Biopriming of Pseudomonas aeruginosa Abates Fluoride Toxicity in Oryza sativa L. by Restricting Fluoride Accumulation, Enhancing Antioxidative System, and Boosting Activities of Rhizospheric Enzymes
Abstract
1. Introduction
2. Results and Discussion
2.1. Fluoride Resistance and Removal
2.2. Fluoride Biosorption Potential of P. aeruginosa
2.3. Colonization of P. aeruginosa on the Roots and F Accumulation in Plant Tissues
2.4. Plant Growth-Promoting Traits of P. aeruginosa and Its Impact on Plant Growth and Agronomic Characteristics
2.5. Soil Enzymes
2.6. Total Chlorophyll and Nutrient Contents
2.7. Oxidative Stress and Antioxidant Defense Mechanisms
3. Materials and Methods
3.1. Selection of Bacterial Strain
3.2. Fluoride Resistance and Removal Assays
3.3. Determination of F Biosorption by P. aeruginosa
3.4. Plant Growth-Promoting Activities of P. aeruginosa Under F-Stress
3.5. Model Plant and Experimental Design
3.6. Rhizosphere Colonization by P. aeruginosa
3.7. Determination of Soil Enzymes Activities
3.8. Assessment of Growth Attributes and Membrane Stability Index
3.9. Determination of Total Chlorophyll
3.10. Measurement of F Content in Plant Tissues
3.11. Determination of Agronomical Attributes
3.12. Determination of Protein, Total Sugar, Zinc, and Iron in the Grains
3.13. Generation of ROS
3.14. Fluorescence Microscopy
3.15. Lipid Peroxidation
3.16. Enzyme Extraction
3.17. Antioxidant Enzyme Assays
3.18. Gene Expression Analysis
3.19. Statistical Analysis
4. Conclusions and Future Prospectus
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Banerjee, A.; Roychoudhary, A. Melatonin application reduces fluoride uptake and toxicity in rice seedlings by altering abscisic acid, gibberellin, auxin and antioxidant homeostasis. Plant Physiol. Biochem. 2019, 145, 164–173. [Google Scholar] [CrossRef] [PubMed]
- Yadu, B.; Chandrakar, V.; Korram, J.; Satnami, M.L.; Kumar, M.; Keshavkant, S. Silver nanoparticle modulates gene expressions, glyoxalase system and oxidative stress markers in fluoride tressed Cajanus cajan L. J. Hazard. Mater. 2018, 353, 44–52. [Google Scholar] [CrossRef] [PubMed]
- Mukherjee, I.; Singh, U.K.; Patra, P.K. Exploring a multi-exposure-pathway approach to assess human health risk associated with groundwater fluoride exposure in the semi-arid region of east India. Chemosphere 2019, 233, 164–173. [Google Scholar] [CrossRef]
- Banerjee, A.; Singh, A.; Sudarshan, M.; Roychoudhary, A. Silicon nanoparticle-pulsing mitigates fluoride stress in rice by fine-tuning the ionomic and metabolomic balance and refining agronomic traits. Chemosphere 2021, 262, 127826. [Google Scholar] [CrossRef]
- Yadav, A.; Sahu, Y.K.; Rajhans, K.P.; Sahu, P.K.; Chakradhari, S.; Sahu, B.L.; Ramteke, S.; Patel, K.S. Fluoride contamination of groundwater and skeleton fluorosis in central India. J. Environ. Protec. 2016, 7, 784–792. [Google Scholar] [CrossRef]
- Rawat, N.; Bafana, A. Health risk modeling and risk factors of fluorosis in the fluoride endemic village of Maharashtra: A cross-sectional study. Environ. Monit. Assess. 2024, 196, 1230. [Google Scholar] [CrossRef]
- Yadu, B.; Chandrakar, V.; Meena, R.K.; Poddar, A.; Keshavkant, S. Spermidine and melatonin attenuate fluoride toxicity by regulating gene expression of antioxidants in Cajanus cajan L. J. Plant Growth Regul. 2018, 37, 1113–1126. [Google Scholar] [CrossRef]
- Debska, K.; Bogatek, R.; Gniazdowska, A. Protein carbonylation and its role in physiological processes in plants. Postep. Biochem. 2012, 58, 34–43. [Google Scholar]
- Che-Othman, M.H.; Millar, A.H.; Taylor, N.L. Connecting salt stress signalling pathways with salinity-induced changes in mitochondrial metabolic processes inC3 plants. Plant Cell Environ. 2017, 40, 2875–2905. [Google Scholar] [CrossRef]
- Yin, X.M.; Huang, L.F.; Zhang, X.; Wang, M.L.; Xu, G.Y.; Xia, X.J. OsCML4 improves drought tolerance through scavenging of reactive oxygen species in rice. J. Plant Biol. 2015, 58, 68–73. [Google Scholar] [CrossRef]
- Singh, A.; Banerjee, A.; Roychoudhury, A. Differential Responses of Vigna radiata and Vigna mungo to Fluoride-Induced Oxidative Stress and Amelioration via Exogenous Application of Sodium Nitroprusside. J. Plant Growth Regul. 2021, 40, 2342–2357. [Google Scholar] [CrossRef]
- Ghassemi, G.K.; Farhangi, A.S. Biochar alleviates fluoride toxicity and oxidative stress in safflower (Carthamus tinctorius L.) seedlings. Chemosphere 2019, 223, 406–415. [Google Scholar] [CrossRef] [PubMed]
- Prasad, R.; Bhattacharyya, A.; Nguyen, Q.D. Nanotechnology in Sustainable Agriculture: Recent Developments, Challenges, and Perspectives. Front. Microbiol. 2017, 8, 1014. [Google Scholar] [CrossRef]
- Katiyar, P.; Pandey, P.; Keshavkant, S. Biological approaches of fluoride remediation: Potential for environmental clean-up. Environ. Sci. Pollut. Res. 2020, 27, 13044–13055. [Google Scholar] [CrossRef]
- Jain, D.; Kour, R.; Bhojiya, A.A.; Meena, R.H.; Singh, A.; Mohanty, S.R.; Rajpurohit, D.; Ameta, K.D. Zinc tolerant plant growth promoting bacteria alleviates phytotoxic effects of zinc on maize through zinc immobilization. Sci. Rep. 2020, 10, 13865. [Google Scholar] [CrossRef]
- van Loveren, C.; Hoogenkamp, M.A.; Deng, D.M.; ten Cate, J.M. Effects of different kinds of fluorides on enolase and ATPase activity of Streptococcus mutans. Caries Res. 2008, 42, 429–434. [Google Scholar] [CrossRef]
- Mukherjee, S.; Sahu, P.; Halder, G. Microbial remediation of fluoride-contaminated water via a novel bacterium Providencia vermicola (KX926492). J. Environ. Manag. 2017, 204, 413–423. [Google Scholar] [CrossRef]
- Mukherjee, S.; Sahu, P.; Halder, G. Comparative assessment of the fluoride removal capability of immobilized and dead cells of Staphylococcus lentus (KX941098) isolated from contaminated groundwater. Environ. Prog. Sustain. Energy 2017, 37, 1573–1586. [Google Scholar] [CrossRef]
- Juwarkar, A.A.; Yadav, S.K. Bioaccumulation and biotransformation of heavymetals. In Bioremediation Technology; Fulekar, M.H., Ed.; Springer: Amsterdam, The Netherlands, 2010; pp. 266–284. [Google Scholar]
- Katiyar, P.; Pandey, N.; Keshavkant, S. Bio-prospecting fluoride tolerant bacteria for their optimistic contribution in instigating resilience against fluoride stress in Oryza sativa L. Biocatal. Agric. Biotechnol. 2024, 62, 103412. [Google Scholar] [CrossRef]
- Chouhan, S.; Tuteja, U.; Flora, S.J.S. Isolation, identification and characterization of fluoride resistant bacteria: Possible role in bioremediation. Appl. Biochem. Microbiol. 2012, 48, 43–50. [Google Scholar] [CrossRef]
- Vazquez, I.T.; Cruz, R.S.; Domínguez, M.A.; Ruan, V.L.; Reyes, A.S.; Chacon, D.P.; Garcia, R.A.B.; Mallol, J.L. FIsolation and characterization of psychrophilic and psychrotolerant plant-growth promoting microorganisms from a high-altitude volcano crater in Mexico. Microbiol Res. 2020, 232, 126394. [Google Scholar]
- Yang, Y.; Chen, Y.; Li, Z.; Zhang, Y.; Lu, L. Microbial community and soil enzyme activities driving microbial metabolic efficiency patterns in riparian soils of the Three Gorges Reservoir. Front. Microbiol. 2023, 14, 1108025. [Google Scholar] [CrossRef] [PubMed]
- Ren, H.; Lv, C.; Fernández-García, V.; Huang, B.; Yao, J.; Ding, W. Biochar and PGPR amendments influence soil enzyme activities and nutrient concentrations in a eucalyptus seedling plantation. Biomass-Convers. Biorefinery 2021, 11, 1865–1874. [Google Scholar] [CrossRef]
- Reed, M.; Glick, B.R. Applications of plant growth-promoting bacteria for plant and soil systems. In Applications of Microbial Engineering. Enfield 809 (CT); Gupta, V.K., Schmoll, M., Maki, M., Tuohy, M., Mazutti, M.A., Eds.; Taylor and Francis: Enfield, UK, 2013; pp. 181–229. [Google Scholar]
- Ma, M.C. Risk analysis and management measure on micro-organism in microbial organic fertilizers. Qual. Saf. Agro-Prod. 2019, 06, 57–61. [Google Scholar]
- Chandra, H.; Kumari, P.; Bisht, R.; Prasad, R.; Yadav, S. Plant growth promoting Pseudomonas aeruginosa from Valeriana walichii displays antagonistic potential against three phytopathogenic fungi. Mol. Biol. Rep. 2020, 47, 6015–6026. [Google Scholar] [CrossRef]
- Balthazar, C.; Novinscak, A.; Cantin, G.; Joly, D.L.; Filion, M. Biocontrol activity of Bacillus spp. and Pseudomonas spp. against Botrytis cinerea and other cannabis fungal pathogens. Phytopathology 2021, 112, 549–560. [Google Scholar] [CrossRef]
- Ghadamgahi, F.; Tarighi, S.; Taheri, P.; Saripella, G.V.; Anzalone, A.; Kalyandurg, P.B.; Catara, V.; Ortiz, R.; Vetukuri, R.R. Plant Growth-Promoting Activity of Pseudomonas aeruginosa FG106 and Its Ability to Act as a Biocontrol Agent against Potato, Tomato and Taro Pathogens. Biology 2022, 11, 140. [Google Scholar] [CrossRef]
- Hesse, C.; Schulz, F.; Bull, C.T.; Shaffer, B.T.; Yan, Q.; Shapiro, N.; Hassan, K.A.; Varghese, N.; Elbourne, L.D.H.; Paulsen, I.T. Genome-based evolutionary history of Pseudomonas spp. Environ. Microbiol. 2018, 20, 2142–2159. [Google Scholar] [CrossRef]
- Selvakumar, G.; Panneerselvam, P.; Bindu, G.H.; Ganeshamurthy, A.N. Pseudomonads: Plant growth promotion and beyond. In Plant Microbes Symbiosis: Applied Facets; Springer: Pune, India, 2015; pp. 193–208. [Google Scholar]
- Islam, F.; Yasmeen, T.; Ali, Q.; Ali, S.; Arif, M.S.; Hussain, S.; Rizvi, H. Influence of Pseudomonas aeruginosa as PGPR on oxidative stress tolerance in wheat under Zn stress. Ecotoxicol. Environ. Saf. 2014, 104, 285–293. [Google Scholar] [CrossRef]
- De Plano, L.M.; Caratozzolo, M.; Conoci, S.; Guglielmino, S.P.P.; Franco, D. Impact of nutrient starvation on bio-film formation in Pseudomonas aeruginosa: An analysis of growth, adhesion, and spatial distribution. Antibiotics 2024, 13, 987. [Google Scholar] [CrossRef]
- Pandey, N.; Bhatt, R. Arsenic resistance and accumulation by two bacteria isolated from a natural arsenic contaminated site. J. Basic Microbiol. 2015, 55, 1275–1286. [Google Scholar] [CrossRef] [PubMed]
- Edward Raja, C.; Pandeeswari, R.; Ramesh, U. Isolation and identification of high fluoride resistant bacteria from water samples of Dindigul district, Tamil Nadu, South India. Curr. Res. Micro. Sci. 2021, 2, 100038. [Google Scholar]
- Edward Raja, C.; Pandeeswari, R.; Ramesh, U. Characterisation of high fluoride resistant Pseudomonas aeruginosa species isolated from water samples. Environ. Res. Technol. 2022, 5, 325–339. [Google Scholar] [CrossRef]
- Singh, A.; Patani, A.; Patel, M.; Vyas, S.; Verma, R.K.; Amari, A.; Osman, H.; Rathod, L.; Elboughdiri, N.; Yadav, V.K.; et al. Tomato seed bio-priming with Pseudomonas aeruginosa strain PAR: A study on plant growth parameters under sodium fluoride stress. Front. Microbiol. 2024, 14, 1330071. [Google Scholar] [CrossRef]
- Thesai, A.S.; Rajakumar, S.; Ayyasamy, P.M. Removal of fluoride in aqueous medium under the optimum conditions through intracellular accumulation in Bacillus flexus (PN4). Environ. Technol. 2018, 41, 1185–1198. [Google Scholar] [CrossRef]
- Shanker, A.S.; Dasaiah, S.; Pindi, P. A study on bioremediation of fluoride-contaminated water via a novel bacterium Acinetobacter sp. (GU566361) isolated from potable water. Results Chem. 2020, 2, 100070. [Google Scholar] [CrossRef]
- Walker, T.S.; Bais, H.P.; Déziel, E.; Schweizer, H.P.; Rahme, L.G.; Fall, R.; Vivanco, J.M. Pseudomonas aeruginosa-plant root interactions. Pathogenicity, biofilm formation, and root exudation. Plant Physiol. 2004, 134, 320–331. [Google Scholar] [CrossRef]
- Kumar, S.; Bauddh, K.; Barman, S.C.; Singh, R.P. Amendments of microbial bio fertilizers and organic substances reduces requirement of urea and DAP with enhanced nutrient availability and productivity of wheat (Triticum aestivum L.). Ecol. Eng. 2014, 71, 432–437. [Google Scholar] [CrossRef]
- Khalid, A.; Arshad, M.; Zahir, Z. Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J. Appl. Microbiol. 2004, 96, 473–480. [Google Scholar] [CrossRef]
- Pandey, N.; Bhatt, R. Role of soil associated Exiguobacterium in reducing arsenic toxicity and promoting plant growth in Vigna radiata. Eur. J. Soil Biol. 2016, 75, 142–150. [Google Scholar] [CrossRef]
- Pandey, N.; Manjunath, K.; Sahu, K. Screening of plant growth promoting attributes and arsenic remediation efficacy of bacteria isolated from agricultural soils of Chhattisgarh. Arch. Microbiol. 2019, 202, 567–578. [Google Scholar] [CrossRef] [PubMed]
- Yang, R.; Luo, C.; Chen, Y.; Wang, G.; Xu, Y.; Shen, Z. Copper-resistant bacteria enhance plant growth and copper phytoextraction. Int. J. Phytoremediat. 2013, 15, 573–584. [Google Scholar] [CrossRef] [PubMed]
- Olanrewaju, O.S.; Glick, B.R.; Babalola, O.O. Mechanisms of action of plant growth promoting bacteria. World J. Microbiol. Biotechnol. 2017, 33, 197. [Google Scholar] [CrossRef] [PubMed]
- Patten, C.L.; Glick, B.R. Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl. Environ. Microbiol. 2002, 68, 3795–3801. [Google Scholar] [CrossRef]
- Garcia de Salamone, I.E.; Hynes, R.K.; Nelson, L.M. Cytokinin production by plant growth promotin rhizobacteria and selected mutants. Can. J. Microbiol. 2001, 47, 404–411. [Google Scholar]
- Lambrecht, M.; Okon, Y.; Broek, A.V.; Vanderleyden, J. Indole-3-acetic acid: A reciprocal signalling molecule in bacteria–plant interactions. Trends Microbiol. 2000, 8, 298–300. [Google Scholar] [CrossRef]
- Steenhoudt, O.; Vanderleyden, J. Azospirillum a free-living nitrogen-fixing bacterium closely associated with grasses: Genetic, biochemical and ecological aspects. FEMS Microbiol. Rev. 2000, 24, 487–506. [Google Scholar] [CrossRef]
- Egamberdieva, D. Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol. Plant. 2009, 31, 861–864. [Google Scholar] [CrossRef]
- Lepinay, C.; Rigaud, T.; Salon, C.; Lemanceau, P.; Mougel, C. Interaction between Medicago truncatula and Pseudomonas fluorescens: Evaluation of costs and benefits across an elevated atmospheric CO2. PLoS ONE 2012, 7, e45740. [Google Scholar] [CrossRef]
- Khan, M.S.; Zaidi, A.; Wani, P.A. Role of phosphate-solubilizing microorganisms in sustainable agriculture—A review. Agron. Sustain. Dev. 2009, 27, 29–43. [Google Scholar] [CrossRef]
- Sharma, S.B.; Sayyed, R.Z.; Trivedi, M.H.; Gobi, T.A. Phosphate solubilizing microbes: Sustainable approach for managing phosphorus deficiency in agricultural soils. Springer Plus 2013, 2, 587. [Google Scholar] [CrossRef] [PubMed]
- Jiang, H.; Qi, P.; Wang, T.; Wang, M.; Chen, M.; Chen, N.; Pan, L.; Chi, X. Isolation and characterization of halotolerant phosphate-solubilizing microorganisms from saline soils. 3 Biotech 2019, 8, 461. [Google Scholar] [CrossRef] [PubMed]
- Krewulak, K.D.; Vogel, H.J. Structural biology of bacterial iron uptake. Biochim. Biophys. Acta 2008, 1778, 1781–1804. [Google Scholar] [CrossRef] [PubMed]
- Burd, G.I.; Dixon, D.G.; Glick, B.R. Plant growth promoting bacteria that decrease heavy metal toxicity. Can. J. Microbiol. 2000, 46, 237–245. [Google Scholar] [CrossRef]
- Dimkpa, C.O.; Merten, D.; Svatos, A.; Buchel, G.; Kothe, E. Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J. App. Microbiol. 2009, 107, 1687–1696. [Google Scholar] [CrossRef]
- Glick, B.R. Plant Growth-promoting bacteria: Mechanisms and applications. Scientifica 2012, 2012, 963401. [Google Scholar] [CrossRef]
- Marques, A.P.; Moreira, H.; Franco, A.R.; Rangel, A.O.; Castro, P.M. Inoculating Helianthus annuus (sunflower) grown in zinc and cadmium contaminated soils with plant growth promoting bacteria—Effects on phytoremediation strategies. Chemosphere 2013, 92, 74–83. [Google Scholar] [CrossRef]
- Bhattacharyya, C.; Banerjee, S.; Acharya, U.; Mitra, A.; Mallick, I.; Haldar, A.; Haldar, S.; Ghosh, A.; Ghosh, A. Evaluation of plant growth promotion properties and induction of antioxidative defense mechanism by tea rhizobacteria of Darjeeling, India. Sci. Rep. 2020, 10, 15536. [Google Scholar] [CrossRef]
- Abd El-Rahman, A.F.; Shaheen, H.A.; Abd El-Aziz, R.M.; Ibrahim, D.S.S. Influence of hydrogen cyanide-producing rhizobacteria in controlling the crown gall and root-knot nematode, Meloidogyne incognita. Egypt. J. Biol. Pest Control 2019, 29, 41. [Google Scholar] [CrossRef]
- Yadu, B.; Chandrakar, V.; Meena, R.; Keshavkant, S. Glycinebetaine reduces oxidative injury and enhances fluoride stress tolerance via improving antioxidant enzymes, proline and genomic template stability in Cajanus cajan L. S. Afr. J. Bot. 2017, 111, 68–75. [Google Scholar] [CrossRef]
- Yadu, B.; Chandrakar, V.; Tamboli, R.; Keshavkant, S. Dimethylthiourea antagonizes oxidative responses by up-regulating expressions of pyrroline-5-carboxylate synthetase and antioxidant genes under arsenic stress. Int. J. Environ. Sci. Technol. 2019, 16, 8401–8410. [Google Scholar] [CrossRef]
- Zouari, M.; Elloumi, N.; Bellassoued, K.; Ben Ahmed, C.; Krayem, M.; Delmail, D.; Elfeki, A.; Ben Rouina, B.; Ben Abdallah, F.; Labrousse, P. Enzymatic antioxidant responses and mineral status in roots and leaves of olive plants subjected to fluoride stress. S. Afr. J. Bot. 2017, 111, 44–49. [Google Scholar] [CrossRef]
- Wang, A.G.; Xia, T.; Chu, Q.L. Effects of fluoride on lipid peroxidation, DNA damage and apoptosis in human embryo hepatocytes. Biomed. Environ. Sci. 2004, 17, 217–222. [Google Scholar] [PubMed]
- Liang, S.; Zhao, M.; Ock, S.A.; Kim, N.; Cui, X. Fluoride impairs oocyte maturation and subsequent embryonic development in mice. Environ. Toxicol. 2015, 31, 1486–1495. [Google Scholar] [CrossRef]
- Chen, L.; Ning, H.; Yin, Z.; Song, X.; Feng, Y.; Qin, H.; Li, Y.; Wang, J.; Ge, Y.; Wang, W. The effects of fluoride on neuronal function occurs via cytoskeleton damage and decreased signal transmission. Chemosphere 2017, 185, 589–594. [Google Scholar] [CrossRef]
- Pelc, J.; Snioszek, M.; Wrobel, J.; Telesinski, A. Effect of fluoride on germination, early growth and antioxidant en-zymes activity of three winter wheat (Triticum aestivum L.) cultivars. Appl. Sci. 2020, 10, 6971. [Google Scholar] [CrossRef]
- Chahine, S.; Melito, S.; Giannini, V.; Seddaiu, G.; Roggero, P.P. Fluoride stress affects seed germination and seedling growth by altering the morpho-physiology of an African local bean variety. Plant Growth Regul. 2023, 102, 339–350. [Google Scholar] [CrossRef]
- Richardson, A.E.; Barea, J.-M.; McNeill, A.M.; Prigent-Combaret, C. Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 2009, 321, 305–339. [Google Scholar] [CrossRef]
- Katooli, N.; Moghadam, E.M.; Taheri, A.; Nasrollahnejad, S. Management of root-knot nematode (Meloidogyne incognita) on cucumber with the extract and oil of nematicidal Plants. Int. J. Agric. Res. 2010, 5, 582–586. [Google Scholar] [CrossRef]
- Amogou, O.; Agbodjato, N.; Dagbénonbakin, G.; Noumavo, P.; Sina, H.; Sylvestre, A.; Adoko, M.; Nounagnon, M.; Kakai, R.; Adjanohoun, A.; et al. Improved maize growth in condition controlled by PGPR inoculation on ferruginous soil in central Benin. Food Nutr. Sci. 2019, 10, 1433–1451. [Google Scholar] [CrossRef]
- Sedri, M.H.; Niedbała, G.; Roohi, E.; Niazian, M.; Szulc, P.; Rahmani, H.A.; Feiziasl, V. Comparative analysis of plant growth-promoting rhizobacteria (PGPR) and chemical fertilizers on quantitative and qualitative characteristics of rainfed wheat. Agronomy 2022, 12, 1524. [Google Scholar] [CrossRef]
- Lugtenberg, B.; Malfanova, N.; Kamilova, F.; Berg, G. Plant growth promotion by microbes. In Molecular Microbial Ecology of the Rhizosphere; de Bruijn, F.J., Ed.; Wiley-Blackwell: Hoboken, NJ, USA, 2013; pp. 561–573. [Google Scholar]
- Barbier, O.; Arreola-Mendoza, L.; Del Razo, L.M. Molecular mechanisms of fluoride toxicity. Chem.-Biol. Interact. 2010, 188, 319–333. [Google Scholar] [CrossRef]
- Yu, S.; Bai, X.; Liang, J.; Wei, Y.; Huang, S.; Li, Y.; Dong, L.; Liu, X.; Qu, J.; Yan, L. Inoculation of Pseudomonas sp. GHD-4 and mushroom residue carrier increased the soil enzyme activities and microbial community diversity in Pb-contaminated soils. J. Soils Sediments 2019, 19, 1064–1076. [Google Scholar] [CrossRef]
- Zorina, S.Y.; Pomazkina, L.V.; Lavrent’eva, A.S.; Zasukhina, T.V. Humus status of different soils affected by pollution with fluorides from aluminum production in the Baikal region. Contemp. Probl. Ecol. 2010, 3, 336–340. [Google Scholar] [CrossRef]
- Montagnolli, R.N.; Lopes, P.R.M.; Cruz, J.M.; Claro, E.L.T.; Quiterio, G.M.; Bidoia, E.D. The effects of fluoride-based fire-fighting foams on soil microbiota activity and plant growth during natural attenuation of perfluorinated compounds. Environ. Toxicol. Pharmacol. 2017, 50, 119–127. [Google Scholar] [CrossRef]
- Wilke, B.M. Fluoride-induced changes in chemical properties and microbial activity of mull, moder and mor soils. Biol. Fertil. Soils 1987, 5, 49–55. [Google Scholar] [CrossRef]
- Reddy, M.P.; Kaur, M. Sodium fluoride induced growth and metabolic changes in Salicornia brachiate Roxb. Water Air Soil Pollut. 2008, 188, 171–179. [Google Scholar] [CrossRef]
- Rao, D.N.; Pal, D. Effect of fluoride pollution on the organic matter content of soil. Plant Soil 1978, 49, 653–656. [Google Scholar] [CrossRef]
- Cronin, S.J.; Manoharan, V.; Hedley, M.J.; Loganathan, P. Fluoride: A review of its fate bioavailability, and risks of fluorosis in grazed-pasture systems in New Zealand. N. Z. J. Agric. Res. 2000, 43, 295–321. [Google Scholar] [CrossRef]
- Ju, W.; Jin, X.; Liu, L.; Shen, G.; Zhao, W.; Duan, C.; Fang, L. Rhizobacteria inoculation benefits nutrient availability for phytostabilization in copper contaminated soil: Drivers from bacterial community structures in rhizosphere. Appl. Soil Ecol. 2019, 150, 103450. [Google Scholar] [CrossRef]
- Hidri, R.; Barea, J.; Mahmoud, O.M.-B.; Abdelly, C.; Azcón, R. Impact of microbial inoculation on biomass accumulation by Sulla carnosa provenances, and in regulating nutrition, physiological and antioxidant activities of this species under non-saline and saline conditions. J. Plant Physiol. 2016, 201, 28–41. [Google Scholar] [CrossRef] [PubMed]
- Marques, A.P.; Pires, C.; Moreira, H.; Rangel, A.O.; Castro, P.M. Assessment of the plant growth promotion abilities of six bacterial isolates using Zea mays as indicator plant. Soil Biol. Biochem. 2010, 42, 1229–1235. [Google Scholar] [CrossRef]
- El-Mageed, T.A.A.; El-Mageed, S.A.A.; El-Saadony, M.T.; Abdelaziz, S.; Abdou, N.M. Plant growth promoting rhizobacteria improve growth, morph-physiological responses, water productivity, and yield of rice plants under full and deficit drip irrigation. Rice 2022, 15, 16. [Google Scholar] [CrossRef] [PubMed]
- Cao, T.; Xie, P.; Ni, L.; Wu, A.; Zhang, M.; Wu, S.; Smolders, A. The role of NH+4 toxicity in the decline of the submersed macrophyte Vallisneria natans in lakes of the Yangtze River basin, China. Mar. Freshw. Res. 2007, 58, 581–587. [Google Scholar] [CrossRef]
- Kumar, K.; Giri, A.; Vivek, P.; Kalaiyarasan, T.; Kumar, B. Effect of fluoride on respiration and photosynthesis in plants: An overview. Ann. Environ. Sci. Toxicol. 2017, 2, 043–047. [Google Scholar] [CrossRef]
- Mondal, N.K. Effect of fluoride on photosynthesis, growth and accumulation of four widely cultivated rice (Oryza sativa L.) varieties in India. Ecotoxicol. Environ. Saf. 2017, 144, 36–44. [Google Scholar] [CrossRef]
- Wang, Q.; Xiong, D.; Zhao, P.; Yu, X.; Tu, B.; Wang, G. Effect of applying an arsenic-resistant and plant growth-promoting rhizobacterium to enhance soil arsenic phytoremediation by Populus deltoides LH05-17. J. Appl. Microbiol. 2011, 111, 1065–1074. [Google Scholar] [CrossRef]
- Elekhtyar, N. Efficiency of Pseudomonas fluorescens as plant growth-promoting rhizobacteria (PGPR) for the en-hancement of seedling vigor nitrogen uptake yield and its attributes of rice (Oryza sativa L). Int. J. Sci. Res. Agric. Sci. 2015, 2, 57–67. [Google Scholar]
- Samaniego-Gámez, B.Y.; Garruña, R.; Tun-Suárez, J.M.; Kantun-Can, J.; Reyes-Ramírez, A.; Cervantes-Díaz, L. Bacillus spp. inoculation improves photosystem II efficiency and enhances photosynthesis in pepper plants. Chil. J. Agric. Res. 2016, 76, 409–416. [Google Scholar] [CrossRef]
- Zhang, W.; Xie, Z.; Zhang, X. Growth-promoting bacteria alleviates drought stress of G uralensis through im-proving photosynthesis characteristics and water status. J. Plant Interact. 2019, 14, 580–589. [Google Scholar] [CrossRef]
- Cai, H.-M.; Peng, C.-Y.; Chen, J.; Hou, R.-Y.; Gao, H.-J.; Wan, X.-C. X-ray photoelectron spectroscopy surface analysis of fluoride stress in tea (Camellia sinensis (L.) O. Kuntze) leaves. J. Fluor. Chem. 2014, 158, 11–15. [Google Scholar] [CrossRef]
- Elloumi, N.; Zouari, M.; Mezghani, I.; Ben Abdallah, F.; Woodward, S.; Kallel, M. Adaptive biochemical and physiological responses of Eriobotrya japonica to fluoride air pollution. Ecotoxicology 2017, 26, 991–1001. [Google Scholar] [CrossRef] [PubMed]
- Tak, Y.; Asthir, B. Fluoride-induced changes in the antioxidant defence system in two contrasting cultivars of Triticum aestivum, L. Fluoride 2017, 50, 324–333. [Google Scholar]
- Banerjee, A.; Roychoudhury, A. Bio-priming with a novel plant growth-promoting Acinetobacter indicus strain alleviates Arsenic-Fluoride Co-toxicity in rice by modulating the physiome and micronutrient homeostasis. Appl. Biochem. Biotechnol. 2023, 195, 6441–6464. [Google Scholar] [CrossRef]
- Batool, T.; Ali, S.; Seleiman, M.F.; Naveed, N.H.; Ali, A.; Ahmed, K.; Abid, M.; Rizwan, M.; Shahid, M.R.; Alotaibi, M.; et al. Plant growth promoting rhizobacteria alleviates drought stress in potato in response to suppressive oxidative stress and antioxidant enzymes activities. Sci. Rep. 2020, 10, 16975. [Google Scholar] [CrossRef]
- Moreno-Galván, A.; Romero-Perdomo, F.; Estrada-Bonilla, G.; Meneses, C.; Bonilla, R. Dry Caribbean Bacillus spp. strains ameliorate drought stress in Maize by a strain-specific antioxidant response modulation. Microorganisms 2020, 8, 823. [Google Scholar] [CrossRef]
- Zandi, P.; Schnug, E. Reactive oxygen species, antioxidant responses and implications from a microbial modulation perspective. Biology 2022, 11, 155. [Google Scholar] [CrossRef]
- Saleh, A.H.; Abdel-Kader, Z. Metabolic responses of two Hellianthus annuus cultivars to different fluoride concentrations during germination and seedling growth stages Egyptian. J. Biol. 2003, 5, 43–54. [Google Scholar]
- Baunthiyal, M.; Ranghar, S. Accumulation of fluoride by plants: Potential for phytoremediation. CLEAN—Soil Air Water 2014, 43, 127–132. [Google Scholar] [CrossRef]
- Ma, Y.; Rajkumar, M.; Vicente, J. Freitas HInoculation of Ni-resistant plant growth promoting bacterium Psychrobacter sp strain SRS8 for the improvement of nickel phytoextraction by energy crops. Int. J. Phytorem. 2011, 13, 126–139. [Google Scholar] [CrossRef]
- Wani, P.A.; Khan, M.S.; Zaidi, A. Effects of heavy metal toxicity on growth, symbiosis, seed yield and metal uptake in pea grown in metal amended soil. Bull. Environ. Contam. Toxicol. 2008, 81, 152–158. [Google Scholar] [CrossRef] [PubMed]
- Khan, A.; Uddin, S.; Zhao, X.Q.; Javed, M.T.; Khan, K.; Bano, A.; Shen, R.F.; Masood, S. Bacillus pumilus enhances tolerance in rice (Oryza sativa L.) to combined stresses of NaCl and high boron due to limited 716 uptake of Na+. Environ. Exp. Bot. 2016, 124, 120–129. [Google Scholar] [CrossRef]
- Gordon, S.A.; Weber, R.P. Colorimetric estimation of indole acetic acid. Plant Physiol. 1951, 26, 192–195. [Google Scholar] [CrossRef] [PubMed]
- Dye, D.W. The inadequacy of the usual determinative tests for the identification of Xanthomonas sp. Nat. Sci. 1962, 5, 393–416. [Google Scholar]
- Castric, P.A. Hydrogen cyanide, a secondary metabolite of Pseudomonas aeruginosa. Can. J. Microbiol. 1975, 5, 613–618. [Google Scholar] [CrossRef]
- Alexander, D.B.; Zuberer, D.A. Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol. Fertil. Soils 1991, 12, 39–45. [Google Scholar] [CrossRef]
- Fiske, C.H.; Subbarow, Y. A colorimetric determination of phosphorus. J. Biol. Chem. 1925, 66, 375–400. [Google Scholar] [CrossRef]
- He, L.-Y.; Chen, Z.-J.; Ren, G.-D.; Zhang, Y.-F.; Qian, M.; Sheng, X.-F. Increased cadmium and lead uptake of a cadmium hyperaccumulator tomato by cadmium-resistant bacteria. Ecotoxicol. Environ. Saf. 2009, 72, 1343–1348. [Google Scholar] [CrossRef]
- Shcherbakova, T.A. Enzymatic Activity of Soils and Transformation of Soil Organic Matter; Nauka i Tekhnika: Minsk, Belarus, 1983. [Google Scholar]
- Schinner, F.; Ohlinger, R.; Margesin, R. Methods in Soil Biology; Springer: Berlin/Heidelberg, Germany, 1996. [Google Scholar] [CrossRef]
- Pancholy, S.K.; Rice, E.L. Soil enzymes in relation to old field succession: Amylase, cellulase, invertase, dehydrogenase, and urease. Soil Sci. Soc. Am. J. 1973, 37, 47–50. [Google Scholar] [CrossRef]
- Deng, S.; Tabatabai, M. Colorimetric determination of reducing sugars in soils. Soil Biol. Biochem. 1994, 26, 473–477. [Google Scholar] [CrossRef]
- Tabatabai, M.A.; Bremner, J.M. Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol. Biochem. 1969, 1, 301–307. [Google Scholar] [CrossRef]
- Alef, K. Estimation of microbial activities. In Methods in Applied Soil Microbiology and Biochemistry; Alef, K., Nannipieri, P., Eds.; Academic Press: London, UK, 1995; pp. 193–270. [Google Scholar]
- Xalxo, R.; Keshavkant, S. Growth and antioxidant responses of Trigonella foenum-graecum L. seedlings to lead and simulated acid rain exposure. Biologia 2020, 75, 1115–1126. [Google Scholar] [CrossRef]
- Rady, M.M. Effect of 24-epibrassinolide on growth, yield, antioxidant system and cadmium content of bean (Phaseolus vulgaris L.) plants under salinity and cadmium stress. Sci. Hortic. 2011, 129, 232–237. [Google Scholar] [CrossRef]
- Arnon, D. Copper enzymes isolated chloroplasts, polyphenoloxidase in Beta vulgaris. Plant Physiol. 1949, 24, 1–15. [Google Scholar] [CrossRef]
- Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248–254. [Google Scholar] [CrossRef]
- DuBois, M.K.; Gilles, A.; Hamilton, J.K.; Rebers, P.A.; Smith, F. Colorimetric method for determination of sugars and related substances. Anal. Chem. 1956, 28, 350–356. [Google Scholar] [CrossRef]
- Malavolta, E.; Vitti, G.C.; Oliveira, S.A. Avaliaçao do Estado Nutricional das Plantas: Princípiose aplicaçoes, 2nd ed.; Potafos: Piracicaba, Brazil, 1997. [Google Scholar]
- Kalaimaghal, R.; Geetha, S.A. Simple rapid method of estimation of iron in milled rice of early segregating generations. Electron. J. Plant Breed. 2014, 5, 63–66. [Google Scholar]
- Sangeetha, P.; Das, V.N.; Koratkar, R.; Suryaprabha, P. Increase in free radical generations and lipid peroxidation following chemotherapy in patients with cancer. Free Radic. Biol. Med. 1990, 8, 15. [Google Scholar] [CrossRef]
- Velikova, V.; Yordanov, I.; Edreva, A. Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Sci. 2000, 151, 59–66. [Google Scholar] [CrossRef]
- Kovacik, J.; Babula, P. Fluorescence microscopy as a tool for visualization of metal-induced oxidative stress in plants. Acta Physiol. Plant. 2017, 39, 157–163. [Google Scholar] [CrossRef]
- Hodges, D.M.; DeLong, J.M.; Forney, C.F.; Prange, R.K. Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 1999, 207, 604–611. [Google Scholar] [CrossRef]
- Marklund, S.; Marklund, G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem. 1974, 47, 469–474. [Google Scholar] [CrossRef] [PubMed]
- Chance, M.; Maehly, A.C. Assay of catalases and peroxidases. Methods Enzymol. 1955, 2, 764–775. [Google Scholar]
- Nakano, Y.; Asada, K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 1981, 22, 867–880. [Google Scholar] [CrossRef]
- Verwoerd, T.C.; Dekker, B.M.; Hoekema, A. A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res. 1989, 17, 2362. [Google Scholar] [CrossRef]
(Properties) | Parameters | Control | P. aeruginosa | F (50 ppm) | F + P. aeruginosa |
---|---|---|---|---|---|
Soil enzyme activity (post-harvest soil samples) | Urease (µg N-NH4+ g−1 dw h−1) | 98.60 c ± 1.18 | 129.88 a ± 1.38 | 67.55 d ± 0.60 | 105.88 b ± 0.99 |
Nitrate reductase (µg N-NO2− g−1 dw h−1) | 1.826 c ± 0.063 | 2.401 a ± 0.078 | 0.487 d ± 0.06 | 1.139 b ± 0.067 | |
Phophatase (µg pNPg−1 dw h−1) | 721.4 b ± 20.3 | 795.6 a ± 19.5 | 621.6 c ± 22.3 | 726.4 b ± 21.6 | |
Cellulase (µg D-Glu g−1dw h−1) | 15.78 b ± 1.09 | 20.87 a ± 1.00 | 8.3 c ± 0.66 | 14.23 b ± 0.77 | |
Dehydrogense (µg TPF g−1 dw h−1) | 68.45 b ± 4.11 | 96.65 a ± 3.26 | 26.76 d ± 2.26 | 54.55 c ± 2.65 | |
Basic physiological parameters | Root length (cm) | 23.4 a ± 1.81 | 25.2 a ± 1.01 | 12 c ± 1.87 | 17.4 b ± 2.07 |
Shoot length (cm) | 82.8 a ± 6.05 | 4.8 a ± 4.03 | 31 c ± 2.64 | 59.6 b ± 3.28 | |
Fresh weight (mg) | |||||
-Root | 90.23 a ± 9.6 | 92.23 a ± 6.2 | 45.12 c ± 4.7 | 65.23 b ± 8.9 | |
-Shoot | 252.1 a ± 13.2 | 264.1 a ± 10.2 | 151.23 c ± 9.8 | 198.87 b ± 12.4 | |
Dry weight (mg) | |||||
-Root | 41.05 a ± 2.6 | 43.05 a ± 3.31 | 23.2 c ± 1.7 | 32.01 b ± 4.7 | |
-Shoot | 95.49 a ± 5.2 | 99.49 a ± 1.02 | 58.21 c ± 3.8 | 65.23 b ± 8.9 | |
Membrane stability index (%) | 72.66 a ± 2.5 | 75.06 a ± 2.5 | 50 c ± 4.0 | 65 b ± 1.0 | |
Total chlorophyll (mg g−1 FM) | 55.4 a ± 3.35 | 57.5 a ± 2.05 | 27.2 c ± 2.41 | 38.78 b ± 0.34 | |
F accumulation | Root (ppm g−1 DM) | Not analyzed | Not analyzed | 30 a ± 3.65 | 20 b ± 3.71 |
Shoot (ppm g−1 DM) | Not analyzed | Not analyzed | 22 a ± 2.75 | 14.24 b ± 3.02 | |
Leaves (ppm g−1 DM) | Not analyzed | Not analyzed | 9 a ± 1.54 | 4.71 b ± 1.13 | |
Grain (ppm g−1 DM) | Not analyzed | Not analyzed | 2.9 a ± 0.12 | 0.74 b ± 0.05 | |
Yield attributes | Panicle length (cm) | 21.8 a ± 1.09 | 22.4 a ± 0.06 | 14.2 b ± 1.4 | 21.4 a ± 0.89 |
Number of spikelets per panicle | 17 b ± 1.6 | 20 a ± 1.0 | 8 b ± 1.14 | 15 b ± 1.3 | |
Number of filled grain per panicle | 95 b ± 1.8 | 107 a ± 1.2 | 26 d ± 3.6 | 79 c ± 6.9 | |
Number of empty grains per panicle | 5 c ± 1.3 | 3 c ± 0.3 | 41 a ± 2.3 | 18 b ± 1.6 | |
Grain length (cm) | 0.8 a ± 0.04 | 0.8 a ± 0.02 | 0.5 b ± 0.05 | 0.7 a ± 0.05 | |
Grain breadth (cm) | 0.26 a ± 0.01 | 0.26 a ± 0.0 | 0.15 c ± 0.01 | 0.2 b ± 0.0 | |
1000 grain weight (g) | 26.8 b ± 1.3 | 28.9 a ± 1.1 | 20.4 c ± 1.14 | 26.8 b ± 1.4 | |
Nutrient Contents | Protein (µg mL−1) | 80.03 a ± 0.73 | 81.04 a ± 0.81 | 78.5 a ± 1.8 | 79.88 a ± 2.78 |
Total sugar (µg mL−1) | 836.6 a ± 3.2 | 840.6 a ± 2.7 | 581.4 c ± 6.7 | 690.9 b ± 3.7 | |
Iron (ppm) | 43.4 a ± 1.5 | 45.1 a ± 1.03 | 33.6 c ± 1.2 | 37.2 b ± 1.6 | |
Zinc (ppm) | 38 a ± 3.78 | 40 a ± 2.08 | 24 b ± 4.58 | 34 a ± 4.04 |
PGPR Traits | Without F | With F (60 mM) |
---|---|---|
Ammonia production (µg mL−1) | 4.9 a ± 0.9 | 4.1 a ± 1.1 |
HCN production | + | + |
Phosphate solubilization (µg mL−1) | 44.93 a ± 1.3 | 44.53 a ± 1.6 |
Siderophore production index | 1.10 a ± 0.1 | 1.23 a ± 0.2 |
IAA production (µg mL−1) | 18.60 a ± 0.62 | 15.95 b ± 0.52 |
Exopolysaccharide production (µg mL−1) | 17 b ± 1.04 | 24 a ± 1.1 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Katiyar, P.; Pandey, N.; Varghese, B.; Sahu, K.K. Biopriming of Pseudomonas aeruginosa Abates Fluoride Toxicity in Oryza sativa L. by Restricting Fluoride Accumulation, Enhancing Antioxidative System, and Boosting Activities of Rhizospheric Enzymes. Plants 2025, 14, 1223. https://doi.org/10.3390/plants14081223
Katiyar P, Pandey N, Varghese B, Sahu KK. Biopriming of Pseudomonas aeruginosa Abates Fluoride Toxicity in Oryza sativa L. by Restricting Fluoride Accumulation, Enhancing Antioxidative System, and Boosting Activities of Rhizospheric Enzymes. Plants. 2025; 14(8):1223. https://doi.org/10.3390/plants14081223
Chicago/Turabian StyleKatiyar, Priya, Neha Pandey, Boby Varghese, and Keshav Kant Sahu. 2025. "Biopriming of Pseudomonas aeruginosa Abates Fluoride Toxicity in Oryza sativa L. by Restricting Fluoride Accumulation, Enhancing Antioxidative System, and Boosting Activities of Rhizospheric Enzymes" Plants 14, no. 8: 1223. https://doi.org/10.3390/plants14081223
APA StyleKatiyar, P., Pandey, N., Varghese, B., & Sahu, K. K. (2025). Biopriming of Pseudomonas aeruginosa Abates Fluoride Toxicity in Oryza sativa L. by Restricting Fluoride Accumulation, Enhancing Antioxidative System, and Boosting Activities of Rhizospheric Enzymes. Plants, 14(8), 1223. https://doi.org/10.3390/plants14081223