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Plant and Soil

, Volume 407, Issue 1–2, pp 217–230 | Cite as

Induced growth promotion and higher salt tolerance in the halophyte grass Puccinellia tenuiflora by beneficial rhizobacteria

  • Shu-Qi Niu
  • Hui-Ru Li
  • Paul W. Paré
  • Mina Aziz
  • Suo-Min Wang
  • Huazhong Shi
  • Jing Li
  • Qing-Qing Han
  • Shi-Qian Guo
  • Jian Li
  • Qiang Guo
  • Qing Ma
  • Jin-Lin Zhang
Regular Article

Abstract

Background and Aims

Soil salinization limits conventional agriculture since most food-based plant cultivars require low soil-sodium (Na+) levels for robust growth. Moreover, modern agricultural practices, especially in arid environments, can exacerbate soil salinization as belowground water sources utilized in irrigation are frequently tainted with salt. While salt tolerance has previously been shown to be augmented in several glycophyte species by the soil bacterium Bacillus subtilis (GB03), here we reported that this beneficial rhizobacterium promotes growth and augments higher salt-tolerance in halophyte grass Puccinellia tenuiflora.

Methods

The optimal Bacillus subtilis strain for P. tenuiflora was screened. P. tenuiflora was grown from seeds with NaCl (0, 100, 200 and 300 mM) for salt treatments with or without inoculation of B. subtilis GB03. Growth parameters, chlorophyll content and endogenous Na+ and K+ contents were determined at the time of harvest. Seedlings were grown in medium with 0 or 200 mM NaCl, then were harvested to extract total RNA after 48 h of exposure to GB03 VOCs. Semi-quantitative RT-PCR was used to investigate the relative amount of PtHKT1;5, PtHKT2;1 and PtSOS1 in P. tenuiflora regulated by GB03.

Results

The optimal Bacillus subtilis strain for P. tenuiflora was GB03. GB03 significantly improved shoot and root growth at two, three, four and five weeks after inoculation. Under various salinity stresses, GB03 significantly promoted growth of P. tenuiflora seedlings. Na+ accumulation was reduced with K+ accumulation unaffected by GB03 exposure. Therefore, GB03 enhanced selective absorption capacity of P. tenuiflora for K+ over Na+ (SA) from media. Gene expression analysis demonstrated that GB03 up-regulated PtHKT1;5 and PtSOS1, but down-regulated PtHKT2;1 expression, specifically in roots when plants are grown under greatly-elevated salt conditions (200 mM NaCl).

Conclusions

Our results presented here established that B. subtilis GB03 promoted the growth and improved the salt tolerance and the selective absorption capacity for K+ over Na+ in the monocotyledonous halophyte P. tenuiflora to a higher level. Interestingly, GB03-triggered up-regulation of PtHKT1;5 and PtSOS1 and down-regulation of PtHKT2;1 in roots reduced Na+ transport from root to shoot as well as Na+ uptake in roots. This study provides the physiological and molecular evidence that application of selected bacteria to salt-tolerant Monocots can ameliorate deleterious effects of high soil saline toxicity.

Keywords

Puccinellia tenuiflora Growth promotion Inducible-salt tolerance Bacillus subtilis (GB03) HKT SOS1 

Notes

Acknowledgments

Authors thank the Responsible Editor and anonymous reviewers for their constructive suggestions on the manuscript. This work was supported by the National Basic Research Program of China (973 Program, grant No. 2014CB138701), the National Natural Science Foundation of China (grant No. 31172256 and 31222053), the Opening Foundation of State Key Laboratory of Grassland Agro-ecosystems (SKLGAE201505), the Fundamental Research Funds for the Central Universities (grant No. lzujbky-2014-m01 and lzujbky-2015-194) and the Scientific Research Project from State Ethnic Affairs Commission of China (14XBZ013).

Supplementary material

11104_2015_2767_MOESM1_ESM.docx (614 kb)
ESM (DOCX 613 kb)

References

  1. Ali Z, Park HC, Ali A, et al. (2012) TsHKT1;2, a HKT1 homolog from the extremophile Arabidopsis relative Thellungiella salsuginea, shows K+ specificity in the presence of NaCl. Plant Physiol 158(3):1463–1474PubMedPubMedCentralCrossRefGoogle Scholar
  2. Amtmann A, Sanders D (1999) Mechanism of Na+ uptake by plant cells. Adv Bot Res 29:75–112CrossRefGoogle Scholar
  3. Ardie SW, Xie L, Takahashi R, Liu S, Takano T (2009) Cloning of a high-affinity K+ transporter gene PutHKT2;1 from Puccinellia tenuiflora and its functional comparison with OsHKT2;1 from rice in yeast and Arabidopsis. J Exp Bot 60(12):3491–3502PubMedPubMedCentralCrossRefGoogle Scholar
  4. Barry CS (2009) The stay-green revolution: recent progress in deciphering the mechanisms of chlorophyll degradation in higher plants. Plant Sci 176(3):325–333CrossRefGoogle Scholar
  5. Belimov AA, Dodd IC, Hontzeas N, Theobald JC, Safronova VI, Davies WJ (2009) Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signalling. New Phytol 181(2):413–423PubMedCrossRefGoogle Scholar
  6. Berthomieu P, Conejero 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(9):2004–2014PubMedPubMedCentralCrossRefGoogle Scholar
  7. Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. BBA-Biomembranes 1465:140–151PubMedCrossRefGoogle Scholar
  8. Böhm J, Scherzer S, Shabala S, Krol E, Neher E, Mueller TD, Hedrich R (2015) Venus flytrap HKT1-type channel provides for prey sodium uptake into carnivorous plant without conflicting with electrical excitability. Mol Plant. doi: 10.1016/j.molp.2015.09.017 PubMedGoogle Scholar
  9. 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):1918–1928PubMedPubMedCentralCrossRefGoogle Scholar
  10. Byrt CS, Xu B, Krishnan M, et al. (2014) The Na+ transporter, TaHKT1;5-D, limits shoot Na+ accumulation in bread wheat. Plant J 80(3):516–526PubMedCrossRefGoogle Scholar
  11. Chao DY, Dilkes B, Luo H, Douglas A, Yakubova E, Lahner B, Salt DE (2013) Polyploids exhibit higher potassium uptake and salinity tolerance in Arabidopsis. Science 341(6146):658–659PubMedPubMedCentralCrossRefGoogle Scholar
  12. Cho SM, Kang BR, Han SH, Anderson AJ, Park JY, Lee YH, Cho BH, Yang KY, Ryu CM, Kim YC (2008) 2R, 3R-butanediol, a bacterial volatile produced by Pseudomonas chlororaphis O6, is involved in induction of systemic tolerance to drought in Arabidopsis thaliana. Mol Plant Microbe In 21(8):1067–1075CrossRefGoogle Scholar
  13. Davenport RJ, Munoz-Mayor A, Jha D, Essah PA, Rus A, Tester M (2007) The Na+ transporter AtHKT1;1 controls retrieval of Na+ from the xylem in Arabidopsis. Plant Cell Environ 30(4):497–507PubMedCrossRefGoogle Scholar
  14. de Zelicourta A, Al-Yousif M, Hirt H (2013) Rhizosphere microbes as essential partners for plant stress tolerance. Mol Plant 6(2):242–245CrossRefGoogle Scholar
  15. Earl AM, Losick R, Kolter R (2008) Ecology and genomics of Bacillus subtilis. Trends Microbiol 16(6):269–275PubMedPubMedCentralCrossRefGoogle Scholar
  16. Farag AM, Mayb T, Marty GD, Easton M, Harper DD, Little EE, Cleveland L (2006) The effect of chronic chromium exposure on the health of chinook salmon (Oncorhynchus tshawytscha). Aquat Toxicol 76(3–4):246–257PubMedCrossRefGoogle Scholar
  17. Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179(4):945–963PubMedCrossRefGoogle Scholar
  18. Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55(396):307–319PubMedCrossRefGoogle Scholar
  19. Gao S, Wu H, Wang W, Yang Y, Xie S, Xie Y, Gao X (2013) Efficient colonization and harpins mediated enhancement in growth and biocontrol of wilt disease in tomato by Bacillus subtilis. Lett Appl Microbiol 57(6):526–533PubMedCrossRefGoogle Scholar
  20. Gassmann W, Rubio F, Schroeder JI (1996) Alkali cation selectivity of the wheat root high-affinity potassium transporter HKT1. Plant J 10(5):869–882CrossRefGoogle Scholar
  21. Guo Q, Wang P, Ma Q, Zhang JL, Bao AK, Wang SM (2012) Selective transport capacity for K+ over Na+ is linked to the expression levels of PtSOS1 in halophyte Puccinellia tenuiflora. Funct Plant Biol 39(12):1047–1057CrossRefGoogle Scholar
  22. Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics 2014:701596PubMedPubMedCentralCrossRefGoogle Scholar
  23. Han QQ, Lü XP, Bai JP, et al. (2014) Beneficial soil bacterium Bacillus subtilis (GB03) augments salt tolerance of white clover. Front Plant Sci 5:525PubMedPubMedCentralGoogle Scholar
  24. Haro R, Banuelos MA, Senn ME, Barrero-Gil J, Rodriguez-Navarro A (2005) HKT1 mediates sodium uniport in roots. Pitfalls in the expression of HKT1 in yeast. Plant Physiol 139(3):1495–1506PubMedPubMedCentralCrossRefGoogle Scholar
  25. Harvey PR, Warren RA, Wakelin S (2009) Potential to improve root access to phosphorus: the role of non-symbiotic microbial inoculants in the rhizosphere. Crop Pasture Sci 60:144–151CrossRefGoogle Scholar
  26. Hill CB, Jha D, Bacic A, Tester M, Roessner U (2013) Characterization of ion contents and metabolic responses to salt stress of different Arabidopsis AtHKT1;1 genotypes and their parental strains. Mol Plant 6(2):350–368PubMedCrossRefGoogle Scholar
  27. Horie T, Costa A, Kim TH, Han MJ, Horie R, Leung HY, Miyao A, Hirochika H, An G, Schroeder JI (2007) Rice OsHKT2;1 transporter mediates large Na+ influx component into K+-starved roots for growth. Embo J 26(12):3003–3014PubMedPubMedCentralCrossRefGoogle Scholar
  28. Horie T, Hauser F, Schroeder JI (2009) HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trends Plant Sci 14(12):660–668PubMedPubMedCentralCrossRefGoogle Scholar
  29. Horie T, Yoshida K, Nakayama H, Yamada K, Oiki S, Shinmyo A (2001) Two types of HKT transporters with different properties of Na+ and K+ transport in Oryza sativa. Plant J 27(2):129–138PubMedCrossRefGoogle Scholar
  30. 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):927–937PubMedCrossRefGoogle Scholar
  31. 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(2):1718–1727PubMedPubMedCentralCrossRefGoogle Scholar
  32. 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 leaves under saline and waterlogged conditions. J Exp Bot 62(8):2939–2947PubMedCrossRefGoogle Scholar
  33. James RA, Davenport RJ, Munns R (2006) Physiological characterization of two genes for Na+ exclusion in durum wheat, Nax1 and Nax2. Plant Physiol 142(4):1537–1547PubMedPubMedCentralCrossRefGoogle Scholar
  34. Järvan M, Edesi L, Adamson A, Võsa T (2014) Soil microbial communities and dehydrogenase activity depending on farming systems. Plant Soil Environ 60:459–463Google Scholar
  35. Kader MA, Seidel T, Golldack D, Lindberg S (2006) Expressions of OsHKT1, OsHKT2, and OsVHA are differentially regulated under NaCl stress in salt-sensitive and salt-tolerant rice (Oryza sativa L.) cultivars. J Exp Bot 57(15):4257–4268PubMedCrossRefGoogle Scholar
  36. Katiyar-Agarwal S, Zhu J, Kim K, Agarwal M, Fu X, Huang A, Zhu JK (2006) The plasma membrane Na+/H+ antiporter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis. P Natl Acad Sci USA 103(49):18816–18821CrossRefGoogle Scholar
  37. Kloepper JW, Rodriguez-Kabana R, Zehnder GW, Murphy J, Sikora E, Fernandez C (1999) Plant root-bacterial interactions in biological control of soilborne diseases and potential extension to systemic and foliar diseases. Aust J Plant Physiol 28(1):21–26Google Scholar
  38. Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance and promotion of 61 plant growth by Bacillus spp. Phytopathology 94(11):1259–1266PubMedCrossRefGoogle Scholar
  39. Kronzucker HJ, Britto DT (2011) Sodium transport in plants: a critical review. New Phytol 189(1):54–81PubMedCrossRefGoogle Scholar
  40. Laurie S, Feeney KA, Maathuis FJ, Heard PJ, Brown SJ, Leigh RA (2002) A role for HKT1 in sodium uptake by wheat roots. Plant J 32(2):139–149PubMedCrossRefGoogle Scholar
  41. Lichtentthaler HK (1987) Chlorophyll and carotenoids: pigments of photosynthetic membranes. Methods Enzymol 148:350–382CrossRefGoogle Scholar
  42. 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):1105–1114CrossRefGoogle Scholar
  43. Liu M, Wang TZ, Zhang WH (2015) Sodium extrusion associated with enhanced expression of SOS1 underlies different salt tolerance between Medicago falcata and Medicago truncatula seedlings. Environ Exp Bot 110:46–55CrossRefGoogle Scholar
  44. Lunde C, Drew DP, Jacobs AK, Tester M (2007) Exclusion of Na+ via sodium ATPase (PpENA1) ensures normal growth of Physcomitrella patens under moderate salt stress. Plant Physiol 144(4):1786–1796PubMedPubMedCentralCrossRefGoogle Scholar
  45. Ma Q, Yue LJ, Zhang JL, Wu GQ, Bao AK, Wang SM (2012) Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum. Tree Physiol 32(1):1–3CrossRefGoogle Scholar
  46. Maathuis FJ, Ahmad I, Patishtan J (2014) Regulation of Na+ fluxes in plants. Front Plant Sci 5:467PubMedPubMedCentralCrossRefGoogle Scholar
  47. Martinez-Atienza J, Jiang X, Garciablades B, Mendoza I, Zhu JK, Pardo JM, Quinteo FJ (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143(2):1001–1012PubMedPubMedCentralCrossRefGoogle Scholar
  48. Mian A, Oomen RJFJ, Isayenkov S, Sentenac H, Maathuis FJM, Very AA (2011) Over-expression of a Na+- and K+-permeable HKT transporter in barley improves salt tolerance. Plant J 68(3):468–479PubMedCrossRefGoogle Scholar
  49. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefGoogle Scholar
  50. Munns R, James RA, Xu B, Athman A, Conn SJ, Gilliham M (2012) Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nat Biotechnol 30(4):360–366PubMedCrossRefGoogle Scholar
  51. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Plant Physiol 15(3):473–497CrossRefGoogle Scholar
  52. Myresiotis CK, Vryzas Z, Papadopoulou-Mourkidou E (2014) Effect of specific plant-growth-promoting rhizobacteria (PGPR) on growth and uptake of neonicotinoid insecticide thiamethoxam in corn (Zea mays L.) seedlings. Pest Manag Sci 71(9):1258–1266PubMedCrossRefGoogle Scholar
  53. Nautiyal CS, Srivastava S, Chauhan PS, Seem K, Mishra A, Sopory SK (2013) Plant growth-promoting bacteria Bacillus amyloliquefaciens NBRISN13 modulates gene expression profile of leaf and rhizosphere community in rice during salt stress. Plant Physiol Bioch 66:1–9CrossRefGoogle Scholar
  54. Oh DH, Gong QQ, Ulanov A, Zhang Q, Li YZ, Ma WY, Yun DJ, Bressan RA, Bohnert HJ (2007) Sodium stress in the halophyte Thellungiella halophila and transcriptional changes in a thsos1-RNA interference line. J Integr Plant Biol 49(10):1484–1496CrossRefGoogle Scholar
  55. Peng YH, Zhu YF, Mao YQ, Wang SM, Su WA, Tang ZC (2004) Alkali grass resists salt stress through high [K+] and an endodermis barrier to Na+. J Exp Bot 55(398):939–949PubMedCrossRefGoogle Scholar
  56. Platten JD, Cotsaftis O, Berthomieu P (2006) Nomenclature for HKT transporters, key determinants of plant salinity tolerance. Trends Plant Sci 11(8):372–374PubMedCrossRefGoogle Scholar
  57. Platten JD, Egdane JA, Ismail AM (2013) Salinity tolerance, Na+ exclusion and allele mining of HKT1;5 in Oryza sativa and O. glaberrima: many sources, many genes, one mechanism? BMC Plant Biol 13:32PubMedPubMedCentralCrossRefGoogle Scholar
  58. Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. P Natl Acad Sci USA 99(12):8436–8441CrossRefGoogle Scholar
  59. Rahnama A, James RA, Poustini K, Munns R (2010) Stomatal conductance as a screen for osmotic stress tolerance in durum wheat growing in saline soil. Funct Plant Biol 37(3):255–263CrossRefGoogle Scholar
  60. 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):1141–1146PubMedCrossRefGoogle Scholar
  61. Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotech 26:115–124PubMedCrossRefGoogle Scholar
  62. Rozema J, Flowers T (2008) Ecology. Crops for a salinized world. Science 322(5907):1478–1480PubMedCrossRefGoogle Scholar
  63. Rubio F, Gassmann W, Schroeder JI (1995) Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270(5242):1660–1663PubMedCrossRefGoogle Scholar
  64. Rus A, Yokoi S, Sharkhuu A, Reddy M, Lee BH, Matsumoto TK, Koiwa H, Zhu JK, Bressan RA, Hasegawa PM (2001) AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. P Natl Acad Sci USA 98(24):14150–14155CrossRefGoogle Scholar
  65. Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Paré PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. P Natl Acad Sci USA 100(8):4927–4932CrossRefGoogle Scholar
  66. Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134(3):1017–1026PubMedPubMedCentralCrossRefGoogle Scholar
  67. Schachtman DP, Schroeder JI (1994) Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature 370(6491):655–658PubMedCrossRefGoogle Scholar
  68. Shabala L, Cuin TA, Newman IA, Shabala S (2005) Salinity-induced ion flux patterns from the excised roots of Arabidopsis sos mutants. Planta 222(6):1041–1050PubMedCrossRefGoogle Scholar
  69. Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plantarum 133(4):651–669CrossRefGoogle Scholar
  70. Shabala S, Pottosin I (2014) Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance. Physiol Plantarum 151(3):257–279CrossRefGoogle Scholar
  71. Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. P Natl Acad Sci USA 97(12):6896–6901CrossRefGoogle Scholar
  72. Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long distance Na+ transport in plants. Plant Cell 14(2):465–477PubMedPubMedCentralCrossRefGoogle Scholar
  73. Shi HZ, Lee BH, Wu SJ, Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21(1):81–85PubMedCrossRefGoogle Scholar
  74. Song GC, Ryu CM (2013) Two volatile organic compounds trigger plant self-defense against a bacterial pathogen and a sucking insect in cucumber under open field conditions. Int J Mol Sci 14(5):9803–9819PubMedPubMedCentralCrossRefGoogle Scholar
  75. Stein T (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56(4):845–857PubMedCrossRefGoogle Scholar
  76. Sunarpi HT, Motoda J, Kubo M (2005) Enhanced salt tolerance mediated by AtHKT1 transporter induced Na+ unloading from xylem vessels to xylem parenchyma cells. Plant J 44(6):928–938PubMedCrossRefGoogle Scholar
  77. Teakle NL, Bazihizina N, Shabala S, Colmer TD, Barrett-Lennard EG, Rodrigo-Moreno A, Läuchli AE (2013) Differential tolerance to combined salinity and O2 deficiency in the halophytic grasses Puccinellia ciliata and Thinopyrum ponticum: the importance of K+ retention in roots. Environ Exp Bot 87:69–78CrossRefGoogle Scholar
  78. Wang CM, Zhang JL, Liu XS, Li Z, Wu GQ, Cai JY, Wang SM (2009) Puccinellia tenuiflora maintains a low Na+ level under salinity by limiting unidirectional Na+ influx resulting in a high selectivity for K+ over Na+. Plant Cell Environ 32(5):486–496PubMedCrossRefGoogle Scholar
  79. Wang SM, Zhao GQ, Gao YS, Tang ZC, Zhang CL (2004) Puccinellia tenuiflora exhibits stronger selectivity for K+ over Na+ than wheat. J Plant Nutr 27(10):1841–1857CrossRefGoogle Scholar
  80. Wang SM, Zhang JL, Flowers TJ (2007) Low-affinity Na+ uptake in the halophyte Suaeda maritima. Plant Physiol 145(2):559–571PubMedPubMedCentralCrossRefGoogle Scholar
  81. Wang SM, Zheng WJ, Ren JZ, Zhang CL (2002) Selectivity of various types of salt-resistant plants for K+ over Na+. J Arid Environ 52:457–472CrossRefGoogle Scholar
  82. Wu SJ, Ding L, Zhu JK (1996) SOS1, a genetic-locus essential for salt tolerance and potassium acquisition. Plant Cell 8(4):617–627PubMedPubMedCentralCrossRefGoogle Scholar
  83. Xie X, Zhang H, Paré PW (2009) Sustained growth promotion in Arabidopsis with long-term exposure to the beneficial soil bacterium Bacillus subtilis (GB03). Plant Signal Behav 4(10):948–953PubMedPubMedCentralCrossRefGoogle Scholar
  84. Yamaguchi T, Hamamoto S, Uozumi N (2013) Sodium transport system in plant cells. Front Plant Sci 4:410PubMedPubMedCentralCrossRefGoogle Scholar
  85. Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14(1):1–4PubMedCrossRefGoogle Scholar
  86. Yu J, Chen S, Zhao Q, Wang T, Yang C, Diaz C, Sun G, Dai S (2011) Physiological and proteomic analysis of salinity tolerance in Puccinellia tenuiflora. J Proteome Res 10(9):3852–3870PubMedCrossRefGoogle Scholar
  87. Zamani Babgohari M, Ebrahimie E, Niazi A (2014) In silico analysis of high affinity potassium transporter (HKT) isoforms in different plants. Aquat Biosyst 10:9PubMedPubMedCentralCrossRefGoogle Scholar
  88. Zhang H, Kim MS, Sun Y, Dowd SE, Shi H, Paré PW (2008a) Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol Plant Microbe In 21(6):737–744CrossRefGoogle Scholar
  89. Zhang H, Kim MS, KrishnamachariV (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226(4):839–851PubMedCrossRefGoogle Scholar
  90. Zhang H, Sun Y, Xie X, Kim MS, Dowd SE, Paré PW (2009) A soil bacterium regulates plant acquisition of iron via deficiency inducible mechanisms. Plant J 58(4):568–577PubMedCrossRefGoogle Scholar
  91. Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Paré PW (2008b) Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J 56(2):264–273PubMedCrossRefGoogle Scholar
  92. Zhang JL, Shi HZ (2013) Physiological and molecular mechanisms of plant salt tolerance. Photosynth Res 115(1):1–22PubMedCrossRefGoogle Scholar
  93. Zhang JL, Aziz M, Yao Q, et al. (2014) Soil microbe Bacillus subtilis (GB03) induces biomass accumulation and salt tolerance with lower sodium accumulation in wheat. Crop Pasture Sci 65(5):423–427CrossRefGoogle Scholar
  94. Zhang JL, Flowers TJ, Wang SM (2010) Mechanisms of sodium uptake by roots of higher plant. Plant Soil 326(1):45–60CrossRefGoogle Scholar
  95. Zhang JL, Wang SM, Flowers TJ (2013) Differentiation of low-affinity Na+ uptake pathways and kinetics of the effects of K+ on Na+ uptake in the halophyte Suaeda maritima. Plant Soil 368:629–640CrossRefGoogle Scholar
  96. Zhang N, Wu K, He X, et al. (2011) A new bioorganic fertilizer can effectively control banana wilt by strong colonization with Bacillus subtilis N11. Plant Soil 344(1):87–97CrossRefGoogle Scholar
  97. Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444(2):139–158PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Shu-Qi Niu
    • 1
  • Hui-Ru Li
    • 1
  • Paul W. Paré
    • 2
  • Mina Aziz
    • 2
  • Suo-Min Wang
    • 1
  • Huazhong Shi
    • 2
  • Jing Li
    • 1
  • Qing-Qing Han
    • 1
  • Shi-Qian Guo
    • 3
  • Jian Li
    • 1
  • Qiang Guo
    • 1
  • Qing Ma
    • 1
  • Jin-Lin Zhang
    • 1
    • 2
  1. 1.State Key Laboratory of Grassland Agro-Ecosystems, College of Pastoral Agriculture Science and TechnologyLanzhou UniversityLanzhouPeople’s Republic of China
  2. 2.Department of Chemistry and BiochemistryTexas Tech UniversityLubbockUSA
  3. 3.Gansu Provincial Agro-Water Saving and Soil Fertilizer StationLanzhouPeople’s Republic of China

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