Effect of foliar application of salicylic acid and inoculation with mycorrhizal fungi on some physiological and biochemical traits of barley (Hordeum vulgare L.) cv. Fortuna under different salinity levels

Articles in Press

Document Type : Original Article

Authors

1 Ph.D. Student in Crop Physiology, Department of Plant Production and Genetics Engineering, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran

2 Professor in Crop Physiology, Department of Plant Ecophysiology, Faculty of Agriculture, University of Tabriz, Tabriz, Iran

3 Professor in Crop Physiology, Department of Plant Production and Genetics Engineering, Faculty of Agriculture and Natural Resources, Ardabil, Iran

4 Associate Professor in Soil Chemistry and Fertility, Department of Soil Science Engineering, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran

5 Assistant Professor, Department of Plant Physiology, Germi Branch, Islamic Azad University, Germi, Iran

Abstract

Introduction
Soil salinity is a major abiotic stress that limits plant growth and productivity. Agricultural soil salinity induces several detrimental effects, including oxidative stress, osmotic stress, and disturbances in nutrient uptake. However, plants that can enhance their defense mechanisms by sustaining antioxidant capacity, maintaining osmotic adjustment, and improving nutrient acquisition under saline conditions are able to exhibit relatively stable growth and acceptable performance under such conditions. Salicylic acid and mycorrhizal fungi symbiosis play essential roles in alleviating the adverse effects of salinity by inducing antioxidant defenses and regulating carbohydrate metabolism in crops. Mycorrhizae can enhance plant growth and performance through several mechanisms, including mitigating the adverse effects of salinity, improving plant water status, producing growth-promoting hormones, and enhancing photosynthesis. Salicylic acid, synthesized in root cells, plays a central role in regulating physiological processes and functions as a key signaling molecule in activating plant defense responses. Soluble sugars, along with free proline, function as osmotic regulators and signaling molecules that trigger diverse defense responses under salt stress.
 
Materials and methods
In the present study, the effects of foliar application of salicylic acid (0, 0.6, and 1.2 mM) on enhancing the symbiotic association with arbuscular mycorrhizal fungi and its consequent impacts on plant growth, membrane stability, antioxidant enzyme activities, free proline and soluble sugar contents, as well as maximum quantum efficiency of photosystem II (Fv/Fm), were investigated in barley (Hordeum vulgare L. cv. Fortuna) under salinity stress (0, 60, and 120 mM NaCl). The present experiment was conducted as a factorial arrangement in a randomized complete block design (RCBD) with three replications at the Research Greenhouse Complex of the Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, during the 2021–2022 growing season.
 
Results and discussion
The combined application of mycorrhizal fungus and salicylic acid significantly increased relative water content of leaves by 125.92% under salt stress. Inoculation with mycorrhizal fungi markedly enhanced cell membrane stability index, maximum quantum yield of photosystem II (Fv/Fm), total chlorophyll, chlorophyll a, free proline content, and polyphenol oxidase (PPO) activity. Foliar application of salicylic acid also led to significant increases in cell membrane stability index, maximum quantum yield of photosystem II, total chlorophyll, chlorophyll a and b content, soluble sugar content, and PPO activity.
 
Conclusion
Application of both salicylic acid and mycorrhizal fungi enhanced the tolerance of barley cv. Fortuna to salinity stress, primarily by improving leaf relative water content, maintaining cell membrane integrity, increasing chlorophyll concentration, and enhancing PPO activity.
 
Acknowledgements
This study was conducted as part of the doctoral dissertation of the first author at the Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili. The authors gratefully acknowledge the valuable assistance and cooperation of all individuals who contributed to the execution and preparation of this work.

Keywords

Main Subjects

References

Abdel-Fattah, G.M., Asrar, A.W.A., 2012. Arbuscular mycorrhizal fungal application to improve growth and tolerance of wheat (Triticum aestivum L.) plants grown in saline soil. Acta Physiologiae Plantarum. 34(1), 267-277. https://doi.org/10.1007/s11738-011-0825-6
Abdoli Nasab, M., Mohammadi Sedaran, Z., 2021. Effect of drought tension application on the germination, physiological and biochemical characteristics of rapeseed cultivars (Brassica napus L.). Crop Physiology Journal. 12(48), 81-96. [In Persian with English Summary]. https://doi.org/10.22034/saps.2022.52705.2901
Aghaei, F., Seyed Sharifi, R., Narimani, H., 2022. Effects of uniconazole and biofertilizers on yield, chlorophyll fluorescence indices and some physiological traits of wheat under salinity soil conditions. Journal of Plant Research (Iranian Journal of Biology). 35, 112-124. [In Persian with English Summary].
Albrecht, S.L., Douglas Jr, C.L., Klepper, E.L., Rasmussen, P.E., Rickman, R.W., Smiley, R.W., Wilkins, D.E., Wysocki, D.J., 1995. Effects of foliar methanol applications on crop yield. Crop Science. 35, 1642-1646. https://doi.org/10.2135/cropsci1995.0011183X003500060021x
Apon, T.A., Ahmed, S.F., Bony, Z.F., Chowdhury, M.R., Asha, J.F., Biswas, A., 2023. Sett priming with salicylic acid improves salinity tolerance of sugarcane (Saccharum officinarum L.) during early stages of crop development. Heliyon, 9(5). https://doi.org/10.1016/j.heliyon.2023.e16030
Arnon, D.I., 1967. Photosynthetic activity of isolated chloroplasts. Physiological Review. 47, 317-58. https://doi.org/10.1152/physrev.1967.47.3.317
Asghari, M., 2023. Effect of Trichoderma and biochar application on some morpho-physiological traits of sainfoin seedlings grown in soils containing heavy metals. Journal of Plant Process and Function. 12, 219-238. [In Persian with English Summary].  http://jispp.iut.ac.ir/article-1-1711-en.html
Bagues, M., Neji, M., Karbout, N., Boussora, F., Triki, T., Guasmi, F., Nagaz, K., 2024. Mitigating salinity stress in barley (Hordeum vulgare L.) through biochar and NPK fertilizers: impacts on physio-biochemical behavior and grain yield. Agronomy, 14(2), 317. https://doi.org/10.3390/agronomy14020317
Basak, H., Mesut Cimrin, K., Turan, M., 2024. Effects of mycorrhiza on plant nutrition, enzyme activities, and lipid peroxidation in Pepper grown under salinity stress. Journal of Agricultural Science and Technology. 26(2), 359-369.
Bates, L.S., Waldren, R.P.A., Teare, I.D., 1973. Rapid determination of free proline for water-stress studies. Plant and Soil, 39(1), 205-207. https://doi.org/10.1007/BF00018060
Bolandi, M., Sheikhzadeh, P., Khomari, S., Zare, N., Sharifi, J., 2023. The effect of seed pretreatment and foliar application of growth regulators and potassium nitrate on physiological, biochemical characteristics, yield and yield components of borage (Borago officinalisL). Iranian Journal of Field Crops Research. 4(21), 459-484. [In Persian with English Summary].  https://doi.org/10.22067/jcesc.2023.82741.1251
Boussora, F., Triki, T., Bennani, L., Bagues, M., Ben Ali, S., Ferchichi, A., Guasmi, F., 2024. Mineral accumulation, relative water content and gas exchange are the main physiological regulating mechanisms to cope with salt stress in barley. Scientific Reports. 14, 14931. https://doi.org/10.1038/s41598-024-65967-5
Chen, G., Yang, A., Wang, J., Ke, L., Chen, S., Li, W., 2024. Effects of the synergistic treatments of arbuscular mycorrhizal fungi and trehalose on adaptability to salt stress in tomato seedlings. Microbiology Spectrum, 12, 03404-23. https://doi.org/10.1128/spectrum.03404-23
Diagne, N., Ngom, M., Djighaly, P.I., Fall, D., Hocher, V., Svistoonoff, S., 2020. Roles of arbuscular mycorrhizal fungi on plant growth and performance: Importance in biotic and abiotic stressed regulation. Diversity, 12(10), 370. https://doi.org/10.3390/d12100370
Dris, H., Marashi, S. K., 2019. Study the effect of different methods of applying salicylic acid on quantitative, qualitative and biochemical parameters of wheat (Triticum aestivum L.) in drained and not drained lands. Environmental Stresses in Crop Sciences. 12, 561-571. [In Persian]. https://doi.org/10.22077/escs.2018.1371.1291
Ebrahimi, F., Salehi, A., Movahedi, D.M., Mirshekari, A., 2023. Morpho-physiological responses of two cultivars of german chamomile (Matricaria‎ chamomilla)‎‏‏ to mycorrhiza application under water deficiet stress. Iranian Journal of Horticultural Science. 53(3), 737-749 [In Persian with English Summary].  https://doi.org/10.22059/ijhs.2022.319917.1901
Farhangjou, S. E., Khavarinezhad, R., Saadatmand, S., Najafi, F., Babakhani, B., 2023. Effect of salicylic acid on some morphological and biochemical traits of rice (Oryza sativa L.) under salt stress. Journal of Plant Production. 30(2), 163-182. [In Persian with English Summary]. https://doi.org/10.22069/JOPP.2023.20675.2970
Fayez, K.A., Abdo, F.A.M., Sabra, H.M., 2024. Effects of salicylic acid, melatonin, and mycorrhizal fungi on the growth and physiological responses of wheat under varying water irrigation stress levels. Sohag Journal of Sciences. 9(3), 334-341. https://doi.org/10.21608/sjsci.2024.264172.1176
Ghojavand, M., Kasraei, P., Moghadam, H.R.T., Nasri, M., Larijani, H.R., 2023. Effects of salicylic acid and microorganisms on morphological and physiological characteristics (Satureja hortensis L.) under drought stress. European Journal of Biology. 82(1), 12-22. https://doi.org/10.26650/EurJBiol.2023.1196479
Ghorbanpour, M., Ahmadian, A., Yousefijavan, I., 2020. Interaction effects of salt stress and salicylic acid levels on physiological trials of saffron (Crocus sativus L.). Journal of Saffron Research. 8, 359-373. [In Persian with English Summary]. https://doi.org/10.22077/jsr.2020.2148.1084
Habibi, G., Hosseini Nejad, O., 2020. Salicylic acid and hydrogen peroxide priming as a means to induce salt stress tolerance of wheat. Journal of Plant Research (Iranian Journal of Biology). 33, 827-839. [In Persian with English Summary]. https://dorl.net/dor/20.1001.1.23832592.1399.33.4.11.7
Hanif, S., Mahmood, A., Javed, T., Bibi, S., Zia, M.A., Asghar, S., Ali, B., 2024. Exogenous application of salicylic acid ameliorates salinity stress in barley (Hordeum vulgare L.). BMC Plant Biology. 24, 1-16. https://doi.org/10.1186/s12870-024-04968-y
Huang, P., Huang, S., Ma, Y., Danish, S., Hareem, M., Syed, A., Wong, L. S., 2024. Alleviation of salinity stress by EDTA chelated-biochar and arbuscular mycorrhizal fungi on maize via modulation of antioxidants activity and biochemical attributes. BMC Plant Biology. 24, 63. https://doi.org/10.1186/s12870-024-04753-x
Ikan, C., Ben-Laouane, R., Ouhaddou, R., Anli, M., Boutasknit, A., Lahbouki, S., Meddich, A., 2023. Interactions between arbuscular mycorrhizal fungus and indigenous compost improve salt stress tolerance in wheat (Triticum durum). South African Journal of Botany. 158, 417-428. https://doi.org/10.1016/j.sajb.2023.05.038
Jam, E., Khomari, S., Ebadi, A., Goli Kalanpa, E., Ghavidel, A., 2024. Reducing the effects of soil heavy metal pollution in Vicia villosa L. by using biochar, trichoderma and phosphorus fertilizer management. Environmental Stresses in Crop Sciences. 17, 523-547. [In Persian with English Summary]. https://doi.org/10.22077/escs.2024.6100.2195
Khosravi, E., Salimi, A., Chavoushi, M., Zeidi, H., 2022. Role of chitosan in reducing the effects of salinity stress through enzymatic and non-enzymatic antioxidants in Portulaca oleracea L. Journal of Plant Research (Iranian Journal of Biology). 35, 786-798. [In Persian with English Summary]. https://dorl.net/dor/20.1001.1.23832592.1401.35.4.6.6
Koochekzadeh, A., Siahposh, A., Moradi-Telavat, M. R., Shafiee, M., 2023. Effect of mycorrhizal inoculation and salicylic acid on growth characteristics, yield and quality of marigold under salinity stress. Journal of Crops Improvement. 25(4), 1141-1156. [In Persian with English Summary]. https://doi.org/10.22059/jci.2023.344308.2719
Kunpratum, N., Phalawat, C., Thoradit, T., Kamoltheptawin, K., Thongyoo, K., Khiaokhoen, P., Pooam, M., 2024. Effect of salicylic acid on germination and seedling growth of KhaoRai Leum Pua Petchabun (Oryza sativa L.) under combined drought stress. Plant Physiology Reports. 29, 51-64. https://doi.org/10.3390/genes12081119
Liang, Q., Tan, D., Chen, H., Guo, X., Afzal, M., Wang, X., Peng, G., 2024. Endophyte-mediated enhancement of salt resistance in Arachis hypogaea L. by regulation of osmotic stress and plant defense-related genes. Frontiers in Microbiology. 15, 1383545. https://doi.org/10.3389/fmicb.2024.1383545
Mahdavian, K. (2023). Application of salicylic acid on chlorophyll, carotenoids, and proline in radish under salinity stress. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences. 93(4), 809-818. https://doi.org/10.1007/s40011-023-01484-1
Mehrabi, S.S., Sabokdast, M., Bihamta, M.R., Dedičová, B., 2024. The coupling effects of PGPR inoculation and foliar spraying of strigolactone in mitigating the negative effect of salt stress in wheat plants: insights from phytochemical, growth, and yield attributes. Agriculture, 14(5), 732. https://doi.org/10.3390/agriculture14050732
Mohammadi Cheraghabadi, M., Roshanfekr, H., Hasibi, P., Meskarbashi, M., 2016. Effect of foliar application of salicylic acid on some physiological traits of sugar beet in salt stress conditions. Iranian Journal of Filed Crop Science. 46, 591- 604. [In Persian with English Summary]. https://doi.org/10.22059/ijfcs.2015.56809
Mohammadi, H., Pirmoradi, M.R., Moghaddam, M., Shamshiri, M.H., Mirzaabolghasemi, M. A., 2022. Effects of salicylic acid on physiological, biochemical, nutrient uptake, and essential oil percentage of Ocimum basilicum cv. Keshkeni luvelou under salinity stress. Iranian Journal of Medicinal and Aromatic Plants Research. 38, 464-475. [In Persian with English Summary]. https://doi.org/10.22092/ijmapr.2022.358101.3147
Mohseni Mohammadjanlou, A. R., Seyed Sharifi, R., Khomari, S., 2022. Effect of biofertilizers and putrescine on grain yield and some physiological indices of wheat (Triticum aestivum L.) at various irrigation levels. Journal of Plant Production Research. 24, 67-83. [In Persian with English Summary].   https://doi.org/10.22059/jci.2021.308522.2439
Morshedi, E., Gharineh, M. H., Kochekzadeh, A., Bakhshandeh, A.M., 2023. Effect of Bacillus and Pseudomonas bacteria on quantitative and qualitative yield and malting efficiency of different barley cultivars in rainfed conditions. Journal of Crops Improvement. 25(2), 313-330. [In Persian with English Summary].   https://doi.org/10.22059/jci.2022.333633.2638
Moustakas, M., Sperdouli, I., Moustaka, J., Şaş, B., İşgören, S., Morales, F., 2023. Mechanistic insights on salicylic acid mediated enhancement of photosystem II function in oregano seedlings subjected to moderate drought stress. Plants. 12(3), 518. https://doi.org/10.3390/plants12030518
Narimani, H., Seyed Sharifi, R., 2023. Effect of Mycorrhiza and methanol on grain filling components, dry matter remobilization and yield of barley under soil salinity conditions. Environmental Stresses in Crop Sciences. 16(2), 383-401. [In Persian with English Summary]. https://doi.org/10.22077/escs.2022.4638.2051
Ogunsiji, E., Umebese, C., Stabentheiner, E., Iwuala, E., Odjegba, V., Oluwajobi, A., 2023. Salicylic acid enhances growth, photosynthetic performance and antioxidant defense activity under salt stress in two mungbean [Vigna radiata (L.) R. Wilczek] variety. Plant Signaling & Behavior. 18(1), 2217605. https://doi.org/10.1080/15592324.2023.2217605
Pirasteh-Anosheh, H., Ranjbar, G., Hasanuzzaman, M., Khanna, K., Bhardwaj, R., Ahmad, P., 2022. Salicylic acid-mediated regulation of morpho-physiological and yield attributes of wheat and barley plants in deferring salinity stress. Journal of Plant Growth Regulation. 41, 1291-1303. https://doi.org/10.1111/tpj.12651
Pooja, P., Tallapragada, S., Yadav, M., Chugh, R. K., Saini, S., Devi, S., 2024. Mycorrhiza in improving morpho-physiological and biochemical parameters of chickpea genotypes (Cicer arietinum L.) under salinity stress. Journal of Crop Health. 76(2), 533-547. https://doi.org/10.1007/s10343-024-00969-x
Ritchie, S.W., Nguyen, H.T., Holaday, A.S., 1990. Leaf Water Content and Gas-Exchange Parameters of Two Wheat Genotypes Differing in Drought Resistance. Crop Science. 30, 105-111. https://doi.org/10.2135/cropsci1990.0011183X003000010025x
Ruelland, E., Pokotylo, I., Djafi, N., Cantrel, C., Repellin, A., . Zachowski, A., 2014. Salicylic acid modulates levels of phosphoinositide dependent-phospholipase C substrates and products to remodel the Arabidopsis suspension cell transcriptome. Frontiers in plant Science. 5, 608. https://doi.org/10.3389/fpls.2014.00608
Saeed, S., Ullah, A., Ullah, S., Elshikh, M.S., Noor, J., Eldin, S.M., Zeng, F., Amin, F., Ali, M.A., Ali, I., 2023. Salicylic acid and α-tocopherol ameliorate salinity impact on wheat. ACS Omega. 8, 26122–26135. https://doi.org/10.1021/acsomega.3c02166
Sajed Gollojeh, K., Khomari, S., Shekhzadeh, P., Sabaghnia, N., Mohebodini, M., 2020. The effect of foliar spray of nano silicone and salicylic acid on physiological traits and seed yield of spring rapeseed at water limitation conditions. Journal of Crop Production Research. 12, 137-156. [In Persian with English Summary]. https://doi.org/10.22069/ejcp.2020.16396.2221
Seyedalikhani, S.N., Pazoki, A.R., 2023. The effect of salicylic and jasmonic acid on antioxidant enzymes activity, soluble carbohydrate and proline in Artichoke (Cynara Scolymus L.) under salt stress conditions. Journal of Crop Production Research. 14, 481-510. [In Persian with English Summary].
Shahbaz, M., M. Ashraf., 2013. Improving salinity tolerance in cereals. Critical Review Plant Science. 32, 237-249. https://doi.org/10.1080/07352689.2013.758544
Sharaya, R., Gill, R., Kalwan, G., Naeem, M., Tuteja, N., Gill, S.S., 2023. Plant-microbe interaction mediated salinity stress tolerance for sustainable crop production. South African Journal of Botany. 161, 454-471. https://doi.org/10.1016/j.sajb.2023.08.043
Silva, T.I., da Silva Ribeiro, J.E., Dias, M.G., Nóbrega, J.S., Gonçalves, A.C.M., de Melo Filho, J.S., Zanuncio, J.C., 2023. Ecophysiology and growth of basil (Ocimum basilicum) under saline stress and salicylic acid. Acta Biológica Colombiana. 28, 128-134. https://doi.org/10.15446/abc.v28n1.97151
Sperdouli, I., Panteris, E., Moustaka, J., Aydın, T., Bayçu, G., Moustakas, M., 2024. Mechanistic insights on salicylic acid-induced enhancement of photosystem II function in basil plants under non-stress or mild drought stress. International Journal of Molecular Sciences. 25, 5728. https://doi.org/10.3390/ijms25115728
Stewart, R.R., Bewley, J.D., 1980. Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiology. 65(2), 245-248. https://doi.org/10.1104/pp.65.2.245
Sudhakar, C., Lakshmi, A., Giridara Kumar, S., 2001. Changes in the antioxidant enzyme efficacy in two high yielding genotypes of mulberry (Morus alba L.) under NaCl salinity. Plant Science. 167, 613-619. https://doi.org/10.1016/S0168-452(01)00450-2
Torabi, S., Alahdadi, I., Akbari, G. A., Ghorbani Javid, M., Fotovat, R., 2023. Effects of foliar application of salicylic acid and nanosilicon on the yield and physiological traits of maize (Zea mays) in heavy metal contaminated fields. Iranian Journal of Field Crop Science. 54, 151-168. [In Persian with English Summary] . https://doi.org/10.22059/ijfcs.2022.346622.654931
Verma, R.P.S., Lal, C., Malik, R., Kharub, A.S., Kumar, L., Kumar, D., 2022. Barley improvement: Current status and future prospects in changing scenario. In: Kashyap, P.L., et al. (eds.), New Horizons in Wheat and Barley Research. Springer, Singapore. https://doi.org/10.1007/978-981-16-4449-8_6
Wang, J., Zhai, L., Ma, J., Zhang, J., Wang, G. G., Liu, X., Zhang, S., Song, J., Wu, Y., 2020. Comparative physiological mechanisms of arbuscular mycorrhizal fungi in mitigating salt-induced adverse effects on leaves and roots of Zelkova serrata. Mycorrhiza. 30, 341–355. https://doi.org/10.1007/s00572-020-00954-y
Wei, L.I., Yan-Lin, Z.H.A.I., Xue-Yi, H.U., Shao-Xia, G.U.O., 2023. 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), 12649-12649. https://doi.org/10.15835/nbha51112649
Yadav, T., Yadav, R.K., Yadav, G., Kumar, A., Makarana, G., 2024. Salicylic acid and thiourea ameliorated adverse effects of salinity and drought-induced changes in physiological traits and yield of wheat. Cereal Research Communications. 52(2), 545-558. https://doi.org/10.3389/fpls.2022.953670
Yarşı, G., 2023. Effects of mycorrhiza, seaweed and bionutrient applied to reduce the salt stress on nutrient content, plant growth, malondialdehyde (MDA) and proline in pepper. Journal of Elementology. 28(3), 533-545. http://dx.doi.org/10.5601/jelem.2023.28.2.2396
Youssef, S.M., López-Orenes, A., Ferrer, M.A., Calderón, A.A., 2023. Foliar application of salicylic acid enhances the endogenous antioxidant and hormone systems and attenuates the adverse effects of salt stress on growth and yield of french bean plants. Horticulturae. 9(1), 75. https://doi.org/10.3390/horticulturae9010075
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(6), 805. https://doi.org/10.3390/plants13060805
Environmental Stresses in Crop Sciences

Articles in Press, Accepted Manuscript
Available Online from 13 December 2025

Files

History

  • Receive Date: 10 October 2024
  • Revise Date: 09 November 2024
  • Accept Date: 18 November 2024

Share

How to cite

Statistics