Dryland Soil Research (DLSR)

Dryland Soil Research (DLSR)

Enhancing salinity tolerance in ornamental sunflower (Helianthus annuus L.) through mycorrhizal symbiosis

Document Type : Original Article

Authors
1 Department of Horticulture, Faculty of Agriculture, Shahrekord University, Shahrekord, Iran
2 Soil Science and engineering, Faculty of Agricultural, Shahrekord University, Iran
Abstract
Salt accumulation in the agricultural soils are inevidable when irrigation is performed by saline water. This phenomenon is a global challenge especially in the drylands. Vesicular-arbuscularmycorrhizal fungi (VAM) as biofertilizers that form symbiotic associations with plant roots are natural and suitable amendments for somehow overcoming this problem. The currentc study aimed to investigate the potential of mycorrhizal fungi (VAM) to enhance the growth of ornamental sunflowers (Helianthus annuus L.) cultivated under salinity stress conditions in a pot culture system. The overarching objective was to identify sustainable strategies that mitigate environmental challenges, such as soil salinity, and decrease reliance on chemical fertilizers. A 3×4 factorial experiment was conducted using a completely randomized design with three replications. The experimental factors included three salinity levels (a control without NaCl, 50 and 100 mM NaCl) and four VAM species (uninoculated plant as the control, and plants inoculated with Rhizophagus irregularis, Funneliformis mosseae, and Glomus howei species). Plant growth parameters, including flower diameter, fresh and dry weights of flowers, shoot and root biomasses, proline level, chlorophyll content, relative water content, malondialdehyde content, ion leakage, and root colonization percentage were measured after plant harvest. The results showed that salinity stress, VAM inoculation, and their interaction significantly affected most plant growth indices. Higher salinity levels led to a decrease root and flower weights, flower diameter, and chlorophyll content, while proline contents and ion leakage were positively affected by high soil salt content. At high salinity levels (100 mM), inoculation with F. mosseae had the greatest effect on improving plant growth. The fresh weight of flowers (16.4 g), shoots (27.6 g pot-1), roots (6.57 gpot-1), and total chlorophyll (36.0 mg g-1 of fresh weight) were higher in the treatment inoculated with F. mosseae and without salinity. The highest proline content (5.6 μmol g-1 fresh weight) and ion leakage (76.4%) values were observed in the non-VAM and 100 mM NaCl treatments. The symbiotic relationship between arbuscular mycorrhizal fungi and plants constitutes a mutually advantageous biological interaction, substantially enhanced plant growth and productivity. The findings suggest that VAM inoculation can improve plant growth and ornamental value under salinity stress. Compared to other species, Funneliformis mosseae showed greater capacity to enhance the quantity and quality of ornamental sunflower production.
Keywords
Subjects

Ahmed, J.U., Linda, I.J., Majid, M.A., (2018). Royal floraholland: Strategic supply chain of cut flowers business. In Sage Business Cases. SAGE Publications, Ltd., ISBN 9781526461919.
Ahmed, M.E., Abdel-Fattah, G.G., Holford, P., Korany, S.M., Alsherif, E.A., AbdElgawad, H., Ulhassan, Z., Josko, I., Ali, B., Sheteiwy, M.S., (2023). Funneliformis constrictum modulates polyamine metabolism to enhance tolerance of Zea mays L. to salinity. Microbiol. Res., 266(2023): 127254.
Alia Mohanty, P., Matysik, J., (2001). Effect of proline on the production of singlet oxygen. Amino Acids., 21(2): 195-200.
Ashraf, M., and Foolad, M.A., (2007). Roles of Glycine Betaine and Proline in Improving Plant Abiotic Stress Resistance. Environ. Experim. Bot., 59, 206-216.
Banuelos, J., Alarcón, A., Larsen, J., Cruz-Sánchez, S., Trejo-Aguilar, D., (2014). Interactions between arbuscular mycorrhizal fungi and Meloidogyne incognita in the ornamental plant Impatiens balsamina. J. Soil Sci. Plant Nutr., 14(1): 63-74.
Bates, L.S., Waldren, R.P., Teare, I.D., (1973). Rapid determination of free proline for water-stress studies. Plant Soil., 39(1): 205-207.
Bencherif, K., Boutekrabt, A., Fontaine, J., Laruelle, F., Dalpè, Y., Lounès-Hadj, A.L., (2015). Impact of soil salinity on arbuscular mycorrhizal fungi biodiversity and microflora biomass associated with Tamarix articulata Vahll rhizosphere in arid and semi-arid Algerian areas. Sci. Total Environ., 533:488-494.
Bennett, A.E., Classen, A.T.  (2020). Climate change influences mycorrhizal fungal–plant interactions, but conclusions are limited by geographical study bias. Ecology, 101(4):e02978. 10.1002/ecy.2978
Boorboori, M.R., Lackóová, L., (2025). Arbuscular mycorrhizal fungi and salinity stress mitigation in plants. Front. Plant Sci., 15:1504970.
Carter, C.T., Grieve, C.M., (2010). Growth and Nutrition of Two Cultivars of Zinnia elegans Under Saline Conditions. Hort. Sci., 45(7): 1058- 1063.
Chen, W., Mou, X., Meng, P., Chen, J., Tang, X., Meng, G., Xin, K., Zhang, Y., Wang, C., (2023). Effects of arbuscular mycorrhizal fungus inoculation on the growth and nitrogen metabolism of Catalpa bungei C.A.Mey. under different nitrogen levels. Front. Plant Sci., 14:1138184. doi: 10.3389/fpls.2023.1138184.
Dastogeer, K.M.G., Zahan, M.I., Tahjib-Ul-Arif, M., Akter, M.A., Okazaki, S., (2020). Plant Salinity Tolerance Conferred by Arbuscular Mycorrhizal Fungi and Associated Mechanisms: A Meta-Analysis. Front. Plant Sci., 11:588550.
Dianti, B., Arghawani, M., Khairi, A.A., Amanifar, S., (2019). The effect of mycorrhizal fungi on the morphophysiological characteristics of Teucrium chamaedrys L. under salinity stress conditions. Iranian J. Hort. Sci., 51(3): 621-632.
Fall, A.F., Nakabonge, G., Ssekandi, J., Founoune-Mboup, H., Apori, S.O., Ndiaye, A., Badji, A., Ngom, K., (2022). Roles of Arbuscular Mycorrhizal Fungi on Soil Fertility: Contribution in the Improvement of Physical, Chemical, and Biological Properties of the Soil. Front. Fungal Biol., 3:723892.
Ferrante, A., Ferrini, F., (2023). Floriculture and landscapes: Perspectives and challenges. Front. Hortic., 2:1123298.
Galal, H., lindell. B., (2010). Evolution of halophytes multiple origins of salt tolerance land plants. Funct. Plant Biol., 37(7):604-612.
Giovannetti, M., Mosse, B., (1980). An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol., 84(3): 489-500. http://dx.doi.org/10.1111/j.1469-8137.1980.tb04556.x
Hasanuzzaman, M., Raihan, M.R.H., Masud, A.A.C., Rahman, K., Nowroz, F., Rahman, M., Nahar, K., Fujita, M., (2021). Regulation of Reactive Oxygen Species and Antioxidant Defense in Plants under Salinity. Int. J.Mol. Sci., 22(17), 9326.
Hashem, A., Alqarawi, A.A., Radhakrishnan, R., Fahad A.B., Horiah, A.A., Aldehaish, A., Egamberdieva, D., Abd-Allah, E.F., (2018). Arbuscular mycorrhizal fungi regulate the oxidative system, hormones and ionic equilibrium to trigger salt stress tolerance in Cucumis sativus L., Saudi J. Biol. Sci., 25 (6): 1102-1114.
Heath, R.L., Packer, L., (1968). Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys., 125(1): 189-198.
Isayenkov, S.V., Maathuis, F.J., (2019). Plant salinity stress: many unanswered questions remain. Front. Plant Sci., 10:80.
Joshan, Y., Sani, B., Jaberi, H., Mozafari, H., Moaveni, P., (2020). The effect of late season drought stress on some morphophysiological characteristics of Iranian safflower varieties in Karaj región. Environ. Stresses Crop Sci., 13(4): 1093-1104.
Kakabouki, I., Stavropoulos, P., Roussis, I., Mavroeidis, A., Bilalis, D., (2023). Contribution of arbuscular mycorrhizal fungi (VAM) in improving the growth and yield performances of flax (Linum usitatissimum L.) to salinity stress. Agronomy, 13(9), 2416.
Kalaji, H., Govindjee, M., Bosa, K., Koscielniak, J., Zuk Gołaszewska, K., (2011). Effects of salt stress on photosystem II efficiency and C assimilation of two Syrian barley landraces. Environ. Exp. Bot., 73: 64-72.
Khaliq, A., Perveen, S., Alamer, K.H., Zia Ul Haq, M., Rafique, Z., Alsudays, I.M., Althobaiti, A.T., Saleh, M.A., Hussain, S., Attia, H., (2022). Arbuscular Mycorrhizal Fungi Symbiosis to Enhance Plant–Soil Interaction. Sustainability, 14(13), 7840.
Khan, M.N., Siddiqui, M.H., Mohammad, F., Khan, M.M.A., Naeem, M., (2007). Salinity induced changes in growth, enzyme activities, photosynthesis, proline accumulation and yield in linseed genotypes. World J. Agr. Sci., 3:685-695.
Khandan Mirkohi, A.A., Sheikh Asadi, M., Taheri, M.R., Babalar, M., (2014). The effect of arbuscular mycorrhizal fungi and different levels of phosphorus on some aspects of Lisianthus plant growth. J. Sci. Techniq. Greenh. Cul., 6(22):57- 67.
Knapp, A.K., Hoover, D.L., Wilcox, K.R., Avolio M.L, Koerner, S.E., La Pierre, K.J, Loik, M.E., Luo, Y.Q., Sala, O.E., Smith, M.D. (2015). Characterizing differences in precipitation regimes of extreme wet and dry years: implications for climate change experiments. Global Change Biol. 21:2624–2633.
Krasilnikov, P., Taboada, M. A., Amanullah, A., (2022). Fertilizer Use, Soil Health and Agricultural Sustainability. Agriculture, 12(4), 462.
Larrainzar, E., Wienkoop, S., (2017). A Proteomic View on the Role of Legume Symbiotic Interactions. Front. Plant Sci., 8: 1267.
Li, W., Chen, K., Li, Q., Tang, Y., Jiang, Y., Su, Y., (2023a). Effects of Arbuscular Mycorrhizal Fungi on Alleviating Cadmium Stress in Medicago truncatula Gaertn. Plants, 12(3):547.
Li, W., Zhai, Y.L., Hu, X.Y., Guo, S.H., (2023b). Effects of arbuscular mycorrhizal fungi on the growth and metabolism of perennial ryegrass (Lolium perenne) under salt stress. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 51(1):12649.
Lichtenthaler, H.K., Wellburn, A.R., (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem. Soc. Trans., 11 (5): 591–592.
Lutts, S., Chinet, J.M., Bouharmont, J., (1995). Changes in plant response to NaCl during development of rice (Oryza sativa L.) varieties differing in salinity resistance. J. Experim. Bot., 46 (293):1843-1852.
Machado, R.M.A., Serralheiro, R.P., (2017). Soil Salinity: Effect on Vegetable Crop Growth. Management practices to prevent and mitigate soil salinization. Sci. Hortic., 10: 339-350.
Nakamichi, N., Takao, S., Kudo, T., Kiba, T., Wang, Y., Kinoshita, T., Sakakibara, H., (2016). Improvement of Arabidopsis biomass and cold, drought and salinity stress tolerance by modified circadian clock-associated PSEUDO-RESPONSE REGULATORs. Plant Cell Physiol., 57(5): 1085-1097.
Negacz, K., Malek, Ž., de Vos, A., Vellinga, P., (2022). Saline soils worldwide: identifying the most promising areas for saline agriculture. J. Arid. Environ., 203:104775.
Nejati-Sini, H., Barzegar, R., Soodaee-Mashaee, S., Ghasemi-Ghahsare, M., Mousavi-Fard, S., Mozafarian, M., (2024). Effects of biofertilizer on the production of bell pepper (Capsicum annuum L.) in greenhouse. J. Agric. Food Res., 16:101060.
Ozlem, F., Unyayar, S., Ortas, I., (2012). Effects of arbuscular mycorrhizal inoculation on biochemical parameters in Capsicum annum grown under long term salt stress. Turk. J. Bot., 36: 63-72.
Paiva, P.D.O., Beruto, M.I., Paiva, R., Verdonk, J.C., (2024). Editorial: Quality of ornamental crops: effect of genotype, preharvest, and improved production chains on quality attributes of ornamental crops, volume II. Front. Plant Sci., 15:1449585.
Pandit, K., Kaur, C.S., Kumar, M., Bhardwaj, R., Kaur, S., (2024). Chapter Six- Salinity stress: Impact on plant growth, Editor(s): Sharma, A., Kumar, M., Sharma, P., Advances in Food Security and Sustainability, Elsevier, 9:145-160.
Parida, A.K., Das, A.B., (2005). Salt tolerance and salinity effects on plants: Review. Ecotoxic. Environ. Saf., 60(3): 324-349.
Porcel, R., Aroca, R., Ruiz-Lozano, J.M., (2012). Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron. Sustainable Dev., 32(1): 181–200.
Porras-Soriano, A., Soriano-Martin, M.L., Porras-Piedra, A., Azcon, R., (2009). Arbuscular mycorrhizal fungi increased growth, nutrient uptake and tolerance to salinity in olive trees under nursery conditions. J. Plant Physiol., 166(13):1350–1359.
Puttamadanayaka, S., Emayavaramban, P., Yadav, P.K., Radhakrishna, A., Mehta, B.K., Chandra, A., Ahmad, S., Sanivarapu, H., Siddaiah, C.N., Yogendra, K., (2024). Unravelling the molecular mechanism underlying drought stress tolerance in Dinanath (Pennisetum pedicellatum Trin.) Grass via integrated transcriptomic and metabolomics analyses. BMC Plant Biol., 24(1):928.
Ratnakar, A., Rai, A., (2013). Alleviation of the Effects of NaCl Salinity in Spinach (Spinacia oleracea L. var. All Green) Using Plant Growth Regulators. J. Stress Physiol. Biochem., 9(3): 122-128.
Raza, A., Charagh, S., Abbas, S., Hassan, M.U., Saeed, F., Haider, S., Sharif, R., Anand, A., Corpas, F.J. Jin, W., (2023). Assessment of proline function in higher plants under extreme temperatures. Plant Biol., 25:379-395.
Renzetti, M., Funck, D., Trovato, M., (2025). Proline and ROS: A Unified Mechanism in Plant Development and Stress Response? Plants, 14(1), 2
Sabra, A., Daayf, F., Renault, S., (2012). Differential physiological and biochemical responses of three Echinacea species to salinity stress. Sci. Hortic., 135: 23-31
Schubert. A., Hayman, D.S., (1986). Plant growth responses to vesicular- arbuscular mycorrhiza: X V I. Effectiveness of different endophytes at different levels of soil phosphate. New Phytol., 103(1):79-90
Sheikh-Assadi, M., Khandan-Mirkohi, A., Taheri, M.R., Babalar, M., Sheikhi, H., Nicola, S., (2023). Arbuscular mycorrhizae contribute to growth, nutrient uptake, and ornamental characteristics of statice (Limonium sinuatum [L.] Mill.) subject to appropriate inoculum and optimal phosphorus. Horticulturae, 9 (5): 564
Shuyskaya, E., Rakhmankulova, Z., Prokofieva, M., Kazantseva, V., Lunkova, N., (2023). Impact of Salinity, Elevated Temperature, and Their Interaction with the Photosynthetic Efficiency of Halophyte Crop Chenopodium quinoa Willd. Agriculture, 13(6), 1198
Siddiqui, M.H., Khan, M.N., Mohammad, F., Khan, M.M.A., (2008). Role of nitrogen and gibberellin (GA3) in the regulation of enzyme activities and in osmoprotectant accumulation in Brassica juncea L. under salt stress. J. Agron. Crop Sci., 194:214–224
Smart, R.E., Bingham, G.E., (1974). Rapid estimates of relative water content. Plant Physiol., 53: 258-260
Tang, H., Du, L., Xia, C., Luo, J., (2024). Bridging gaps and seeding futures: A synthesis of soil salinization and the role of plant-soil interactions under climate change. iScience, 27(9):110804
Valenzuela-Aragon, B., Cardinale, M., Rolli, E., Rustioni, L., Francioli, D., (2025). The role of arbuscular mycorrhizal fungi in abiotic stress management in viticulture under climatic shifts. Plant Stress., 16:100863
Vaudo, A.D., Erickson, E, Patch, H.M., Grozinger, C.M., Mu, J.P., (2022). Impacts of soil nutrition on floral traits, pollinator attraction, and fitness in cucumbers (Cucumis sativus L.). Sci. Rep., 12: 21802
Wahid, F., Fahad, S., Danish, S., Adnan, M., Yue, Z., Saud, S.; Siddiqui, M.H., Brtnicky, M., Hammerschmiedt, T., Datta, R., (2020). Sustainable Management with Mycorrhizae and Phosphate Solubilizing Bacteria for Enhanced Phosphorus Uptake in Calcareous Soils. Agriculture., 10, 334
Wei, H., Li, X., He, W., Kuang, Y., Wang, Z., Hu, W., Tang, M., Chen, H., (2023). Arbuscular mycorrhizal symbiosis enhances perennial ryegrass growth during temperature stress through the modulation of antioxidant defense and hormone levels. Ind. Crops Prod., 195:116412
White, P.J., Hammond, J.P., (2008). The ecophysiology of plant–phosphorus interactions. Berlin, Germany: Springer
Witzel, K., Motos, J.R.A., Atay, E., Çiçek, N., Mistríková, V., Oney-Birol, S., Soto, S.R., Solymosi, K., Yücedağ, C., Papenbrock, J., (2025). Leveraging microorganisms and biostimulants: mitigating salinity stress in crops with agricultural biologicals. Plant Soil., 1573-5036
Xu, W., Liu, Q., Wang, B., Zhang, N., Qiu, R., Yuan, Y., Yang, M., Wang, F., Mei, L., Cui, G., (2024). Arbuscular mycorrhizal fungi communities and promoting the growth of alfalfa in saline ecosystems of northern China. Front. Plant Sci., 15:1438771
Yoshiba, Y., Kiyosue, T., Nakashima, K., Yamaguchi-Shinozaki, K., Shinozaki, K., (1997). Regulation of levels of proline as an osmolyte in plants under water stress. Plant Cell Physiol., 38 (10), 1095–1102
Zeidali, E., Naseri, R., Mirzaei, A., Fathi, A., Darabi, F., (2018). Study the effect of plant nourishment with chemical, PGPR and manure fertilizers on agro-physiologic characteristics and weed density of maize. J. Plant Ecophysiol., 10(32): 198-214
Zhang, D.-J., Tong, C.-L., Wang, Q.-S., Bie, S., (2024). Mycorrhizas affect physiological performance, antioxidant system, photosynthesis, endogenous hormones, and water content in cotton under salt stress. Plants, 13, 805
Zhao, S., Zhang, Q., Liu, M., Zhou, H., Ma, C., Wang, P., (2021). Regulation of plant responses to salt stress. Int. J. Molecular Sci., 22(9):4609
Ziaei, Z., Dehestani-Ardakani, M., Shirmardi, M., Azimi, M.H., (2019). Effect of mycorrhizal fungus on some morphophysiological characteristics of three genotypes of German iris (Iris germanica) under salt stress. Plant Proc. Funct., 9(38): 397- 414
Zou, Y.N., Wu, Q.S., (2011). Efficiencies of five arbuscular mycorrhizal fungi in alleviating salt stress of trifoliate orange. Int. J. Agr. Biol., 13(6): 991-995.

تحت نظارت وف ایرانی