Skip to main content
SpringerLink
Log in

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

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

Abstract

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.

Abstract

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abel GH (1969) Inheritance of the capacity for chloride inclusion and chloride exclusion by soybeans. Crop Sci 9:697–698

    Article  Google Scholar 

  • Abel GH, MacKenzie AJ (1964) Salt tolerance of soybean varieties (Glycine max L. Merill) during germination and later growth. Crop Sci 4:157–161

    Article  Google Scholar 

  • 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 1:80–89

    Google Scholar 

  • 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 14:330

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 10

    Google Scholar 

  • Blanco FF, Folegatti MV, Gheyi HR, Fernandes PD (2007) Emergence and growth of corn and soybean under saline stress. Sci Agric 64:451–459

    Article  CAS  Google Scholar 

  • 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 85:68–76

    Google Scholar 

  • 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 129:1113–1125

    Article  CAS  PubMed  Google Scholar 

  • 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 59:1086–1091

    Article  CAS  Google Scholar 

  • 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 120:1073–1086

    Article  CAS  PubMed  Google Scholar 

  • 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 26:371–376

    Article  CAS  Google Scholar 

  • 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 6:19147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • 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 2:138–141

    Google Scholar 

  • 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 27:657–661

    Article  CAS  Google Scholar 

  • 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 124–127

  • Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Sci 11:929–931

    Article  Google Scholar 

  • 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 13:48

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 121:877–894

    Article  CAS  PubMed  Google Scholar 

  • 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 1:1–8

    Google Scholar 

  • 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 80:937–950

    Article  CAS  PubMed  Google Scholar 

  • 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 123:1375–1385

    Article  CAS  PubMed  Google Scholar 

  • 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 193:79–88

    Article  CAS  Google Scholar 

  • Hamwieh A, Xu DH (2008) Conserved salt tolerance quantitative trait locus (QTL) in wild and cultivated soybeans. Breed Sci 58:355–359

    Article  Google Scholar 

  • 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 179:451–459

    Article  Google Scholar 

  • 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 201:17–31

    Article  CAS  Google Scholar 

  • 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 33:2455–2462

    Article  CAS  PubMed  Google Scholar 

  • 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 290:2147–2162

    Article  CAS  PubMed  Google Scholar 

  • 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 125:406–422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar Tewari A, Charan Tripathy B (1998) Temperature-stress-induced impairment of chlorophyll biosynthetic reactions in cucumber and wheat. Plant Physiol 117:851–858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 109:1610–1619

    Article  CAS  PubMed  Google Scholar 

  • 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 48:2194–2200

    Article  Google Scholar 

  • 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):798–801

    Article  CAS  PubMed  Google Scholar 

  • 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 197:302–310

    Article  CAS  Google Scholar 

  • 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 15:1086

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 108:253–260

    Article  CAS  PubMed  Google Scholar 

  • 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 31:1105–1114

    Article  CAS  Google Scholar 

  • 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 7:1485

    PubMed  PubMed Central  Google Scholar 

  • 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 31:137–152

    Article  CAS  Google Scholar 

  • 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 739–773

    Chapter  Google Scholar 

  • 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 6:19199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phang TH, Shao G, Lam HM (2008) Salt tolerance in soybean. J Integr Plant Biol 50:1196–1212

    Article  CAS  PubMed  Google Scholar 

  • 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 38:282–295

    Article  Google Scholar 

  • 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 5:4340

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 134:653–660

    Article  CAS  Google Scholar 

  • Rabie RK, Kumazawa K (1988) Effect of salt stress on nitrogen nutrition and yield quality of nodulated soybeans. Soil Sci Plant Nutr 34:385–391

    Article  Google Scholar 

  • 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 7:38

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 48:71–77

    Article  CAS  Google Scholar 

  • 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 35:175–186

    Article  Google Scholar 

  • Singleton PW, Bohlool BB (1984) Effect of salinity on nodule formation by soybean. Plant Physiol 74:72–76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e54985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 102–123

    Google Scholar 

  • 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 121:229–236

    Article  CAS  PubMed  Google Scholar 

  • 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 31:79–86

    Article  CAS  Google Scholar 

  • USDA (2011) Breeding plants for a high-ozone world. Agric Res 59:14–17

    Google Scholar 

  • 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 6:23598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Ooijen (2004) MapQTL®5, Software for the mapping of quantitative trait loci in experimental populations. Kyazma BV, Wageningen

    Google Scholar 

  • van Ooijen (2006) JoinMap®4, Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen

    Google Scholar 

  • Várallyay G (2010) The impact of climate change on soils and on their water management. Agron Res 11:385–396

    Google Scholar 

  • Wang D, Shannon MC (1999) Emergence and seedling growth of soybean cultivars and maturity groups under salinity. Plant Soil 214:117–124

    Article  CAS  Google Scholar 

  • 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 5:1441–1447

    CAS  Google Scholar 

  • 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 169:187–196

    Article  Google Scholar 

  • 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 24:721–723

    Article  PubMed  Google Scholar 

  • 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 7:372

    PubMed  PubMed Central  Google Scholar 

  • 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 22:391–403

    Article  CAS  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Division of Plant Sciences, University of Missouri, Columbia, MO, 65211, USA

    Tuyen D. Do, Tri D. Vuong, Gunvant Patil, Dennis C. Yungbluth, Andrew Scaboo & Henry T. Nguyen

  2. Division of Plant Sciences, University of Missouri, Delta Research Center, Portageville, MO, 63873, USA

    David Dunn, Scotty Smothers, Pengyin Chen & J. Grover Shannon

  3. Department of Electric Engineering and Computer Science, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, 65211, USA

    Dong Xu

  4. Soybean and Nitrogen Fixation Unit, USDA-ARS, Raleigh, NC, 27607, USA

    Thomas E. Carter

Authors
  1. Tuyen D. Do
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tri D. Vuong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David Dunn
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Scotty Smothers
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gunvant Patil
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dennis C. Yungbluth
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pengyin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Andrew Scaboo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Dong Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Thomas E. Carter
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Henry T. Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. J. Grover Shannon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Henry T. Nguyen or J. Grover Shannon.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by David A. Lightfoot.

Electronic supplementary material

Below is the link to the electronic supplementary material.

122_2017_3015_MOESM1_ESM.docx

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

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) (http://soybase.org) with salt stress response function in the physical map of Chr. 13 (DOCX 573 kb)

Supplementary material 3 (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Do, T.D., Vuong, T.D., Dunn, D. et al. Mapping and confirmation of loci for salt tolerance in a novel soybean germplasm, Fiskeby III. Theor Appl Genet 131, 513–524 (2018). https://doi.org/10.1007/s00122-017-3015-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-017-3015-0

Search

Navigation