Biostimulants Mitigate Cadmium Stress in Rosemary (Rosmarinus Officinalis L.): A Comparative Analysis of Growth, Mineral Nutrition, and Phytochemical Responses

Year 2025, Volume: 9 Issue: Special, 72 - 81, 28.12.2025

Muhammed Said Yolcu

https://doi.org/10.31015/2025.si.15

Abstract

This study aimed to assess the impacts of varying cadmium doses (0, 25, 100 µmol) and specific biostimulants (ascorbic acid, gibberellic acid, Bacillus megaterium, and Frateuria aurantia) on the growth parameters, macro-micro mineral elements, chlorophylls, total phenolic compounds, total flavonoids, total antioxidants, total carotenoids, MDA, and phenolic compounds of Rosmarinus officinalis L. The study employed a factorial design in a completely randomized experimental setup with three replications conducted in open-field pot trials. Cadmium applications induced significant negative stress across all growth parameters, mineral element absorption except for iron and zinc, biochemical parameters except for total antioxidants and MDA, and all phenolic compoundsIn the gibberellic acid treatments, root length, seedling length, root fresh weight, seedling fresh weight, root dry weight (statistically in the same group as Bacillus megaterium), potassium, magnesium, chlorophyll a, chlorophyll b, total chlorophyll, and catechin hydrate exhibited the highest values compared to the controls and other biostimulants, making it the most effective treatment in mitigating cadmium stress. Ascorbic acid treatments proved to be the most effective in enhancing the plant’s tolerance to cadmium stress by inducing the greatest increases in vanillin, naringin, resveratrol, and chrysin levels among the phenolic compounds. Frateuria aurantia rhizobacteria applications contributed to alleviating cadmium stress by increasing total phenolic and potassium absorption the most compared to other applications. Applications of Bacillus megaterium rhizobacteria were the most effective biostimulant in reducing cadmium stress by maximally increasing calcium, manganese and copper absorption, total flavonoids, total carotenoids and levels of various phenolic compounds such as rutin, rosmarinic acid, salicylic acid and quercetin. In this study, it was demonstrated that each biostimulant used could be effective in mitigating cadmium stress through different parameters.

Keywords

Biochemical parameter , Biostimulants , Cadmium stress , Growth , Rosemary

References

• Abou-Shanab, R. A., Mathai, P. P., Santelli, C., & Sadowsky, M. J. (2020). Indigenous soil bacteria and the hyperaccumulator Pteris vittata mediate phytoremediation of soil contaminated with arsenic species. Ecotoxicology and environmental safety, 195, 110458. https://doi.org/10.1016/j.ecoenv.2020.110458
• Adhikari, S., Ghosh, S., Azahar, I., Adhikari, A., Shaw, A. K., Konar, S., & Hossain, Z. (2018). Sulfate improves cadmium tolerance by limiting cadmium accumulation, modulation of sulfur metabolism and antioxidant defense system in maize. Environmental and Experimental Botany, 153, 143-162. https://doi.org/10.1016/j.envexpbot.2018.05.008
• Ahmad, P., Raja, V., Ashraf, M., Wijaya, L., Bajguz, A., & Alyemeni, M. N. (2021). Jasmonic acid (JA) and gibberellic acid (GA3) mitigated Cd-toxicity in chickpea plants through restricted cd uptake and oxidative stress management. Scientific Reports, 11(1), 19768. https://doi.org/10.1038/s41598-021-98753-8
• Alamzeb, M., Iqbal, A., Inamullah, Iqbal, M., & Ullah, I. (2024). Integrated use of phosphorus sources, phosphate solubilizing bacteria, and rhizobium enhanced growth, nitrogen, and phosphorus uptake in chickpea. Journal of Plant Nutrition, 47(17), 2913-2929. https://doi.org/10.1080/01904167.2024.2369086
• Ali, M., Afzal, S., Parveen, A., Kamran, M., Javed, M. R., Abbasi, G. H., ... & Ali, S. (2021). Silicon mediated improvement in the growth and ion homeostasis by decreasing Na+ uptake in maize (Zea mays L.) cultivars exposed to salinity stress. Plant Physiology and Biochemistry, 158, 208-218. https://doi.org/10.1016/j.plaphy.2020.10.040
• Alikhani, O., Abbaspour, H. (2019) Effects of methyl jasmonate and cadmium on growth traits, cadmium transport, accumulation and allene-oxide cyclase gene expression in wheat seedlings. J Neotrop Agric 6:20–29. https://doi.org/10.32404/rean.v6i3.3322
• Al-Sereiti, M. R., Abu-Amer, K. M., & Sen, P. (1999). Pharmacology of rosemary (Rosmarinus officinalis Linn.) and its therapeutic potentials. Indian journal of experimental biology, 37(2), 124-130.
• Andresen, E., Kappel, S., Stärk, H. J., Riegger, U., Borovec, J., Mattusch, J., ... & Küpper, H. (2016). Cadmium toxicity investigated at the physiological and biophysical levels under environmentally relevant conditions using the aquatic model plant Ceratophyllum demersum. New Phytologist, 210(4), 1244-1258. https://doi: 10.1111/nph.13840
• Begum, A., Sandhya, S., Vinod, K. R., Reddy, S., & Banji, D. (2013). An in-depth review on the medicinal flora Rosmarinus officinalis (Lamiaceae). Acta scientiarum polonorum Technologia alimentaria, 12(1), 61-74.
• Carrubba, A., Abbate, L., Sarno, M., Sunseri, F., Mauceri, A., Lupini, A., & Mercati, F. (2020). Characterization of Sicilian rosemary (Rosmarinus officinalis L.) germplasm through a multidisciplinary approach. Planta, 251(2), 37. https://doi.org/10.1007/s00425-019-03327-8
• Chauhan, A., Saini, R., & Sharma, J. C. (2021). Plant growth promoting rhizobacteria and their biological properties for soil enrichment and growth promotion. Journal of Plant Nutrition, 45(2), 273-299. https://doi.org/10.1080/01904167.2021.1952221
• Colebrook, E. H., Thomas, S. G., Phillips, A. L., & Hedden, P. (2014). The role of gibberellin signalling in plant responses to abiotic stress. Journal of experimental biology, 217(1), 67-75. https://doi.org/10.1242/jeb.089938
• El-Esawi, M. A., Elkelish, A., Soliman, M., Elansary, H. O., Zaid, A., & Wani, S. H. (2020). Serratia marcescens BM1 enhances cadmium stress tolerance and phytoremediation potential of soybean through modulation of osmolytes, leaf gas exchange, antioxidant machinery, and stress-responsive genes expression. Antioxidants, 9(1), 43. https://doi.org/10.3390/antiox9010043
• Falkowska, M., Pietryczuk, A., Piotrowska, A., Bajguz, A., Grygoruk, A., & Czerpak, R. (2011). The effect of gibberellic acid (GA3) on growth, metal biosorption and metabolism of the green algae Chlorella vulgaris (Chlorophyceae) Beijerinck exposed to cadmium and lead stress. Pol J Environ Stud, 20(1), 53-9.
• Ghassemi-Golezani, K., & Farhangi-Abriz, S. (2018). Foliar sprays of salicylic acid and jasmonic acid stimulate H+-ATPase activity of tonoplast, nutrient uptake and salt tolerance of soybean. Ecotoxicology and environmental safety, 166, 18-25. https://doi.org/10.1016/j.ecoenv.2018.09.059
• Glick, B. R. (2014). Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiological research, 169(1), 30-39. https://doi.org/10.1016/j.micres.2013.09.009
• Goswami, M., Deka, S. (2020). Plant growth-promoting rhizobacteria—alleviators of abiotic stresses in soil: a review. Pedosphere 30(1):40-61. https://doi.org/10.1016/S1002-0160(19)60839-8
• Gupta, R., Anshu Noureldeen, A., & Darwish, H. (2021). Rhizosphere mediated growth enhancement using phosphate solubilizing rhizobacteria and their tri-calcium phosphate solubilization activity under pot culture assays in Rice (Oryza sativa.). Saudi J Biol Sci 28: 3692–3700. https://doi.org/10.1016/j.sjbs.2021.05.052
• Hadi, F., Ali, N. A., Ahmad, N. (2014). Enhanced phytoremediation of cadmium-contaminated soil by Parthenium hysterophorus plant: effect of gibberellic acid (GA3) and synthetic chelator, alone and in combinations. Bioremediation J 18(1):46. https://doi.org/10.1080/10889868.2013.834871
• Hasan, S., Sehar, Z., Khan, N. A. (2020). Gibberellic acid and sulfur-mediated reversal of cadmium-inhibited photosynthetic performance in mungbean (Vigna radiata L.) involves nitric oxide. J Plant Growth Regul 39:1605–1615. https://doi.org/10.1007/s00344-020-10175-4
• Heath, R. L., Packer, L. (1968). Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189-198. https://doi.org/10.1016/0003-9861(68)90654-1
• Huang, S., Song, Q., Li, Q., Zhang, H., Luo, X., & Zheng, Z. (2020). Damage of heavy metals to Vallisneria natans (V. natans) and characterization of microbial community in biofilm. Aquatic Toxicology, 225, 105515. https://doi.org/10.1016/j.aquatox.2020.105515
• Jain, A., Singh, A., Singh, S., Singh, H. B. (2015). Biological management of Sclerotinia sclerotiorum in pea using plant growth-promoting microbial consortium. J Basic Microbiol 55(8):961-972. https://doi.org/10.1002/jobm.201400628
• Jancikova, S., Jamróz, E., Kulawik, P., Tkaczewska, J., & Dordevic, D. (2019). Furcellaran/gelatin hydrolysate/rosemary extract composite films as active and intelligent packaging materials. International Journal of Biological Macromolecules, 131, 19-28. https://doi.org/10.1016/j.ijbiomac.2019.03.050
• Jeong, H., Choi, J. Y., Lee, J., Lim, J., & Ra, K. (2020). Heavy metal pollution by road-deposited sediments and its contribution to total suspended solids in rainfall runoff from intensive industrial areas. Environmental Pollution, 265, 115028. https://doi.org/10.1016/j.envpol.2020.115028
• Jian, L., Bai, X., Zhang, H., Song, X., & Li, Z. (2019). Promotion of growth and metal accumulation of alfalfa by coinoculation with Sinorhizobium and Agrobacterium under copper and zinc stress. PeerJ, 7, e6875. http://doi.org/10.7717/peerj.6875
• Jung, H. I., Lee, B. R., Chae, M. J., Lee, E. J., Lee, T. G., Jung, G. B., ... & Lee, J. (2020). Ascorbate-mediated modulation of cadmium stress responses: reactive oxygen species and redox status in Brassica napus. Frontiers in Plant Science, 11, 586547. https://doi.org/10.3389/fpls.2020.586547
• Khan, M. N., Khan, Z., Luo, T., Liu, J., Rizwan, M., Zhang, J., ... & Hu, L. (2020). Seed priming with gibberellic acid and melatonin in rapeseed: Consequences for improving yield and seed quality under drought and non-stress conditions. Industrial Crops and Products, 156, 112850. https://doi.org/10.1016/j.indcrop.2020.112850
• Khanna, K., Jamwal, V. L., Sharma, A., Gandhi, S. G., Ohri, P., Bhardwaj, R., ... & Ahmad, P. (2019). Supplementation with plant growth promoting rhizobacteria (PGPR) alleviates cadmium toxicity in Solanum lycopersicum by modulating the expression of secondary metabolites. Chemosphere, 230, 628-639. https://doi.org/10.1016/j.chemosphere.2019.05.072
• Lichtenthaler, H. K. (1987). Chlorophyll fluorescence signatures of leaves during the autumnal chlorophyll breakdown. J Plant Physiol 131:101-110. https://doi.org/10.1016/S0176-1617(87)80271-7
• Lutz, M., Jorquera, K., Cancino, B., Ruby, R., & Henriquez, C. (2011). Phenolics and antioxidant capacity of table grape (Vitis vinifera L.) cultivars grown in Chile. Journal of food science, 76(7), 1088-1093. https://doi.org/10.1111/j.1750-3841.2011.02298.x
• Malik, L., Sanaullah, M., Mahmood, F., Hussain, S., Siddique, M. H., Anwar, F., & Shahzad, T. (2022). Unlocking the potential of co-applied biochar and plant growth-promoting rhizobacteria (PGPR) for sustainable agriculture under stress conditions. Chemical and biological technologies in agriculture, 9(1), 58. https://doi.org/10.1186/s40538-022-00327-x
• Moss, M., Smith, E., Milner, M., McCready, J. (2018). Acute ingestion of rosemary water: evidence of cognitive and cerebrovascular effects in healthy adults. J Psychopharmacol 32(12):1319–1329 https://doi.org/10.1177/0269881118798339.
• Nieto, G., Ros, G., Castillo, J. (2018). Antioxidant and antimicrobial properties of rosemary (Rosmarinus officinalis, L.): A review. Medicines 5(3):98. https://doi.org/10.3390/medicines5030098
• Obanda, M., Owuor, P. O., Taylor, S. J. (1997). Flavanol composition and caffeine content of green leaf as quality potential indicators of Kenyan black teas. J Sci Food Agric 74:209-215. https://doi.org/10.1002/(SICI)1097-0010(199706)74:2%3C209::AID-JSFA789%3E3.0.CO;2-4
• Paithankar, J. G., Saini, S., Dwivedi, S., Sharma, A., & Chowdhuri, D. K. (2021). Heavy metal associated health hazards: An interplay of oxidative stress and signal transduction. Chemosphere, 262, 128350. https://doi.org/10.1016/j.chemosphere.2020.128350
• Parveen, A., Saleem, M. H., Kamran, M., Haider, M. Z., Chen, J. T., Malik, Z., ... & Azeem, M. (2020). Effect of citric acid on growth, ecophysiology, chloroplast ultrastructure, and phytoremediation potential of jute (Corchorus capsularis L.) seedlings exposed to copper stress. Biomolecules, 10(4), 592. https://doi.org/10.3390/biom10040592
• Quettier-Deleu, C., Gressier, B., Vasseur, J., Dine, T., Brunet, C., Luyckx, M., ... & Trotin, F. (2000). Phenolic compounds and antioxidant activities of buckwheat (Fagopyrum esculentum Moench) hulls and flour. Journal of ethnopharmacology, 72(1-2), 35-42. https://doi.org/10.1016/S0378-8741(00)00196-3
• Saijo, Y., Loo, P. (2020). Plant immunity in signal integration between biotic and abiotic stress responses. New Phytol 225:87–104. https://doi.org/10.1111/nph.15989
• Sairam, R., Saxena, D. (2000). Oxidative stress and antioxidants in wheat genotypes: possible mechanism of water stress tolerance. J Agron Crop Sci 184:55-61. https://doi.org/10.1046/j.1439-037x.2000.00358.x
• Shahid, M., Dumat, C., Khalid, S., Niazi, N. K., & Antunes, P. M. (2016). Cadmium bioavailability, uptake, toxicity and detoxification in soil-plant system. Reviews of environmental contamination and toxicology volume 241, 73-137. https://doi.org/10.1007/398_2016_8
• Shakya, P., Marslin, G., Siram, K., Beerhues, L., & Franklin, G. (2019). Elicitation as a tool to improve the profiles of high-value secondary metabolites and pharmacological properties of Hypericum perforatum. Journal of Pharmacy and Pharmacology, 71(1), 70-82. https://doi.org/10.1111/jphp.12743
• Sharma, R. K., Archana, G. (2016). Cadmium minimization in food crops by cadmium-resistant plant growth-promoting rhizobacteria. Appl Soil Ecol 107:66–78. https://doi.org/10.1016/j.apsoil.2016.05.009
• Tai, J., Cheung, S., Wu, M., Hasman, D. (2012). Antiproliferation effect of rosemary (Rosmarinus officinalis) on human ovarian cancer cells in vitro. Phytomedicine 19(5):436–443. https://doi.org/10.1016/j.phymed.2011.12.012
• Yaseen, S., Amjad, S. F., Mansoora, N., Kausar, S., Shahid, H., Alamri, S. A., ... & Datta, R. (2021). Supplemental effects of biochar and foliar application of ascorbic acid on physio-biochemical attributes of barley (Hordeum vulgare L.) under cadmium-contaminated soil. Sustainability, 13(16), 9128. https://doi.org/10.3390/su13169128
• Yu, M. H., Choi, J. H., Chae, I. G., Im, H. G., Yang, S. A., More, K., ... & Lee, J. (2013). Suppression of LPS-induced inflammatory activities by Rosmarinus officinalis L. Food Chemistry, 136(2), 1047-1054. https://doi.org/10.1016/j.foodchem.2012.08.085
• Zaid, A., Mohammad, F., Fariduddin, Q. (2020). Plant growth regulators improve growth, photosynthesis, mineral nutrient and antioxidant system under cadmium stress in menthol mint (Mentha arvensis L.). Physiol Mol Biol Plants 26:25–39. https://doi.org/10.1007/s12298-019-00715-y
• Zhang, K., Wang, G., Bao, M., Wang, L., & Xie, X. (2019). Exogenous application of ascorbic acid mitigates cadmium toxicity and uptake in Maize (Zea mays L.). Environmental Science and Pollution Research, 26(19), 19261-19271. https://doi.org/10.1007/s11356-019-05265-0
• Zhu, J., Wu, F., Yue, S., Chen, C., Song, S., Wang, H., & Zhao, M. (2019). Functions of reactive oxygen species in apoptosis and ganoderic acid biosynthesis in Ganoderma lucidum. FEMS Microbiology Letters, 366(23), fnaa015. https://doi.org/10.1093/femsle/fnaa015