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Identification of quantitative trait loci for ion homeostasis and salt tolerance in barley (Hordeum vulgare L.)

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Abstract

Ion homeostasis is considered to be one of the most important mechanisms underlying salt stress tolerance. We used the Steptoe × Morex barley doubled haploid population to screen for genetic variation in response to salinity stress at an early development stage in a hydroponics system, focusing on ion homeostasis. Salinity induced a strong adverse effect on growth of the parents and their derived population, with Steptoe as the more tolerant parent. Steptoe maintained higher concentrations of K+, Na+ and Cl− in the roots and a similar shoot/root ion ratio (<1) under stress conditions compared to control conditions. In contrast, Morex had higher concentrations of these ions in the shoots under stress and a doubled shoot/root ion ratio relative to control conditions, indicating that salt exclusion might contribute to the higher tolerance of Steptoe. Correlation and path analysis demonstrated that shoot Cl− contents most strongly affected salt tolerance and suggest that both Na+ and Cl− contents are important for salinity stress tolerance in barley. We identified 11 chromosomal regions involved in the control of the variation observed for salt tolerance and various salt stress response traits, including Na+, Cl− and K+ contents in shoots. Two specific regions on chromosomes 2H and 3H were found controlling ion contents and salt tolerance, pointing to genes involved in ion homeostasis that contribute to salt tolerance.

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References

  • Abel GH (1969) Inheritance of capacity for chloride inclusion and chloride exclusion by soybeans. Crop Sci 9(6):697

    Article  Google Scholar 

  • 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(4):1918–1928. doi:10.1104/pp.093476

    Article  PubMed  CAS  Google Scholar 

  • Chen F, Hayes PM (1989) A comparison of Hordeum bulbosum-mediated haploid production efficiency in barley using in vitro floret and tiller culture. Theor Appl Genet 77:701–704

    Google Scholar 

  • Chen Z, Newman I, Zhou M, Mendham N, Zhang G, Shabala S (2005) Screening plants for salt tolerance by measuring K + flux: a case study for barley. Plant, Cell Environ 28(10):1230–1246

    Article  CAS  Google Scholar 

  • Chen Z, Pottosin II, Cuin TA, Fuglsang AT, Tester M, Jha D, Zepeda-Jazo I, Zhou M, Palmgren MG, Newman IA, Shabala S (2007) Root plasma membrane transporters controlling K +/Na + homeostasis in salt-stressed barley. Plant Physiol 145(4):1714–1725. doi:10.1104/pp.107.110262

    Article  PubMed  CAS  Google Scholar 

  • Choi DW, Close TJ (2000) A newly identified barley gene, Dhn12 encoding a YSK2 DHN, is located on chromosome 6H and has embryo-specific expression. Theor Appl Genet 100(8):1274–1278

    Article  CAS  Google Scholar 

  • Close TJ, Bhat PR, Lonardi S, Wu Y, Rostoks N, Ramsay L, Druka A, Stein N, Svensson JT, Wanamaker S, Bozdag S, Roose ML, Moscou MJ, Chao S, Varshney RK, Szucs P, Sato K, Hayes PM, Matthews DE, Kleinhofs A, Muehlbauer GJ, DeYoung J, Marshall DF, Madishetty K, Fenton RD, Condamine P, Graner A, Waugh R (2009) Development and implementation of high-throughput SNP genotyping in barley. BMC Genomics 10:582

    Article  PubMed  Google Scholar 

  • Dewey DRLK (1959) A correlation and path coefficient analysis of components of crested wheatgrass seed production. Agron J 51:515–518

    Article  Google Scholar 

  • Dubcovsky J, Maria GS, Epstein E, Luo MC, Dvorak J (1996) Mapping of the K +/Na + discrimination locus Kna1 in wheat. Theor Appl Genet 92(3–4):448–454

    Article  CAS  Google Scholar 

  • 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(1):149–157

    Article  CAS  Google Scholar 

  • Ellis RP, Forster BP, Gordon DC, Handley LL, Keith RP, Lawrence P, Meyer R, Powell W, Robinson D, Scrimgeour CM, Young G, Thomas WT (2002) Phenotype/genotype associations for yield and salt tolerance in a barley mapping population segregating for two dwarfing genes. J Exp Bot 53(371):1163–1176

    Article  PubMed  CAS  Google Scholar 

  • FAO (2008) FAO land and plant nutrition management service. http://wwwfaoorg/ag/agl/agll/spush

  • Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55(396):307–319

    Article  PubMed  CAS  Google Scholar 

  • Flowers TJ, Hajibagheri MA (2001) Salinity tolerance in Hordeum vulgare: ion concentrations in root cells of cultivars differing in salt tolerance. Plant Soil 231(1):1–9

    Article  CAS  Google Scholar 

  • Garcia de Moral LF, Rharrabti Y, Elhani S, Martos V, Royo C (2005) Yield formation in Mediterranean durum wheat under two contrasting water regimes based on path-coefficient analysis. Euphytica 146:203–212

    Article  Google Scholar 

  • Genc Y, Oldach K, Verbyla AP, Lott G, Hassan M, Tester M, Wallwork H, McDonald GK (2010a) Sodium exclusion QTL associated with improved seedling growth in bread wheat under salinity stress. Theor Appl Genet 121(5):877–894. doi:10.1007/s00122-010-1357-y

    Article  PubMed  CAS  Google Scholar 

  • Genc Y, Tester M, McDonald GK (2010b) Calcium requirement of wheat in saline and non-saline conditions. Plant Soil 327(1–2):331–345. doi:10.1007/s11104-009-0057-3

    Article  CAS  Google Scholar 

  • Gorham J, Bridges J, Dubcovsky J, Dvorak J, Hollington PA, Luo MC, Khan JA (1997) Genetic analysis and physiology of a trait for enhanced K +/Na + discrimination in wheat. New Phytol 137(1):109–116

    Article  CAS  Google Scholar 

  • Greenway H, Munns R (1980) Mechanisms of salt tolerance in non-halophytes. Annu Rev Plant Physiol 31:149–190

    Article  CAS  Google Scholar 

  • Han F, Ullrich SE, Romagosa I, Clancy JA, Froseth JA, Wesenberg DM (2003) Quantitative genetic analysis of acid detergent fibre content in barley grain. J Cereal Sci 38(2):167–172. doi:10.1016/S0733-5210(03)00020-1

    Article  Google Scholar 

  • 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(4):552–565

    Article  CAS  Google Scholar 

  • Huang SB, 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(4):1718–1727. doi:10.1104/pp.106.088864

    Article  PubMed  CAS  Google Scholar 

  • 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(4):927–937. doi:10.1093/jxb/ern033

    Article  PubMed  CAS  Google Scholar 

  • Hui Z, Zhang ZB, Shao HB, Ping X, Foulkes MJ (2008) Genetic correlation and path analysis of transpiration efficiency for wheat flag leaves. Environ Exp Bot 64(2):128–134. doi:10.1016/j.envexpbot.2007.11.001

    Article  CAS  Google Scholar 

  • Isla R, Aragues R, Royo A (1998) Validity of various physiological traits as screening criteria for salt tolerance in barley. Field Crop Res 58(2):97–107

    Article  Google Scholar 

  • James RA, Davenport RJ, Munns R (2006a) Physiological characterization of two genes for Na + exclusion in durum wheat, Nax1 and Nax2. Plant Physiol 142(4):1537–1547

    Article  PubMed  CAS  Google Scholar 

  • James RA, Munns R, Von Caemmerer S, Trejo C, Miller C, Condon AG (2006b) Photosynthetic capacity is related to the cellular and subcellular partitioning of Na + , K + and Cl-salt-affected barley and durum wheat. Plant, Cell Environ 29:2185–2197

    Article  CAS  Google Scholar 

  • James RA, Blake C, Byrt CS, Munns R (2011) Major genes for Na + exclusion Nax1 and Nax2 (wheat HKT1;4 and HKT1;5) decrease Na + accumulation in bread wheat under saline and waterlogged conditions. J Exp Bot 62:2939–2947

    Article  PubMed  CAS  Google Scholar 

  • Kaneko T, Zhang WS, Takahashi H, Ito K, Takeda K (2001) QTL mapping for enzyme activity and thermostability of beta-amylase in barley (Hordeum vulgare L.). Breed Sci 51(2):99–105

    Article  CAS  Google Scholar 

  • Kleinhofs A, Kilian A, Maroof MAS, Biyashev RM, Hayes P, Chen FQ, Lapitan N, Fenwick A, Blake TK, Kanazin V, Ananiev E, Dahleen L, Kudrna D, Bollinger J, Knapp SJ, Liu B, Sorrells M, Heun M, Franckowiak JD, Hoffman D, Skadsen R, Steffenson BJ (1993) A molecular, isozyme and morphological map of the barley (Hordeum vulgare) genome. Theor Appl Genet 86(6):705–712

    Article  CAS  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(1):406–422

    Article  PubMed  CAS  Google Scholar 

  • Lee SY, Ahn JH, Cha YS, Yun DW, Lee MC, Ko JC, Lee KS, Eun MY (2006) Mapping of quantitative trait loci for salt tolerance at the seedling stage in rice. Mol Cell 21(2):192–196

    CAS  Google Scholar 

  • Ligaba A, Katsuhara M (2010) Insights into the salt tolerance mechanism in barley (Hordeum vulgare) from comparisons of cultivars that differ in salt sensitivity. J Plant Res 123(1):105–118. doi:10.1007/s10265-009-0272-2

    Article  PubMed  CAS  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(2):253–260. doi:10.1007/s00122-003-1421-y

    Article  PubMed  CAS  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(11):1105–1114. doi:10.1071/Fp04111

    Article  CAS  Google Scholar 

  • Liu JP, Zhu JK (1998) A calcium sensor homolog required for plant salt tolerance. Science 280(5371):1943–1945

    Article  PubMed  CAS  Google Scholar 

  • Maas EV, Hoffman GJ (1977) Crop salt tolerance-current assessment. J Irrig Drain 103(IR2):115–134

    Google Scholar 

  • 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(3):263–272

    Article  Google Scholar 

  • Mano Y, Nakazumi H, Takeda K (1996) Varietal variation in and effects of some major genes on salt tolerance at the germination stage in barley. Breed Sci 46:227–233

    Google Scholar 

  • Mather DE (1995) Base maps of NABGMP crosses. http://gnome.agrenv.mcgill.ca/info/basemaps.htm

  • Munns R, Rawson HM (1999) Effect of salinity on salt accumulation and reproductive development in the apical meristem of wheat and barley. Aust J Plant Physiol 26(5):459–464

    Article  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. doi:10.1146/annurev.arplant.59.032607.092911

    Article  PubMed  CAS  Google Scholar 

  • Munns R, Husain S, Rivelli AR, James RA, Condon AG, Lindsay MP, Lagudah ES, Schachtman DP, Hare RA (2002) Avenues for increasing salt tolerance of crops, and the role of physiologically based selection traits. Plant Soil 247(1):93–105

    Article  CAS  Google Scholar 

  • Munns R, James RA, Lauchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57(5):1025–1043. doi:10.1093/jxb/erj100

    Article  PubMed  CAS  Google Scholar 

  • Munns R, James RA, Xu B, Athman A, Conn SJ, Jordans C, Byrt CS, Hare RA, Tyerman SD, Tester M, Plett D, Gilliham M (2012) Wheat grain yield on saline soils is improved by an ancestral Na(+) transporter gene. Nat Biotechnol. doi:10.1038/nbt.2120

    PubMed  Google Scholar 

  • Rajendran K, Tester M, Roy SJ (2009) Quantifying the three main components of salinity tolerance in cereals. Plant, Cell Environ 32(3):237–249. doi:10.1111/j.1365-3040.2008.01916.x

    Article  CAS  Google Scholar 

  • 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. Nat Genet 37(10):1141–1146. doi:10.1038/Ng1643

    Article  PubMed  CAS  Google Scholar 

  • Rivandi J, Miyazaki J, Hrmova M, Pallotta M, Tester M, Collins NC (2011) A SOS3 homologue maps to HvNax4, a barley locus controlling an environmentally sensitive Na(+) exclusion trait. J Exp Bot 62:1201–1216

    Article  PubMed  CAS  Google Scholar 

  • Salvi S, Tuberosa R (2005) To clone or not to clone plant QTLs: present and future challenges. Trends Plant Sci 10(6):297–304

    Article  PubMed  CAS  Google Scholar 

  • Shabala SN, Shabala SI, Martynenko AI, Babourina O, Newman IA (1998) Salinity effect on bioelectric activity, growth, Na + accumulation and chlorophyll fluorescence of maize leaves: a comparative survey and prospects for screening. Aust J Plant Physiol 25(5):609–616

    Article  CAS  Google Scholar 

  • Shabala S, Cuin TA, Pang J, Percey W, Chen Z, Conn S, Eing C, Wegner LH (2010) Xylem ionic relations and salinity tolerance in barley. Plant J 61(5):839–853. doi:10.1111/j.1365-313X.2009.04110.x

    Article  PubMed  CAS  Google Scholar 

  • Shavrukov Y, Gupta NK, Miyazaki J, Baho MN, Chalmers KJ, Tester M, Langridge P, Collins NC (2010) HvNax3—a locus controlling shoot sodium exclusion derived from wild barley (Hordeum vulgare ssp. spontaneum). Funct Integr Genomics 10(2):277–291. doi:10.1007/s10142-009-0153-8

    Article  PubMed  CAS  Google Scholar 

  • Siahsar BA, Narouei M (2010) Mapping QTLs of physiological traits associated with salt tolerance in ‘Steptoe’x‘Morex’ doubled haploid lines of barley at seedling stage. J Food Agric Environ 8(2):751–759

    Google Scholar 

  • Silva P, Geros H (2009) Regulation by salt of vacuolar H + -ATPase and H + -pyrophosphatase activities and Na +/H + exchange. Plant Signal Behav 4(8):718–726

    Article  PubMed  CAS  Google Scholar 

  • Sirault XRR, James RA, Furbank RT (2009) A new screening method for osmotic component of salinity tolerance in cereals using infrared thermography. Funct Plant Biol 36(10–11):970–977. doi:10.1071/Fp09182

    Article  CAS  Google Scholar 

  • Storey R, Jones RGW (1978) Salt stress and comparative physiology in gramineae. I-Ion relations of two salt and water stressed barley cultivars, California Mariout and Arimar. Aust J Plant Physiol 5:801–816

    Google Scholar 

  • Tavakkoli E, Rengasamy P, McDonald GK (2010) The response of barley to salinity stress differs between hydroponic and soil systems. Funct Plant Biol 37(7):621–633. doi:10.1071/Fp09202

    Article  Google Scholar 

  • Tavakkoli E, Fatehi F, Coventry S, Rengasamy P, McDonald GK (2011) Additive effects of Na + and Cl- ions on barley growth under salinity stress. J Exp Bot 62(6):2189–2203. doi:10.1093/Jxb/Erq422

    Article  PubMed  CAS  Google Scholar 

  • Teakle NL, Tyerman SD (2010) Mechanisms of Cl- transport contributing to salt tolerance. Plant, Cell Environ 33(4):566–589. doi:10.1111/j.1365-3040.2009.02060.x

    Article  CAS  Google Scholar 

  • Van Ooijen JW (2009) MapQTL6, software for the mapping of quantitative trait loci in experimental populations of diploid species. Kyazma BV, Wageningen

    Google Scholar 

  • Verhoeven KJ, Biere A, Nevo E, van Damme JM (2004) Differential selection of growth rate-related traits in wild barley, Hordeum spontaneum, in contrasting greenhouse nutrient environments. J Evol Biol 17(1):184–196

    Article  PubMed  CAS  Google Scholar 

  • Volis S, Verhoeven KJ, Mendlinger S, Ward D (2004) Phenotypic selection and regulation of reproduction in different environments in wild barley. J Evol Biol 17(5):1121–1131. doi:10.1111/j.1420-9101.2004.00738.xJEB738

    Article  PubMed  CAS  Google Scholar 

  • Volkov V, Amtmann A (2006) Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, has specific root ion-channel features supporting K +/Na + homeostasis under salinity stress. Plant J 48:342–353

    Article  PubMed  CAS  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78

    Article  PubMed  CAS  Google Scholar 

  • Walia H, Wilson C, Wahid A, Condamine P, Cui X, Close TJ (2006) Expression analysis of barley (Hordeum vulgare L.) during salinity stress. Funct Integr Genomics 6(2):143–156. doi:10.1007/s10142-005-0013

    Article  PubMed  CAS  Google Scholar 

  • Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Close TJ (2007) Large-scale expression profiling and physiological characterization of jasmonic acid-mediated adaptation of barley to salinity stress. Plant, Cell Environ 30(4):410–421. doi:10.1111/j.1365-3040.2006.01628.x

    Article  CAS  Google Scholar 

  • White PJ, Broadley MR (2001) Chloride in soils and its uptake and movement within the plant: a review. Ann Bot 88(6):967–988. doi:10.1006/anbo.2001.1540

    Article  CAS  Google Scholar 

  • Witzel K, Weidner A, Surabhi GK, Borner A, Mock HP (2009) Salt stress-induced alterations in the root proteome of barley genotypes with contrasting response towards salinity. J Exp Bot 60(12):3545–3557. doi:10.1093/Jxb/Erp198

    Article  PubMed  CAS  Google Scholar 

  • Witzel K, Weidner A, Surabhi GK, Varshney RK, Kunze G, Buck-Sorlin GH, Borner A, Mock HP (2010) Comparative analysis of the grain proteome fraction in barley genotypes with contrasting salinity tolerance during germination. Plant, Cell Environ 33(2):211–222. doi:10.1111/j.1365-3040.2009.02071

    Article  CAS  Google Scholar 

  • Xue DW, Huang YZ, Zhang XQ, Wei K, Westcott S, Li CD, Chen MC, Zhang GP, Lance R (2009) Identification of QTLs associated with salinity tolerance at late growth stage in barley. Euphytica 169(2):187–196. doi:10.1007/s10681-009-9919-2

    Article  Google Scholar 

  • Zhou GF, Johnson P, Ryan PR, Delhaize E, Zhou MX (2012) Quantitative trait loci for salinity tolerance in barley (Hordeum vulgare L.). Mol Breed 29:427–436

    Article  CAS  Google Scholar 

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Acknowledgments

This work was financially supported by the Ministry of EL&I, The Netherlands and the Vietnamese Ministry of Education. The expert assistance of Geurt Versteeg in the greenhouse is gratefully acknowledged.

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  1. Graduate School Experimental Plant Sciences, Wageningen UR Plant Breeding, Wageningen University and Research Centre (WUR), PO Box 386, 6700 AJ, Wageningen, The Netherlands

    Viet Long Nguyen

  2. Wageningen UR Plant Breeding, Wageningen University and Research Centre (WUR), PO Box 386, 6700 AJ, Wageningen, The Netherlands

    Viet Long Nguyen, Simon A. Ribot, Oene Dolstra, Rients E. Niks, Richard G. F. Visser & C. Gerard van der Linden

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  1. Viet Long Nguyen
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  2. Simon A. Ribot
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Correspondence to C. Gerard van der Linden.

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11032_2012_9777_MOESM1_ESM.doc

Ion contents in shoot (a) and in root (b) of Steptoe, Morex and the mean of the derived DH population. Ion contents were measured from pooled samples of four replications grown in two environments, viz. control (C) and salt stress (S). Shoot and root cation (Na+, K+, Mg2+ and Ca2+), anion (Cl−; PO4 3− and SO4 2−) and total ion content (sum of all studied cation and anion) ratio of Steptoe (St), Morex (Mx) and DH population mean (c). (DOC 157 kb)

11032_2012_9777_MOESM2_ESM.xls

Coefficient of correlations for the traits under both control and stress condition grown for 3 weeks on hydroponics (XLS 58 kb)

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Nguyen, V.L., Ribot, S.A., Dolstra, O. et al. Identification of quantitative trait loci for ion homeostasis and salt tolerance in barley (Hordeum vulgare L.). Mol Breeding 31, 137–152 (2013). https://doi.org/10.1007/s11032-012-9777-9

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