Bio-Amelioration of Saline Soil Using Aeluropus littoralis, Arbuscular Mycorrhizal Fungus (AMF) and Salt-Resistant PGPB

Document Type : Original Research

Authors
Masoumeh Zarei
Elham Malekzadeh
Alireza Movahedi Naeini
Department of Soil Science, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Islamic Republic of Iran.
10.48311/jast.2026.16859
Abstract
This study aimed to evaluate the capability of the halophyte A. littoralis in symbiosis with Rhizophagus intraradices and Nocardia halotolerans, an indigenous bacterium of saline soils, on phyto-extraction of Na under saline conditions. Salinity treatments included 0 (S0), 100 mM NaCl (S1), 200 mM NaCl (S2), 100 mM NaCl+50mM K2SO4 (S3), and 200 mM NaCl+50mM K2SO4 (S4) levels. Plant fresh and dry weight and chlorophyll content decreased as salinity increased up to S2 level and increased thereafter. Plant root colonization in the inoculation and co-inoculation of AMF+SR-PGPB (Arbuscular Mycorrhizal Fungi (AMF) and Salt-Resistant Plant Growth-Promoting Bacteria) were similar. Compared to the S0 treatment, root colonization in the AMF group decreased by 23.5, 32.6, 13.5, and 26.7% under S1, S2, S3, and S4 treatments, respectively. In the Bacteria+AMF group, the reduction was smaller, with decreases of 2.8%, 3.4%, and an increase of 6.8 and 1.4% under S1, S2, S3, and S4 treatments, respectively. These results indicate that co-inoculation with PGPB mitigated the negative effects of salinity on root colonization. The root and soil glomalin contents increased as salinity increased. Root glomalin in plants inoculated by AMF+SR-PGPB was more than in a single inoculation of AMF under salt stress. This study highlights the potential application of salt-tolerant bacteria and AMF as effective strategies for enhancing plant growth and productivity in saline environments, contributing to sustainable agricultural practices in affected regions.
Keywords
Halophyte
Mycorrhizal symbiosis
Plant growth promoting traits
phytoremediation
Salinity stress
Subjects
1.       Aalipour, H., Nikbakht, A., Etemadi, N. and MacDonald, J. E. 2021. Co-Inoculation of Arizona cypress with Mycorrhizae and Rhizobacteria Affects Biomass, Nutrient Status, Water-Use Efficiency, and Glomalin-Related Soil Protein Concentration. Urban For. Urban Green., 60: 1-9.
2.       Adak, E. and Sengupta, S. 2023. Role of Polyhalite in Soil-Plant Nutrition Studies. Int. J. Agric. Nutr., 6(2): 32-34.
3.       Akram, M. S., Ashraf, M. and Akram, N. A. 2009. Effectiveness of Potassium Sulfate in Mitigating Salt-Induced Adverse Effects on Different Physio-Biochemical Attributes in Sunflower (Helianthus annuus L.). Flora: Morphol. Distrib. Funct. Ecol. Plants, 204(6): 471-483.
4.       Alexander, D. B. and Zuberrer, D. A. 1991. Use of Chrome Azurol S Reagent to Evaluate Siderophore Production by Rhizobacteria. Biol. Fertil. Soils, 12(1): 39-45.
5.       Al-Garni, S. M., Khan, M. M. and Bahieldin, A. 2019. Plant Growth-Promoting Bacteria and Silicon Fertilizer Enhance Plant Growth and Salinity Tolerance in Coriandrum sativum. J. Plant Interact., 14: 386-396.
6.       Animasaun, D. A., Oyedeji, S., Joseph, G. G., Adedibu, P. A. and Krishnamurthy, R. 2020. Sodium Chloride Stress Induced Differential Growth, Biomass Yield, and Phytochemical Composition Responses in the Halophytic Grass Aeluropus lagopoides L. West Afr. J. Appl. Ecol., 28(2): 31-40.
7.       Ansari, M., Shekari, F., Mohammadi, M. H., Juhos, K., Végvári, G. and Biró, B. 2019. Salt-Tolerant Plant Growth-Promoting Bacteria Enhanced Salinity Tolerance of Salt-Tolerant Alfalfa (Medicago sativa L.) Cultivars at High Salinity. Acta Physiol. Plant, 41: 195.
8.       Arnon, A. N. 1967. Method of Extraction of Chlorophyll in the Plants. Agron. J., 23: 112-121
9.       Ashfaq, M., Hassan, H. M., Ghazali, A. H. and Ahmad, M. 2020. Halotolerant Potassium Solubilizing Plant Growth Promoting Rhizobacteria May Improve Potassium Availability under Saline Conditions. Environ. Monit. Assess., 192: 697.
10.    Barhoumi, Z. 2018. Physiological Response of the Facultative Halophyte, Aeluropus littoralis, to Different Salt Types and Levels. Plant Biosyst., 153(2): 298-305.
11.    Barzegargolchini, B., Movafeghi, A., Dehestani, A. and Mehrabanjoubani, P. 2017. Morphological and Anatomical Changes in Stems of Aeluropus littoralis under Salt Stress. J. Plant Mol. Breed., 5(1): 40-48.
12.    Begum, N., Qin, C., Ahanger, MA., Raza, S, Khan, MI., Ashraf, M., Ahmed, N. and Zhang, L. 2019. Role of Arbuscular Mycorrhizal Fungi in Plant Growth Regulation: Implications in Abiotic Stress Tolerance. Front. Plant Sci., 10: 1068.
13.    Bradford, M. M. 1976. A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Anal. Biochem., 72: 248-254.
14.    Britto, D. T. and Kronzucker, H. J. 2008. Cellular Mechanisms of Potassium Transport in Plants. Physiol. Plant., 133(4): 637-650.
15.    Cakmak, I. 2005. The Role of Potassium in Alleviating Detrimental Effects of Abiotic Stresses in Plants. J. Plant Nutr. Soil Sci., 168(4): 521-530.
16.    Dashtebani, F., Hajiboland, R. and Aliasgharzad, N. 2014. Characterization of Salt-Tolerance Mechanisms in Mycorrhizal (Claroideoglomus etunicatum) Halophytic Grass,
Puccinellia distans. Acta Physiol. Plant., 36: 1713–1726.
17.    Debouba, M., Gouia, H., Suzuki, A. and Ghorbel, M. H. 2006. NaCl Stress Effects on Enzymes Involved in Nitrogen Assimilation Pathway in Tomato “Lycopersicon esculentum” Seedlings. J. Plant Physiol., 163(12): 1247-1258.
18.    Dey G, Banerjee, P., Sharma, R. K., Maity, J. P., Etesami, H., Shaw, A. K., Huang, Y. H., Huang, H. B. and Chen, C. Y. 2021. Management of Phosphorus in Salinity-Stressed Agriculture for Sustainable Crop Production by Salt-Tolerant Phosphate-Solubilizing Bacteria—A Review. Agronomy, 11(8): 1552.
19.    Diao, F., Dang, Z., Xu, J., Ding, S., Hao, B., Zhang, Z., Zhang, J., Wang, L. and Guo, W. 2021. Effect of Arbuscular Mycorrhizal Symbiosis Onion Homeostasis and Salt Tolerance-Related Gene Expression in Halophyte Suaeda salsa under Salt Treatments. Microbiol. Res., 24: 126688.
20.    Elhindi, K. M., El-Din, A. S. and Elgorban, A. M. 2017. The Iimpact of Arbuscular Mycorrhizal Fungi in Mitigating Salt-Induced Adverse Effects in Sweet Basil (Ocimum basilicum L.). Saud. J. Biol. Sci., 24:170-179.
21.    Fakhrfeshani, M., Shahriari-Ahmadi, F., Niazi, A., Moshtaghi, N. and Zare-Mehrjerdi, M. 2015. The Effect of Salinity Stress on Na+, K+ Concentration, Na+/K+ Ratio, Electrolyte Leakage and HKT Expression Profile in Roots of Aeluropus littoralis. J. Plant Mol. Breed., 3(2): 1-10.
22.    Feng, K., Cai, Z., Ding, T., Yan, H., Liu, X. and Zhang, Z. 2019. Effects of Potassium-Solubilizing and Photosynthetic Bacteria on Tolerance to Salt Stress in Maize. J. Appl. Microbiol., 126(5): 1530-1540.
23.    Filek, M., Walas, S., Mrowiec, H., Rudolphy-Skórska, E., Sieprawska, A. and Biesaga-Kościelniak, J. 2012. Membrane Permeability and Micro- and Macroelement Accumulation in Spring Wheat Cultivars during the Short-Term Effect of Salinity- and PEG-Induced Water Stress. Acta Physiol. Plant, 34: 985-995.
24.    Flowers, T. J., Munns, R. and Colmer, T. D. 2015. Sodium Chloride Toxicity and the Cellular Basis of Salt Tolerance in Halophytes. Annal. Bot., 115(3): 419-431.
25.    Garcia, CL., Dattamudi, S., Chanda, S. and Jayachandran, K. 2019. Effect of Salinity Stress and Microbial Inoculations on Glomalin Production and Plant Growth Parameters of Snap Bean (Phaseolus vulgaris). Agronomy, 9(9): 545.
26.    Gengmao, Z., Yu, H., Xing, S., Shihui, L., Quanmei, S. and Changhai, W. 2015. Salinity Stress Increases Secondary Metabolites and Enzyme Activity in Safflower. Ind. Crops Prod., 64: 175-181.
27.    Hajiboland, R., Dashtebani, F. and Aliasgharzad, N. 2015. Physiological Responses of Halophytic C4 Grass Aeluropus littoralis to Salinity and Arbuscular Mycorrhizal Fungi Colonization. Photosynthetica, 53: 572-584.
28.    Hashem, A., Abd_Allah, E. F., Alqarawi, A. A., Al-Huqail, A. A., Wirth, S. and Egamberdieva, D. 2016. The Interaction between Arbuscular Mycorrhizal Fungi and Endophytic Bacteria Enhances Plant Growth of Acacia gerrardii under Salt Stress. Front. Microbiol., 7: 1089.
29.    Jeon, J. S., Lee, S. S., Kim, H. Y., Ahn, T. S. and Song, H. G. 2003. Plant Growth Promoting in Soil by Some Inoculated Microorganism. J. Microbiol., 41(4): 271-276.
30.    Kormanik, P. P. and McGraw A. C. 1982. Quantification of Vesicular-Arbuscular Mycorrhizae in Plant Roots. In: “Methods and Principles of Mycorrhizal Research”, (Ed.): Schenck, N. C. American Phytopathological Society, St. Paul, PP. 37-45.
31.    Kutilek, M. and Nielsen, D. R. 1994. Soil Hydrology. Catena Verlag, Cremlingen.
32.    Meena, V. S., Maurya, B. R., Verma, J. P., Aeron, A., Kumar, A., Kim, K. and Bajpai, V. K. 2015. Potassium Solubilizing Rhizobacteria (KSR): Isolation, Identification, and K-Release Dynamics from Waste Mica. Ecol. Eng., 81: 340-347.
33.    Millner, P. D. and Kitt, D. G. 1992. The Beltsville Method for Soilless Production of
Vesicular Arbuscular Mycorrhizal Fungi. Mycorrhiza, 2: 9-15.
34.    Moreira, H., Pereira, S. I., Vega, A., Castro, P. M. and Marques, A. P. 2020. Synergistic Effects of Arbuscular Mycorrhizal Fungi and Plant Growth-Promoting Bacteria Benefit Maize Growth under Increasing Soil Salinity. J. Environ. Manag., 257: 109982.
35.    Moshtaghi Nikou, M., Ramezani, M., Ali Amoozegar, M., Rasooli, M., Harirchi, S., Shahzadeh Fazeli, S. A., Schumann, P., Spröer, C. and Ventosa, A. 2015. Nocardia halotolerans sp. nov., a Halotolerant Actinomycete Isolated from Saline Soil. Int. J. Syst. Evol. Microbiol., 65(9):3148-3154.
36.    Oksana, O., Hermansah, H., Agustian, A., Syafrimen, S. and Yasin, S. 2024. Soil Sulfur Dynamics and Their Role in Plant Growth and Development. J. Agron. Tanaman Tropika (JUATIKA), 6(3): 850-868.
37.    Patten, C. L. and Glick, B. R. 2002. Role of Pseudomonas putida Indoleacetic Acid in Development of the Host Plant Root System. Appl. Environ. Microbiol., 68(8): 3795-3801.
38.    Penrose, D. M. and Glick, B. R. 2001. Levels of ACC and Related Compounds in Exudate and Extracts of Canola Seeds Treated with ACC Deaminase-Containing Plant Growth-Promoting Bacteria. Can. J. Microbiol., 47(4): 368-372.
39.    Praveen, A. and Singh, S. 2024. The Role of Potassium under Salinity Stress in Crop Plants. Cereal Res. Commun., 52(2): 315-322.
40.    Qin, S., Feng, W. W., Zhang, Y. J., Wang, T. T., Xiong, Y. W. and Xing, K. 2018. Diversity of Bacterial Microbiota of Coastal Halophyte Limonium sinense and Amelioration of Salinity Stress Damage by Symbiotic Plant Growth-Promoting Actinobacterium Glutamicibacter halophytocola KLBMP 5180. Appl. Environ. Microbiol., 84: e01533-18.
41.    Rojas-Tapias, D., Moreno-Galván, A., Pardo-Díaz, S., Obando, M., Rivera, D. and Bonilla, R. 2012. Effect of Inoculation with Plant Growth-Promoting Bacteria (PGPB) on Amelioration of Saline Stress in Maize (Zea mays). Appl. Soil Ecol., 61: 264-272.
42.    Rosier, C. L., Hoye, A. T. and Rillig, M. C. 2006. Glomalin-Related Soil Protein: Assessment of Current Detection and Quantification Tools. Soil. Biol. Biochem., 38: 2205-2211.
43.    Shiferaw, B. and Baker, D. A. 1996. An Evaluation of Drought Screening Techniques for Eragrostis tef. Trop. Sci., 36: 74-85.
44.    Solórzano-Acosta, R., Toro, M. and Zúñiga-Dávila, D. 2023. Plant Growth Promoting Bacteria and Arbuscular Mycorrhizae Improve the Growth of Persea americana var. Zutano under Salt Stress Conditions. J. Fungi., 9: 233.
45.    Suarez, C., Cardinale, M., Ratering, S., Steffens, D., Jung, S., Montoya, A. M., Geissler-Plaum, R. and Schnell, S. 2015. Plant Growth-Promoting Effects of Hartmannibacter diazotrophicus on Summer Barley (Hordeum vulgare L.) under Salt Stress. Appl. Soil Ecol., 95: 23-30.
46.    Talbi Zribi, O., Mbarki, S., Metoui, O., Trabelsi, N., Zribi, F., Ksouri, R. and Abdelly, C. 2020. Salinity and Phosphorus Availability Differentially Affect Plant Growth, Leaf Morphology, Water Relations, Solutes Accumulation and Antioxidant Capacity in Aeluropus littoralis. Plant Biosyst., 155(4): 935-943.
47.    Wang, H., An, T., Huang, D., Liu, R., Xu, B., Zhang, S., Deng, X., Siddique, K. H. and Chen, Y. 2021. Arbuscular Mycorrhizal Symbiosis Alleviating Salt Stress in Maize is Associated with a Decline in Root-to-Leaf Gradient of Na+/K+ Ratio. BMC Plant Biol., 21: 457.
48.    Wang, Y., Lin J., Huang, S., Zhang, L., Zhao, W. andYang, C. 2019. Isobaric Tags for Relative and Absolute Quantification-Based Proteomic Analysis of Puccinellia tenuiflora Inoculated with Arbuscular Mycorrhizal Fungi Reveal Stress Response Mechanisms in Alkali-Degraded Soil. Land Degrad. Dev., 30: 1584-1598.
49.    Wasaya, A., Affan, M., Ahmad Yasir, T., Mubeen, K., Rehman, H. U., Ali, M., Nawaz, F., Galal, A., Iqbal, M. A., Islam, M. S., El-Sharnouby, M., Rahman, M. H. u. and EL Sabagh, A. 2021. Foliar Potassium Sulfate Application Improved Photosynthetic Characteristics, Water Relations and Seedling Growth of Drought-Stressed Maize. Atmosphere, 12(6): 663.
50.    Wei, D. D., Cheng, D., Liu, W. B., Liu, T., Yang, X. H. and Zheng, Y. H. 2016. Adequate Potassium Application Enhances Salt Tolerance of Moderate-Halophyte Sophora alopecuroides. Plant Soil Environ. 61: 364–370.
51.    Wright, S. F., Franke-Snyder, M., Morton, J. B. and Upadhyaya, A. 1996. Time-Course Study and Partial Characterization of a Protein on Hyphae of Arbuscular Mycorrhizal Fungi during Active Colonization of Roots. Plant Soil., 181: 193-203.
52.    Yañez-Yazlle, M. F., Romano-Armada, N., Acreche, M. M., Rajal, V. B. and Irazusta, V. P. 2021. Halotolerant Bacteria Isolated from Extreme Environments Induce Seed Germination and Growth of Chia (Salvia hispanica L.) and Quinoa (Chenopodium quinoa Willd.) under Saline Stress. Ecotoxicol. Environ. Saf., 218: 112273.
53.    Yang, C. X., Zhao, W. N. and Wang, Y. D. 2019. Isolation and Identification of Three Dominant Arbuscular Mycorrhizal Fungi in Rhizosphere of Puccinellia tenuiflora from Saline-Alkaline Grassland of Songnen Plain. Sydowia., 71: 247–253.
54.    Yasmin, H., Naeem, S., Bakhtawar, M., Jabeen, Z., Nosheen, A., Naz, R., Keyani, R., Mumtaz, S. and Hassan, M. N. 2020. Halotolerant Rhizobacteria Pseudomonas pseudoalcaligenes and Bacillus subtilis Mediate Systemic Tolerance in Hydroponically Grown Soybean (Glycine max L.) against Salinity Stress. PLoS ONE, 15(4): e0231348.
55.    Zhou, N., Zhao, S. and Tian, C. Y. 2017. Effect of Halotolerant Rhizobacteria Isolated from Halophytes on the Growth of Sugar Beet (Beta vulgaris L.) under Salt Stress. FEMS Microbiol. Lett., 364(11): fnx091.
 
Journal of Agricultural Science and Technology
Volume 28, Issue 3
May and June 2026
Pages 731-745