Theoretical and Applied Genetics

, Volume 131, Issue 3, pp 513–524 | Cite as

Mapping and confirmation of loci for salt tolerance in a novel soybean germplasm, Fiskeby III

  • Tuyen D. Do
  • Tri D. Vuong
  • David Dunn
  • Scotty Smothers
  • Gunvant Patil
  • Dennis C. Yungbluth
  • Pengyin Chen
  • Andrew Scaboo
  • Dong Xu
  • Thomas E. Carter
  • Henry T. Nguyen
  • J. Grover Shannon
Original Article


Key message

The confirmation of a major locus associated with salt tolerance and mapping of a new locus, which could be beneficial for improving salt tolerance in soybean.


Breeding soybean for tolerance to high salt conditions is important in some regions of the USA and world. Soybean cultivar Fiskeby III (PI 438471) in maturity group 000 has been reported to be highly tolerant to multiple abiotic stress conditions, including salinity. In this study, a mapping population of 132 F2 families derived from a cross of cultivar Williams 82 (PI 518671, moderately salt sensitive) and Fiskeby III (salt tolerant) was analyzed to map salt tolerance genes. The evaluation for salt tolerance was performed by analyzing leaf scorch score (LSS), chlorophyll content ratio (CCR), leaf sodium content (LSC), and leaf chloride content (LCC) after treatment with 120 mM NaCl under greenhouse conditions. Genotypic data for the F2 population were obtained using the SoySNP6K Illumina Infinium BeadChip assay. A major allele from Fiskeby III was significantly associated with LSS, CCR, LSC, and LCC on chromosome (Chr.) 03 with LOD scores of 19.1, 11.0, 7.7 and 25.6, respectively. In addition, a second locus associated with salt tolerance for LSC was detected and mapped on Chr. 13 with an LOD score of 4.6 and an R 2 of 0.115. Three gene-based polymorphic molecular markers (Salt-20, Salt14056 and Salt11655) on Chr.03 showed a strong predictive association with phenotypic salt tolerance in the present mapping population. These molecular markers will be useful for marker-assisted selection to improve salt tolerance in soybean.



This research was supported in part by the Missouri Soybean Merchandising Council and the Missouri Agricultural Experiment Station. Mr. Tuyen Do would like to thank Cuu Long Delta Rice Research Institute and the Vietnam Ministry of Agriculture for a graduate student scholarship.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

122_2017_3015_MOESM1_ESM.docx (279 kb)
Supplementary Figure S1: A genetic linkage map was constructed in an F2 population derived from a cross of Williams 82 and Fiskeby III (DOCX 279 kb)
122_2017_3015_MOESM2_ESM.docx (574 kb)
Supplementary Figure S2: Physical positions of the most significant markers associated with salt tolerance, Gm13_38988256 (ss715616164), Gm13_39054715 (ss715616173) and Gm13_3965528 (ss715616176) and three candidate genes (Glyma.13g305700, Glyma.13g305800 and Glyma.13g305900) ( with salt stress response function in the physical map of Chr. 13 (DOCX 573 kb)
122_2017_3015_MOESM3_ESM.docx (15 kb)
Supplementary material 3 (DOCX 14 kb)


  1. Abel GH (1969) Inheritance of the capacity for chloride inclusion and chloride exclusion by soybeans. Crop Sci 9:697–698CrossRefGoogle Scholar
  2. Abel GH, MacKenzie AJ (1964) Salt tolerance of soybean varieties (Glycine max L. Merill) during germination and later growth. Crop Sci 4:157–161CrossRefGoogle Scholar
  3. Akond M, Liu S, Schoener L, Anderson JA, Kantartzi SK, Meksem K, Song Q, Wang D, Wen Z, Lightfoot DA, Kassem MA (2013) A SNP-based genetic linkage map of soybean using the SoySNP6K Illumina Infinium BeadChip genotyping array. J Plant Genome Sci 1:80–89Google Scholar
  4. Bargsten JW, Nap JP, Sanchez-Perez GF, van Dijk AD (2014) Prioritization of candidate genes in QTL regions based on associations between traits and biological processes. BMC Plant Biol 14:330CrossRefPubMedPubMedCentralGoogle Scholar
  5. Batlle-Sales J (2011) Salinization: an environmental concern under climate change scenarios. In: Thomas RP (ed) Proceedings of the global forum on salinization and climate change (GFSCC2010), Valencia, 25–29 October 2010. FAO, Rome, p 10Google Scholar
  6. Blanco FF, Folegatti MV, Gheyi HR, Fernandes PD (2007) Emergence and growth of corn and soybean under saline stress. Sci Agric 64:451–459CrossRefGoogle Scholar
  7. Bonilla P, Dvorak J, Mackill D, Deal K, Gregorio G (2002) RFLP and SSLP mapping of salinity tolerance genes in chromosome 1 of rice (Oryza sativa L.) using recombinant inbred lines. Philipp Agric Sci 85:68–76Google Scholar
  8. Burton AL, Burkey KO, Carter TE Jr, Orf J, Cregan PB (2016) Phenotypic variation and identification of quantitative trait loci for ozone tolerance in a Fiskeby III × Mandarin (Ottawa) soybean population. Theor Appl Genet 129:1113–1125CrossRefPubMedGoogle Scholar
  9. Chen HT, Cui SY, Fu SX, Gai JY, Yu DY (2008) Identification of quantitative trait loci associated with salt tolerance during seedling growth in soybean (Glycine max L.). Aust J Agric Res 59:1086–1091CrossRefGoogle Scholar
  10. Chin JH, Lu X, Haefele SM, Gamuyao R, Ismail A, Wissuwa M, Heuer S (2010) Development and application of gene-based markers for the major rice QTL Phosphorus uptake 1. Theor Appl Genet 120:1073–1086CrossRefPubMedGoogle Scholar
  11. Delgado MJ, Ligero F, Lluch C (1994) Effects of salt stress on srowth and sitrogen–sixation by pea, faba-bean, common bean and soybean plants. Soil Biol Biochem 26:371–376CrossRefGoogle Scholar
  12. Do TD, Chen H, Hien VT, Hamwieh A, Yamada T, Sato T, Yan Y, Cong H, Shono M, Suenaga K, Xu D (2016) Ncl synchronously regulates Na(+), K(+), and Cl(−) in soybean and greatly increases the grain yield in saline field conditions. Sci Rep 6:19147CrossRefPubMedPubMedCentralGoogle Scholar
  13. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  14. El-Sabagh A, Sorour S, Ueda A, Saneoka H, Barutcular C (2015) Evaluation of salinity stress effects on seed yield and quality of three soybean cultivars. Azarian J Agric 2:138–141Google Scholar
  15. Elsheikh EAE, Wood M (1995) Nodulation and N-2 fixation by soybean inoculated with salt-tolerant Rhizobia or salt-sensitive Bradyrhizobia in saline soil. Soil Biol Biochem 27:657–661CrossRefGoogle Scholar
  16. FAO, ITPS (2015) Status of the world’s soil resources (SWSR)—main report. Food and Agriculture Organization of the United Nations and Intergovernmental Technical Panel on Soils, Rome, Italy, pp 124–127Google Scholar
  17. Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Sci 11:929–931CrossRefGoogle Scholar
  18. Galeano CH, Cortes AJ, Fernandez AC, Soler A, Franco-Herrera N, Makunde G, Vanderleyden J, Blair MW (2012) Gene-based single nucleotide polymorphism markers for genetic and association mapping in common bean. BMC Genet 13:48CrossRefPubMedPubMedCentralGoogle Scholar
  19. Genc Y, Oldach K, Verbyla AP, Lott G, Hassan M, Tester M, Wallwork H, McDonald GK (2010) Sodium exclusion QTL associated with improved seedling growth in bread wheat under salinity stress. Theor Appl Genet 121:877–894CrossRefPubMedGoogle Scholar
  20. Ghassemi-Golezani K, Taifeh-Noori M, Oustan S, Moghaddam M, Rahmani SS (2011) Physiological performance of soybean cultivars under salinity stress. J Plant Physiol Breed 1:1–8Google Scholar
  21. Guan RX, Qu Y, Guo Y, Yu LL, Liu Y, Jiang JH, Chen JG, Ren YL, Liu GY, Tian L, Jin LG, Liu ZX, Hong HL, Chang RZ, Gilliham M, Qiu LJ (2014) Salinity tolerance in soybean is modulated by natural variation in GmSALT3. Plant J 80:937–950CrossRefPubMedGoogle Scholar
  22. Gutierrez-Gonzalez JJ, Vuong TD, Zhong R, Yu O, Lee JD, Shannon G, Ellersieck M, Nguyen HT, Sleper DA (2011) Major locus and other novel additive and epistatic loci involved in modulation of isoflavone concentration in soybean seeds. Theor Appl Genet 123:1375–1385CrossRefPubMedGoogle Scholar
  23. Ha BK, Vuong TD, Velusamy V, Nguyen HT, Shannon JG, Lee JD (2013) Genetic mapping of quantitative trait loci conditioning salt tolerance in wild soybean (Glycine soja) PI 483463. Euphytica 193:79–88CrossRefGoogle Scholar
  24. Hamwieh A, Xu DH (2008) Conserved salt tolerance quantitative trait locus (QTL) in wild and cultivated soybeans. Breed Sci 58:355–359CrossRefGoogle Scholar
  25. Hamwieh A, Tuyen DD, Cong H, Benitez ER, Takahashi R, Xu DH (2011) Identification and validation of a major QTL for salt tolerance in soybean. Euphytica 179:451–459CrossRefGoogle Scholar
  26. Hossain H, Rahman MA, Alam MS, Singh RK (2015) Mapping of quantitative trait loci associated with reproductive-stage salt tolerance in rice. J Agron Crop Sci 201:17–31CrossRefGoogle Scholar
  27. Hu H, Wang L, Wang Q, Jiao L, Hua W, Zhou Q, Huang X (2014) Photosynthesis, chlorophyll fluorescence characteristics, and chlorophyll content of soybean seedlings under combined stress of bisphenol A and cadmium. Environ Toxicol Chem 33:2455–2462CrossRefPubMedGoogle Scholar
  28. Kan G, Zhang W, Yang W, Ma D, Zhang D, Hao D, Hu Z, Yu D (2015) Association mapping of soybean seed germination under salt stress. Mol Genet Genomics 290:2147–2162CrossRefPubMedGoogle Scholar
  29. Koyama ML, Levesley A, Koebner RM, Flowers TJ, Yeo AR (2001) Quantitative trait loci for component physiological traits determining salt tolerance in rice. Plant Physiol 125:406–422CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kumar Tewari A, Charan Tripathy B (1998) Temperature-stress-induced impairment of chlorophyll biosynthetic reactions in cucumber and wheat. Plant Physiol 117:851–858CrossRefPubMedPubMedCentralGoogle Scholar
  31. Lee GJ, Carter TE Jr, Villagarcia MR, Li Z, Zhou X, Gibbs MO, Boerma HR (2004) A major QTL conditioning salt tolerance in S-100 soybean and descendent cultivars. Theor Appl Genet 109:1610–1619CrossRefPubMedGoogle Scholar
  32. Lee JD, Smothers SL, Dunn D, Villagarcia M, Shumway CR, Carter TE, Shannon JG (2008) Evaluation of a simple method to screen soybean genotypes for salt tolerance. Crop Sci 48:2194–2200CrossRefGoogle Scholar
  33. Lee J-D, Shannon JG, Vuong TD, Nguyen HT (2009) Inheritance of salt tolerance in wild Soybean (Glycine soja Sieb. and Zucc.) Accession PI483463. J Hered 100(6):798–801CrossRefPubMedGoogle Scholar
  34. Lenis JM, Ellersieck M, Blevins DG, Sleper DA, Nguyen HT, Dunn D, Lee JD, Shannon JG (2011) Differences in ion accumulation and salt tolerance among Glycine accessions. J Agron Crop Sci 197:302–310CrossRefGoogle Scholar
  35. Li B, Tian L, Zhang J, Huang L, Han F, Yan S, Wang L, Zheng H, Sun J (2014) Construction of a high-density genetic map based on large-scale markers developed by specific length amplified fragment sequencing (SLAF-seq) and its application to QTL analysis for isoflavone content in Glycine max. BMC Genomics 15:1086CrossRefPubMedPubMedCentralGoogle Scholar
  36. Lin HX, Zhu MZ, Yano M, Gao JP, Liang ZW, Su WA, Hu XH, Ren ZH, Chao DY (2004) QTLs for Na+ and K+ uptake of the shoots and roots controlling rice salt tolerance. Theor Appl Genet 108:253–260CrossRefPubMedGoogle Scholar
  37. Lindsay MP, Lagudah ES, Hare RA, Munns R (2004) A locus for sodium exclusion (Nax1), a trait for salt tolerance, mapped in durum wheat. Funct Plant Biol 31:1105–1114CrossRefGoogle Scholar
  38. Liu Y, Yu L, Qu Y, Chen J, Liu X, Hong H, Liu Z, Chang R, Gilliham M, Qiu L, Guan R (2016) GmSALT3, which confers improved soybean salt tolerance in the field, increases leaf Cl exclusion prior to Na+ exclusion but does not improve early vigor under salinity. Front Plant Sci 7:1485PubMedPubMedCentralGoogle Scholar
  39. Nguyen VL, Ribot SA, Dolstra O, Niks RE, Visser RGF, van der Linden CG (2013) Identification of quantitative trait loci for ion homeostasis and salt tolerance in barley (Hordeum vulgare L.). Mol Breed 31:137–152CrossRefGoogle Scholar
  40. Pathan MS, Lee J-D, Shannon JG, Nguyen HT (2007) Recent advances in breeding for drought and salt stress tolerance in soybean. In: Jenks MA, Hasegawa PM, Jain SM (eds) Advances in molecular breeding toward drought and salt tolerant crops. Springer, Dordrecht, pp 739–773CrossRefGoogle Scholar
  41. Patil G, Do T, Vuong TD, Valliyodan B, Lee JD, Chaudhary J, Shannon JG, Nguyen HT (2016) Genomic-assisted haplotype analysis and the development of high-throughput SNP markers for salinity tolerance in soybean. Sci Rep 6:19199CrossRefPubMedPubMedCentralGoogle Scholar
  42. Phang TH, Shao G, Lam HM (2008) Salt tolerance in soybean. J Integr Plant Biol 50:1196–1212CrossRefPubMedGoogle Scholar
  43. Qadir M, Quillerou E, Nangia V, Murtaza G, Singh M, Thomas RJ, Drechsel P, Noble AD (2014) Economics of salt-induced land degradation and restoration. Nat Resour Forum 38:282–295CrossRefGoogle Scholar
  44. Qi X, Li MW, Xie M, Liu X, Ni M, Shao G, Song C, Kay-Yuen Yim A, Tao Y, Wong FL, Isobe S, Wong CF, Wong KS, Xu C, Li C, Wang Y, Guan R, Sun F, Fan G, Xiao Z, Zhou F, Phang TH, Liu X, Tong SW, Chan TF, Yiu SM, Tabata S, Wang J, Xu X, Lam HM (2014) Identification of a novel salt tolerance gene in wild soybean by whole-genome sequencing. Nat Commun 5:4340PubMedPubMedCentralGoogle Scholar
  45. Qiu XJ, Yuan ZH, Liu H, Xiang XJ, Yang LW, He WJ, Du B, Ye GY, Xu JL, Xing DY (2015) Identification of salt tolerance-improving quantitative trait loci alleles from a salt-susceptible rice breeding line by introgression breeding. Plant Breed 134:653–660CrossRefGoogle Scholar
  46. Rabie RK, Kumazawa K (1988) Effect of salt stress on nitrogen nutrition and yield quality of nodulated soybeans. Soil Sci Plant Nutr 34:385–391CrossRefGoogle Scholar
  47. Reinprecht Y, Pauls KP (2016) Microsomal omega-3 fatty acid desaturase genes in low linolenic acid soybean line RG10 and validation of major linolenic acid QTL. Front Genet 7:38CrossRefPubMedPubMedCentralGoogle Scholar
  48. Resurreccion AP, Makino A, Bennett J, Mae T (2002) Effect of light intensity on the growth and photosynthesis of rice under different sulfur concentrations. Soil Sci Plant Nutr 48:71–77CrossRefGoogle Scholar
  49. Shi Z, Bachleda N, Pham AT, Bilyeu K, Shannon G, Nguyen H, Li ZL (2015) High-throughput and functional SNP detection assays for oleic and linolenic acids in soybean. Mol Breed 35:175–186CrossRefGoogle Scholar
  50. Singleton PW, Bohlool BB (1984) Effect of salinity on nodule formation by soybean. Plant Physiol 74:72–76CrossRefPubMedPubMedCentralGoogle Scholar
  51. Song Q, Hyten DL, Jia G, Quigley CV, Fickus EW, Nelson RL, Cregan PB (2013) Development and evaluation of SoySNP50K, a high-density genotyping array for soybean. PLoS One 8:e54985CrossRefPubMedPubMedCentralGoogle Scholar
  52. Squires VR, Glenn EP (2011) Salination, desertification and soil erosion. In: Squires VR (ed) The role of food, agriculture, forestry and fisheries in human nutrition, vol 3. Encyclopedia of Life Support Systems (EOLSS), Australia, pp 102–123Google Scholar
  53. Tuyen DD, Lal SK, Xu DH (2010) Identification of a major QTL allele from wild soybean (Glycine soja Sieb. & Zucc.) for increasing alkaline salt tolerance in soybean. Theor Appl Genet 121:229–236CrossRefPubMedGoogle Scholar
  54. Tuyen DD, Zhang HM, Xu DH (2013) Validation and high-resolution mapping of a major quantitative trait locus for alkaline salt tolerance in soybean using residual heterozygous line. Mol Breed 31:79–86CrossRefGoogle Scholar
  55. USDA (2011) Breeding plants for a high-ozone world. Agric Res 59:14–17Google Scholar
  56. Valliyodan B, Dan Q, Patil G, Zeng P, Huang J, Dai L, Chen C, Li Y, Joshi T, Song L, Vuong TD, Musket TA, Xu D, Shannon JG, Shifeng C, Liu X, Nguyen HT (2016) Landscape of genomic diversity and trait discovery in soybean. Sci Rep 6:23598CrossRefPubMedPubMedCentralGoogle Scholar
  57. van Ooijen (2004) MapQTL®5, Software for the mapping of quantitative trait loci in experimental populations. Kyazma BV, WageningenGoogle Scholar
  58. van Ooijen (2006) JoinMap®4, Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, WageningenGoogle Scholar
  59. Várallyay G (2010) The impact of climate change on soils and on their water management. Agron Res 11:385–396Google Scholar
  60. Wang D, Shannon MC (1999) Emergence and seedling growth of soybean cultivars and maturity groups under salinity. Plant Soil 214:117–124CrossRefGoogle Scholar
  61. Weisany W, Sohrabi Y, Heidari G, Siosemardeh A, Ghassemi-Golezani K (2011) Physiological responses of soybean (Glycine max L.) to zinc application under salinity stress. Aust J Crop Sci 5:1441–1447Google Scholar
  62. Xue D, Huang Y, Zhang X, Wei K, Westcott S, Li C, Chen M, Zhang G, Lance R (2009) Identification of QTLs associated with salinity tolerance at late growth stage in barley. Euphytica 169:187–196CrossRefGoogle Scholar
  63. Yang J, Hu C, Hu H, Yu R, Xia Z, Ye X, Zhu J (2008) QTLNetwork: mapping and visualizing genetic architecture of complex traits in experimental populations. Bioinformatics 24:721–723CrossRefPubMedGoogle Scholar
  64. Zhang D, Li H, Wang J, Zhang H, Hu Z, Chu S, Lv H, Yu D (2016) High-density genetic mapping identifies new major loci for tolerance to low-phosphorus stress in soybean. Front Plant Sci 7:372PubMedPubMedCentralGoogle Scholar
  65. Zhao DL, Reddy KR, Kakani VG, Reddy VR (2005) Nitrogen deficiency effects on plant growth, leaf photosynthesis, and hyperspectral reflectance properties of sorghum. Eur J Agron 22:391–403CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Tuyen D. Do
    • 1
  • Tri D. Vuong
    • 1
  • David Dunn
    • 2
  • Scotty Smothers
    • 2
  • Gunvant Patil
    • 1
  • Dennis C. Yungbluth
    • 1
  • Pengyin Chen
    • 2
  • Andrew Scaboo
    • 1
  • Dong Xu
    • 3
  • Thomas E. Carter
    • 4
  • Henry T. Nguyen
    • 1
  • J. Grover Shannon
    • 2
  1. 1.Division of Plant SciencesUniversity of MissouriColumbiaUSA
  2. 2.Division of Plant SciencesUniversity of Missouri, Delta Research CenterPortagevilleUSA
  3. 3.Department of Electric Engineering and Computer Science, Christopher S. Bond Life Sciences CenterUniversity of MissouriColumbiaUSA
  4. 4.Soybean and Nitrogen Fixation UnitUSDA-ARSRaleighUSA

Personalised recommendations