The effect of plant growth promoting potentials of rhizosphere bacteria isolated from several halophytic species on vegetative growth and ionic content of wheat

Amini Hajiabadi, Alireza; Mosleh Arani, Asghar; Ghasemi, Someh; Rad, Mohammad Hadi; Shabazi, Shima; Etesami, Hassan

doi:10.52547/nbr.8.2.104

The effect of plant growth promoting potentials of rhizosphere bacteria isolated from several halophytic species on vegetative growth and ionic content of wheat

Authors

alireza Amini Hajiabadi ¹

Asghar Mosleh Arani ²

Someh Ghasemi ³

mohammad hadi Rad ⁴

Shima Shabazi ³

Hassan Etesami ⁵

¹ Central Office of Natural Resources & Watershed Management, Yazd, Iran

² Department of Environmental Sciences, Faculty of Natural Resources, Yazd University, Yazd, Iran

³ Department of Soil Sciences, Faculty of Natural Resources, Yazd University, Yazd, Iran

⁴ Forest and Rangeland Division, Yazd Agricultural and Natural Resource Research and Education Center, Yazd, Iran

⁵ Department of Soil Science, University of Tehran, Karaj, Iran

https://doi.org/10.52547/nbr.8.2.104

Abstract

Salinity stress is an important challenge for wheat production in the world. Plant growth promoting rhizosphere bacteria, isolated from halophytic plants, can increase the tolerance of crop plants to salinity by direct and indirect mechanisms. In this study, plant growth-promoting traits of bacterial strains (Bacillus safensis, Bacillus pumilus and Zhihengliuella halotolerans), isolated from the rhizosphere of several halophyte plants, were deterimined and their effects on some vegetative traits and ionic content of wheat plant irrigated with saline water ( 0.2, as control, 4, 8 and 16 dS/m) were measured. Result showed that all three bacteria were able to produce auxin, hydrogen cyanide, siderophore, 1-aminocyclopropane-1-carboxylic acid deaminase and soluble phosphate. The increase in salinity levels caused increase in the concentration of sodium and decrease in the concentration of potassium, calcium and phosphorus in wheat leaves, as well as decrease in stem length, shoot and root dry weight, root to shoot dry weight ratio and total biomass. In wheat plants irrigated with saline water and inoculated with the bacterial strains, sodium concentration decreased up to 17.7% and concentrations of potassium, calcium, phosphorus and potassium to sodium ratio increased up to 33, 25.7, 200.4 and 41%, respectively. The most efficient bacterium was found to be Z. halotolerans. All bacterial isolates also increased stem length, shoot and root dry weight, root to shoot dry weight ratio and total biomass by 17, 58.6, 137, 88 and 66 %, respectively. The results of this study showed that the plant growth-promoting bacteria of rangeland halophytic plants potentionally improve the growth indices of wheat plants in saline conditions. These results also showed that the rhizosphere of halophytic plants in rangelands can be a good source for the isolation of salinity-resistant bacteria to improve the resistance of wheat plants to salinity.

Keywords

Atriplex

Bacillus

morphology

plant promoting rhizosphere bacteria

seidlitzea

20.1001.1.24236330.1400.8.2.7.8

Agathokleous, E., Belz, E., Kitao, R.G., Koike, T. & Calabrese, E. 2019. Does the root to shoot ratio show a hormetic response to stress? An ecological and environmental perspective. Journal of Forestry Research 30: 1569-1580.
Akbari, A., Gharanjik, S., Koobaz, P. & Sadeghi, A. 2020. Plant growth promoting Streptomyces strains are selectively interacting with the wheat cultivars especially in saline conditions. Heliyon Journal 6: 34-45.
Alexander, D.B., & Zuberer, D.A. 1991. Use of Chrome Azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biology and Fertility of Soils 12: 39-45.
Alikhani, H.A., Etesami, H. & Mohammadi, L. 2018. Evaluation of the effect of rhizospheric and non-rhizospheric phosphate solubilizing bacteria on improving the growth indices of wheat under salinity and drought Stress. Journal of Soil Biology 6: 1-15. (In Persian).
Al-Karaki, G.N. 2000. Growth, sodium and potassium uptake and translocation in salt stressed tomato. Journal of Plant Nutrition 23: 369-379.
Alori, E.T., Glick, B.R. & Babalola, O.O. 2017. Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Frontiers in Microbiology 8: 971-984.
Amini Hajiabadi, A., Mosleh Arani, A., Ghasemi, S., Rad, M.H., Etesami, H., Shabazi Manshadi, S., & Dolati, A. 2021.Mining the rhizosphere of halophytic rangeland plants for halotolerant bacteria to improve growth and yield of salinity-stressed wheat. Plant Physiology and Biochemistry 163: 139-153.
Amna, U., Sarfraz, S., Xia, Y., Kamran, M.A., Javed, M.A., Sultan, T., Hussain Munis, M.F. & Chaudhary, H.J. 2019. Mechanistic elucidation of germination potential and growth of wheat inoculated with exopolysaccharide and ACC-deaminase producing Bacillus strains under induced salinity stress. Cotoxicology and Environmental Safety Available from: https://europepmc.org/article/med/ 31408821 [accessed 13 October 2019].
Ansari, F.A., Ahmad, I. & Pichtel, J. 2019. Growth stimulation and alleviation of salinity stress to wheat by the biofilm forming Bacillus pumilus strain FAB10. Applied Soil Ecology 143: 45-54.
Bent, E., Tvzun, S., Chanway, C.P. & Enebak, S. 2001. Alterations in plant growth and root hormone levels of lodge pole pines inoculated with rhizobacteria. Canadian Journal of Microbiology 47: 793-800.
Bose, J., Munns, R., Shabala, S., Gilliham, M., Pogson, B. & Tyerman, S.D. 2017. Chloroplast function and ion regulation in plants growing on saline soils: lessons from halophytes. Journal of Experimental Botany 68: 3129-3143.
Byrt, C.S., Munns, R., Burton, R.A., Gilliham, M. & Wege, S. 2018. Root cell wall solutions for crop plants in saline soils. Plant Science 269:47-55.
Davenport, R.J., Reid, R.J. & Smith, F.A. 1997. Sodium-calcium interactions in two wheat species differing in salinity tolerance. Physiologia Plantarum 99: 323-327.
Donate-Correa, J., León-Barrios, M. & Pérez-Galdona, R. 2004. Screening for plant growth-promoting rhizobacteria in Chamaecytisus proliferus (tagasaste), a forage treeshrub legume endemic to the Canary Island. Plant and Soil 266: 261-272.
Ehghaghi, R., Mosleh Arani, A., Azimzadeh, H., Zargaran, M. & Kiani, B. 2015. Investigation of some ecological characteristics of four Calligonum species in Yazd province. Iranian Journal of Range and Desert Research 22: 168-182.
El-Nahrawy, S. & Yassin, M. 2020. Response of different cultivars of Wheat plants (Triticum aestivum L.) to inoculation by Azotobacter sp. under salinity stress conditions. Journal of Advances in Microbiology 20: 59-79.
Etesami, H. & Beattie, G.A. 2018. Mining halophytes for plant growth-promoting halotolerant bacteria to enhance the salinity tolerance of non-halophytic crops. Frontiers in Microbiology 9: 148-156.
Etesami, H., Emami, S. & Alikhani, H.A. 2017. Potassium solubilizing bacteria (KSB): mechanisms, promotion of plant growth, and future prospects: A review. Journal of Soil Science and Plant Nutrition 17: 897-911.
Eskandari Torbaghan, M., Lakzian, A., Astaraei, A.R., Fotovat, A. & Besharati, H. 2017. Measurement of ACC-Deaminase production in halophilic, alkalophilic and haloalkalophilic bacterial isolates in soil. International Biological and Biomedical Journal 3: 194-202.
Ghahremaninejad, F., Hoseini, E. & Jalali, S. 2021. The cultivation and domestication of wheat and barley in Iran, brief review of a long history. Botanical Review 87: 1-22.
https://doi.org/10.1007/s12229-020-09244-w.
Ghassemi, F., Jakeman, A.J. & Nix, H.A. 1995. Salinization of land and water resources: human causes, extent, management and case studies. Wallingford: CABI Publishing, 526 pp.
Glick, B.R. 2012. Plant growth-promoting bacteria: Mechanisms and applications. Hindawi Publishing Corporation Scientifica, 15 pp.
Glick, B.R. 2014. Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiological Research 169: 30-39.
Goswami, M., & Deka, S. 2020. Plant growth-promoting rhizobacteria|alleviators of abioticstresses in soil: A review. Pedosphere 30: 40-61.
Haddadi M. & Ghezelbash, G.R. 2020. Isolation of halophilic urease producing bacteria and study of their nanocrystal production. Nova Biologica Reperta 7: 37-45. (In Persian).
Hadi, M.R. & Karimi, N. 2012. The role of calcium in plants’ salt tolerance. Journal of Plant Nutrition 35: 2037-2054.
Honma, M. & Shimomura, T. 1978. Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agricultural and Biological Chemistry 42: 1825-1831.
Hu, L., Zehui, H., Shuqian, L. & Fu, J. 2012. Growth response and gene expression in antioxidant-related enzymes in two bermudagrass genotypes differing in salt tolerance. Journal of the American Society for Horticultural Science 137: 134-143.
Ilyas, N., Mazhar, R., Yasmin, H., Khan, W., Iqbal, S., Enshasy, H.E. & Dailin, D.J. 2020. Rhizobacteria isolated from saline soil induce systemic tolerance in Wheat (Triticum aestivum L.) against salinity stress. Agronomy 10: 989-1009.
Iqbal Hussain, M. Naeem Asghar, H., Javed Akhtar, M. & Arshad, M. 2013. Impact of phosphate solubilizing bacteria on growth and yield of maize. Soil & Environment 32: 71-78.
Jha, C.K. & Saraf, M. 2015. Plant growth promoting rhizobacteria (PGPR): A review. Journal of Agricultural Research and Development 5: 108-119.
Jha, B., Gontia, I. & Hartmann, A. 2012. The roots of the halophyte Salicornia brachiata are a source of new halotolerant diazotrophic bacteria with plant growth-promoting potential. Plant Soil 356: 265-277.
Jamil, A., Riaz, S., Ashraf, M. & Foolad, M.R. 2011. Gene expression profiling of plants under salt stress. Critical Reviews in Plant Sciences 30: 435-458.
Jeon, J.S., Lee, S.S., Kim, H.Y., Ahn, T.S. & Song, H.G. 2003. Plant growth promoting in soil by some inoculated microorganism. The Journal of Microbiology 4: 271-276.
Kouhifayegh, S.H., Hakimi, M.H., Mosleh Arani, A., Mirshamsi, H.A. and Kiani, B. 2014. The effects of sodium nitroproside and salicylic acid on some physiological characteristis of Melia azedarach under salinity conditions. Arid Biom Scientific and Research Journal 3: 62-71.
Kudla, J., Becker, D., Grill, E., Hedrich, R., Hippler, M. & Kummer, U. 2018. Advances and current challenges in calcium signaling. New Phytology 218: 414-431.
Kumar, A. & Verma, J.P. 2018. Does plant-Microbe interaction confer stress tolerance in plants: A review? Microbiology Research 207: 41-52.
Lynch, J. & Lauchli, A. 1988. Salinity affects intracellular calcium in corn root protoplasts. Plant Physiology 87: 351-356.
Machado, R.M.A. & Serralheiro, R.P. 2017. Soil salinity: Effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization. Horticulturae 3: 30-38.
Maksimovic, I. & Ilin, Z. 2012. Effects of salinity on vegetable growth and nutrients uptake. In: Lee, T.S. (ed.), Irrigation systems and practices in challenging environments. pp: 169-190. London, UK, IntechOpen
Mohajel Kazemi, E., Pazhouhandeh, M., Jonoubi, P. & Kazemian, M. 2020. The optimization of gene transfer to tomato and the study of expression possibility of salt-tolerance gene (SOS3). Nova Biologica Reperta 7: 76-84. (In Persian).
Mosleh Arani, A., Bakhshi Khaniki, G., Nemati, N., & Soltani, M. 2011. Investigation on the effect of salinity stress on seed germination of Salsola abarghuensis, Salsola arbuscula and Salsola yazdiana. Iranian Journal of Rangelands and Forests Plant Breeding and Genetic Research 18: 267-279. (In Persian).
Mosleh Arani, A., Rafiei, A., Tabandeh, A. & Azimzadeh, H. 2018. Morphological and physiological responses of root and leave in Gleditschia caspica to salinity stress. Iranian Journal of Plant Biology 9: 1-12. (In Persian).
Mukherjee, A., Gaurav, A.K., Singh, S., Chouhan, G.K., Kumar, A. & Das, S. 2019. Role of potassium (K) solubilising microbes (KSM) in growth and induction of resistance against biotic and abiotic stress in plant. Climate Change Environmental Sustainability 7: 212-214.
Munns, R., Day, D.A. and Fricke, W. 2020. Energy costs of salt tolerance in crop plants. New Phytologist 225: 1072-1090.
Nawaz, A., Shahbaz, M., Asadullah Imran, A., Marghoob, M.U., Imtiaz, M. & Mubeen, F. 2020. Potential of salt tolerant PGPR in growth and yield augmentation of Wheat (Triticum aestivum L.) under saline conditions. Frontiers in Microbiology 11: 201-213.
Olsen, S.R., & Sommers, L.E. 1982. Phosphorous. In: Methods of soil analisis. Soil Science Society of America, Madison, WI. pp: 423-424.
Qi, Z. & Spalding, E.P. 2004. Protection of plasma membrane K+ transport by the salt overly sensitive Na+/H+ antiporter during salinity stress. Plant Physiology 136: 2548-2555.
Razzaghi Komaresofla, B., Alikhani, H.A., Etesami, H. & Khoshkholgh-Sima, N.A. 2019. Improved growth and salinity tolerance of the halophyte Salicornia sp. by co–inoculation with endophytic and rhizosphere bacteria. Applied Soil Ecology 138: 160-170.
Rijavec, T. & Lapanje, A. 2016. Hydrogen cyanide in the rhizosphere: not suppressing plant pathogens, but rather regulating availability of phosphate. Frontiers in Microbiology 7: 1785-1794.
Rubin, R.L., Van Groenigen, K.J. & Hungate, B.A. 2017. Plant growth promoting rhizobacteria are more effective under drought: A meta-analysis. Plant Soil 416: 309-323.
Rubio, F., Nieves-Cordones, M., Horie, T. & Shabala, S. 2020. Doing ‘business as usual’ comes with a cost: evaluating energy cost of maintaining plant intracellular K+ homeostasis under saline conditions. New Phytologist 225: 1097-1104.
Safdarian, M., Askari, H. & Shariati, J. 2019. Transcriptional responses of wheat roots inoculated with Arthrobacter nitroguajacolicus to salt stress. Scientific Reports 9: 1792-1799.
Sashidhar, B. & Podile, A.R. 2010. Mineral phosphate solubilization by rhizosphere bacteria and scope for manipulation of the direct oxidation pathway involving glucose dehydrogenase. Journal of Applied Microbiology 109: 1-12.
Satomi, M., La Duc, M.T. & Venkateswaran, K. 2006. Bacillus safensis sp. nov., isolated from spacecraft and assembly-facility surfaces. International Journal of Systematic and Evolutionary Microbiology 56: 1735-1740.
Seed and Plant Research Improvement Institute. 2016. Crop cultivars report (food security and health-1). Agricultural research, education and extension organization. Press, Tehran, 231 pp. (In Persian).
Sadat, a.a.V. & Savaghebi Firouzabadi, G.R. 2010. Effects of some arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria on the growth and yield indices of two Wheat varieties in a saline soil. Journal of Water and soil Agricultural Science and Technology 24: 53-62.
Seifikalhor, M., Aliniaeifard, S., Shomali, A., Azad, N., Hassani, B., Lastochkina, O. & Li, T. 2019. Calcium signaling and salt tolerance are diversely entwined in plants. Plant Signaling & Behavior 14: 11-20.
Shahidi, A., & miri, Z. 2018. The effect of salinity on yield and yield components of two wheat cultivars in the plain of Birjand. Electronic Journal of Crop Production 11: 51-61. (In Persian).
Shahriaripour, R, Pour, A.T. & Mozaffari, V. 2011. Effects of salinity and soil phosphorus application on growth and chemical composition of pistachio seedlings. Communications in Soil Science and Plant Analysis 42: 144-158.
Shi-Ying, Z., Cong, F., Yong-xia, W., Yun-sheng, X., Wei, X. & Xiao-Long, C. 2018. Salt-tolerant and plant growth-promoting bacteria isolated from high-yield paddy soil. Canadian Journal of Microbiology 64: 968-978.
Sindhu, S.S., Dua, S., Verma, M.K. & Khandelwal, A. 2010. Growth promotion of legumes by inoculation of rhizosphere bacteria. In: Khan, M.S. et al. (eds.), Microbes for legume improvement. pp: 195-235. Springer-Verlag, Wien.
Singh, R.P & Jha, P.N. 2017. The PGPR Stenotrophomonas maltophilia SBP-9 augments resistance against biotic and abiotic stress in Wheat plants. Frontiers in Microbiology 8: 1945-1953.
Souza, R.D., Ambrosini, A. & Passaglia, L.M.P. 2015. Plant growth promoting bacteria as inoculants in agricultural soils. Genetics and Molecular Biology 38: 401-419.
Szymańska, S., Płociniczak, T., Piotrowska-Seget, Z. & Hrynkiewicz, K. 2016. Endophytic and rhizosphere bacteria associated with the roots of the halophyte Salicornia europaea L. – community structure and metabolic potential. Microbiological Research 192: 37-51.
Tuna, A.L., Kaya, C., Ashraf, M., Altunlu, H., Yokas, I. & Yagmur, B. 2007. The effects of calcium sulfate on growth, membrane stability and nutrient uptake of tomato plants grown under salt stress. Environmental and Experimental Botany 59: 173-178.
Legendre, L., Wisniewski-Dyé, F. & Prigent-Combaret, C. 2013. Plant growth-promoting Upadhyay, S.K. & Singh, D.P. 2015. Effect of salt tolerant plant growth promoting rhizobacteria on Wheat plants and soil health in a saline environment. Plant Biology 17: 288-293.
Vacheron, J., Desbrosses, G., Bouffaud, M.L., Touraine, B., Moënne-Loccoz, Y., Muller, D., rhizobacteria and root system functioning. Frontiers in Plant Science 4: 1-19.
Waling, I., Van Vark, W., Houba, V.J.G. & Van der lee, J.J. 1980. Soil and plant analysis Wageningen Agriculture University, 123 pp.
Wang, J., Li, R. & Zhang, H. 2020. Beneficial bacteria activate nutrients and promote wheat growth under conditions of reduced fertilizer application. BMC Microbiology 20: 38-48.
Weisburg, W.G., Barns, S.M., Pelletier, D.A. & Lane, D.J. 1991. 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology 173: 697-703.
Wang, Q., Dodd, I.C., Belimov, A.A. & Jiang, F. 2016. Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase growth and photosynthesis of pea plants under salt stress by limiting Na+ accumulation. Functional Plant Biology 43: 161-172.
World Bank. 2019. World population prospects 2019: Highlights. United Nations, 39 pp.
Wu, H.H., Zhang, X.C., Giraldo, J.P. & Shabala, S. 2018. It is not all about sodium: revealing tissue specificity and signalling roles of potassium in plant responses to salt stress. Plant Soil 431: 1-17.
Zhang, Y.Q., Schumann, L.Y., Liu, H.Y., Zhang, Y.Q., Xu, L.H., Stackebrandt, E., Jiang, C.L. & Li, W.J. 2007. Zhihengliuella halotolerans gen. nov., sp. nov., a novel member of the family Micrococcaceae. International Journal of Systematic and Evolutionary Microbiology 57: 1018-1023.