Skip to main content
Log in

Genome-wide association study of pre-harvest sprouting tolerance using a 90K SNP array in common wheat (Triticum aestivum L.)

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

Three major loci for pre-harvest sprouting tolerance (PHST) were mapped on chromosomes 1AL, 3BS, and 6BL, and two CAPS and one dCAPS markers were validated. Sixteen lines with favorable alleles and increased PHST were identified.

Abstract

Pre-harvest sprouting (PHS) significantly affects wheat grain yield and quality. In the present study, the PHS tolerance (PHST) of 192 wheat varieties (lines) was evaluated by assessment of field sprouting, seed germination index, and period of dormancy in different environments. A high-density Illumina iSelect 90K SNP array was used to genotype the panel. A genome-wide association study (GWAS) based on single- and multi-locus mixed linear models was used to detect loci for PHST. The single-locus model identified 23 loci for PHST (P < 0.0001) and explained 6.0–18.9% of the phenotypic variance. Twenty loci were consistent with known quantitative trait loci (QTLs). Three single-nucleotide polymorphism markers closely linked with three major loci (Qphs.ahau-1A, Qphs.ahau-3B, and Qphs.ahau-6B) on chromosomes 1AL, 3BS, and 6BL, respectively, were converted to two cleaved amplified polymorphic sequences (CAPS) and one derived-CAPS markers, and validated in 374 wheat varieties (lines). The CAPS marker EX06323 for Qphs.ahau-6B co-segregated with a novel major QTL underlying PHST in a recombinant inbred line population raised from the cross Jing 411 × Wanxianbaimaizi. Linear regression showed a clear dependence of PHST on the number of favorable alleles. Sixteen varieties showing an elevated degree of PHST were identified and harbored more than 16 favorable alleles. The multi-locus model detected 39 marker–trait associations for PHST (P < 0.0001), of which five may be novel. Six loci common to the two models were identified. The combination of the two GWAS methods contributes to efficient dissection of the complex genetic mechanism of PHST.

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
Fig. 3

Similar content being viewed by others

References

  • Albrecht T, Oberforster M, Kempf H, Ramgraber L, Schacht J, Kazman E, Zechner E, Neumayer A, Hartl L, Mohler V (2015) Genome-wide association mapping of preharvest sprouting resistance in a diversity panel of European winter wheat. J Appl Genet 56:277–285

    Article  CAS  PubMed  Google Scholar 

  • Bailey PC, mckibbin RS, Lenton JR, Holdsworth MJ, Flintham JE, Gale MD, (1999) Genetic map locations for orthologous Vp1 genes in wheat and rice. Theor Appl Genet 98:281–284

    Article  CAS  Google Scholar 

  • Bates D, Maechler M, Bolker BM, Walker S (2015) lme4: linear mixed-effects models using Eigen and S4. J Stat Softw. Available from: https://lme4.r-forge.r-project.org/

  • Bradbury PJ, Zhang ZW, Kroon DE, Casstevens TM, 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  PubMed Central  Google Scholar 

  • Brown LK, Wiersma AT, Olson EL (2018) Preharvest sprouting and α-amylase activity in soft winter wheat. J Cereal Sci 79:311–318

    Article  CAS  Google Scholar 

  • Cabral AL, Jordan MC, McCartney CA, You FM, Humphreys DG, MacLachlan R, Pozniak CJ (2014) Identification of candidate genes, regions and markers for pre-harvest sprouting resistance in wheat (Triticum aestivum L.). BMC Plant Biol 14:340–352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cavanagh CR, Chao S, Wang S, Huang BE, Stephen S, Kiani S, Forrest K, Saintenac C, Brown-Guedira GL, Akhunova A, See D, Bai G, Pumphrey M, Tomar L, Wong D, Kong S, Reynolds M, da Silva ML, Bockelman H, Talbert L, Anderson JA, Dreisigacker S, Baenziger S, Carter A, Korzun V, Morrell PL, Dubcovsky J, Morell MK, Sorrells ME, Hayden MJ, Akhunov E (2013) Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proc Natl Acad Sci USA 110:8057–8062

    Article  PubMed  PubMed Central  Google Scholar 

  • Chang C, Feng JM, Si HQ, Yin B, Zhang HP, Ma CX (2010a) Validating a novel allele of viviparous-1 (Vp-1Bf) associated with high seed dormancy of Chinese wheat landrace, Wanxianbaimaizi. Mol Breed 25:517–525

    Article  CAS  Google Scholar 

  • Chang C, Zhang HP, Feng JM, Yin B, Si HQ, Ma CX (2010b) Identifying alleles of Viviparous-1B associated with pre-harvest sprouting in micro-core collections of Chinese wheat germplasm. Mol Breed 25:481–490

    Article  Google Scholar 

  • Chang C, Zhang HP, Zhao QX, Feng JM, Si HQ, Lu J, Ma CX (2011) Rich allelic variations of Viviparous-1A and their associations with seed dormancy/pre-harvest sprouting of common wheat. Euphytica 179:343–353

    Article  CAS  Google Scholar 

  • Chen CX, Cai SB, Bai GH (2008) A major QTL controlling seed dormancy and pre-harvest sprouting resistance on chromosome 4A in a Chinese wheat landrace. Mol Breeding 21:351–358

    Article  CAS  Google Scholar 

  • Chen YH, Carver BF, Wang SW, Zhang FQ, Yan LL (2009) Genetic loci associated with stem elongation and winter dormancy release in wheat. Theor Appl Genet 118:881–889

    Article  CAS  PubMed  Google Scholar 

  • Chen GF, Zhang H, Deng ZY, Wu RG, Li DM, Wang MY, Tian JC (2016) Genome-wide association study for kernel weight-related traits using SNPs in a Chinese winter wheat population. Euphytica 212:173–185

    Article  CAS  Google Scholar 

  • Derera NF, Bhatt GM (1980) Germination inhibition of the bracts in relation to pre-harvest sprouting tolerance in wheat. Cereal Res Commun 8:199–201

    Google Scholar 

  • Emebiri LC, Oliver JR, Mrva K, Mares D (2010) Association mapping of late maturity α-amylase (LMA) activity in a collection of synthetic hexaploid wheat. Mol Breed 26:39–49

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gao F, Ayele BT (2014) Functional genomics of seed dormancy in wheat: advances and prospects. Front Plant Sci 5:458–469

    PubMed  PubMed Central  Google Scholar 

  • Gatford KT, Heamden P, Ogbonnaya F (2002) Novel resistance to pre-harvest sprouting in Australian wheat from the wild relative Triticum tauschii. Euphytica 126:67–76

    Article  CAS  Google Scholar 

  • Griffiths S, Simmonds J, leverington M, Wang YK, Fish L, Sayers L, Alibert L, Orford S, Wingen L, Herry L, Faure S, Laurie D, Bilham L, Snape J, (2009) Meta-QTL analysis of the genetic control of ear emergence in elite European winter wheat germplasm. Theor Appl Genet 119:383–395

    Article  CAS  PubMed  Google Scholar 

  • Groos C, Gay G, Perretant RM, Bernard GM, Charmet DG (2002) Study of the relationship between pre-harvest sprouting and grain color by quantitative trait loci analysis in a white red grain bread-wheat cross. Theor Appl Genet 104:39–47

    Article  CAS  PubMed  Google Scholar 

  • Gupta PK, Kulwal PL, Jaiswal V (2014) Association mapping: opportunities and challenges. Adv Genet 85:109–148

    Article  CAS  PubMed  Google Scholar 

  • Hickey LT, Dieters MJ, DeLacy IH, Kravchuk OY, Mares DJ, Banks PM (2009) Grain dormancy in fixed lines of white-grained wheat (Triticum aestivum L.) grown under controlled environmental conditions. Euphytica 168:303–310

    Article  CAS  Google Scholar 

  • Himi E, Mares DJ, Yanagisawa A, Noda K (2002) Effect of grain colour gene (R) on grain dormancy and sensitivity of the embryo to abscisic acid (ABA) in wheat. J Exp Bot 53:1569–1574

    Article  CAS  PubMed  Google Scholar 

  • Himi E, Maekawa M, Miura H, Noda K (2011) Development of PCR markers for Tamyb10 related to R-1, red grain color gene in wheat. Theor Appl Genet 122:1561–1576

    Article  CAS  PubMed  Google Scholar 

  • International Wheat Genome Sequencing Consortium (IWGSC) (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:eaar7191

    Article  CAS  Google Scholar 

  • Jaiswal V, Mir RR, Mohan A, Balyan HS, Gupta PK (2012) Association mapping for pre-harvest sprouting tolerance in common wheat (Triticum aestivum L.). Euphytica 188:89–102

    Article  CAS  Google Scholar 

  • Jiang H, Zhao LX, Chen XJ, Cao JJ, Wu ZY, Liu K, Zhang C, Wei WX, Xie HY, Li L, Gan YG, Lu J, Chang C, Zhang HP, Xia XC, Xiao SH, Ma CX (2018) A novel 33-bp insertion in the promoter of TaMFT-3A is associated with pre-harvest sprouting resistance in common wheat. Mol Breed 38:69–83

    Article  CAS  Google Scholar 

  • King RW, Richards RA (1984) Water uptake and pre-harvest sprouting damage in wheat: ear characteristics. Aust J Agr Res 35:327–336

    Article  Google Scholar 

  • Kulwal PL, Singh R, Balyan HS, Gupta PK (2004) Genetic basis of pre-harvest sprouting tolerance using single-locus and two-locus QTL analyses in bread wheat. Funct Integr Genomics 4:94–101

    Article  CAS  PubMed  Google Scholar 

  • Kulwal PL, Kumar N, Gaur A, Khurana P, Khurana JP, Tyagi AK, Balyan HS, Gupta PK (2005) Mapping of a major QTL for pre-harvest sprouting tolerance on chromosome 3A in bread wheat. Theor Appl Genet 111:1052–1059

    Article  CAS  PubMed  Google Scholar 

  • Kulwal P, Ishikawa G, Benscher D, Feng ZY, Yu LX, Jadhav A, Mehetre S, Sorrells ME (2012) Association mapping for pre-harvest sprouting resistance in white winter wheat. Theor Appl Genet 125:793–805

    Article  CAS  PubMed  Google Scholar 

  • Kumar A, Kumar J, Singh R, Garg T, Chhuneja P, Balyan HS, Gupta PK (2009) QTL analysis for grain colour and pre-harvest sprouting in bread wheat. Plant Sci 177:114–122

    Article  CAS  Google Scholar 

  • Kumar S, Knox RE, Clarke FR, Pozniak CJ, DePauw RM, Cuthbert RD, Fox S (2015) Maximizing the identification of QTL for pre-harvest sprouting resistance using seed dormancy measures in a white-grained hexaploid wheat population. Euphytica 205:287–309

    Article  Google Scholar 

  • Li HH, Ye GY, Wang JK (2007) A modified algorithm for the improvement of composite interval mapping. Genetics 175:361–374

    Article  PubMed  PubMed Central  Google Scholar 

  • Lin M, Cai SH, Wang S, Liu SB, Zhang GR, Bai GH (2015) Genotyping-by-sequencing (GBS) identified SNP tightly linked to QTL for pre-harvest sprouting resistance. Theor Appl Genet 128:1385–1395

    Article  CAS  PubMed  Google Scholar 

  • Lin M, Zhang DD, Liu SB, Zhang GR, Yu JM, Fritz AK, Bai GH (2016) Genome-wide association analysis on pre-harvest sprouting resistance and grain color in U.S. winter wheat. BMC Genomics 17:794–810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu SB, Cai SB, Robert G, Chen CX, Bai GH (2008) Quantitative trait loci for resistance to pre-harvest sprouting in US hard white winter wheat Rio Blanco. Theor Appl Genet 117:691–699

    Article  CAS  PubMed  Google Scholar 

  • Liu SB, Bai GH, Cai SB, Chen CX (2011) Dissection of genetic components of preharvest sprouting resistance in white wheat. Mol Breed 27:511–523

    Article  Google Scholar 

  • Liu SB, Sehgal SK, Li JR, Lin M, Trick HN, Yu JM, Gill BS, Bai GH (2013) Cloning and characterization of a critical regulator for pre-harvest sprouting in wheat. Genetics 195:263–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu SB, Sehgal SK, Lin M, Li J, Trick H, Gill BS, Bai GH (2015) Independent mis-splicing mutations in TaPHS1 causing loss of pre-harvest sprouting (PHS) resistance during wheat domestication. New Phytol 208:936–948

    Article  CAS  PubMed  Google Scholar 

  • Liu JD, He ZH, Rasheed A, Wen W, Yan J, Zhang PZ, Wan YX, Zhang Y, Xie CJ, Xia XC (2017) Genome-wide association mapping of black point reaction in common wheat (Triticum aestivum L.). BMC Plant Biol 17:220–232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maccaferri M, Zhang JL, Bulli P, Abate Z, Chao S, Cantu D, Bossolini E, Chen XM, Pumphrey M, Dubcovsky J (2015) A genome-wide association study of resistance to stripe rust (Puccinia striiformis f. sp. tritici) in a worldwide collection of hexaploid spring wheat (Triticum aestivum L.). G3 5:449–465

    Article  PubMed  PubMed Central  Google Scholar 

  • Mares DJ, Mrva K (2014) Wheat grain preharvest sprouting and late maturity alpha-amylase. Planta 240:1167–1178

    Article  CAS  PubMed  Google Scholar 

  • Martinez SA, Godoy J, Huang M, Zhang ZW, Carter AH, Garland Campbell KA, Steber CM (2018) Genome-wide association mapping for tolerance to preharvest sprouting and low falling numbers in wheat. Front Plant Sci 9:141–157

    Article  PubMed  PubMed Central  Google Scholar 

  • Merk HL (2014) Estimating heritability and BLUPs for traits using tomato phenotypic data. Plant Breed Genomics. Available from: https://articles.extension.org/pages/61006/

  • Mohan A, Kulwal PL, Singh S, Kumar V, Mir RR, Kumar J, Prasad M, Balyan HS, Gupta PK (2009) Genome-wide QTL analysis for pre-harvest sprouting tolerance in bread wheat. Euphytica 168:319–329

    Article  CAS  Google Scholar 

  • Mori M, Uchino N, Chono M, Kato K, Miura H (2005) Mapping QTLs for grain dormancy on wheat chromosome 3A and group 4 chromosomes, and their combined effect. Theor Appl Genet 110:1315–1323

    Article  CAS  PubMed  Google Scholar 

  • Moser G, Lee SH, Hayes BJ, Goddard ME, Wray NR, Visscher PM (2015) Simultaneous discovery, estimation and prediction analysis of complex traits using a Bayesian mixture model. PLoS Genet 11:e1004969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munkvold JD, Tanaka J, Benscher D, Sorrells ME (2009) Mapping quantitative trait loci for preharvest sprouting resistance in white wheat. Theor Appl Genet 119:1223–1235

    Article  CAS  PubMed  Google Scholar 

  • Nakamura S, Abe F, Kawahigashi H, Nakazono K, Tagiri A, Matsumoto T, Utsugi S, Ogawa T, Handa H, Ishida H, Mori M, Kawaura K, Ogihara Y, Miura H (2011) A wheat homolog of MOTHER OF FT AND TFL1 acts in the regulation of germination. Plant Cell 23:3215–3229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ogbonnaya FC, Imtiaz M, Ye G, Hearnden PR, Hernandez E, Eastwood RF, Van Ginkel M, Shorter SC, Winchester JM (2008) Genetic and QTL analysis of seed dormancy and preharvest sprouting resistance in the wheat germplasm CN10955. Theor Appl Genet 116:891–902

    Article  CAS  PubMed  Google Scholar 

  • Osa M, Kato K, Mori M, Shindo C, Torada A, Miura H (2003) Mapping QTLs for seed dormancy and Vp1 homologue on chromosome 3A of wheat. Theor Appl Genet 106:1491–1496

    Article  CAS  PubMed  Google Scholar 

  • Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38:904–909

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rehman Arif MA, Neumann K, Nagel M, Kobiljski B, Lohwasser U, Börner A (2012) An association mapping analysis of dormancy and pre-harvest sprouting in wheat. Euphytica 188:409–417

    Article  CAS  Google Scholar 

  • Reif JC, Maurer HP, Korzun V, Ebmeyer E, Miedaner T, Wurschum T (2011) Mapping QTLs with main and epistatic effects underlying grain yield and heading time in soft winter wheat. Theor Appl Genet 123:283–292

    Article  PubMed  Google Scholar 

  • Ren WL, Wen YJ, Dunwell JM, Zhang YM (2018) pKWmEB: Integration of Kruskal-Wallis test with empirical Bayes under polygenic background control for multi-locus genome-wide association study. Heredity 120:208–218

    Article  CAS  PubMed  Google Scholar 

  • Saintenac C, Jiang D, Wang S, Akhunov E (2013) Sequence based mapping of the polyploid wheat genome. G3(3):1105–1114

    Google Scholar 

  • Segura V, Vilhjálmsson BJ, Platt A, Korte A, Seren Ü, Long Q, Nordborg M (2012) An efficient multi-locus mixed-model approach for genome-wide association studies in structured populations. Nat Genet 44:825–830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh R, Matus-Cádiz M, Båga M, Hucl P, Chibbar RN (2010) Identification of genomic regions associated with seed dormancy in white-grained wheat. Euphytica 174:391–408

    Article  CAS  Google Scholar 

  • Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109:1105–1114

    Article  CAS  PubMed  Google Scholar 

  • Somyong S, Ishikawa G, Munkvold JD, Tanaka J, Benscher D, Cho YG, Sorrells ME (2014) Fine mapping of a preharvest sprouting QTL interval on chromosome 2B in white wheat. Theor Appl Genet 127:1843–1855

    Article  PubMed  Google Scholar 

  • Song QJ, Shi JR, Singh S, Fickus EW, Costa JM, Lewis J, Gill BS, Ward R, Cregan PB (2005) Development and mapping of microsatellite (SSR) markers in wheat. Theor Appl Genet 110:550–560

    Article  CAS  PubMed  Google Scholar 

  • Sugimoto K, Takeuchi Y, Ebana K, Miyao A, Hirochika H, Hara N, Ishiyama K, Kobayashi M, Ban Y, Hattori T, Yano M (2010) Molecular cloning of Sdr4, a regulator involved in seed dormancy and domestication of rice. PNAS 107:5792–5797

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamba CL, Zhang YM (2018) A fast mrMLM algorithm for multi-locus genome-wide association studies. bioRxiv 341784

  • Tamba CL, Ni YL, Zhang YM (2017) Iterative sure independence screening EM-Bayesian LASSO algorithm for multi-locus genome-wide association studies. PLoS Comput Biol 13:e1005357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torada A, Ikeguchi S, Koike M (2005) Mapping and validation of PCR-based markers associated with a major QTL for seed dormancy in wheat. Euphytica 143:251–255

    Article  CAS  Google Scholar 

  • Torada A, Koike M, Ogawa T, Takenouchi Y, Tadamura K, Wu J, Matsumoto T, Kawaura K, Ogihara Y (2016) A causal gene for seed dormancy on wheat chromosome 4A encodes a MAP kinase kinase. Curr Biol 26:782–787

    Article  CAS  PubMed  Google Scholar 

  • Tyagi S, Gupta PK (2012) Meta-analysis of QTLs involved in pre-harvest sprouting tolerance and dormancy in bread wheat. TGG 3:9–24

    Google Scholar 

  • Wang SC, 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, Guedira GB, Korol A, Akhunova AR, Feuillet C, Salse J, Morgante M, Pozniak C, Luo MC, Dvorak J, Morell M, Dubcovsky J, Ganal M, Tuberosa R, Lawley C, Mikoulitch I, Cavanagh C, Edwards KJ, Hayden M, Akhunov E (2014a) Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array. Plant Biotechnol J 12:787–796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang SX, Zhu YL, Zhang HP, Chang C, Ma CX (2014b) Analysis of genetic diversity and relationship among wheat breeding parents by SSR markers. J Triticeae Crops 34:621–627 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Wang SB, Feng JY, Ren WL, Huang B, Zhou L, Wen YJ, Zhang J, Dunwell JM, Xu S, Zhang YM (2016) Improving power and accuracy of genome-wide association studies via a multi-locus mixed linear model methodology. Sci Rep-UK 6:19444

    Article  CAS  Google Scholar 

  • Wang SX, Zhu YL, Zhang DX, Shao H, Liu P, Hu JB, Zhang H, Zhang HP, Chang C, Lu J, Xia XC, Sun GL, Ma CX (2017) Genome-wide association study for grain yield and related traits in elite wheat varieties and advanced lines using SNP markers. PLoS ONE 12:e0188662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wen YJ, Zhang H, Ni YL, Huang B, Zhang J, Feng JY, Wang SB, Dunwell JM, Zhang YM, Wu R (2018) Methodological implementation of mixed linear models in multi-locus genome-wide association studies. Brief Bioinform 19:700–712

    Article  PubMed  Google Scholar 

  • Xiao SH, Zhang XY, Yan CS, Lin H (2002) Germplasm improvement for preharvest sprouting resistance in Chinese white-grained wheat: an overview of the current strategy. Euphytica 126:35–38

    Article  CAS  Google Scholar 

  • Yang Y, Zhao XL, Xia LQ, Chen XM, Xia XC, Yu Z, He ZH, Rŏder M (2007) Development and validation of a Viviparous-1 STS marker for pre-harvest sprouting tolerance in Chinese wheat. Theor Appl Genet 115:971–980

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Chen XM, He ZH, Röder M, Xia LQ (2009) Distribution of Vp-1 alleles in Chinese white-grained landraces, historical and current wheat cultivars. Cereal Res Commun 37:169–177

    Article  CAS  Google Scholar 

  • Yang Y, Zhang CL, Liu SX, Sun YQ, Meng JY, Xia LQ (2014) Characterization of the rich haplotypes of Viviparous-1A in Chinese wheats and development of a novel sequence-tagged site marker for pre-harvest sprouting resistance. Mol Breed 33:75–88

    Article  CAS  Google Scholar 

  • Zanke CD, Ling J, Plieske J, Kollers S, Ebmeyer E, Korzun V, Argillier O, Stiewe G, Hinze M, Beier S, Ganal MW, Röder MS (2014) Genetic architecture of main effect QTL for heading date in European winter wheat. Front Plant Sci 5:217–229

    Article  PubMed  PubMed Central  Google Scholar 

  • Zanke CD, Ling J, Plieske J, Kollers S, Ebmeyer E, Korzun V, Argillier O, Stiewe G, Hinze M, Neumann K, Ganal MW, Röder MS (2014b) Whole genome association mapping of plant height in winter wheat (Triticum aestivum L.). PLoS ONE 9:e113287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zanke CD, Ling J, Plieske J, Kollers S, Ebmeyer E, Korzun V, Argillier O, Stiewe G, Hinze M, Neumann F, Eichhorn A, Polley A, Jaenecke C, Ganal MW, Röder MS (2015) Analysis of main effect QTL for thousand grain weight in European winter wheat (Triticum aestivum L.) by genome-wide association mapping. Front Plant Sci 6:644–658

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang HP, Chang C, Xia GY, Zhang XY, Yan CS, Xiao SH, Si HQ, Lu J, Ma CX (2010) Identification of molecular markers associated with seed dormancy in micro-core collections of Chinese wheat and landraces. Acta Agron Sin 36:1649–1656 (in Chinese with English abstract)

    Article  CAS  Google Scholar 

  • Zhang YJ, Miao XL, Xia XC, He ZH (2014) Cloning of seed dormancy genes (TaSdr) associated with tolerance to pre-harvest sprouting in common wheat and development of a functional marker. Theor Appl Genet 127:855–866

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Feng JY, Ni YL, Wen YJ, Niu Y, Tamba CL, Yue C, Song QJ, Zhang YM (2017a) pLARmEB: Integration of least angle regression with empirical Bayes for multi-locus genome-wide association studies. Heredity 118:517–524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YJ, Xia XC, He ZH (2017b) The seed dormancy allele TaSdr-A1a associated with pre-harvest sprouting tolerance is mainly present in Chinese wheat landraces. Theor Appl Genet 130:81–89

    Article  PubMed  Google Scholar 

  • Zhang XF, Chen JH, Yan Y, Yan XF, Shi CN, Zhao L, Chen F (2018) Genome-wide association study of heading and fowering dates and construction of its prediction equation in Chinese common wheat. Theor Appl Genet 131:2271–2285

    Article  CAS  PubMed  Google Scholar 

  • Zhou X, Carbonetto P, Stephens M (2013) Polygenic modeling with Bayesian sparse linear mixed models. PLoS Genet 9:e1003264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou Y, Tang H, Cheng MP, Dankwa KO, Chen ZX, Li ZY, Gao S, Liu YX, Jiang QT, Lan XJ, Pu ZE, Wei YM, Zheng YL, Hickey LT, Wang JR (2017) Genome-wide association study for pre-harvest sprouting resistance in a large germplasm collection of Chinese wheat landraces. Front Plant Sci 8:401–414

    PubMed  PubMed Central  Google Scholar 

  • Zhu YL, Wang SX, Zhao LX, Zhang DX, Hu JB, Yang YJ, Chang C, Ma CX, Zhang HP (2014) Exploring molecular markers of preharvest sprouting resistance gene using wheat intact spikes by association analysis. Acta Agron Sin 40:1725–1732 (in Chinese with English abstract)

    Article  CAS  Google Scholar 

  • Zhu YL, Wang SX, Zhang HP, Zhao LX, Wu ZY, Jiang H, Cao JJ, Liu K, Qin M, Lu J, Sun GL, Xia XC, Chang C, Ma CX (2016) Identification of major loci for seed dormancy at different post-ripening stages after harvest and validation of a novel locus on chromosome 2AL in common wheat. Mol Breed 36:174–186

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (31871608, 31401372), The National Key Research and Development Plan “Breeding new wheat varieties with high-yielding, high-quality and water-saving in the south of Huang-Huai River winter wheat area”—the breeding of new wheat germplasm and varieties with resistance to adversity (2017YFD0100703), the China Agriculture Research System (CARS-03), the Natural Science Foundation of Anhui Province (1508085MC57), the Wheat genetics and breeding research platform innovation team of Anhui's University (2015-), Jiangsu Collaborative Innovation Center for Modern Crop Production (JCIC-MCP), and the Agriculture Research System of Anhui Province (AHCYTX-02). We thank Robert McKenzie, PhD, from Liwen Bianji, Edanz Group China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Haiping Zhang or Cheng Chang.

Ethics declarations

Conflict of interest

We declare no conflicts of interest in regard to this manuscript.

Ethical standards

The experiments conducted in this study comply with the current laws of China.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 2412 kb)

Supplementary file2 (XLSX 103 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhu, Y., Wang, S., Wei, W. et al. Genome-wide association study of pre-harvest sprouting tolerance using a 90K SNP array in common wheat (Triticum aestivum L.). Theor Appl Genet 132, 2947–2963 (2019). https://doi.org/10.1007/s00122-019-03398-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-019-03398-x

Navigation