How nano-iron chelate and arbuscular mycorrhizal fungi mitigate water stress in Lallemantia species: A growth and physio-biochemical properties
Corresponding Author
Arezoo Paravar
Department of Crop Production and Plant Breeding, College of Agriculture, Shahed University, Tehran, Iran
Correspondence
Arezoo Paravar, Saeideh Maleki Farahani, Department of Crop Production and Plant Breeding,College of Agriculture, Shahed University, P. O. Box 18155/159, Tehran, Iran.
Email: [email protected]; [email protected]
Search for more papers by this authorCorresponding Author
Saeideh Maleki Farahani
Department of Crop Production and Plant Breeding, College of Agriculture, Shahed University, Tehran, Iran
Correspondence
Arezoo Paravar, Saeideh Maleki Farahani, Department of Crop Production and Plant Breeding,College of Agriculture, Shahed University, P. O. Box 18155/159, Tehran, Iran.
Email: [email protected]; [email protected]
Search for more papers by this authorAlireza Rezazadeh
Department of Plant Protection, College of Agriculture, Shahed University, Tehran, Iran
Search for more papers by this authorReza Keshavarz Afshar
VP- Soil, Feed and Water Research, Dairy Management Inc, Kutztown, Pennsylvania, USA
Search for more papers by this authorCorresponding Author
Arezoo Paravar
Department of Crop Production and Plant Breeding, College of Agriculture, Shahed University, Tehran, Iran
Correspondence
Arezoo Paravar, Saeideh Maleki Farahani, Department of Crop Production and Plant Breeding,College of Agriculture, Shahed University, P. O. Box 18155/159, Tehran, Iran.
Email: [email protected]; [email protected]
Search for more papers by this authorCorresponding Author
Saeideh Maleki Farahani
Department of Crop Production and Plant Breeding, College of Agriculture, Shahed University, Tehran, Iran
Correspondence
Arezoo Paravar, Saeideh Maleki Farahani, Department of Crop Production and Plant Breeding,College of Agriculture, Shahed University, P. O. Box 18155/159, Tehran, Iran.
Email: [email protected]; [email protected]
Search for more papers by this authorAlireza Rezazadeh
Department of Plant Protection, College of Agriculture, Shahed University, Tehran, Iran
Search for more papers by this authorReza Keshavarz Afshar
VP- Soil, Feed and Water Research, Dairy Management Inc, Kutztown, Pennsylvania, USA
Search for more papers by this authorThis article has been edited by Xian-Zheng Yuan.
Abstract
Background
Water deficit can seriously affect the growth, yield, and biochemical properties of plants; however, the application of nano-iron chelate and arbuscular mycorrhizal fertilizers in water deficit has been considered one of the most promising methods to improve plant growth and enhance drought tolerance.
Aims
This study aimed to investigate the effects of nano-iron chelated (nFe) fertilizer and arbuscular mycorrhizal fungi (AMFs) on the growth, yield, root colonization, mycorrhizal dependency, water use efficiency (WUE), physio-biochemical properties, and seed biochemical properties of Lallemantia iberica and Lallemantia royleana species under drought stress.
Methods
A split-factorial experiment was conducted using a randomized complete block design with three replications. The main plot consisted of three drought stress levels (according to the depletion of soil available water) of 30% (I1; without stress), 60% (I2; mild stress), and 90% (I3; severe stress). The subplots were the factorial combination of fertilizers (F) (without fertilizer, nano-iron chelate [nFe], and AMFs) and plant species (S) of Lallemantia (L. iberica and L. royleana).
Results
A decrease in the irrigation regime caused a reduction in growth, seed yield, WUE, chlorophyll content, nutrient uptake, seed oil, and mucilage content, as well as an increase in lipid peroxidation and hydrogen peroxide. Compared with nFe, AMF significantly increased root colonization by mycorrhizal fungi in both species across irrigation regimes. Furthermore, AMF inoculation enhanced nutrient uptake, mucilage, oil, and fatty acids by increasing the WUE. Higher mycorrhizal dependency in inoculated plants played an important role in increasing proline and antioxidant activities in the leaves of the host plant. The water stress and fertilization treatments resulted in the highest root colonization, mycorrhizal dependency, proline content, and antioxidant enzyme activities in L. royleana, as well as the highest WUE, accumulation of fatty acids, and nutrient uptake was observed in L. iberica. Interestingly, the mycorrhization potential of Lallemantia sp. is clearly defined.
Conclusions
The results highlighted that AMFs can promote Lallemantia to increase seed mucilage and oil under water stress. Overall, we found that both Lallemantia species responded well to AMF inoculation under water deficit conditions, where nFe was found to be less effective.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Supporting Information
Filename | Description |
---|---|
jpln202300115-sup-0001-SuppMat.pdf134.4 KB | Supporting Information |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Abdi, N., van Biljon, A., Steyn, C., & Labuschagne, M. T. (2021). Bread wheat (Triticum aestivum) responses to arbuscular mycorrhizae inoculation under drought stress conditions. Plants, 10(9), 1756. https://doi.org/10.3390/plants10091756
- Abdolahi, M., & Farahani, S. M. (2019). Seed quality, water use efficiency and eco physiological characteristics of Lallemantia (Lallemantia sp.) species as effected by soil moisture content. Acta Agriculturae Slovenica, 113(2), 307–320.
- Ahanger, M. A., Morad-Talab, N., Abd-Allah, E. F., Ahmad, P., & Hajiboland, R. (2016). Plant growth under drought stress: Significance of mineral nutrients. Water Stress and Crop Plants: A Sustainable Approach, 2, 649–668.
10.1002/9781119054450.ch37 Google Scholar
- Ahmad, P., John, R., Sarwat, M., & Umar, S. (2012). Responses of proline, lipid peroxidation and antioxidative enzymes in two varieties of Pisum sativum L. under salt stress. International Journal of Plant Production, 2(4), 353–366.
- Allen, M. M., & Allen, D. J. (2020). Biostimulant potential of acetic acid under drought stress is confounded by pH-dependent root growth inhibition. Frontiers in Plant Science, 11, 647. https://doi.org/10.3389/fpls.2020.00647
- Amani Machiani, M., Javanmard, A., Morshedloo, R. M., Janmohammadi, M., & Maggi, F. (2021). Funneliformis mosseae application improves the oil quantity and quality and eco-physiological characteristics of soybean (Glycine max L.) under water stress conditions. Journal of Soil Science and Plant Nutrition, 21, 3076–3090.
- Arnon, D. I. (1949). Copper enzymes in isolated chloroplasts. Polyphenoloxidase in beta vulgaris. Plant Physiology, 24(1), 1–15.
- Askari, A., Ardakani, M. R., Paknejad, F., & Hosseini, Y. (2019). Effects of mycorrhizal symbiosis and seed priming on yield and water use efficiency of sesame under drought stress condition. Scientia Horticulturae, 257, 108749. https://doi.org/10.1016/j.scienta.2019.108749
- Askary, M., Amirjani, M. R., & Saberi, T. (2017). Comparison of the effects of nano-iron fertilizer with iron-chelate on growth parameters and some biochemical properties of Catharanthus roseus. Journal of Plant Nutrition, 40(7), 974–982.
- Aslam, M. M., Karanja, J. K., Dodd, I. C., Waseem, M., & Weifeng, X. (2022). Rhizosheath: An adaptive root trait to improve plant tolerance to phosphorus and water deficits? Plant, Cell & Environment, 45(10), 2861–2874.
- Attarzadeh, M., Balouchi, H., Rajaie, M., Dehnavi, M. M., & Salehi, A. (2020). Improving growth and phenolic compounds of Echinacea purpurea root by integrating biological and chemical resources of phosphorus under water deficit stress. Industrial Crops and Products, 154, 112763. https://doi.org/10.1016/j.indcrop.2020.112763
- 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. https://doi.org/10.1002/ecy.297
- Berry, W. L., & Johnson, C. M. (1966). Determination of calcium and magnesium in plant material and culture solutions, using atomic-absorption spectroscopy. Applied Spectroscopy, 20(4), 209–211.
- Borzoo, S., Mohsenzadeh, S., Moradshahi, A., Kahrizi, D., Zamani, H., & Zarei, M. (2021). Characterization of physiological responses and fatty acid compositions of Camelina sativa genotypes under water deficit stress and symbiosis with Micrococcus yunnanensis. Symbiosis, 83, 79–90.
- Chance, B., & Maehly, A. (1955). Assay of catalases and peroxidases. Methods in Enzymology, 2, 764–775.
- Cheng, H. Q., Giri, B., Wu, Q. S., Zou, Y. N., & Kuča, K. (2022). Arbuscular mycorrhizal fungi mitigate drought stress in citrus by modulating root microenvironment. Archives of Agronomy and Soil Science, 68(9), 1217–1228.
- Chi, Y. X., Gao, F., Muhammad, I., Huang, J. H., & Zhou, X. B. (2023). Effect of water conditions and nitrogen application on maize growth, carbon accumulation and metabolism of maize plant in subtropical regions. Archives of Agronomy and Soil Science, 69, 693–707. https://doi.org/10.1080/03650340.2022.2026931
- Chun, S. C., Paramasivan, M., & Chandrasekaran, M. (2018). Proline accumulation influenced by osmotic stress in arbuscular mycorrhizal symbiotic plants. Frontiers in Microbiology, 9, 2525. https://doi.org/10.3389/fmicb.2018.02525
- Dai, L., Li, J., Harmens, H., Zheng, X., & Zhang, C. (2020). Melatonin enhances drought resistance by regulating leaf stomatal behaviour, root growth and catalase activity in two contrasting rapeseed (Brassica napus L.) genotypes. Plant Physiology and Biochemistry, 149, 86–95.
- Dien, D. C., Mochizuki, T., & Yamakawa, T. (2019). Effect of various drought stresses and subsequent recovery on proline, total soluble sugar and starch metabolisms in rice (Oryza sativa L.) varieties. Plant Production Science, 22(4), 530–545.
- Dowarah, B., Gill, S. S., & Agarwala, N. (2022). Arbuscular mycorrhizal fungi in conferring tolerance to biotic stresses in plants. Journal of Plant Growth Regulation, 41, 1429–1444. https://doi.org/10.1007/s00344-021-10392-5
- Driouich, A., Smith, C., Ropitaux, M., Chambard, M., Boulogne, I., Bernard, S., Follet-Gueye, M. L., Vicré, M., & Moore, J. (2019). Root extracellular traps versus neutrophil extracellular traps in host defence, a case of functional convergence? Biological Reviews, 94(5), 1685–1700.
- Ebrahimian, E., Seyyedi, S. M., Bybordi, A., & Damalas, C. A. (2019). Seed yield and oil quality of sunflower, safflower, and sesame under different levels of irrigation water availability. Agricultural Water Management, 218, 149–157.
- El-Metwally, I., Geries, L., & Saudy, H. (2022). Interactive effect of soil mulching and irrigation regime on yield, irrigation water use efficiency and weeds of trickle–irrigated onion. Archives of Agronomy and Soil Science, 68(8), 1103–1116.
- Ezzati Lotfabadi, Z., Weisany, W., Abdul-razzak Tahir, N., & Mohammadi Torkashvand, A. (2022). Arbuscular mycorrhizal fungi species improve the fatty acids profile and nutrients status of soybean cultivars grown under drought stress. Journal of Applied Microbiology, 132(3), 2177–2188.
- Filipek-Mazur, B., Tabak, M., Koncewicz-Baran, M., & Bobowiec, A. (2019). Mineral fertilizers with iron influence spring rape, maize and soil properties. Archives of Agronomy and Soil Science, 65(11), 1575–1585.
- Gao, S., Wang, Y., Yu, S., Huang, Y., Liu, H., Chen, W., & He, X. (2020). Effects of drought stress on growth, physiology and secondary metabolites of Two Adonis species in Northeast China. Scientia Horticulturae, 259, 108795. https://doi.org/10.1016/j.scienta.2019.108795
- Ghanbarzadeh, Z., Mohsenzadeh, S., Rowshan, V., & Moradshahi, A. (2019). Evaluation of the growth, essential oil composition and antioxidant activity of Dracocephalum moldavica under water deficit stress and symbiosis with Claroideoglomus etunicatum and Micrococcus yunnanensis. Scientia Horticulturae, 256, 108652.https://doi.org/10.1016/j.scienta.2019.108652
- Ghanbarzadeh, Z., Mohsenzadeh, S., Rowshan, V., & Zarei, M. (2020). Mitigation of water deficit stress in Dracocephalum moldavica by symbiotic association with soil microorganisms. Scientia Horticulturae, 272, 109549. https://doi.org/10.1016/j.scienta.2020.109549
- Ghassemi Golezani, K., Ardalan, N., Raei, Y., & Dalil, B. (2022). Improving some physiological and yield parameters of safflower by foliar sprays of Fe and Zn under drought stress. Journal of Plant Physiology and Breeding, 12(1), 15–27.
- Gholinezhad, E. (2017). Effect of drought stress and Fe nano-fertilizer on seed yield, morphological traits, essential oil percentage and yield of dill (Anethum graveolens L.). Journal of Essential Oil Bearing Plants, 20(4), 1006–1017.
- Gholinezhad, E., Darvishzadeh, R., Moghaddam, S. S., & Popović-Djordjević, J. (2020). Effect of mycorrhizal inoculation in reducing water stress in sesame (Sesamum indicum L.): The assessment of agrobiochemical traits and enzymatic antioxidant activity. Agricultural Water Management, 238, 106234. https://doi.org/10.1016/j.agwat.2020.106234
- Haghighi, T. M., & Saharkhiz, M. J. (2022). Mycorrhizal colonization and silicon nutrition mitigates drought stress in Licorice (Glycyrrhiza glabra L.) with morphophysiological and biochemical perspectives. Industrial Crops and Products, 178, 114650. https://doi.org/10.1016/j.indcrop.2022.114650
- Heath, R. L., & Packer, L. (1968). Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of biochemistry and biophysics, 125(1), 189–198.
- Heydari, S., & Pirzad, A. (2021). Efficiency of Funneliformis mosseae and Thiobacillus sp. on the secondary metabolites (essential oil, seed oil and mucilage) of Lallemantia iberica under salinity stress. The Journal of Horticultural Science and Biotechnology, 96(2), 249–259.
- Hosseinzadeh, M. H., Ghalavand, A., Mashhadi-Akbar-Boojar, M., Modarres-Sanavy, S. A. M., & Mokhtassi-Bidgoli, A. (2020). Increased medicinal contents of purslane by nitrogen and arbuscular mycorrhiza under drought stress. Communications in Soil Science and Plant Analysis, 51(1), 118–135.
- Jongen, M., Albadran, B., Beyschlag, W., & Unger, S. (2022). Can arbuscular mycorrhizal fungi mitigate drought stress in annual pasture legumes? Plant and Soil, 472(1–2), 295–310.
- Kamali, S., & Mehraban, A. (2020). Effects of Nitroxin and arbuscular mycorrhizal fungi on the agro-physiological traits and grain yield of sorghum (Sorghum bicolor L.) under drought stress conditions. PLoS One, 15(12), e0243824. https://doi.org/10.1371/journal.pone.0243824
- Kambona, C. M., Koua, P. A., Léon, J., & Ballvora, A. (2023). Stress memory and its regulation in plants experiencing recurrent drought conditions. Theoretical and Applied Genetics, 136(2), 26. https://doi.org/10.1007/s00122–023–04313–1
- Khademian, R., Asghari, B., Sedaghati, B., & Yaghoubian, Y. (2019). Plant beneficial rhizospheric microorganisms (PBRMs) mitigate deleterious effects of salinity in sesame (Sesamum indicum L.): Physio-biochemical properties, fatty acids composition and secondary metabolites content. Industrial Crops and Products, 136, 129–139.
- Khan, Y., Shah, S., & Tian, H. (2022). The roles of arbuscular mycorrhizal fungi in influencing plant nutrients, photosynthesis, and metabolites of cereal crops—A review. Agronomy, 12(9), 2191. https://doi.org/10.3390/agronomy12092191
- Kormanik, P., & McGraw, A. (1982). Quantification of vesicular-arbuscular mycorrhizae in plant roots. In N. C. Schenck (Ed.), Methods and principles of mycorrhizal research (pp. 37–46). American Phytopathological Society.
- Lahbouki, S., Ben-Laouane, R., Anli, M., Boutasknit, A., Ait-Rahou, Y., Ait-El-Mokhtar, M., El Gabardi, S., Douira, A., Wahbi, S., & Meddich, A. (2022). Arbuscular mycorrhizal fungi and/or organic amendment enhance the tolerance of prickly pear (Opuntia ficus-indica) under drought stress. Journal of Arid Environments, 199, 104703. https://doi.org/10.1016/j.jaridenv.2021.104703
- Langeroodi, A. R. S., Osipitan, O. A., Radicetti, E., & Mancinelli, R. (2020). To what extent arbuscular mycorrhiza can protect chicory (Cichorium intybus L.) against drought stress. Scientia Horticulturae, 263, 109109. https://doi.org/10.1016/j.scienta.2019.109109
- Li, C., Tan, D. X., Liang, D., Chang, C., Jia, D., & Ma, F. (2015). Melatonin mediates the regulation of ABA metabolism, free-radical scavenging, and stomatal behaviour in two Malus species under drought stress. Journal of Experimental Botany, 66(3), 669–680.
- Loreto, F., & Velikova, V. (2001). Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiology, 127(4), 1781–1787.
- Mahmoud, A. W. M., & Taha, S. S. (2018). Main sulphur content in essential oil of Eruca sativa as affected by nano iron and nano zinc mixed with organic manure. Agriculture (Pol'nohospodárstvo), 64(2), 65–79.
10.2478/agri-2018-0007 Google Scholar
- Mitra, D., Nayeri, F. D., Sansinenea, E., Ortiz, A., Bhatta, B. B., Adeyemi, N. O., Janeeshma, E., Tawfeeq Al-Ani, L. K., Sharma, S. B., Boutaj, H., Priyadarshini, A., Chakroborty, D., Senapati, A., Guerra Siewrra, B. E., Chidambaranathan, P., & Das Mohapatra, P. K. (2023). Unraveling arbuscular mycorrhizal fungi interaction in rice for plant growth development and enhancing phosphorus use efficiency through recent development of regulatory genes. Journal of Plant Nutrition, 46, 3184–3220. https://doi.org/10.1080/01904167.2023.2191638
- Mittal, S., Kumari, N., & Sharma, V. (2012). Differential response of salt stress on Brassica juncea: Photosynthetic performance, pigment, proline, D1 and antioxidant enzymes. Plant Physiology and Biochemistry, 54, 17–26.
- Mohammad Ghasemi, V., Siavash Moghaddam, S., Rahimi, A., Pourakbar, L., & Popović-Djordjević, J. (2020). Winter cultivation and nano fertilizers improve yield components and antioxidant traits of dragon's head (Lallemantia iberica (MB) Fischer & Meyer). Plants, 9(2), 252. https://doi.org/10.3390/plants9020252
10.3390/plants9020252 Google Scholar
- Mohasseli, V., Farbood, F., & Moradi, A. (2020). Antioxidant defense and metabolic responses of lemon balm (Melissa officinalis L.) to Fe-nano-particles under reduced irrigation regimes. Industrial Crops and Products, 149, 112338. https://doi.org/10.1016/j.indcrop.2020.112338
- Mokhtassi-Bidgoli, A., AghaAlikhani, M., Nassiri-Mahallati, M., Zand, E., Gonzalez-Andujar, J. L., & Azari, A. (2013). Agronomic performance, seed quality and nitrogen uptake of Descurainia sophia in response to different nitrogen rates and water regimes. Industrial Crops and Products, 44, 583–592.
- Nobahar, A., Zakerin, H. R., Mostafavi Rad, M., Sayfzadeh, S., & Valadabady, A. R. (2019). Response of Yield and Some Physiological Traits of Groundnut (Arachis hypogaea L.) to Topping Height and Application Methods of Zn and Ca Nano–Chelates. Communications in Soil Science and Plant Analysis, 50(6), 749–762.
- Oliveira, T. C., Cabral, J. S. R., Santana, L. R., Tavares, G. G., Santos, L. D. S., Paim, T. P., Müller, C., Silva, F. G., Costa, A. C., Souchie, E. L., & Mendes, G. C. (2022). The arbuscular mycorrhizal fungus Rhizophagus clarus improves physiological tolerance to drought stress in soybean plants. Scientific Reports, 12(1), 9044. https://doi.org/10.1038/s41598–022–13059–7
- Ostadi, A., Javanmard, A., Amani Machiani, M., Sadeghpour, A., Maggi, F., Nouraein, M., Morshedloo, M. R., Hano, C., & Lorenzo, J. M. (2022). Co-application of TiO2 nanoparticles and arbuscular mycorrhizal fungi improves essential oil quantity and quality of sage (Salvia officinalis L.) in drought stress conditions. Plants, 11(13), 1659. https://doi.org/10.3390/plants11131659
- Paravar, A., Farahani, S. M., & Rezazadeh, A. (2021). Lallemantia species response to drought stress and Arbuscular mycorrhizal fungi application. Industrial Crops and Products, 172, 114002. https://doi.org/10.1016/j.indcrop.2021.114002
- Paravar, A., Farahani, S. M., & Rezazadeh, A. (2022a). Fatty acid composition and eco-agronomical traits of Lallemantia species modulated upon exposed to arbuscular mycorrhizal fungi and nano-iron chelate fertilizers under water deficit conditions. Journal of Soil Science and Plant Nutrition, 22(3), 3463–3478.
- Paravar, A., Farahani, S. M., & Rezazadeh, A. (2022b). Lallemantia iberica and Lallemantia royleana: The Effect of mycorrhizal fungal inoculation on growth and mycorrhizal dependency under sterile and non-sterile soils. Communications in Soil Science and Plant Analysis, 53(7), 880–891.
- Paravar, A., Farahani, S. M., & Rezazadeh, A. (2023). Morphological, physiological and biochemical response of Lallemantia species to elevated temperature and light duration during seed development. Heliyon, 9(4), e15149. https://doi.org/10.1016/j.heliyon.2023.e15149
- Park, S. I., Kim, J. J., Shin, S. Y., Kim, Y. S., & Yoon, H. S. (2020). ASR enhances environmental stress tolerance and improves grain yield by modulating stomatal closure in rice. Frontiers in Plant Science, 10, 1752. https://doi.org/10.3389/fpls.2019.01752
- Pawar, P. B., Khadilkar, J. P., Kulkarni, M. V., & Melo, J. S. (2018). An approach to enhance nutritive quality of groundnut (Arachis hypogaea L.) seed oil through endo mycorrhizal fertigation. Biocatalysis and Agricultural Biotechnology, 14, 18–22.
- Rahimzadeh, S., & Pirzad, A. (2019). Pseudomonas and mycorrhizal fungi co-inoculation alter seed quality of flax under various water supply conditions. Industrial Crops and Products, 129, 518–524.
- Rahman, S., Iqbal, M., & Husen, A. (2023). Medicinal plants and abiotic stress: An overview. In Medicinal plants: Their response to abiotic stress (pp. 1–34). Springer. https://doi.org/10.1007/978–981–19–5611–9_1
10.1007/978-981-19-5611-9_1 Google Scholar
- Reis, M. N. O., Vitorino, L. C., Lourenço, L. L., & Bessa, L. A. (2022). Microbial inoculation improves growth, nutritional and physiological aspects of Glycine max (L.) Merr. Microorganisms, 10(7), 1386. https://doi.org/10.3390/microorganisms10071386
10.3390/microorganisms1007138 Google Scholar
- Rezaei-Chiyaneh, E., Mahdavikia, H., Subramanian, S., Alipour, H., Siddique, K. H., & Smith, D. L. (2021). Co-inoculation of phosphate-solubilizing bacteria and mycorrhizal fungi: Effect on seed yield, physiological variables, and fixed oil and essential oil productivity of ajowan (Carum copticum L.) under water deficit. Journal of Soil Science and Plant Nutrition, 21, 3159–3179.
- Savage, G. P., McNeil, D. L., & Dutta, P. C. (1997). Lipid composition and oxidative stability of oils in hazelnuts (Corylus avellana L.) grown in New Zealand. Journal of the American Oil Chemists' Society, 74(6), 755–759.
- Schenck, N. C., & Perez, Y. (1990). Manual for the identification of VA mycorrhizal fungi. Synergistic Publications.
- Shahsavandi, F., Eshghi, S., Gharaghani, A., Ghasemi-Fasaei, R., & Jafarinia, M. (2020). Effects of bicarbonate induced iron chlorosis on photosynthesis apparatus in grapevine. Scientia Horticulturae, 270, 109427. https://doi.org/10.1016/j.scienta.2020.109427
- Sharma, P. K., & Koul, A. K. (1986). Mucilage in seeds of Plantago ovata and its wild allies. Journal of Ethnopharmacology, 17(3), 289–295.
- Shoaib, M., Banerjee, B. P., Hayden, M., & Kant, S. (2022). Roots’ drought adaptive traits in crop improvement. Plants, 11(17), 2256. https://doi.org/10.3390/plants11172256
- Simkin, A. J., Faralli, M., Ramamoorthy, S., & Lawson, T. (2020). Photosynthesis in non-foliar tissues: Implications for yield. The Plant Journal, 101(4), 1001–1015.
- Stanhill, G. (1986). Water use efficiency. Advances in Agronomy, 39, 53–85.
- Stuffins, C. B. (1967). The determination of phosphate and calcium in feeding stuffs. Analyst, 92(1091), 107–111.
- Taghizadeh, Y., Jalilian, J., & Siavash Moghaddam, S. (2019). Do fertilizers and irrigation disruption change some physiological traits of safflower? Journal of Plant Growth Regulation, 38, 1439–1448.
- Tang, H., Hassan, M. U., Feng, L., Nawaz, M., Shah, A. N., Qari, S. H., Liu, Y., & Miao, J. (2022). The critical role of arbuscular mycorrhizal fungi to improve drought tolerance and nitrogen use efficiency in crops. Frontiers in Plant Science, 13, 919166. https://doi.org/10.3389/fpls.2022.919166
- Tariq, A., Pan, K., Olatunji, O. A., Graciano, C., Li, N., Li, Z., Song, D., Sun, F., Justine, M. F., Huang, D., Gong, Z., Pandey, B., Idrees, M., & Dakhil, M. A. (2019). Role of nitrogen supplementation in alleviating drought-associated growth and metabolic impairments in Phoebe zhennan seedlings. Journal of Plant Nutrition and Soil Science, 182(4), 586–596.
- Tyagi, J., Shrivastava, N., Sharma, A. K., Varma, A., & Pudake, R. (2021). Effect of Rhizophagus intraradices on growth and physiological performance of Finger Millet (Eleusine coracana L.) under drought stress. Plant Science Today, 8(4), 912–923.
- Vallejos-Torres, G., Espinoza, E., Marín-Díaz, J., Solis, R., & Arévalo, L. A. (2021). The role of arbuscular mycorrhizal fungi against root-knot nematode infections in coffee plants. Journal of Soil Science and Plant Nutrition, 21(1), 364–373.
- Visavadiya, N. P., Soni, B., & Dalwadi, N. (2009). Free radical scavenging and antiatherogenic activities of Sesamum indicum seed extracts in chemical and biological model systems. Food and Chemical Toxicology, 47(10), 2507–2515.
- Vurukonda, S. S. K. P., Vardharajula, S., Shrivastava, M., & SkZ, A. (2016). Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiological Research, 184, 13–24.
- Wang, S., Xie, X., Che, X., Lai, W., Ren, Y., Fan, X., Hu, W., Tang, M., & Chen, H. (2023). Host-and virus-induced gene silencing of HOG1-MAPK cascade genes in Rhizophagus irregularis inhibit arbuscule development and reduce resistance of plants to drought stress. Plant Biotechnology Journal. https://doi.org/10.1111/pbi.14006
- Wu, Q. S., He, J. D., Srivastava, A. K., Zou, Y. N., & Kuča, K. (2019). Mycorrhizas enhance drought tolerance of citrus by altering root fatty acid compositions and their saturation levels. Tree Physiology, 39(7), 1149–1158.
- Xu, X., Qiu, Y., Zhang, K., Yang, F., Chen, M., Luo, X., Yan, X., Wang, P., Zhang, Y., Chen, H., Guo, H., Jiang, L., & Hu, S. (2022). Climate warming promotes deterministic assembly of arbuscular mycorrhizal fungal communities. Global Change Biology, 28(3), 1147–1161.
- Xu, X., Zhang, M., Li, J., Liu, Z., Zhao, Z., Zhang, Y., Zhou, S., & Wang, Z. (2018). Improving water use efficiency and grain yield of winter wheat by optimizing irrigations in the North China Plain. Field Crops Research, 221, 219–227.
- Yasmin, H., Bano, A., Wilson, N. L., Nosheen, A., Naz, R., Hassan, M. N., Ilyas, N., Saleem, M. H., Noureldeen, A., Ahmad, P., & Kennedy, I. (2022). Drought-tolerant Pseudomonas sp. showed differential expression of stress-responsive genes and induced drought tolerance in Arabidopsis thaliana. Physiologia Plantarum, 174(1), e13497. https://doi.org/10.1111/ppl.13497
- Zahedifar, M., & Najafian, S. (2017). Ocimum basilicum L. growth and nutrient status as influenced by biochar and potassium-nano chelate fertilizers. Archives of Agronomy and Soil Science, 63(5), 638–650.
- Zai, X. M., Fan, J. J., Hao, Z. P., Liu, X. M., & Zhang, W. X. (2021). Effect of co-inoculation with arbuscular mycorrhizal fungi and phosphate solubilizing fungi on nutrient uptake and photosynthesis of beach palm under salt stress environment. Scientific Reports, 11(1), 1–11.