OPTIMIZING SUNFLOWER YIELD IN LEAD CONTAMINATED SOIL VIA PGPR INDUCED ANTIOXIDANT DEFENSE MECHANISM
Main Article Content
Keywords
Sunflower, PGPR Inoculation, Lead Stress, Antioxidants, ROS, Yield
Abstract
Lead (Pb) is a toxic heavy metal that can have detrimental effects on plant growth and development. Sunflowers are effective in bioremediation, utilizing their extensive root systems to absorb and remove heavy metals and other contaminants from soil and water. PGPR (plant growth promoting rhizobacteria) can enhance plant growth and reduce heavy metal accumulation by sequestering metals in the rhizosphere, thus minimizing their uptake by plants. The present study aims to investigate the efficacy of PGPR in mitigating lead (Pb) stress in sunflowers for which a pot experiment was conducted. The trial was performed according to factorial CRD (Completely Randomized Design) with four replications. Four treatments were used in this trial, L1P1(No Lead + No PGPR), L1P2 (No Lead + PGPR), L2P1 (Lead stress + No PGPR) and L2P2 (Lead stress + PGPR). Half seeds of five sunflower cultivars, FH-825, FH-721, Agsun5270, HSF-350 and T-40318 were inoculated with PGPR and sown in plastic pots containing nutrient rich loam. Lead stress @ 200ppm was applied 37 days after seed sowing. Plants were sampled 21 days after application of lead stress. Seed treatment with PGPR significantly enhanced dry weight of shoot and root, total achene weight per plant and 100 achene weight. Additionally, it increased catalase, SOD, peroxidase activities, total soluble proteins, total phenolic content, ascorbic acid levels. This enhancement suggests that PGPR-treated sunflowers were better equipped to handle oxidative stress induced by Pb compared to non-treated plants. Additionally, PGPR application significantly reduced lipid peroxidation levels, as shown by lower malondialdehyde content in PGPR treated plants under Pb contaminated soil. Among the sunflower varieties tested, T-40318 exhibited robust performance and showed increased tolerance to Pb stress. In contrast, Agsun-5270 cultivar was extremely sensitivity to Pb stress but performed best upon PGPR application compared to all other sunflower cultivars. Therefore, it can be concluded that sunflower cultivars sensitive to Pb stress can even perform better by improving morpho-biochemical attributes, especially antioxidant defence mechanism upon application of PGPR and help in mitigating Pb stress. Hence there is a dire need for incorporation of sustainable strategies, like inoculation of crops seeds with PGPR to improve crop resilience and food security in metal contaminated soils and different agro-climatic conditions.
References
1. Ahemad, M., & Kibret, M. (2014). Mechanisms and applications of plant growth-promoting rhizobacteria: Current perspective. Journal of King Saud University-Science, 26(1), 1–20.
2. Ahmed, M., Imran, A., Naveed, M., Khan, A., & Yousaf, S. (2021). Plant growth-promoting rhizobacteria (PGPR) improve growth and yield of cotton under drought stress. Journal of Plant Growth Regulation, 40(2), 559-568.
3. Akram, M., Jamil, M., Shah, S. M., & Zahid, H. (2022). PGPR-mediated antioxidant defense in sunflower under lead stress: A review. Journal of Plant Physiology, 272, 110442.
4. Alkio, M., & Grimm, E. (2013). Vascular connections between the receptacle and empty achenes in sunflower (Helianthus annuus L.). Journal of Experimental Botany, 54(381), 345–348.
5. Ali, B., Wang, X., Saleem, M.H., Sumaira, Hafeez, A., Afridi, M.S., Khan, S., Ullah, I., Amaral Júnior, A.T.D., Alatawi, A. and Ali, S. (2022). PGPR-mediated salt tolerance in maize by modulating plant physiology, antioxidant defense, compatible solutes accumulation and bio-surfactant producing genes. Plants, 11(3),345.
6. Alshaal, T., Alharbi, K., Naif, E., Rashwan, E., Omara, A. E. D., & Hafez, E. M. (2024). Strengthen sunflowers' resilience to cadmium in saline-alkali soil by PGPR-augmented biochar. Ecotoxicology and Environmental Safety, 280, 116555.
7. Al-Turki, A., Murali, M., Omar, A. F., Rehan, M., & Sayyed, R. Z. (2023). Recent advances in PGPR-mediated resilience toward interactive effects of drought and salt stress in plants. Frontiers in Microbiology, 14, 1214845.
8. Ayub, A., Shabaan, M., Malik, M., Asghar, H. N., Zulfiqar, U., Ejaz, M., Alarjani, K. M., & Al Farraj, D. A. (2024). Synergistic application of Pseudomonas strains and compost mitigates lead (Pb) stress in sunflower (Helianthus annuus L.) via improved nutrient uptake, antioxidant defense, and physiology. Ecotoxicology and Environmental Safety, 274, 116194.
9. Azeem, M. A., Shah, F. H., Ullah, A., Ali, K., Jones, D. A., Khan, M. E. H., & Ashraf, A. (2022). Biochemical characterization of halotolerant Bacillus safensis PM22 and its potential to enhance growth of maize under salinity stress. Plants, 11, 1721-1735.
10. Bacher, H., Sharaby, Y., Walia, H., & Peleg, Z. (2022). Modifying root-to-shoot ratio improves root water influxes in wheat under drought stress. Journal of Experimental Botany, 73(5), 1643-1654.
11. Bakhoum, N., Hamed, A. M., & Hafez, M. M. (2020). Lead stress affects capitulum diameter and achene yield in chickpea. Journal of Environmental Science & Health, B, 55, 39–47.
12. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2), 248-254.
13. Carmak, I., & Horst, W. J. (1991). Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiologia Plantarum, 83(3), 463-468.
14. Chance, B., & Maehly, A. C. (1955). Assay of catalases and peroxidases. Methods in Enzymology, 136, 764–775.
15. Chandwani, S., Kayasth, R., Naik, H., & Amaresan, N. (2023). Current status and future prospect of managing lead (Pb) stress through microbes for sustainable agriculture. Environmental Monitoring and Assessment, 195(4), 479.
16. Chang, W., Hou, X., Yan, Y., Liu, T., Dai, X., Igarashi, Y., Fan, L., Yang, C., & Luo, F. (2024). Plant growth-promoting and arsenic accumulation reduction effects of two endophytic bacteria isolated from Brassica napus. Journal of Plant Growth Regulation, 43(1), 76-88.
17. Chaturvedi, S., Khan, S., Bhunia, R. K., Kaur, K., & Tiwari, S. (2022). Metabolic engineering in food crops to enhance ascorbic acid production: Crop biofortification perspectives for human health. Physiologia Plantarum, 28, 871-884.
18. Cheema, A., & Garg, N. (2023). Arbuscular mycorrhizae reduced arsenic-induced oxidative stress by coordinating nutrient uptake and proline-glutathione levels in Cicer arietinum L. (chickpea). Ecotoxicology, 33(2), 205-225.
19. Chen, Y., Liu, S., Wang, L., Zhang, H., Li, Q., & Wang, S. (2021). Molecular mechanisms of lead stress in sunflowers: A review. Journal of Hazardous Materials, 443, 126964.
20. Cid, C. V., Pignata, M. L., & Rodriguez, J. H. (2020). Effects of co-cropping on soybean growth and stress response in lead-polluted soils. Chemosphere, 246, 125833.
21. Cui, K., Xu, T., Chen, J., Yang, H., Liu, X., Zhuo, R., Peng, Y., Tang, W., Wang, R., Chen, L., & Zhang, X. (2022). Siderophores, a potential phosphate solubilizer from the endophyte Streptomyces sp. CoT10, improved phosphorus mobilization for host plant growth and rhizosphere modulation. Journal of Cleaner Production, 367, 133110.
22. Dalyan, E., Yüzbaşıoğlu, E., & Akpınar, I. (2020). Physiological and biochemical changes in plant growth and different plant enzymes in response to lead stress. In Lead in Plants and the Environment (pp. 129-147).
23. Danish, S., Sarkar, S., Khatun, M., Era, F. M., Islam, A. M., Anwar, M. P., Datta, R., & Islam, A. A. (2021). Abiotic stresses: Alteration of composition and grain quality in food legumes. Agronomy, 11(11), 2238.
24. Dwivedi, A., Singh, A. N., Kumar, A., Nath, G., & Sharma, R. K. (2024). Cadmium content, metabolite profile, and biological properties of Eclipta alba (L.) Hassk plant exposed to elevated cadmium in soil. Environmental and Experimental Botany, 105865.
25. Fu, J., Li, L., Wang, S., Yu, N., Shan, H., Shi, Z., ... & Zhong, X. (2023). Effect of gibberellic acid on photosynthesis and oxidative stress response in maize under weak light conditions. Frontiers in Plant Science, 14, 1128780.
26. Giannopolitis, C. N., & Ries, S. K. (1977). Superoxide dismutases: II. Purification and quantitative relationship with water-soluble
27. Gowtham, H. G., Singh, B., Murali, M., Shilpa, N., Prasad, M., Aiyaz, M., Amruthesh, K. N., & Niranjana, S. R. (2020). Induction of drought tolerance in tomato upon the application of ACC deaminase producing plant growth-promoting rhizobacterium Bacillus subtilis Rhizo SF 48. Microbiological Research, 234, 126422.
28. Gupta, A., Singh, R., Sharma, P., & Kumar, V. (2022). PGPR-mediated enhancement of antioxidant enzyme activities in maize under heavy metal stress. Journal of Microbiology and Biotechnology, 32(1), 14-21.
29. Gupta, S., Rangari, S. K., Sahu, A., Naik, Y. D., Satayavathi, C. T., Punnuri, S., & Thudi, M. (2024). Meta-QTL analysis reveals the important genomic regions for biotic stresses, nutritional quality, and yield-related traits in pearl millet. CABI Agriculture and Bioscience, 5(1), 36.
30. Hasanuzzaman, M., Alam, M. M., Naz, F., Rummana, S., Siddika, A., Sultana, A., Sinthi, F., & Prasad, P. V. (2024). Modulating reactive oxygen species and ion homeostasis for combined salt and cadmium stress tolerance in Brassica campestris: The role of beneficial microbes. Plant Stress, 14, 100605.
31. Hatami, M., Mohammadi, H., Hazrati, S. (2023). Effects of plant growth regulators on physiological and phytochemical parameters in medicinal plants under stress conditions. In Plant Stress Mitigators (pp. 159-167). Academic Press.
32. Hossain, M. S., Abdelrahman, M., Tran, C. D., Nguyen, K. H., Chu, H. D., Watanabe, Y., Fujita, M., & Tran, L. S. P. (2022). Modulation of osmoprotection and antioxidant defense by exogenously applied acetate enhances cadmium stress tolerance in lentil seedlings. Environmental Pollution, 308, 119687.
33. Hussain, M., Arif, M. S., & Ahmad, M. (2022). Drought tolerance in sorghum: Physiological and molecular mechanisms. Journal of Plant Physiology, 227, 133–144.
34. Hussain, M., Kaousar, R., Ali, S., Shan, C., Wang, G., Wang, S., & Lan, Y. (2024). Tryptophan seed treatment improves morphological, biochemical, and photosynthetic attributes of sunflower under cadmium stress. Plants, 13(2), 237.
35. Julkenen-Titto, R. (1985). Phenolic constituents in the leaves of northern willows: Methods for the analysis of certain phenolics. Agricultural and Food Chemistry, 33, 213-217.
36. Khalid, S., Imran, A., Naveed, M., & Yousaf, S. (2020). PGPR-induced increase in capitulum diameter and achene yield in sunflower cultivars. Journal of Microbiology & Biotechnology, 30(1), 14–25.
37. Khan, A., Ahmed, M., Imran, A., Naveed, M., & Yousaf, S. (2021). Plant growth-promoting rhizobacteria (PGPR) improve growth and yield of cotton under drought stress. Journal of Plant Growth Regulation, 40(2), 559-568.
38. Khan, N., Bano, A. M., & Babar, A. (2020). Impacts of plant growth promoters and plant growth regulators on rainfed agriculture. PLoS ONE, 18, 234-249.
39. Khan, V., Umar, S., & Iqbal, N. (2023). Palliating salt stress in mustard through plant growth-promoting rhizobacteria: Regulation of secondary metabolites, osmolytes, antioxidative enzymes, and stress ethylene. Plants, 12(4), 705.
40. Khatun, M., Sarkar, S., Era, F. M., Islam, A. K. M. M., Anwar, M. P., Fahad, S., Datta, R., & Islam, A. K. M. A. (2021). Drought stress in grain legumes: Effects, tolerance mechanisms and management. Agronomy, 11(11), 2374.
41. Kou, X., Han, W., & Kang, J. (2022). Responses of root system architecture to water stress at multiple levels: A meta-analysis of trials under controlled conditions. Frontiers in Plant Science, 13, 1085409.
42. Kour, D., Khan, S. S., Kour, H., Kaur, T., Devi, R., Rai, A. K., & Yadav, A. N. (2024). ACC deaminase producing phytomicrobiomes for amelioration of abiotic stresses in plants for agricultural sustainability. Journal of Plant Growth Regulation, 43(4), 963–985.
43. Kumar, R., Pandey, S., & Sharma, V. (2020). PGPR-mediated mitigation of heavy metal stress in wheat. Journal of Environmental Science and Health, Part B, 55, 19-28.
44. Kunsah, B., Kartikorini, N., Ariana, D., & Mardiyah, S. (2024). Potential bioabsorbent extract of skin and leaves of Ananas comosus on reduction of copper, mercury, and lead in Anadara granosa. Research Journal of Pharmacy and Technology, 17(3), 1190-1195.
45. Lalarukh, I., & Shahbaz, M. (2020). Alpha-tocopherol induced modulations in morpho-physiological attributes of sunflower (Helianthus annuus) grown under saline environment. International Journal of Agriculture and Biology, 20(3), 661-668.
46. Lalarukh, I., Al-Dhumri, S. A., Al-Ani, L. K. T., Hussain, R., Al Mutairi, K. A., Mansoora, N., & Galal, T. M. (2022). A combined use of rhizobacteria and moringa leaf extract mitigates the adverse effects of drought stress in wheat (Triticum aestivum L.). Frontiers in Microbiology, 13, 813415.
47. Lalay, G., Ullah, A., Iqbal, N., Raza, A., Asghar, M. A., & Ullah, S. (2024). The alleviation of drought-induced damage to growth and physio-biochemical parameters of Brassica napus L. genotypes using an integrated approach of biochar amendment and PGPR application. Environment, Development and Sustainability, 26(2), 3457-3480.
48. Liang, L. M. H., Zhu, J., & Jiang, J. G. (2019). Carotenoids biosynthesis and cleavage related genes from bacteria to plants. Critical Reviews in Food Science and Nutrition, 13, 1-20.
49. Liu, T., Chang, W., Hou, X., Yan, Y., Dai, X., Igarashi, Y., Fan, L., Yang, C., & Luo, F. (2024). Plant growth-promoting and arsenic accumulation reduction effects of two endophytic bacteria isolated from Brassica napus. Journal of Plant Growth Regulation, 43(1), 76–88.
50. Magray, J. A., Sharma, D. P., Deva, M. A., & Thoker, S. A. (2023). Phenolics: Accumulation and role in plants grown under heavy metal stress. In Plant Phenolics in Abiotic Stress Management (pp. 321–351).
51. Maqsood, M., Ahmad, M., Khan, A. S., & Ali, S. (2021). PGPR-mediated mitigation of heavy metal stress in plants. Journal of Microbiology & Biotechnology, 31(1), 14-25.
52. Martinez, V., Santos, M., Rivera, S., & Gomez, M. (2022). Bioactive compounds in sunflowers: A review of their health benefits and applications. Foods, 11(11), 1629.
53. Mhlongo, M. I., Piater, L. A., Steenkamp, P. A., Labuschagne, N., & Dubery, I. A. (2020). Metabolic profiling of PGPR-treated tomato plants reveals priming-related adaptations of secondary metabolites and aromatic amino acids. Metabolites, 10(5), 210.
54. Mondal, S., Pramanik, K., Ghosh, S. K., Pal, P., Ghosh, P. K., Ghosh, A., & Maiti, T. K. (2022). Molecular insight into arsenic uptake, transport, phytotoxicity, and defense responses in plants: A critical review. Planta, 255(4), 87.
55. Mosupiemang, M. (2024). Safflower growth, development, yield, and oil content as influenced by genotype and environment interaction under on-farm conditions (Doctoral dissertation, Botswana University of Agriculture & Natural Resources).
56. Mukherjee, S. P., & Choudhari, M. A. (1983). Implications of water stress-induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiologia Plantarum, 58, 116–170.
57. Pandey, A., Khan, M. K., Hamurcu, M., Athar, T., Yerlikaya, B. A., Yerlikaya, S., Kavas, M., Rustagi, A., Zargar, S. M., Sofi, P. A., & Chaudhry, B. (2023). Role of exogenous nitric oxide in protecting plants against abiotic stresses. Agronomy, 13(5), 1201.
58. Pattnaik, S., Mohapatra, B., & Gupta, A. (2021). Plant growth-promoting microbe mediated uptake of essential nutrients (Fe, P, K) for crop stress management: Microbe–soil–plant continuum. Frontiers in Agronomy, 3, 689972.
59. Qadir, M., Hussain, A., Shah, M., Hamayun, M., Iqbal, A., Irshad, M., Ahmad, A., Alrefaei, A. F., & Ali, S. (2024). Staphylococcus arlettae mediated defense mechanisms and metabolite modulation against arsenic stress in Helianthus annuus. Frontiers in Plant Science, 15, 1391348.
60. Rajendran, A., Lal, S. K., Raju, D., & Ramlal, A. (2022). Associations of direct and indirect selection for pregermination anaerobic stress tolerance in soybean (Glycine max). Plant Breeding, 141(5), 634-643.
61. Rajput, L., Imran, A., Mubeen, F., & Hafeez, F. Y. (2018). Wheat (Triticum aestivum L.) growth promotion by halo-tolerant PGPR-consortium. International Journal of Environmental Science and Technology, 15(12), 2581–2588.
62. Rajput, V. D., Harish, R. K., Singh, K. K., Verma, L., Sharma, F. R., Quiroz-Figueroa, M., Meena, V. S., Gour, T., Minkina, T., Sushkova, S., & Mandzhieva, S. (2021). Recent developments in enzymatic antioxidant defence mechanism in plants with special reference to abiotic stress. Biology, 10, 258-267.
63. Ramesh, M., Bindu, C. F., Mohanthi, S., Hema, T., Poopal, R.-K., Ren, Z., & Li, B. (2023). Efficiency of hematological, enzymological, and oxidative stress biomarkers of Cyprinus carpio to an emerging organic compound (alphamethrin) toxicity. Environmental Toxicology and Pharmacology, 101, 104186.
64. Rani, M., Vikas, Kumar, R., Lathwal, M., & Kamboj, A. (2024). Effect and responses of lead toxicity in plants. In Lead Toxicity Mitigation: Sustainable Nexus Approaches (pp. 211-241). Cham: Springer Nature Switzerland.
65. Rehan, A. I., Rasee, A. I., Awual, M. E., Waliullah, R. M., Hossain, M. S., Kubra, K. T., & Awual, M. R. (2023). Improving toxic dye removal and remediation using novel nanocomposite fibrous adsorbent. Colloids and Surfaces A: Physicochemical and Engineering Aspects, 131859.
66. Roychoudhury, A., & Tripathi, D. K. (Eds.). (2020). Protective chemical agents in the amelioration of plant abiotic stress: Biochemical and molecular perspectives. John Wiley & Sons.
67. Sagar, N., Sadekov, A., Jenner, T., Chapuis, L., Scott, P., Choudhary, M., & McCulloch, M. (2022). Heavy metal incorporation in foraminiferal calcite under variable environmental and acute level seawater pollution: Multi-element culture experiments for Amphisorus hemprichii. Environmental Science and Pollution Research, 29(3), 3826–3839.
68. Sahoo, R., Sow, S., Ranjan, S., Dharminder, Kumar, R., Roy, D. K., Kumar, S., Kumar, A., Srivastava, R. K., Prasad, R., & Padhan, S. R. (2024). Unveiling the potential of plant growth-promoting rhizobacteria (PGPR) in phytoremediation of heavy metals. Discover Applied Sciences, 6(6), 324.
69. Salam, U., Ullah, S., Tang, Z.H., Elateeq, A.A., Khan, Y., Khan, J., Khan, A. and Ali, S. (2023). Plant metabolomics: An overview of the role of primary and secondary metabolites against different environmental stress factors. Life, 13(3), p.706.
70. Santos, M., Martinez, V., Gomez, M., & Rivera, S. (2023). Sunflower production and trade: A global overview. Agricultural Economics, 54(1), 123-134.
71. Sarkar, S., Khatun, M., Era, F. M., Islam, A. M., Anwar, M. P., Danish, S., Datta, R., & Islam, A. A. (2021). Abiotic stresses: Alteration of composition and grain quality in food legumes. Agronomy, 11(11), 2238.
72. Shaheen, S., Lalarukh, I., Ahmad, J., Kausar, A., & Nazli, Z. H. (2024). Evaluation of potentially high yielding modern wheat cultivars for drought tolerance using key physio-biochemical and morphological indicators. Pakistan Journal of Botany, 56, 839-852.
73. Sharma, A., Singh, R., Kumar, V., & Verma, P. (2020). Heavy metal stress and its impact on plant growth and development. Journal of Environmental Science and Health, Part B, 54, 39-50.
74. Sharma, K., Sharma, S., Vaishnav, A., Jain, R., Singh, D., Singh, H. B., Goel, A., & Singh, S. (2022). Salt-tolerant PGPR strain Priestia endophytica SK1 promotes fenugreek growth under salt stress by inducing nitrogen assimilation and secondary metabolites. Journal of Applied Microbiology, 133(5), 2802-2813.
75. Sharma, V., Singh, C.M., Chugh, V., Prajapati, P.K., Mishra, A., Kaushik, P., Dhanda, P.S. & Yadav, A. (2023). Morpho-physiological and biochemical responses of field pea genotypes under terminal heat stress. Plants, 12(2), 256.
76. Shehzad, J., Mustafa, G., Arshad, H., Ali, A., Naveed, N. H., Riaz, Z., & Khan, I. (2023). Morpho-physiological and biochemical responses of Brassica species toward lead (Pb) stress. Acta Physiologiae Plantarum, 45(1), 8.
77. Singh, D., Prabha, R., Sharma, R., & Jain, A. (2020). Plant growth-promoting rhizobacteria (PGPR): A review on their role in plant abiotic stress tolerance. Journal of Plant Growth Regulation, 39(2), 531-544.
78. Singh, T., Bisht, N., Ansari, M. M., & Chauhan, P. S. (2023). The hidden harmony: Exploring ROS-phytohormone nexus for shaping plant root architecture in response to environmental cues. Plant Physiology and Biochemistry, 108273.
79. Singh, T., Sandhu, P. S., Chahal, G. K., & Walia, S. S. (2022). Foliar thiourea confers moisture stress tolerance in rainfed maize through elevated antioxidative defence system, osmolyte accumulation and starch synthesis grown under different planting methods. Journal of Plant Growth Regulation, 1-19.
80. Srivastava, A. K., Sharma, H., Kumari, A., Raigar, O. P., Augustine, G., Verma, V., Lakhar, C., Boparai, A. K., Aggarwal, H., Kumar, A. (2023). Strategies for improving tolerance to the combined effect of drought and salinity stress in crops. In Salinity and Drought Tolerance in Plants (pp. 137–172). Physiological Perspectives.
81. Tonelli, F. M. P., Bhat, R. A., Dar, G. H., & Hakeem, K. R. (Eds.). (2024). Nano-Phytoremediation and Environmental Pollution: Strategies and Mechanisms. CRC Press.
82. Velikova, V., Yordanov, I., & Edreva, A. (2000). Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective roles of exogenous polyamines. Plant Science, 151, 59–66.
83. Zafar, S., Khan, A. R., Qadir, M. A., & Yasmin, S. (2022). Sunflower (Helianthus annuus L.) response to lead stress: A review of the physiological and biochemical mechanisms. Journal of Environmental Science & Health, B, 57, 39-48.
84. Zahid, A., ul Din, K., Ahmad, M., Hayat, U., Zulfiqar, U., Askri, S. M. H., Anjum, M. Z., Maqsood, M. F., Aijaz, N., Chaudhary, T., & Ali, H. M. (2024). Exogenous application of sulfur-rich thiourea (STU) to alleviate the adverse effects of cobalt stress in wheat. BMC Plant Biology, 24(1), 126.
85. Zhou, W., Yang, J., Qi, L., Wang, G., Guan, C., & Li, Q. (2024). The role of Ni-and Cd-resistant rhizobacteria in promoting the growth of rice seedlings and alleviating the combined phytotoxicity of Ni and Cd. Ecotoxicology and Environmental Safety, 285, 117138.
2. Ahmed, M., Imran, A., Naveed, M., Khan, A., & Yousaf, S. (2021). Plant growth-promoting rhizobacteria (PGPR) improve growth and yield of cotton under drought stress. Journal of Plant Growth Regulation, 40(2), 559-568.
3. Akram, M., Jamil, M., Shah, S. M., & Zahid, H. (2022). PGPR-mediated antioxidant defense in sunflower under lead stress: A review. Journal of Plant Physiology, 272, 110442.
4. Alkio, M., & Grimm, E. (2013). Vascular connections between the receptacle and empty achenes in sunflower (Helianthus annuus L.). Journal of Experimental Botany, 54(381), 345–348.
5. Ali, B., Wang, X., Saleem, M.H., Sumaira, Hafeez, A., Afridi, M.S., Khan, S., Ullah, I., Amaral Júnior, A.T.D., Alatawi, A. and Ali, S. (2022). PGPR-mediated salt tolerance in maize by modulating plant physiology, antioxidant defense, compatible solutes accumulation and bio-surfactant producing genes. Plants, 11(3),345.
6. Alshaal, T., Alharbi, K., Naif, E., Rashwan, E., Omara, A. E. D., & Hafez, E. M. (2024). Strengthen sunflowers' resilience to cadmium in saline-alkali soil by PGPR-augmented biochar. Ecotoxicology and Environmental Safety, 280, 116555.
7. Al-Turki, A., Murali, M., Omar, A. F., Rehan, M., & Sayyed, R. Z. (2023). Recent advances in PGPR-mediated resilience toward interactive effects of drought and salt stress in plants. Frontiers in Microbiology, 14, 1214845.
8. Ayub, A., Shabaan, M., Malik, M., Asghar, H. N., Zulfiqar, U., Ejaz, M., Alarjani, K. M., & Al Farraj, D. A. (2024). Synergistic application of Pseudomonas strains and compost mitigates lead (Pb) stress in sunflower (Helianthus annuus L.) via improved nutrient uptake, antioxidant defense, and physiology. Ecotoxicology and Environmental Safety, 274, 116194.
9. Azeem, M. A., Shah, F. H., Ullah, A., Ali, K., Jones, D. A., Khan, M. E. H., & Ashraf, A. (2022). Biochemical characterization of halotolerant Bacillus safensis PM22 and its potential to enhance growth of maize under salinity stress. Plants, 11, 1721-1735.
10. Bacher, H., Sharaby, Y., Walia, H., & Peleg, Z. (2022). Modifying root-to-shoot ratio improves root water influxes in wheat under drought stress. Journal of Experimental Botany, 73(5), 1643-1654.
11. Bakhoum, N., Hamed, A. M., & Hafez, M. M. (2020). Lead stress affects capitulum diameter and achene yield in chickpea. Journal of Environmental Science & Health, B, 55, 39–47.
12. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2), 248-254.
13. Carmak, I., & Horst, W. J. (1991). Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiologia Plantarum, 83(3), 463-468.
14. Chance, B., & Maehly, A. C. (1955). Assay of catalases and peroxidases. Methods in Enzymology, 136, 764–775.
15. Chandwani, S., Kayasth, R., Naik, H., & Amaresan, N. (2023). Current status and future prospect of managing lead (Pb) stress through microbes for sustainable agriculture. Environmental Monitoring and Assessment, 195(4), 479.
16. Chang, W., Hou, X., Yan, Y., Liu, T., Dai, X., Igarashi, Y., Fan, L., Yang, C., & Luo, F. (2024). Plant growth-promoting and arsenic accumulation reduction effects of two endophytic bacteria isolated from Brassica napus. Journal of Plant Growth Regulation, 43(1), 76-88.
17. Chaturvedi, S., Khan, S., Bhunia, R. K., Kaur, K., & Tiwari, S. (2022). Metabolic engineering in food crops to enhance ascorbic acid production: Crop biofortification perspectives for human health. Physiologia Plantarum, 28, 871-884.
18. Cheema, A., & Garg, N. (2023). Arbuscular mycorrhizae reduced arsenic-induced oxidative stress by coordinating nutrient uptake and proline-glutathione levels in Cicer arietinum L. (chickpea). Ecotoxicology, 33(2), 205-225.
19. Chen, Y., Liu, S., Wang, L., Zhang, H., Li, Q., & Wang, S. (2021). Molecular mechanisms of lead stress in sunflowers: A review. Journal of Hazardous Materials, 443, 126964.
20. Cid, C. V., Pignata, M. L., & Rodriguez, J. H. (2020). Effects of co-cropping on soybean growth and stress response in lead-polluted soils. Chemosphere, 246, 125833.
21. Cui, K., Xu, T., Chen, J., Yang, H., Liu, X., Zhuo, R., Peng, Y., Tang, W., Wang, R., Chen, L., & Zhang, X. (2022). Siderophores, a potential phosphate solubilizer from the endophyte Streptomyces sp. CoT10, improved phosphorus mobilization for host plant growth and rhizosphere modulation. Journal of Cleaner Production, 367, 133110.
22. Dalyan, E., Yüzbaşıoğlu, E., & Akpınar, I. (2020). Physiological and biochemical changes in plant growth and different plant enzymes in response to lead stress. In Lead in Plants and the Environment (pp. 129-147).
23. Danish, S., Sarkar, S., Khatun, M., Era, F. M., Islam, A. M., Anwar, M. P., Datta, R., & Islam, A. A. (2021). Abiotic stresses: Alteration of composition and grain quality in food legumes. Agronomy, 11(11), 2238.
24. Dwivedi, A., Singh, A. N., Kumar, A., Nath, G., & Sharma, R. K. (2024). Cadmium content, metabolite profile, and biological properties of Eclipta alba (L.) Hassk plant exposed to elevated cadmium in soil. Environmental and Experimental Botany, 105865.
25. Fu, J., Li, L., Wang, S., Yu, N., Shan, H., Shi, Z., ... & Zhong, X. (2023). Effect of gibberellic acid on photosynthesis and oxidative stress response in maize under weak light conditions. Frontiers in Plant Science, 14, 1128780.
26. Giannopolitis, C. N., & Ries, S. K. (1977). Superoxide dismutases: II. Purification and quantitative relationship with water-soluble
27. Gowtham, H. G., Singh, B., Murali, M., Shilpa, N., Prasad, M., Aiyaz, M., Amruthesh, K. N., & Niranjana, S. R. (2020). Induction of drought tolerance in tomato upon the application of ACC deaminase producing plant growth-promoting rhizobacterium Bacillus subtilis Rhizo SF 48. Microbiological Research, 234, 126422.
28. Gupta, A., Singh, R., Sharma, P., & Kumar, V. (2022). PGPR-mediated enhancement of antioxidant enzyme activities in maize under heavy metal stress. Journal of Microbiology and Biotechnology, 32(1), 14-21.
29. Gupta, S., Rangari, S. K., Sahu, A., Naik, Y. D., Satayavathi, C. T., Punnuri, S., & Thudi, M. (2024). Meta-QTL analysis reveals the important genomic regions for biotic stresses, nutritional quality, and yield-related traits in pearl millet. CABI Agriculture and Bioscience, 5(1), 36.
30. Hasanuzzaman, M., Alam, M. M., Naz, F., Rummana, S., Siddika, A., Sultana, A., Sinthi, F., & Prasad, P. V. (2024). Modulating reactive oxygen species and ion homeostasis for combined salt and cadmium stress tolerance in Brassica campestris: The role of beneficial microbes. Plant Stress, 14, 100605.
31. Hatami, M., Mohammadi, H., Hazrati, S. (2023). Effects of plant growth regulators on physiological and phytochemical parameters in medicinal plants under stress conditions. In Plant Stress Mitigators (pp. 159-167). Academic Press.
32. Hossain, M. S., Abdelrahman, M., Tran, C. D., Nguyen, K. H., Chu, H. D., Watanabe, Y., Fujita, M., & Tran, L. S. P. (2022). Modulation of osmoprotection and antioxidant defense by exogenously applied acetate enhances cadmium stress tolerance in lentil seedlings. Environmental Pollution, 308, 119687.
33. Hussain, M., Arif, M. S., & Ahmad, M. (2022). Drought tolerance in sorghum: Physiological and molecular mechanisms. Journal of Plant Physiology, 227, 133–144.
34. Hussain, M., Kaousar, R., Ali, S., Shan, C., Wang, G., Wang, S., & Lan, Y. (2024). Tryptophan seed treatment improves morphological, biochemical, and photosynthetic attributes of sunflower under cadmium stress. Plants, 13(2), 237.
35. Julkenen-Titto, R. (1985). Phenolic constituents in the leaves of northern willows: Methods for the analysis of certain phenolics. Agricultural and Food Chemistry, 33, 213-217.
36. Khalid, S., Imran, A., Naveed, M., & Yousaf, S. (2020). PGPR-induced increase in capitulum diameter and achene yield in sunflower cultivars. Journal of Microbiology & Biotechnology, 30(1), 14–25.
37. Khan, A., Ahmed, M., Imran, A., Naveed, M., & Yousaf, S. (2021). Plant growth-promoting rhizobacteria (PGPR) improve growth and yield of cotton under drought stress. Journal of Plant Growth Regulation, 40(2), 559-568.
38. Khan, N., Bano, A. M., & Babar, A. (2020). Impacts of plant growth promoters and plant growth regulators on rainfed agriculture. PLoS ONE, 18, 234-249.
39. Khan, V., Umar, S., & Iqbal, N. (2023). Palliating salt stress in mustard through plant growth-promoting rhizobacteria: Regulation of secondary metabolites, osmolytes, antioxidative enzymes, and stress ethylene. Plants, 12(4), 705.
40. Khatun, M., Sarkar, S., Era, F. M., Islam, A. K. M. M., Anwar, M. P., Fahad, S., Datta, R., & Islam, A. K. M. A. (2021). Drought stress in grain legumes: Effects, tolerance mechanisms and management. Agronomy, 11(11), 2374.
41. Kou, X., Han, W., & Kang, J. (2022). Responses of root system architecture to water stress at multiple levels: A meta-analysis of trials under controlled conditions. Frontiers in Plant Science, 13, 1085409.
42. Kour, D., Khan, S. S., Kour, H., Kaur, T., Devi, R., Rai, A. K., & Yadav, A. N. (2024). ACC deaminase producing phytomicrobiomes for amelioration of abiotic stresses in plants for agricultural sustainability. Journal of Plant Growth Regulation, 43(4), 963–985.
43. Kumar, R., Pandey, S., & Sharma, V. (2020). PGPR-mediated mitigation of heavy metal stress in wheat. Journal of Environmental Science and Health, Part B, 55, 19-28.
44. Kunsah, B., Kartikorini, N., Ariana, D., & Mardiyah, S. (2024). Potential bioabsorbent extract of skin and leaves of Ananas comosus on reduction of copper, mercury, and lead in Anadara granosa. Research Journal of Pharmacy and Technology, 17(3), 1190-1195.
45. Lalarukh, I., & Shahbaz, M. (2020). Alpha-tocopherol induced modulations in morpho-physiological attributes of sunflower (Helianthus annuus) grown under saline environment. International Journal of Agriculture and Biology, 20(3), 661-668.
46. Lalarukh, I., Al-Dhumri, S. A., Al-Ani, L. K. T., Hussain, R., Al Mutairi, K. A., Mansoora, N., & Galal, T. M. (2022). A combined use of rhizobacteria and moringa leaf extract mitigates the adverse effects of drought stress in wheat (Triticum aestivum L.). Frontiers in Microbiology, 13, 813415.
47. Lalay, G., Ullah, A., Iqbal, N., Raza, A., Asghar, M. A., & Ullah, S. (2024). The alleviation of drought-induced damage to growth and physio-biochemical parameters of Brassica napus L. genotypes using an integrated approach of biochar amendment and PGPR application. Environment, Development and Sustainability, 26(2), 3457-3480.
48. Liang, L. M. H., Zhu, J., & Jiang, J. G. (2019). Carotenoids biosynthesis and cleavage related genes from bacteria to plants. Critical Reviews in Food Science and Nutrition, 13, 1-20.
49. Liu, T., Chang, W., Hou, X., Yan, Y., Dai, X., Igarashi, Y., Fan, L., Yang, C., & Luo, F. (2024). Plant growth-promoting and arsenic accumulation reduction effects of two endophytic bacteria isolated from Brassica napus. Journal of Plant Growth Regulation, 43(1), 76–88.
50. Magray, J. A., Sharma, D. P., Deva, M. A., & Thoker, S. A. (2023). Phenolics: Accumulation and role in plants grown under heavy metal stress. In Plant Phenolics in Abiotic Stress Management (pp. 321–351).
51. Maqsood, M., Ahmad, M., Khan, A. S., & Ali, S. (2021). PGPR-mediated mitigation of heavy metal stress in plants. Journal of Microbiology & Biotechnology, 31(1), 14-25.
52. Martinez, V., Santos, M., Rivera, S., & Gomez, M. (2022). Bioactive compounds in sunflowers: A review of their health benefits and applications. Foods, 11(11), 1629.
53. Mhlongo, M. I., Piater, L. A., Steenkamp, P. A., Labuschagne, N., & Dubery, I. A. (2020). Metabolic profiling of PGPR-treated tomato plants reveals priming-related adaptations of secondary metabolites and aromatic amino acids. Metabolites, 10(5), 210.
54. Mondal, S., Pramanik, K., Ghosh, S. K., Pal, P., Ghosh, P. K., Ghosh, A., & Maiti, T. K. (2022). Molecular insight into arsenic uptake, transport, phytotoxicity, and defense responses in plants: A critical review. Planta, 255(4), 87.
55. Mosupiemang, M. (2024). Safflower growth, development, yield, and oil content as influenced by genotype and environment interaction under on-farm conditions (Doctoral dissertation, Botswana University of Agriculture & Natural Resources).
56. Mukherjee, S. P., & Choudhari, M. A. (1983). Implications of water stress-induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiologia Plantarum, 58, 116–170.
57. Pandey, A., Khan, M. K., Hamurcu, M., Athar, T., Yerlikaya, B. A., Yerlikaya, S., Kavas, M., Rustagi, A., Zargar, S. M., Sofi, P. A., & Chaudhry, B. (2023). Role of exogenous nitric oxide in protecting plants against abiotic stresses. Agronomy, 13(5), 1201.
58. Pattnaik, S., Mohapatra, B., & Gupta, A. (2021). Plant growth-promoting microbe mediated uptake of essential nutrients (Fe, P, K) for crop stress management: Microbe–soil–plant continuum. Frontiers in Agronomy, 3, 689972.
59. Qadir, M., Hussain, A., Shah, M., Hamayun, M., Iqbal, A., Irshad, M., Ahmad, A., Alrefaei, A. F., & Ali, S. (2024). Staphylococcus arlettae mediated defense mechanisms and metabolite modulation against arsenic stress in Helianthus annuus. Frontiers in Plant Science, 15, 1391348.
60. Rajendran, A., Lal, S. K., Raju, D., & Ramlal, A. (2022). Associations of direct and indirect selection for pregermination anaerobic stress tolerance in soybean (Glycine max). Plant Breeding, 141(5), 634-643.
61. Rajput, L., Imran, A., Mubeen, F., & Hafeez, F. Y. (2018). Wheat (Triticum aestivum L.) growth promotion by halo-tolerant PGPR-consortium. International Journal of Environmental Science and Technology, 15(12), 2581–2588.
62. Rajput, V. D., Harish, R. K., Singh, K. K., Verma, L., Sharma, F. R., Quiroz-Figueroa, M., Meena, V. S., Gour, T., Minkina, T., Sushkova, S., & Mandzhieva, S. (2021). Recent developments in enzymatic antioxidant defence mechanism in plants with special reference to abiotic stress. Biology, 10, 258-267.
63. Ramesh, M., Bindu, C. F., Mohanthi, S., Hema, T., Poopal, R.-K., Ren, Z., & Li, B. (2023). Efficiency of hematological, enzymological, and oxidative stress biomarkers of Cyprinus carpio to an emerging organic compound (alphamethrin) toxicity. Environmental Toxicology and Pharmacology, 101, 104186.
64. Rani, M., Vikas, Kumar, R., Lathwal, M., & Kamboj, A. (2024). Effect and responses of lead toxicity in plants. In Lead Toxicity Mitigation: Sustainable Nexus Approaches (pp. 211-241). Cham: Springer Nature Switzerland.
65. Rehan, A. I., Rasee, A. I., Awual, M. E., Waliullah, R. M., Hossain, M. S., Kubra, K. T., & Awual, M. R. (2023). Improving toxic dye removal and remediation using novel nanocomposite fibrous adsorbent. Colloids and Surfaces A: Physicochemical and Engineering Aspects, 131859.
66. Roychoudhury, A., & Tripathi, D. K. (Eds.). (2020). Protective chemical agents in the amelioration of plant abiotic stress: Biochemical and molecular perspectives. John Wiley & Sons.
67. Sagar, N., Sadekov, A., Jenner, T., Chapuis, L., Scott, P., Choudhary, M., & McCulloch, M. (2022). Heavy metal incorporation in foraminiferal calcite under variable environmental and acute level seawater pollution: Multi-element culture experiments for Amphisorus hemprichii. Environmental Science and Pollution Research, 29(3), 3826–3839.
68. Sahoo, R., Sow, S., Ranjan, S., Dharminder, Kumar, R., Roy, D. K., Kumar, S., Kumar, A., Srivastava, R. K., Prasad, R., & Padhan, S. R. (2024). Unveiling the potential of plant growth-promoting rhizobacteria (PGPR) in phytoremediation of heavy metals. Discover Applied Sciences, 6(6), 324.
69. Salam, U., Ullah, S., Tang, Z.H., Elateeq, A.A., Khan, Y., Khan, J., Khan, A. and Ali, S. (2023). Plant metabolomics: An overview of the role of primary and secondary metabolites against different environmental stress factors. Life, 13(3), p.706.
70. Santos, M., Martinez, V., Gomez, M., & Rivera, S. (2023). Sunflower production and trade: A global overview. Agricultural Economics, 54(1), 123-134.
71. Sarkar, S., Khatun, M., Era, F. M., Islam, A. M., Anwar, M. P., Danish, S., Datta, R., & Islam, A. A. (2021). Abiotic stresses: Alteration of composition and grain quality in food legumes. Agronomy, 11(11), 2238.
72. Shaheen, S., Lalarukh, I., Ahmad, J., Kausar, A., & Nazli, Z. H. (2024). Evaluation of potentially high yielding modern wheat cultivars for drought tolerance using key physio-biochemical and morphological indicators. Pakistan Journal of Botany, 56, 839-852.
73. Sharma, A., Singh, R., Kumar, V., & Verma, P. (2020). Heavy metal stress and its impact on plant growth and development. Journal of Environmental Science and Health, Part B, 54, 39-50.
74. Sharma, K., Sharma, S., Vaishnav, A., Jain, R., Singh, D., Singh, H. B., Goel, A., & Singh, S. (2022). Salt-tolerant PGPR strain Priestia endophytica SK1 promotes fenugreek growth under salt stress by inducing nitrogen assimilation and secondary metabolites. Journal of Applied Microbiology, 133(5), 2802-2813.
75. Sharma, V., Singh, C.M., Chugh, V., Prajapati, P.K., Mishra, A., Kaushik, P., Dhanda, P.S. & Yadav, A. (2023). Morpho-physiological and biochemical responses of field pea genotypes under terminal heat stress. Plants, 12(2), 256.
76. Shehzad, J., Mustafa, G., Arshad, H., Ali, A., Naveed, N. H., Riaz, Z., & Khan, I. (2023). Morpho-physiological and biochemical responses of Brassica species toward lead (Pb) stress. Acta Physiologiae Plantarum, 45(1), 8.
77. Singh, D., Prabha, R., Sharma, R., & Jain, A. (2020). Plant growth-promoting rhizobacteria (PGPR): A review on their role in plant abiotic stress tolerance. Journal of Plant Growth Regulation, 39(2), 531-544.
78. Singh, T., Bisht, N., Ansari, M. M., & Chauhan, P. S. (2023). The hidden harmony: Exploring ROS-phytohormone nexus for shaping plant root architecture in response to environmental cues. Plant Physiology and Biochemistry, 108273.
79. Singh, T., Sandhu, P. S., Chahal, G. K., & Walia, S. S. (2022). Foliar thiourea confers moisture stress tolerance in rainfed maize through elevated antioxidative defence system, osmolyte accumulation and starch synthesis grown under different planting methods. Journal of Plant Growth Regulation, 1-19.
80. Srivastava, A. K., Sharma, H., Kumari, A., Raigar, O. P., Augustine, G., Verma, V., Lakhar, C., Boparai, A. K., Aggarwal, H., Kumar, A. (2023). Strategies for improving tolerance to the combined effect of drought and salinity stress in crops. In Salinity and Drought Tolerance in Plants (pp. 137–172). Physiological Perspectives.
81. Tonelli, F. M. P., Bhat, R. A., Dar, G. H., & Hakeem, K. R. (Eds.). (2024). Nano-Phytoremediation and Environmental Pollution: Strategies and Mechanisms. CRC Press.
82. Velikova, V., Yordanov, I., & Edreva, A. (2000). Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective roles of exogenous polyamines. Plant Science, 151, 59–66.
83. Zafar, S., Khan, A. R., Qadir, M. A., & Yasmin, S. (2022). Sunflower (Helianthus annuus L.) response to lead stress: A review of the physiological and biochemical mechanisms. Journal of Environmental Science & Health, B, 57, 39-48.
84. Zahid, A., ul Din, K., Ahmad, M., Hayat, U., Zulfiqar, U., Askri, S. M. H., Anjum, M. Z., Maqsood, M. F., Aijaz, N., Chaudhary, T., & Ali, H. M. (2024). Exogenous application of sulfur-rich thiourea (STU) to alleviate the adverse effects of cobalt stress in wheat. BMC Plant Biology, 24(1), 126.
85. Zhou, W., Yang, J., Qi, L., Wang, G., Guan, C., & Li, Q. (2024). The role of Ni-and Cd-resistant rhizobacteria in promoting the growth of rice seedlings and alleviating the combined phytotoxicity of Ni and Cd. Ecotoxicology and Environmental Safety, 285, 117138.
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Aug 23, 2024
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Nayab Zehra, Irfana Lalarukh, Muhammad Shahbaz, Noreen Akhter, & Farhat Jabeen. (2024). OPTIMIZING SUNFLOWER YIELD IN LEAD CONTAMINATED SOIL VIA PGPR INDUCED ANTIOXIDANT DEFENSE MECHANISM. Journal of Population Therapeutics and Clinical Pharmacology, 31(8), 3162-3178. https://doi.org/10.53555/fts5y096
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Author Biographies
Nayab Zehra
Department of Botany, Government College Women University, Faisalabad, Pakistan
Irfana Lalarukh
Department of Botany, Government College Women University, Faisalabad, Pakistan
Muhammad Shahbaz
Department of Botany, University of Agriculture, Faisalabad, 38040, Pakistan
Noreen Akhter
Department of Botany, Government College Women University, Faisalabad, Pakistan
Farhat Jabeen
Department of Chemistry, Government College Women University Faisalabad, Pakistan
How to Cite
Nayab Zehra, Irfana Lalarukh, Muhammad Shahbaz, Noreen Akhter, & Farhat Jabeen. (2024). OPTIMIZING SUNFLOWER YIELD IN LEAD CONTAMINATED SOIL VIA PGPR INDUCED ANTIOXIDANT DEFENSE MECHANISM. Journal of Population Therapeutics and Clinical Pharmacology, 31(8), 3162-3178. https://doi.org/10.53555/fts5y096