Abstract
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This study revealed a complex genetic architecture of male floral traits in wheat, and Rht-D1 was identified as the only major QTL. Genome-wide prediction approaches but also phenotypic recurrent selection appear promising to increase outcrossing ability required for hybrid wheat seed production.
Abstract
Hybrid wheat breeding is a promising approach to increase grain yield and yield stability. However, the identification of lines with favorable male floral characteristics required for hybrid seed production currently poses a severe bottleneck for hybrid wheat breeding. This study therefore aimed to unravel the genetic architecture of floral traits and to assess the potential of genomic approaches to accelerate their improvement. To this end, we employed a panel of 209 diverse winter wheat lines assessed for male floral traits and genotyped with genome-wide markers as well as for Rht-B1 and Rht-D1. We found the highest proportion of explained genotypic variance for the Rht-D1 locus (11–24 %), for which the dwarfing allele Rht-D1b had a negative effect on anther extrusion, visual anther extrusion and pollen mass. The genome-wide scan detected only few QTL with small or medium effects, indicating a complex genetic architecture. Consequently, marker-assisted selection yielded only moderate prediction abilities (0.44–0.63), mainly relying on Rht-D1. Genomic selection based on weighted ridge-regression best linear unbiased prediction achieved higher prediction abilities of up to 0.70 for anther extrusion. In conclusion, recurrent phenotypic selection appears most cost-effective for the initial improvement of floral traits in wheat, while genome-wide prediction approaches may be worthwhile when complete marker profiles are already available in a hybrid wheat breeding program.
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References
Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664
Aulchenko YS, Ripke S, Isaacs A, van Duijn CM (2007) GenABEL: an R library for genome-wide association analysis. Bioinformatics 23:1294–1296
Balding DJ (2006) A tutorial on statistical methods for population association studies. Nat Rev Genet 7:781–791
Beri SM, Anand SC (1971) Factors affecting pollen shedding capacity in wheat. Euphytica 20:327–332
Boeven PHG, Longin CFH, Würschum T (2016) A unified framework for hybrid breeding and the establishment of heterotic groups in wheat. Theor Appl Genet 129:1231–1245
Börner A, Plaschke J, Korzun V, Worland AJ (1996) The relationships between the dwarfing genes of wheat and rye. Euphytica 89:69–75
Buerstmayr M, Buerstmayr H (2015) Comparative mapping of quantitative trait loci for Fusarium head blight resistance and anther retention in the winter wheat population Capo × Arina. Theor Appl Genet 128:1519–1530
Buerstmayr M, Lemmens M, Steiner B, Buerstmayr H (2011) Advanced backcross QTL mapping of resistance to Fusarium head blight and plant morphological traits in a Triticum macha × T. aestivum population. Theor Appl Genet 123:293–306
Butler DG, Cullis BR, Gilmour AR, Gogel BJ (2009) Mixed models for S language environments. ASReml-R reference manual: Release 3.0. Technical report. ASReml estimates variance components under a general linear mixed model by residual maximum likelihood (REML). https://www.vsni.co.uk/software/asreml
Cheng H, Qin L, Lee S, Fu X, Richards DE, Cao D, Luo D, Harberd NP, Peng J (2004) Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131:1055–1064
Cullis BR, Smith AB, Coombes NE (2006) On the design of early generation variety trials with correlated data. J Agric Biol Environ Stat 11:381–393
De Vries AP (1971) Flowering biology of wheat, particularly in view of hybrid seed production—a review. Euphytica 20:152–170
De Vries AP (1972) Some aspects of cross-pollination in wheat (Triticum aestivum L.). 1. Pollen concentration in the field as influenced by variety, diurnal pattern, weather conditions and level as compared to the height of the pollen donor. Euphytica 21:185–203
De Vries AP (1974) Some aspects of cross-pollination in wheat (Triticum aestivum L.). 3. Anther length and number of pollen grains per anther. Euphytica 23:11–19
d’Souza L (1970) Untersuchungen über die Eignung des Weizens als Pollenspender bei der Fremdbefruchtung, verglichen mit Roggen, Triticale und Secalutricum (In German). Z Pflanzenzucht 63:246–269
Echeverry-Solarte M, Kumar A, Kianian S, Mantovani EE, Simsek S, Alamri MS, Mergoum M (2014) Genome-wide genetic dissection of supernumerary spikelet and related traits in common wheat. Plant Genome 7. doi:10.3835/plantgenome2014.03.0013
Ellis MH, Spielmeyer W, Gale KR, Rebetzke GJ, Richards RA (2002) “Perfect” markers for the Rht-B1b and Rht-D1b dwarfing genes in wheat. Theor Appl Genet 105:1038–1042
Endelman JB (2011) Ridge regression and other kernels for genomic selection with R package rrBLUP. Plant Genome 4:250–255
FAOSTAT (2016) Statistical databases and datasets of the Food and Agriculture Organization of the United Nations. http://faostat.fao.org/. Accessed 16 May 2016
Foley JA, Ramankutty N, Brauman KA, Cassidy ES, Gerber JS, Johnston M, Mueller ND, O’Connell C, Ray DK, West PC, Balzer C, Bennett EM, Carpenter SR, Hill J, Monfreda C, Polasky S, Rockström J, Sheehan J, Siebert S, Tilman D, Zaks DPM (2011) Solutions for a cultivated planet. Nature 478:337–342
Fruwirth C (1905) Das Blühen von Weizen und Hafer (in German). Dt landwirt Presse 32:737–738
Gale MD, Youssefian S (1985) Dwarfing genes in wheat. In: Russell G (ed) Progress in Plant Breeding–1. Butterworth-Heinemann, London, pp 1–35
Godfray HCJ, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818
Gower JC (1966) Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53:325–338
Gupta R, Chakrabarty SK (2013) Gibberellic acid in plant: still a mystery unresolved. Plant Signal Behav 8:e25504
Hedden P (2003) The genes of the Green Revolution. Trends Genet 19:5–9
Heffner EL, Sorrells ME, Jannink J (2009) Genomic selection for crop improvement. Crop Sci 49:1–12
Jannink J, Lorenz AJ, Iwata H (2010) Genomic selection in plant breeding: from theory to practice. Brief Funct Genom Proteom 9:166–177
Joppa LR, McNeal FH, Berg MA (1968) Pollen production and pollen shedding of hard red spring (Triticum aestivum L. em Thell.) and durum (T. durum Desf.) wheats. Crop Sci 8:487–490
Kempe K, Gils M (2011) Pollination control technologies for hybrid breeding. Mol Breeding 27:417–437
Khush GS (2001) Green revolution: the way forward. Nat Rev Genet 2:815–822
Knopf C, Becker H, Ebmeyer E, Korzun V (2008) Occurrence of three dwarfing Rht genes in German winter wheat varieties. Cer Res Comm 36:553–560
Lande R, Thompson R (1990) Efficiency of marker-assisted selection in the improvement of quantitative traits. Genetics 124:743–756
Langer SM, Longin CFH, Würschum T (2014) Phenotypic evaluation of floral and flowering traits with relevance for hybrid breeding in wheat (Triticum aestivum L.). Plant Breed 133:433–441
Li Y, Xiao J, Wu J, Duan J, Liu Y, Ye X, Zhang X, Guo X, Gu Y, Zhang L, Jia J, Kong X (2012) A tandem segmental duplication (TSD) in green revolution gene Rht-D1b region underlies plant height variation. New Phytol 196:282–291
Longin CFH, Mühleisen J, Maurer HP, Zhang H, Gowda M, Reif JC (2012) Hybrid breeding in autogamous cereals. Theor Appl Genet 125:1087–1096
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
Longin CFH, Reif JC, Würschum T (2014) Long-term perspective of hybrid versus line breeding in wheat based on quantitative genetic theory. Theor Appl Genet 127:1635–1641
Longin CFH, Mi X, Würschum T (2015) Genomic selection in wheat: optimum allocation of test resources and comparison of breeding strategies for line and hybrid breeding. Theor Appl Genet 128:1297–1306
Lu Q, Lillemo M, Skinnes H, He X, Shi J, Ji F, Dong Y, Bjørnstad Å (2013) Anther extrusion and plant height are associated with Type I resistance to Fusarium head blight in bread wheat line ‘Shanghai-3/Catbird’. Theor Appl Genet 126:317–334
Ma Z, Zhao D, Zhang C, Zhang Z, Xue S, Lin F, Kong Z, Tian D, Luo Q (2007) Molecular genetic analysis of five spike-related traits in wheat using RIL and immortalized F2 populations. Mol Genet Genomics 277:31–42
Maurer HP, Melchinger AE, Frisch M (2008) Population genetic simulation and data analysis with Plabsoft. Euphytica 161:133–139
Meuwissen T, Hayes BJ, Goddard ME (2001) Prediction of total genetic value using genome-wide dense marker maps. Genetics 157:1819–1829
Money D, Gardner K, Migicovsky Z, Schwaninger H, Zhong G, Myles S (2015) LinkImpute: Fast and accurate genotype imputation for nonmodel organisms. G3 (Bethesda) 5:2383–2390
Mühleisen J, Piepho H, Maurer HP, Longin CFH, Reif JC (2014) Yield stability of hybrids versus lines in wheat, barley, and triticale. Theor Appl Genet 127:309–316
Muqaddasi QH, Lohwasser U, Nagel M, Börner A, Pillen K, Röder MS (2016) Genome-wide association mapping of anther extrusion in hexaploid spring wheat. PLoS ONE 11:e0155494
Mutasa-Göttgens E, Hedden P (2009) Gibberellin as a factor in floral regulatory networks. J Exp Bot 60:1979–1989
Ogutu JO, Schulz-Streeck T, Piepho H (2012) Genomic selection using regularized linear regression models: ridge regression, lasso, elastic net and their extensions. BMC Proc 6(Suppl 2):S10
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290
Patterson HD (1997) Analysis of series of variety trials. In: Kempton RA, Fox PN, Cerezo M (eds) Statistical methods for plant variety evaluation, 1st edn. Chapman & Hall, London, pp 139–161
Pearce S, Saville R, Vaughan SP, Chandler PM, Wilhelm EP, Sparks CA, Al-Kaff N, Korolev A, Boulton MI, Phillips AL, Hedden P, Nicholson P, Thomas SG (2011) Molecular characterization of Rht-1 dwarfing genes in hexaploid wheat. Plant Physiol 157:1820–1831
Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, Sudhakar D, Christou P, Snape JW, Gale MD, Harberd NP (1999) `Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261
Piepho H, Möhring J (2007) Computing heritability and selection response from unbalanced plant breeding trials. Genetics 177:1881–1888
R Core Team (2015) R: A Language and Environment for Statistical Computing. http://www.R-project.org/
Ray DK, Mueller ND, West PC, Foley JA (2013) Yield trends are insufficient to double global crop production by 2050. PLoS ONE 8:e66428
Sage G, de Isturiz MJ (1974) The inheritance of anther extrusion in two spring wheat varieties. Theor Appl Genet 45:126–133
Sala OE, Chapin Iii FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774
Singh SK, Arun B, Joshi AK (2007) Comparative evaluation of exotic and adapted germplasm of spring wheat for floral characteristics in the Indo-Gangetic Plains of northern India. Plant Breed 126:559–564
Singh SK, Chatrath R, Mishra B (2010) Perspective of hybrid wheat research: a review. Indian J Agric Sci 80:1013–1027
Skinnes H, Semagn K, Tarkegne Y, Marøy AG, Bjørnstad T (2010) The inheritance of anther extrusion in hexaploid wheat and its relationship to Fusarium head blight resistance and deoxynivalenol content. Plant Breed 129:149–155
Spindel JE, Begum H, Akdemir D, Collard B, Redoña E, Jannink J, McCouch S (2016) Genome-wide prediction models that incorporate de novo GWAS are a powerful new tool for tropical rice improvement. Heredity 116:395–408
Srinivasachary Gosman N, 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
Stram DO, Lee JW (1994) Variance components testing in the longitudinal mixed effects model. Biometrics 50:1171–1177
Taiz L, Zeiger E, Møller IM, Murphy A (2015) Plant physiology and development, 6th edn. Sinauer Associates Inc., Publishers, Sunderland
Tester M, Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327:818–822
Tilman D, Balzer C, Hill J, Befort BL (2011) Global food demand and the sustainable intensification of agriculture. Proc Natl Acad Sci USA 108:20260–20264
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
Waines JG, Hegde SG (2003) Intraspecific gene flow in bread wheat as affected by reproductive biology and pollination ecology of wheat flowers. Crop Sci 43:451–463
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 M, Dvorak J, Morell M, Dubcovsky J, Ganal M, Tuberosa R, Lawley C, Mikoulitch I, Cavanagh C, Edwards KJ, Hayden M, Akhunov E (2014) Characterization of polyploid wheat genomic diversity using a high-density 90000 single nucleotide polymorphism array. Plant Biotech J 12:787–796
Whitford R, Fleury D, Reif JC, Garcia M, Okada T, Korzun V, Langridge P (2013) Hybrid breeding in wheat: technologies to improve hybrid wheat seed production. J Exp Bot 64:5411–5428
Whittaker JC, Thompson R, Denham MC (2000) Marker-assisted selection using ridge regression. Genet Res 75:249–252
Wilhelm EP, Mackay IJ, Saville RJ, Korolev AV, Balfourier F, Greenl AJ, Boulton MI, Powell W (2013a) Haplotype dictionary for the Rht-1 loci in wheat. Theor Appl Genet 126:1733–1747
Wilhelm EP, Boulton MI, Al-Kaff N, Balfourier F, Bordes J, Greenland AJ, Powell W, Mackay IJ (2013b) Rht-1 and Ppd-D1 associations with height, GA sensitivity, and days to heading in a worldwide bread wheat collection. Theor Appl Genet 126:2233–2243
Williams E, Piepho H, Whitaker D (2011) Augmented p-rep designs. Biom J 53:19–27
Wilson P, Driscoll CJ (1983) Hybrid Wheat. In: Frankel R (ed) Heterosis: reappraisal of theory and practice, 1st edn. Springer, Berlin, pp 94–123
Wright S (1978) Evolution and genetics of populations, variability within and among natural populations, vol 4. The University of Chicago Press, Chicago, p 91
Würschum T (2012) Mapping QTL for agronomic traits in breeding populations. Theor Appl Genet 125:201–210
Würschum T, Langer SM, Longin CFH (2015) Genetic control of plant height in European winter wheat cultivars. Theor Appl Genet 128:865–874
Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208
Zhao Y, Mette MF, Gowda M, Longin CFH, Reif JC (2014) Bridging the gap between marker-assisted and genomic selection of heading time and plant height in hybrid wheat. Heredity 112:638–645
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. doi:10.1073/pnas.1514547112
Zohary D (1967) Disruptive selection, pollination systems and the origin of old world cultivated cereals. Cienc Cult 19:218
Acknowledgments
We thank Sabit Rrecaj and Sebastian Hajek for their outstanding work in the field at the research station of the University of Hohenheim and we highly appreciate the help of the Bachelor student Nadine Bauer. The authors thank KWS for providing the genotypic data and parts of phenotypes and highly appreciate the work of the breeding teams at the KWS research stations in Seligenstadt and Wohlde, in particular Nicolas Roperch and Hugo Gonzales Dupuy, for collecting phenotypic data.
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Boeven, P.H.G., Longin, C.F.H., Leiser, W.L. et al. Genetic architecture of male floral traits required for hybrid wheat breeding. Theor Appl Genet 129, 2343–2357 (2016). https://doi.org/10.1007/s00122-016-2771-6
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DOI: https://doi.org/10.1007/s00122-016-2771-6