, Volume 191, Issue 1, pp 23–33 | Cite as

Fine mapping of a major flowering time QTL on soybean chromosome 6 combining linkage and association analysis

  • Dan Zhang
  • Hao Cheng
  • Zhenbin Hu
  • Hui Wang
  • Guizheng Kan
  • Chunying Liu
  • Deyue YuEmail author


Flowering time is a key trait in the plant life cycle and an important selection criterion for soybean. Here, we combine the advantages of genome-wide association and linkage mapping to identify and fine map quantitative trait loci (QTLs) associated with flowering time. Linkage mapping was performed using 152 recombinant inbred lines and a major QTL, qFT6, affecting flowering time was found on chromosome 6. To refine the qFT6, the 192 natural accessions were genotyped using eight new simple sequence repeats and 10 single nucleotide polymorphisms markers covering the qFT6 region Haplotype analysis showed that the haplotype between markers BARC-014947-01929 and Satt365 could explain more phenotypic variation (26.5 %) than any other combination of markers. These results suggested that the target flowering time gene was located in ~300 kb between BARC-014947-01929 and Satt365, including three predicted genes. High-resolution map in qFT6 region will be useful not only for marker-assisted selection of flowering time but also for further positional cloning of the target gene. These results indicate that combining association and linkage mapping provides an efficient approach for fine mapping of soybean genes.


Fine mapping Flowering time Association mapping Linkage mapping Soybean 



We thank Mr. Wang Wen Liang at Henan Agricultural University for assistance in investigating flowering time and performing the field experiments. Dr Zhiwu Zhang from Cornell University is thanked for his critical reading of this manuscript. This work was supported by National Basic Research Program of China (973 Program) (2010CB125906, 2009CB118400); National Natural Science Foundation of China (31000718, 31171573, 31201230), and Jiangsu Provincial Programs (BE2012328, BK2012768).

Supplementary material

10681_2012_840_MOESM1_ESM.docx (654 kb)
Supplementary material 1 (DOCX 654 kb)


  1. Andersson L (2001) Genetic dissection of phenotypic diversity in farm animals. Nat Rev Genet 2:130–137PubMedCrossRefGoogle Scholar
  2. Brachi B, Faure N, Horton M, Flahauw E, Vazquez A, Nordborg M, Bergelson J, Cuguen J, Roux F (2010) Linkage and association mapping of Arabidopsis thaliana flowering time in nature. PLoS Genet 6:e1000940PubMedCrossRefGoogle Scholar
  3. 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 23:2633–2635PubMedCrossRefGoogle Scholar
  4. Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1172PubMedCrossRefGoogle Scholar
  5. Cheng L, Wang Y, Zhang C, Wu C, Xu J, Zhu H, Leng J, Bai Y, Guan R, Hou W, Zhang L, Han T (2011) Genetic analysis and QTL detection of reproductive period and post-flowering photoperiod responses in soybean. Theor Appl Genet 123:421–429PubMedCrossRefGoogle Scholar
  6. Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971Google Scholar
  7. Cohen-Zinder M, Seroussi E, Larkin DM, Loor JJ, Everts-van der Wind A, Lee JH, Drackley JK, Band MR, Hernandez A, Shani M (2005) Identification of a missense mutation in the bovine ABCG2 gene with a major effect on the QTL on chromosome 6 affecting milk yield and composition in Holstein cattle. Genome Res 15:936–944PubMedCrossRefGoogle Scholar
  8. Curtis D, Luzzi J, BM Hume D (2000) Agronomic and phenological differences of soybean isolines differing in maturity and growth habit. Crop Sci 40:1624–1629CrossRefGoogle Scholar
  9. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  10. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578PubMedCrossRefGoogle Scholar
  11. Fehr W, Caviness C, Burmood D, Pennington J (1971) Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Sci 11:929–931CrossRefGoogle Scholar
  12. Goddard M (2005) The use of association to map quantitative trait loci. Aust J Exp Agr 45:837–845CrossRefGoogle Scholar
  13. Hanson W (1985) Association of seed yield with partitioned lengths of the reproductive period in soybean genotypes. Crop Sci 25:525–529CrossRefGoogle Scholar
  14. Hao D, Cheng H, Yin Z, Cui S, Zhang D, Wang H, Yu D (2012) Identification of single nucleotide polymorphisms and haplotypes associated with yield and yield components in soybean (Glycine max) landraces across multiple environments. Theor Appl Genet 124:447–458PubMedCrossRefGoogle Scholar
  15. Higginson T, Li SF, Parish RW (2003) AtMYB103 regulates tapetum and trichome development in Arabidopsis thaliana. Plant J 35:177–192PubMedCrossRefGoogle Scholar
  16. Hu GL, Zhang DL, Pan HQ, Li B, Wu JT, Zhou XY, Zhang QY, Zhou L, Yao GX, Li JZ (2011) Fine mapping of the awn gene on chromosome 4 in rice by association and linkage analyses. Chinese Sci Bull 56:835–839CrossRefGoogle Scholar
  17. Jun TH, Van K, Kim MY, Lee SH, Walker DR (2008) Association analysis using SSR markers to find QTL for seed protein content in soybean. Euphytica 162:179–191CrossRefGoogle Scholar
  18. Kantolic AG, Slafer GA (2007) Development and seed number in indeterminate soybean as affected by timing and duration of exposure to long photoperiods after flowering. Ann Bot 99:925–933PubMedCrossRefGoogle Scholar
  19. Keim P, Diers B, Olson T, Shoemaker R (1990) RFLP mapping in soybean: association between marker loci and variation in quantitative traits. Genetics 126:735–742PubMedGoogle Scholar
  20. Klein J, Saedler H, Huijser P (1996) A new family of DNA binding proteins includes putative transcriptional regulators of the Antirrhinum majus floral meristem identity gene SQUAMOSA. Mol Gen Genet 250:7–16PubMedGoogle Scholar
  21. Li J, Yang X, Wang Y, Li X, Gao Z, Pei M, Chen Z, Qu LJ, Gu H (2006) Two groups of MYB transcription factors share a motif which enhances trans-activation activity. Biochem Bioph Res Co 341:1155–1163CrossRefGoogle Scholar
  22. Li L, Li H, Li Q, Yang X, Zheng D, Warburton M, Chai Y, Zhang P, Guo Y, Yan J (2011) An 11-bp Insertion in Zea mays fatb reduces the palmitic acid content of fatty acids in maize grain. PLoS ONE 6:e24699PubMedCrossRefGoogle Scholar
  23. Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129PubMedCrossRefGoogle Scholar
  24. Liu P, Vikis H, Lu Y, Wang D, You M (2007) Large-scale in silico mapping of complex quantitative traits in inbred mice. PLoS ONE 2:e651PubMedCrossRefGoogle Scholar
  25. Liu B, Kanazawa A, Matsumura H, Takahashi R, Harada K, Abe J (2008) Genetic redundancy in soybean photoresponses associated with duplication of the phytochrome A gene. Genetics 180:995–1007PubMedCrossRefGoogle Scholar
  26. Lu Y, Zhang S, Shah T, Xie C, Hao Z, Li X, Farkhari M, Ribaut JM, Cao M, Rong T (2010) Joint linkage-association mapping is a powerful approach to detecting quantitative trait loci underlying drought tolerance in maize. P Natl Acad Sci 107:19585–19590CrossRefGoogle Scholar
  27. Manenti G, Galvan A, Pettinicchio A, Trincucci G, Spada E, Zolin A, Milani S, Gonzalez-Neira A, Dragani TA (2009) Mouse genome-wide association mapping needs linkage analysis to avoid false-positive loci. PLoS Genet 5:e1000331PubMedCrossRefGoogle Scholar
  28. Mansur L, Lark K, Kross H, Oliveira A (1993) Interval mapping of quantitative trait loci for reproductive, morphological, and seed traits of soybean [Glycine max (L.) Merr.]. Theor Appl Genet 86:907–913Google Scholar
  29. Mansur L, Orf J, Chase K, Jarvik T, Cregan P, Lark K (1996) Genetic mapping of agronomic traits using recombinant inbred lines of soybean. Crop Sci 36:1327–1336CrossRefGoogle Scholar
  30. Meuwissen THE, Karlsen A, Lien S, Olsaker I, Goddard ME (2002) Fine mapping of a quantitative trait locus for twinning rate using combined linkage and association mapping. Genetics 161:373–379PubMedGoogle Scholar
  31. Molnar SJ, Rai S, Charette M, Cober ER (2003) Simple sequence repeat (SSR) markers linked to E1, E3, E4, and E7 maturity genes in soybean. Genome 46:1024–1036PubMedCrossRefGoogle Scholar
  32. Nemri A, Atwell S, Tarone AM, Huang YS, Zhao K, Studholme DJ, Nordborg M, Jones JDG (2010) Genome-wide survey of Arabidopsis natural variation in downy mildew resistance using combined association and linkage mapping. Proc Natl Acad Sci 107:10302–10307PubMedCrossRefGoogle Scholar
  33. Olsen HG, Lien S, Gautier M, Nilsen H, Roseth A, Berg PR, Sundsaasen KK, Svendsen M, Meuwissen THE (2005) Mapping of a milk production quantitative trait locus to a 420-kb region on bovine chromosome 6. Genetics 169:275–283PubMedCrossRefGoogle Scholar
  34. Orf J, Chase K, Jarvik T, Mansur L, Cregan P, Adler F, Lark K (1999) Genetics of soybean agronomic traits: comparison of three related recombinant inbred populations. Crop Sci 39:1642–1651CrossRefGoogle Scholar
  35. Pelucchi N, Fornara F, Favalli C, Masiero S, Lago C, Pe EM, Colombo L, Kater MM (2002) Comparative analysis of rice MADS-box genes expressed during flower development. Sex Plant Reprod 15:113–122CrossRefGoogle Scholar
  36. Preston J, Wheeler J, Heazlewood J, Li SF, Parish RW (2004) AtMYB32 is required for normal pollen development in Arabidopsis thaliana. Plant J 40:979–995PubMedCrossRefGoogle Scholar
  37. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183PubMedCrossRefGoogle Scholar
  38. Shore P, Sharrocks AD (1995) The MADS-box family of transcription factors. Eur J Biochem 229:1–13PubMedCrossRefGoogle Scholar
  39. Stracke S, Presterl T, Stein N, Perovic D, Ordon F, Graner A (2007) Effects of introgression and recombination on haplotype structure and linkage disequilibrium surrounding a locus encoding Bymovirus resistance in barley. Genetics 175:805–817PubMedCrossRefGoogle Scholar
  40. Su CF, Lu WG, Zhao TJ, Gai JY (2010) Verification and fine-mapping of QTLs conferring days to flowering in soybean using residual heterozygous lines. Chinese Sci Bull 55:499–508CrossRefGoogle Scholar
  41. Tasma I, Lorenzen L, Green D, Shoemaker R (2001) Mapping genetic loci for flowering time, maturity, and photoperiod insensitivity in soybean. Mol Breeding 8:25–35CrossRefGoogle Scholar
  42. Tuinstra M, Ejeta G, Goldsbrough P (1997) Heterogeneous inbred family (HIF) analysis: a method for developing near-isogenic lines that differ at quantitative trait loci. Theor Appl Genet 95:1005–1011CrossRefGoogle Scholar
  43. Wang Y (2001) Establishment and adjustment of RIL population and its application to map construction, mapping genes resistant to SMV and QTL analysis of agronomic and quality traits in soybeans. Nanjing Agricultural University, Doctor DissertationGoogle Scholar
  44. Wang S, Basten C, Zeng Z (2005) Windows QTL cartographer version 2.5. Statistical genetics. North Carolina State University, RaleighGoogle Scholar
  45. Watanabe S, Hideshima R, Xia Z, Tsubokura Y, Sato S, Nakamoto Y, Yamanaka N, Takahashi R, Ishimoto M, Anai T (2009) Map-based cloning of the gene associated with the soybean maturity locus E3. Genetics 182:1251–1262PubMedCrossRefGoogle Scholar
  46. Yamaguchi A, Wu MF, Yang L, Wu G, Poethig RS, Wagner D (2009) The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell 17:268–278PubMedCrossRefGoogle Scholar
  47. Yamanaka N, Ninomiya S, Hoshi M, Tsubokura Y, Yano M, Nagamura Y, Sasaki T, Harada K (2001) An informative linkage map of soybean reveals QTLs for flowering time, leaflet morphology and regions of segregation distortion. DNA Res 8:61–72PubMedCrossRefGoogle Scholar
  48. Yamanaka N, Watanabe S, Toda K, Hayashi M, Fuchigami H, Takahashi R, Harada K (2005) Fine mapping of the FT1 locus for soybean flowering time using a residual heterozygous line derived from a recombinant inbred line. Theor Appl Genet 110:634–639PubMedCrossRefGoogle Scholar
  49. Yang Z, Wang X, Gu S, Hu Z, Xu H, Xu C (2008) Comparative study of SBP-box gene family in Arabidopsis and rice. Gene 407:1–11PubMedCrossRefGoogle Scholar
  50. Yu J, Pressoir G, Briggs W, Bi I, Yamasaki M, Doebley J, McMullen M, Gaut B, Nielsen D, Holland J (2005) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208PubMedCrossRefGoogle Scholar
  51. Zhang WK, Wang YJ, Luo GZ, Zhang JS, He CY, Wu XL, Gai JY, Chen SY (2004) QTL mapping of ten agronomic traits on the soybean [Glycine max (L.) Merr.] genetic map and their association with EST markers. Theor Appl Genet 108:1131–1139PubMedCrossRefGoogle Scholar
  52. Zhang D, Cheng H, Geng L, Kan G, Cui S, Meng Q, Gai J, Yu D (2009) Detection of quantitative trait loci for phosphorus deficiency tolerance at soybean seedling stage. Euphytica 167:313–322CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Dan Zhang
    • 1
    • 2
  • Hao Cheng
    • 1
  • Zhenbin Hu
    • 1
  • Hui Wang
    • 1
  • Guizheng Kan
    • 1
  • Chunying Liu
    • 1
  • Deyue Yu
    • 1
    Email author
  1. 1.National Key Laboratory of Crop Genetics and Germplasm EnhancementNational Center for Soybean Improvement, Nanjing Agricultural UniversityNanjingChina
  2. 2.Department of AgronomyHenan Agricultural UniversityZhengzhouChina

Personalised recommendations