Theoretical and Applied Genetics

, Volume 121, Issue 5, pp 877–894 | Cite as

Sodium exclusion QTL associated with improved seedling growth in bread wheat under salinity stress

  • Y. GencEmail author
  • K. Oldach
  • A. P. Verbyla
  • G. Lott
  • M. Hassan
  • M. Tester
  • H. Wallwork
  • G. K. McDonald
Original Paper


Worldwide, dryland salinity is a major limitation to crop production. Breeding for salinity tolerance could be an effective way of improving yield and yield stability on saline-sodic soils of dryland agriculture. However, this requires a good understanding of inheritance of this quantitative trait. In the present study, a doubled-haploid bread wheat population (Berkut/Krichauff) was grown in supported hydroponics to identify quantitative trait loci (QTL) associated with salinity tolerance traits commonly reported in the literature (leaf symptoms, tiller number, seedling biomass, chlorophyll content, and shoot Na+ and K+ concentrations), understand the relationships amongst these traits, and determine their genetic value for marker-assisted selection. There was considerable segregation within the population for all traits measured. With a genetic map of 527 SSR-, DArT- and gene-based markers, a total of 40 QTL were detected for all seven traits. For the first time in a cereal species, a QTL interval for Na+ exclusion (wPt-3114-wmc170) was associated with an increase (10%) in seedling biomass. Of the five QTL identified for Na+ exclusion, two were co-located with seedling biomass (2A and 6A). The 2A QTL appears to coincide with the previously reported Na+ exclusion locus in durum wheat that hosts one active HKT1;4 (Nax1) and one inactive HKT1;4 gene. Using these sequences as template for primer design enabled mapping of at least three HKT1;4 genes onto chromosome 2AL in bread wheat, suggesting that bread wheat carries more HKT1;4 gene family members than durum wheat. However, the combined effects of all Na+ exclusion loci only accounted for 18% of the variation in seedling biomass under salinity stress indicating that there were other mechanisms of salinity tolerance operative at the seedling stage in this population. Na+ and K+ accumulation appear under separate genetic control. The molecular markers wmc170 (2A) and cfd080 (6A) are expected to facilitate breeding for salinity tolerance in bread wheat, the latter being associated with seedling vigour.


Quantitative Trait Locus Bread Wheat Salinity Stress Durum Wheat Salinity Tolerance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Mr. Robin Hosking (Australian Centre for Plant Functional Genomics) for his construction and creative modification of the supported hydroponic system and technical support throughout this project, Mr. David Keetch (The University of Adelaide) for his help with the supported hydroponic experiments, and Mrs. Teresa Fowles and Mr. Lyndon Palmer (The University of Adelaide) for their help with the elemental analyses, Mrs. Kerrie Willsmore and Dr. Kevin Williams (South Australian Research and Development Institute) for the initial construction of the map, Dr. Neil Coombes for designing the experiments (Department of Primary Industries, New South Wales, Australia), and, editor and anonymous reviewers for their constructive comments on this manuscript. This work was supported by the Molecular Plant Breeding Cooperative Research Centre, South Australian Research and Development Institute, The Grains Research and Development Corporation, Australian Centre for Plant Functional Genomics, and The University of Adelaide, Australia.

Supplementary material

122_2010_1357_MOESM1_ESM.doc (1.9 mb)
Supplementary material 1 (DOC 1,953 kb)


  1. Akbari M, Wenzl P, Caig V et al (2006) Diversity arrays technology (DArT) for high-throughput profiling of the hexaploid wheat genome. Theor Appl Genet 113:1409–1420CrossRefPubMedGoogle Scholar
  2. Altschul SF, Madden TL, Schäffer AA et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefPubMedGoogle Scholar
  3. Ashraf M, McNeilly T (1988) Variability in salt tolerance of nine spring wheat cultivars. J Agron Crop Sci 160:14–21CrossRefGoogle Scholar
  4. Ashraf M, O’Leary JW (1996) Responses of newly developed salt-tolerant genotype of spring wheat to salt stress: yield components and ion distribution. J Agron Crop Sci 176:91–101CrossRefGoogle Scholar
  5. Bagci SA, Ekiz H, Yilmaz A (2007) Salt tolerance of sixteen wheat genotypes during seedling growth. Turk J Agric For 31:363–372Google Scholar
  6. Barker SJ, Stummer B, Gao L et al (1998) A mutant in Lycopersicon esculentum Mill. with highly reduced VA mycorrhizal colonisation: isolation and preliminary characterization. Plant J 15:791–797CrossRefGoogle Scholar
  7. Bonilla P, Dvorak J, Mackill D et al (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. Byrt CS, Platten JD, Spielmeyer W et al (2007) HKT1;5-Like cation transporters linked to Na+ exclusion loci in wheat, Nax2 and Kna1. Plant Physiol 143:1918–1928CrossRefPubMedGoogle Scholar
  9. Chen Z, Zhou M, Newman IA et al (2007) Potassium and sodium relations in salinised barley tissues as a basis of differential salt tolerance. Funct Plant Biol 34:150–162CrossRefGoogle Scholar
  10. Colmer TD, Munns R, Flowers TJ (2005) Improving salt tolerance of wheat and barley: future prospects. Aust J Exp Agric 45:1425–1443CrossRefGoogle Scholar
  11. Coombes NE (2002) The reactive tabu search for efficient correlated experimental designs. PhD thesis, John Moores University, LiverpoolGoogle Scholar
  12. Cuin TA, Betts SA, Chalmandrier R et al (2008) A root’s ability to retain K+ correlates with salt tolerance in wheat. J Exp Bot 59:2697–2706CrossRefPubMedGoogle Scholar
  13. Dubcovsky J, Maria GS, Epstein E et al (1996) Mapping of the K+/Na+ discrimination locus Kna1 in wheat. Theor Appl Genet 92:448–454CrossRefGoogle Scholar
  14. Edwards J, Shavrukov Y, Ramsey C et al (2008) Identification of a QTL on chromosome 7AS for sodium exclusion. In: Appels R, Eastwood R, Lagudah E, Langridge P, Mackay M, McIntyre L, Sharp P (eds) Proceedings of 11th international wheat genetics symposium. Sydney University Press, AustraliaGoogle Scholar
  15. Ellis RP, Forster BP, Waugh R et al (1997) Mapping physiological traits in barley. New Phytol 137:149–157CrossRefGoogle Scholar
  16. Ellis RP, Forster BP, Gordon DC et al (2002) Phenotype/genotype associations for yield and salt tolerance in a barley mapping population segregating for two dwarfing genes. J Exp Bot 53:1163–1176CrossRefPubMedGoogle Scholar
  17. Flowers TJ (2004) Improving salt tolerance. J Exp Bot 55:307–319CrossRefPubMedGoogle Scholar
  18. Flowers TJ, Yeo AR (1995) Breeding for salinity resistance in crop plants: where next? Aust J Plant Physiol 22:875–884CrossRefGoogle Scholar
  19. Francki MG, Walker E, Crawford AC et al (2009) Comparison of genetic and cytogenetic maps of hexaploid wheat (Triticum aestivum L.) using SSR and DArT markers. Mol Genet Genomics 281:181–191CrossRefPubMedGoogle Scholar
  20. Fu D, Szücs P, Yan L et al (2005) Large deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat. Mol Genet Genomics 273:54–65CrossRefPubMedGoogle Scholar
  21. Garcia A, Rizzo CA, Ud-Din J et al (1997) Sodium and potassium transport to the xylem are inherited independently in rice and the mechanisms of sodium: potassium selectivity differs between rice and wheat. Plant Cell Environ 20:1167–1174CrossRefGoogle Scholar
  22. Genc Y, McDonald GK, Tester M (2007) Re-assessment of tissue Na+ concentration as a criterion for salinity tolerance in bread wheat. Plant Cell Environ 30:1486–1498CrossRefPubMedGoogle Scholar
  23. Genc Y, Tester M, McDonald GK (2010) Calcium requirement of wheat under saline and non-saline conditions. Plant Soil 327:331–345CrossRefGoogle Scholar
  24. Gregorio GB (1997) Tagging salinity tolerance genes in rice using amplified fragment length polymorphism (ALFP). PhD thesis, University of the Philippines, Las BanosGoogle Scholar
  25. Gupta PK (2002) Molecular markers and QTL analysis in crop plants. Curr Sci 83:113–114Google Scholar
  26. Gupta PK, Balyan HS, Edwards KJ et al (2002) Genetic mapping of 66 new microsatellite (SSR) loci in bread wheat. Theor Appl Genet 105:413–422CrossRefPubMedGoogle Scholar
  27. Guyomarc’h H, Sourdille P, Charmet G et al (2002) Characterisation of polymorphic microsatellite markers from Aegilops tauschii and transferability to the d-genome of bread wheat. Theor Appl Genet 104:1164–1172CrossRefPubMedGoogle Scholar
  28. Hayden MJ, Nguyen TM, Waterman A et al (2008) Application of multiplex-ready PCR for fluorescence-based SSR genotyping in barley and wheat. Mol Breed 21:271–281CrossRefGoogle Scholar
  29. Hollington PA (2000) Technological breakthroughs in screening/breeding wheat varieties for salt tolerance. In: Gupta SK, Sharma SK, Tyagi NK (eds) National conference on salinity management in agriculture. Central Soil Salinity Research Institute, Karnal, pp 273–289Google Scholar
  30. Huang Y, Zhang G, Wu F et al (2006a) Differences in physiological traits among salt-stressed barley genotypes. Commun Soil Sci Plant Anal 37:567–570CrossRefGoogle Scholar
  31. Huang S, Spielmeyer W, Lagudah ES et al (2006b) A sodium transporter (HKT7) is a candidate for Nax1, a gene for salt tolerance in durum wheat. Plant Physiol 142:1718–1727CrossRefPubMedGoogle Scholar
  32. Huang S, Spielmeyer W, Lagudah ES et al (2008) Comparative mapping of HKT genes in wheat, barley, and rice, key determinants of Na+ transport, and salt tolerance. J Exp Bot 59:927–937CrossRefPubMedGoogle Scholar
  33. Husain S, Munns R, Condon AG (2003) Effect of sodium exclusion on chlorophyll retention and growth of durum wheat in saline soil. Aust J Agric Res 54:589–597CrossRefGoogle Scholar
  34. James RA, Davenport RJ, Munns R (2006) Physiological characterization of two genes for Na exclusion in durum wheat, Nax1 and Nax2. Plant Physiol 142:1537–1547CrossRefPubMedGoogle Scholar
  35. Koyama ML, Levesley A, Koebner RMD et al (2001) Quantitative trait loci for component physiological traits determining salt tolerance in rice. Plant Physiol 125:406–422CrossRefPubMedGoogle Scholar
  36. Lee SY, Ahn JH, Cha YS et al (2007) Mapping QTLs related to salinity tolerance of rice at the young seedling stage. Plant Breed 126:43–46CrossRefGoogle Scholar
  37. Lin HX, Zhu MZ, Yano M et al (2004) QTLs for Na+ and K+ uptake of the shoots and roots controlling rice salt tolerance. Theor Appl Genet 108:253–260CrossRefPubMedGoogle Scholar
  38. Lindsay MP, Lagudah ES, Hare RA et al (2004) A locus for sodium exclusion (Nax1), a trait for salt tolerance, mapped in durum wheat. Funct Plant Biol 31:1105–1114CrossRefGoogle Scholar
  39. Liu CJ, Atkinson MD, Chinoy CN et al (1992) Nonhomoeologous translocations between group 4, 5 and 7 chromosomes within wheat and rye. Theor Appl Genet 83:305–312CrossRefGoogle Scholar
  40. Ma L, Zhou E, Huo N et al (2007) Genetic analysis of salt tolerance in a recombinant inbred population of wheat (Triticum aestivum L.). Euphytica 153:109–117CrossRefGoogle Scholar
  41. Manly KF, Cudmore RH Jr, Meer JM (2001) Map Manager QTX, cross platform software for genetic mapping. Mamm Genome 12:930–932CrossRefPubMedGoogle Scholar
  42. Mano Y, Takeda K (1997) Mapping quantitative trait loci for salt tolerance at germination and the seedling stage in barley (Hordeum vulgare L.). Euphytica 94:263–272CrossRefGoogle Scholar
  43. Munns R, James RA (2003) Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant Soil 253:201–218CrossRefGoogle Scholar
  44. Munns R, Tester M (2008) Mechanisms of salt tolerance. Annu Rev Plant Biol 59:651–681CrossRefPubMedGoogle Scholar
  45. Munns R, Husain S, Rivelli AR et al (2002) Avenues for increasing salt tolerance of crops, and the role of physiologically based selection traits. Plant Soil 247:93–105CrossRefGoogle Scholar
  46. Munns R, James RA, Islam AKMR et al (2008) Sodium excluding genes from durum wheat and sea barleygrass improve sodium exclusion of bread wheat. In: 2nd international salinity forum salinity, water and society—global issues, local action. Adelaide, South AustraliaGoogle Scholar
  47. Naqvi SAM, Tandon JP (1991) Wheat varieties for salt affected lands. Indian Farming 41:11–14Google Scholar
  48. Ogbonnaya FC, Huang S, Steadman E et al (2008) Mapping quantitative trait loci associated with salinity tolerance in synthetic derived backcrossed bread lines. In: Appels R, Eastwood R, Lagudah E, Langridge P, Mackay M, McIntyre L, Sharp P (eds) Proceedings of 11th international wheat genetics symposium. Sydney University Press, AustraliaGoogle Scholar
  49. Peleg Z, Saranga Y, Suprunova T et al (2008) High-density genetic map of durum wheat and wild emmer wheat based on SSR and DArT markers. Theor Appl Genet 117:103–115CrossRefPubMedGoogle Scholar
  50. Pestsova E, Korzun V, Goncharov NP et al (2000) Microsatellite analysis of Aegilops tauschii germplasm. Theor Appl Genet 101:100–106CrossRefGoogle Scholar
  51. Platten JD, Cotsaftis O, Berthomieu P et al (2006) Nomenclature for HKT transporters, key determinants of plant salinity tolerance. Trends Plant Sci 11:372–374CrossRefPubMedGoogle Scholar
  52. Poustini K, Siosemardeh A (2004) Ion distribution in wheat cultivars in response to salinity stress. Field Crops Res 85:125–133CrossRefGoogle Scholar
  53. Prasad S, Bagali P, Hittalmani S et al (2000) Molecular mapping of quantitative trait loci associated with seedling tolerance to salt stress in rice (Oryza sativa L.). Curr Sci 78:162–164Google Scholar
  54. Quarrie SA, Steed A, Calestani C et al (2005) A high-density genetic map of hexaploid wheat (Triticum aestivum L.) from the cross Chinese Spring × SQ1 and its use to compare QTLs for grain yield across a range of environments. Theor Appl Genet 110:865–880CrossRefPubMedGoogle Scholar
  55. Rajendran K, Tester M, Stuart JR (2009) Quantifying the three main components of salinity tolerance in cereals. Plant Cell Environ 32:237–249CrossRefPubMedGoogle Scholar
  56. Rashid A, Querishi RH, Hollington PA et al (1999) Comparative responses of wheat cultivars to salinity at the seedling stage. J Agron Crop Sci 182:199–207CrossRefGoogle Scholar
  57. Rengasamy P (2002) Transient salinity and subsoil constraints to dryland farming in Australian sodic soils: an overview. Aust J Exp Agric 42:351–361CrossRefGoogle Scholar
  58. Rengasamy P (2006) World salinization with emphasis on Australia. J Exp Bot 57:1017–1023CrossRefPubMedGoogle Scholar
  59. Reuter DJ, Robinson AD (1997) Plant analysis: an interpretation manual, 2nd edn. CSIRO, AustraliaGoogle Scholar
  60. Richards RA (1983) Should selection for yield in saline regions be made on saline or non-saline soils. Euphytica 32:431–438CrossRefGoogle Scholar
  61. Richards RA, Dennett CW, Qualset CO et al (1987) Variation in yield of grain and biomass in wheat, barley and triticale in a salt-affected field. Field Crops Res 15:277–287CrossRefGoogle Scholar
  62. Rivandi A (2009) Toward map-based cloning of a Na+ exclusion gene from barley (Hordeum vulgare L.). PhD thesis, The University of Adelaide, AustraliaGoogle Scholar
  63. Röder MS, Korzun V, Wendehake K et al (1998) A microsatellite map of wheat. Genetics 149:2007–2023PubMedGoogle Scholar
  64. Schachtman DP, Lagudah ES, Munns R (1992) The expression of salt tolerance from Triticum tauschii in hexaploid wheat. Theor Appl Genet 84:714–719CrossRefGoogle Scholar
  65. Sears ER (1954) The aneuploids of common wheat. Missouri Agricultural Experiment Station Research Bulletin No. 572Google Scholar
  66. Shannon MC, Noble CL (1990) Genetic approaches for developing economic salt tolerant crops. In: Tanji KK (ed) Agricultural salinity assessment and management. ACSE Manuals and reports on engineering practice No. 71. ASCE, New York, pp 165–185Google Scholar
  67. Shannon MC, Rhoades JD, Draper JH et al (1998) Assessment of salt tolerance in rice cultivars in response to salinity problems in California. Crop Sci 38:394–398CrossRefGoogle Scholar
  68. Shavrukov Y, Gupta NK, Miyazaki J et al (2010) HvNax3-a locus controlling shoot sodium exclusion derived from wild barley (Hordeum vulgare ssp. spontaneum) Funct Integr Genomics. doi: 10.1007/s10142-009-0153-8
  69. Singh K, Ghai M, Garg M et al (2007) An integrated molecular linkage map of diploid wheat based on a Triticum boeoticum and T. monococcum RIL population. Theor Appl Genet 115:301–312CrossRefPubMedGoogle Scholar
  70. Smith A, Cullis B, Thompson R (2001) Analyzing variety by environment data using multiplicative mixed models and adjustments for spatial field trend. Biometrics 57:1138–1147CrossRefPubMedGoogle Scholar
  71. Song QJ, Fickus EW, Cregan PB (2002) Characterization of trinucleotide SSR motifs in wheat. Theor Appl Genet 104:286–293CrossRefPubMedGoogle Scholar
  72. Song QJ, Shi JR, Singh S et al (2005) Development and mapping of microsatellite (SSR) markers in wheat. Theor Appl Genet 110:550–560CrossRefPubMedGoogle Scholar
  73. Sorrells ME, La Rota M, Bermudez-Kandianis CE et al (2003) Comparative DNA sequence analysis of wheat and rice genomes. Genome Res 13:1818–1827PubMedGoogle Scholar
  74. Sourdille P, Cadalen T, Guyomarc’h H et al (2003) An update of the Courtot × Chinese Spring intervarietal molecular marker linkage map for the QTL detection of agronomic traits in wheat. Theor Appl Genet 106:530–538PubMedGoogle Scholar
  75. Spielmeyer W, Hyles J, Joaquim P et al (2007) A QTL on chromosome 6A in bread wheat (Triticum aestivum L.) is associated with longer coleoptiles, greater seedling vigour and final plant height. Theor Appl Genet 115:59–66CrossRefPubMedGoogle Scholar
  76. Taeb M, Koebner RMD, Forster BP et al (1992) Association between genes controlling flowering time and shoot sodium accumulation in the Triticeae. Plant Soil 146:117–121CrossRefGoogle Scholar
  77. Van Os H, Stam P, Visser R et al (2005) RECORD: a novel method for ordering loci on a genetic linkage map. Theor Appl Genet 112:30–40CrossRefPubMedGoogle Scholar
  78. Verbyla AP, Cullis BR (2010) Multivariate whole genome average interval mapping. Theor Appl Genet (submitted)Google Scholar
  79. Verbyla AP, Cullis BR, Thompson R (2007) The analysis of QTL by simultaneous use of the full linkage map. Theor Appl Genet 116:95–111CrossRefPubMedGoogle Scholar
  80. Williams KJ, Willsmore KL, Olson S et al (2006) Mapping of a novel QTL for resistance to cereal cyst nematode in wheat. Theor Appl Genet 112:1480–1486CrossRefPubMedGoogle Scholar
  81. Xue D, Huang Y, Zhang X et al (2009) Identification of QTLs associated with salinity tolerance at late growth stage in barley. Euphytica 169:187–196CrossRefGoogle Scholar
  82. Yeo AR, Yeo ME, Flowers SA et al (1990) Screening of rice genotypes for physiological characters contributing to salinity tolerance. Theor Appl Genet 79:377–384CrossRefGoogle Scholar
  83. Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421CrossRefGoogle Scholar
  84. Zarcinas BA, Cartwright B, Spouncer LR (1987) Nitric acid digestion and multi-element analysis of plant material by inductively coupled plasma spectrometry. Commun Soil Sci Plant Anal 18:131–146CrossRefGoogle Scholar
  85. Zhang GY, Guo Y, Chen S-L et al (1995) RFLP tagging of a salt tolerance gene in rice. Plant Sci 110:227–234CrossRefGoogle Scholar
  86. Zhu J-K, Liu J, Xiong L (1998) Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell 10:1181–1191CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Y. Genc
    • 1
    • 2
    Email author
  • K. Oldach
    • 1
    • 2
    • 3
  • A. P. Verbyla
    • 2
    • 4
  • G. Lott
    • 1
    • 2
  • M. Hassan
    • 3
  • M. Tester
    • 2
    • 5
  • H. Wallwork
    • 1
    • 3
  • G. K. McDonald
    • 1
    • 2
  1. 1.Molecular Plant Breeding Cooperative Research CentreUniversity of AdelaideGlen OsmondAustralia
  2. 2.School of Agriculture, Food and WineUniversity of AdelaideGlen OsmondAustralia
  3. 3.South Australian Research and Development InstituteGlen OsmondAustralia
  4. 4.Mathematics, Informatics and StatisticsCSIROGlen OsmondAustralia
  5. 5.Australian Centre for Plant Functional GenomicsUniversity of AdelaideGlen OsmondAustralia

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