (1996) Quantitative-genetic basis of aggressiveness of 42 Fusarium culmorum isolates for winter rye head blight. Plant Dis 80:500–504
Miedaner T, Würschum T, Maurer HP, Korzun V, Ebmeyer E, Reif JC (2011) Association mapping for Fusarium head blight resistance in soft European winter wheat. Mol Breed 28:647–655
Miedaner T, Schulthess AW, Gowda M, Reif JC, Longin CFH (2017) High accuracy of predicting hybrid performance of Fusarium head blight resistance by mid-parent values in wheat. Theor Appl Genet 130:461–470
Mirdita V, He S, Zhao Y, Korzun V, Bothe R, Ebmeyer E, Reif JC, Jiang Y (2015a) 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
Mirdita V, Liu G, Zhao Y, Miedaner T, Longin CFH, Gowda M, Mette MF, Reif JC (2015b) Genetic architecture is more complex for resistance to Septoria tritici blotch than to Fusarium head blight in Central European winter wheat. BMC Genom 16:430. https://doi.org/10.1186/s12864-015-1628-8
Möhring J, Piepho HP (2009) Comparison of weighting in two-stage analysis of plant breeding trials. Crop Sci 49:1977–1988
Montesinos-López OA, Montesinos-López A, Crossa J, Toledo FH, Pérez-Hernández O, Eskridge KM, Rutkoski J (2016) A genomic Bayesian multi-trait and multi-environment model. G3 6:2725–2744
Neumann K, Klukas C, Friedel S, Rischbeck P, Chen D, Entzian A, Stein N, Graner A, Kilian B (2015) Dissecting spatiotemporal biomass accumulation in barley under different water regimes using high-throughput image analysis. Plant, Cell Environ 38:1980–1996
Paaby AB, Rockman MV (2013) The many faces of pleiotropy. Trends Genet 29:66–73
Paillard S, Schnurbusch T, Tiwari R, Messmer M, Winzeler M, Keller B, Schachermayr G (2004) QTL analysis of resistance to Fusarium head blight in Swiss winter wheat (Triticum aestivum L.). Theor Appl Genet 109:323–332
Parry DW, Jenkinson P, McLeod L (1995) Fusarium ear blight (scab) in small grain cereals—a review. Plant Pathol 44:207–238
Piepho HP, Williams ER, Fleck M (2006) A note on the analysis of designed experiments with complex treatment structure. HortScience 41:446–452
Pisanello D (2014) EU regulations on chemicals in foods. In: Pisanello D (ed) Chemistry of foods: EU legal and regulatory approaches. SpringerBriefs in Molecular Science, Springer, Cham, pp 15–77
Pszczola M, Strabel T, van Arendonk JAM, Calus MPL (2012) The impact of genotyping different groups of animals on accuracy when moving from traditional to genomic selection. J Dairy Sci 95:5412–5421
Pszczola M, Veerkamp RF, de Haas Y, Wall E, Strabel T, Calus MPL (2013) Effect of predictor traits on accuracy of genomic breeding values for feed intake based on a limited cow reference population. Animal 7:1759–1768
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org. Accessed 21 June 2016
Rutkoski J, Benson J, Jia Y, Brown-Guedira G, Jannink JL, Sorrells ME (2012) Evaluation of genomic prediction methods for Fusarium head blight resistance in wheat. Plant Genome 5:51–61
Rutkoski J, Poland J, Mondal S, Autrique E, González Pérez L, Crossa J, Reynolds M, Singh R (2016) Canopy temperature and vegetation indices from high-throughput phenotyping improve accuracy of pedigree and genomic selection for grain yield in wheat. G3 6:2799–2808
Santos JPR, Vasconcellos RCC, Pires LPM, Balestre M, Von Pinho RG (2016) Inclusion of dominance effects in the multivariate GBLUP model. PLoS ONE 11:e0152045
Schmolke M, Zimmermann G, Buerstmayr H, Schweizer G, Miedaner T, Korzun V, Ebmeyer E, Hartl L (2005) Molecular mapping of Fusarium head blight resistance in the winter wheat population Dream/Lynx. Theor Appl Genet 111:747–756
Schrag TA, Frisch M, Dhillon BS, Melchinger AE (2009) Marker-based prediction of hybrid performance in maize single-crosses involving doubled haploids. Maydica 54:353–362
Schulthess AW, Wang Y, Miedaner T, Wilde P, Reif JC, Zhao Y (2016) Multiple-trait- and selection indices-genomic predictions for grain yield and protein content in rye for feeding purposes. Theor Appl Genet 129:273–287
Schulthess AW, Reif JC, Ling J, Plieske J, Kollers S, Ebmeyer E, Korzun V, Argillier O, Stiewe G, Ganal MW, Röder MS, Jiang Y (2017) The roles of pleiotropy and close linkage as revealed by association mapping of yield and correlated traits of wheat (Triticum aestivum L.). J Exp Bot 68:4089–4101
Schulz-Streeck T, Ogutu JO, Gordillo A, Karaman Z, Knaak C, Piepho HP (2013) Genomic selection allowing for marker-by-environment interaction. Plant Breed 132:532–538
Searle SR (2006) Matrix algebra useful for statistics, 2nd edn. Wiley, New York
Snijders CHA (1990) The inheritance of resistance to head blight caused by Fusarium culmorum in winter wheat. Euphytica 50:11–18
VanRaden PM (2008) Efficient methods to compute genomic predictions. J Dairy Sci 91:4414–4423
Varona L, Gomez-Raya L, Rauw WM, Clop A, Ovilo C, Noguera JL (2004) Derivation of a Bayes factor to distinguish between linked or pleiotropic quantitative trait loci. Genetics 166:1025–1035
Wang Y, Mette MF, Miedaner T, Gottwald M, Wilde P, Reif JC, Zhao Y (2014a) The accuracy of prediction of genomic selection in elite hybrid rye populations surpasses the accuracy of marker-assisted selection and is equally augmented by multiple field evaluation locations and test years. BMC Genom 15:556. https://doi.org/10.1186/1471-2164-15-556
Wang S, Wong D, Forrest K, Allen A, Chao S, Huang BE, Maccaferri M, Salvi S, Milner SG, Cattivelli L, Mastrangelo AM, Whan A, Stephen S, Barker G, Wieseke R, Plieske J, Lillemo M, Mather D, Appels R, Dolferus R, Brown-Guedira G, Korol A, Akhunova AR, Feuillet C, Salse J, Morgante M, Pozniak C, Luo MC, Dvorak J, Morell M, Dubcovsky J, Ganal M, Tuberosa R, Lawley C, Mikoulitch I, Cavanagh C, Edwards KJ, Hayden M, Akhunov E, International Wheat Genome Sequencing C (2014b) Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array. Plant Biotech J 12:787–796
Wang X, Li L, Yang Z, Zheng X, Yu S, Xu C, Hu Z (2016) Predicting rice hybrid performance using univariate and multivariate GBLUP models based on North Carolina mating design II. Heredity 118:302–310
Wilks SS (1938) The large-sample distribution of the likelihood ratio for testing composite hypotheses. Ann Math Stat 9:60–62
Windhausen VS, Atlin GN, Hickey JM, Crossa J, Jannink JL, Sorrels ME, Raman B, Cairns JE, Tarekegne A, Semagn K, Beyene Y, Grudloyma P, Technow F, Riedelsheimer C, Melchinger AE (2012) Effectiveness of genomic prediction of maize hybrid performance in different breeding populations and environments. G3 2:1427–1436
Würschum T, Langer SM, Longin CFH, Korzun V, Akhunov E, Ebmeyer E, Schachschneider R, Schacht J, Kazman E, Reif JC (2013) Population structure, genetic diversity and linkage disequilibrium in elite winter wheat assessed with SNP and SSR markers. Theor Appl Genet 126:1477–1486
Zhao Y, Gowda M, Würschum T, Longin CFH, Korzun V, Kollers S, Schachschneider R, Zeng J, Fernando R, Dubcovsky J (2013) Dissecting the genetic architecture of frost tolerance in Central European winter wheat. J Exp Bot 64:4453–4460
Zhao Y, Li Z, Liu G, Jiang Y, Maurer HP, Würschum T, Mock HP, Matros A, Ebmeyer E, Schachschneider R, Kazman E, Schacht J, Gowda M, Longin CFH, Reif JC (2015) Genome-based establishment of a high-yielding heterotic pattern for hybrid wheat breeding. Proc Natl Acad Sci USA 112:15624–15629
Acknowledgements
This research work was conducted within the scope of the HYWHEAT project funded by BMBF (Grant no. FKZ031–5945D).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors declare that they have no conflict of interest.
Ethical statement
All experiments were performed under the current laws of Germany.
Additional information
Communicated by Laurence Moreau.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Schulthess, A.W., Zhao, Y., Longin, C.F.H. et al. Advantages and limitations of multiple-trait genomic prediction for Fusarium head blight severity in hybrid wheat (Triticum aestivum L.). Theor Appl Genet 131, 685–701 (2018). https://doi.org/10.1007/s00122-017-3029-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-017-3029-7