Abstract
Maize is both an exciting model organism in plant genetics and also the most important crop worldwide for food, animal feed and bioenergy production. Recent genome-wide association and metabolic profiling studies aimed to resolve quantitative traits to their causal genetic loci and key metabolic regulators. Here we present a complementary approach that exploits large-scale genomic and metabolic information to predict complex, highly polygenic traits in hybrid testcrosses. We crossed 285 diverse Dent inbred lines from worldwide sources with two testers and predicted their combining abilities for seven biomass- and bioenergy-related traits using 56,110 SNPs and 130 metabolites. Whole-genome and metabolic prediction models were built by fitting effects for all SNPs or metabolites. Prediction accuracies ranged from 0.72 to 0.81 for SNPs and from 0.60 to 0.80 for metabolites, allowing a reliable screening of large collections of diverse inbred lines for their potential to create superior hybrids.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Schnable, P.S. et al. The B73 maize genome: complexity, diversity, and dynamics. Science 326, 1112–1115 (2009).
Montes, J.M., Technow, F., Dhillon, B.S., Mauch, F. & Melchinger, A.E. High-throughput non-destructive biomass determination during early plant development in maize under field conditions. Field Crops Res. 121, 268–273 (2011).
Montes, J.M., Melchinger, A.E. & Reif, J.C. Novel throughput phenotyping platforms in plant genetic studies. Trends Plant Sci. 12, 433–436 (2007).
Steinfath, M. et al. Discovering plant metabolic biomarkers for phenotype prediction using an untargeted approach. Plant Biotechnol. J. 8, 900–911 (2010).
Meyer, R.C. et al. The metabolic signature related to high plant growth in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 104, 4759–4764 (2007).
Schauer, N. et al. Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat. Biotechnol. 24, 447–454 (2006).
Kump, K.L. et al. Genome-wide association study of quantitative resistance to southern leaf blight in the maize association mapping population. Nat. Genet. 43, 163–168 (2011).
Tian, F. et al. Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat. Genet. 43, 159–162 (2011).
Poland, J.A. et al. Genome-wide nested association mapping of quantitative resistance to northern leaf blight in maize. Proc. Natl. Acad. Sci. USA 108, 6893–6898 (2011).
Bernardo, R. Molecular markers and selection for complex traits in plants: learning from the last 20 years. Crop Sci. 48, 1649–1664 (2008).
Xu, Y. & Crouch, J. Marker-assisted selection in plant breeding: from publications to practice. Crop Sci. 48, 391–407 (2008).
Heffner, E.L., Sorrells, M.E. & Jannink, J.-L. Genomic selection for crop improvement. Crop Sci. 49, 1–12 (2009).
Lippman, Z.B. & Zamir, D. Heterosis: revisiting the magic. Trends Genet. 23, 60–66 (2007).
Hallauer, A.R., Carena, M.J. & Filho, J.B.M. Quantitative Genetics in Maize Breeding (Iowa State University Press, 2010).
Meuwissen, T.H.E., Hayes, B.J. & Goddard, M.E. Prediction of total genetic value using genome-wide dense marker maps. Genetics 157, 1819–1829 (2001).
Hayes, B.J. et al. Invited review: genomic selection in dairy cattle: progress and challenges. J. Dairy Sci. 92, 433–443 (2009).
Jannink, J.-L., Lorenz, A.J. & Iwata, H. Genomic selection in plant breeding: from theory to practice. Brief Funct. Genomics 9, 166–177 (2010).
Lorenzana, R.E. & Bernardo, R. Accuracy of genotypic value predictions for marker-based selection in biparental plant populations. Theor. Appl. Genet. 120, 151–161 (2009).
Yang, J. et al. Common SNPs explain a large proportion oft the heritability for human height. Nat. Genet. 42, 565–569 (2010).
Yang, J. et al. Genome partitioning of genetic variation for complex traits using common SNPs. Nat. Genet. 43, 519–525 (2011).
de los Campos, G., Gianola, D. & Allison, D.B. Predicting genetic predispositions in humans: the promise of whole-genome markers. Nat. Rev. Genet. 11, 880–886 (2010).
Smith, J.S.C. et al. Use of doubled haploids in maize breeding: implications for intellectual property protection and genetic diversity in hybrid crops. Mol. Breed. 22, 51–59 (2008).
Slatkin, M. Linkage disequilibrium—understanding the evolutionary past and mapping the medical future. Nat. Rev. Genet. 9, 477–485 (2008).
Ching, A. et al. SNP frequency, haplotype structure and linkage disequilibrium in elite maize inbred lines. BMC Genet. 3, 19 (2002).
Van Inghelandt, D. et al. Extent and genome-wide distribution of linkage disequilibrium in commercial maize germplasm. Theor. Appl. Genet. 123, 11–20 (2011).
Yan, J. et al. Genetic characterization and linkage disequilibrium estimation of a global maize collection using SNP markers. PLoS ONE 4, e8451 (2009).
Elshire, R.J. et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6, e19379 (2011).
Meuwissen, T. & Goddard, M. Accurate prediction of genetic values for complex traits by whole-genome resequencing. Genetics 185, 623–631 (2010).
Fernie, A.R. & Schauer, N. Metabolomics-assisted breeding: a viable option for crop improvement? Trends Genet. 25, 39–48 (2009).
Stitt, M., Sulpice, R. & Keurentjes, J. Metabolic networks: how to identify key components in the regulation of metabolism and growth. Plant Physiol. 152, 428–444 (2010).
Sulpice, R. et al. Starch as a major integrator in the regulation of plant growth. Proc. Natl. Acad. Sci. USA 106, 10348–10353 (2009).
Lisec, J., Schauer, N., Kopka, J., Willmitzer, L. & Fernie, A.R. Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat. Protoc. 1, 387–396 (2006).
Keurentjes, J.J.B. et al. The genetics of plant metabolism. Nat. Genet. 38, 842–849 (2006).
Yu, J. et al. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat. Genet. 38, 203–208 (2006).
Piepho, H.-P. Ridge regression and extensions for genomewide selection in maize. Crop Sci. 49, 1165–1176 (2009).
Albrecht, T. et al. Genome-based prediction of testcross values in maize. Theor. Appl. Genet. 123, 339–350 (2011).
Habier, D., Fernando, R.L., Kizilkaya, K. & Garrick, D.J. Extension of the bayesian alphabet for genomic selection. BMC Bioinformatics 12, 186 (2011).
Clark, S.A., Hickey, J.M. & van der Werf, J.H.J. Different models of genetic variation and their effect on genomic evaluation. Genet. Sel. Evol. 43, 18 (2011).
Goddard, M. Genomic selection: prediction of accuracy and maximation of long term response. Genetica 136, 245–257 (2009).
Duvick, D.N., Smith, J.S.C. & Cooper, M. Long term selection in a commercial hybrid maize breeding program. Plant Breed. Rev. 24, 109–151 (2004).
Eyre-Walker, A., Gaut, R.L., Hilton, H., Feldman, D.L. & Gaut, B.S. Investigation of the bottleneck leading to the domestication of maize. Proc. Natl. Acad. Sci. USA 95, 4441–4446 (1998).
Hoisington, D. et al. Plant genetic resources: what can they contribute toward increased crop productivity. Proc. Natl. Acad. Sci. USA 96, 5937–5943 (1999).
Nelson, P.T. et al. Molecular characterization of maize inbreds with expired U.S. plant variety protection. Crop Sci. 48, 1673–1685 (2008).
Melchinger, A.E., Gumber, R.K., Leipert, R.B., Vuylsteke, M. & Kuiper, M. Prediction of testcross means and variances among F3 progenies of F1 crosses from testcross means and genetic distances of their parents in maize. Theor. Appl. Genet. 96, 503–512 (1999).
Saito, K. & Matsuda, F. Metabolomics for functional genomics, systems biology, and biotechnology. Annu. Rev. Plant Biol. 61, 463–489 (2010).
Fischer, S. et al. Trends in genetic variance components during 30 years of hybrid maize breeding at the University of Hohenheim. Plant Breed. 127, 446–451 (2009).
Desper, R. & Gascuel, O. Fast and accurate phylogeny reconstruction algorithms based on the minimum-evolution principle. J. Comput. Biol. 9, 687–705 (2002).
Cross, J.M. et al. Variation of enzyme activities and metabolite levels in 24 Arabidopsis accessions growing in carbon-limited conditions. Plant Physiol. 142, 1574–1588 (2006).
Cuadros-Inostroza, Á. et al. TargetSearch—a bioconductor package for the efficient preprocessing of GC-MS metabolite profiling data. BMC Bioinformatics 10, 428 (2009).
Chen, W.-M. & Abecasis, G.R. Family-based association tests for genome-wide association scans. Am. J. Hum. Genet. 81, 913–926 (2007).
Hayes, B.J., Visscher, P.M. & Goddard, M.E. Increased accuracy of artificial selection by using the realized relationship matrix. Genet. Res. (Camb). 91, 47–60 (2009).
Yang, J., Lee, H., Goddard, M.E. & Visscher, P.M. GCTA: a tool for fenome-wide complex trait analysis. Am. J. Hum. Genet. 88, 76–82 (2011).
Legarra, A., Robert-Granié, C., Manfredi, E. & Elsen, J.-M. Performance of genomic selection in mice. Genetics 180, 611–618 (2008).
Acknowledgements
We thank the staff of the experimental research stations of the University of Hohenheim for assistance in conducting the field experiments. This research was funded by the Max-Planck Society and the German Federal Ministry of Education and Research (BMBF) within the project GABI-Energy (FKZ: 0315045) and the AgroClustEr 'Synbreed—Synergistic plant and animal breeding' (FKZ: 0315528D).
Author information
Authors and Affiliations
Contributions
T.A., M.S., L.W. and A.E.M. designed the experiments and supervised research. C.R. and C.G. conducted the field experiments. C.R., A.C.-E., R.S. and J.L. performed the metabolic profiling. C.G. analyzed the phenotypic data. C.R. analyzed genomic and metabolic data and developed software. F.T. contributed to the statistical analysis. C.R. and A.E.M. wrote the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Text and Figures
Supplementary Figures 1–12, Supplementary Tables 1–4 and Supplementary Note (PDF 3802 kb)
Rights and permissions
About this article
Cite this article
Riedelsheimer, C., Czedik-Eysenberg, A., Grieder, C. et al. Genomic and metabolic prediction of complex heterotic traits in hybrid maize. Nat Genet 44, 217–220 (2012). https://doi.org/10.1038/ng.1033
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ng.1033
This article is cited by
-
OsLSC6 Regulates Leaf Sheath Color and Cold Tolerance in Rice Revealed by Metabolite Genome Wide Association Study
Rice (2024)
-
Multi-omics assists genomic prediction of maize yield with machine learning approaches
Molecular Breeding (2024)
-
Metabolomic-genomic prediction can improve prediction accuracy of breeding values for malting quality traits in barley
Genetics Selection Evolution (2023)
-
Reciprocal testcross design for genome-wide prediction of maize single-cross performance
Theoretical and Applied Genetics (2023)
-
Genomic prediction in hybrid breeding: I. Optimizing the training set design
Theoretical and Applied Genetics (2023)