Abstract
Microorganisms are cost-effective and eco-friendly alternative methods for removing heavy metals (HM) from contaminated agricultural soils. Therefore, this study aims to identify and characterize HM-tolerant (HMT) plant growth-promoting rhizobacteria (PGPR) isolated from industry-contaminated soils to determine their impact as bioremediators on HM-stressed pepper plants. Four isolates [Pseudomonas azotoformans (Pa), Serratia rubidaea (Sr), Paenibacillus pabuli (Pp) and Bacillus velezensis (Bv)] were identified based on their remarkable levels of HM tolerance in vitro. Field studies were conducted to evaluate the growth promotion and tolerance to HM toxicity of pepper plants grown in HM-polluted soils. Plants exposed to HM stress showed improved growth, physio-biochemistry, and antioxidant defense system components when treated with any of the individual isolates, in contrast to the control group that did not receive PGPR. The combined treatment of the tested HMT PGPR was, however, relatively superior to other treatments. Compared to no or single PGPR treatment, the consortia (Pa+Sr+Pp+Bv) increased the photosynthetic pigment contents, relative water content, and membrane stability index but lowered the electrolyte leakage and contents of malondialdehyde and hydrogen peroxide by suppressing the (non) enzymatic antioxidants in plant tissues. In pepper, Cd, Cu, Pb, and Ni contents decreased by 88.0-88.5, 63.8-66.5, 66.2-67.0, and 90.2-90.9% in leaves, and 87.2-88.1, 69.4-70.0%, 80.0-81.3, and 92.3%% in fruits, respectively. Thus, these PGPR are highly effective at immobilizing HM and reducing translocation in planta. These findings indicate that the application of HMT PGPR could be a promising “bioremediation” strategy to enhance growth and productivity of crops cultivated in soils contaminated with HM for sustainable agricultural practices.
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References
Abdul G (2010) Effect of lead toxicity on growth, chlorophyll and lead (Pb+) contents of two varieties of maize (Zea mays L.). Pak J Nutr 9:887–891
Ahmad I, Akhtar MJ, Mehmood S, Akhter K, Tahir M, Saeed MF, Hussain MB, Hussain S (2018) Combined application of compost and Bacillus sp. CIK-512 ameliorated the lead toxicity in radish by regulating the homeostasis of antioxidants and lead. Ecotoxicol Environ Saf 148:805–812. https://doi.org/10.1016/j.ecoenv.2017.11.054
Ahmad P, Jaleel CA, Azooz MM, Nabi G (2009) Generation of ROS and non-enzymatic antioxidants during abiotic stress in plants. Bot Res Intern 2:11–20
Alam MZ, McGee R, Hoque MA, Ahammed GJ, Carpenter-Boggs L (2019) Effect of arbuscular mycorrhizal fungi, selenium and biochar on photosynthetic pigments and antioxidant enzyme activity under arsenic stress in mung bean (Vigna radiata). Front Physiol 10:193. https://doi.org/10.3389/fphys.2019.00193
Alengebawy A, Abdelkhalek ST, Qureshi SR, Wang MQ (2021) Heavy metals and pesticides toxicity in agricultural soil and plants: ecological risks and human health implications. Toxics 9:42. https://doi.org/10.3390/toxics9030042
Alexander A, Singh VK, Mishra A (2020) Halotolerant PGPR Stenotrophomonas maltophilia BJ01 induces salt tolerance by modulating physiology and biochemical activities of Arachis hypogaea. Front Microbiol 11:568289. https://doi.org/10.3389/fmicb.2020.568289
Alexander M (1997) Introduction to Soil Microbiology. John Wiley and Sons, New York, USA, p 467
Ali J, Ali F, Ahmad I, Rafique M, Munis MFH, Hassan SW, Sultan T, Iftikhar M, Chaudhary HJ (2021) Mechanistic elucidation of germination potential and growth of Sesbania sesban seedlings with Bacillus anthracis PM21 under heavy metals stress: An in vitro study. Ecotoxicol Environ Saf 208:111769. https://doi.org/10.1016/j.ecoenv.2020.111769
Alwahshi KJ, Purayil GP, Saeed EE, Abufarajallah HA, Aldhaheri SJ, AbuQamar SF, El-Tarabily KA (2022) The 1-aminocyclopropane-1-carboxylic acid deaminase-producing Streptomyces violaceoruber UAE1 can provide protection from sudden decline syndrome on date palm. Front Plant Sci 13:904166. https://doi.org/10.3389/fpls.2022.904166
Aman Shamil N (2022) Role of exogenous application of proline and glycine betaine in the salinity tolerance of Solanaceae family: a review. Acta Sci Agric 6:46–54. https://doi.org/10.31080/ASAG.2022.06.1179
Ashfaq MY, Da’na DA, Al-Ghouti MA (2022) Application of MALDI-TOF MS for identification of environmental bacteria: a review. J Environ Manag 305:114359. https://doi.org/10.1016/j.jenvman.2021.114359
Ashry NM, Alaidaroos BA, Mohamed SA, Badr OAM, El-Saadony MT, Esmael A (2022) Utilization of drought-tolerant bacterial strains isolated from harsh soils as a plant growth-promoting rhizobacteria (PGPR). Saudi J Biol Sci 29:1760–1769. https://doi.org/10.1016/j.sjbs.2021.10.054
Awasthi S, Chauhan R, Dwivedi S, Srivastava S, Srivastava S, Tripathi RD (2018) A consortium of alga (Chlorella vulgaris) and bacterium (Pseudomonas putida) for amelioration of arsenic toxicity in rice: A promising and feasible approach. Environ Exp Bot 150:115–126. https://doi.org/10.1016/j.envexpbot.2018.03.001
Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428. https://doi.org/10.1071/BI9620413
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Bhaduri AM, Fulekar MH (2012) Antioxidant enzyme responses of plants to heavy metal stress. Rev Environ Sci Biotechnol 11:55–69. https://doi.org/10.1007/s11157-011-9251-x
Bhat MA, Mishra AK, Jan S, Bhat MA, Kamal MA, Rahman S, Shah AA, Jan AT (2023) Plant growth promoting rhizobacteria in plant health: A perspective study of the underground interaction. Plants 12:629. https://doi.org/10.3390/plants12030629
Bhuyan B, Kotoky R, Maheshwari DK, Pandey P (2022) Rhizoremediation of Cd-contaminated soil using Zea mays Sturt, with heavy metal resistant rhizobacteria that alleviate Cd-induced stress in plant. Environ Sustain 5:375–387. https://doi.org/10.1007/s42398-022-00241-w
Bille E, Dauphin B, Leto J, Bougnoux ME, Beretti JL, Lotz A, Suarez S, Meyer J, Lambert OJ, Descamps P, Grall N, Mory F, Dubreuil L, Berche P, Nassif X, Ferroni A (2012) MALDI-TOF MS Andromas strategy for the routine identification of bacteria, mycobacteria, yeasts, Aspergillus spp. and positive blood cultures. Clin Microbiol Infect 18:1117–1125. https://doi.org/10.1111/j.1469-0691.2011.03688.x
Biswas MS, Mano J (2021) Lipid peroxide-derived reactive carbonyl species as mediators of oxidative stress and signaling. Front Plant Sci 12:720867. https://doi.org/10.3389/fpls.2021.720867
Black CA (1958) Soil-plant relationships. Soil Sci 85:175. https://doi.org/10.1097/00010694-195803000-00023
Burd GI, Dixon DG, Glick BR (1998) A plant growth-promoting bacterium that decreases nickel toxicity in seedlings. Appl Environ Microbiol 64:3663–3668. https://doi.org/10.1128/AEM.64.10.3663-3668.1998
Busnelli MP, Lazzarini Behrmann IC, Ferreira ML, Candal RJ, Ramirez SA, Vullo DL (2021) Metal- Pseudomonas veronii 2E interactions as strategies for innovative process developments in environmental biotechnology. Front Microbiol 12:622600. https://doi.org/10.3389/fmicb.2021.622600
Chen LL, Wang HY, Gong XC, Zeng ZH, Xue XZ, Hu YG (2021) Transcriptome analysis reveals effects of red and blue light-emitting diodes (LEDs) on the growth, chlorophyll fluorescence and endogenous plant hormones of potato (Solanum tuberosum L.) plantlets cultured in vitro. J Integr Agric 20:2914–2931. https://doi.org/10.1016/S2095-3119(20)63393-7
Chen XX, Liu YM, Zhao QY, Cao WQ, Chen XP, Zou CQ (2020) Health risk assessment associated with heavy metal accumulation in wheat after long-term phosphorus fertilizer application. Environ Pollut 262:114348. https://doi.org/10.1016/j.envpol.2020.114348
Chen Y, Hua CY, Jia MR, Fu JW, Liu X, Han YH, Liu Y, Rathinasabapathi B, Cao Y, Ma LQ (2017) Heterologous expression of Pteris vittata arsenite antiporter PvACR3; 1 reduces arsenic accumulation in plant shoots. Environ Sci Technol 51:10387–10395. https://doi.org/10.1021/acs.est.7b03369
Cheng B, Wang Z, Yan X, Yu Y, Liu L, Gao Y, Zhang H, Yang X (2023) Characteristics and pollution risks of Cu, Ni, Cd, Pb, Hg and As in farmland soil near coal mines. SEH. 1:100035. https://doi.org/10.1016/j.seh.2023.100035
Ching LS, Mohamed S (2001) Alpha-tocopherol content in 62 edible tropical plants. J Agric Food Chem 49:3101–3105. https://doi.org/10.1021/jf000891u
Cuypers A, Vanbuel I, Iven V, Kunnen K, Vandionant S, Huybrechts M, Hendrix S (2023) Cadmium-induced oxidative stress responses and acclimation in plants require fine-tuning of redox biology at subcellular level. Free Radic Biol Med 199:81–96. https://doi.org/10.1016/j.freeradbiomed.2023.02.010
Demidchik V, Straltsova D, Medvedev SS, Pozhvanov GA, Sokolik A, Yurin V (2014) Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment. J Exp Bot 65:1259–1270. https://doi.org/10.1093/jxb/eru004
Desoky E-SM, Elrys AS, Rady MM (2019) Integrative moringa and licorice extracts application improves Capsicum annuum fruit yield and declines its contaminant contents on a heavy metals-contaminated saline soil. Ecotoxicol Environ Saf 169:50–60. https://doi.org/10.1016/j.ecoenv.2018.10.117
Desoky E-SM, Merwad AM, Semida WM, Ibrahim SA, El-Saadony MT, Rady MM (2020) Heavy metals-resistant bacteria (HM-RB): Potential bioremediators of heavy metals-stressed Spinacia oleracea plant. Ecotoxicol Environ Saf 198:110685. https://doi.org/10.1016/j.ecoenv.2020.110685
Devireddy AR, Zandalinas SI, Fichman Y, Mittler R (2021) Integration of reactive oxygen species and hormone signaling during abiotic stress. Plant J 105:459–476. https://doi.org/10.1111/tpj.15010
Din BU, Amna RM, Javed MT, Kamran MA, Mehmood S, Khan M, Sultan T, Hussain Munis MF, Chaudhary HJ (2020) Assisted phytoremediation of chromium spiked soils by Sesbania sesban in association with Bacillus xiamenensis PM14: a biochemical analysis. Plant Physiol Biochem 146:249–258. https://doi.org/10.1016/j.plaphy.2019.11.010
Dong MF, Feng R, Wang R, Sun Y, Ding YZ, Xu YM, Fan Z, Guo J (2016) Inoculation of Fe/Mn-oxidizing bacteria enhances Fe/Mn plaque formation and reduces Cd and As accumulation in rice plant tissues. Plant Soil 404:75–83. https://doi.org/10.1007/s11104-016-2829-x
Dutta D, Pal AK (2019) Physiological basis of cadmium tolerance in groundnut (Arachis hypogaea L.). J Pharmacogn Phytochem 8:548–552
Duxbury T (1981) Toxicity of heavy metals to soil bacteria. FEMS Microbiol Lett 11:217–220. https://doi.org/10.1111/j.1574-6968.1981.tb06967.x
Efe D (2020) Potential plant growth-promoting bacteria with heavy metal resistance. Curr Microbiol 77:3861–3868. https://doi.org/10.1007/s00284-020-02208-8
El-Meihy RM, Abou-Aly HE, Youssef AM, Tewfike TA, El-Alkshar EA (2019) Efficiency of heavy metals-tolerant plant growth promoting bacteria for alleviating heavy metals toxicity on sorghum. Environ Exp Bot 162:295–301. https://doi.org/10.1016/j.envexpbot.2019.03.005
Elnahal AS, El-Saadony MT, Saad AM, Desoky E-SM, El-Tahan AM, Rady MM, AbuQamar SF, El-Tarabily KA (2022) The use of microbial inoculants for biological control, plant growth promotion, and sustainable agriculture: a review. Eur J Plant Pathol 162:759–792. https://doi.org/10.1007/s10658-021-02393-7
El-Saadony MT, Desoky E-SM, Saad AM, Eid RSM, Selem E, Elrys AS (2021) Biological silicon nanoparticles improve Phaseolus vulgaris L. yield and minimize its contaminant contents on a heavy metals-contaminated saline soil. J Environ Sci 106:1–14. https://doi.org/10.1016/j.jes.2021.01.012
Eltahawy AMAE, Awad EAM, Ibrahim AH, Merwad AMA, Desoky E-SM (2022) Integrative application of heavy metal–resistant bacteria, moringa extracts, and nano-silicon improves spinach yield and declines its contaminant contents on a heavy metal–contaminated soil. Front Plant Sci 13:1019014. https://doi.org/10.3389/fpls.2022.1019014
El-Tarabily KA, AlKhajeh AS, Ayyash MM, Alnuaimi LH, Sham A, ElBaghdady KZ, Saeed T, AbuQamar SF (2019) Growth promotion of Salicornia bigelovii by Micromonospora chalcea UAE1, an endophytic 1-aminocyclopropane-1-carboxylic acid deaminase-producing actinobacterial isolate. Front Microbiol 10:1694. https://doi.org/10.3389/fmicb.2019.01694
El-Tarabily KA, ElBaghdady KZ, AlKhajeh AS, Ayyash M, Aljneibi RS, El-Keblawy A, AbuQamar SF (2020) Polyamine-producing actinobacteria enhance biomass production and seed yield in Salicornia bigelovii. Biol Fertil Soils 56:499–519. https://doi.org/10.1007/s00374-020-01450-3
El-Tarabily KA, Sham A, Elbadawi AA, Hassan AH, Alhosani BKK, El-Esawi MA, AlKhajeh AS, AbuQamar SF (2021) A consortium of rhizosphere-competent actinobacteria exhibiting multiple plant growth-promoting traits improves the growth of Avicennia marina in the United Arab Emirates. Front Mar Sci 8:715123. https://doi.org/10.3389/fmars.2021.715123
Fadeel AA (1962) Location and properties of chloroplasts and pigment determination in roots. Physiol Plant 15:130–146. https://doi.org/10.1111/j.1399-3054.1962.tb07994.x
Faize M, Faize L, Petri C, Barba-Espin G, Diaz-Vivancos P, Clemente-Moreno MJ, Koussa T, Rifai LA, Burgos L, Hernandez JA (2013) Cu/Zn superoxide dismutase and ascorbate peroxidase enhance in vitro shoot multiplication in transgenic plum. J Plant Physiol 170:625–632. https://doi.org/10.1016/j.jplph.2012.12.016
Gall JE, Boyd RS, Rajakaruna N (2015) Transfer of heavy metals through terrestrial food webs: a review. Environ Monit Assess 187:201. https://doi.org/10.1007/s10661-015-4436-3
Ghori N-H, Ghori T, Hayat MQ, Imadi SR, Gul A, Altay V, Ozturk M (2019) Heavy metal stress and responses in plants. Int J Environ Sci Technol 16:1807–1828. https://doi.org/10.1007/s13762-019-02215-8
Ghosh UK, Islam MN, Siddiqui MN, Cao X, Khan MAR (2022) Proline, a multifaceted signalling molecule in plant responses to abiotic stress: understanding the physiological mechanisms. Plant Biol 24:227–239. https://doi.org/10.1111/plb.13363
Górski F, Gerotti GM, Gonçalves JE, Gazim ZC, Magalhães HM (2023) Methyl jasmonate and copper activate volatiles and antioxidant mechanisms in 'Grecco a Palla' basil produced in vitro. J Crop Sci Biotechnol 26:615. https://doi.org/10.1007/s12892-023-00206-3
Gu CS, Liu LQ, Deng YM, Zhang YX, Wang ZQ, Yuan HY, Huang SZ (2017) De novo characterization of the Iris lactea var. chinensis transcriptome and an analysis of genes under cadmium or lead exposure. Ecotoxicol Environ Saf 144:507–513. https://doi.org/10.1016/j.ecoenv.2017.06.071
Guo J, Qin S, Rengel Z, Gao W, Nie Z, Liu H, Li C, Zhao P (2019) Cadmium stress increases antioxidant enzyme activities and decreases endogenous hormone concentrations more in Cd-tolerant than Cd-sensitive wheat varieties. Ecotoxicol Environ Saf 172:380–387. https://doi.org/10.1016/j.ecoenv.2019.01.069
Hasanuzzaman M, Bhuyan MHMB, Zulfiqar F, Raza A, Mohsin SM, Mahmud JA, Fujita M, Fotopoulos V (2023) Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants 9:681. https://doi.org/10.3390/antiox9080681
He F, Zhao L, Zheng X, Abdelhai MH, Boateng NS, Zhang X, Zhang H (2020) Investigating the effect of methyl jasmonate on the biocontrol activity of Meyerozyma guilliermondii against blue mold decay of apples and the possible mechanisms involved. Physiol Mol Plant Pathol 109:101454. https://doi.org/10.1016/j.pmpp.2019.101454
Heath RL, 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
Hniličková H, Hnilička F, Orsák M, Hejnák V (2019) Effect of salt stress on growth, electrolyte leakage, Na+ and K+ content in selected plant species. Plant Soil Environ 65:90–96. https://doi.org/10.17221/620/2018-PSE
Hussein H-AA, Darwesh OM, Mekki BB, El-Hallouty SM (2019) Evaluation of cytotoxicity, biochemical profile and yield components of groundnut plants treated with nano-selenium. Biotechnol Rep 24:e00377. https://doi.org/10.1016/j.btre.2019.e00377
Irigoyen J, Einerich D, Sánchez-Díaz M (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiol Plant 84:55–60. https://doi.org/10.1111/j.1399-3054.1992.tb08764.x
Islam F, Yasmeen T, Ali Q, Mubin M, Ali S, Arif MS, Hussain S, Riaz M, Abbas F (2016) Copper-resistant bacteria reduces oxidative stress and uptake of copper in lentil plants: potential for bacterial bioremediation. Environ Sci Pollut Res Int 23:220–233. https://doi.org/10.1007/s11356-015-5354-1
Jackson M (1958) Soil chemical analysis. Prentice-Hall, Inc., Englewood Cliffs, NJ, p 498
Jones DL, Darrah PR (1994) Role of root derived organic acids in the mobilization of nutrients from the rhizosphere. Plant Soil 166:247–257. https://doi.org/10.1007/BF00008338
Jung HI, Lee TG, Lee J, Chae MJ, Lee EJ, Kim MS, Jung GB, Emmanuel A, Jeon S, Lee BR (2021) Foliar-applied glutathione mitigates cadmium-induced oxidative stress by modulating antioxidant-scavenging, redox-regulating, and hormone-balancing systems in Brassica napus. Front Plant Sci 12:700413. https://doi.org/10.3389/fpls.2021.700413
Kakan X, Yu Y, Li S, Li X, Huang R, Wang J (2021) Ascorbic acid modulation by ABI4 transcriptional repression of VTC2 in the salt tolerance of Arabidopsis. BMC Plant Biol 21:112. https://doi.org/10.1186/s12870-021-02882-1
Kamran MA, Bibi S, Xu RK, Hussain S, Mehmood K, Chaudhary HJ (2017) Phyto-extraction of chromium and influence of plant growth promoting bacteria to enhance plant growth. J Geochem Explor 182:269–274. https://doi.org/10.1016/j.gexplo.2016.09.005
Kang SM, Khan AL, Waqas M, You YH, Kim JH, Kim JG, Hamayun M, Lee IJ (2014) Plant growth-promoting rhizobacteria reduce adverse effects of salinity and osmotic stress by regulating phytohormones and antioxidants in Cucumis sativus. J Plant Interact 9:673–682. https://doi.org/10.1080/17429145.2014.894587
Kaur J, Pandove G (2023) Understanding the beneficial interaction of plant growth promoting rhizobacteria and endophytic bacteria for sustainable agriculture: a bio-revolution approach. J Plant Nutr 202:3569–3597. https://doi.org/10.1080/01904167.2023.2206425
Khan MIR, Jahan B, AlAjmi MF, Rehman MT, Iqbal N, Irfan M, Sehar Z, Khan NA (2021) Crosstalk of plant growth regulators protects photosynthetic performance from arsenic damage by modulating defense systems in rice. Ecotoxicol Environ Saf 222:112535. https://doi.org/10.1016/j.ecoenv.2021.112535
Khan N, Ryu KY, Choi JY, Nho EY, Habte G, Choi H, Kim MH, Park KS, Kim KS (2015) Determination of toxic heavy metals and speciation of arsenic in seaweeds from South Korea. Food Chem 169:464–470. https://doi.org/10.1016/j.foodchem.2014.08.020
Khatun M, Matsushima D, Rhaman MS, Okuma E, Nakamura T, Nakamura Y, Munemasa S, Murata Y (2020) Exogenous proline enhances antioxidant enzyme activities but does not mitigate growth inhibition by selenate stress in tobacco BY-2 cells. Biosci Biotechnol Biochem 84:2281–2292. https://doi.org/10.1080/09168451.2020.1799747
Khoso MA, Wagan S, Alam I, Hussain A, Ali Q, Saha S, Poudel TR, Manghwar H, Liu F (2024) Impact of plant growth-promoting rhizobacteria (PGPR) on plant nutrition and root characteristics: Current perspective. Plant Stress 11:100341. https://doi.org/10.1016/j.stress.2023.100341
Kobya M, Demirbas E, Senturk E, Ince M (2005) Adsorption of heavy metal ions from aqueous solutions by activated carbon prepared from apricot stone. Bioresour Technol 96:1518–1521. https://doi.org/10.1016/j.biortech.2004.12.005
Kohli SK, Handa N, Gautam V, Bali S, Sharma A, Khanna K, Arora S, Thukral AK, Ohri P, Karpets YV, Kolupaev YE, Bhardwaj R (2017) ROS signaling in plants under heavy metal stress. In: Khan M, Khan N (eds) Reactive oxygen species and antioxidant systems in plants: Role and regulation under abiotic stress. Springer, Singapore, pp 185–214. https://doi.org/10.1007/978-981-10-5254-5_8
Konings EJ, Roomans HH, Beljaars PR (1996) Liquid chromatographic determination of tocopherols and tocotrienols in margarine, infant foods, and vegetables. J AOAC Int 79:902–906. https://doi.org/10.1093/jaoac/79.4.902
Kowalska-Krochmal B, Dudek-Wicher R (2021) The minimum inhibitory concentration of antibiotics: Methods, interpretation, clinical relevance. Pathogens 10:165. https://doi.org/10.3390/pathogens10020165
Kubiś J (2008) Exogenous spermidine differentially alters activities of some scavenging system enzymes, H2O2 and superoxide radical levels in water-stressed cucumber leaves. J Plant Physiol 165:397–406. https://doi.org/10.1016/j.jplph.2007.02.005
Kumari S, Mishra A (2021) Heavy metal contamination. In: Larramendy ML, Soloneski S (eds) Soil contamination-threats and sustainable solutions. IntechOpenLimited, London, United Kingdom. https://doi.org/10.5772/intechopen.93412
Lamhamdi M, El Galiou O, Bakrim A, Novoa-Munoz JC, Arias-Estevez M, Aarab A, Lafont R (2013) Effect of lead stress on mineral content and growth of wheat (Triticum aestivum) and spinach (Spinacia oleracea) seedlings. Saudi J Biol Sci 20:29–36. https://doi.org/10.1016/j.sjbs.2012.09.001
Li S, Zhao B, Jin M, Hu L, Zhong H, He Z (2020) A comprehensive survey on the horizontal and vertical distribution of heavy metals and microorganisms in soils of a Pb/Zn smelter. J Hazard Mater 400:123255. https://doi.org/10.1016/j.jhazmat.2020.123255
Li Y, Ye Z, Yu Y, Li Y, Jiang J, Wang L, Wang G, Zhang H, Li N, Xie X, Cheng X, Liu K, Liu M (2023) A combined method for human health risk area identification of heavy metals in urban environments. J Hazard Mater 449:131067. https://doi.org/10.1016/j.jhazmat.2023.131067
Liu J, Lu B, Xun AL (2000) An improved method for the determination of hydrogen peroxide in leaves. Prog Biochem Biophys 27:548–551
Logan NA, De Vos P (2009) Genus I. Bacillus Cohn 1872, 174AL. In: De Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer KH, Whitman WB (eds) Bergey's Manual of Systematic Bacteriology, vol 3, 2nd edn. Springer, New York, pp 21–128
Luo X, Bing H, Luo Z, Wang Y, Jin L (2019) Impacts of atmospheric particulate matter pollution on environmental biogeochemistry of trace metals in soil-plant system: a review. Environ Pollut 255:113138. https://doi.org/10.1016/j.envpol.2019.113138
Madhu PM, Sadagopan RS (2020) Effect of heavy metals on growth and development of cultivated plants with reference to cadmium, chromium and lead–a review. J Stress Physiol Biochem 16:84–102
Mahmoud A, AbdElgawad H, Hamed BA, Beemster GTS, El-Shafey NM (2021) Differences in cadmium accumulation, detoxification and antioxidant defenses between contrasting maize cultivars implicate a role of superoxide dismutase in Cd tolerance. Antioxidants 10:1812. https://doi.org/10.3390/antiox10111812
Manaf HH, Zayed MS (2015) Productivity of cowpea as affected by salt stress in presence of endomycorrhizae and Pseudomonas fluorescens. Ann Agric Sci 60:219–226. https://doi.org/10.1016/j.aoas.2015.10.013
Mantelin S, Desbrosses G, Larcher M, Tranbarger TJ, Cleyet-Marel JC, Touraine B (2006) Nitrate-dependent control of root architecture and N nutrition are altered by a plant growth-promoting Phyllobacterium sp. Planta 223:591–603
Manzoor N, Ali L, Ahmed T, Noman M, Adrees M, Shahid MS, Ogunyemi SO, Radwan KSA, Wang G, Zaki HEM (2022) Recent advancements and development in nano-enabled agriculture for improving abiotic stress tolerance in plants. Front Plant Sci 13:951752. https://doi.org/10.3389/fpls.2022.951752
Maruta T, Ishikawa T (2022) Analysis of ascorbate metabolism in Arabidopsis under high-light stress. Methods Mol Biol 2526:15–24. https://doi.org/10.1007/978-1-0716-2469-2_2
Mathew BT, Torky Y, Amin A, Mourad A-HI, Ayyash MM, El-Keblawy A, Hilal-Alnaqbi A, AbuQamar SF, El-Tarabily KA (2020) Halotolerant marine rhizosphere-competent actinobacteria promote Salicornia bigelovii growth and seed production using seawater irrigation. Front Microbiol 11:552. https://doi.org/10.3389/fmicb.2020.00552
McClean C, Davison GW (2022) Circadian clocks, redox homeostasis, and exercise: Time to connect the dots? Antioxidants. 11:256. https://doi.org/10.3390/antiox11020256
Misra S, Chauhan PS (2020) ACC deaminase-producing rhizosphere competent Bacillus spp. mitigate salt stress and promote Zea mays growth by modulating ethylene metabolism. 3 Biotech 10:119. https://doi.org/10.1007/s13205-020-2104-y
Mukarram M, Choudhary S, Kurjak D, Petek A, Khan MMA (2021) Drought: sensing, signalling, effects and tolerance in higher plants. Physiol Plant 172:1291–1300. https://doi.org/10.1111/ppl.13423
MuKherjee SP, Choudhuri MA (1983) Implication of water stress—induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedling. Physiol Plant 58:166–170. https://doi.org/10.1111/j.1399-3054.1983.tb04162.x
Nagalakshmi N, Prasad MN (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160:291–299. https://doi.org/10.1016/s0168-9452(00)00392-7
Nagrale DT, Chaurasia A, Kumar S, Gawande SP, Hiremani NS, Shankar R, Gokte-Narkhedkar N, Renu PYG (2023) PGPR: the treasure of multifarious beneficial microorganisms for nutrient mobilization, pest biocontrol and plant growth promotion in field crops. World J Microbiol Biotechnol 39:100. https://doi.org/10.1007/s11274-023-03536-0
Nazli F, Wang X, Ahmad M, Hussain A, Bushra DA, Nasim M, Jamil M, Panpluem N, Mustafa A (2021) Efficacy of indole acetic acid and exopolysaccharides-producing Bacillus safensis strain FN13 for inducing Cd-stress tolerance and plant growth promotion in Brassica juncea (L.). Appl Sci 11:4160. https://doi.org/10.3390/app11094160
Noor I, Sohail H, Sun J, Nawaz MA, Li G, Hasanuzzaman M, Liu J (2022) Heavy metal and metalloid toxicity in horticultural plants: Tolerance mechanism and remediation strategies. Chemosphere 303:135196. https://doi.org/10.1016/j.chemosphere.2022.135196
Oubohssaine M, Sbabou L, Aurag J (2022) Native heavy metal-tolerant plant growth promoting rhizobacteria improves Sulla spinosissima (L.) growth in post-mining contaminated soils. Microorganisms 10:838. https://doi.org/10.3390/microorganisms10050838
Oyenike MA, Akpan HB, Otulana OJ, Adefule AK, Adedokun KA, Oluogun WA, Muhibi MA, Ojokuku HO (2019) In vitro anti-sickling and membrane stability potentials of Mishenland polyherbal extract on sickle red blood cells. Egy J Haematol 44:65–71. https://doi.org/10.4103/ejh.ejh_33_18
Pandey N, Bhatt R (2016) Role of soil associated Exiguobacterium in reducing arsenic toxicity and promoting plant growth in Vigna radiata. Eur J Soil Biol 75:142–150. https://doi.org/10.1016/j.ejsobi.2016.05.007
Patil S, Ansari A, Sarje A, Bankar A (2023) Heavy Metals Pollution and Role of Soil PGPR: A Mitigation Approach. In: Parray JA (ed) Climate Change and Microbiome Dynamics. Climate Change Management. Springer, Cham, pp 349–371. https://doi.org/10.1007/978-3-031-21079-2_18
Pawar A, Ismail S, Mundhe S, Patil VD (2015) Solubilization of insoluble zinc compounds by different microbial isolates in vitro condition. Int J Trop Agric 33:865–869
Premachandra GS, Saneoka H, Fujita K, Ogata S (1990) Cell membrane stability and leaf water relations as affected by phosphorus nutrition under water stress in maize. Soil Sci Plant Nutr 36:661–666. https://doi.org/10.1080/00380768.1990.10416803
Priyanka N, Geetha N, Manish T, Sahi S, Venkatachalam P (2021) Zinc oxide nanocatalyst mediates cadmium and lead toxicity tolerance mechanism by differential regulation of photosynthetic machinery and antioxidant enzymes level in cotton seedlings. Toxicol Rep 8:295–302. https://doi.org/10.1016/j.toxrep.2021.01.016
Rady MM, Alshallash KS, Desoky E-SM, Taie HA, Mohamed IA, El-Badri AM, Howladar SM, AbdelKhalik A (2023) Synergistic effect of trans-zeatin and silymarin on mitigation of cadmium stress in chili pepper through modulating the activity of antioxidant enzymes and gene expressions. J Appl Res Med 35:100498. https://doi.org/10.1016/j.jarmap.2023.100498
Rady MM, EL-Yazal MA, Taie HA, Ahmed SM (2021) Physiological and biochemical responses of wheat (Triticum aestivum L.) plants to polyamines under lead stress. Innovare J Agric Sci 9:1–10. https://doi.org/10.22159/ijags.2021.v9i1.40687
Rahman SU, Nawaz MF, Gul S, Yasin G, Hussain B, Li Y, Cheng H (2022) State-of-the-art OMICS strategies against toxic effects of heavy metals in plants: a review. Ecotoxicol Environ Saf 242:113952. https://doi.org/10.1016/j.ecoenv.2022.113952
Rajkumar M, Ma Y, Freitas H (2013) Improvement of Ni phytostabilization by inoculation of Ni resistant Bacillus megaterium SR28C. J Environ Manag 128:973–980. https://doi.org/10.1016/j.jenvman.2013.07.001
Rao MV, Paliyath G, Ormrod DP (1996) Ultraviolet-B- and ozone induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiol 110:125–136. https://doi.org/10.1104/pp.110.1.125
Rizvi A, Khan MS (2018) Heavy metal induced oxidative damage and root morphology alterations of maize (Zea mays L.) plants and stress mitigation by metal tolerant nitrogen fixing Azotobacter chroococcum. Ecotoxicol Environ Saf 157:9–20. https://doi.org/10.1016/j.ecoenv.2018.03.063
Rodríguez-Ruiz M, González-Gordo S, Cañas A, Campos MJ, Paradela A, Corpas FJ, Palma JM (2019) Sweet pepper (Capsicum annuum L.) fruits contain an atypical peroxisomal catalase that is modulated by reactive oxygen and nitrogen species. Antioxidants 8:374. https://doi.org/10.3390/antiox8090374
Santosh K (2013) Genetic variability studies in bell pepper (Capsicum annuum L.). Asian J Hort 8:280–284
Sapre S, Gontia-Mishra I, Tiwari S (2018) Klebsiella sp. confers enhanced tolerance to salinity and plant growth promotion in oat seedlings (Avena sativa). Microbiol Res 206:25–32. https://doi.org/10.1016/j.micres.2017.09.009
Sarkar A, Ghosh PK, Pramanik K, Mitra S, Soren T, Pandey S, Mondal MH, Maiti TK (2018) A halotolerant Enterobacter sp. displaying ACC deaminase activity promotes rice seedling growth under salt stress. Res Microbiol 169:20–32. https://doi.org/10.1016/j.resmic.2017.08.005
Shaffique S, Khan MA, Alomrani SO, Injamum-Ul-Hoque M, Peter O, Imran M, Kang SM, Lee I (2023) Unlocking the potential of newly isolated phytohormone-producing bacterial strains for enhanced plant growth and stress tolerance. Plant Stress 10:100260. https://doi.org/10.1016/j.stress.2023.100260
Shahid M, Ameen F, Maheshwari HS, Ahmed B, AlNadhari S, Khan MS (2021) Colonization of Vigna radiata by a halotolerant bacterium Kosakonia sacchari improves the ionic balance, stressor metabolites, antioxidant status and yield under NaCl stress. Appl Soil Ecol 158:103809. https://doi.org/10.1016/j.apsoil.2020.103809
Shahid M, Singh UB, Khan MS, Singh P, Kumar R, Singh RN, Kumar A, Singh HV (2023) Bacterial ACC deaminase: Insights into enzymology, biochemistry, genetics, and potential role in amelioration of environmental stress in crop plants. Front Microbiol 14:1132770. https://doi.org/10.3389/fmicb.2023.1132770
Sharma RK, Devi S, dan Dhyani PP (2010) Comparative assessment of the toxic effects of copper and cypermethrin using seeds of Spinacia Oleracea L. plants. Trop Ecol 51:375–387.
Singh A, Mishra S, Choudhary M, Chandra P, Rai AK, Yadav RK, Sharma PC (2023) Rhizobacteria improve rice zinc nutrition in deficient soils. Rhizosphere 25:100646. https://doi.org/10.1016/j.rhisph.2022.100646
Sofy AR, Dawoud RA, Sofy MR, Mohamed HI, Hmed AA, El-Dougdoug NK (2020) Improving regulation of enzymatic and non-enzymatic antioxidants and stress-related gene stimulation in cucumber mosaic cucumovirus-infected cucumber plants treated with glycine betaine, chitosan and combination. Molecules. 25:2341. https://doi.org/10.3390/molecules25102341
Sorour AA, Khairy H, Zaghloul EH, Zaghloul HAH (2022) Microbe-plant interaction as a sustainable tool for mopping up heavy metal contaminated sites. BMC Microbiol 22:174. https://doi.org/10.1186/s12866-022-02587-x
Srivastava S, Srivastava S, Bist V, Awasthi S, Chauhan R, Chaudhry V, Singh PC, Dwivedi S, Niranjan A, Agrawal L, Chauhan PS, Tripathi RD, Nautiyal CS (2018) Chlorella vulgaris and Pseudomonas putida interaction modulates phosphate trafficking for reduced arsenic uptake in rice (Oryza sativa L.). J Hazard Mater 351:177–187. https://doi.org/10.1016/j.jhazmat.2018.02.039
Sun S, Xu X, Jiang X, Yue Y, Dai Y, Yang X, Xiu Q, Duan L, Zhao S (2023) Unveiling the neglected roles of chloride and sulfate in the removal of nitro compounds by sulfidated zero-valent iron/ferrous ion systems. ACS EST Water 3:1212–1222. https://doi.org/10.1021/acsestwater.2c00661.s001
Taie HAA, Seif El-Yazal MA, Ahmed SMA, Rady MM (2019) Polyamines modulate growth, antioxidant activity, and genomic DNA in heavy metal–stressed wheat plant. Environ Sci Pollut Res 26:22338–22350. https://doi.org/10.1007/s11356-019-05555-7
Tang Z, Wang HQ, Chen J, Chang JD, Zhao FJ (2023) Molecular mechanisms underlying the toxicity and detoxification of trace metals and metalloids in plants. J Integr Plant Biol 65:570–593. https://doi.org/10.1111/jipb.13440
Thiem D, Złoch M, Gadzała-Kopciuch R, Szymańska S, Baum C, Hrynkiewicz K (2018) Cadmium-induced changes in the production of siderophores by a plant growth promoting strain of Pseudomonas fulva. J Basic Microbiol 58:623–632. https://doi.org/10.1002/jobm.201800034
Topić Popović N, Kazazić SP, Bojanić K, Strunjak-Perović I, Čož-Rakovac R (2023) Sample preparation and culture condition effects on MALDI-TOF MS identification of bacteria: a review. Mass Spectrom Rev 42:1589–1603. https://doi.org/10.1002/mas.21739
Tripthi DK, Varma RK, Singh S, Sachan M, Guerriero G, Kushwaha BK, Bhardwaj S, Ramawat N, Sharma S, Singh VP, Prasad SM (2020) Silicon tackles butachlor toxicity in rice seedlings by regulating anatomical characteristics, ascorbate-glutathione cycle, proline metabolism and levels of nutrients. Sci Rep 10:14078. https://doi.org/10.1038/s41598-020-65124-8
Tsiasioti A, Tzanavaras PD (2023) Determination of glutathione and glutathione disulfide using liquid chromatography: A review on recent applications. Microchem J 193:109157. https://doi.org/10.1016/j.microc.2023.109157
Ur Rehman MZU, Zafar M, Waris AA, Rizwan M, Ali S, Sabir M, Usman M, Ayub MA, Ahmad Z (2020) Residual effects of frequently available organic amendments on cadmium bioavailability and accumulation in wheat. Chemosphere 244:125548. https://doi.org/10.1016/j.chemosphere.2019.125548
Vaid SK, Kumar B, Sharma A, Shukla AK, Srivastava PC (2014) Effect of zinc solubilizing bacteria on growth promotion and zinc nutrition of rice. J Soil Sci Plant Nutr 14:889–910. https://doi.org/10.4067/S0718-95162014005000071
Wang Q, Chen L, He LY, Sheng XF (2016) Increased biomass and reduced heavy metal accumulation of edible tissues of vegetable crops in the presence of plant growth-promoting Neorhizobium huautlense T1-17 and biochar. Agric Ecosyst Environ 228:9–18. https://doi.org/10.1016/j.agee.2016.05.006
Wu W, Chen W, Liu S, Wu J, Zhu Y, Qin L, Zhu B (2021) Beneficial relationships between endophytic bacteria and medicinal plants. Front Plant Sci 12:646146. https://doi.org/10.3389/fpls.2021.646146
Yin Y, Wang X, Hu Y, Li F, Cheng H (2023) Soil bacterial community structure in the habitats with different levels of heavy metal pollution at an abandoned polymetallic mine. J Hazard Mater 442:130063. https://doi.org/10.1016/j.jhazmat.2022.130063
Yu Y, Gui Y, Li Z, Jiang C, Guo J, Niu D (2022) Induced systemic resistance for improving plant immunity by beneficial microbes. Plants 11:386. https://doi.org/10.3390/plants11030386
Zainab N, Amna DBU, Javed MT, Afridi MS, Mukhtar T, Kamran MA, Ain QU, Khan AA, Ali J, Jatoi WN, Hussain Munis MF, Chaudhary HJ (2020) Deciphering metal toxicity responses of flax (Linum usitatissimum L.) with exopolysaccharide and ACC-deaminase producing bacteria in industrially contaminated soils. Plant Physiol Biochem 152:90–99. https://doi.org/10.1016/j.plaphy.2020.04.039
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This project was supported by Khalifa Center for Biotechnology and Genetic Engineering-UAEU (Grant number: 31R286), Abu Dhabi Award for Research Excellence-Department of Education and Knowledge (Grant number: 21S105), and UAEU program of Advanced Research (Grant number: 12S169).
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El-Saadony, M.T., Desoky, ES.M., El-Tarabily, K.A. et al. Exploiting the role of plant growth promoting rhizobacteria in reducing heavy metal toxicity of pepper (Capsicum annuum L.). Environ Sci Pollut Res 31, 27465–27484 (2024). https://doi.org/10.1007/s11356-024-32874-1
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DOI: https://doi.org/10.1007/s11356-024-32874-1