The effect of Serendipitia indica fungus and foliar application of selenate on physiological and morphological traits of lettuce under the stress of the heavy metal cadmium in hydroponic culture

Khanmohammadi, Hajar; Behrouz Ismailpour, Behrouz; Azarmi, Rasoul; Tahami, Seyed Karim; Shahi, Ali; Aslani, Zahra; Maham, Nastaran

doi:10.22034/iuvs.2023.2009342.1309

The effect of Serendipitia indica fungus and foliar application of selenate on physiological and morphological traits of lettuce under the stress of the heavy metal cadmium in hydroponic culture

Document Type : Original Article

Authors

Hajar Khanmohammadi ¹

behrouz Behrouz Ismailpour ²

Rasoul Azarmi ³

seyed karim tahami ⁴

ali shahi ⁵

Zahra Aslani ⁶

Nastaran Maham ⁷

¹ MSc. Student, Department of Horticulture, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran.

² Professor, Department of Horticulture, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran.

³ Associate Professor, Department of Horticulture, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran.

⁴ PhD. Student, Department of Horticulture, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran Faculty of Iranian Academic Center for Education, Culture & Research (ACECR), Ardabil. Iran

⁵ Assistant Professor, Department of Horticulture, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran.

⁶ PhD Graduate, Visiting Researcher, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran.

⁷ PhD. Student, Department of Horticulture, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran.

10.22034/iuvs.2023.2009342.1309

Abstract

Extended Abstract
1. Introduction: Persistent pollutants that cause biological effects in the food chain are called heavy metals. Heavy metals are more persistent than organic pollutants. This has become one of the most dangerous groups of environmental pollutants. Cadmium has attracted much attention due to its toxicity at high concentrations, and the effect of cadmium varies depending on the type of plant. Cadmium harms the growth and development of plants. Also, the most obvious destructive effects of heavy metals on plants are the reduction in the ability to absorb nutrients required for normal plant growth and development. When the concentration of this element in soil is 8 mg/kg, it is considered toxic to plants. Selenium is one of the main elements found in lettuce, which has particular importance in the nutritional status of lettuce. In the hydroponic system, symbiotic fungi can improve plant growth. This study aimed to investigate the effect of Serendipitia indica and selenium foliar application on the growth and biochemical and physiological properties of lettuce under the conditions of heavy element cadmium contamination in hydroponic culture.
2. Materials and Methods: To evaluate the effect of Serendipitia indica fungs and selenium foliar application on the physiological characteristics, growth, and performance of red Little Gem lettuce under the conditions of contamination with the heavy element cadmium, a factorial experiment was carried out in the form of a completely randomized design with four replications under hydroponic cultivation conditions. The first factor of cadmium toxicity in food solution (control, 11.85 and 18.7 mg/liter) and the second factor of Serendipitia indica fungi (inoculation and non-inoculation) and selenium foliar spraying in three concentrations (control, 75 and 150 µM) and the combined treatments of these two It was an invoice. In this research, the wet and dry weight of leaf and root shoot, leaf number, chlorophyll fluorescence, stomatal conductance, electrolyte leakage, symbiosis percentage, chlorophyll a, b, total, malondialdehyde, hydrogen peroxide, soluble sugar, proline, catalase, ascorbate peroxidase, was measured.
3. Results and Discussion: Selenium foliar application and inoculation with Serendipitia indica improved growth indices and biochemical traits in lettuce plants under cadmium stress conditions. The application of mushroom and selenium has a significant effect on leaf weight and dry weight, root weight and dry weight, leaf number, chlorophyll fluorescence, relative water content, stomatal conductance, chlorophyll a, b and total chlorophyll, carotenoid, ascorbate peroxidase, anthocyanin, proline, the percentage of coexistence, electrolyte leakage, malondialdehyde, hydrogen peroxide and catalase.The application of the treatment combination (0 μM cadmium + 150 μM selenium + inoculation of Serendipitya indica fungus caused a significant effect on leaf fresh weight (95.90 g) and dry weight (4.92 g), root fresh weight (34.99 g) and dry weight (1.92), leaf number (20.48), chlorophyll fluorescence (0.897 ms), relative water content (69.27%), stomatal conductance (31.97 mmol/m2/s), chlorophyll a, b (0.19 mg/g wet weight; 0.078 mg/g wet weight) and total chlorophyll (0.626 mg/g wet weight), carotenoids (0.71 mg/g wet weight), ascorbate peroxidase (0.067), proline (0.664 μg/fresh weight), percentage Symbiosis (89.75%), electrolyte leakage (38.88%), malondialdehyde (0.067), soluble sugar (0.829 mg/fresh weight), hydrogen peroxide (0.090), and catalase (0.076). The fungus Serendipitya indica increases the amount of auxin and cytokinin in the plant, and since auxin and cytokinin increase the production of adventitious roots, it is effective in increasing the fresh and dry weight of the aerial parts. In the present study, selenium foliar spraying improved the levels of chlorophyll a, b, total chlorophyll, and carotenoids in lettuce plants. In another similar finding, selenium foliar spraying increased chlorophyll a, b, and carotenoids in lettuce leaves. By improving the absorption of elements, the Serendipitia indica fungus increases the plant's resistance to these conditions and enhances its growth and development in metal-contaminated soils. Selenium foliar spraying showed that the use of elicitors increased the amount of proline, and with the intensification of cadmium stress, the amount of proline increased.
4. Conclusion: From this research, it can be concluded that the use of symbiotic fungus (Serendipitia indica) in foliar spraying of lettuce and selenium in a hydroponic system can improve the growth and absorption of elements, and also the combined use of these two factors has a positive effect in comparison using these two factors separately. More about the growth and physiological characteristics of lettuce.

Keywords

Keywords: Piriformospora indica fungus

selenium foliar application

cadmium

Lettuce

Abadi, V. A., Sepehri, H. A. Rahmani, H. K., Dolatabad, M., Shamshiripour, M. & Khatabi, B. (2021). Diversity and abundance of culturable nitrogen‐fixing bacteria in the phyllosphere of maize. Journal of Applied Microbiology, 131(2), 898-912. https://doi.org/10.1111/jam.14975

Abdollahi, A., Barin, M., Soltani, A. A., Torabi Giglou, M., Behrouz Ismailpour, B., & Tahami, S. K. (2023). Evaluation of Influence of Selenium Foliar Application on Growth and Physiological Characteristics of Basil (Ocimum basilicum L.) in Arsenic-Contaminated Soil. Journal of Vegetables Sciences, 7(14), 59-76.‏ https://doi.org/10.22034/iuvs.2019400.134

Aebi, H. 1984. Catalase in vitro. In Methods in Enzymology. Academic Press. 105, 121-126. http://dx.doi.org/10.1016/S00766879(84)05016-3

Auge, R. M. (2021). Water relations, drought, and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza, 11, 3–42. http:// doi.org/10.ohld.ag.utk.edu/auge

Azari, A., Modares Sanavi, S. A. M. Askari, H. Ghanati, F. Naji, A. M., & Alizade, B. (2012). Effect of salinity stress on the morphological and physiological of canola and turnip (Brassica napus and B. rapa). Iran. J. Crop Sci., 14: 2. 121-135. (in Persian).

Azizi, I., Esmaielpour, B. & Fatemi, H. (2020). Effect of foliar application of selenium on morphological and physiological indices of savory (Satureja hortensis) under cadmium stress. Food Science & Nutrition, 8(12), 6539-6549. http://doi.org/10.1002/fsn3.1943

Baltruschat, H., Fodor, J. B. D., Harrach, E., Niemczyk, B., Barna, G. & Skoczowski, A. (2019). Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytologist, 180, 501-510. http://doi.org/10.1111/j.1469-8137.2008.02583.x

Baryla, A., Carrier, P., Franck, F., Coulomb, C., Sahut, C. & Havaux, M. (2021). Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth. Planta, 212, 696–709. http:// doi.org/10. 1007/s004250000439

Benavides, M. P., Gallego, S. M. & Tomaro, M. L. (2019). Cadmium toxicity in plants. Brazilian journal of plant physiology, 17, 21-34. http://doi.org/10. 1590/S1677-04202005000100003

Chaudhury, S. & Panda, S. K. (2014). Toxic effects, oxidative stress, and ultrastructural changes in moss Taxithelium nepalense (Schwaegr.) broth. Under chromium and lead phytotoxicity. Water Air Soil Pollut, 167, 73-90. http://doi.org/10.1007/s11270-005-8682-9

Clemens, S., Palmgren, M. G. & Krämer, U. (2018). A long way ahead: understanding and engineering plant metal accumulation. Trends in plant science, 7(7), 309-315. http://doi.org/10.2225/vol6-issue3-fulltext-6

Darqui, F.S., Radonic, L. M., Trotz, P. M., López, N., Rovere, C. V., Hopp, H. E. & Bilbao, M.L. (2018). Potato snakin-1 gene enhances tolerance to Rhizoctonia solani and Sclerotinia sclerotiorum in transgenic lettuce plants. Journal of biotechnology, 283, 62-69. http://doi.org/10.16/j.jbiotec.2018.07.017

Das, P., Samantaray, S. & Rout, G. R. (2020). Studies on cadmium toxicity in plants: a review. Environmental pollution, 98(1), 29-36. https://doi.org/10.3389/fpls.2020.773815

Daryaii, F., Karmat, B., & Arvin, M. (2013). The effect of selenium foliar application on some physiological and morphological traits of two wheat cultivars (Kavir-Roshan) under cadmium stress. Journal of Plant Process and Function, 3, 101-114. https://doi.org/10.22034/csrar.2021.257878.1069

Djanaguiraman, M., Shanker, A. K., Sheeba, J. A., Devi, D. D. & Bangarusamy, U. (2005). Selenium – an antioxidative protectant in soybean during senescence. Plant and Soil, 272, 77-86. https://doi.org/10.1007/s11104-004-4039-1

Ekmekçi, Y., Tanyolac, D. & Ayhan, B. (2008). Effects of cadmium on antioxidant enzymes and photosynthetic activities in leaves of two maize cultivars. J. Plant Physiol., 165(6): 600-611. https://doi.org/10.1016/j.jplph.2007.01.017

Errsus, S., & Barrett, D. (2010). Determination of membrane integrity in onion tissues treated by pulsed electric fields: Use of microscopic images and ion leakage measurements. Innov. Food Sci. Emer. Technol. 11 (14), 598-603.

https://doi.org/10.1016/j.ifset.2010.08.001

Germ, M., Kreft, I., & Osvald, J. (2005). Influence of UV-B exclusion and selenium treatment on photochemical efficiency of photosystem II, yield, and respiratory potential in pumpkins (Cucurbita pepo L.). Plant Physiology and Biochemistry, 43, 445-448. https://doi.org/10.1016/j.plaphy.2005.03.004

Gill, S. S., Khan, N. A., & Tuteja, N. (2012). Cadmium at high dose perturbs growth, photosynthesis, and nitrogen metabolism, while at low dose it upregulates sulfur assimilation and antioxidant machinery in garden cress (Lepidium Sativum L.). Journal of Plant Sciences, 182, 112-120. https://doi.org/10.1016/j.plantsci.2011.04.018

Ghabooli, M. (2014). Effect of Piriformospora indica inoculation on some physiological traits of barley(Hordeum vulgare) under salt stress. Chemistry of Natural Compounds, 50(6),1082-1087. http://dx.doi.org/10.1007/s10600-014-1164-9

Ghorbani, A., Razavi, S. M., Omran, V. O. G., & Pirdashti, H. (2018). Piriformospora indica alleviates salinity by boosting the redox poise and antioxidative potential of tomato. Russian Journal of Plant Physiology, 65(6), 898-907. https://doi.org/10.1134/S1021443718060079

Hawrylak-Nowak, B., Dresler, S., Rubinowska, K., Matraszek-Gawron, R., Woch, W. & Hasanuzzaman, M. (2018). Selenium biofortification enhances the growth and alters the physiological response of lamb's lettuce grown under high temperature stress. Plant Physiology and Biochemistry, 127,446-456. http://dx.doi.org/10.1016/j.plaphy.2018.04.018

He, Y., Yang, Z., Li, M., Jiang, M., Zhan, F., Zu, Y., Li, T. & Zaho, Z. (2017). Effects of a dark septate endophyte (DSE) on growth, cadmium content, and physiology in maize under cadmium stress. Environ Sci. Pollut. Res., 24(2), 119-128. http://dx.doi.org/10. 10.1016/j.plaphy.2018.04.018

Heath, R. L., & Packer, L. (1968). Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Journal of Biochemistry and Biophysics, 125, 180-198. http://dx.doi.org/10.1016/00039861(68)90654-1

Irigoyen, J. J., Emerich, D.W., & Sanchez-Diaz, M. 1992. Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiologia Plantarum, 84, 55-60. https://doi.org/10.1111/j.1399 3054.1992.tb08764.x

Kabata-Pendias, A. (2021). Trace metals in soils: current issue in Poland. Acta Universitatis Wratislaviensis. Prace Botaniczne, 79,13-20. http://dx.doi.org/10.1007/978-3-540-32714-1

Kafi, M., Kamili, A. N., Husaini, A. M., Ozturk, M., & Altay, V. (2018). An expensive spice saffron (Crocus sativus L.): a case study from Kashmir, Iran, and Turkey. In Global perspectives on underutilized crops (pp. 109-149). Springer, Cham. http://dx.doi.org/10.1007/978-3-319-77776-4_4

Karami, A., & Zarea, M. J. (2019). Physiological and nutritional responses of inoculated Alfalfa (Medicago sativa, cv hamedani) with the fungus Piriformospora indica and bacterium Azospirillum Spp under salt stress. Journal of Crop Production, 7 (1), 109-129. (In Persian). http://dx.doi.org/10.1001.1.2008739.1393.7.1.7.0

Khan, M. I. R., Nazir, F., Asgher, M., Per, T. S. & Khan, N. A. (2015). Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. Journal of plant physiology, 173, 9-18. http://dx.doi.org/10.1016/j.jplph.2014.09.011. Epub 2014 Oct 7

Khan, M. Y., Prakash, V. Yadav, V. Chauhan, D. K., Prasad, S. M., Ramawat, N. & Sharma, S. (2019). Regulation of cadmium toxicity in roots of tomato by indole acetic acid with special emphasis on reactive oxygen species production and their scavenging. Plant Physiology and Biochemistry, 142, 193-201.http://dx.doi.org/10.1016/j.plaphy.2019.05.006.

Lyons, I. M., & Beilock, S. L. (2019). Numerical ordering ability mediates the relation between number-sense and arithmetic competence. Cognition, 121(2), 256-261. http://dx.doi.org/10.1016/j.cognition.2011.07.009

Malar, M., Schiavon, M. S., dall’Acqua, E., & Pilon-Smits, A. (2016). Effects of selenium biofortification on crop nutritional quality. Frontiers in plant science, 6, 280-291. https://doi.org/10.3389/fpls.2015.00280

Maghsoudi, K., Ashrafi Dehkordi, E. & Mazloumi, S. M. (2021). The role of brassinosteroids and salicylic acid on spinach growth and cadmium accumulation under cadmium stress.Journal of Vegetable Sciences, 4(2), 15-33. http://dx.doi.org/10.22034/iuvs.2021.139084.1125

Nanda, R., & Agrawal, V. (2018). Piriformospora indica, an excellent system for heavy metal sequestration and amelioration of oxidative stress and DNA damage in Cassia angustifolia Vahl under copper stress. Ecotoxicology and Environmental Safety, 156, 409-419. http://dx.doi.org/10.10.1016/j.ecoenv.2018.03.016

Mohebodini, M., Mokhtar, J. J., Mahboudi, F., & Alizadeh, H. (2011). Effects of genotype, explant age, and growth regulators on callus induction and direct shoot regeneration of Lettuce (Lactuca sativa L.). Australian Journal of Crop Science, 5(1), 92-95.

Nowak, J., Kaklewski, K., & Ligocki, M. (2004). Influence of selenium on the oxidoreductive enzymes activity in soil and in plants. Soil Biology and Biochemistry, 36, 15531558. https://doi.org/10.1016/j.soilbio.2004.07.002

Oraei, M., Tabatabaei, S. J., Imani, A. & Fallahi, E. (2010). Interactive effect of boron toxicity and rootstock on the growth, photosynthetic rate, and nutrient concentrations of almond tree. Journal of Agricultural Science and Sustainable Production, 20(2), 49-63. http://dx.doi.org/10.1001.1.24764310.1389.20.2.5.8

Paquin, R., & Lechasseur, P. 1979. Observations sur une methode de dosage de la proline libre dans les extraits de plants. Canadian Journal of Botany, 57: 1851-1854. https:// dx.doi.org/10.1139/b79-233

Philips, J., & Hayman, D. (1999). Improved Procedures for Cleaning Roots and staining parasitic and vesicular arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society, 55, 158-161. http://dx.doi.org/10.1016/S00071536(70)80110-3

Pirdashti, H., Yaghoubian, Y., Mohammadi Goltapeh, E., & Hosseini, S. J. (2012). Effect of mycorrhiza-like endophyte (Sebacina vermifera) on growth, yield, and nutrition of rice (Oryza sativa L.) under salt stress. Journal of Agricultural Technology, 5, 1651-1661.

Prasad, R., Kamal, S., Sharma, P. K., Oelmüller, R., & Varma, A. (2013). Root endophyte Piriformospora indica DSM 11827 alters plant morphology, enhances biomass, and antioxidant activity of medicinal plant Bacopa monniera. The Journal of Basic Microbiology, 53, 1016–1024. http://dx.doi.org/10.1002/jobm.201200367

Rainbow, P. S. (2022). Trace metal concentrations in aquatic invertebrates: why and so what?. Environmental pollution, 120(3), 497-507. http://dx.doi.org/10.10.1016/S0269-7491(02)00238-5

Salimi Tamalla, N., Seraj, F., Pirdashti, H., & Yaghoubian, Y. (2014). The effect of seed biopriming by Piriformospora indica and Trichoderma virens on the growth, morphological, and physiological parameters of mung bean (Vigna radiata L.) seedlings. Iran. J. Seed Sci. Res., 1(2), 67-78. (In Persian). http://dx.doi.org/10.1001.1.24763780.1393.1.2.6.8

Saremi Rad, B., Esfandiari, E. A., Shokrpour, M., Sofalian, O., Avanes, A., & Mousavi, S. B. (2021). Cadmium effects on some morphological and physiological parameters in wheat at the seedling stage. Journal of Plant Research, 27(1), 1-11.

Sepehri, N., Saleh Rastin, N., Hossieni Salkedeh, G., & Khayam Nekouie, M. (2009). Effect of endophytic fungus, Piriformospora indica, on growth and resistance of Hordeum vulgare L. to salinity stress. Rangeland, 3 (3), 508-518. [In Persian with English Summary].

Seppanen, M., Turakainen, M., & Hartikainen, H. (2003). Selenium effects on oxidative stress in potato. Plant Science, 165, 311-319. http://dx.doi.org/10.1016/S01689452(03)00085-2

Seraj, F., Salimi Tamali, N., Pirdashti, H., & Yaghoubian, Y. (2018). The response of wheat (Triticum aestivum L.) vegetative and physiological attributes to salt stress and the effect of seed biopriming by Piriformospora indica and Trichoderma virens in improving salinity compatibility. Iran. Seed Science and Technology, 6(2), 77-90. (In Persian). https://doi.org/10.22034/ijsst.2018.116529

Sergiev, I., Alexieva, V., & Karanov, E. (1997). Effect of spermine, atrazine, and their combination between on some endogenous protective systems and stress markers in plants. Comptes Rendus de l’Academie Bulgare des Sciences, 51, 121-12. https://doi.org/10.1046/j.13653040.2001.00778.x

Shanker, A. K., Cervantes, C., Loza-Tavera, H., & Avudainayagam, S. (2021). Chromium toxicity in plants. Environment international, 31(5), 739-753. https://doi.org/10.1016/j.envint.2005.02.003

Spanany, A., & Fallah, S. (2016). The effect of cadmium stress on seeds germination characteristics of some medicinal plants under in vitro conditions.‏ Iranian Journal of Medicinal and Aromatic Plants, 3,528-542. http://dx.doi.org/10.22092/ijmapr.2016.106833

Soon, Y. K., & Abboud, S. (1993). Cadmium, chromium, lead, and nickel. Soil sampling and methods of analysis, 101-108.

Sharmila, P., Kumari, P. K., & Singh, K. (2017). Cadmium toxicity-induced proline accumulation is coupled to iron depletion. Protoplasma 254, 763–770. http://dx.doi.org/10.10.1007/s00709-016-0988-5

Sun, C., Johnson, J. M., Cai, D., Sherameti, I., Oelmüller, R., & Lou, B. (2015). Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes, and the plastid-localized CAS protein. Journal of Plant Physiology, 167, 1009-1017. http://dx.doi.org/10.10.1016/j.jplph.2010.02.013

Sudhakar, C., Lakshmi, A., & Giridarakumar, S. 2001. Changes in the antioxidant enzyme efficacy in two high-yielding genotypes of mulberry (Morus alba L.) under NaCl salinity. Plant Science, 161(3), 613-619. http://dx.doi.org/10.1016/S0168-9452(01)00450-2

Tapiero, H., Townsend, D. M., & Tew, K. D. (2003). Dossier: Oxidative stress pathologies and antioxidants: The antioxidant role of selenium and seleno-compounds. Biomedicine and Pharmacotherapy, 57, 134-144. http://dx.doi.org/10.1016/s0753-3322(03)00035-0

Turner, N. C. (1981). Techniques and experimental approaches for measurement of plant water status. International Journal of Plant-Soil Relationships, 58: 339-366. http://dx.doi.org/10.1007/BF02180062

Valentovic, P., Luxova, M., Kolarovic, L., & Gasparikova, O. (2016). Effect of osmotic stress on compatible solutes content, membrane stability, and water relations in two maize cultivars. Plant Soil and Environment, 52(1), 186-191. http://dx.doi.org/10. 17221/3364-PSE

Varma, A., Singh, A., Sahay, N.S., Sharma. J., Kumari, M., Rana. D., Takeran, S., Deka, D. & Baharti K. (2001). Piriformospora indica: An axenically cultivable mycorrhiza-like endosymbiotic fungus. Mycota IX. Spiringer Series, pp. 123-150.

Wang, L., Zhou, Q., Ding, L., & Sun, Y. (2018). Effect of cadmium toxicity on nitrogen metabolism in leaves of Solanum nigrum L. Journal of Hazardous Materials, 154(1-3): 818-825.http://dx.doi.org/10.1016/j.jhazmat.2007.10.097

Wu, C., Dun, Y., Zhang, Z., Li, M., & Wu, G. (2020). Foliar application of selenium and zinc to alleviate wheat (Triticum aestivum L.) cadmium toxicity and uptake from cadmium-contaminated soil. Ecotoxicology and Environmental Safety, 190, 110091. http://dx.doi.org/10.1016/j.ecoenv.2019.110091

Xue, T. L., Hartikainen, H., & Piironen, V. (2001). Antioxidative and growth-promoting effects of selenium on senescing lettuce. Plant and Soil, 237, 55-61. http://dx.doi.org/10.1023/A:1013369804867

Zarea, M. J., Chordia, P., & Varma, A. (2013). Piriformospora indica Versus Salt Stress. Soil Biology, 33, 263-281.

Zarea, M. J., Hajinia, S., Karimi, N., Goltapeh, E. M., Rejali, F. & Varma, A. (2016). Effect of Piriformospora indica and Azospirillum strains from saline or non-saline soil on mitigation of the effects of NaCl. Soil Biology and Biochemistry, 45, 139-146. http://dx.doi.org/10.1016/j.soilbio.2011.11.006

Zhang, X. D., Meng, J. G., Zhao, K. X., Chen, X., & Yang, Z. M. (2018). Annotation and characterization of Cd-responsive metal transporter genes in rapeseed (Brassica napus). Biometals, 31,107-121.http://dx.doi.org/10.1007/s10534-017-0072-4

Zhu, X. C., Song, F. B., & Liu, S. Q. (2021). Arbuscular mycorrhiza impacts on drought stress of maize plants by lipid peroxidation, proline content, and activity of antioxidant system. Journal of Food, Agriculture and Environment, 9, 583-587.

http://dx.doi.org/10.1016/j.soilbio.2011.11.006