Including marker x environment interactions improves genomic prediction in red clover (Trifolium pratense L.)
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
38916032
PubMed Central
PMC11194335
DOI
10.3389/fpls.2024.1407609
Knihovny.cz E-zdroje
- Klíčová slova
- genomic prediction, marker x environment interaction, population structure, predictive ability, red clover, trifolium pratense,
- Publikační typ
- časopisecké články MeSH
Genomic prediction has mostly been used in single environment contexts, largely ignoring genotype x environment interaction, which greatly affects the performance of plants. However, in the last decade, prediction models including marker x environment (MxE) interaction have been developed. We evaluated the potential of genomic prediction in red clover (Trifolium pratense L.) using field trial data from five European locations, obtained in the Horizon 2020 EUCLEG project. Three models were compared: (1) single environment (SingleEnv), (2) across environment (AcrossEnv), (3) marker x environment interaction (MxE). Annual dry matter yield (DMY) gave the highest predictive ability (PA). Joint analyses of DMY from years 1 and 2 from each location varied from 0.87 in Britain and Switzerland in year 1, to 0.40 in Serbia in year 2. Overall, crude protein (CP) was predicted poorly. PAs for date of flowering (DOF), however ranged from 0.87 to 0.67 for Britain and Switzerland, respectively. Across the three traits, the MxE model performed best and the AcrossEnv worst, demonstrating that including marker x environment effects can improve genomic prediction in red clover. Leaving out accessions from specific regions or from specific breeders' material in the cross validation tended to reduce PA, but the magnitude of reduction depended on trait, region and breeders' material, indicating that population structure contributed to the high PAs observed for DMY and DOF. Testing the genomic estimated breeding values on new phenotypic data from Sweden showed that DMY training data from Britain gave high PAs in both years (0.43-0.76), while DMY training data from Switzerland gave high PAs only for year 1 (0.70-0.87). The genomic predictions we report here underline the potential benefits of incorporating MxE interaction in multi-environment trials and could have perspectives for identifying markers with effects that are stable across environments, and markers with environment-specific effects.
Department of Plant Biotechnology and Bioinformatics Ghent University Ghent Belgium
Division of Plant Breeding Fodder Plant Breeding Agroscope Zurich Switzerland
DLF Seeds Hladké Životice Czechia
Germinal Horizon Plas Gogerddan Aberystwyth United Kingdom
Graminor Breeding Ltd Bjørke Forsøksgård Norway
Institute for Forage Crops Kruševac Serbia
Lantmännen Lantbruk Svalöv Sweden
Molecular Plant Breeding Institute of Agricultural Sciences ETH Zurich Zurich Switzerland
Plant Sciences Unit Flanders Research Institute for Agriculture Fisheries and Food Melle Belgium
The Nordic Genetic Resource Centre Plant Section Alnarp Sweden
Zobrazit více v PubMed
Annicchiarico P., Nazzicari N., Li X., Wei Y., Pecetti L., Brummer E. C. (2015). Accuracy of genomic selection for alfalfa biomass yield in different reference populations. BMC Genomics 16, 1–13. doi: 10.1186/s12864-015-2212-y PubMed DOI PMC
Annicchiarico P., Nazzicari N., Wei Y., Pecetti L., Brummer E. C. (2017). Genotyping-by-sequencing and its exploitation for forage and cool-season grain legume breeding. Front. Plant Sci. 8. doi: 10.3389/fpls.2017.00679 PubMed DOI PMC
Arojju S. K., Cao M., Zulfi Jahufer M. Z., Barrett B. A., Faville M. J. (2020). Genomic predictive ability for foliar nutritive traits in perennial ryegrass. G3.: Genes|Genomes|Genetics. 10, 695–708. doi: 10.1534/g3.119.400880 PubMed DOI PMC
Arojju S. K., Conaghan P., Barth S., Milbourne D., Casler M. D., Hodkinson T. R., et al. . (2018). Genomic prediction of crown rust resistance in Lolium perenne. BMC Genet. 19, 35. doi: 10.1186/s12863-018-0613-z PubMed DOI PMC
Baird N. A., Etter P. D., Atwood T. S., Currey M. C., Shiver A. L., Lewis Z. A., et al. . (2008). Rapid SNP discovery and genetic mapping using sequenced RAD markers. PloS One 3, e3376. doi: 10.1371/journal.pone.0003376 PubMed DOI PMC
Bandeira E Sousa M., Cuevas J., De Oliveira Couto E. G., Pérez-Rodríguez P., Jarquín D., Fritsche-Neto R., et al. . (2017). Genomic-enabled prediction in maize using kernel models with genotype × Environment interaction. G3.: Genes|Genomes|Genetics. 7, 1995–2014. doi: 10.1534/g3.117.042341 PubMed DOI PMC
Barre P., Asp T., Byrne S., Casler M., Faville M., Rognli O. A., et al. . (2022). Genomic prediction of complex traits in forage plants species: perennial grasses case. Methods Mol. Biol. 2467, 521–541. doi: 10.1007/978-1-0716-2205-6_19 PubMed DOI
Bassi F. M., Bentley A. R., Charmet G., Ortiz R., Crossa J. (2016). Breeding schemes for the implementation of genomic selection in wheat (Triticum spp.). Plant Sci. (Oxford). 242, 23–36. doi: 10.1016/j.plantsci.2015.08.021 PubMed DOI
Burgueño J., De Los Campos G., Weigel K., Crossa J. (2012). Genomic Prediction of Breeding Values when Modeling Genotype × Environment Interaction using Pedigree and Dense Molecular Markers. Crop Sci. 52, 707–719. doi: 10.2135/cropsci2011.06.0299 DOI
Byrne S., Czaban A., Studer B., Panitz F., Bendixen C., Asp T. (2013). Genome wide allele frequency fingerprints (GWAFFs) of populations via genotyping by sequencing. PloS One 8, e57438. doi: 10.1371/journal.pone.0057438 PubMed DOI PMC
Byrne S. L., Conaghan P., Barth S., Arojju S. K., Casler M., Michel T., et al. . (2017). Using variable importance measures to identify a small set of SNPs to predict heading date in perennial ryegrass. Sci. Rep. 7, 3566. doi: 10.1038/s41598-017-03232-8 PubMed DOI PMC
Campbell M. T., Hu H., Yeats T. H., Brzozowski L. J., Caffe-Treml M., Gutiérrez L., et al. . (2021). Improving genomic prediction for seed quality traits in oat (Avena sativa L.) using trait-specific relationship matrices. Front. Genet. 12. doi: 10.3389/fgene.2021.643733 PubMed DOI PMC
Cericola F., Lenk I., Fè D., Byrne S., Jensen C. S., Pedersen M. G., et al. . (2018). Optimized use of low-depth genotyping-by-sequencing for genomic prediction among multi-parental family pools and single plants in perennial ryegrass (Lolium perenne L.). Front. Plant Sci. 9. doi: 10.3389/fpls.2018.00369 PubMed DOI PMC
Crossa J., De Los Campos G., Maccaferri M., Tuberosa R., Burgueño J., Pérez-Rodríguez P. (2016). Extending the marker × Environment interaction model for genomic-enabled prediction and genome-wide association analysis in durum wheat. Crop Sci. 56, 2193–2209. doi: 10.2135/cropsci2015.04.0260 DOI
Cuevas J., Crossa J., Soberanis V., Perez-Elizalde S., Perez-Rodriguez P., de los Campos G., et al. . (2016). Genomic prediction of Genotype x Environment interaction Kernel regression model. Plant Genome 9. doi: 10.3835/plantgenome2016.03.0024 PubMed DOI
Cui Y., Li R., Li G., Zhang F., Zhu T., Zhang Q., et al. . (2020). Hybrid breeding of rice via genomic selection. Plant Biotechnol. J. 18, 57–67. doi: 10.1111/pbi.13170 PubMed DOI PMC
Elshire R. J., Glaubitz J. C., Sun Q., Poland J. A., Kawamoto K., Buckler E. S., et al. . (2011). A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PloS One 6, e19379. doi: 10.1371/journal.pone.0019379 PubMed DOI PMC
Ergon Å., Milvang Ø.W., Skøt L., Ruttink T. (2022). Identification of loci controlling timing of stem elongation in red clover using genotyping by sequencing of pooled phenotypic extremes. Mol. Genet. Genomics 297, 1587–1600. doi: 10.1007/s00438-022-01942-x PubMed DOI PMC
Ergon Å., Skøt L., Sæther V. E., Rognli O. A. (2019). Allele frequency changes provide evidence for selection and identification of candidate loci for survival in red clover (Trifolium pratense L.). Front. Plant Sci. 10. doi: 10.3389/fpls.2019.00718 PubMed DOI PMC
Faville M. J., Cao M., Schmidt J., Ryan D. L., Ganesh S., Jahufer M. Z. Z., et al. . (2020). Divergent genomic selection for herbage accumulation and days-to-heading in perennial ryegrass. Agronomy 10, 340. doi: 10.3390/agronomy10030340 DOI
Faville M. J., Ganesh S., Cao M., Jahufer M. Z. Z., Bilton T. P., Easton H. S., et al. . (2018). Predictive ability of genomic selection models in a multi-population perennial ryegrass training set using genotyping-by-sequencing. Theor. Appl. Genet. 131, 703–720. doi: 10.1007/s00122-017-3030-1 PubMed DOI PMC
Fè D., Ashraf B. H., Pedersen M. G., Janss L., Byrne S., Roulund N., et al. . (2016). Accuracy of genomic prediction in a commercial perennial ryegrass breeding program. Plant Genome 9, 3. doi: 10.3835/plantgenome2015.11.0110 PubMed DOI
Fè D., Cericola F., Byrne S., Lenk I., Ashraf B., Pedersen M., et al. . (2015). Genomic dissection and prediction of heading date in perennial ryegrass. BMC Genomics 16, 1–15. doi: 10.1186/s12864-015-2163-3 PubMed DOI PMC
Forster J. W., Hand M. L., Cogan N. O. I., Hayes B. J., Spangenberg G. C., Smith K. F. (2014). Resources and strategies for implementation of genomic selection in breeding of forage species. Crop Pasture Sci. 65, 1238–1247. doi: 10.1071/CP13361 DOI
Frame J., Charlton J. F. L., Laidlaw A. S. (1998). Temperate forage Legumes (Wallingford: CAB International; ), 327, ISBN: ISBN 0–85199-2145.
Frey L. A., Vleugels T., Ruttink T., Schubiger F. X., Pégard M., Skøt L., et al. . (2022). Phenotypic variation and quantitative trait loci for resistance to southern anthracnose and clover rot in red clover. Theor. Appl. Genet. 135, 4337–4349. doi: 10.1007/s00122-022-04223-8 PubMed DOI PMC
Griffiths A., Ehoche G., Arojju S., Larking A., Jauregui R., Cousins G., et al. . (2022). Developing genomic selection for dry matter yield in white clover. J. New Z. Grasslands. 83, 83–90. doi: 10.33584/jnzg.2021.83.3502 DOI
Grinberg N. F., Lovatt A., Hegarty M., Lovatt A., Skøt K. P., Kelly R., et al. . (2016). Implementation of genomic prediction in Lolium perenne (L.) breeding populations. Front. Plant Sci. 7. doi: 10.3389/fpls.2016.00133 PubMed DOI PMC
Guo Z., Tucker D. M., Basten C. J., Gandhi H., Ersoz E., Guo B., et al. . (2014). The impact of population structure on genomic prediction in stratified populations. Theor. Appl. Genet. 127, 749–762. doi: 10.1007/s00122-013-2255-x PubMed DOI
Hayes B. J., Cogan N. O. I., Pembleton L. W., Goddard M. E., Wang J., Spangenberg G. C., et al. . (2013. a). Prospects for genomic selection in forage plant species. Plant Breed. 132, 133–143. doi: 10.1111/pbr.12037 DOI
Hayes B. J., Lewin H. A., Goddard M. E. (2013. b). The future of livestock breeding: genomic selection for efficiency, reduced emissions intensity, and adaptation. Trends Genet. 29, 206–214. doi: 10.1016/j.tig.2012.11.009 PubMed DOI
Heslot N., Akdemir D., Sorrells M., Jannink J.-L. (2014). Integrating environmental covariates and crop modeling into the genomic selection framework to predict genotype by environment interactions. Theor. Appl. Genet. 127, 463–480. doi: 10.1007/s00122-013-2231-5 PubMed DOI
Jarquín D., Crossa J., Lacaze X., Cheyron P., Daucourt J., Lorgeou J., et al. . (2014). A reaction norm model for genomic selection using high-dimensional genomic and environmental data. Theor. Appl. Genet. 127, 595–607. doi: 10.1007/s00122-013-2243-1 PubMed DOI PMC
Jia C., Zhao F., Wang X., Han J., Zhao H., Liu G., et al. . (2018). Genomic prediction for 25 agronomic and quality traits in alfalfa (Medicago sativa). Front. Plant Sci. 9. doi: 10.3389/fpls.2018.01220 PubMed DOI PMC
Juliana P., Singh R. P., Braun H.-J., Huerta-Espino J., Crespo-Herrera L., Govindan V., et al. . (2020). Genomic selection for grain yield in the CIMMYT wheat breeding program—Status and perspectives. Front. Plant Sci. 11. doi: 10.3389/fpls.2020.564183 PubMed DOI PMC
Keep T., Sampoux J. P., Blanco-Pastor J. L., Dehmer K. J., Hegarty M. J., Ledauphin T., et al. . (2020). High-throughput genome-wide genotyping to optimize the use of natural genetic resources in the grassland species perennial ryegrass (Lolium perenne l.). G3 10, 3347–3364. doi: 10.1534/g3.120.401491 PubMed DOI PMC
Lee M. R. F. (2014). Forage polyphenol oxidase and ruminant livestock nutrition. Front. Plant Sci. 5. doi: 10.3389/fpls.2014.00694 PubMed DOI PMC
Li X., Wei Y., Acharya A., Hansen J. L., Crawford J. L., Viands D. R., et al. . (2015). Genomic prediction of biomass yield in two selection cycles of a tetraploid alfalfa breeding population. Plant Genome 8, 90. doi: 10.3835/plantgenome2014.12.0090 PubMed DOI
Lin Z., Cogan N. O. I., Pembleton L. W., Spangenberg G. C., Forster J. W., Hayes B. J., et al. . (2016). Genetic gain and inbreeding from genomic selection in a simulated commercial breeding program for perennial ryegrass. Plant Genome 9, 46. doi: 10.3835/plantgenome2015.06.0046 PubMed DOI
Lin Z., Wang J., Cogan N. O. I., Pembleton L. W., Badenhorst P., Forster J. W., et al. . (2017). Optimizing resource allocation in a genomic breeding program for perennial ryegrass to balance genetic gain, cost, and inbreeding. Crop Sci. 57, 243–252. doi: 10.2135/cropsci2016.07.0577 DOI
Liu H., Zhou H., Wu Y., Li X., Zhao J., Zuo T., et al. . (2015). The impact of genetic relationship and linkage disequilibrium on genomic selection. PloS One 10, e0132379. doi: 10.1371/journal.pone.0132379 PubMed DOI PMC
Lopez-Cruz M., Crossa J., Bonnett D., Dreisigacker S., Poland J., Jannink J.-L., et al. . (2015). Increased prediction accuracy in wheat breeding trials using a marker × Environment interaction genomic selection model. G3.: Genes|Genomes|Genetics. 5, 569–582. doi: 10.1534/g3.114.016097 PubMed DOI PMC
Lüscher A., Mueller-Harvey I., Soussana J. F., Rees R. M., Peyraud J. L. (2014). Potential of legume-based grassland–livestock systems in Europe: a review. Grass. Forage. Sci. 69, 206–228. doi: 10.1111/gfs.12124 PubMed DOI PMC
McKenna P., Cannon N., Conway J., Dooley J. (2018). The use of red clover (Trifolium pratense) in soil fertility-building: A Review. Field Crops Res. 221, 38–49. doi: 10.1016/j.fcr.2018.02.006 DOI
Meuwissen T. H. E., Hayes B. J., Goddard M. E. (2001). Prediction of total genetic value using genome-wide dense marker maps. Genetics 157, 1819–1829. doi: 10.1093/genetics/157.4.1819 PubMed DOI PMC
Nay M. M., Grieder C., Frey L. A., Amdahl H., Radovic J., Jaluvka L., et al. . (2023). Multi-location trials and population-based genotyping reveal high diversity and adaptation to breeding environments in a large collection of red clover. Front. Plant Sci. 14. doi: 10.3389/fpls.2023.1128823 PubMed DOI PMC
Pégard M., Barre P., Delaunay S., Surault F., Karagić D., Milić D., et al. . (2023). Genome-wide genotyping data renew knowledge on genetic diversity of a worldwide alfalfa collection and give insights on genetic control of phenology traits. Front. Plant Sci. 14. doi: 10.3389/fpls.2023.1196134 PubMed DOI PMC
Pembleton L. W., Inch C., Baillie R. C., Drayton M. C., Thakur P., Ogaji Y. O., et al. . (2018). Exploitation of data from breeding programs supports rapid implementation of genomic selection for key agronomic traits in perennial ryegrass. Theor. Appl. Genet. 131, 1891–1902. doi: 10.1007/s00122-018-3121-7 PubMed DOI PMC
Pérez P., De Los Campos G. (2014). Genome-wide regression; prediction with the BGLR statistical package. Genetics 198, 483–495. doi: 10.1534/genetics.114.164442 PubMed DOI PMC
Puglisi D., Delbono S., Visioni A., Ozkan H., Kara İ., Casas A. M., et al. . (2021). Genomic prediction of grain yield in a barley MAGIC population modeling genotype per environment interaction. Front. Plant Sci. 12. doi: 10.3389/fpls.2021.664148 PubMed DOI PMC
R Core Team (2023). R: A Language and Environment for Statistical Computing (Vienna, Austria: R Foundation for Statistical Computing; ).
Sabag I., Bi Y., Peleg Z., Morota G. (2023). Multi-environment analysis enhances genomic prediction accuracy of agronomic traits in sesame. Front. Genet. 14. doi: 10.3389/fgene.2023.1108416 PubMed DOI PMC
Schefers J. M., Weigel K. A. (2012). Genomic selection in dairy cattle: Integration of DNA testing into breeding programs. Anim. Front. 2, 4–9. doi: 10.2527/af.2011-0032 DOI
Smith A., Cullis B. (2018). Plant breeding selection tools built on factor analytic mixed models for multi-environment trial data. Euphytica 214, 143. doi: 10.1007/s10681-018-2220-5 DOI
Smith A., Cullis B., Thompson R. (2001). Analyzing Variety by environment data using multiplicative mixed models and adjustments for spatial field trend. Biometrics 57, 1138–1147. doi: 10.1111/j.0006-341X.2001.01138.x PubMed DOI
Sukumaran S., Jarquin D., Crossa J., Reynolds M. (2018). Genomic-enabled prediction accuracies increased by modeling genotype × Environment interaction in durum wheat. Plant Genome 11, 170112. doi: 10.3835/plantgenome2017.12.0112 PubMed DOI
VanRaden P. M. (2008). Efficient models to compute genomic predictions. J. Dairy. Sci. 91, 4414–4423. doi: 10.3168/jds.2007-0980 PubMed DOI
Walsh B., Lynch M. (2018). Evolution and selection of quantitative traits Vol. 1 (Oxford, UK: Oxford University Press; ).
Werner C. R., Gaynor R. C., Gorjanc G., Hickey J. M., Kox T., Abbadi A., et al. . (2020). How population structure impacts genomic selection accuracy in cross-validation: Implications for practical breeding. Front. Plant Sci. 11. doi: 10.3389/fpls.2020.592977 PubMed DOI PMC
Wiggans G. R., Cole J. B., Hubbard S. M., Sonstegard T. S. (2017). Genomic selection in dairy cattle: the USDA experience. Annu. Rev. Anim. Biosci. 5, 309–327. doi: 10.1146/annurev-animal-021815-111422 PubMed DOI
Xu Y., Ma K., Zhao Y., Wang X., Zhou K., Yu G., et al. . (2021). Genomic selection: A breakthrough technology in rice breeding. Crop J. 9, 669–677. doi: 10.1016/j.cj.2021.03.008 DOI
Zanotto S., Ruttink T., Pégard M., Skøt L., Grieder C., Kölliker R., et al. . (2023). A genome-wide association study of freezing tolerance in red clover (Trifolium pratense L.) germplasm of European origin. Front. Plant Sci. 14. doi: 10.3389/fpls.2023.1189662 PubMed DOI PMC
Zhao Y., Gowda M., Liu W., Würschum T., Maurer H., Longin F., et al. . (2012). Accuracy of genomic selection in European maize elite breeding populations. Theor. Appl. Genet. 124, 769–776. doi: 10.1007/s00122-011-1745-y PubMed DOI