Enhancing salinity tolerance and growth of Spinacia oleracea L. using halophilic plant growth-promoting bacteria

enhancing-salinity-tolerance-and-growth-of-spinacia-oleracea-l.-using-halophilic-plant-growth-promoting-bacteria
Enhancing salinity tolerance and growth of Spinacia oleracea L. using halophilic plant growth-promoting bacteria

References

  1. John, J. E. et al. Biomining sesuvium portulacastrum for halotolerant PGPR and endophytes for promotion of salt tolerance in Vigna mungo L. Front. Microbiol. 14, (2023).

  2. El Sabagh, A. et al. Consequences of salinity stress on the quality of crops and its mitigation strategies for sustainable crop production: an outlook of arid and semi-arid regions. 503–533. https://doi.org/10.1007/978-3-030-49732-3_20 (Springer, 2020).

  3. Kumar, P. & Sharma, P. K. Soil salinity and food security in India. Front. Sustain. Food Syst. 4, (2020).

  4. Balasubramaniam, T., Shen, G., Esmaeili, N. & Zhang, H. Plants’ response mechanisms to salinity stress. Plants 12, 2253 (2023).

    Google Scholar 

  5. Shahid, M. A. et al. Insights into the physiological and biochemical impacts of salt stress on plant growth and development. Agronomy 10, 938 (2020).

    Google Scholar 

  6. Isayenkov, S. V. & Maathuis, F. J. M. Plant salinity stress: many unanswered questions remain. Front. Plant. Sci. 10, (2019).

  7. Kapadia, C. et al. Evaluation of plant growth-promoting and salinity ameliorating potential of halophilic bacteria isolated from saline soil. Front. Plant. Sci. 13, (2022).

  8. Oren, A. Halophilic microbial communities and their environments. Curr. Opin. Biotechnol. 33, 119–124 (2015).

    Google Scholar 

  9. Vreeland, R. H., Mcdonnough, S., Meyers, S. S. & Piselli, A. F. Jr Distribution and diversity of halophilic bacteria in a subsurface salt formation. Extremophiles 2, 321–331 (1998).

    Google Scholar 

  10. Oren, A. Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J. Ind. Microbiol. Biotechnol. 28, 56–63 (2002).

    Google Scholar 

  11. Bolhuis, H. et al. The genome of the square archaeon haloquadratum walsbyi: life at the limits of water activity. BMC Genomics 7, (2006).

  12. Kim, K. K., Lee, J. S. & Stevens, D. A. Microbiology and epidemiology of Halomonas species. Future Microbiol. 8, 1559–1573 (2013).

    Google Scholar 

  13. Sharma, A. et al. Halophilic bacteria: potential bioinoculants for sustainable agriculture and environment management under salt stress. 297–325. https://doi.org/10.1007/978-981-10-2854-0_14 (Springer, 2016).

  14. León, M. J. et al. Compatible solute synthesis and import by the moderate halophile spiribacter salinus: physiology and genomics. Front. Microbiol. 9, (2018).

  15. Viver, T. et al. Genomic comparison between members of the salinibacteraceae family, and description of a new species of salinibacter (Salinibacter altiplanensis sp. nov.) isolated from high altitude hypersaline environments of the Argentinian Altiplano. Syst. Appl. Microbiol. 41, 198–212 (2018).

    Google Scholar 

  16. Cui, H. L. & Dyall-Smith, M. L. Cultivation of halophilic archaea (class Halobacteria) from thalassohaline and athalassohaline environments. Mar. Life Sci. Technol. 3, 243–251 (2021).

    Google Scholar 

  17. Ali, I., Khaliq, S., Akbar, A. & Sajid, S. Biotechnological applications of halophilic fungi: past, present, and future. 291–306. https://doi.org/10.1007/978-3-030-19030-9_15 (Springer, 2019).

  18. Gunde-Cimerman, N. & Plemenitaš, A. Ecology and molecular adaptations of the halophilic black yeast hortaea werneckii. Reviews Environ. Sci. Bio/Technology. 5, 323–331 (2006).

    Google Scholar 

  19. Castillo-Carvajal, L. C., Barragán-Huerta, B. E. & Sanz-Martín, J. L. Biodegradation of organic pollutants in saline wastewater by halophilic microorganisms: a review. Environ. Sci. Pollut. Res. 21, 9578–9588 (2014).

    Google Scholar 

  20. Adamiak, J., Otlewska, A. & Gutarowska, B. Halophilic microbial communities in deteriorated buildings. World J. Microbiol. Biotechnol. 31, 1489–1499 (2015).

    Google Scholar 

  21. Haque, M. M. et al. Halotolerant biofilm-producing rhizobacteria mitigate seawater-induced salt stress and promote growth of tomato. Sci. Rep. 12, (2022).

  22. Paul, D. & Lade, H. Plant-growth-promoting rhizobacteria to improve crop growth in saline soils: a review. Agron. Sustain. Dev. 34, 737–752 (2014).

    Google Scholar 

  23. Orhan, F. & Demirci, A. Salt stress mitigating potential of Halotolerant/Halophilic plant growth promoting. Geomicrobiol J. 37, 663–669 (2020).

    Google Scholar 

  24. Singh, R. P. & Jha, P. N. Alleviation of salinity-induced damage on wheat plant by an ACC deaminase-producing halophilic bacterium Serratia sp. SL- 12 isolated from a salt lake. Symbiosis 69, 101–111 (2016).

    Google Scholar 

  25. Sanchez-Porro, C., Mellado, E., Martin, S. & Ventosa, A. Diversity of moderately halophilic bacteria producing extracellular hydrolytic enzymes. J. Appl. Microbiol. 94, 295–300 (2003).

    Google Scholar 

  26. Etesami, H. & Alikhani, H. A. Halotolerant plant growth-promoting fungi and bacteria as an alternative strategy for improving nutrient availability to salinity-stressed crop plants. 103–146. https://doi.org/10.1007/978-981-13-8335-9_5 (Springer, 2019).

  27. Saghafi, D., Lajayer, B. A., Ghorbanpour, M. & Delangiz, N. An overview on improvement of crop productivity in saline soils by halotolerant and halophilic PGPRs. 3 Biotech 9, (2019).

  28. Zhang, M. et al. Nitrogen recovery by a halophilic ammonium-assimilating microbiome: A new strategy for saline wastewater treatment. Water Res. 207, 117832 (2021).

    Google Scholar 

  29. Tripathi, S., Chakrabarti, K. & Barua, S. Site specific bioinoculants for sustainable agriculture in coastal saline soil. 209–234. https://doi.org/10.1007/978-3-319-14595-2_8 (Springer, 2015).

  30. Sadfi-Zouaoui, N. et al. Biological control of botrytis cinerea on stem wounds with moderately halophilic bacteria. World J. Microbiol. Biotechnol. 24, 2871–2877 (2008).

    Google Scholar 

  31. Masmoudi, F., Abdelmalek, N., Tounsi, S., Dunlap, C. A. & Trigui, M. Abiotic stress resistance, plant growth promotion and antifungal potential of halotolerant bacteria from a Tunisian solar saltern. Microbiol. Res. 229, 126331 (2019).

    Google Scholar 

  32. Bharti, N., Pandey, S. S., Barnawal, D., Kalra, A. & Patel, V. K. Plant growth promoting rhizobacteria dietzia Natronolimnaea modulates the expression of stress responsive genes providing protection of wheat from salinity stress. Sci. Rep. 6, 34768 (2016).

    Google Scholar 

  33. Abuqamar, S. F. et al. Halotolerant plant growth-promoting rhizobacteria improve soil fertility and plant salinity tolerance for sustainable agriculture A review. Plant. Stress. 12, 100482 (2024).

    Google Scholar 

  34. Haque, M. M. et al. Decolorization, degradation and detoxification of mutagenic dye Methyl orange by novel biofilm producing plant growth-promoting rhizobacteria. Chemosphere 346, 140568 (2023).

    Google Scholar 

  35. Grote, M. & O’Malley, M. A. Enlightening the life sciences: the history of halobacterial and microbial rhodopsin research. FEMS Microbiol. Rev. 35, 1082–1099 (2011).

    Google Scholar 

  36. Oren, A. Life in hypersaline environments. 301–339. https://doi.org/10.1007/978-3-319-28071-4_8 (Springer, 2016).

  37. Joulak, I. et al. Evaluation of the production of exopolysaccharides by newly isolated Halomonas strains from Tunisian hypersaline environments. Int. J. Biol. Macromol. 138, 658–666 (2019).

    Google Scholar 

  38. Joulak, I. et al. Structural characterization and functional properties of novel exopolysaccharide from the extremely halotolerant Halomonas elongata S6. Int. J. Biol. Macromol. 164, 95–104 (2020).

    Google Scholar 

  39. Paul, V. G. & Mormile, M. R. A case for the protection of saline and hypersaline environments: a microbiological perspective. FEMS Microbiol. Ecol. 93, (2017).

  40. Deole, R. & Hoff, W. D. A potassium chloride to glycine betaine osmoprotectant switch in the extreme halophile halorhodospira halophila. Sci. Rep. 10, (2020).

  41. Jones, B. E., Grant, W. D., Owenson, G. G. & Duckworth, A. W. Microbial diversity of soda lakes. Extremophiles 2, 191–200 (1998).

    Google Scholar 

  42. Harirchi, S. et al. Bacillales: from taxonomy to biotechnological and industrial perspectives. Microorganisms 10, 2355 (2022).

    Google Scholar 

  43. Phulpoto, I. A. et al. Enhanced oil recovery by potential Biosurfactant-Producing Halo-thermotolerant bacteria using soil washing and Sand-Packed glass column techniques. Curr. Microbiol. 77, 3300–3309 (2020).

    Google Scholar 

  44. Saibi, A. N. E. et al. Antimicrobial and enzymatic profiling of halophilic and halotolerant bacteria from a hypersaline lake ‘The great Sebkha of Oran, Northwestern algeria’. Geomicrobiol J. 39, 816–831 (2022).

    Google Scholar 

  45. Kanekar, P. P., Dhakephalkar, P. K., Kanekar, S. P. & Kelkar, A. S. Halophiles – taxonomy, diversity, physiology and applications. 1–34. https://doi.org/10.1007/978-94-007-2229-3_1 (Springer, 2011).

  46. Gil, T. et al. Isolation and characterization of culturable osmotolerant microbiota in hypersaline and hypergypsic soils as new treatment for osmotic stress in plants. Soil. Syst. 7, 86 (2023).

    Google Scholar 

  47. Khan, M. A. et al. Halotolerant bacteria mitigate the effects of salinity stress on soybean growth by regulating secondary metabolites and molecular responses. BMC Plant. Biol. 21, (2021).

  48. Sarmiento-López, L. G. et al. Production of indole-3-acetic acid by Bacillus circulans E9 in a low-cost medium in a bioreactor. J. Biosci. Bioeng. 134, 21–28 (2022).

    Google Scholar 

  49. Ko, S. H. et al. Antioxidant effects of spinach (Spinacia Oleracea L.) supplementation in hyperlipidemic rats. Prev. Nutr. Food Sci. 19, 19–26 (2014).

    Google Scholar 

  50. Mitova, I., Nenova, L. & Shaban, N. Abiotic factors and their impact on growth characteristics of spinach (Spinacia oleracea). Bulg. J. Agric. Sci. 23, 817–824 (2017).

    Google Scholar 

  51. Ramezanifar, H., Hamzee Yazd, G., Mahmoodabadi, H., Yazdanpanah, M., Tavousi, M. & N. & Spinach growth regulation due to interactive Salinity, Water, and nitrogen stresses. J. Plant Growth Regul. 41, 1654–1671 (2021).

    Google Scholar 

  52. Liu, C., Yuan, Z. & Jiang, X. Plant responses and adaptations to salt stress: A review. Horticulturae 10, 1221 (2024).

    Google Scholar 

  53. Xu, C. & Mou, B. Responses of spinach to salinity and nutrient deficiency in Growth, Physiology, and nutritional value. J. Am. Soc. Hortic. Sci. 141, 12–21 (2016).

    Google Scholar 

  54. Saddique, M. et al. Amino acids application alleviated salinity stress in spinach (Spinacia Oleracea L.) by improving oxidative defense, osmolyte accumulation, and nutrient balance. Turkish J. Agric. Forestry. 46, 875–887 (2022).

    Google Scholar 

  55. Bates, L. S., Waldren, R. P. & Teare, I. D. Rapid determination of free proline for water-stress studies. Plant. Soil. 39, 205–207 (1973).

    Google Scholar 

  56. Ramasamy, K. P. & Mahawar, L. Coping with salt stress-interaction of halotolerant bacteria in crop plants: A mini review. Front. Microbiol. 14, 1077561 (2023).

    Google Scholar 

  57. Egamberdieva, D. et al. Diversity and plant Growth-Promoting ability of Endophytic, halotolerant bacteria associated with tetragonia tetragonioides (Pall.) Kuntze. Plants 11, 49 (2021).

    Google Scholar 

  58. Naik, A. A., Tidke, S. D., Chambhare, M. R., Bansode, R. D. & Kabnoorkar, P. S. Impact of salinity on the morpho-biochemical traits of hydroponically cultivated spinacia Oleracea L. Biotechnologia 106, 49–62 (2025).

    Google Scholar 

  59. Rathakrishnan, D. & Gopalan, A. K. Isolation and characterization of halophilic isolates from Indian salterns and their screening for production of hydrolytic enzymes. Environ. Challenges. 6, 100426 (2021).

    Google Scholar 

  60. Gautam, A. & Phenol-Chloroform, D. N. A. Isolation method. 33–39 . https://doi.org/10.1007/978-3-030-94230-4_3 (Springer, 2022).

  61. Pérez-Inocencio, J. et al. Identification of halophilic and halotolerant bacteria from the root soil of the halophyte sesuvium verrucosum Raf. Plants 11, 3355 (2022).

    Google Scholar 

  62. Albdaiwi, R. N., Khyami-Horani, H., Al-Sayaydeh, R., Alananbeh, K. M. & Ayad, J. Y. Isolation and characterization of halotolerant plant growth promoting rhizobacteria from durum wheat (Triticum turgidum subsp. durum) cultivated in saline areas of the dead sea region. Front. Microbiol. 10, (2019).

  63. Jha, C. K., Saraf, M., Maheshwari, D. K., Patel, B. V. & Aeron, A. Enterobacter: role in plant growth promotion. 159–182. https://doi.org/10.1007/978-3-642-20332-9_8 (Springer, 2011).

  64. Kumar, S. R. et al. Methane-derived microbial biostimulant reduces greenhouse gas emissions and improves rice yield. Front. Plant. Sci. 15, (2024).

  65. Lim, J. M., Kim, C. J., Song, S. M. & Jeon, C. O. Pontibacillus chungwhensis gen. nov., sp. nov., a moderately halophilic Gram-positive bacterium from a solar saltern in Korea. Int. J. Syst. Evol. MicroBiol. 55, 165–170 (2005).

    Google Scholar 

  66. Sridhar, D. et al. The soil microbiome enhances sesame growth and oil composition, and soil nutrients under saline conditions. Sci. Rep. 15, (2025).

  67. Heath, R. L. & Packer, L. Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys. 125, 189–198 (1968).

    Google Scholar 

  68. Venkat, A., Bae, D. W. & Muneer, S. Circadian clock contributes to modulate salinity Stress-Responsive antioxidative mechanisms and Chloroplast proteome in spinacia Oleracea. Agriculture 13, 429 (2023).

    Google Scholar 

  69. Bajpai, V. K., Park, Y. H., Agrawal, P. & Phytochemicals Antioxidant and Anti-Lipid peroxidation activities of ethanolic extract of a medicinal Plant, A ndrographis paniculata. J. Food Biochem. 38, 584–591 (2014).

    Google Scholar 

  70. Pandey, S. & Gupta, S. Evaluation of Pseudomonas sp. for its multifarious plant growth promoting potential and its ability to alleviate biotic and abiotic stress in tomato (Solanum lycopersicum) plants. Sci. Rep. 10, (2020).

  71. Yadav, A. N. et al. Diversity and phylogenetic profiling of niche-specific bacilli from extreme environments of India. Ann. Microbiol. 65, 611–629 (2014).

    Google Scholar 

  72. Hänelt, I. & Müller, V. Molecular mechanisms of adaptation of the moderately halophilic bacterium halobacillis halophilus to its environment. Life 3, 234–243 (2013).

    Google Scholar 

  73. Chaiharn, M., Chunhaleuchanon, S. & Lumyong, S. Screening siderophore producing bacteria as potential biological control agent for fungal rice pathogens in Thailand. World J. Microbiol. Biotechnol. 25, 1919–1928 (2009).

    Google Scholar 

  74. Zhou, W., Qin, S., Lyu, D. & Zhang, P. Soil sterilisation and plant growth-promoting rhizobacteria promote root respiration and growth of sweet Cherry rootstocks. Arch. Agron. Soil. Sci. 61, 361–370 (2014).

    Google Scholar 

  75. Orhan, F. Alleviation of salt stress by halotolerant and halophilic plant growth-promoting bacteria in wheat (Triticum aestivum). Brazilian J. Microbiol. 47, 621–627 (2016).

    Google Scholar 

  76. Kearl, J. et al. Salt-tolerant halophyte rhizosphere bacteria stimulate growth of alfalfa in salty soil. Front. Microbiol. 10, (2019).

  77. Ha-Tran, D. M., Huang, E., Huang, C. C., Nguyen, T. T. M. & Hung, S. H. Roles of plant growth-promoting rhizobacteria (PGPR) in stimulating salinity stress defense in plants: A review. https://doi.org/10.20944/preprints202103.0041.v1 (2021).

  78. Zhao, J. et al. Synergistic effects of salt-Tolerant PGPR and foliar silicon on Pak Choi antioxidant defense under salt stress. Plants (Basel Switzerland). 14, 2065 (2025).

    Google Scholar 

  79. Shultana, R. et al. The PGPR mechanisms of salt stress adaptation and plant growth promotion. Agronomy 12, 2266 (2022).

    Google Scholar 

  80. Waheed, S. et al. Ca2SiO4 chemigation reduces cadmium localization in the subcellular leaf fractions of spinach (Spinacia Oleracea L.) under cadmium stress. Ecotoxicol. Environ. Saf. 207, 111230 (2020).

    Google Scholar 

  81. Gupta, S., Chauhan, R. & Pandey, S. Biopriming with halotolerant microbes enhances growth performance, resilience and rhizospheric microbial diversity of solanum melongena under saline conditions. Plant Physiol. Biochem. PPB 229, (2025).

  82. Kumar Arora, N. et al. Halo-tolerant plant growth promoting rhizobacteria for improving productivity and remediation of saline soils. J. Adv. Res. 26, 69–82 (2020).

    Google Scholar 

  83. Daraz, U. et al. Plant growth promoting rhizobacteria induced metal and salt stress tolerance in brassica juncea through ion homeostasis. Ecotoxicol. Environ. Saf. 267, 115657 (2023).

    Google Scholar 

  84. Khan, M. Y. et al. Potential of plant growth promoting bacterial consortium for improving the growth and yield of wheat under saline conditions. Front. Microbiol. 13, (2022).

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