Evaluation of Influence of Selenium Foliar Application on Growth and Physiological Characteristics of Basil (Ocimum basilicum L.) in Arsenic-Contaminated Soil

Abdollahi, Ali; Barin, Mohsen; Soltani, Ali Ashraf; Torabi Giglou, Mousa; Behrouz Ismailpour, Behrouz; Tahami, Seyed Karim

doi:10.22034/iuvs.2022.1973789.1250

Evaluation of Influence of Selenium Foliar Application on Growth and Physiological Characteristics of Basil (Ocimum basilicum L.) in Arsenic-Contaminated Soil

Document Type : Original Article

Authors

Ali Abdollahi ¹

Mohsen Barin ²

Ali Ashraf Soltani ³

Mousa Torabi Giglou ⁴

behrouz Behrouz Ismailpour ⁵

seyed karim tahami ⁶

¹ Ph.D. Student, Department of Horticultural Sciences, Faculty of Agriculture, University of Mohaghegh Ardabili, Ardabil, Iran

² Associate Professor, Department of Soil Sciences & Engineering, Faculty of Agriculture, Urmia University, Urmia, Iran

³ Associate Professor, Department of Soil Sciences & Engineering, Faculty of Agriculture, University of Mohaghegh Ardabili, Ardabil, Iran

⁴ Associate Professor, Department of Horticultural Sciences, Faculty of Agriculture, University of Mohaghegh Ardabili, Ardabil, Iran

⁵ Professor, Department of Horticultural Sciences, Faculty of Agriculture, University of Mohaghegh Ardabili, Ardabil, Iran

⁶ Ph.D. Student, Department of Horticultural Sciences, Faculty of Agriculture, University of Mohaghegh Ardabili, Ardabil, Iran Faculty of Iranian Academic Center for Education, Culture & Research (ACECR), Ardabil. Iran.

10.22034/iuvs.2022.1973789.1250

Abstract

Extended Abstract

Introduction: Basil (Ocimum basilicum), as an annual plant, belongs to the family Lamiaceae, native to Asia (Iran, India, Pakistan, Thailand, etc.) and grows in warm and semi-warm regions. Arsenic (As) is a highly dangerous heavy metal for plants and human. This quasi-metal is widely distributed in the earth's crust, and also is the twentieth most abundant element in the earth's crust. Selenium (Se) is a non-metallic chemical element and also has similarities to arsenic. Global interest in the biological effects of selenium on the environment and the food chain is growing because selenium is essential as a micronutrient for many organisms, including humans and other animals (although it is toxic in high concentrations). Given that arsenic is one of the most important factors limiting crop production in the agricultural sector, it seems necessary to conduct researches in this field to eliminate or reduce the toxic effects of these element on agricultural plants.
Materials and Methods: In this study, the effect of selenium on increasing the tolerance rate of basil plant against arsenic heavy metal stress was investigated as a factorial experiment based on completely randomized design under greenhouse condition. The first factor included arsenic-contaminated soil (4576 mg kg^-1) and non-contaminated soil, and the second factor included different concentrations of selenium treatment (0, 5 and 10 mg L^-1 selenium sodium). Foliar application of selenium was conducted at two stages. The first stage of foliar application was carried out at 4-leaf stage and the second stage of foliar application was done two weeks after the first stage. Leaf number, leaf area, stem height, fresh and dry weight of leaf and stem, chlorophyll and carotenoid content, free proline content, phenol, flavonoid and anthocyanin content, electrolyte leakage and antioxidant enzymes activity were evaluated at the end of the experiment.
Results and Discussion: The results showed that arsenic stress negatively affected the morphological traits such as leaf number and area, fresh and dry weight of leaf, fresh and dry weight of stem and plant height, but selenium treatment alleviated the toxicity of arsenic and increased the values of these traits, so that treated plants had higher values of morphological characteristics comparing to control plants under arsenic heavy metal stress. The highest values of morphological traits were observed in plants treated with the highest concentration of selenium (10 mg L^-1). In terms of physiological traits, arsenic heavy metal stress reduced the values of some of these traits, so that the lowest amounts of chlorophyll a, chlorophyll b and total chlorophyll, anthocyanin, phenol, and flavonoids were recorded in plants grown in arsenic-contaminated soil without foliar application of selenium. On the other hand, the lowest activity rates of guaiacol peroxidase, catalase and ascorbate peroxidase were observed in plants grown in non-contaminated soil and without selenium foliar application. Also, the both arsenic stress and selenium treatment increased proline accumulation and soluble sugars content of treated plants comparing to control plants. Heavy metal stress increases the production and accumulation of reactive oxygen species (ROS) and damages the membrane structure resulting in more electrolyte leakage. Selenium application led to increasing plant resistance rate against arsenic stress, mainly by enhancing cells antioxidant capacity and osmotic potential.
Conclusion: Considering basil is one of the most important aromatic vegetables which has fresh consumption, crispness and wateriness of its leaves and young shoots is one of the most important commercially traits which directly affect crop marketability. Considering arsenic stress has a negative effect on leaf morphological traits (number, area, fresh weight and dry weight) and stem characteristics (fresh weight, dry weight and height), it is recommended to use selenium foliar application as an efficient technique to overcome adverse effects of arsenic stress on basil production in regions with contaminated soils.

Keywords

Antioxidant enzymes

Biochemical compounds

Heavy metal stress

Leafy vegetable

Medicinal plant

- Abbasi, B., Maleki, R. & Pirkharrati, H. (2017). Study effects of mining and gold extraction on amount of water contamination to As and Hg in Zarshouran area of Takab. Journal of Environmental Geology, 11 (40), 39-48.
- Abdelatey, L. M., Khalil, W. K., Ali, T. H. & Mahrous, K. F. (2011). Heavy metal resistance and gene expression analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Egyptian soils. Journal of Applied Science in Eenvironmental Sanitation, 6, 201-211.
- Aebi, H. (1984). Catalase activity. Methods in Enzymology, 105, 121-126.
- Aghaei, K., Rakhosravani, B., Moghanlou, L. & Ghotbi Ravandi, A. A. (2019). Study of the effect of cadmium accumulation on some physiological and biochemical characteristics of basil plants (Ocimum basilicum L.). Journal of Plant Process and Function, 8(33), 107-122.
- Alam, M. Z., Hoque, M. D. A., Jalal Ahammed, G. & Carpenter-Boggs, L. (2020). Effects of arbuscular mycorrhizal fungi, biochar, selenium, silica gel, and sulfur on arsenic uptake and biomass growth in Pisum sativum L. Emerging Contaminants, 6, 312-322.
- Ali, B., Tao, Q., Zhou, Y., Gill, R. A., Ali, S., Rafiq, M. T., Xu, L. & Zhou, W. (2013). 5-Aminolevolinic acid mitigates the cadmium-induced changes in Brassica napus as revealed by the biochemical and ultra-structural evaluation of roots. Ecotoxicology and Environmental Safety, 92, 271-280.
- Alves, L. R., Rossatto, D. R. & Gratao, P. L. (2020). Selenium improves photosynthesis and induces ultrastructural changes but does not alleviation cadmium-stress damage in tomato plants. Protoplasma, 257, 597-605.
- Asghari, M., Masoumi Zavariyan, A. & Yousefi Rad, M. (2020). Investigating the effect of sodium nitroprusside in reducing cadmium toxicity in basil (Ocimum basilicum L.) Plant. Environmental Stresses In Crop Science, 13(3), 1009-1018.
- Ashraf, M. & Foolad, M. R. (2007). Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany, 59, 206-216.
- Azizi, I., Esmaeilpour, B. & Fatemi, H. (2020). Effect of foliar application of selenium on morphological and physiological indices of savory (Satureja hortensis) under cadmium stress. Food Science and Nutrition, 8(12), 6539-6549.
- Beauchamp, C. & Fridovich, I. (1971). Superoxide dismutase: improved assay and an assay applicable to acrylamide gels. Analytical biochemistry, 44(1), 276-287.
- Broadley, M., Brown, P., Cakmak, I., Ma, J. F., Rengel, Z. & Zhao, F. (2012). Beneficial elements. In: P. Marschner (Ed.) Marschner's mineral nutrition of higher plants, 3nd Edition. Academic Press Inc. San Diego, 672 p.
- Chauhan, R., Awasthi, S., Tripathi, P., Mishra, S., Dwivedi, S., Niranjan, A., Mallick, S., Tripathi, P., Pande, V. & Tripathi, R. D. (2017). Selenite modulates the level of phenolics and nutrient element to alleviate the toxicity of arsenite in rice (Oryza sativa L.). Ecotoxicology and Environmental Safety, 138, 47-55.
- Conte, F., Copat, C., Longo, S., Conti, G. O., Grasso, A., Arena, G., Brundo, M. V. & Ferrante, M. (2015). First data on trace elements in Haliotis tuberculata (Linnaeus, 1758) from southern Italy: safety issues. Food and Chemical Toxicology, 81, 143-150.
- Copat, C., Grasso, A., Fiore, M., Cristaldi, A., Zuccarello, P., Signorelli, S. S., Conti, G. O. & Ferrante, M. (2018). Trace elements in seafood from the Mediterranean Sea: an exposure risk assessment. Food and Chemical Toxicology, 115, 13-19.
- Fakhria, Y., Mohseni-Bandpei, A., Conti, G. O., Ferrante, M., Cristaldi, A., Jeihooni, A. K., Dehkordi, K. K., Alinejad, A., Rasoulzadeh, H., Mohseni, S. M., Sarkhosh, M., Keramati, H., Moradii, B., Amanidaz, N. & Baninameh, Z. (2018). Systematic review and health risk assessment of arsenic and lead in the fished shrimps from the Persian Gulf. Food and Chemical Toxicology, 113, 278-286.
- Fatemi, H., Esmaielpour, B., Sefidkon, F., Soltani, A. A. & Nematollahzadeh, A. (2020). How mycorrhiza symbiosis help coriander (Coriandrum sativum L.) plants grow better under contaminated soil?. Journal of Plant Nutrition, 43(13), 2040-2053.
- Fattahi, B., Arzani, K., Souri, M. K. & Barzegar, M. (2020). Effect of cadmium and lead on morpho-physiological traits and photosynthesis of sweet basil (Ocimum basilicum L.). Iranian Journal of Horticultural Science, 50(4), 839-849. (In Farsi)
- Feizi, Kh., Amirinejad, A. & Ghobadi, M. (2021). The effects of biochar and salicylic acid on reducing Pb-induced stress in basil crop (Ocimum basilicum L.). Iranian Journal of Soil and Water Research, 52 (2), 539-547. (In Farsi)
- Gill, R. A., Zang, L., Ali, B., Farooq, M. A., Cui, P., Yang, S., Ali, S. & Zhou, W. (2015). Chromium-induced physio-chemical and ultrastructural changes in four cultivars of Brassica napus L. Chemosphere, 120, 154-164.
- Gupta, D. K., Srivastava, S., Huang, H. G., Romero-Puertas, M. C. & Sandalio, L. M. 2011. Arsenic tolerance and detoxiﬁcation mechanisms in plants. In: I. Sherameti and A. Varma (eds.), Detoxiﬁcation of Heavy Metals, Soil Biology, 30, 169-179.
- Hekmati, J., Hamidoghli, Y., Esmaielpour, B. & Ghasemnezhad, M. (2021). Effect of arsenic and phosphate biofertilizer on physiological and biochemical properties of green mint (Mentha spicata L.). Journal of Plant Production Research, 28(1), 127-139. (In Farsi)
- Huang, L, M., Rizwan M., Dai, Z., Yuan, Y., Hossain, M. M., Cao, M., Xiong, M. & Tu, S. (2021). Synergistic effect of silicon and selenium on the alleviation of cadmium toxicity in rice plants. Journal of Hazardous Materials, 401, 123393.
- Islam, E., Tahir Khan, M. & Irem, S. (2015). Biochemical mechanisms of signaling: perspectives in plants under arsenic stress. Ecotoxicology and Environmental Safety, 114, 126-133.
- Jamwal, A., Naderia, M. & Niyogiab, S. (2016). An in vitro examination of selenium cadmium antagonism using primary cultures of rainbow trout (Oncorhynchus mykiss) hepatocytes. Metall, 8, 218-227.
- Jia, H., Song, Z., Wu, F., Ma, M., Li, Y., Han, D., Yang, Y., Zhang, S. & Cui, H. (2018). Low selenium increases the auxin concentration and enhances tolerance to low phosphorous stress in tobacco. Environmental and Experimental Botany, 153, 127-134.
- Karimi, N. & Souri, Z. (2016). Antioxidant enzymes and compounds complement each other during arsenic detoxification in shoots of Isatis cappadocica Desv. Chemistry and Ecology, 32(10), 937-951.
- Karimi, N., Ghaderian, S. M., Marofi, H. & Schat, H. (2010). Analysis of arsenic in soil and vegetation of a contaminated area in Zarshuran, Iran, identify two angiosperm arsenic hyperaccumulators. International Journal of Phytoremedation, 12, 159-173.
- Kohli, S. K., Bali, S., Tejpal, R., Bhalla, V., Verma, V., Bhardwaj, R., Alqarawi, A. A., Abd-Allah, E. F. & Ahmad, P. (2019). In-situ localization and biochemical analysis of bio-molecules reveals Pb-stress amelioration in Brassica juncea L. by co-application of 24-Epibrassinolide and salicylic acid. Scientific reports, 9(1), 1-15.
- Luo, H. T., Wang, Q., He, Z. L., Wu, Y. H., Long, A. M. & Yang, Y. F. (2019). Protection of dietary selenium-enriched seaweed Gracilaria lemaneiformis against cadmium toxicity to abalone Haliotis discus hannai. Ecotoxicology and Environmental Safety, 171, 398-405.
- 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. (In Farsi)
- Malik, J. A., Goel, S., Kaur, N., Sharma, S., Singh, I. & Nayyar, H. (2012). Selenium antagonises the toxic effects of arsenic on mungbean (Phaseolus aureus Roxb.) plants by restricting its uptake and enhancing the antioxidative and detoxification mechanisms. Environmental and Experimental Botany, 77, 242-248.
- Mawia, A. M., Hui, S., Zhou, L., Li, H., Tabassum, J., Lai, C., Wang, J., Shao, G., Wei, X., Tang, S., Luo, J., Hu, H. & Hu, P. (2021). Inorganic arsenic toxicity and alleviation strategies in rice. Journal of Hazardous Materials, 408, 124751.
- Mithofer, A., Schulze, B. & Boland, W. (2014). Biotic and heavy metal stress response in plants: evidence for common signals. FEBS Letters, 566, 1-5.
- Nakano, Y. & Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in Spanish chloroplasts. Plant and Cell Physiology, 22(5), 867-880.
- Nie, M., Hu, C., Shi, G., Cai, M., Wang, X. & Zhao, X. (2021). Selenium restores mitochondrial dysfunction to reduce Cr-induced cellapoptosis in Chinese cabbage (Brassica campestris L. ssp. Pekinensis) root tips. Ecotoxicology and Environmental Safety, 223, 112564.
- Paquin, R. & Lechasseur, P. (1979). Observationssur une methode de dosage de la proline libre dans les extraits de plantes. Canadian Journal of Botany, 57, 1851-1854.
- Pereira, A. S., Dorneles, A. O. S., Bernardy, K., Sasso, V. M., Bernardy, D., Possebom, G., Rossato, L. V., Dressler, V. L. & Tabaldi, L. A. (2018). Selenium and silicon reduce cadmium uptake and mitigate cadmium toxicity in Pfaffia glomerata (Spreng.) Pedersen plants by activation antioxidant enzyme system. Environmental Science and Pollution Research International, 25(19), 18548-18558.
- Piršelová, B., Boleček, P. & Gálusová, T. (2016). Effect of cadmium and arsenic on chlorophyll fluorescence of selected soybean cultivars. Russian Journal of Plant Physiology, 63(4), 469-473.
- Prasad, A., Kumar, S., Khaliq, A. & Pandey, A. (2011). Heavy metals and arbuscular mycorrhizal (AM) fungi can alter the yield and chemical composition of volatile oil of sweet basil (Ocimum basilicum L.). Biology and Fertility of Soils, 47, 853-861.
- Rahman, M. M., Hossain, K. F. B., Banik, S., Sikder, M. T., Akter, M., Bondad, S. E. C., Rahaman, M. S., Hosokawa, T., Saito, T. & Kurasaki, M. (2019). Selenium and zinc protections against metal-(loids)-induced toxicity and disease manifestations: a review. Ecotoxicology and Environmental Safety, 168, 146-163.
- Retondario, A., Fernandes, R., Rockenbach, G., lves, M. A., Bricarello, L. P., Trindade, E. B. S. M. & de Vasconcelos, F. A. G. (2018). Selenium intake and metabolic syndrome: a systematic review. Clinical Nutrition, 38(2), 603-614.
- Sheikhalipour, M., Esmaielpour, B., Behnamian, M., Gohari, G., Giglou, M. T., Vachova, P. & Skalicky, M. (2021). Chitosan–selenium nanoparticle (Cs–Se NP) foliar spray alleviates salt stress in bitter melon. Nanomaterials, 11(3), 684.
- Shekari, L., Aroiee, H., Mirshekari, A. & Nemati, H. (2018). Application of selenium in lowering damage of cadmium, nickel, and lead stresses on germination and antioxidant activity of cucumber seedlings (Cucumis sativus L.). Journal of Seed Research, 8 (2), 55-72. (In Farsi)
- Siriporndulsil, S., Traina, S., Verma, D. P. & Sayre, R. T. (2002). Molecular mechanism of proline mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell, 14, 2837-47.
- Sun, H., Dai, H., Wang, X. & Wang, G. (2016). Physiological and proteomic analysis of selenium-mediated tolerance to Cd stress in cucumber (Cucumis sativus L.). Ecotoxicology and Environmental Safety, 133, 114-126.
- Tang, L., Hamid, Y., Liu, D., Jahidul Islam Shohag, M. D., Zehra, A., He, Z., Feng, Y. & Yang, X. (2020). Foliar application of zinc and selenium alleviates cadmium and lead toxicity of water spinach–Bioavailability/cytotoxicity study with human cell lines. Environment International, 145, 106-122.
- Ulhassan, Z., Gill, R. A., Huang, H., Ali, S., Mwamba, T. M., Ali, B., Huang, Q., Hamid, Y., Khan, A. R., Wang, J. & Zhou, W. (2019). Selenium mitigates the chromium toxicity in Brassicca napus L. by ameliorating nutrients uptake, amino acids metabolism and antioxidant defense system. Plant Physiology and Biochemistry, 145, 142-152.
- Ullah, A., Heng, S., Munis, M.F.H., Fahad, S. & Yang, X. (2015). Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: A review. Environmental and Experimental Botany, 117, 28-40.
- Wang, L., Gao, Y., Wang, X., Qin, Z., Liu, B., Zhang, X. & Wang, G. (2021). Warming enhances the cadmium toxicity on macrophyte Myriophyllum aquaticum (Vell.) Verd seedlings. Environmental Pollution, 268, 115912.
- Wankhede, D. P., Gupta, M., Singh, A. K. (2013). Arsenic toxicity in crop plants: approaches for stress resistance. In: N. Tuteja, S.S. Gill (Eds.), Crop Improvement under Adverse Conditions, Springer Science+Business Media New York. 347-360.
- Wu, J. T., Hsieh, M. T. & Kow, L. C. (2020). Role of proline in response to toxic copper in Chlorella sp. (Chlorophyceae) cells. Journal of Phycology, 31, 113-7.
- Wu, Z., Liu, S., Zhao, J., Wang, F., Du, Y., Zou, S., Li, H., Wen, D. & Huang, Y. (2017). Comparative responses to silicon and selenium in relation to antioxidant enzyme system and the glutathione-ascorbate cycle in flowering Chinese cabbage (Brassica campestris L. ssp. Chinensis var. utilis) under cadmium stress. Environmental and Experimental Botany, 133, 1-11.
- Zembala, M., Filek, M., Walas, S., Mrowiec, H., Kornas, A., Miszalski, Z. & Hartikainen, H. (2010). Effect of selenium on macro- and microelement distribution and physiological parameters of rape and wheat seedlings exposed to cadmium stress. Plant Soil, 329, 457-468.
- Zhao, Y., Hu, C., Wang, X., Qing, X., Wang, P., Zhang, Y., Zhang, X. & Zhao, X., (2019). Selenium alleviated chromium stress in Chinese cabbage (Brassica campestris L. ssp. Pekinensis) by regulating root morphology and metal element uptake. Ecotoxicology and Environmental Safety, 173, 314-321.