HvNax3—a locus controlling shoot sodium exclusion derived from wild barley (Hordeum vulgare ssp. spontaneum)

Abstract

Previous work identified the wild barley (Hordeum vulgare ssp. spontaneum) accession CPI-71284-48 as being capable of limiting sodium (Na+) accumulation in the shoots under saline hydroponic growth conditions. Quantitative trait locus (QTL) analysis using a cross between CPI-71284-48 and a selection of the cultivated barley (H. vulgare ssp. vulgare) cultivar Barque (Barque-73, a moderate Na+ excluder) attributed the control of the Na+ exclusion trait from CPI-71284-48 to a single locus on the short arm of chromosome 7H, which was named HvNax3. The locus reduced shoot Na+ accumulation by 10–25% in plants grown in 150 mM NaCl. Markers generated using colinearity with rice and Brachypodium, together with the analysis of introgression lines and F2 and F3 families, enabled HvNax3 to be mapped to a 1.3-cM interval. Genes from the corresponding rice and Brachypodium intervals encode 16 different classes of proteins and include several plausible candidates for HvNax3. The potential of HvNax3 to provide a useful trait contributing to salinity tolerance in cultivated barley is discussed.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311:91–94

    Article  CAS  PubMed  Google Scholar 

  2. Bao AK, Wang SM, Wu GQ, Xi JJ, Zhang JL, Wang CM (2009) Overexpression of the Arabidopsis H+-PPase enhanced resistance to salt and drought stress in transgenic alfalfa (Medicago sativa L.). Plant Sci 176:232–240

    Article  CAS  Google Scholar 

  3. Bilgic H, Cho S, Garvin DF, Muehlbauer GJ (2007) Mapping barley genes to chromosome arms by transcript profiling of wheat–barley ditelosomic chromosome addition lines. Genome 50:898–906

    Article  CAS  PubMed  Google Scholar 

  4. Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218:683–692

    Article  CAS  PubMed  Google Scholar 

  5. Brini F, Hanin M, Mezghani I, Berkowitz GA, Masmoudi K (2007) Overexpression of wheat Na+/H+ antiporter TNHX1 and H+-pyrophosphatase TVP1 improve salt- and drought-stress tolerance in Arabidopsis thaliana plants. J Exp Bot 58:301–308

    Article  CAS  PubMed  Google Scholar 

  6. Byrt CS, Platten JD, Spielmeyer W, James RA, Lagudah ES, Dennis ES, Tester M, Munns R (2007) HKT1;5-like cation transporters linked to Na+ exclusion loci in wheat, Nax2 and Kna1. Plant Physiol 143:1918–1928

    Article  CAS  PubMed  Google Scholar 

  7. Caldwell KS, Russell J, Langridge P, Powell W (2006) Extreme population-dependent linkage disequilibrium detected in an inbreeding plant species, Hordeum vulgare. Genetics 172:557–567

    Article  CAS  PubMed  Google Scholar 

  8. Carter C, Pan S, Zouhar J, Avila EL, Girke T, Raikhel NV (2004) The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpressed proteins. Plant Cell 16:3285–3303

    Article  CAS  PubMed  Google Scholar 

  9. Chen Z, Zhou M, Newman IA, Mendham NJ, Zhang G, Shabala S (2007) Potassium and sodium relations in salinised barley tissues as a basis of different salt tolerance. Funct Plant Biol 34:150–162

    Article  CAS  Google Scholar 

  10. Chen A, Baumann U, Fincher GB, Collins NC (2009) Flt-2L, a locus in barley controlling flowering time, spike density, and plant height. Funct Integr Genomics 9:243–254

    Article  CAS  PubMed  Google Scholar 

  11. Cheng H, Qin L, Lee S, Fu X, Richards DE, Cao D, Luo D, Harberd NP, Peng J (2004) Gibberellin regulated Arabidopsis floral development via suppression of DELLA protein function. Development 131:1055–1064

    Article  CAS  PubMed  Google Scholar 

  12. Chhipa BR, Lal P (1995) Na/K ratios as the basis of salt tolerance in wheat. Aust J Agric Res 46:533–539

    Article  Google Scholar 

  13. Colmer TD, Munns R, Flowers TJ (2005) Improving salt tolerance of wheat and barley: future prospects. Aust J Agric Res 45:1425–1443

    Article  CAS  Google Scholar 

  14. Colmer TD, Flowers TJ, Munns R (2006) Use of wild relatives to improve salt tolerance in wheat. J Exp Bot 57:1059–1078

    Article  CAS  PubMed  Google Scholar 

  15. Doerks T, Huber S, Buchner E, Bork P (2002) BSD: a novel domain in transcription factors and synapse-associated proteins. Trends Biochem Sci 27:168–170

    Article  CAS  PubMed  Google Scholar 

  16. Drader T, Johnson K, Brueggeman R, Kudrna D, Kleinhofs A (2009) Genetic and physical mapping of a high recombination region on chromosome 7H(1) in barley. Theor Appl Genet 118:811–820

    Article  CAS  PubMed  Google Scholar 

  17. Dubcovsky J, Santa Maria G, Epstein E, Luo MC, Dvořák J (1996) Mapping of the K+/Na+ discrimination locus Kna1 in wheat. Theor Appl Genet 92:448–454

    Article  CAS  Google Scholar 

  18. Eglinton JK, Jefferies SP, Ceccarelli S, Grando S, McDonald G, Barr AR (2000) A comparative assessment of osmotic adjustment and oxidative stress responses in Hordeum vulgare ssp. spontaneum. In: Proceedings of the 8th International Barley Genetics Symposium, Adelaide, pp 267–269

  19. Eglinton JK, Coventry SJ, Mather DE, Kretschmer J, McMichael GL, Chalmers KJ (2004) Advanced backcross QTL analysis in barley. In: Proceedings of the 9th International Barley Genetics Symposium, Brno, Czech Republic, p 65, http://www.ibgs.cz/

  20. Ellis RP, Forster BP, Waugh R, Bonar N, Handley LL, Robinson D, Gordon DC, Powell W (1997) Mapping physiological traits in barley. New Phytol 137:149–157

    Article  CAS  Google Scholar 

  21. Ellis RP, Forster BP, Robinson D, Handley LL, Gordon DC, Russell JR, Powell W (2000) Wild barley: a source of genes for crop improvement in the 21st century? J Exp Bot 51:9–17

    Article  CAS  PubMed  Google Scholar 

  22. Ellis RP, Forster BP, Gordon DC, Handley LL, Keith RP, Lawrence P, Meyer R, Powell W, Robinson D, Scrimgeour CM, Young G, Thomas WTB (2002) Phenotype/genotype association for yield and salt tolerance in an barley mapping population segregating for two dwarfing genes. J Exp Bot 53:1163–1176

    Article  CAS  PubMed  Google Scholar 

  23. Eudes A, Mouille G, Thévenin J, Goyallon A, Minic Z, Jouanin L (2008) Purification, cloning and functional characterization of an endogenous beta-glucuronidase in Arabidopsis thaliana. Plant Cell Physiol 49:1331–1341

    Article  CAS  PubMed  Google Scholar 

  24. Ezawa S, Tada Y (2009) Identification of salt tolerance genes from the mangrove plant Bruguiera gymnorhiza using Agrobacterium functional screening. Plant Sci 176:272–278

    Article  CAS  Google Scholar 

  25. Forster BP (2001) Mutation genetics of salt tolerance in barley: an assessment of Golden Promise and other semi-dwarf mutants. Euphytica 120:317–328

    Article  CAS  Google Scholar 

  26. Forster BP, Miller TE, Law CN (1988) Salt tolerance of two wheat—Agropyron junceum disomic addition lines. Genome 30:559–564

    Google Scholar 

  27. Forster BP, Phillips MS, Miller TE, Baird E, Powell W (1990) Chromosome location of genes controlling tolerance to salt (NaCl) and vigour in Hordeum vulgare and H. chilense. Heredity 65:99–107

    Article  Google Scholar 

  28. Forster BP, Russell JR, Ellis RP, Handley LL, Robinson D, Hackett CA, Nevo E, Waugh R, Gordon DC, Keith R, Powell W (1997) Locating genotypes and genes for abiotic stress tolerance in barley: a strategy using maps, markers and the wild species. New Phytol 137:141–147

    Article  Google Scholar 

  29. Fu H, Girod PA, Doelling JH, van Nocker S, Hochstrasser M, Finley D, Vierstra RD (1999) Structure and functional analyses of the 26S proteasome subunits from plants. Mol Biol Reports 26:137–146

    Article  CAS  Google Scholar 

  30. Fukuda A, Chiba K, Maeda M, Nakamura A, Maeshima M, Tanaka Y (2004) Effect of salt and osmotic stresses on the expression of genes for the vacuolar H+-pyrophosphatase, H+-ATPase subunit A, and Na+/H+ antiporter from barley. J Exp Bot 55:585–594

    Article  CAS  PubMed  Google Scholar 

  31. Gao F, Gao Q, Duan XG, Yue GD, Yang AF, Zhang JR (2006) Cloning of an H+-PPase gene from Thellungiella halophila and its heterologous expression to improve tobacco salt tolerance. J Exp Bot 57:3259–3270

    Article  CAS  PubMed  Google Scholar 

  32. Garthwaite AJ, von Bothmer R, Colmer TD (2005) Salt tolerance in wild Hordeum species is associated with restricted entry of Na+ and Cl into the shoots. J Exp Bot 56:2365–2378

    Article  CAS  PubMed  Google Scholar 

  33. Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR (2001) Drought- and salt-tolerant plants results from overexpression of the AVP1 H+-pump. Proc Natl Acad Sci USA 98:11444–11449

    Article  CAS  PubMed  Google Scholar 

  34. Genc Y, McDonald G, Tester M (2007) Reassessment of tissue Na+ concentration as a criterion for salinity tolerance in bread wheat. Plant Cell Environ 30:1486–1498

    Article  CAS  PubMed  Google Scholar 

  35. Gorham J, Hardy C, Wyn Jones RG, Joppa LR, Law CN (1987) Chromosomal localisation of a K/Na discrimination character in the D genome of wheat. Theor Appl Genet 74:584–588

    Article  CAS  Google Scholar 

  36. Gorham J, Bristol A, Young EM, Wyn Jones RG, Kashour G (1990) Salt tolerance in the Triticeae: K/Na discrimination in barley. J Exp Bot 41:1095–1101

    Article  CAS  Google Scholar 

  37. Guo S, Yin H, Zhang X, Zhao F, Li P, Chen S, Zhao Y, Zhang H (2006) Molecular cloning and characterization of a vacuolar H+-pyrophosphatase gene, SsVP, from the halophyte Suaeda salsa and its overexpression increases salt and drought tolerance of Arabidopsis. Plant Mol Biol 60:41–50

    Article  CAS  PubMed  Google Scholar 

  38. Hearnden PR, Eckermann PJ, McMichael GL, Hayden MJ, Eglinton JK, Chalmers KJ (2007) A genetic map of 1, 000 SSR and DArT markers in a wide barley cross. Theor Appl Genet 115:383–391

    Article  CAS  PubMed  Google Scholar 

  39. Holstein SHE, Oliviusson P (2005) Sequence analysis of Arabidopsis thaliana E/ANTH-domain-containing proteins: membrane tethers of the clathrin-dependent vesicle budding machinery. Protoplasma 226:13–21

    Article  CAS  PubMed  Google Scholar 

  40. Hossein KG, Kalavacharla V, Lazo GR, Hegstad J et al (2004) A chromosome bin map of 2148 expressed sequence tag loci of wheat homoelogous group 7. Genetics 168:687–699

    Article  CAS  Google Scholar 

  41. Huang S, Spielmeyer W, Lagudah ES, James RA, Platten JD, Dennis ES, Munns R (2006) A sodium transporter (HKT7) is a candidate for Nax1, a gene for salt tolerance in durum wheat. Plant Physiol 142:1718–1727

    Article  CAS  PubMed  Google Scholar 

  42. Huang S, Spielmeyer W, Lagudah ES, Munns R (2008) Comparative mapping of HKT genes in wheat, barley, and rice, key determinants of Na+ transport, and salt tolerance. J Exp Bot 59:927–937

    Article  CAS  PubMed  Google Scholar 

  43. Isla R, Royo A, Aragüés R (1997) Field screening of barley cultivars to soil salinity using a sprinkler and drip irrigation system. Plant Soil 197:105–117

    Article  CAS  Google Scholar 

  44. Jahn R, Lang T, Südhof TC (2003) Membrane fusion. Cell 112:519–533

    Article  CAS  PubMed  Google Scholar 

  45. James RA, Davenport RJ, Munns R (2006) Physiological characterization of two genes for Na+ exclusion in durum wheat, Nax1 and Nax2. Plant Physiol 142:1537–1547

    Article  CAS  PubMed  Google Scholar 

  46. Jensen JK, Sørensen SO, Harholt J, Geshi N, Sakuragi Y, Møller I, Zandleven J, Bernal AJ, Jensen NB, Sørensen C, Pauly M, Beldman G, Willats WGT, Scheller HV (2008) Identification of a xylogalacturonan xylosyltransferase involved in pectin biosynthesis in Arabidopsis. Plant Cell 20:1289–1302

    Article  CAS  PubMed  Google Scholar 

  47. Leshem Y, Melamed-Book N, Cagnac O, Ronen G, Nishri Y, Solomon M, Cohen G, Levine A (2006) Suppression of Arabidopsis vesicle-SNARE expression inhibited fusion of H2O2-containing vesicles with tonoplast and increased salt tolerance. Proc Natl Acad Sci USA 103:18008–18013

    Article  CAS  PubMed  Google Scholar 

  48. Levin JZ, de Framond AJ, Tuttle A, Bauer MW, Heifetz PB (2000) Methods of double-stranded RNA-mediated gene inactivation in Arabidopsis and their use to define an essential gene in methionine biosynthesis. Plant Mol Biol 44:759–775

    Article  CAS  PubMed  Google Scholar 

  49. Li X, Cordero I, Caplan J, Mølhøj M, Reiter WD (2004) Molecular analysis of 10 coding regions from Arabidopsis that are homologous to the MUR3 xyloglucan galactosyltransferase. Plant Physiol 134:940–950

    Article  CAS  PubMed  Google Scholar 

  50. 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 

  51. Lonergan PF, Pallotta MA, Lorimer M, Paull JG, Barker SJ, Graham RD (2009) Multiple genetic loci for zinc uptake and distribution in barley (Hordeum vulgare). New Phytol 184:168–179

    Article  CAS  PubMed  Google Scholar 

  52. Luo MC, Dubcovsky J, Goyal S, Dvořák J (1996) Engineering of interstitial foreign chromosome segments containing the K+/Na+ selectivity gene Kna1 by sequential homoeologous recombination in durum wheat. Theor Appl Genet 93:1180–1184

    Article  CAS  Google Scholar 

  53. Ma L, Zhou E, Huo N, Zhou R, Wang G, Jia J (2007) Genetic analysis of salt tolerance in a recombinant inbred population of wheat (Triticum aestivum L.). Euphytica 153:109–117

    Article  CAS  Google Scholar 

  54. Mahmood A, Quarrie SA (2006) Effects of salinity on growth, ionic relations and physiological traits of wheat, disomic addition lines from Thinopyrum bessarabicum, and two amphiploids. Plant Breed 110:265–276

    Article  Google Scholar 

  55. Manly KF, Cudmore JRH, Meer JM (2001) MapManager QTX cross-platform software for genetic mapping. Mammal Genome 12:930–932

    Article  CAS  Google Scholar 

  56. Mano Y, Takeda K (1997) Mapping quantitative trait loci for salt tolerance at germination and the seedling stage in barley (Hordeum vulgare L.). Euphytica 94:263–272

    Article  Google Scholar 

  57. Mano Y, Takeda K (1998) Genetic resources of salt tolerance in wild Hordeum species. Euphytica 103:137–141

    Article  Google Scholar 

  58. Møller IS, Gilliham M, Jha D, Mayo GM, Roy SJ, Coates JC, Haseloff J, Tester M (2009) Shoot Na+ exclusion and increased salinity tolerance engineering by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell. doi:10.1105/tpc.108.064568

    PubMed  Google Scholar 

  59. Mullan DJ, Colmer TD, Francki MG (2007) Arabidopsis–rice–wheat gene orthologues of Na+ transport and transcript analysis in wheat–L. elongatum aneuploids under salt stress. Mol Genet Genomics 277:199–212

    Article  CAS  PubMed  Google Scholar 

  60. Munns R, James RA (2003) Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant Soil 253:201–218

    Article  CAS  Google Scholar 

  61. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681

    Article  CAS  Google Scholar 

  62. Omielan JA, Epstein E, Dvořák J (1991) Salt tolerance and ionic relations of wheat as affected by individual chromosomes of salt-tolerant Lophopyrum elongatum. Genome 34:961–974

    Google Scholar 

  63. Pakniyat H, Handley LL, Thomas WTB, Connolly T, Macaulay M, Caligari PDS, Forster BP (1997a) Comparison of shoot dry weight, Na+ content and δ 13C values of ari-e and other semi-dwarf barley mutants under salt-stress. Euphytica 94:7–14

    Article  CAS  Google Scholar 

  64. Pakniyat H, Thomas WTB, Caligari PDS, Forster BP (1997b) Comparison of salt tolerance of GPert and non-GPert barleys. Plant Breed 116:189–191

    Article  CAS  Google Scholar 

  65. Pakniyat H, Powell W, Baird E, Handley LL, Robinson D, Scrimgeour CM, Hackett CA, Forster BP, Nevo E, Caligari PDS (1997c) AFLP variation in wild barley (Hordeum spontaneum C. Koch) with reference to salt tolerance and associated ecogeography. Genome 40:332–341

    Article  CAS  PubMed  Google Scholar 

  66. Pao SS, Paulsen IT, Saier MH (1998) Major facilitator superfamily. Microbiol Mol Biol Rev 62:1–34

    CAS  PubMed  Google Scholar 

  67. Park J, Kim MJ, Jung SJ, Suh MC (2009) Identification of a novel transcription factor, AtBSD1, containing a BSD domain in Arabidopsis thaliana. J Plant Biol 52:141–146

    Article  CAS  Google Scholar 

  68. Pickering R, Johnson PA (2005) Recent progress in barley improvement using wild species of Hordeum. Cytogenet Genome Res 109:344–349

    Article  CAS  PubMed  Google Scholar 

  69. Poustini K, Siosemardeh A (2004) Ion distribution in wheat cultivars in response to salinity stress. Field Crops Res 85:125–133

    Article  Google Scholar 

  70. Qi LL, Echalier B, Chao S, Lazo GR et al (2004) A chromosome bin map of 16, 000 expressed sequence tag loci and distribution of genes among the three genomes of polyploid wheat. Genetics 168:701–712

    Article  CAS  PubMed  Google Scholar 

  71. Qu Y, Egelund J, Gilson PR, Houghton F, Gleeson PA, Schultz CJ, Bacic A (2008) Identification of a novel group of putative Arabidopsis thaliana β-(1, 3)-galactosyltransferases. Plant Mol Biol 68:43–59

    Article  CAS  PubMed  Google Scholar 

  72. Quarrie SA, Steed A, Calestani C, Semikhodskii A, Lebreton C, Chinoy C, Steele N, Pljevjakusić W, Weyen J, Schondelmaier J, Habash DZ, Farmer P, Saker L, Clarkson DT, Abugalieva A, Yessimbekova M, Turuspekov Y, Abugalieva S, Tuberosa R, Sanguineti MC, Hollington PA, Aragués R, Royo A, Dodig D (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 110:865–880

    Article  CAS  PubMed  Google Scholar 

  73. Ramsay L, Macaulay M, degli Ivanissevich S, MacLean K, Cardle L, Fuller J, Edwards KJ, Tuvesson S, Morgante M, Massari A, Maestri E, Marmiroli N, Sjakste T, Ganal M, Powell W, Waugh R (2000) A simple sequence repeat-based linkage map of barley. Genetics 156:1997–2005

    CAS  PubMed  Google Scholar 

  74. Ren ZH, Gao JP, Li LG, Cai XL, Huang W, Chao DY, Zhu MZ, Wang ZY, Luan S, Lin HX (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nature Genet 17:1141–1146

    Article  CAS  Google Scholar 

  75. Rengasamy P (2006) World salinization with emphasis on Australia. J Exp Bot 57:1017–1023

    Article  CAS  PubMed  Google Scholar 

  76. Royo A, Aragüés R (1999) Salinity-yield response functions of barley genotypes assessed with a triple line source sprinkler system. Plant Soil 209:9–20

    Article  CAS  Google Scholar 

  77. Rus A, Baxter I, Muthukumar B, Gustin J, Lahner B, Yakubova E, Salt DE (2006) Natural variants of AtHKT1 enhance Na+ accumulation in two wild populations of Arabidopsis. PLoS Genet 2:1964–1973

    Article  CAS  Google Scholar 

  78. Russell J, Booth A, Fuller J, Harrower B, Hedley P, Machray G, Powell W (2004) A comparison of sequence-based polymorphism and haplotype content in transcribed and anonymous regions of the barley genome. Genome 47:389–398

    CAS  PubMed  Article  Google Scholar 

  79. Salse J, Bolot S, Throude M, Jouffe V, Piegu B, Quraischi UM, Calcagno T, Cooke R, Delseny M, Feuillet C (2008) Identification and characterization of shared duplications between rice and wheat provide new insight into grass genome evolution. Plant Cell 20:11–24

    Article  CAS  PubMed  Google Scholar 

  80. Shavrukov Y, Bowne J, Langridge P, Tester M (2006) Screening for sodium exclusion in wheat and barley. In: Proceedings of the 13th Australian Society of Agronomy Conference, Perth, http://www.regional.org.au/au/asa/2006/concurrent/environment/4581_shavrukoky.htm. Accessed 10 Sep 2006

  81. Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97:6896–6901

    Article  CAS  PubMed  Google Scholar 

  82. Stein N, Prasad M, Scholz U, Thiel T, Zhang H, Wolf M, Kota R, Varshney RK, Perovic D, Grosse I, Graner A (2007) A 1,000-loci transcript map of the barley genome: new anchoring points for integrative grass genomics. Theor Appl Genet 114:823–839

    Article  CAS  PubMed  Google Scholar 

  83. Stracke R, de Vos RCH, Bartelniewoehner L, Ishihara H, Sagasser M, Martens S, Weisshaar B (2009) Metabolomic and genetic analyses of flavonol synthesis in Arabidopsis thaliana support the in vivo involvement of leucoanthocyanidin dioxygenase. Planta 229:427–445

    Article  CAS  PubMed  Google Scholar 

  84. Tenhaken R, Doerks T, Bork P (2005) DCD—a novel plant specific domain in proteins involved in development and programmed cell death. BMC Bioinformatics 6:169. doi:10.1186/1471-2105-6-169

    Article  PubMed  CAS  Google Scholar 

  85. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Article  CAS  PubMed  Google Scholar 

  86. Uemura T, Ueda T, Ohniwa RL, Nakano A, Takeyasu K, Sato MH (2004) Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. Cell Struct Funct 29:49–65

    Article  CAS  PubMed  Google Scholar 

  87. Vincill ED, Szczyglowski K, Roberts DM (2005) GmN70 and LjN70. Anion transporters of the symbiosome membrane of nodules with a transport preference for nitrate. Plant Physiol 137:1435–1444

    Article  CAS  PubMed  Google Scholar 

  88. Wang MC, Peng ZY, Li CL, Li F, Liu C, Xia GM (2008) Proteomic analysis on a high salt tolerance introgression strain of Triticum aestivum/Thinopyrum ponticum. Proteomics 8:1470–1489

    Article  CAS  PubMed  Google Scholar 

  89. Woo HH, Jeong BR, Hirsch AM, Hawes MC (2007) Characterization of Arabidopsis AtUGT85A and AtGUS gene families and their expression in rapidly dividing tissues. Genomics 90:143–153

    Article  CAS  PubMed  Google Scholar 

  90. 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 

  91. Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, Sanchez A, Valarik M, Yasuda S, Dubcovsky J (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci U S A 103:19581–19586

    Article  CAS  PubMed  Google Scholar 

  92. Yan J, Chen G, Cheng J, Nevo E, Gutterman Y (2008) Phenotypic variation in caryopsis dormancy and seedling salt tolerance in wild barley, Hordeum spontaneum, from different habitats in Israel. Genet Resour Crop Evol 55:995–1005

    Article  Google Scholar 

  93. Yeo AR, Flowers TJ (1986) Salinity resistance in rice (Oryza sativa L.) and a pyramiding approach to breeding varieties for saline soils. Aust J Plant Physiol 13:161–173

    Article  Google Scholar 

  94. Yuan Q, Ouyang S, Wang A, Zhu W, Maiti R, Lin H, Hamilton J, Haas B, Sultana R, Cheung F, Wortman J, Buell CR (2005) The Institute for Genomic Research Osa1 rice genome annotation database. Plant Physiol 138:18–26

    Article  CAS  PubMed  Google Scholar 

  95. Zhao FY, Zhang XJ, Li PH, Zhao YX, Zhang H (2006) Co-expression of the Suaeda salsa SsNHX1 and Arabidopsis AVP1 confer greater salt tolerance to transgenic rice than the single SsNHX1. Mol Breed. doi:10.1007/s11032-006-9005-6

    Google Scholar 

  96. Zhong GY, Dvorak J (1995) Chromosomal control of the tolerance of gradually and suddenly imposed salt stress in the Lophopyrum elongatum and wheat, Triticum aestivum L., genomes. Theor Appl Genet 90:229–236

    Article  Google Scholar 

Download references

Acknowledgments

We thank Jason Eglinton, Stewart Coventry, and Julie Hayes for helpful discussions, Nilmini Dharmathilake and Anita Lapina for technical assistance, Jason Eglinton and Stewart Coventry for sharing unpublished data, the MPB-CRC for genetic resources, and codirectors of the Brachypodium Genome Sequencing Project for permission to use unpublished genomic sequence. This project was supported by a GRDC grant UA00090 to MT, a DBT grant (India) to NKG, research grant of the Institute of International Education (USA) to MNB, and by ARC, GRDC, and South Australian Government funding to ACPFG.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Yuri Shavrukov.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Shavrukov, Y., Gupta, N.K., Miyazaki, J. et al. HvNax3—a locus controlling shoot sodium exclusion derived from wild barley (Hordeum vulgare ssp. spontaneum). Funct Integr Genomics 10, 277–291 (2010). https://doi.org/10.1007/s10142-009-0153-8

Download citation

Keywords

  • Sodium transport
  • Barley
  • H. vulgare ssp. spontaneum
  • Salinity tolerance
  • Pyrophosphatase