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Utilizing the Indigenous Plant Growth-Promoting Rhizobacteria and Sulfur in Improving Yield and Nutrients Uptake of Wheat in Saline-Sodic Soils

  • AGRICULTURAL CHEMISTRY AND SOIL FERTILITY
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Abstract

The salinity and sodicity of soils lead to the inhibition of the plant’s growth and disequilibrium of the nutrients, and thus reduce their plant uptake in the soil. The aims of this study were to characterize the indigenous plant growth-promoting rhizobacteria (PGPR) of wheat rhizosphere and to evaluate their ability with sulfur to improve nutrient uptake and wheat yield in saline-sodic soils. To do so, the bacteria were isolated from wheat rhizosphere cultivated in saline-sodic soils and screened for plant growth-promoting (PGP) traits. The superior PGPR was identified by 16S rRNA gene sequencing. A greenhouse experiment was carried out in a completely randomized factorial design with different levels of salinity and sodicity, bacteria inoculation, and levels of sulfur along with Thiobacillus thiooxidans. Results showed that Pseudomonas alcaliphila, Bacillus subtilis, and Rhizobium pusense were the superior PGPR in the wheat rhizosphere. Grain yield and nutrient concentrations of wheat grain decreased with increasing soil salinity and sodicity. Bacteria inoculation, especially R. pusense showed a marked exopolysaccharide and ACC-deaminase production increased grain yield, N and P concentrations and Ca/Mg ratio at different levels of soil sodicity and salinity. R. pusence and B. subtilis facilitated higher concentrations of N and P in wheat when used concurrently with sulfur and T. thiooxidans, respectively. Overall, the results indicated that the application of isolated PGPR of wheat rhizosphere possessed PGP traits especially R. pusense along with sulfur and T. thiooxidans, resulted in excellent benefits on wheat growth in saline-sodic soils.

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REFERENCES

  1. P. Abbas-Zadeh, N. Saleh-Rastin, H. Asadi-Rahmani, K. Khavazi, A. Soltani, A. Shoary-Nejati, and M. Miransari, “Plant growth-promoting activities of fluorescent pseudomonads, isolated from the Iranian soils,” Acta Physiol. Plant. 32, 281–288 (2010).

    Article  Google Scholar 

  2. R. Abbas, S. Rasul, K. Aslam, M. Baber, M. Shahid, F. Mubeen, and T. Naqqash, “Halotolerant PGPR: a hope for cultivation of saline soils,” J. King Saud Univ., Sci. 31, 1195–1201 (2019).

    Google Scholar 

  3. M. Abbasi, S. Sharif, M. Kazmi, T. Sultan, and M. Aslam, “Isolation of plant growth promoting rhizobacteria from wheat rhizosphere and their effect on improving growth, yield and nutrient uptake of plants,” Plant Biosyst. 145, 159–168 (2011).

    Article  Google Scholar 

  4. K. Ahmed, G. Qadir, A. R. Jami, A. I. Saqib, M. Nawaz, M. Kamal, and E. Haq, “Comparative reclamation efficiency of gypsum and sulfur for improvement of salt affected,” Bulg. J. Agric. Sci. 23, 126–133 (2017).

    Google Scholar 

  5. A. A. Al-Enazy, F. Al-Barakah, S. Al-Oud, and A. Usman, “Effect of phosphogypsum application and bacteria co-inoculation on biochemical properties and nutrient availability to maize plants in a saline soil,” Arch. Agron. Soil Sci. 64, 1394–1406 (2018).

    Article  Google Scholar 

  6. D. Alexander and D. Zuberer, “Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria,” Biol. Fertil. Soils 12, 39–45 (1991).

    Article  Google Scholar 

  7. S. Z. Ali, V. Sandhya, and L. Venkateswar Rao, “Isolation and characterization of drought-tolerant ACC deaminase and exopolysaccharide-producing fluorescent Pseudomonas sp.,” Ann. Biol. Res. 64, 493–502 (2014).

    Google Scholar 

  8. Z. T. Alipour and A. Sobhanipour, “The effect of Thiobacillus and Pseudomonas fluorescent inoculation on maize growth and Fe uptake,” Ann. Biol. Res. 3, 1661–1666 (2012).

    Google Scholar 

  9. M. M. Aria, A. Lakzian, G. H. Haghnia, A. R. Berenji, H. Besharati, and A. Fotovat, “Effect of Thiobacillus, sulfur, and vermicompost on the water-soluble phosphorus of hard rock phosphate,” Bioresour. Technol. 101, 551–554 (2010).

    Article  Google Scholar 

  10. H. Asadi Rahmani, K. Khavazi, V. A. Jahandideh Mahjen Abadi, M. Ramezanpour, M. Mirzapour, and K. Mirzashahi, “Effect of Thiobacillus, sulfur, and phosphorus on the yield and nutrient uptake of canola and the chemical properties of calcareous soils in Iran,” Commun. Soil Sci. Plant Anal. 49, 1671–1683 (2018).

    Article  Google Scholar 

  11. A.B. Bleecker and H. Kende, “Ethylene: a gaseous signal molecule in plants,” Annu. Rev. Cell Dev. Biol. 16, 1–18 (2000).

    Article  Google Scholar 

  12. T. Chaudhary, R. Gera, and P. Shukla, “Deciphering the potential of Rhizobium pusense MB-17a, a plant growth-promoting root endophyte, and functional annotation of the genes involved in the metabolic pathway,” Front. Bioeng. Biotechnol. 8, 617034 (2021).

    Article  Google Scholar 

  13. T. Damodaran, V. Mishra, S. Jha, U. Pankaj, G. Gupta, and R. Gopal, “Identification of rhizosphere bacterial diversity with promising salt tolerance, PGP traits and their exploitation for seed germination enhancement in sodic soil,” Agric. Res. 8, 36–43 (2019).

    Article  Google Scholar 

  14. T. Damodaran, D. Sharma, V. Mishra, S. Jha, R. Kannan, V. Sah, and R. Rai, “Isolation of salt tolerant endophytic and rhizospheric bacteria by natural selection and screening for promising plant growth-promoting rhizobacteria (PGPR) and growth vigour in tomato under sodic environment,” Afr. J. Microbiol. Res. 7, 5082–5089 (2013).

    Google Scholar 

  15. S. Day, J. Norton, C. Strom, T. Kelleners, and E. Aboukila, “Gypsum, langbeinite, sulfur, and compost for reclamation of drastically disturbed calcareous saline–sodic soils,” Int. J. Environ. Sci. Technol. 16, 295–304 (2019).

    Article  Google Scholar 

  16. E. Dell’Amico, L. Cavalca, and V. Andreoni, “Analysis of rhizobacterial communities in perennial Graminaceae from polluted water meadow soil, and screening of metal-resistant, potentially plant growth-promoting bacteria,” FEMS Microbiol. Ecol. 52, 153–162 (2005).

    Article  Google Scholar 

  17. M. Dworkin and J. Foster, “Experiments with some microorganisms which utilize ethane and hydrogen,” J. Bacteriol. 75, 592–603 (1958).

    Article  Google Scholar 

  18. A. M. El-Sawah, A. El-Keblawy, D. F. I. Ali, H. M. Ibrahim, M. A. El-Sheikh, A. Sharma, Y. Alhaj Hamoud, H. Shaghaleh, M. Brestic, and M. Skalicky, “Arbuscular mycorrhizal fungi and plant growth-promoting rhizobacteria enhance soil key enzymes, plant growth, seed yield, and qualitative attributes of guar,” Agriculture 11, 194 (2021).

    Article  Google Scholar 

  19. A. Elgharably and N. A. Nafady, “Inoculation with Arbuscular mycorrhizae, Penicillium funiculosum and Fusarium oxysporum enhanced wheat growth and nutrient uptake in the saline soil,” Rhizosphere 18, 100345 (2021).

    Article  Google Scholar 

  20. H. Evelin, T. S. Devi, S. Gupta, and R. Kapoor, “Mitigation of salinity stress in plants by arbuscular mycorrhizal symbiosis: current understanding and new challenges,” Front. Plant Sci. 10, 470 (2019).

    Article  Google Scholar 

  21. C. M. Ferreira, Â. Vilas-Boas, C. A. Sousa, H. M. Soares, and E. V. Soares, “Comparison of five bacterial strains producing siderophores with ability to chelate iron under alkaline conditions,” AMB Express 9, 1–12 (2019).

    Article  Google Scholar 

  22. R. Flores-Vargas and G. O’hara, “Isolation and characterization of rhizosphere bacteria with potential for biological control of weeds in vineyards,” J. Appl. Microbiol. 100, 946–954 (2006).

    Article  Google Scholar 

  23. R. Fusconi and M. Godinho, “Screening for exopolysaccharide-producing bacteria from sub-tropical polluted groundwater,” Braz. J. Biol. 62, 363–369 (2002).

    Article  Google Scholar 

  24. K. E. Gerhardt, G. J. MacNeill, P. D. Gerwing, and B. M. Greenberg, “Phytoremediation of salt-impacted soils and use of plant growth-promoting rhizobacteria (PGPR) to enhance phytoremediation,” in Phytoremediation, Ed. by A. A. Ansari (Springer International Publishing, 2017), pp. 19–51.

    Google Scholar 

  25. B. R. Glick, “Bacteria with ACC deaminase can promote plant growth and help to feed the world,” Microbiol. Res. 169, 30–39 (2014).

    Article  Google Scholar 

  26. S. A. Gordon and R. P. Weber, “Colorimetric estimation of indoleacetic acid,” Plant Physiol. 26, 192 (1951).

    Article  Google Scholar 

  27. Y. W. Gui, M. S. Sheteiwy, S. G. Zhu, A. Batool, and Y. C. Xiong, “Differentiate effects of non-hydraulic and hydraulic root signaling on yield and water use efficiency in diploid and tetraploid wheat under drought stress,” Environ. Exp. Bot. 181, 104287 (2021).

    Article  Google Scholar 

  28. S. Hajinia, M. J. Zarea, F. Rejali, and A. Varma, “Yield and yield components of wheat as affected by salinity and inoculation with Azospirillum strains from saline or non-saline soil,” J. Saudi Soc. Agric. Sci. 11, 113–121 (2012).

    Google Scholar 

  29. M. Huber, W. V. Bienvenut, E. Linster, I. Stephan, L. Armbruster, C. Sticht, D. Layer, K. Lapouge, T. Meinnel, and I. Sinning, “NatB-mediated N-terminal acetylation affects growth and biotic stress responses,” Plant Physiol. 182, 792–806 (2020).

    Article  Google Scholar 

  30. H. M. Ibrahim and A. M. El-Sawah, “The mode of integration between azotobacter and rhizobium affect plant growth, yield, and physiological responses of pea (Pisum sativum L.),” J. Soil Sci. Plant Nutr. 22, 1238–1251 (2022).

    Article  Google Scholar 

  31. N. O. Igiehon, O. O. Babalola, and B. R. Aremu, “Genomic insights into plant growth promoting rhizobia capable of enhancing soybean germination under drought stress,” BMC Microbiol. 19, 1–22 (2019).

    Article  Google Scholar 

  32. V. A. Jahandideh Mahjenabadi and M. Sepehri, “Effect of Piriformospora indica and Azotobacter chroococcum on mitigation of zinc deficiency stress in wheat (Triticum aestivum L.),” Symbiosis 69, 9–19 (2016).

    Article  Google Scholar 

  33. V. A. Jahandideh Mahjenabadi, M. Sepehri, B. Khatabi, and M. Rezaei, “Alleviation of zinc deficiency in wheat inoculated with root endophytic fungus Piriformospora indica and rhizobacterium Pseudomonas putida,” Rhizosphere 17, 100311 (2021).

    Article  Google Scholar 

  34. V. A. Jahandideh Mahjenabadi, M. Sepehri, H. A. Rahmani, M. Zarei, A. Ronaghi, S. M. Taghavi, and M. Shamshiripour, “Role of dominant phyllosphere bacteria with plant growth–promoting characteristics on growth and nutrition of maize (Zea mays L.),” J. Soil Sci. Plant Nutr. 20, 2348–2363 (2020).

    Article  Google Scholar 

  35. A. Jamil, S. Riaz, M. Ashraf, and M. Foolad, “Gene expression profiling of plants under salt stress,” Crit. Rev. Plant Sci. 30, 435–458 (2011).

    Article  Google Scholar 

  36. H. Jiang, H. Dong, G. Zhang, B. Yu, L. R. Chapman, and M. W. Fields, “Microbial diversity in water and sediment of Lake Chaka, an athalassohaline lake in northwestern China,” Appl. Environ. Microbiol. 72, 3832–3845 (2006).

    Article  Google Scholar 

  37. A. Karnwal, “Screening, isolation and characterization of culturable stress-tolerant bacterial endophytes associated with Salicornia brachiata and their effect on wheat (Triticum aestivum L.) and maize (Zea mays) growth,” J. Plant Prot. Res. 59, 293–303 (2019).

    Google Scholar 

  38. M. Keisham, S. Mukherjee, and S. C. Bhatla, “Mechanisms of sodium transport in plants—progresses and challenges,” Int. J. Mol. Sci. 19, 647 (2018).

    Article  Google Scholar 

  39. K. Khavazi, V. A. Jahandideh Mahjanabadi, and F. Taghipoor, “Effect of sulfur, Thiobacillus bacteria and phosphorus on the yield and nutrient elements uptake of wheat in calcareous soil,” J. Soil Manage. Sustainable Prod. 8, 23–41 (2018).

    Google Scholar 

  40. P. M. Kopittke, N. W. Menzies, P. Wang, B. A. McKenna, and E. Lombi, “Soil and the intensification of agriculture for global food security,” Environ. Int. 132, 105078 (2019).

    Article  Google Scholar 

  41. A. Kumar, S. Singh, A. K. Gaurav, S. Srivastava, and J. P. Verma, “Plant growth-promoting bacteria: biological tools for the mitigation of salinity stress in plants,” Front. Microbiol. 11, 1216 (2020).

    Article  Google Scholar 

  42. R. Leogrande and C. Vitti, “Use of organic amendments to reclaim saline and sodic soils: a review,” Arid Land Res. Manage. 33, 1–21 (2019).

    Article  Google Scholar 

  43. H. Li and X. Jiang, “Inoculation with plant growth-promoting bacteria (PGPB) improves salt tolerance of maize seedling,” Russ. J. Plant Physiol. 64, 235–241 (2017).

    Article  Google Scholar 

  44. A. K. Manesh, M. Armin, and M. J. Moeini, “The effect of sulfur application on yield and yield components of corn in two different planting methods in saline conditions,” Int. J. Agron. Plant Prod. 4, 1474–1478 (2013).

    Google Scholar 

  45. A. Maxton, P. Singh, and S. A. Masih, “ACC deaminase-producing bacteria mediated drought and salt tolerance in Capsicum annuum,” J. Plant Nutr. 41, 574–583 (2018).

    Article  Google Scholar 

  46. U. Mc Carthy, I. Uysal, R. Badia-Melis, S. Mercier, C. O’Donnell, and A. Ktenioudaki, “Global food security–issues, challenges and technological solutions,” Trends Food Sci. Technol. 77, 11–20 (2018).

    Article  Google Scholar 

  47. M. I. Mir, B. K. Kumar, S. Gopalakrishnan, S. Vadlamudi, and B. Hameeda, “Characterization of rhizobia isolated from leguminous plants and their impact on the growth of ICCV 2 variety of chickpea (Cicer arietinum L.),” Heliyon 7, e08321 (2021).

    Article  Google Scholar 

  48. S. Misra, V. K. Dixit, M. H. Khan, S. K. Mishra, G. Dviwedi, S. Yadav, A. Lehri, and P. S. Chauhan, “Exploitation of agro-climatic environment for selection of 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase producing salt tolerant indigenous plant growth promoting rhizobacteria,” Microbiol. Res. 205, 25–34 (2017).

    Article  Google Scholar 

  49. V. Nair, D. Graetz, and K. Portier, “Forms of phosphorus in soil profiles from dairies of South Florida,” Soil Sci. Soc. Am. J. 59, 1244–1249 (1995).

    Article  Google Scholar 

  50. G. Najar, S. Singh, F. Akhtar, and S. Hakeem, “Influence of sulphur level on yield, uptake and quality of soybean (Glycine max) under temperate conditions of Kashmir valley,” Indian J. Agric. Sci. 81, 340–343 (2011).

    Google Scholar 

  51. F. X. Nascimento, M. J. Rossi, and B. R. Glick, “Role of ACC deaminase in stress control of leguminous plants,” in Plant Growth Promoting Actinobacteria, Ed. by G. Subramaniam, S. Arumugam, and V. Rajendran (Springer Science, Singapore, 2016), pp. 179–192.

    Google Scholar 

  52. H. Naseem, M. Ahsan, M. A. Shahid, and N. Khan, “Exopolysaccharides producing rhizobacteria and their role in plant growth and drought tolerance,” J. Basic Microbiol. 58, 1009–1022 (2018).

    Article  Google Scholar 

  53. A. Nazarov, L. Anan’ina, A. Gorbunov, and A. Pyankova, “Bacteria producing ectoine in the rhizosphere of plants growing on technogenic saline soil,” Eurasian Soil Sci. 55, 1074–1081 (2022).

    Article  Google Scholar 

  54. K. T. Osman, “Saline and sodic soils,” in Management of Soil Problems, Ed. by K. T. Osman (Springer, Cham, 2028), pp. 255–298.

  55. J. Pan, F. Peng, X. Xue, Q. You, W. Zhang, T. Wang, and C. Huang, “The growth promotion of two salt-tolerant plant groups with PGPR inoculation: a meta-analysis,” Sustainability 11, 378 (2019).

    Article  Google Scholar 

  56. Z. Rahneshan, F. Nasibi, and A. A. Moghadam, “Effects of salinity stress on some growth, physiological, biochemical parameters and nutrients in two pistachio (Pistacia vera L.) rootstocks,” J. Plant Interact. 13, 73–82 (2018).

    Article  Google Scholar 

  57. S. Rezvani Borujeni, K. Khavazi, A. Asgharzadeh, and I. Rezvani Borujeni, “Use of bacterial acc deaminase to increase oil (especially poly aromatic hydrocarbons) phytoremediation efficiency for maize (zea mays) seedlings,” Int. J. Phytorem. 20, 476–482 (2018).

    Article  Google Scholar 

  58. D. Saghafi, M. Ghorbanpour, and B. A. Lajayer, “Efficiency of Rhizobium strains as plant growth promoting rhizobacteria on morpho-physiological properties of Brassica napus L. under salinity stress,” J. Soil Sci. Plant Nutr. 18, 253–268 (2018).

    Google Scholar 

  59. J. Sambrook and D. Russell, Molecular Cloning: a Laboratory Manual (Cold Spring Harbor, New York, 2001).

    Google Scholar 

  60. V. Sandhya and S. Z. Ali, “The production of exopolysaccharide by Pseudomonas putida GAP-P45 under various abiotic stress conditions and its role in soil aggregation,” Microbiology 84, 512–519 (2015).

    Article  Google Scholar 

  61. B. Sashidhar and A. R. Podile, “Mineral phosphate solubilization by rhizosphere bacteria and scope for manipulation of the direct oxidation pathway involving glucose dehydrogenase,” J. Appl. Microbiol. 109, 1–12 (2010).

    Article  Google Scholar 

  62. G. Selvakumar, P. Panneerselvam, and A. N. Ganeshamurthy, “Bacterial mediated alleviation of abiotic stress in crops,” in Bacteria in Agrobiology: Stress Management, Ed. by D. K. Maheshwari (Springer-Verlag, Berlin Heidelberg, 2012), pp. 205–224.

    Google Scholar 

  63. R. Shahriaripour, A. T. Pour, V. Mozaffari, H. Dashti, and E. Adhami, “Effects of salinity and soil zinc application on growth and chemical composition of pistachio seedlings,” J. Plant Nutr. 33, 1166–1179 (2010).

    Article  Google Scholar 

  64. A. Sharma, K. Dev, A. Sourirajan, and M. Choudhary, “Isolation and characterization of salt-tolerant bacteria with plant growth-promoting activities from saline agricultural fields of Haryana, India,” Genet. Eng. Biotechnol. 19, 1–10 (2021).

    Google Scholar 

  65. M. S. Sheteiwy, H. Abd Elgawad, Y. C. Xiong, A. Macovei, M. Brestic, M. Skalicky, H. Shaghaleh, Y. Alhaj Hamoud, and A. M. El-Sawah, “Inoculation with Bacillus amyloliquefaciens and mycorrhiza confers tolerance to drought stress and improve seed yield and quality of soybean plant,” Physiol. Plant. 172, 2153–2169 (2021).

    Article  Google Scholar 

  66. J. I. Sperber, “The incidence of apatite-solubilizing organisms in the rhizosphere and soil,” Aust. J. Agric. Res. 9, 778–781 (1958).

    Article  Google Scholar 

  67. K. Tamura, J. Dudley, M. Nei, and S. Kumar, “M-EGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0,” Mol. Boil. Evol. 24, 1596–1599 (2007).

    Article  Google Scholar 

  68. S. Tewari and N. K. Arora, “Multifunctional exopolysaccharides from Pseudomonas aeruginosa PF23 involved in plant growth stimulation, biocontrol and stress amelioration in sunflower under saline conditions,” Curr. Microbiol. 69, 484–494 (2014).

    Article  Google Scholar 

  69. S. Upadhyay, J. Singh, and D. Singh, “Exopolysaccharide-producing plant growth-promoting rhizobacteria under salinity condition,” Pedosphere 21, 214–222 (2011).

    Article  Google Scholar 

  70. R. Vidyalakshmi, R. Paranthaman, and R. Bhakyaraj, “Sulphur oxidizing bacteria and pulse nutrition- a review,” World J. Agric. Sci. 5, 270–278 (009).

  71. S. S. K. P. Vurukonda, S. Vardharajula, M. Shrivastava, and A. SkZ, “Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria,” Microbiol. Res. 184, 13–24 (2016).

    Article  Google Scholar 

  72. A. Wakeel, “Potassium–sodium interactions in soil and plant under saline-sodic conditions,” J. Plant Nutr. Soil Sci. 176, 344–354 (2013).

    Article  Google Scholar 

  73. I. Walinga, W. V. Vark, V. J. Houba, and J. J. Van der Lee, Soil and Plant Analysis: a Series of Syllabi, Part 7: Plant Analysis Procedures (Wageningen Agriculture Univ., Wageningen, 1989).

  74. M. Zafar-ul-Hye, H. M. Farooq, and M. Hussain, “Bacteria in combination with fertilizers promote root and shoot growth of maize in saline-sodic soil,” Braz. J. Microbiol. 46, 97–102 (2015).

    Article  Google Scholar 

  75. M. Zafar-ul-Hye, A. Nasir, M. Aon, S. Hussain, M. Ahmad, and I. Naz, “Seed inoculation with Pseudomonas fluorescens and Pseudomonas syringae enhanced maize growth in a compacted saline-sodic soil,” Phyton 87, 25 (2018).

    Article  Google Scholar 

  76. Y. Zheng, X. Li, Y. Li, B. Miao, H. Xu, M. Simmons, and X. Yang, “Contrasting responses of salinity-stressed salt-tolerant and intolerant winter wheat (Triticum aestivum L.) cultivars to ozone pollution,” Plant Physiol. Biochem. 52, 169–178 (2012).

    Article  Google Scholar 

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This study was funded by the Soil and Water Research Institute (SWRI), Karaj, Iran.

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Javadzadeh, M., Khavazi, K., Ghanavati, N. et al. Utilizing the Indigenous Plant Growth-Promoting Rhizobacteria and Sulfur in Improving Yield and Nutrients Uptake of Wheat in Saline-Sodic Soils. Eurasian Soil Sc. 56, 1101–1113 (2023). https://doi.org/10.1134/S106422932360015X

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