Abstract
Key message
Simultaneous improvement of protein content and grain yield by index selection is possible but its efficiency largely depends on the weighting of the single traits. The genetic architecture of these indices is similar to that of the primary traits.
Abstract
Grain yield and protein content are of major importance in durum wheat breeding, but their negative correlation has hampered their simultaneous improvement. To account for this in wheat breeding, the grain protein deviation (GPD) and the protein yield were proposed as targets for selection. The aim of this work was to investigate the potential of different indices to simultaneously improve grain yield and protein content in durum wheat and to evaluate their genetic architecture towards genomics-assisted breeding. To this end, we investigated two different durum wheat panels comprising 159 and 189 genotypes, which were tested in multiple field locations across Europe and genotyped by a genotyping-by-sequencing approach. The phenotypic analyses revealed significant genetic variances for all traits and heritabilities of the phenotypic indices that were in a similar range as those of grain yield and protein content. The GPD showed a high and positive correlation with protein content, whereas protein yield was highly and positively correlated with grain yield. Thus, selecting for a high GPD would mainly increase the protein content whereas a selection based on protein yield would mainly improve grain yield, but a combination of both indices allows to balance this selection. The genome-wide association mapping revealed a complex genetic architecture for all traits with most QTL having small effects and being detected only in one germplasm set, thus limiting the potential of marker-assisted selection for trait improvement. By contrast, genome-wide prediction appeared promising but its performance strongly depends on the relatedness between training and prediction sets.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Acreche MM, Slafer GA (2009) Variation of grain nitrogen content in relation with grain yield in old and modern Spanish wheats grown under a wide range of agronomic conditions in a Mediterranean region. J Agric Sci 147:657–667. https://doi.org/10.1017/S0021859609990190
Addison CK, Mason RE, Brown-Guedira G et al (2016) QTL and major genes influencing grain yield potential in soft red winter wheat adapted to the southern United States. Euphytica 209:665–677. https://doi.org/10.1007/s10681-016-1650-1
Avni R, Nave M, Barad O et al (2017) Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science (80-) 357:93–97. https://doi.org/10.1126/science.aan0032
Blanco A, Simeone R, Gadaleta A (2006) Detection of QTLs for grain protein content in durum wheat. Theor Appl Genet 112:1195–1204. https://doi.org/10.1007/s00122-006-0221-6
Blanco A, Mangini G, Giancaspro A et al (2012) Relationships between grain protein content and grain yield components through quantitative trait locus analyses in a recombinant inbred line population derived from two elite durum wheat cultivars. Mol Breed 30:79–92. https://doi.org/10.1007/s11032-011-9600-z
Boeven PHG, Longin CFH, Leiser WL, Kollers K, Ebmeyer E, Würschum T (2016) 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
Bogard M, Allard V, Brancourt-Hulmel M et al (2010) Deviation from the grain protein concentration-grain yield negative relationship is highly correlated to post-anthesis N uptake in winter wheat. J Exp Bot 61:4303–4312. https://doi.org/10.1093/jxb/erq238
Bogard M, Allard V, Martre P et al (2013) Identifying wheat genomic regions for improving grain protein concentration independently of grain yield using multiple inter-related populations. Mol Breed 31:587–599. https://doi.org/10.1007/s11032-012-9817-5
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635. https://doi.org/10.1093/bioinformatics/btm308
Brevis JC, Dubcovsky J (2010) Effects of the chromosome region including the Gpc-B1 locus on wheat grain and protein yield. Crop Sci 50:93–104. https://doi.org/10.2135/cropsci2009.02.0057
CNR InterOmics (2017) CNR InterOmics Consortium. http://www.interomics.eu/wild-emmer-wheat-genome. Accessed 26 Oct 2017
Cochran WG, Cox GM (1957) Experimental designs, second. Wiley, New York
Crossa J, Pérez P, Hickey J et al (2014) Genomic prediction in CIMMYT maize and wheat breeding programs. Heredity 112:48–60. https://doi.org/10.1038/hdy.2013.16
Dao HQ, Byrne PF, Reid SD, Haley SD (2017) Validation of quantitative trait loci for grain quality-related traits in a winter wheat mapping population. Euphytica 213:1–13. https://doi.org/10.1007/s10681-016-1793-0
Díaz A, Zikhali M, Turner AS, Isaac P, Laurie DA (2012) Copy number variation affecting the photoperiod-B1 and vernalization-A1 genes is associated with altered flowering time in wheat (Triticum aestivum). PLoS One 7:e33234. https://doi.org/10.1371/journal.pone.0033234
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-L (2012) Shrinkage estimation of the realized relationship matrix. G3 Genes Genomes Genet Genet 2:1405–1413. https://doi.org/10.1534/g3.112.004259
Fois S, Schlichting L, Marchylo B, Dexter J, Motzo R, Giunta F (2011) Environmental conditions affect semolina quality in durum wheat (Triticum turgidum ssp. durum L.) cultivars with different gluten strength and gluten protein composition. J Sci Food Agric 91:2664–2673. https://doi.org/10.1002/jsfa.4509
Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2009) ASReml user guide release 3.0. VSN International Ltd, Hemel Hempstead
Gonzalez-Hernandez JL, Elias EM, Kianian SF (2004) Mapping genes for grain protein concentration and grain yield on chromosome 5B of Triticum turgidum (L.) var. dicoccoides. Euphytica 139:217–225. https://doi.org/10.1007/s10681-004-3157-4
He S, Schulthess AW, Mirdita V et al (2016) Genomic selection in a commercial winter wheat population. Theor Appl Genet 129:641–651. https://doi.org/10.1007/s00122-015-2655-1
Kaur A, Singh N, Kaur S et al (2015) Relationship of various flour properties with noodle making characteristics among durum wheat varieties. Food Chem 188:517–526. https://doi.org/10.1016/j.foodchem.2015.05.009
Koekemoer FP, Labuschagne MT, Van Deventer CS (1999) A selection strategy for combining high grain yield and high protein content in South African wheat cultivars. Cereal Res Commun 27:107–114
Kurasch AK, Hahn V, Leiser WL, Starck N, Würschum T (2017) Phenotypic analysis of major agronomic traits in 1008 RILs from a diallel of early European soybean varieties. Crop Sci 57:726–738. https://doi.org/10.2135/cropsci2016.05.0318
Li H, Vikram P, Singh RP et al (2015) A high density GBS map of bread wheat and its application for dissecting complex disease resistance traits. BMC Genom. https://doi.org/10.1186/s12864-015-1424-5
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 11:1–19. https://doi.org/10.1371/journal.pone.0158635
Longin CFH, Sieber AN, Reif JC (2013) Combining frost tolerance, high grain yield and good pasta quality in durum wheat. Plant Breed 132:353–358. https://doi.org/10.1111/pbr.12064
Maccaferri M, Sanguineti MC, Corneti S et al (2008) Quantitative trait loci for grain yield and adaptation of durum wheat (Triticum durum Desf.) across a wide range of water availability. Genetics 178:489–511. https://doi.org/10.1534/genetics.107.077297
Mahjourimajd S, Taylor J, Rengel Z et al (2016) The genetic control of grain protein content under variable nitrogen supply in an Australian wheat mapping population. PLoS One 11:1–13. https://doi.org/10.1371/journal.pone.0159371
Marulanda JJ, Mi X, Melchinger AE, Xu J-L, Würschum T, Longin CFH (2016) Optimum breeding strategies using genomic selection for hybrid breeding in wheat, maize, rye, barley, rice and triticale. Theor Appl Genet 129:1901–1913. https://doi.org/10.1007/s00122-016-2748-5
Monaghan JM, Snape JW, Chojecki JS, Kettlewell PS (2001) The use of grain protein deviation for identifying wheat cultivars with high grain protein concentration and yield. Euphytica 122:309–317
Money D, Gardner K, Migicovsky Z, Schwaninger H, Zhong G-Y, Myles S (2015) LinkImpute: fast and accurate genotype imputation for non-model organisms. G3 Genes Genomes Genet 5:2383–2390. https://doi.org/10.1534/g3.115.021667
Muterko A, Kalendar R, Salina E (2016) Novel alleles of the vernalization1 genes in wheat are associated with modulation of DNA curvature and flexibility in the promoter region. BMC Plant Biol 16:65–81. https://doi.org/10.1186/s12870-015-0691-2
Olmos S, Distelfeld A, Chicaiza O et al (2003) Precise mapping of a locus affecting grain protein content in durum wheat. Theor Appl Genet 107:1243–1251. https://doi.org/10.1007/s00122-003-1377-y
Oury FX, Godin C (2007) Yield and grain protein concentration in bread wheat: how to use the negative relationship between the two characters to identify favourable genotypes? Euphytica 157:45–57. https://doi.org/10.1007/s10681-007-9395-5
Piepho H-P, Möhring J (2007) Computing heritability and selection response from unbalanced plant breeding trials. Genetics 177:1881–1888. https://doi.org/10.1534/genetics.107.074229
Quarrie SA, Steed A, Calestani C et al (2005) A high-density genetic map of hexaploid wheat (Triticum aestivum L.) from the cross Chinese Spring × SQ1 and its use to compare QTLs for grain yield across a range of environments. Theor Appl Genet 110:865–880. https://doi.org/10.1007/s00122-004-1902-7
R Development Core Team (2017) R: a language and environment for statistical computing. http://www.r-project.org. Accessed 26 Oct 2017
Raman R, Allen H, Diffey S, Raman H, Martin P, McKelvie K (2009) Localisation of quantitative trait loci for quality attributes in a doubled haploid population of wheat (Triticum aestivum L.). Genome 52:701–715. https://doi.org/10.1139/g09-045
Riedelsheimer C, Endelman JB, Stange M, Sorrells ME, Jannink J-L, Melchinger AE (2013) Genomic predictability of interconnected biparental maize populations. Genetics 194:493–503. https://doi.org/10.1534/genetics.113.150227
Sieber AN, Würschum T, Longin CFH (2015) Vitreosity, its stability and relationship to protein content in durum wheat. J Cereal Sci 61:71–77. https://doi.org/10.1016/j.jcs.2014.10.008
Sieber A-N, Longin CFH, Würschum T (2017) Molecular characterization of winter durum wheat (Triticum durum) based on a genotyping-by-sequencing approach. Plant Genet Resour 15:36–44. https://doi.org/10.1017/S1479262115000349
Soriano JM, Malosetti M, Rosello M, Sorrells ME, Royo C (2017) Dissecting the old Mediterranean durum wheat genetic architecture for phenology, biomass and yield formation by association mapping and QTL meta-analysis. PLoS One 12:1–19. https://doi.org/10.1371/journal.pone.0178290
Stram DO, Lee JW (1994) Variance components testing in the longitudinal mixed effects model. Biometrics 50:1171–1177
Suprayogi Y, Pozniak CJ, Clarke FR, Clarke JM, Knox RE, Singh AK (2009) Identification and validation of quantitative trait loci for grain protein concentration in adapted Canadian durum wheat populations. Theor Appl Genet 119:437–448. https://doi.org/10.1007/s00122-009-1050-1
Tiwari C, Wallwork H, Arun B et al (2016) Molecular mapping of quantitative trait loci for zinc, iron and protein content in the grains of hexaploid wheat. Euphytica 207:563–570. https://doi.org/10.1007/s10681-015-1544-7
Wang Y, Li H, Zhang L, Lü W, Wang J (2012) On the use of mathematically-derived traits in QTL mapping. Mol Breed 29:661–673. https://doi.org/10.1007/s11032-011-9580-z
Williams E, Piepho HP, Whitaker D (2011) Augmented p-rep designs. Biom J 53:19–27. https://doi.org/10.1002/bimj.201000102
Würschum T, Reif JC, Kraft T, Janssen G, Zhao Y (2013) Genomic selection in sugar beet breeding populations. BMC Genet. https://doi.org/10.1186/1471-2156-14-85
Würschum T, Abel S, Zhao Y (2014) Potential of genomic selection in rapeseed (Brassica napus L.) breeding. Plant Breed 133:45–51. https://doi.org/10.1111/pbr.12137
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, Leiser WL, Kazman E, Longin CFH (2016) Genetic control of protein content and sedimentation volume in European winter wheat cultivars. Theor Appl Genet 129:1685–1696. https://doi.org/10.1007/s00122-016-2732-0
Würschum T, Leiser WL, Longin CFH (2017) Molecular genetic characterization and association mapping in spelt wheat. Plant Breed. https://doi.org/10.1111/pbr.12462
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, Gowda M, Longin FH, Würschum T, Ranc N, Reif JC (2012) Impact of selective genotyping in the training population on accuracy and bias of genomic selection. Theor Appl Genet 125:707–713. https://doi.org/10.1007/s00122-012-1862-2
Zhao Y, Mette MF, Reif JC (2015) Genomic selection in hybrid breeding. Plant Breed 134:1–10. https://doi.org/10.1111/pbr.12231
Acknowledgements
We thank the international consortium of the CNR Inter Omics project of providing us access to their online platform and allowing us to substantiate our results from the genome-wide association mapping with estimated physical map positions. The financial support of Deutsche Forschungsgemeinschaft is highly acknowledged (DFG LO 1816–2/1, DFG LO 1816–4/1).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical standard
The authors declare that the experiments comply with the current laws of Germany.
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Xianchun Xia.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rapp, M., Lein, V., Lacoudre, F. et al. Simultaneous improvement of grain yield and protein content in durum wheat by different phenotypic indices and genomic selection. Theor Appl Genet 131, 1315–1329 (2018). https://doi.org/10.1007/s00122-018-3080-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-018-3080-z