Eurasian Journal of Soil Science

Volume 6, Issue 3, Jun 2017, Pages 216-225
DOI: 10.18393/ejss.289460
Stable URL: http://ejss.fess.org/10.18393/ejss.289460
Copyright © 2017 The authors and Federation of Eurasian Soil Science Societies



Sodium-resistant plant growth-promoting rhizobacteria isolated from a halophyte, Salsola grandis, in saline-alkaline soils of Turkey

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Kataoka,R., Güneri,E., Turgay ,O., Yaprak ,A., Sevilir,B., Başköse,I., 2017. Sodium-resistant plant growth-promoting rhizobacteria isolated from a halophyte, Salsola grandis, in saline-alkaline soils of Turkey. Eurasian J Soil Sci 6(3):216-225. DOI : 10.18393/ejss.289460
Kataoka,R.Güneri,E.Turgay ,O.,Yaprak ,A.Sevilir,B.,& Başköse,I. Sodium-resistant plant growth-promoting rhizobacteria isolated from a halophyte, Salsola grandis, in saline-alkaline soils of Turkey Eurasian Journal of Soil Science, 6(3):216-225. DOI : 10.18393/ejss.289460
Kataoka,R.Güneri,E.Turgay ,O.,Yaprak ,A.Sevilir,B., and ,Başköse,I."Sodium-resistant plant growth-promoting rhizobacteria isolated from a halophyte, Salsola grandis, in saline-alkaline soils of Turkey" Eurasian Journal of Soil Science, 6.3 (2017):216-225. DOI : 10.18393/ejss.289460
Kataoka,R.Güneri,E.Turgay ,O.,Yaprak ,A.Sevilir,B., and ,Başköse,I. "Sodium-resistant plant growth-promoting rhizobacteria isolated from a halophyte, Salsola grandis, in saline-alkaline soils of Turkey" Eurasian Journal of Soil Science,6(Jun 2017):216-225 DOI : 10.18393/ejss.289460
R,Kataoka.E,Güneri.O,Turgay .AE,Yaprak .B,Sevilir.I,Başköse "Sodium-resistant plant growth-promoting rhizobacteria isolated from a halophyte, Salsola grandis, in saline-alkaline soils of Turkey" Eurasian J. Soil Sci, vol.6, no.3, pp.216-225 (Jun 2017), DOI : 10.18393/ejss.289460
Kataoka,Ryota ;Güneri,Esra ;Turgay ,Oguz Can ;Yaprak ,Ahmet ;Sevilir,Bahar ;Başköse,Isa Sodium-resistant plant growth-promoting rhizobacteria isolated from a halophyte, Salsola grandis, in saline-alkaline soils of Turkey. Eurasian Journal of Soil Science, (2017),6.3:216-225. DOI : 10.18393/ejss.289460

How to cite

Kataoka, R., Güneri, E., Turgay , O., Yaprak , A., E. Sevilir, B., E. Başköse, I., E.2017. Sodium-resistant plant growth-promoting rhizobacteria isolated from a halophyte, Salsola grandis, in saline-alkaline soils of Turkey. Eurasian J. Soil Sci. 6(3): 216-225. DOI : 10.18393/ejss.289460

Author information

Ryota Kataoka , University of Yamanashi, Faculty of Life & Environmental Sciences, Department of Environmental Sciences, Takeda, Kofu, Yamanashi, Japan
Esra Güneri , Ankara University, Faculty of Agriculture Department of Soil Science and Plant Nutrition, Ankara, Turkey
Oguz Can Turgay , Ankara University, Faculty of Agriculture Department of Soil Science and Plant Nutrition, Ankara, Turkey Ankara, Turkey
Ahmet Yaprak , Ankara University, Faculty of Science Department of Biology, Ankara, Turkey
Bahar Sevilir , Ankara University, Faculty of Agriculture Department of Soil Science and Plant Nutrition, Ankara, Turkey
Isa Başköse , Ankara University, Faculty of Science Department of Biology, Ankara, Turkey

Publication information

Article first published online : 03 Feb 2017
Manuscript Accepted : 26 Jan 2017
Manuscript Received: 27 Sep 2016
DOI: 10.18393/ejss.289460
Stable URL: http://ejss.fesss.org/10.18393/ejss.289460

Abstract

Phytoremediation is an expanding field of research in environmental studies due to the benefits of its cost effectiveness and environmental friendliness. The use of this technology in saline and alkaline soils can be a promising approach because soil salinity inhibits crop growth and causes tremendous yield losses in many regions of the world, especially in arid and semi-arid regions. However, little is known about the plants that can be applicable in the phytoremediation of saline soils and role of their rhizobacteria in the phytoremediation processes. In this study, we examined sodium (Na) uptake by the halophyte Salsola grandis and screened Na resistant rhizobacteria inhabiting in an extremely saline soil environment. S. grandis could uptake Na at the value of 15447 mg·kg-1 and transported Na to stem and leaves from roots. We found that 50 out of the 131 strains were Na resistant and 8 out of these 50 strains contributed to the growth of S. grandis. Using 16S ribosomal RNA sequencing, we determined these eight strains to be within the genera Arthrobacter spp. and Bacillus spp. Moreover, four of the eight strains (A22, WP5, B14, AP20) showed traits of being both siderophore and indole-3-acetic acid producers. Therefore, these eight strains appear to be suitable candidates for plant growth-promoting rhizobacteria of S. grandis.

Keywords

Arthrobacter, Bacillus, phytoremediation, Salsola, salinity in soil

Corresponding author

References

Acuña, J.J., Jorquera, M.A., Martínez, O.A., Menezes−Blackburn, D., Fernández, M.T., Marschner, P., Greiner, R., Mora, M.L., 2011. Indole acetic acid and phytase activity produced by rhizosphere bacilli as affected by pH and metals. Journal of Soil Science and Plant Nutrition 11(3): 1-12.

Ahmad, F., Ahmad, I., Khan, M.S., 2006. Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiological Research 163(2): 173-181.

Ashraf, M., Hasnain, S., Berge, O., Mahmood, T., 2004. Inoculating wheat seedlings with exopolysaccharide-producing bacteria restricts sodium uptake and stimulates plant growth under salt stress. Biology and Fertility of Soils 40(3): 157–162.

Berendsen, R.L., Pieterse, C.M.J., Bakker, P.A.H.M., 2012. The rhizosphere microbiome and plant health. Trends in Plant Science 17: 478–486.

Chakraborty, N., Ghosh, R., Ghosh, S., Narula, K., Tayal, R., Datta, A., Chakraborty, S., 2013. Reduction of oxalate levels in tomato fruit and consequentmetabolic remodeling following overexpression of a fungal oxalate decarboxylase. Plant Physiology 162(1): 364–378.

Colla, G., Rouphael, Y., Fallovo, C., Cardarelli, M., Graifenberg, A., 2006. Use of Salsola soda as a companion plant to improve greenhouse pepper (Capsicum annuum) under saline conditions. New Zealand Journal of Crop and Horticultural Science 34(4): 283-290.

Forni, C., Riov, J., Grilli Caiola, M., Tel-Or, E., 1992. Indole-3-acetic acid (IAA) production by Arthrobacter species isolated from Azolla. Journal of General Microbiology 138(2): 377-381.

Freitag, H., Vural, M., Adigüzel, N., 1999. A remarkable new Salsola and some new records of Chenopodiaceae from Central Anatolia, Turkey. Willdenowia 29: 123-139.

Gadd, G.M., 2004. Microbial influence on metal mobility and application for bioremediation. Geoderma 122: 109–119.

Goswamia, D., Dhandhukiab, P., Patela, P., Thakker, J.N., 2014. Screening of PGPR from saline desert of Kutch: Growth promotion in Arachis hypogea by Bacillus licheniformis A2. Microbiological Research 169(1): 66-75.

Hanbo, Z., Changqun, D., Qiyong, S., Weimin, R., Tao, S., Lizhong, C., Zhiwei, Z., Bin, H., 2004. Genetic and physiological diversity of phylogenetically and geographically distinct groups of Arthrobacter isolated from lead–zinc mine tailings. FEMS Microbiology Ecology 49(2): 333-341.  

Hasanuzzaman, M.,Nahar, K., Alam, M.M., Bhowmik, P.C., Hossain, M.A., Rahman, M.M., Prasad, M.N.V., Ozturk, M., Fujita, M., 2014. Potential use of halophytes to remediate saline soils. BioMed Research International Volume 2014, Article ID 589341.

Henne, K.L., Nakatsu, C.H., Thompson, D.K., Konopka, A.E., 2009. High-level chromate resistance in Arthrobacter sp. strain FB24 requires previously uncharacterized accessory genes. BMC Microbiology 9: 199.

Hotchkiss, M., 1923. Studies on salt action: VI. The stimulating and ınhibitive effect of certain cations upon bacterial growth. Journal of Bacteriology 8: 141-62.

Jing, R.L., X.P. Chang, 2003. Genetic diversity in wheat (T. aestivum L.) germplasm resources with drought resistance. Acta Botany Boreal-Occident Sinica 23(3): 410-416.

Jukes, T. H., Cantor, C.R., 1969. Evolution of protein molecules. In: Mammalian protein metabolism. Vol. 3, Munro, H.N. (Ed.). Academic Press, New York, USA. pp. 21–213.

Kacar, B., İnal, A., 2010. Bitki Analizleri. Nobel Akademik Yayıncılık, Ankara, Turkey.  912s. [in Turkish]

Kendirli, B., Cakmak, B., Ucar, Y., 2005 Salinity in the Southeastern Anatolia project (GAP), Turkey: Issues and Options. Journal of Irrigation and Drainage Engineering 54(1): 115-122.

Lasat, M.M., 2002. Phytoextraction of toxic metals: a review of biological mechanisms. Journal of Environmental Quality 31(1): 109–120.

Liu, W., Hou, J., Wang, Q., Ding, L., Luo, Y., 2014. Isolation and characterization of plant growth-promoting rhizobacteria and their effects on phytoremediation of petroleum-contaminated saline-alkali soil. Chemosphere 117: 303-308.

Liu, W., Wang, Q., Hou, J., Tu, C., Luo, Y., Christie, P., 2016. Whole genome analysis of halotolerant and alkalotolerant plant growth-promoting rhizobacterium Klebsiella sp. D5A. Scientific Reports, 6: Article number: 26710.

Maimaiti, A., Iwanaga, F., Taniguchi, T., Hara, N., Matsuo, N., Mori, N., Yunus, Q., Yamanaka, N., 2012. Cation content of five halophytes growing in saline soil around Aiding Lake in the Turpan Basin, Xinjiang, China. Sand Dune Research 58: 95-102.

Maas, E.V., Hoffman, G.J., 1977. Crop salt tolerance – current assessment. Journal of the Irrigation and Drainage Division of the American Society of Civil Engineering 103(2): 115–134.

Megharaj, M., Avudainayagam, S., Naidu, R., 2003. Toxicity of hexavalent chromium and ıts reduction by bacteria isolated from soil contaminated with tannery waste. Current Microbiology 47(1): 51-54.

Munns, R., James, R.A., Läuchli, A., 2005. Approaches to increasing the salt tolerance of wheat and other cereals. Journal of Experimental Botany 57(5): 1025-1043.

Paul, D., Lade, H,. 2014. Plant-growth-promoting rhizobacteria to improve crop growth in saline soils: a review. Agronomy for Sustainable Development 34(4): 737–752.

Pikovskaya, R.I., 1948. Mobilization of phosphorus in soil in connection with the vital activity of some microbial species. Mikrobiologiya 17: 362-370.

Pérez-Miranda, S., Cabirol, N., George-Téllez, R., Zamudio-Rivera, L.S., Fernández, F.J., 2007. O-CAS, a fast and universal method for siderophore detection. Journal of Microbiological Methods 70(1): 127-131.

Qadir, M., Qureshi, R.H., Ahmad, N., 2002. Amelioration of calcareous saline sodic soils through phytoremediation and chemical strategies. Soil Use and Management 18(4): 381-385.

Qadir, M., Steffens, D., Yan, F., Schubert, S., 2003. Sodium removal from a calcareous saline–sodic soil through leaching and plant uptake during phytoremediation. Land Degradation and Development 14(3): 301-307.

Qadir, M., Oster, J.D., Schubert, S., Noble, A.D., Sahrawat, K.L., 2007. Phytoremediation of sodic and saline-sodic soils. Advances in Agronomy 96: 197-247.

Ravindrana, K.C., Venkatesana, K., Balakrishnana, V., Chellappana, K.P., Balasubramanian, T., 2007. Restoration of saline land by halophytes for Indian soils. Soil Biology and Biochemistry 39(10): 2661-2664.

Ruppel, S., Franken, P., and Witzel, K., 2013. Properties of the halophyte microbiome and their implications for plant salt tolerance. Functional Plant Biology 40: 940–951.

Sadeghi, A., Karimi, E., Dahaji, P.A., Javid, M.G., Dalvand, Y., Askari, H., 2012. Plant growth promoting activity of an auxin and siderophore producing isolate of Streptomyces under saline soil conditions. World Journal of Microbiology and Biotechnology 28(4): 1503–1509.

Saitou, N., Nei, M., 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4(4): 406–425.

Schwyn, B., Neilands, J.B., 1987. Universal chemical assay for the detection and determination of siderophores, Analytical Biochemistry 160(1): 47-56.

Siddikee, M.A., Chauhan, P.S., Anandham, R., Han, G-H, Sa, T., 2010. Isolation, characterization, and use for plant growth promotion under salt stress, of ACC deaminase-producing halotolerant bacteria derived from coastal soil. Journal of Microbiology Biotechnology 20(11): 1577–1584.

Siebert, S., Doll, P., Hoogeveen, J., Faures, J.-M., Frenken, K., Feick, S., 2005. Development and validation of the global map of irrigation areas. Hydrology and Earth System Sciences 9: 535-547.

Silver, S., 1996. Bacterial resistances to toxic metal ions – a review. Gene 179(1): 9-19.

Tundis, R., Loizzo, M.R., Bonesi, M., Menichini, F., Statti, G.A., Menichini, F., 2008. In vitro cytotoxic activity of Salsola oppositifolia Desf. (Amaranthaceae) in a panel of tumour cell lines. Zeitschrift für Naturforschung C 63(5-6): 347-354.

Turgay, O.C., Bilen, S., 2012. The role of plant growth-promoting rhixosphere bacteria in toxic metal extraction by Brassica spp. in the plant family Brassicaceae contribution towards phytoremediation. In: The plant family brassicaceae: contribution towards phytoremediation. Anjum, N.A., Ahmad, I., Pereira, M.E., Duarte, A.C., Umar, S., Khan, N.A. (Eds.). Springer, pp.213–238.

Upadhyay, S.K., Singh, D.P., Saikia, R., 2009. Genetic diversity of plant growth promoting rhizobacteria isolated from rhizospheric soil of wheat under saline condition. Current Microbiology 59(5): 489-496.

Upadhyay, S.K., Singh, J.S., Saxena, A.K., Singh, D.P., 2012. Impact of PGPR inoculation on growth and antioxidant status of wheat under saline conditions. Plant Biology, 14: 605–611.

USDA-ARS. 2005. George E. Brown Jr Salinity Laboratory, Riverside, CA, USA. Available at: http://www.ars.usda.gov/Services/docs.htm?docid=8908

Whiting, S.N., de Souza, M.P., Terry, N., 2001. Rhizosphere bacteria mobilize Zn for hyperaccumulation by Thlaspi caerulescens. Environmental Science & Technology 35(15): 3144–3150.

Zhu, J.K., 2001. Plant salt tolerance. Trends in Plant Science 6(2): 66-71.

Zuccarini, P., 2008. Ion uptake by halophytic plants to mitigate saline stress in Solanum lycopersicon L., and different effect of soil and water salinity. Soil and Water Research 3: 62–73.

Abstract

Phytoremediation is an expanding field of research in environmental studies due to the benefits of its cost effectiveness and environmental friendliness. The use of this technology in saline and alkaline soils can be a promising approach because soil salinity inhibits crop growth and causes tremendous yield losses in many regions of the world, especially in arid and semi-arid regions. However, little is known about the plants that can be applicable in the phytoremediation of saline soils and role of their rhizobacteria in the phytoremediation processes. In this study, we examined sodium (Na) uptake by the halophyte Salsola grandis and screened Na resistant rhizobacteria inhabiting in an extremely saline soil environment. S. grandis could uptake Na at the value of 15447 mg·kg-1 and transported Na to stem and leaves from roots. We found that 50 out of the 131 strains were Na resistant and 8 out of these 50 strains contributed to the growth of S. grandis. Using 16S ribosomal RNA sequencing, we determined these eight strains to be within the genera Arthrobacter spp. and Bacillus spp. Moreover, four of the eight strains (A22, WP5, B14, AP20) showed traits of being both siderophore and indole-3-acetic acid producers. Therefore, these eight strains appear to be suitable candidates for plant growth-promoting rhizobacteria of S. grandis.

Keywords: Arthrobacter, Bacillus, phytoremediation, Salsola, salinity in soil.

References

Acuña, J.J., Jorquera, M.A., Martínez, O.A., Menezes−Blackburn, D., Fernández, M.T., Marschner, P., Greiner, R., Mora, M.L., 2011. Indole acetic acid and phytase activity produced by rhizosphere bacilli as affected by pH and metals. Journal of Soil Science and Plant Nutrition 11(3): 1-12.

Ahmad, F., Ahmad, I., Khan, M.S., 2006. Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiological Research 163(2): 173-181.

Ashraf, M., Hasnain, S., Berge, O., Mahmood, T., 2004. Inoculating wheat seedlings with exopolysaccharide-producing bacteria restricts sodium uptake and stimulates plant growth under salt stress. Biology and Fertility of Soils 40(3): 157–162.

Berendsen, R.L., Pieterse, C.M.J., Bakker, P.A.H.M., 2012. The rhizosphere microbiome and plant health. Trends in Plant Science 17: 478–486.

Chakraborty, N., Ghosh, R., Ghosh, S., Narula, K., Tayal, R., Datta, A., Chakraborty, S., 2013. Reduction of oxalate levels in tomato fruit and consequentmetabolic remodeling following overexpression of a fungal oxalate decarboxylase. Plant Physiology 162(1): 364–378.

Colla, G., Rouphael, Y., Fallovo, C., Cardarelli, M., Graifenberg, A., 2006. Use of Salsola soda as a companion plant to improve greenhouse pepper (Capsicum annuum) under saline conditions. New Zealand Journal of Crop and Horticultural Science 34(4): 283-290.

Forni, C., Riov, J., Grilli Caiola, M., Tel-Or, E., 1992. Indole-3-acetic acid (IAA) production by Arthrobacter species isolated from Azolla. Journal of General Microbiology 138(2): 377-381.

Freitag, H., Vural, M., Adigüzel, N., 1999. A remarkable new Salsola and some new records of Chenopodiaceae from Central Anatolia, Turkey. Willdenowia 29: 123-139.

Gadd, G.M., 2004. Microbial influence on metal mobility and application for bioremediation. Geoderma 122: 109–119.

Goswamia, D., Dhandhukiab, P., Patela, P., Thakker, J.N., 2014. Screening of PGPR from saline desert of Kutch: Growth promotion in Arachis hypogea by Bacillus licheniformis A2. Microbiological Research 169(1): 66-75.

Hanbo, Z., Changqun, D., Qiyong, S., Weimin, R., Tao, S., Lizhong, C., Zhiwei, Z., Bin, H., 2004. Genetic and physiological diversity of phylogenetically and geographically distinct groups of Arthrobacter isolated from lead–zinc mine tailings. FEMS Microbiology Ecology 49(2): 333-341.  

Hasanuzzaman, M.,Nahar, K., Alam, M.M., Bhowmik, P.C., Hossain, M.A., Rahman, M.M., Prasad, M.N.V., Ozturk, M., Fujita, M., 2014. Potential use of halophytes to remediate saline soils. BioMed Research International Volume 2014, Article ID 589341.

Henne, K.L., Nakatsu, C.H., Thompson, D.K., Konopka, A.E., 2009. High-level chromate resistance in Arthrobacter sp. strain FB24 requires previously uncharacterized accessory genes. BMC Microbiology 9: 199.

Hotchkiss, M., 1923. Studies on salt action: VI. The stimulating and ınhibitive effect of certain cations upon bacterial growth. Journal of Bacteriology 8: 141-62.

Jing, R.L., X.P. Chang, 2003. Genetic diversity in wheat (T. aestivum L.) germplasm resources with drought resistance. Acta Botany Boreal-Occident Sinica 23(3): 410-416.

Jukes, T. H., Cantor, C.R., 1969. Evolution of protein molecules. In: Mammalian protein metabolism. Vol. 3, Munro, H.N. (Ed.). Academic Press, New York, USA. pp. 21–213.

Kacar, B., İnal, A., 2010. Bitki Analizleri. Nobel Akademik Yayıncılık, Ankara, Turkey.  912s. [in Turkish]

Kendirli, B., Cakmak, B., Ucar, Y., 2005 Salinity in the Southeastern Anatolia project (GAP), Turkey: Issues and Options. Journal of Irrigation and Drainage Engineering 54(1): 115-122.

Lasat, M.M., 2002. Phytoextraction of toxic metals: a review of biological mechanisms. Journal of Environmental Quality 31(1): 109–120.

Liu, W., Hou, J., Wang, Q., Ding, L., Luo, Y., 2014. Isolation and characterization of plant growth-promoting rhizobacteria and their effects on phytoremediation of petroleum-contaminated saline-alkali soil. Chemosphere 117: 303-308.

Liu, W., Wang, Q., Hou, J., Tu, C., Luo, Y., Christie, P., 2016. Whole genome analysis of halotolerant and alkalotolerant plant growth-promoting rhizobacterium Klebsiella sp. D5A. Scientific Reports, 6: Article number: 26710.

Maimaiti, A., Iwanaga, F., Taniguchi, T., Hara, N., Matsuo, N., Mori, N., Yunus, Q., Yamanaka, N., 2012. Cation content of five halophytes growing in saline soil around Aiding Lake in the Turpan Basin, Xinjiang, China. Sand Dune Research 58: 95-102.

Maas, E.V., Hoffman, G.J., 1977. Crop salt tolerance – current assessment. Journal of the Irrigation and Drainage Division of the American Society of Civil Engineering 103(2): 115–134.

Megharaj, M., Avudainayagam, S., Naidu, R., 2003. Toxicity of hexavalent chromium and ıts reduction by bacteria isolated from soil contaminated with tannery waste. Current Microbiology 47(1): 51-54.

Munns, R., James, R.A., Läuchli, A., 2005. Approaches to increasing the salt tolerance of wheat and other cereals. Journal of Experimental Botany 57(5): 1025-1043.

Paul, D., Lade, H,. 2014. Plant-growth-promoting rhizobacteria to improve crop growth in saline soils: a review. Agronomy for Sustainable Development 34(4): 737–752.

Pikovskaya, R.I., 1948. Mobilization of phosphorus in soil in connection with the vital activity of some microbial species. Mikrobiologiya 17: 362-370.

Pérez-Miranda, S., Cabirol, N., George-Téllez, R., Zamudio-Rivera, L.S., Fernández, F.J., 2007. O-CAS, a fast and universal method for siderophore detection. Journal of Microbiological Methods 70(1): 127-131.

Qadir, M., Qureshi, R.H., Ahmad, N., 2002. Amelioration of calcareous saline sodic soils through phytoremediation and chemical strategies. Soil Use and Management 18(4): 381-385.

Qadir, M., Steffens, D., Yan, F., Schubert, S., 2003. Sodium removal from a calcareous saline–sodic soil through leaching and plant uptake during phytoremediation. Land Degradation and Development 14(3): 301-307.

Qadir, M., Oster, J.D., Schubert, S., Noble, A.D., Sahrawat, K.L., 2007. Phytoremediation of sodic and saline-sodic soils. Advances in Agronomy 96: 197-247.

Ravindrana, K.C., Venkatesana, K., Balakrishnana, V., Chellappana, K.P., Balasubramanian, T., 2007. Restoration of saline land by halophytes for Indian soils. Soil Biology and Biochemistry 39(10): 2661-2664.

Ruppel, S., Franken, P., and Witzel, K., 2013. Properties of the halophyte microbiome and their implications for plant salt tolerance. Functional Plant Biology 40: 940–951.

Sadeghi, A., Karimi, E., Dahaji, P.A., Javid, M.G., Dalvand, Y., Askari, H., 2012. Plant growth promoting activity of an auxin and siderophore producing isolate of Streptomyces under saline soil conditions. World Journal of Microbiology and Biotechnology 28(4): 1503–1509.

Saitou, N., Nei, M., 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4(4): 406–425.

Schwyn, B., Neilands, J.B., 1987. Universal chemical assay for the detection and determination of siderophores, Analytical Biochemistry 160(1): 47-56.

Siddikee, M.A., Chauhan, P.S., Anandham, R., Han, G-H, Sa, T., 2010. Isolation, characterization, and use for plant growth promotion under salt stress, of ACC deaminase-producing halotolerant bacteria derived from coastal soil. Journal of Microbiology Biotechnology 20(11): 1577–1584.

Siebert, S., Doll, P., Hoogeveen, J., Faures, J.-M., Frenken, K., Feick, S., 2005. Development and validation of the global map of irrigation areas. Hydrology and Earth System Sciences 9: 535-547.

Silver, S., 1996. Bacterial resistances to toxic metal ions – a review. Gene 179(1): 9-19.

Tundis, R., Loizzo, M.R., Bonesi, M., Menichini, F., Statti, G.A., Menichini, F., 2008. In vitro cytotoxic activity of Salsola oppositifolia Desf. (Amaranthaceae) in a panel of tumour cell lines. Zeitschrift für Naturforschung C 63(5-6): 347-354.

Turgay, O.C., Bilen, S., 2012. The role of plant growth-promoting rhixosphere bacteria in toxic metal extraction by Brassica spp. in the plant family Brassicaceae contribution towards phytoremediation. In: The plant family brassicaceae: contribution towards phytoremediation. Anjum, N.A., Ahmad, I., Pereira, M.E., Duarte, A.C., Umar, S., Khan, N.A. (Eds.). Springer, pp.213–238.

Upadhyay, S.K., Singh, D.P., Saikia, R., 2009. Genetic diversity of plant growth promoting rhizobacteria isolated from rhizospheric soil of wheat under saline condition. Current Microbiology 59(5): 489-496.

Upadhyay, S.K., Singh, J.S., Saxena, A.K., Singh, D.P., 2012. Impact of PGPR inoculation on growth and antioxidant status of wheat under saline conditions. Plant Biology, 14: 605–611.

USDA-ARS. 2005. George E. Brown Jr Salinity Laboratory, Riverside, CA, USA. Available at: http://www.ars.usda.gov/Services/docs.htm?docid=8908

Whiting, S.N., de Souza, M.P., Terry, N., 2001. Rhizosphere bacteria mobilize Zn for hyperaccumulation by Thlaspi caerulescens. Environmental Science & Technology 35(15): 3144–3150.

Zhu, J.K., 2001. Plant salt tolerance. Trends in Plant Science 6(2): 66-71.

Zuccarini, P., 2008. Ion uptake by halophytic plants to mitigate saline stress in Solanum lycopersicon L., and different effect of soil and water salinity. Soil and Water Research 3: 62–73.



Eurasian Journal of Soil Science