Skip to main content
Log in

Genome-wide association mapping of agronomic traits and carbon isotope discrimination in a worldwide germplasm collection of spring wheat using SNP markers

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Association mapping has been proposed to identify polymorphisms involved in phenotypic variations and may prove useful in identifying interesting alleles for breeding purposes. Using this approach, a total of 382 cultivars and advanced lines of spring wheat obtained from three breeding programs (Chile, Uruguay and CIMMYT) were evaluated for plant height (PH), kernels per spike (KS), 1,000 kernel weight (TKW), grain yield and carbon isotope discrimination (Δ13C) and tested for genotyping-by-sequencing-derived SNP markers across the hexaploid wheat genome. A Bayesian clustering approach via Markov chain Monte Carlo was performed to examine the genetic differentiation (F ST) among different genetic groups. The results indicated the existence of two distinct and strongly differentiated genetic groups. Cluster I contained 215 genotypes (56.3 %), over 60 % (137/215) of which were collected from CIMMYT. Cluster II showed the highest F ST value, according to 95 % credible interval. Linkage disequilibrium (LD) among SNPs was calculated for the A, B and D genomes and at the whole-genome level. LD decayed over a longer genetic distance for the D genome than for the A and B genomes. In the A and B genomes, LD declined to 50 % of its initial value at about 2 cM. In the D genome, LD was much more extensive, declining to 50 % of its initial value only at 22 cM. In the whole genome, LD declined to 50 % of its initial value at an average of 4 cM. Important genomic regions associated with complex traits in spring wheat were identified. Selection on these regions may increase the efficiency of the current breeding programs. Although most of the associations were environment specific, some stable associations were detected for Δ13C, KS, PH and TKW. Chromosomes 1A, 3A, 4A and 5A were the most important chromosomes, as they comprised quantitative trait loci (QTL) for Δ13C, a trait that can be used as an indirect tool for increased water-use efficiency in wheat. Environment-specific genomic regions were detected, indicating the presence of QTL-by-environment interaction. To produce suitable genotypes under contrasting water availability conditions, QTL × E interactions (and genotype-by-environment interaction) should be considered in the current spring wheat breeding program.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alheit KV, Maurer HP, Reif JC, Tucker MR, Hahn V, Weissmann EA, Würschum T (2012) Genome-wide evaluation of genetic diversity and linkage disequilibrium in winter and spring triticale (× Triticosecale Wittmack). BMC Genom 13:235

    Article  CAS  Google Scholar 

  • Araus JL, Slafer GA, Reynolds M, Royo C (2002) Plant breeding and drought in C3 cereals: what should we breed for? Ann Bot 89:925–940

    Article  PubMed Central  PubMed  Google Scholar 

  • Araus JL, Slafer GA, Royo C, Serret MD (2008) Breeding for yield potential and stress adaptation in cereals. Crit Rev Plant Sci 27:377–412

    Article  Google Scholar 

  • Arriagada O, Mora F, Dellarossa JC, Ferreira MFS, Cervigni GDL, Schuster I (2012) Bayesian mapping of quantitative trait loci (QTL) controlling soybean cyst nematode resistant. Euphytica 186:907–917

    Article  Google Scholar 

  • Bertioli DJ, Ozias-Akins P, Chu Y, Dantas KM, Santos SP, Gouvea E, Guimarães PM, Leal-Bertioli SCM, Knapp SJ, Moretzsohn MC (2014) The use of SNP markers for linkage mapping in diploid and tetraploid peanuts. G3 4:89–96

    Article  PubMed Central  PubMed  Google Scholar 

  • Bradbury PJ, Zhang ZW, Kroon DE, Casstevens RM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    Article  CAS  PubMed  Google Scholar 

  • Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177

    Article  PubMed Central  PubMed  Google Scholar 

  • Cattivelli L, Rizza F, Badeck F-W, Mazzucotelli E, Mastrangelo AM, Francia E, Marè C, Tondelli A, Stanca AM (2008) Drought tolerance improvement in crop plants: an integrated view from breeding to genomics. Field Crop Res 105:1–14

    Article  Google Scholar 

  • Chao S, Dubcovsky J, Dvorak J, Luo MC, Baenziger SP, Matnyazov R, Clark DR, Talbert LE, Anderson JA, Dreisigacker S, Glover K, Chen J, Campbell K, Bruckner PL, Rudd JC, Haley S, Carver BF, Perry S, Sorrells ME (2010) Akhunov ED (2010), Population- and genome-specific patterns of linkage disequilibrium and SNP variation in spring and winter wheat (Triticum aestivum L.). BMC Genom 11:727

    Article  CAS  Google Scholar 

  • Chenu K, Cooper M, Hammer GL, Mathews KL, Dreccer MF, Chapman SC (2012) Environment characterization as an aid to wheat improvement: interpreting genotype–environment interactions by modelling water-deficit patterns in North-Eastern Australia. J Exp Bot 62:1743–1755

    Article  Google Scholar 

  • Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2004) Breeding for high water-use efficiency. J Exp Bot 55:2447–2460

    Article  CAS  PubMed  Google Scholar 

  • Crossa J, Burgueñ J, Dreisigacker S, Vargas M, Herrera-Foessel SA, Lillemo M, Singh RP, Trethowan R, Warburton M, Franco J, Reynolds M, Crouch JH, Ortiz R (2007) Association analysis of historical bread wheat germplasm using additive genetic covariance of relatives and population structure. Genetics 177:1889–1913

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cuesta-Marcos A, Szűcs P, Close TJ, Filichkin T, Muehlbauer GJ, Smith KP, Hayes PM (2010) Genome-wide SNPs and re-sequencing of growth habit and inflorescence genes in barley: implications for association mapping in germplasm arrays varying in size and structure. BMC Genom. doi:10.1186/1471-2164-11-707

    Google Scholar 

  • del Pozo A, del Canto P (1999) Áreas agroclimáticas y sistemas productivos en la VII y VIII regiones. Instituto de Investigaciones Agropecuarias. Ministerio de Agricultura. Serie Quilamapu N◦ 113, 115 p

  • Dodig D, Zori M, Kobiljski B, Savi J, Kandi V, Quarrie S, Barnes J (2012) Genetic and association mapping study of wheat agronomic traits under contrasting water regimes. Int J Mol Sci 13:6167–6188

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Edae EA, Byrne PF, Haley SD, Lopes MS, Reynolds MP (2014) Genome-wide association mapping of yield and yield components of spring wheat under contrasting moisture regimes. Theor Appl Genet. doi:10.1007/s00122-013-2257-8

    PubMed  Google Scholar 

  • El-Soda M, Malosetti M, Zwaan BJ, Koornneef M, Aarts MGM (2014) Genotype × environment interaction QTL mapping in plants: lessons from Arabidopsis. Trends Plant Sci. doi:10.1016/j.tplants.2014.01.001

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software Structure: a simulation study. Mol Ecol 14:2611–2620

  • Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374

    Article  CAS  PubMed  Google Scholar 

  • Gupta PK, Rustgi S, Kulwal PL (2005) Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Mol Biol 57:461–485

    Article  CAS  PubMed  Google Scholar 

  • Hamblin MT, Buckler ES, Jannink JL (2011) Population genetics of genomics-based crop improvement methods. Trends Genet 27:98–106

    Article  CAS  PubMed  Google Scholar 

  • Hao C, Wang L, Ge H, Dong Y, Zhang X (2011) Genetic diversity and linkage disequilibrium in Chinese bread wheat (Triticum aestivum L.) revealed by SSR markers. PLoS ONE 6:e17279. doi:10.1371/journal.pone.0017279.t001

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Heidelberger P, Welch PD (1983) Simulation run length control in the presence of an initial transient. Oper Res 31:1109–1114

  • Inostroza L, del Pozo A, Matus I, Castillo D, Hayes P, Machado S, Corey A (2009) Association mapping of plant height, yield, and yield stability in recombinant chromosome substitution lines (RCSLs) using Hordeum vulgare subsp. spontaneum as a source of donor alleles in a Hordeum vulgare subsp. vulgare background. Mol Breed 23:365–376

    Article  Google Scholar 

  • Kirigwi FM, Van Ginkel M, Brown-Guedira G, Gill BS, Paulsen GM, Fritz AK (2007) Markers associated with a QTL for grain yield in wheat under drought. Mol Breed 20:401–413

    Article  CAS  Google Scholar 

  • Kumar S, Singh B (2009) Effect of water stress on carbon isotope discrimination and Rubisco activity in bread and durum wheat genotypes. Physiol Mol Biol Plants 15(3):281–286

    Article  PubMed Central  PubMed  Google Scholar 

  • Lado L, Matus I, Rodríguez A, Inostroza L, Poland J, Belzile F, del Pozo A, Quincke M, von Zitzewitz J (2013) Increased genomic prediction accuracy in wheat breeding through spatial adjustment of field trial data. G3 3:2105–2114

    Article  PubMed Central  PubMed  Google Scholar 

  • Laidò G, Marone D, Russo MA, Colecchia SA, Mastrangelo AM, De Vita P, Papa R (2014) Linkage disequilibrium and genome-wide association mapping in tetraploid wheat (Triticum turgidum L.). PLoS ONE 9:e95211. doi:10.1371/journal.pone.0095211

    Article  PubMed Central  PubMed  Google Scholar 

  • Liu L, Wang L, Yao J, Zheng Y, Zhao C (2010) Association mapping of six agronomic traits on chromosome 4A of wheat (Triticum aestivum L.). Mol. Plant Breed. doi:10.5376/mpb.2010.01.0005

    Google Scholar 

  • Mackay I, Powell W (2007) Methods for linkage disequilibrium mapping in crops. Trends Plant Sci 12:57–63

    Article  CAS  PubMed  Google Scholar 

  • Mamidi S, Chikara S, Goos RJ, Hyten DL, Annam D, Moghaddam SM, Lee RK, Cregan PB, McClean PE (2011) Genome-wide association analysis identifies candidate genes associated with iron deficiency chlorosis in soybean. Plant Genome 4:154–164

    Article  CAS  Google Scholar 

  • Marquez-Cedillo LA, Hayes PM, Jones BL, Kleinhofs A, Legge WG, Rossnagel BG, Sato K, Ullrich E, Wesenberg DM (2000) QTL analysis of malting quality in barley based on the doubled-haploid progeny of two elite North American varieties representing different germplasm groups. Theor Appl Genet 101:173–184

    Article  CAS  Google Scholar 

  • McNally KL, Childs KL, Bohnert R, Davidson RM, Zhao K, Ulata VJ, Zellerc G, Clark RM, Hoeng DR, Bureaug TE, Stokowski R, Ballinger DG, Frazer KA, Cox DR, Padhukasahasram B, Bustamante CD, Weigel D, Mackill DJ, Bruskiewich RM, Ratsch G, Buell CR, Leung H, Leach JE (2009) Genomewide SNP variation reveals relationships among landraces and modern varieties of rice. PNAS 106(30):12273–12278

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mora F, Serra N (2014) Bayesian estimation of genetic parameters for growth, stem straightness, and survival in Eucalyptus globulus on an Andean Foothill site. Tree Genet Genomes. doi:10.1007/s11295-014-0716-2

    Google Scholar 

  • Moragues M, Comadran J, Waugh R, Milne I, Flavell AJ, Russell JR (2010) Effects of ascertainment bias and marker number on estimations of barley diversity from high-throughput SNP genotype data. Theor Appl Genet 120:1525–1534

    Article  CAS  PubMed  Google Scholar 

  • Myles S, Peiffer J, Brown PJ, Ersoz ES, Zhang Z, Costich DE, Buckler ES (2009) Association mapping: critical considerations shift from genotyping to experimental design. Plant Cell 21:2194–2202

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nadeau JH, Frankel WN (2000) The roads from phenotypic variation to gene discovery: mutagenesis versus QTLs. Nat Genet 25:381–384

    Article  CAS  PubMed  Google Scholar 

  • Nei M, Li WH (1976) The transient distribution of allele frequencies under mutation pressure. Genet Res 28:205–214

    Article  CAS  PubMed  Google Scholar 

  • Nordborg M, Tavare S (2002) Linkage disequilibrium: what history has to tell us. Trend Genet 18:83–90

    Article  CAS  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peleg Z, Fahima T, Krugman T, Abbo S, Yakir D, Korol AB, Saranga Y (2009) Genomic dissection of drought resistance in durum wheat × wild emmer wheat recombinant inbreed line population. Plant, Cell Environ 32:758–779

    Article  CAS  Google Scholar 

  • Poland JA, Brown PJ, Sorrells ME, Jannink JL (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS ONE 7:e32253

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ranc N, Muños S, Xu J, Le Paslier MC, Chauveau A, Bounon R, Rolland S, Bouchet JP, Brunel D, Causse M (2012) Genome-wide association mapping in tomato (Solanum lycopersicum) is possible using genome admixture of Solanum lycopersicum var. cerasiforme. G3 2:853–864

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rebetzke GJ, van Herwaarden AF, Jenkeins C, Weiss M, Lewis D, Ruuska S, Tabe L, Fettell NA, Richards RA (2008a) Quantitative trait loci for water-soluble carbohydrates and associations with agronomic traits in wheat. Aust J Agric Res 59:891–905

    Article  CAS  Google Scholar 

  • Rebetzke GJ, Condon AG, Farquhar GD, Appels R, Richards RA (2008b) Quantitative trait loci for carbon isotope discrimination are repeatable across environments and wheat mapping populations. Theor Appl Genet 118:123–137

    Article  CAS  PubMed  Google Scholar 

  • Reynolds M, Mujeeb-kazi A, Sawkins M (2005) Prospects for utilising plant-adaptive mechanisms to improve wheat and other crops in drought- and salinity-prone environments. Ann Appl Biol 146:239–259

    Article  CAS  Google Scholar 

  • Saavedra J, Silva TA, Mora F, Scapim CA (2013) Bayesian analysis of genetic structure of a Brazilian popcorn germplasm using data from simple sequence repeats (SSR). Chil J Agric Res 73:99–107

    Article  Google Scholar 

  • Simko I, Haynes KG, Jones RW (2006) Assessment of linkage disequilibrium in potato genome with single nucleotide polymorphism markers. Genetics 173(4):2237–2245

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Snape JW, Foulkes MJ, Simmonds J, Leverington M, Fish LJ, Wang Y, Ciavarrella M (2007) Dissecting gene × environmental effects on wheat yields via QTL and physiological analysis. Euphytica 154:401–408

    Article  Google Scholar 

  • Stolpe NB (2006) Descripciones de los principales suelos de la VIII Región de Chile. Universidad de Concepción, Departamento de Suelos y recursos naturales 112

    Google Scholar 

  • Sved JA (1971) Linkage disequilibrium and homozygosity of chromosome segments in finite populations. Theor Popul Biol 2:125–141

    Article  CAS  PubMed  Google Scholar 

  • Tambussi EA, Bort J, Araus JL (2007) Water use efficiency in C3 cereals under Mediterranean conditions: a review of physiological aspects. Ann Appl Biol 150:307–321

    Article  Google Scholar 

  • Tondelli A, Francia E, Barabaschi D, Aprile A, Skinner JS, Stockinger EJ, Stanca AM, Pecchioni N (2006) Mapping regulatory genes as candidates for cold and drought stress tolerance in barley. Theor Appl Genet 112:445–454

    Article  CAS  PubMed  Google Scholar 

  • Wei W, Zhang Y, Lü H, Li D, Wang L, Zhang X (2013) Association analysis for quality traits in a diverse panel of Chinese sesame (Sesamum indicum L.) germplasm. INTEGR. Plant Biol 55(8):745–758

    CAS  Google Scholar 

  • Wu X, Chang X, Jing R (2012) Genetic insight into yield-associated traits of wheat grown in multiple rain-fed environments. PLoS ONE 7:e31249

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Yang D, Jing R, Chang X, Li W (2007) Identification of quantitative trait loci and environmental interactions for accumulation and remobilization of water-soluble carbohydrates in wheat (Triticum aestivum L.) stems. Genetics 176:571–584

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yu J, Buckler ES (2006) Genetic association mapping and genome organization of maize. Curr Opin Biotechnol 17:155–160

    Article  CAS  PubMed  Google Scholar 

  • Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421

  • Zhang H, Cui F, Wang L, Li J, Ding A, Zhao C, Bao Y, Yang Q, Wang H (2013) Conditional and unconditional QTL mapping of drought-tolerance-related traits of wheat seedling using two related RIL populations. J Genet 92:213–231. doi:10.1371/journal.pone.0031249

    Article  PubMed  Google Scholar 

  • Zhao F, Xu S (2012) Genotype by environment interaction of quantitative traits: a case study in barley. G3 2:779–788

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhu Ch, Gore M, Buckler ES, Jianming Yu (2008) Status and prospects of association mapping in plants. The Plant Genome 1:5–20

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the research grants FONDECYT No. 1110732 and FONTAGRO ATN/OC-11943. We thank Alejandro Castro for technical assistance in field experiments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alejandro del Pozo.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mora, F., Castillo, D., Lado, B. et al. Genome-wide association mapping of agronomic traits and carbon isotope discrimination in a worldwide germplasm collection of spring wheat using SNP markers. Mol Breeding 35, 69 (2015). https://doi.org/10.1007/s11032-015-0264-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11032-015-0264-y

Keywords

Navigation