Synergistic Effect of Bacillus thuringiensis IAGS 199 and Putrescine on Alleviating Cadmium-Induced Phytotoxicity in Capsicum annum
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
RSP-2020/194
Researchers Supporting Project, King Saud University, Riyadh, Saudi Arabia
PubMed
33171611
PubMed Central
PMC7695146
DOI
10.3390/plants9111512
PII: plants9111512
Knihovny.cz E-zdroje
- Klíčová slova
- Capsicum annum, cadmium, growth, microbe, priming, putrescine,
- Publikační typ
- časopisecké články MeSH
Plant growth-promoting bacteria (PGPB) and putrescine (Put) have shown a promising role in the mitigation of abiotic stresses in plants. The present study was anticipated to elucidate the potential of Bacillus thuringiensis IAGS 199 and Put in mitigation of cadmium (Cd)-induced toxicity in Capsicum annum. Cadmium toxicity decreased growth, photosynthetic rate, gas exchange attributes and activity of antioxidant enzymes in C. annum seedlings. Moreover, higher levels of protein and non-protein bound thiols besides increased Cd contents were also observed in Cd-stressed plants. B. thuringiensis IAGS 199 and Put, alone or in combination, reduced electrolyte leakage (EL), hydrogen peroxide (H2O2) and malondialdehyde (MDA) level in treated plants. Synergistic effect of B. thuringiensis IAGS 199 and Put significantly enhanced the activity of stress-responsive enzymes including peroxidase (POD), ascorbate peroxidase (APX), catalase (CAT) and superoxide dismutase (SOD). Furthermore, Put and microbial interaction enhanced the amount of proline, soluble sugars, and total soluble proteins in C. annum plants grown in Cd-contaminated soil. Data obtained during the current study advocates that application of B. thuringiensis IAGS 199 and Put establish a synergistic role in the mitigation of Cd-induced stress through modulating physiochemical features of C. annum plants.
Department of Agronomy Faculty of Agriculture Gomal University Dera Ismail Khan 29050 Pakistan
Department of Agronomy The University of Haripur Haripur 22620 Pakistan
Department of Botany University of Narowal Narowal 51801 Pakistan
Vegetable research institute Guangdong Academy of Agriculture Science Guangzhou 510640 China
Zobrazit více v PubMed
Genchi G., Sinicropi M.S., Lauria G., Carocci A., Catalano A. The effects of cadmium toxicity. Int. J. Environ. Res. Public Health. 2020;17:3782. doi: 10.3390/ijerph17113782. PubMed DOI PMC
Lin Y.-F., Aarts M.G.M. The molecular mechanism of zinc and cadmium stress response in plants. Cell. Mol. Life Sci. 2012;69:3187–3206. doi: 10.1007/s00018-012-1089-z. PubMed DOI PMC
Fiaz K., Danish S., Younis U., Malik S.A., Raza Shah M.H., Niaz S. Drought impact on Pb/Cd toxicity remediated by biochar in Brassica campestris. J. Soil Sci. Plant Nutr. 2014;14:845–854. doi: 10.4067/S0718-95162014005000067. DOI
Ajmal Z., Usman M., Anastopoulos I., Qadeer A., Zhu R., Wakeel A., Dong R. Use of nano-/micro-magnetite for abatement of cadmium and lead contamination. J. Environ. Manag. 2020;264:110477. doi: 10.1016/j.jenvman.2020.110477. PubMed DOI
Liu M., Bi J., Liu X., Kang J., Korpelainen H., Niinemets Ü., Li C. Microstructural and physiological responses to cadmium stress under different nitrogen levels in Populus cathayana females and males. Tree Physiol. 2020;40:30–45. doi: 10.1093/treephys/tpz115. PubMed DOI
Lei G.J., Sun L., Sun Y., Zhu X.F., Li G.X., Zheng S.J. Jasmonic acid alleviates cadmium toxicity in Arabidopsis via suppression of cadmium uptake and translocation. J. Integr. Plant Biol. 2019;62:218–227. doi: 10.1111/jipb.12801. PubMed DOI
Nakbanpote W., Prasad M.N.V., Mongkhonsin B., Panitlertumpai N., Munjit R., Rattanapolsan L. Bio-Geotechnologies for Mine Site Rehabilitation. Elsevier; Amsterdam, The Netherlands: 2018. Strategies for Rehabilitation of Mine Waste/Leachate in Thailand; pp. 617–643.
Kubo K., Kobayashi H., Fujita M., Ota T., Minamiyama Y., Watanabe Y., Nakajima T., Shinano T. Varietal differences in the absorption and partitioning of cadmium in common wheat (Triticum aestivum L.) Environ. Exp. Bot. 2016;124:79–88. doi: 10.1016/j.envexpbot.2015.12.007. DOI
Santos M.C.D., Nascimento Y.M., Monteiro J.D., Alves B.E.B., Melo M.F., Paiva A.A.P., Pereira H.W.B., Medeiros L.G., Morais I.C., Neto J.C.F., et al. ATR-FTIR spectroscopy with chemometric algorithms of multivariate classification in the discrimination between healthy vs. dengue vs. chikungunya vs. zika clinical samples. Anal. Methods. 2018;10:1280–1285. doi: 10.1039/C7AY02784B. DOI
Kumar A. Toxicity of Heavy Metals to Legumes and Bioremediation. Springer; Wien, Austria: 2012. Role of plant-growth-promoting rhizobacteria in the management of cadmium-contaminated soil.
Abid M., Danish S., Zafar-ul-Hye M., Shaaban M., Iqbal M.M., Rehim A., Qayyum M.F., Naqqash M.N. Biochar increased photosynthetic and accessory pigments in tomato (Solanum lycopersicum L.) plants by reducing cadmium concentration under various irrigation waters. Environ. Sci. Pollut. Res. 2017;24:22111–22118. doi: 10.1007/s11356-017-9866-8. PubMed DOI
Younis U., Shah M.H.R., Danish S., Malik S.A., Ameer A. Biochar role in improving biometric and growth attributes of S. oleracea and T. corniculata under cadmium stress. Int. J. Biosci. 2014;5:84–90.
Khan H.A., Ziaf K., Amjad M., Iqbal Q. Exogenous Application of Polyamines Improves Germination and Early Seedling Growth of Hot Pepper. Chil. J. Agric. Res. 2012;72:429–433. doi: 10.4067/S0718-58392012000300018. DOI
Ahanger M.A., Aziz U., Alsahli A., Alyemeni M.N., Ahmad P. Combined Kinetin and Spermidine Treatments Ameliorate Growth and Photosynthetic Inhibition in Vigna angularis by Up-Regulating Antioxidant and Nitrogen Metabolism under Cadmium Stress. Biomolecules. 2020;10:147. doi: 10.3390/biom10010147. PubMed DOI PMC
Chiang H.C., Lo J.C., Yeh K.C. Genes associated with heavy metal tolerance and accumulation in Zn/Cd hyperaccumulator Arabidopsis halleri: A genomic survey with cDNA microarray. Environ. Sci. Technol. 2006;40:6792–6798. doi: 10.1021/es061432y. PubMed DOI
Huo L., Guo Z., Wang P., Zhang Z., Jia X., Sun Y., Sun X., Gong X., Ma F. MdATG8i functions positively in apple salt tolerance by maintaining photosynthetic ability and increasing the accumulation of arginine and polyamines. Environ. Exp. Bot. 2020;172 doi: 10.1016/j.envexpbot.2020.103989. DOI
Tang W., Newton R.J. Polyamines reduce salt-induced oxidative damage by increasing the activities of antioxidant enzymes and decreasing lipid peroxidation in Virginia pine. Plant Growth Regul. 2005;46:31–43. doi: 10.1007/s10725-005-6395-0. DOI
Fariduddin Q., Varshney P., Yusuf M., Ahmad A. Polyamines: Potent modulators of plant responses to stress. J. Plant Interact. 2013;8:1–16. doi: 10.1080/17429145.2012.716455. DOI
Zhao J.-L., Zhou L.-G., Wu J.-Y. Effects of biotic and abiotic elicitors on cell growth and tanshinone accumulation in Salvia miltiorrhiza cell cultures. Appl. Microbiol. Biotechnol. 2010;87:137–144. doi: 10.1007/s00253-010-2443-4. PubMed DOI
Danish S., Younis U., Akhtar N., Ameer A., Ijaz M., Nasreen S., Huma F., Sharif S., Ehsanullah M. Phosphorus solubilizing bacteria and rice straw biochar consequence on maize pigments synthesis. Int. J. Biosci. 2015;5:31–39. doi: 10.12692/ijb/5.12.31-39. DOI
Gupta A., Meyer J.M., Goel R. Development of heavy metal-resistant mutants of phosphate solubilizing Pseudomonas sp. NBRI 4014 and their characterization. Curr. Microbiol. 2002;45:323–327. doi: 10.1007/s00284-002-3762-1. PubMed DOI
Danish S., Zafar-ul-Hye M. Co-application of ACC-deaminase producing PGPR and timber-waste biochar improves pigments formation, growth and yield of wheat under drought stress. Sci. Rep. 2019;9 doi: 10.1038/s41598-019-42374-9. PubMed DOI PMC
Danish S., Kiran S., Fahad S., Ahmad N., Ali M.A., Tahir F.A., Rasheed M.K., Shahzad K., Li X., Wang D., et al. Alleviation of chromium toxicity in maize by Fe fortification and chromium tolerant ACC deaminase producing plant growth promoting rhizobacteria. Ecotoxicol. Environ. Saf. 2019;185:109706. doi: 10.1016/j.ecoenv.2019.109706. PubMed DOI
Danish S., Zafar-Ul-Hye M., Hussain S., Riaz M., Qayyum M.F. Mitigation of drought stress in maize through inoculation with drought tolerant ACC deaminase containing PGPR under axenic conditions. Pakistan J. Bot. 2020;52:49–60. doi: 10.30848/PJB2020-1(7). DOI
Danish S., Zafar-ul-Hye M., Fahad S., Saud S., Brtnicky M., Hammerschmiedt T., Datta R. Drought Stress Alleviation by ACC Deaminase Producing Achromobacter xylosoxidans and Enterobacter cloacae, with and without Timber Waste Biochar in Maize. Sustainability. 2020;12:6286. doi: 10.3390/su12156286. DOI
Danish S., Zafar-ul-Hye M., Mohsin F., Hussain M. ACC-deaminase producing plant growth promoting rhizobacteria and biochar mitigate adverse effects of drought stress on maize growth. PLoS ONE. 2020;15:e0230615. doi: 10.1371/journal.pone.0230615. PubMed DOI PMC
Zafar-ul-Hye M., Tahzeeb-ul-Hassan M., Abid M., Fahad S., Brtnicky M., Dokulilova T., Datta R., Danish S. Potential role of compost mixed biochar with rhizobacteria in mitigating lead toxicity in spinach. Sci. Rep. 2020;10:1–12. doi: 10.1038/s41598-020-69183-9. PubMed DOI PMC
Zafar-ul-hye M., Naeem M., Danish S., Khan M.J., Fahad S., Datta R., Brtnicky M., Kintl A., Hussain M.S., El-esawi M.A. Effect of Cadmium-Tolerant Rhizobacteria on Growth Attributes and Chlorophyll Contents of Bitter Gourd under Cadmium Toxicity. Plants. 2020;9:1386. doi: 10.3390/plants9101386. PubMed DOI PMC
Zafar-ul-Hye M., Danish S., Fahad S., Datta R., Abbas M.O., Rahi A.A., Brtnicky M., Holátko J., Tarar Z.H., Nasir M., et al. Alleviation of Cadmium Adverse Effects by Improving Nutrients Uptake in Bitter Gourd through Cadmium Tolerant Rhizobacteria. Environments. 2020;7:54. doi: 10.3390/environments7080054. DOI
Adnan M., Fahad S., Zamin M., Shah S., Mian I.A., Danish S., Zafar-ul-Hye M., Battaglia M.L., Naz R.M.M., Saeed B. Coupling phosphate-solubilizing bacteria with phosphorus supplements improve maize phosphorus acquisition and growth under lime induced salinity stress. Plants. 2020;9:900. doi: 10.3390/plants9070900. PubMed DOI PMC
Dhawi F. Plant Growth Promoting Rhizobacteria ({PGPR}) Regulated Phyto and Microbial Beneficial Protein Interactions. Open Life Sci. 2020;15:68–78. doi: 10.1515/biol-2020-0008. DOI
Mahmood A., Turgay O.C., Farooq M., Hayat R. Seed biopriming with plant growth promoting rhizobacteria: A review. Microbiol. Ecol. 2016;92:fiw112. doi: 10.1093/femsec/fiw112. PubMed DOI
Danish S., Zafar-ul-Hye M., Hussain M., Shaaban M., Núñez-delgado A. Rhizobacteria with ACC-Deaminase Activity Improve Nutrient Uptake, Chlorophyll Contents and Early Seedling Growth of Wheat under PEG- Induced Osmotic Stress. Int. J. Agric. Biol. 2019;21:1212–1220. doi: 10.17957/IJAB/15.1013. DOI
Naser H.M., Hanan E.-H., Elsheery N.I., Kalaji H.M. Effect of biofertilizers and putrescine amine on the physiological features and productivity of date palm (Phoenix dactylifera L.) grown on reclaimed-salinized soil. Trees. 2016;30:1149–1161. doi: 10.1007/s00468-016-1353-1. DOI
Etesami H. Bacterial mediated alleviation of heavy metal stress and decreased accumulation of metals in plant tissues: Mechanisms and future prospects. Ecotoxicol. Environ. Saf. 2018;147:175–191. doi: 10.1016/j.ecoenv.2017.08.032. PubMed DOI
Jebara S.H., Ayed S.A., Chiboub M., Fatnassi I.C., Saadani O., Abid G., Jebara M. Cadmium Toxicity and Tolerance in Plants. Elsevier; Amsterdam, The Netherlands: 2019. Phytoremediation of Cadmium-Contaminated Soils by Using Legumes Inoculated by Efficient and Cadmium-Resistant Plant Growth-Promoting Bacteria; pp. 479–493.
Abbas M., Anwar J., Zafar-ul-Hye M., Khan R.I., Saleem M., Rahi A.A., Danish S., Datta R. Effect of Seaweed Extract on Productivity and Quality Attributes of Four Onion Cultivars. Horticulturae. 2020;6:28. doi: 10.3390/horticulturae6020028. DOI
Izhar Shafi M., Adnan M., Fahad S., Wahid F., Khan A., Yue Z., Danish S., Zafar-ul-Hye M., Brtnicky M., Datta R. Application of Single Superphosphate with Humic Acid Improves the Growth, Yield and Phosphorus Uptake of Wheat (Triticum aestivum L.) in Calcareous Soil. Agronomy. 2020;10:1224. doi: 10.3390/agronomy10091224. DOI
Ullah A., Ali M., Shahzad K., Ahmad F., Iqbal S., Habib M., Rahman M., Ahmad S., Iqbal M., Danish S., et al. Impact of Seed Dressing and Soil Application of Potassium Humate on Cotton Plants Productivity and Fiber Quality. Plants. 2020;9:1444. doi: 10.3390/plants9111444. PubMed DOI PMC
Zarei T., Danish S. Effect of micronutrients foliar supplementation on the production and eminence of plum (Prunus domestica L.) Qual. Assur. Saf. Crop. Foods. 2020;12:32–40. doi: 10.15586/qas.v12iSP1.793. DOI
Rafiullah Khan M.J., Muhammad D., Fahad S., Adnan M., Wahid F., Alamri S., Khan F., Dawar K.M., Irshad I. Phosphorus Nutrient Management through Synchronization of Application Methods and Rates in Wheat and Maize Crops. Plants. 2020;9:1389. doi: 10.3390/plants9101389. PubMed DOI PMC
Agostinelli E., Arancia G., Dalla Vedova L., Belli F., Marra M., Salvi M., Toninello A. The biological functions of polyamine oxidation products by amine oxidases: Perspectives of clinical applications. Amino Acids. 2004;27:347–358. doi: 10.1007/s00726-004-0114-4. PubMed DOI
del Rio B., Linares D.M., Ladero V., Redruello B., Fernández M., Martin M.C., Alvarez M.A. Putrescine production via the agmatine deiminase pathway increases the growth of Lactococcus lactis and causes the alkalinization of the culture medium. Appl. Microbiol. Biotechnol. 2014;99:897–905. doi: 10.1007/s00253-014-6130-8. PubMed DOI
Gadd G.M. Microbial influence on metal mobility and application for bioremediation. Geoderma. 2004;122:109–119. doi: 10.1016/j.geoderma.2004.01.002. DOI
Babu A.G., Shea P.J., Sudhakar D., Jung I.-B., Oh B.-T. Potential use of Pseudomonas koreensis {AGB}-1 in association with Miscanthus sinensis to remediate heavy metal(loid)-contaminated mining site soil. J. Environ. Manage. 2015;151:160–166. doi: 10.1016/j.jenvman.2014.12.045. PubMed DOI
Harzalli Jebara S., Fatnassi I.C., Ayed S.A., Saadani O., Chiboub M., Abid G., Jebara M. Potentialities and Limit of Legume-Plant Growth Promoting Bacteria Symbioses Use in Phytoremediation of Heavy Metal Contaminated Soils. Int. J. Plant Biol. 2017;5:1077.
Mishra J., Singh R., Arora N.K. Alleviation of Heavy Metal Stress in Plants and Remediation of Soil by Rhizosphere Microorganisms. Front. Microbiol. 2017;8 doi: 10.3389/fmicb.2017.01706. PubMed DOI PMC
Sun L.-N., Zhang Y.-F., He L.-Y., Chen Z.-J., Wang Q.-Y., Qian M., Sheng X.-F. Genetic diversity and characterization of heavy metal-resistant-endophytic bacteria from two copper-tolerant plant species on copper mine wasteland. Bioresour. Technol. 2010;101:501–509. doi: 10.1016/j.biortech.2009.08.011. PubMed DOI
Sharma R.K., Archana G. Cadmium minimization in food crops by cadmium resistant plant growth promoting rhizobacteria. Appl. Soil Ecol. 2016;107:66–78. doi: 10.1016/j.apsoil.2016.05.009. DOI
Li Y., Pang H.-D., He L.-Y., Wang Q., Sheng X.-F. Cd immobilization and reduced tissue Cd accumulation of rice (Oryza sativa wuyun-23) in the presence of heavy metal-resistant bacteria. Ecotoxicol. Environ. Saf. 2017;138:56–63. doi: 10.1016/j.ecoenv.2016.12.024. PubMed DOI
Silveira M.L.A., Alleoni L.R.F., Guilherme L.R.G. Biosolids and heavy metals in soils. Sci. Agric. 2003;60:793–806. doi: 10.1590/S0103-90162003000400029. DOI
Madhaiyan M., Poonguzhali S., Sa T. Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L.) Chemosphere. 2007;69:220–228. doi: 10.1016/j.chemosphere.2007.04.017. PubMed DOI
Lin X., Mou R., Cao Z., Xu P., Wu X., Zhu Z., Chen M. Characterization of cadmium-resistant bacteria and their potential for reducing accumulation of cadmium in rice grains. Sci. Total Environ. 2016;569–570:97–104. doi: 10.1016/j.scitotenv.2016.06.121. PubMed DOI
Park J.H., Bolan N., Megharaj M., Naidu R. Isolation of phosphate solubilizing bacteria and their potential for lead immobilization in soil. J. Hazard. Mater. 2011;185:829–836. doi: 10.1016/j.jhazmat.2010.09.095. PubMed DOI
Chen H., Cutright T.J. Preliminary Evaluation of Microbially Mediated Precipitation of Cadmium, Chromium, and Nickel by Rhizosphere Consortium. J. Environ. Eng. 2003;129:4–9. doi: 10.1061/(ASCE)0733-9372(2003)129:1(4). DOI
Hsu Y.T., Kao C.H. Cadmium-induced oxidative damage in rice leaves is reduced by polyamines. Plant Soil. 2007;291:27–37. doi: 10.1007/s11104-006-9171-7. DOI
Groppa M.D., Tomaro M.L., Benavides M.P. Polyamines and heavy metal stress: The antioxidant behavior of spermine in cadmium- and copper-treated wheat leaves. BioMetals. 2006;20:185–195. doi: 10.1007/s10534-006-9026-y. PubMed DOI
Soudek P., Ursu M., Petrová Š., Vaněk T. Improving crop tolerance to heavy metal stress by polyamine application. Food Chem. 2016;213:223–229. doi: 10.1016/j.foodchem.2016.06.087. PubMed DOI
Sobkowiak R., Deckert J. The effect of cadmium on cell cycle control in suspension culture cells of soybean. Acta Physiol. Plant. 2004;26:335–344. doi: 10.1007/s11738-004-0023-x. DOI
Zeid I.M., Shedeed Z.A. Response of alfalfa to putrescine treatment under drought stress. Biol. Plant. 2006;50:635–640. doi: 10.1007/s10535-006-0099-9. DOI
Zhao Y., Song X., Zhong D.B., Yu L., Yu X. γ-Aminobutyric acid (GABA) regulates lipid production and cadmium uptake by Monoraphidium sp. QLY-1 under cadmium stress. Bioresour. Technol. 2020;297:122500. doi: 10.1016/j.biortech.2019.122500. PubMed DOI
Zhang Q., Liu X., Zhang Z., Liu N., Li D., Hu L. Melatonin Improved Waterlogging Tolerance in Alfalfa (Medicago sativa) by Reprogramming Polyamine and Ethylene Metabolism. Front. Plant Sci. 2019;10 doi: 10.3389/fpls.2019.00044. PubMed DOI PMC
Vuosku J., Karppinen K., Muilu-Mäkelä R., Kusano T., Sagor G.H.M., Avia K., Alakärppä E., Kestilä J., Suokas M., Nickolov K., et al. Scots pine aminopropyltransferases shed new light on evolution of the polyamine biosynthesis pathway in seed plants. Ann. Bot. 2018;121:1243–1256. doi: 10.1093/aob/mcy012. PubMed DOI PMC
Banerjee A., Samanta S., Roychoudhury A. Spermine ameliorates prolonged fluoride toxicity in soil-grown rice seedlings by activating the antioxidant machinery and glyoxalase system. Ecotoxicol. Environ. Saf. 2020;189:109737. doi: 10.1016/j.ecoenv.2019.109737. PubMed DOI
Liu K., Fu H., Bei Q., Luan S. Inward Potassium Channel in Guard Cells As a Target for Polyamine Regulation of Stomatal Movements. Plant Physiol. 2000;124:1315–1326. doi: 10.1104/pp.124.3.1315. PubMed DOI PMC
Cui J., Pottosin I., Lamade E., Tcherkez G. What is the role of putrescine accumulated under potassium deficiency? Plant, Cell Environ. 2020;43:1331–1347. doi: 10.1111/pce.13740. PubMed DOI
Rahdari P., Hoseini S.M. Roll of Poly Amines (Spermidine and Putrescine) on Protein, Chlorophyll and Phenolic Compounds in Wheat (Triticum aestivum L.) under Salinity Stress. J Nov. Appl Sci. 2013;2:746–751.
Larbi A., Kchaou H., Gaaliche B., Gargouri K., Boulal H., Morales F. Supplementary potassium and calcium improves salt tolerance in olive plants. Sci. Hortic. (Amsterdam) 2020;260:108912. doi: 10.1016/j.scienta.2019.108912. DOI
Shi Y., Pu R., Guo L., Man J., Shang B., Ou X., Dai C., Liu P., Cui X., Ye Y. Formula fertilization of nitrogen and potassium fertilizers reduces cadmium accumulation in Panax notoginseng. Arch. Agron. Soil Sci. 2019;66:343–357. doi: 10.1080/03650340.2019.1616176. DOI
Marschner H. Mineral Nutrition of Higher Plants. 2nd ed. Academic Press; London, UK: 1995.
Rady M.M., El-Yazal M.A.S., Taie H.A.A., Ahmed S.M.A. Response of wheat growth and productivity to exogenous polyamines under lead stress. J. Crop Sci. Biotechnol. 2016;19:363–371. doi: 10.1007/s12892-016-0041-4. DOI
Armada E., Roldán A., Azcon R. Differential Activity of Autochthonous Bacteria in Controlling Drought Stress in Native Lavandula and Salvia Plants Species Under Drought Conditions in Natural Arid Soil. Microb. Ecol. 2014;67:410–420. doi: 10.1007/s00248-013-0326-9. PubMed DOI
Huda K.M.K., Banu M.S.A., Garg B., Tula S., Tuteja R., Tuteja N. OsACA6, a P-type IIB Ca2+ATPase promotes salinity and drought stress tolerance in tobacco by ROS scavenging and enhancing the expression of stress-responsive genes. Plant J. 2013;76:997–1015. doi: 10.1111/tpj.12352. PubMed DOI
Li R., Shen H., Li M. Effects of acid stress on the contents of proline and putrescine in several forest trees. J. Nanjing For. Univ. 1995;9:88–93.
Hassan N., Ebeed H., Aljaarany A. Exogenous application of spermine and putrescine mitigate adversities of drought stress in wheat by protecting membranes and chloroplast ultra-structure. Physiol. Mol. Biol. Plants. 2020;26:233–245. doi: 10.1007/s12298-019-00744-7. PubMed DOI PMC
Pál M., Szalai G., Janda T. Speculation: Polyamines are important in abiotic stress signaling. Plant Sci. 2015;237:16–23. doi: 10.1016/j.plantsci.2015.05.003. PubMed DOI
Szalai G., Janda K., Darkó É., Janda T., Peeva V., Pál M. Comparative analysis of polyamine metabolism in wheat and maize plants. Plant Physiol. Biochem. 2017;112:239–250. doi: 10.1016/j.plaphy.2017.01.012. PubMed DOI
Sharma S.S., Dietz K.J. The Significance of Amino Acids and Amino Acid derived Molecules in Plant Responses and Adaptation to Heavy Metal Stress. J. Exp. Bot. 2006;57:711–726. doi: 10.1093/jxb/erj073. PubMed DOI
Sun X., Wang Y., Tan J. Effects of exogenous putrescine and D-Arg on physiological and biochemical indices of anthurium under chilling stress. Jiangsu J. Agric. Sci. 2018;34:152–157.
Mohammadi H., Ghorbanpour M., Brestic M. Exogenous putrescine changes redox regulations and essential oil constituents in field-grown Thymus vulgaris L. under well-watered and drought stress conditions. Ind. Crops Prod. 2018;122:119–132. doi: 10.1016/j.indcrop.2018.05.064. DOI
Kuramshina Z.M., Smirnova Y.V., Khairullin R.M. Increasing Triticum aestivum tolerance to cadmium stress through endophytic strains of Bacillus subtilis. Russ. J. Plant Physiol. 2016;63:636–644. doi: 10.1134/S1021443716050083. DOI
Jan M., Shah G., Masood S., Shinwari K.I., Hameed R., Rha E.S., Jamil M. Bacillus Cereus Enhanced Phytoremediation Ability of Rice Seedlings under Cadmium Toxicity. Res. Int. 2019;2019:1–12. doi: 10.1155/2019/8134651. PubMed DOI PMC
Rizwan M., Ali S., Adrees M., Rizvi H., Zia-ur-Rehman M., Hannan F., Qayyum M.F., Hafeez F., Ok Y.S. Cadmium stress in rice: Toxic effects, tolerance mechanisms, and management: A critical review. Environ. Sci. Pollut. Res. 2016;23:17859–17879. doi: 10.1007/s11356-016-6436-4. PubMed DOI
Singh R.K., Anandhan S., Singh S., Patade V.Y., Ahmed Z., Pande V. Metallothionein-like gene from Cicer microphyllum is regulated by multiple abiotic stresses. Protoplasma. 2010;248:839–847. doi: 10.1007/s00709-010-0249-y. PubMed DOI
Emamverdian A., Ding Y., Mokhberdoran F., Xie Y. Heavy Metal Stress and Some Mechanisms of Plant Defense Response. Sci. World J. 2015;2015:1–18. doi: 10.1155/2015/756120. PubMed DOI PMC
Sofia C., Sofia P., Ana L., Etelvina F. Toxicity of Heavy Metals to Legumes and Bioremediation. Springer; Berlin/Heidelberg, Germany: 2012. The Influence of Glutathione on the Tolerance of Rhizobium leguminosarum to Cadmium; pp. 89–100.
Cetin S.C., Karaca A., Kizilkaya R., Turgay O.C. Soil Biology. Springer; Berlin/Heidelberg, Germany: 2011. Role of Plant Growth Promoting Bacteria and Fungi in Heavy Metal Detoxification; pp. 369–388.
Aly A.A., Mohamed A.A. The impact of copper ion on growth, thiol compounds and lipid peroxidation in two maize cultivars (Zea mays L.) grown in vitro. Aust. J. Crop Sci. 2012;6:541–549.
Nagalakshmi N., Prasad M.N. V Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci. 2001;160:291–299. doi: 10.1016/S0168-9452(00)00392-7. PubMed DOI
Awasthi S., Chauhan R., Srivastava S., Tripathi R.D. The Journey of Arsenic from Soil to Grain in Rice. Front. Plant Sci. 2017;8 doi: 10.3389/fpls.2017.01007. PubMed DOI PMC
Awasthi S., Chauhan R., Dwivedi S., Srivastava S., Srivastava S., Tripathi R.D. 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. 2018;150:115–126. doi: 10.1016/j.envexpbot.2018.03.001. DOI
Hassan T.U., Bano A. Effects of Putrescine Foliar Spray on Nutrient Accumulation, Physiology, and Yield of Wheat. Commun. Soil Sci. Plant Anal. 2016;47:931–940. doi: 10.1080/00103624.2016.1165828. DOI
Ahmad I., Akhtar M.J., Zahir Z.A., Naveed M., Mitter B., Sessitsch A. Cadmium-tolerant bacteria induce metal stress tolerance in cereals. Environ. Sci. Pollut. Res. 2014;21:11054–11065. doi: 10.1007/s11356-014-3010-9. PubMed DOI
Zafar-ul-Hye M., Shahjahan A., Danish S., Abid M., Qayyum M.F. Mitigation of cadmium toxicity induced stress in wheat by ACC-deaminase containing PGPR isolated from cadmium polluted wheat rhizosphere. Pakistan J. Bot. 2018;50:1727–1734.
Glickmann E., Dessaux Y. A critical examination of the specificity of the Salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl. Environ. Microbiol. 1995;61:793–796. doi: 10.1128/AEM.61.2.793-796.1995. PubMed DOI PMC
Chen L., He L., Wang Q., Sheng X. Synergistic effects of plant growth-promoting Neorhizobium huautlense T1-17 and immobilizers on the growth and heavy metal accumulation of edible tissues of hot pepper. J. Hazard. Mater. 2016;312:123–131. doi: 10.1016/j.jhazmat.2016.03.042. PubMed DOI
Ebeed H.T., Hassan N.M., Aljarani A.M. Exogenous applications of Polyamines modulate drought responses in wheat through osmolytes accumulation, increasing free polyamine levels and regulation of polyamine biosynthetic genes. Plant Physiol. Biochem. 2017;118:438–448. doi: 10.1016/j.plaphy.2017.07.014. PubMed DOI
Anwaar S.A., Ali S., Ali S., Ishaque W., Farid M., Farooq M.A., Najeeb U., Abbas F., Sharif M. Silicon (Si) alleviates cotton (Gossypium hirsutum L.) from zinc (Zn) toxicity stress by limiting Zn uptake and oxidative damage. Environ. Sci. Pollut. Res. 2014;22:3441–3450. doi: 10.1007/s11356-014-3938-9. PubMed DOI
Lichtenthaler H.K. Methods in Enzymology. Elsevier; Amsterdam, The Netherlands: 1987. Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes; pp. 350–382.
Arnon D.I. Copper Enzymes in Isolated Chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol. 1949;24:1–15. doi: 10.1104/pp.24.1.1. PubMed DOI PMC
Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein dye binding. Anal. Biochem. 1976;72:248–254. doi: 10.1016/0003-2697(76)90527-3. PubMed DOI
Dubois M., Gilles K.A., Hamilton J.K., Rebers P.A., Smith F. Colorimetric Method for Determination of Sugars and Related Substances. Anal. Chem. 1956;28:350–356. doi: 10.1021/ac60111a017. DOI
Li W., Nguyen K.H., Chu H.D., Van Ha C., Watanabe Y., Osakabe Y., Leyva-González M.A., Sato M., Toyooka K., Voges L., et al. The karrikin receptor KAI2 promotes drought resistance in Arabidopsis thaliana. PLoS Genet. 2017;13:e1007076. doi: 10.1371/journal.pgen.1007076. PubMed DOI PMC
Dhindsa R.S., Plumb-Dhindsa P.L., Reid D.M. Leaf senescence and lipid peroxidation: Effects of some phytohormones, and scavengers of free radicals and singlet oxygen. Physiol. Plant. 1982;56:453–457. doi: 10.1111/j.1399-3054.1982.tb04539.x. DOI
Pütter J. Methods of Enzymatic Analysis. Elsevier; Amsterdam, The Netherlands: 1974. Peroxidases; pp. 685–690.
Aebi H. Methods in Enzymology. Volume 105. Academic Press Inc.; Cambridge, MA, USA: 1984. Catalase in vitro; pp. 121–126. PubMed
Nakano Y., Asada K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 1981;22:867–880. doi: 10.1093/oxfordjournals.pcp.a076232. DOI
Bates L.S., Waldren R.P., Teare I.D. Rapid determination of free proline for water-stress studies. Plant Soil. 1973;39:205–207. doi: 10.1007/BF00018060. DOI
Mattina M.J.I., Lannucci-Berger W., Musante C., White J.C. Concurrent plant uptake of heavy metals and persistent organic pollutants from soil. Environ. Pollut. 2003;124:375–378. doi: 10.1016/S0269-7491(03)00060-5. PubMed DOI
Sedlak J., Lindsay R.H. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal. Biochem. 1968;25:192–205. doi: 10.1016/0003-2697(68)90092-4. PubMed DOI
Antioxidant Defences under Hyperoxygenic and Hyperosmotic Conditions in Leaves of Two Lines of Maize with Differential Sensitivity to Drought. Plant Cell Physiol. 1993;34:1023–1028. doi: 10.1093/oxfordjournals.pcp.a078515. DOI
Steel R.G., Torrie J.H., Dickey D.A. Principles and Procedures of Statistics: A Biometrical Approach. 3rd ed. McGraw Hill Book International Co.; Singapore: 1997.