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Advances in Genetics and Breeding of Salt Tolerance in Soybean

  • Huatao Chen
  • Heng Ye
  • Tuyen D. Do
  • Jianfeng Zhou
  • Babu Valliyodan
  • Grover J. Shannon
  • Pengyin Chen
  • Xin Chen
  • Henry T. Nguyen
Chapter

Abstract

Salt stress is one of the major abiotic factors affecting crop growth and production. In general, soybean is sensitive to salt stress. The success of soybean improvement for salt tolerance depends on discovery and utilization of genetic variation in the germplasm. In this chapter, advance in salt-tolerant research and breeding was summarized by highlighting the genetic diversity, quantitative trait loci (QTL), identification of the major locus (Glyma03g32900), and improvement of soybean varieties in salt tolerance. The ion exclusion and tissue tolerance mechanisms regulated by this major locus are discussed. In addition, genomic resources and high-throughput phenotyping platforms that can facilitate a better understanding of phenotype-genotype association and formulate genomic-assisted breeding strategies are prospected.

Keywords

Soybean QTL QTN Next-generation sequencing Marker-assisted selection Single nucleotide polymorphism 

Abbreviations

CAX

Cation exchanger

GWAS

Genome-wide association studies

MAS

Marker-assisted selection

NGS

Next-generation sequencing (NGS)

NHX

Na+/H+ antiporter

QTL

Quantitative trait loci

QTN

Quantitative trait nucleotides

SNP

Single nucleotide polymorphism

Notes

Acknowledgments

This chapter is a joint contribution from the University of Missouri (MU), USA, and Jiangsu Academy of Agricultural Sciences (JAAS), China. We thank JAAS for Huatao Chen visiting scholarship at MU.

References

  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. Merrill) during germination and later growth. Crop Sci 4:157–161CrossRefGoogle Scholar
  3. Ashraf M (1994) Breeding for salinity tolerance in plants. Crit. Rev. Plant Sci. 13, 17–42. https://doi.org/10.1080/713608051. CrossRefGoogle Scholar
  4. Batelli G, Verslues PE, Agius F et al (2007) SOS2 promotes salt tolerance in part by interacting with the vacuolar H+-ATPase and upregulating its transport activity. Mol Cell Biol 27:7781–7790CrossRefPubMedPubMedCentralGoogle Scholar
  5. Berthomieu P, Conéjéro G, Nublat A et al (2003) Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. EMBO J 22:2004–2014CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bhandal IS, Malik CP (1988) Potassium estimation, uptake, and its role in the physiology and metabolism of flowering plants. Int Rev Cytol 110:205–254CrossRefGoogle Scholar
  7. Brown ME, Funk CC (2008) Food security under climate change. Science 319:580–581CrossRefPubMedGoogle Scholar
  8. Chang RZ, Chen YW, Shao GH et al (1994) Effect of salt stress on agronomic characters and chemical quality of seeds in soybean. Soybean Sci 13:101–105Google Scholar
  9. Chen H, Cui S, Fu S et al (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. Chen H, He H, Yu D (2011a) Overexpression of a novel soybean gene modulating Na+ and K+ transport enhances salt tolerance in transgenic tobacco plants. Physiol Plant 141(1):11–18CrossRefPubMedGoogle Scholar
  11. Chen HT, Chen X, Yu DY (2011b) Inheritance analysis and mapping quantitative trait loci (QTLs) associated with salt tolerance during seedling growth in soybean. Chin J Oil Crop Sci 33(3):231–234Google Scholar
  12. Chen P, Yan K, Shao H et al (2013) Physiological mechanisms for high salt tolerance in wild soybean (Glycine soja) from Yellow River Delta, China: Photosynthesis, Osmotic Regulation, Ion Flux and antioxidant Capacity. PLoS One 8(12):e83227CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chen H, Chen X, Gu H et al (2014) GmHKT1;4, a novel soybean gene regulating Na+/K+ ratio in roots enhances salt tolerance in transgenic plants. Plant Growth Regul 73:299–308CrossRefGoogle Scholar
  14. Cheng NH, Pittman JK, Zhu JK et al (2004) The protein kinase SOS2 activates the Arabidopsis H+/Ca2+ antiporter CAX1 to integrate calcium transport and salt tolerance. J Biol Chem 279:2922–2926CrossRefPubMedGoogle Scholar
  15. Do TD, Chen H, Hien VT et al (2016) Ncl synchronously regulates Na+, K+, and Cl− in soybean and greatly increases the grain yield in saline field conditions. Scientific Reports, 6, https://doi.org/10.1038/srep19147
  16. Do TD, Vuong TD, Dunn D, Smothers S, Patil G, Yungbluth DC, Chen P, Scaboo A, Xu D, Carter TE, Nguyen HT, Grover Shannon J (2018) Mapping and confirmation of loci for salt tolerance in a novel soybeangermplasm, Fiskeby III. Theor Appl Genet 131(3):513–524. https://doi.org/10.1007/s00122-017-3015-0. CrossRefPubMedGoogle Scholar
  17. Essa TA (2002) Effect of salinity stress on growth and nutrient composition of three soybean (Glycine max L. Merrill) cultivars. J Agron Crop Sci 188:86–93CrossRefGoogle Scholar
  18. FAO A (2000) Extent and causes of salt affected soils in participating countries. Available from http://www.fao.org/ag/agl/agll/spush/topic2.htm
  19. Fredj MB, Zhani K, Hannachi C, Mehwachi T (2013) Effect of NaCl priming on seed germination of four coriander cultivars (Coriandrum sativum). Eurasia J Bio Sci 7:11–29Google Scholar
  20. Gassmann W, Rubio F, Schroeder JI (1996) Alkali cation selectivity of the wheat root high-affinity potassium transporter HKT1. Plant J 10:869–952CrossRefGoogle Scholar
  21. Gierth M, Mäser P (2007) Potassium transporters in plants – involvement in K+ acquisition, redistribution and homeostasis. FEBS Lett 581:2348–2356CrossRefPubMedGoogle Scholar
  22. Gizlice Z, Carter Jr TE, Burton JW (1994) Genetic base for the North American public soybean cultivars released between 1947 and 1988. Crop Sci 34:1143–1151Google Scholar
  23. Guan R, Qu Y, Guo Y et al (2014) Salinity tolerance in soybean is modulated by natural variation in GmSALT3. Plant J 80:937–950CrossRefPubMedGoogle Scholar
  24. Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genom 2014:1–18. https://doi.org/10.1155/2014/701596 CrossRefGoogle Scholar
  25. Ha BK, Vuong TD, Velusamy V et al (2013) Genetic mapping of quantitative trait loci conditioning salt tolerance in wild soybean (Glycine soja) PI 483463. Euphytica 193:79–88CrossRefGoogle Scholar
  26. Halfter U, Ishitani M, Zhu JK (2000) The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc Natl Acad Sci U S A 97:3735–3740CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hamayun M, Hussain A, Khan SA et al (2015) Kinetin modulates physio-hormonal attributes and isoflavone contents of soybean grown under salinity stress. Front Plant Sci 6:377. https://doi.org/10.3389/fpls CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hamwieh A, Xu DH (2008) Conserved salt tolerance quantitative trait locus (QTL) in wild and cultivated soybeans. Breed Sci 58:355–359CrossRefGoogle Scholar
  29. Hamwieh A, Do DD, Cong H et al (2011) Identification and validation of a major QTL for salt tolerance in soybean. Euphytica 79:451–459CrossRefGoogle Scholar
  30. Hao D, Chao M, Yin Z et al (2012) Genome-wide association analysis detecting significant single nucleotide polymorphisms for chlorophyll and chlorophyll fluorescence parameters in soybean (Glycine max) landraces. Euphytica 186:919–931CrossRefGoogle Scholar
  31. Hasegawa PM (2013) Sodium (Na+) homeostasis and salt tolerance of plants. Environ Exp Bot 92:19–31CrossRefGoogle Scholar
  32. Hauser F, Horie T (2010) A conserved primary salt tolerance mechanism mediated by HKT transporters: a mechanism for sodium exclusion and maintenance of high K+/Na+ ratio in leaves during salinity stress. Plant Cell Environ 33:552–565CrossRefPubMedGoogle Scholar
  33. He Y, Fu J, Yu C et al (2015) Increasing cyclic electron flow is related to Na+ sequestration into vacuoles for salt tolerance in soybean. J Exp Bot 66:6877–6889CrossRefPubMedPubMedCentralGoogle Scholar
  34. Hosseini MK, Powell AA, Bingham IJ (2002) Comparison of the seed germination and early seedling growth of soybean in saline conditions. Seed Sci Res 12:165–172CrossRefGoogle Scholar
  35. Hrabak EM, Chan CW, Gribskov M et al (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666–680CrossRefPubMedPubMedCentralGoogle Scholar
  36. Huertas R, Olías R, Eljakaoui Z et al (2012) Overexpression of SlSOS2 (SlCIPK24) confers salt tolerance to transgenic tomato. Plant Cell Environ 35:1467–1482CrossRefPubMedGoogle Scholar
  37. Hwang EY, Song Q, Jia G et al (2014) A genome-wide association study of seed protein and oil content in soybean. BMC Genomics 15:1CrossRefPubMedPubMedCentralGoogle Scholar
  38. Ishitani M, Liu J, Halfter U et al (2000) SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell 12(9):1667–1678CrossRefPubMedPubMedCentralGoogle Scholar
  39. Jacobs TB, LaFayette PR, Schmitz RJ, Parrott WA (2015) Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol12;15:16. https://doi.org/10.1186/s12896-015-0131-2 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Jaspers P, Brosché M, Overmyer K et al (2010) The transcription factor interacting protein RCD1 contains a novel conserved domain. Plant Signal Behav 5:78–80CrossRefPubMedPubMedCentralGoogle Scholar
  41. Ji H, Pardo JM, Batelli G et al (2013) The salt overly sensitive (SOS) pathway: established and emerging roles. Mol Plant 6:275–286CrossRefPubMedGoogle Scholar
  42. Kan GZ, Zhang W, Yang W et al (2015) Association mapping of soybean seed germination under salt stress. Mol Gen Genomics 290:2147–2162CrossRefGoogle Scholar
  43. Kan G, Ning L, Li Y et al (2016) Identification of novel loci for salt stress at the seed germination stage in soybean. Breed Sci 66(4):530–541CrossRefPubMedPubMedCentralGoogle Scholar
  44. Katiyar-Agarwal S, Zhu J, Kim K et al (2006) The plasma membrane Na+/H+ antiporter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis. Proc Natl Acad Sci U S A 103:18816–18821CrossRefPubMedPubMedCentralGoogle Scholar
  45. Lee GJ, Carter TE Jr, Villagarcia MR et al (2004) A major QTL conditioning salt tolerance in S-100 soybean and descendent cultivars. Theor Appl Genet 109:1610–1619CrossRefPubMedGoogle Scholar
  46. Lee JD, Shannon JG, Vuong TD et al (2009) Inheritance of salt tolerance in wild soybean (Glycine soja Sieb. and Zucc.) accession PI483463. J Hered 100:798–801CrossRefPubMedGoogle Scholar
  47. Liu J, Zhu JK (1998) A calcium sensor homolog required for plant salt tolerance. Science 280:1943–1945CrossRefPubMedGoogle Scholar
  48. Liu J, Ishitani M, Halfter U et al (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci U S A 97:3730–3734CrossRefPubMedPubMedCentralGoogle Scholar
  49. Liu Y, Yu L, Qu Y et al (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
  50. Luo GZ, Wang HW, Huang J et al (2005a) A putative plasma membrane cation/proton antiporter from soybean confers salt tolerance in Arabidopsis. Plant Mol Biol 59:809–820CrossRefPubMedGoogle Scholar
  51. Luo Q, Yu B, Liu Y (2005b) Differential sensitivity to chloride and sodium ions in seedlings of Glycine max and G. soja under NaCl stress. J Plant Physiol 162:1003–1012CrossRefPubMedGoogle Scholar
  52. Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann Bot 84:123–133CrossRefGoogle Scholar
  53. Mamidi S, Chikara S, Goos RJ et al (2011) Genome-wide association analysis identifies candidate genes associated with iron deficiency chlorosis in soybean. Plant Genome 4:154–164CrossRefGoogle Scholar
  54. Mäser P, Eckelman B, Vaidyanathan R et al (2002) Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1. FEBS Lett 531:157–161CrossRefPubMedGoogle Scholar
  55. Mickelbart MV, Hasegawa PM, Bailey-Serres J (2015) Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability. Nat. Rev. Genet16:237–251. https://doi.org/10.1038/nrg3901 CrossRefPubMedGoogle Scholar
  56. Møller IS, Gilliham M, Jha D et al (2009) Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell 21:2163–2178CrossRefPubMedPubMedCentralGoogle Scholar
  57. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681CrossRefPubMedGoogle Scholar
  58. Munns R, James AJ, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043CrossRefPubMedGoogle Scholar
  59. Niu X, Bressan RA, Hasegawa PM et al (1995) Ion homeostasis in NaCl stress environments. Plant Physiol 109(3):735–742CrossRefPubMedPubMedCentralGoogle Scholar
  60. Oh DH, Lee SY, Bressan RA et al (2010) Intracellular consequences of SOS1 deficiency during salt stress. J Exp Bot 61:1205–1213CrossRefPubMedPubMedCentralGoogle Scholar
  61. Ohta M, Guo Y, Halfter U et al (2003) A novel domain in the protein kinase SOS2 mediates interaction with the protein phosphatase 2C ABI2. Proc Natl Acad Sci U S A 100:11771–11776CrossRefPubMedPubMedCentralGoogle Scholar
  62. Papiernik SK, Grieve CM, Lesch SM et al (2005) Effects of salinity, imazethapyr, and chlorimuron application on soybean growth and yield. Commun Soil Sci Plant Anal 36:951–967CrossRefGoogle Scholar
  63. Parker MB, Gascho GJ, Gains TP (1983) Chloride toxicity of soybeans grown on Atlantic Coast flatwoods soils. Agron J 75:439–443CrossRefGoogle Scholar
  64. Pathan MS, Lee JD, Shannon JG et al (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
  65. Patil G, Do T, Vuong TD et al (2016) Genomic-assisted haplotype analysis and the development of high-throughput SNP markers for salinity tolerance in soybean. Sci Rep 6:19199CrossRefPubMedPubMedCentralGoogle Scholar
  66. Phang TH, Shao GH, Lam HM (2008) Salt tolerance in soybean. J Integr Plant Biol 50(10):1196–1212CrossRefPubMedGoogle Scholar
  67. Pimentel D, Berger B, Filiberto D et al (2004) Water resources: agricultural and environmental issues. Bioscience 54:909–918CrossRefGoogle Scholar
  68. Qi X, Li MW, Xie M et al (2014) Identification of a novel salt tolerance gene in wild soybean by whole-genome sequencing. Nat Commun 5:4340CrossRefPubMedPubMedCentralGoogle Scholar
  69. Qiu QS, Guo Y, Dietrich MA et al (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci U S A 99:8436–8441CrossRefPubMedPubMedCentralGoogle Scholar
  70. Qiu QS, Guo Y, Quintero FJ et al (2004) Regulation of vacuolar Na+/H+ exchange in Arabidopsis thaliana by the salt-overly-sensitive (SOS) pathway. J Biol Chem 279:207–215CrossRefPubMedGoogle Scholar
  71. Ren ZH, Gao JP, Li LG et al (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37:1141–1146CrossRefPubMedGoogle Scholar
  72. Ren S, Weeda S, Li H et al (2012) Salt tolerance in soybean WF-7 is partially regulated by ABA and ROS signaling and involves withholding toxic Cl ions from aerial tissues. Plant Cell Rep 31:1527–1533CrossRefPubMedGoogle Scholar
  73. Rosegrant MW, Cline SA (2003) Global food security: challenges and policies. Science 302:1917–1919CrossRefPubMedGoogle Scholar
  74. Roy SJ, Negrao S, Tester M (2014) Salt resistant crop plants. Curr. Opin. Biotechnol. 26:115–124.https://doi.org/10.1016/j.copbio.2013.12.004 CrossRefPubMedGoogle Scholar
  75. Rubio F, Gassmann W, Schroeder JI (1995) Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270:1660–1663CrossRefPubMedGoogle Scholar
  76. Rus A, Lee BH, Muñoz-Mayor A et al (2004) AtHKT1 facilitates Na+ homeostasis and K+ nutrition in planta. Plant Physiol 136:2500–2511CrossRefPubMedPubMedCentralGoogle Scholar
  77. Schmidhuber J, Tubiello FN (2007) Global food security under climate change. Proc Natl Acad Sci U S A 104:19703–19708CrossRefPubMedPubMedCentralGoogle Scholar
  78. Serrano R, Mulet JM, Rios G et al (1999) A glimpse of the mechanisms of ion homeostasis during salt stress. J Exp Bot 50:1023–1036CrossRefGoogle Scholar
  79. Shao GH, Chang RZ, Chen YW et al (1994) Study on inheritance of salt tolerance in soybean. Acta Agron Sin 20:721–726Google Scholar
  80. Shi HZ, Quintero FJ, Pardo JM et al (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477CrossRefPubMedPubMedCentralGoogle Scholar
  81. Shi H, Lee BH, Wu SJ et al (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21:81–85CrossRefPubMedGoogle Scholar
  82. Singleton PW, Bohlool BB (1984) Effect of salinity on nodule formation by soybean. Plant Physiol 74:72–76CrossRefPubMedPubMedCentralGoogle Scholar
  83. Sneller CH (1994) Pedigree analysis of elite soybean cultivars. Crop Sci. 34:1515–1522CrossRefGoogle Scholar
  84. Stocking MA (2003) Tropical soils and food security: the next 50 years. Science 302:1356–1359CrossRefPubMedGoogle Scholar
  85. Sun YX, Wang D, Bai YL et al (2006) Studies on the overexpression of the soybean GmNHX1 in Lotus corniculatus: the reduced Na+ level is the basis of the increased salt tolerance. Chin Sci Bull 51:1306–1315CrossRefGoogle Scholar
  86. Sun X, Hu Z, Chen R, Jiang Q, Song G, Zhang H, Xi, Y (2015) Targeted mutagenesis in soybean using the CRISPR-Cas9 system. Sci Rep 5: 10342.CrossRefPubMedPubMedCentralGoogle Scholar
  87. Sunarpi TH, Motoda J, Kubo M et al (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem parenchyma cells. Plant J 44:928–938CrossRefPubMedGoogle Scholar
  88. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527CrossRefPubMedPubMedCentralGoogle Scholar
  89. Tilman D, Balzer C, Hill J et al (2011) Global food demand and the sustainable intensification of agriculture. Proc Natl Acad Sci U S A 108:20260–20264CrossRefPubMedPubMedCentralGoogle Scholar
  90. Verslues PE, Batelli G, Grillo S et al (2007) Interaction of SOS2 with Nucleoside Diphosphate Kinase 2 and catalases reveals a point of connection between salt stress and H2O2 signaling in Arabidopsis thaliana. Mol Cell Biol 27:7771–7780CrossRefPubMedPubMedCentralGoogle Scholar
  91. Wan C, Shao G, Chen Y et al (2002) Relationship between salt tolerance and chemical quality of soybean under salt stress. Chin J Oil Crop Sci 24:67–72Google Scholar
  92. Wei P, Wang L, Liu A et al (2016) GmCLC1 confers enhanced salt tolerance through regulating chloride accumulation in soybean. Front Plant Sci 7:1082PubMedPubMedCentralGoogle Scholar
  93. Wen ZX, Tan R, Yuan J et al (2014) Genome-wide association mapping of quantitative resistance to sudden death syndrome in soybean. BMC Genomics 15:1Google Scholar
  94. Wen ZX, Boyse JF, Song Q et al (2015) Genomic consequences of selection and genome-wide association mapping in soybean. BMC Genomics 16:671CrossRefPubMedPubMedCentralGoogle Scholar
  95. Wu SJ, Lei D, Zhu JK (1996) SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell 8:617–627CrossRefPubMedPubMedCentralGoogle Scholar
  96. Xu DH, Do TD, Chen HT et al (2016) Genetic analysis of salt tolerance in soybean. Plant & animal genome conference XXIV, P0983. (https://pag.confex.com/pag/xxiv/webprogram/Paper20285.html)
  97. Yang J, Blanchar RW (1993) Differentiating chloride susceptibility in soybean cultivars. Agron J 85:880–885CrossRefGoogle Scholar
  98. Yu L, Nie J, Cao C et al (2010) Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol 188:762–773CrossRefPubMedGoogle Scholar
  99. Zeng A, Chen P, Korth K et al (2017) Genome-wide association study (GWAS) of salt tolerance in worldwide soybean germplasm lines. Mol Breed 37:1–14. https://doi.org/10.1007/s11032-017-0634-8 CrossRefGoogle Scholar
  100. Zhang WJ, Niu Y, Bu SH et al (2014) Epistatic association mapping for alkaline and salinity tolerance traits in the soybean germination stage. PLoS One 9(1):e84750CrossRefPubMedPubMedCentralGoogle Scholar
  101. Zhang J, Song Q, Cregan PB et al (2015) Genome-wide association study for flowering time, maturity dates and plant height in early maturing soybean (Glycine max) germplasm. BMC Genomics 16:217CrossRefPubMedPubMedCentralGoogle Scholar
  102. Zhao Y, Wang T, Zhang W et al (2011) SOS3 mediates lateral root development under low salt stress through regulation of auxin redistribution and maxima in Arabidopsis. New Phytol 189:1122–1134CrossRefPubMedGoogle Scholar
  103. Zhu JK (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol 124:941–948CrossRefPubMedPubMedCentralGoogle Scholar
  104. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273CrossRefPubMedPubMedCentralGoogle Scholar
  105. Zhu JK, Liu J, Xiong L (1998) Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell 10:1181–1191CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Huatao Chen
    • 1
    • 2
  • Heng Ye
    • 1
  • Tuyen D. Do
    • 1
  • Jianfeng Zhou
    • 3
  • Babu Valliyodan
    • 1
  • Grover J. Shannon
    • 1
  • Pengyin Chen
    • 4
  • Xin Chen
    • 2
  • Henry T. Nguyen
    • 1
  1. 1.Division of Plant SciencesUniversity of MissouriColumbiaUSA
  2. 2.Institute of Industrial Crops, Jiangsu Academy of Agricultural SciencesNanjingChina
  3. 3.Division of Agricultural Systems ManagementUniversity of MissouriColumbiaUSA
  4. 4.Division of Plant SciencesUniversity of Missouri, Delta Research CenterPortagevilleUSA

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