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Opportunities and challenges in the remediation of metal-contaminated soils by using tobacco (Nicotiana tabacum L.): a critical review

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Abstract

The successful phytoextraction of potentially toxic elements (PTEs) from polluted soils can be achieved by growing non-food and industrial crops. Tobacco (Nicotiana tabacum L.) is one of the main industrial crops and is widely grown in many countries. Tobacco can uptake high concentrations of PTEs especially in aboveground biomass without suffering from toxicity. This review highlighted the potential of tobacco for the phytoextraction of heavy metals and tolerance mechanisms under metal stress. Different management practices have been discussed which can enhance the potential of this plant for metal extraction. Finally, suitable options for the management/disposal of biomass enriched in excess metal have been elaborated to prevent secondary pollution.

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References

  • Abbas T, Rizwan M, Ali S, Adrees M, Rehman MZ, Qayyum MF, Ok YS, Murtaza G (2018) Effect of biochar on alleviation of cadmium toxicity in wheat (Triticum aestivum L.) grown on Cd-contaminated saline soil. Environ Sci Pollut Res 25:25668–25680

    Article  CAS  Google Scholar 

  • Adamo P, Agrelli D, Zampella M (2018) Chemical speciation to assess bioavailability, bioaccessibility and geochemical forms of potentially toxic metals (PTMs) in polluted soils. Chapter 9. In: De Vivo B, Belkin HE, Lima A (eds) Environmental geochemistry, site characterization, data analysis and case histories. Second Edition, Amsterdam, pp 153–194

  • Adrees M, Ali S, Rizwan M, Rehman MZ, Ibrahim M, Abbas F, Farid M, Qayyum MF, Irshad MK (2015a) Mechanisms of silicon-mediated alleviation of heavy metal toxicity in plants: a review. Ecotoxicol Environ Saf 119:186–197

    Article  CAS  Google Scholar 

  • Adrees M, Ali S, Iqbal M, Bharwana SA, Siddiqi Z, Farid M, Ali Q, Saeed R, Rizwan M (2015b) Mannitol alleviates chromium toxicity in wheat plants in relation to growth, yield, stimulation of anti-oxidative enzymes, oxidative stress and Cr uptake in sand and soil media. Ecotoxicol Environ Saf 122:1–8

    Article  CAS  Google Scholar 

  • Afshan S, Ali S, Bharwana SA, Rizwan M, Farid M, Abbas F, Ibrahim M, Mehmood MA, Abbasi GH (2015) Citric acid enhances the phytoextraction of chromium, plant growth, and photosynthesis by alleviating the oxidative damages in Brassica napus L. Environ Sci Pollut Res 22:11679–11689

    Article  CAS  Google Scholar 

  • Ahmad J, Ali AA, Baig MA, Iqbal M, Haq I, Qureshi MI (2019) Role of phytochelatins in cadmium stress tolerance in plants. In: Cadmium Toxicity and Tolerance in Plants. From Physiology to Remediation, pp 185–212

    Chapter  Google Scholar 

  • Aiken GR, Hsu-Kim H, Ryan JN (2011) Influence of dissolved organic matter on the environmental fate of metals, nanoparticles, and colloids. Environ Sci Technol 45:3196–4201

    Article  CAS  Google Scholar 

  • Akhtar T, Rehman MZ, Naeem A, Nawaz R, Ali S, Murtaza G, Maqsood MA, Azhar M, Khalid H, Rizwan M (2017) Photosynthesis and growth response of maize (Zea mays L.) hybrids exposed to cadmium stress. Environ Sci Pollut Res 24:5521–5529

    Article  CAS  Google Scholar 

  • Alburquerque JA, De La Fuente C, Bernal MP (2011) Improvement of soil quality after “alperujo” compost application to two contaminated soils characterised by differing heavy metal solubility. J Environ Manag 92:733–741

    Article  CAS  Google Scholar 

  • Ali S, Rizwan M, Noureen S, Anwar S, Ali B, Naveed M, Abd_Allah EF, Alqarawi AA, Ahmad P (2019) Combined use of biochar and zinc oxide nanoparticle foliar spray improved the plant growth and decreased the cadmium accumulation in rice (Oryza sativa L.) plant. Environ Sci Pollut Res 26:11288–11299

    Article  CAS  Google Scholar 

  • Alvarenga P, Gonçalves AP, Fernandes RM, De Varennes A, Vallini G, Duarte E, Cunha-Queda AC (2009a) Organic residues as immobilizing agents in aided phytostabilization:(I) effects on soil chemical characteristics. Chemos 74:1292–1300

    Article  CAS  Google Scholar 

  • Alvarenga P, Palma P, Gonçalves AP, Fernandes RM, De Varennes A, Vallini G, Duarte E, Cunha-Queda AC (2009b) Organic residues as immobilizing agents in aided phytostabilization:(II) effects on soil biochemical and ecotoxicological characteristics. Chemos 74:1301–1308

    Article  CAS  Google Scholar 

  • Álvarez-López V, Prieto-Fernández A, Janssen J, Herzig R, Vangronsveld J, Kidd PS (2016) Inoculation methods using Rhodococcus erythropolis strain P30 affects bacterial assisted phytoextraction capacity of Nicotiana tabacum. Int J Phytorem 18:406–415

    Article  CAS  Google Scholar 

  • Antoniadis V, Shaheen SM, Boersch J, Frohne T, Du Laing G, Rinklebe J (2017) Bioavailability and risk assessment of potentially toxic elements in garden edible vegetables and soils around a highly contaminated former mining area in Germany. J Environ Manag 186:192–200

    Article  CAS  Google Scholar 

  • Audet P, Charest C (2006) Effects of AM colonization on “wild tobacco” plants grown in zinc-contaminated soil. Mycorrhiz 16:277–283

    Article  CAS  Google Scholar 

  • Azhar M, Rehman MZ, Ali S, Qayyum MF, Naeem A, Ayub MA, ul Haq MA, Iqbal A, Rizwan M (2019) Comparative effectiveness of different biochars and conventional organic materials on growth, photosynthesis and cadmium accumulation in cereals. Chemosphere 227:72–81

    Article  CAS  Google Scholar 

  • Baker AJM, McGrath SP, Reeves RD, Smith JAC (2000) Metal hyper- accumulator plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils. In: Terry N, Banuelos G (eds) Phytoremediation of Contaminated Soil and Water. Lewis Publishers, Boca Raton, pp 85–107

    Google Scholar 

  • Bañuelos GS (2000) Factors influencing field phytoremediation of selenium-laden soils. CRC Press, Boca Raton, pp 41–60

    Google Scholar 

  • Barbafieri M, Tassi E (2011) Brassinosteroids for phytoremediation application. Springer 403-437

  • Barona A, Aranguiz I, Elıas A (2001) Metal associations in soils before and after EDTA extractive decontamination: implications for the effectiveness of further clean-up procedures. Environ Pollut 113:79–85

    Article  CAS  Google Scholar 

  • Bedini S, Pellegrino E, Avio L, Pellegrini S, Bazzoffi P, Argese E, Giovannetti M (2009) Changes in soil aggregation and glomalin-related soil protein content as affected by the arbuscular mycorrhizal fungal species Glomus mosseae and Glomus intraradices. Soil Biol Biochem 41:1491–1496

    Article  CAS  Google Scholar 

  • Beesley L, Moreno-Jiménez E, Gomez-Eyles JL (2010) Effects of biochar and greenwaste compost amendments on mobility, bioavailability and toxicity of inorganic and organic contaminants in a multi-element polluted soil. Environ Pollut 158:2282–2287

    Article  CAS  Google Scholar 

  • Bingham G (1986) Resolving environmental disputes. A decade of experience. Conversation Foundation, Washington DC, p 99

    Google Scholar 

  • Blaylock MJ, Salt DE, Dushenkov S, Zakharova O, Gussman C, Kapulnik Y, Ensley BD, Raskin I (1997) Enhanced accumulation of Pb in Indian mustard by soil-applied chelating agents. Environ Sci Technol 31:860–865

    Article  Google Scholar 

  • Bluemlein K, Klimm E, Raab A, Feldmann J (2009) Selenite enhances arsenate toxicity in Thunbergia alata. Environ Chem 6:486–494

    Article  CAS  Google Scholar 

  • Bolan NS, Duraisamy VP (2003) Role of inorganic and organic soil amendments on immobilisation and phytoavailability of heavy metals: a review involving specific case studies. Soil Res 41:533–555

    Article  CAS  Google Scholar 

  • Bolan N, Kunhikrishnan A, Thangarajan R, Kumpiene J, Park J, Makino T, Kirkham MB, Scheckel K (2014) Remediation of heavy metal (loid) s contaminated soils–to mobilize or to immobilize? J Hazard Mater 266:141–166

    Article  CAS  Google Scholar 

  • Boonyapookana B, Parkpian P, Techapinyawat S, DeLaune RD, Jugsujinda A (2005) Phytoaccumulation of lead by sunflower (Helianthus annuus), tobacco (Nicotiana tabacum), and vetiver (Vetiveria zizanioides). J Environ Sci Health A 40:117–137

    Article  CAS  Google Scholar 

  • Boyter MJ, Brummer JE, Leininger WC (2009) Growth and metal accumulation of Geyer and mountain willow grown in topsoil versus amended mine tailings. Water Air Soil Pollut 198:17–29

    Article  CAS  Google Scholar 

  • Brown SL, Chaney RL, Angle JS, Ryan JA (1998) The phytoavailability of cadmium to lettuce in long-term biosolids-amended soils. J Environ Qual 27:1071–1078

    Article  CAS  Google Scholar 

  • Bukhari SA, Shang S, Zhang M, Zheng W, Zhang G, Wang TZ, Shamsi IH, Wu F (2015) Genome-wide identification of chromium stress-responsive micro RNAs and their target genes in tobacco (Nicotiana tabacum) roots. Environ Toxicol Chem 34:2573–2582

    Article  CAS  Google Scholar 

  • Burges A, Alkorta I, Epelde L, Garbisu C (2018) From phytoremediation of soil contaminants to phytomanagement of ecosystem services in metal contaminated sites. Int J Phytoreme 20:384–397

    Article  CAS  Google Scholar 

  • Burklew CE, Ashlock J, Winfrey WB, Zhang B (2012) Effects of aluminum oxide nanoparticles on the growth, development, and microRNA expression of tobacco (Nicotiana tabacum). PLoS One 7:e34783

    Article  CAS  Google Scholar 

  • Burzyński M, Kłobus G (2004) Changes of photosynthetic parameters in cucumber leaves under Cu, Cd, and Pb stress. Photosynt 42:505–510

    Article  CAS  Google Scholar 

  • Cartes P, Jara AA, Pinilla L, Rosas A, Mora ML (2010) Selenium improves the antioxidant ability against aluminium-induced oxidative stress in ryegrass roots. Ann Appl Biol 156:297–307

    Article  CAS  Google Scholar 

  • Chen H, Cutright T (2001) EDTA and HEDTA effects on Cd, Cr, and Ni uptake by Helianthus annuus. Chemos 45:21–28

    Article  CAS  Google Scholar 

  • Chen YX, Lin Q, Luo YM, He YF, Zhen SJ, Yu YL, Tian GM, Wong MH (2003) The role of citric acid on the phytoremediation of heavy metal contaminated soil. Chemos 50:807–811

    Article  CAS  Google Scholar 

  • Chen TF, Zheng WJ, Wong YS, Yang F (2008) Selenium-induced changes in activities of antioxidant enzymes and content of photosynthetic pigments in Spirulina platensis. J Integr Plant Biol 50:40–48

    Article  CAS  Google Scholar 

  • Cheng J, Li Y, Gao W, Chen Y, Pan W, Lee X, Tang Y (2018) Effects of biochar on Cd and Pb mobility and microbial community composition in a calcareous soil planted with tobacco. Biol Fertil Soils 54:373–383

    Article  CAS  Google Scholar 

  • Cherian S, Oliveira MM (2005) Transgenic plants in phytoremediation: recent advances and new possibilities. Environ Sci Technol 39:9377–9390

    Article  CAS  Google Scholar 

  • Chiang PN, Wang MK, Chiu CY, Chou SY (2006) Effects of cadmium amendments on low-molecular-weight organic acid exudates in rhizosphere soils of tobacco and sunflower. Environ Toxicol: An Int J 21:479–488

    Article  CAS  Google Scholar 

  • Chiu KK, Ye ZH, Wong MH (2006) Growth of Vetiveria zizanioides and Phragmities australis on Pb/Zn and Cu mine tailings amended with manure compost and sewage sludge: a greenhouse study. Bioresour Technol 97:158–170

    Article  CAS  Google Scholar 

  • Choi YE, Harada E (2005) Roles of calcium and cadmium on Cd-containing intra-and extracellular formation of Ca crystals in tobacco. J Plant Biol 48:113–119

    Article  CAS  Google Scholar 

  • Choi YE, Harada E, Wada M, Tsuboi H, Morita Y, Kusano T, Sano H (2001) Detoxification of cadmium in tobacco plants: formation and active excretion of crystals containing cadmium and calcium through trichomes. Planta 213:45–50

    Article  CAS  Google Scholar 

  • Christeller JT (1981) The effects of bivalent cations on ribulose bisphosphate carboxylase/oxygenase. Biochem J 193:839–844

    Article  CAS  Google Scholar 

  • Clarke BB, Brennan E (1989) Differential cadmium accumulation and phytotoxicity in sixteen tobacco cultivars. Japca 39:1319–1322

    Article  CAS  Google Scholar 

  • Clemens S, Palmgren MG, Krämer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315

    Article  CAS  Google Scholar 

  • Clemente R, Bernal MP (2006) Fractionation of heavy metals and distribution of organic carbon in two contaminated soils amended with humic acids. Chemos 64:1264–1273

    Article  CAS  Google Scholar 

  • Clemente R, Walker DJ, Bernal MP (2005) Uptake of heavy metals and As by Brassica juncea grown in a contaminated soil in Aznalcóllar (Spain): the effect of soil amendments. Environ Pollut 138:46–58

    Article  CAS  Google Scholar 

  • Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    Article  CAS  Google Scholar 

  • Cristaldi A, Conti GO, Jho EH, Zuccarello P, Grasso A, Copat C, Ferrante M (2017) Phytoremediation of contaminated soils by heavy metals and PAHs. A brief review Environ Technol Innov 8:309–326

    Article  Google Scholar 

  • Cui L, Pan G, Li L, Yan J, Zhang A, Bian R, Chang A (2012) The reduction of wheat Cd uptake in contaminated soil via biochar amendment: a two-year field experiment. Biores 7:5666–5676

    Article  Google Scholar 

  • Cvetanovska L, Klincharska-Jovanovska I, Dimeska G, Srbinoska M, Cvetanovska A (2010) Anatomic and physiological disorder after intoxication with heavy metals in tobacco (Nicotiana tabacum L.). Biotechnol Biotechnol Equip 24:4–9

    Article  Google Scholar 

  • Cvjetko P, Zovko M, Štefanić PP, Biba R, Tkalec M, Domijan AM, Vrček IV, Letofsky-Papst I, Šikić S, Balen B (2018) Phytotoxic effects of silver nanoparticles in tobacco plants. Environ Sci Pollut Res 25:5590–5602

    Article  CAS  Google Scholar 

  • Davies FT Jr, Puryear JD, Newton RJ, Egilla JN, Grossi JA (2001) Mycorrhizal fungi enhance accumulation and tolerance of chromium in sunflower (Helianthus annuus). J Plant Physiol 158:777–786

    Article  CAS  Google Scholar 

  • Davies FT Jr, Puryear JD, Newton RJ, Egilla JN, Saraiva Grossi JA (2002) Mycorrhizal fungi increase chromium uptake by sunflower plants: influence on tissue mineral concentration, growth, and gas exchange. J Plant Nutr 25:2389–2407

    Article  CAS  Google Scholar 

  • Davis RD (1984) Cadmium-a complex environmental problem. Part II. Cadmium in sludges used as fertilizer. Exper 40:117–126

    CAS  Google Scholar 

  • Degola F, Fattorini L, Bona E, Sprimuto CT, Argese E, Berta G, di Toppi LS (2015) The symbiosis between Nicotiana tabacum and the endomycorrhizal fungus Funneliformis mosseae increases the plant glutathione level and decreases leaf cadmium and root arsenic contents. Plant Physiol Biochem 92:11–18

    Article  CAS  Google Scholar 

  • Dmitriev AP (2003) Signal molecules for plant defense responses to biotic stress. Russ J Plant Physiol 50:417–425

    Article  CAS  Google Scholar 

  • Dobrikova AG (2017) Signaling molecules in plants: exogenous application. Acta Sci Agri 1:38–41

    Google Scholar 

  • Doganlar ZB (2012) Physiological and genetic responses to pesticide mixture treatment of Veronica beccabunga. Water Air Soil Pollut 223:6201–6212

    Article  CAS  Google Scholar 

  • Doroszewska T, Berbeć A (2004) Variation for cadmium uptake among Nicotiana species. Genetic Res Crop Evol 51:323–333

    Article  CAS  Google Scholar 

  • Drake EN (2006) Cancer chemoprevention: selenium as a prooxidant, not an antioxidant. Medical Hypoth 67:318–322

    Article  CAS  Google Scholar 

  • Drazkiewicz M (1994) Chlorophyllase: occurrence, functions, mechanism of action, effects of external and internal factors. Photosyn 30:321–331

  • Duarte B, Delgado M, Caçador I (2007) The role of citric acid in cadmium and nickel uptake and translocation, in Halimione portulacoides. Chemos 69:836–840

    Article  CAS  Google Scholar 

  • Duri LG, Fiorentino N, Cozzolino E, Ottaiano L, Agrelli D, Fagnano M (2018) Bioassays for evaluation of sanitary risks from food crops cultivated in potentially contaminated sites. Ital J Agron 13:45–52

    Google Scholar 

  • Ebbs S, Leonard W (2001) Alteration of selenium transport and volatilization in barley (Hordeum vulgare) by arsenic. J Plant Physiol 158:1231–1233

    Article  CAS  Google Scholar 

  • Erdem H, Kınay A, Gunal E, Yaban H, Tutus Y (2017) The effects of biochar application on cadmium uptake of tobacco. Carpatian J Env Sci 12:447–456

    Google Scholar 

  • Evangelou MW, Daghan H, Schaeffer A (2004) The influence of humic acids on the phytoextraction of cadmium from soil. Chemos 57:207–213

    Article  CAS  Google Scholar 

  • Evangelou E, Kyzas PA, Trikalinos TA (2005) Comparison of the diagnostic accuracy of lymphatic endothelium markers: Bayesian approach. Mod Pathol 18:1490–1497

    Article  CAS  Google Scholar 

  • Evangelou MW, Ebel M, Schaeffer A (2006) Evaluation of the effect of small organic acids on phytoextraction of Cu and Pb from soil with tobacco Nicotiana tabacum. Chemos 63:996–1004

    Article  CAS  Google Scholar 

  • Evangelou MW, Bauer U, Ebel M, Schaeffer A (2007a) The influence of EDDS and EDTA on the uptake of heavy metals of Cd and Cu from soil with tobacco Nicotiana tabacum. Chemos 68:345–353

    Article  CAS  Google Scholar 

  • Evangelou MW, Ebel M, Schaeffer A (2007b) Tobacco (Nicotiana tabacum) a potent phytoremediator. Terrest Aquatic Environ Toxicol 1:46–53

    Google Scholar 

  • Facknath S, Lalljee B (2000) Allelopathic strategies for eco-friendly crop protection. InAllelopathy in Ecological Agriculture and Forestry. Springer, Dordrecht, pp 33–46

    Book  Google Scholar 

  • Fagnano M (2018) Definition of a site as contaminated: problems related to agricultural soils. Ital J Agron 13:1–5

    Google Scholar 

  • Farahat E, Linderholm HW (2015) The effect of long-term wastewater irrigation on accumulation and transfer of heavy metals in Cupressus sempervirens leaves and adjacent soils. Sci Total Environ 512:1–7

    Article  CAS  Google Scholar 

  • Fargasova A, Pastierová J, Svetková K (2006) Effect of Se-metal pair combinations (Cd, Zn, Cu, Pb) on photosynthetic pigments production and metal accumulation in Sinapis alba L. seedlings. Plant Soil Environ 52:8–15

    Article  CAS  Google Scholar 

  • Fässler E, Robinson BH, Stauffer W, Gupta SK, Papritz A, Schulin R (2010) Phytomanagement of metal-contaminated agricultural land using sunflower, maize and tobacco. Agric Ecosyst Environ 136:49–58

    Article  CAS  Google Scholar 

  • Feng X, Liu W, Sehar S, Zheng W, Zhang G, Wu F (2018) Application of sulfur fertilizer reduces cadmium accumulation and toxicity in tobacco seedlings (Nicotiana tabacum). Plant Growth Rregul 85:165–170

    Article  CAS  Google Scholar 

  • Fernández-Martínez M, Vicca S, Janssens IA, Sardans J, Luyssaert S, Campioli M, Chapin FS III, Ciais P, Malhi Y, Obersteiner M, Papale D (2014) Nutrient availability as the key regulator of global forest carbon balance. Nat Clim Chang 4:471–476

    Article  CAS  Google Scholar 

  • Filek M, Zembala M, Hartikainen H, Miszalski Z, Kornaś A, Wietecka-Posłuszny R, Walas P (2009) Changes in wheat plastid membrane properties induced by cadmium and selenium in presence/absence of 2, 4-dichlorophenoxyacetic acid. Plant Cell Tissue Org Cult 96:19–28

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875

    Article  CAS  Google Scholar 

  • Frazier TP, Burklew CE, Zhang B (2014) Titanium dioxide nanoparticles affect the growth and microRNA expression of tobacco (Nicotiana tabacum). Func Integ Genom 14:75–83

    Article  CAS  Google Scholar 

  • Freeman JL, Persans MW, Nieman K, Albrecht C, Peer W, Pickering IJ, Salt DE (2004) Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16:2176–2191

    Article  CAS  Google Scholar 

  • Freitas EV, Nascimento CW, Souza A, Silva FB (2013) Citric acid-assisted phytoextraction of lead: A field experiment. Chemos 92:213–217

    Article  CAS  Google Scholar 

  • Gao Y, Miao C, Mao L, Zhou P, Jin Z, Shi W (2010) Improvement of phytoextraction and antioxidative defense in Solanum nigrum L. under cadmium stress by application of cadmium-resistant strain and citric acid. J Hazard Mater 181:771–777

    Article  CAS  Google Scholar 

  • Garg N, Bhandari P (2014) Cadmium toxicity in crop plants and its alleviation by arbuscular mycorrhizal (AM) fungi: an overview. Plant Bios-An Int J Aspects Plant Biol 148:609–621

    Google Scholar 

  • Garnier L, Simon-plas FR, Thuleau P, Agnel JP, Blein JP, Ranjeva R, Montillet JL (2006) Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. Plant Cell Environ 29:1956–1969

    Article  CAS  Google Scholar 

  • Gerhardt KE, Gerwing PD, Greenberg BM (2017) Opinion: taking phytoremediation from proven technology to accepted practice. Plant Sci 256:170–185

    Article  CAS  Google Scholar 

  • Gichner T, Patková Z, Száková J, Demnerová K (2004) Cadmium induces DNA damage in tobacco roots, but no DNA damage, somatic mutations or homologous recombination in tobacco leaves. Mutation Research/Genetic Toxicol Environ Mut 559:49–57

    Article  CAS  Google Scholar 

  • Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374

    Article  CAS  Google Scholar 

  • Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39

    Article  CAS  Google Scholar 

  • Göhre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223:1115–1122

    Article  CAS  Google Scholar 

  • Golia EE, Dimirkou A, Mitsios IK (2009) Heavy-metal concentration in tobacco leaves in relation to their available soil fractions. Commun Soil Sci Plant Anal 40:106–120

    Article  CAS  Google Scholar 

  • Golia EE, Füleky G, Dimirkou A, Antoniadis V, Tsiropoulos NG, Gizas G (2017) Influence of Zeolite and Posidonia oceanica (L.) in the reduction of heavy metal uptake by tobacco (Nicotiana tabacum) plants of Central Greece. Water Air Soil Pollut 228(324). https://doi.org/10.1007/s11270-017-3522-2

  • Gomes MA, Hauser-Davis RA, de Souza AN, Vitória AP (2016) Metal phytoremediation: general strategies, genetically modified plants and applications in metal nanoparticle contamination. Ecotoxicol Environ Saf 134:133–147

    Article  CAS  Google Scholar 

  • Gong X, Huang D, Liu Y, Zeng G, Wang R, Wei J, Huang C, Xu P, Wan J, Zhang C (2018) Pyrolysis and reutilization of plant residues after phytoremediation of heavy metals contaminated sediments: for heavy metals stabilization and dye adsorption. Bioresour Technol 253:64–71

    Article  CAS  Google Scholar 

  • Gonzalez-Chavez MC, Carrillo-Gonzalez R, Wright SF, Nichols KA (2004) The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environ Pollut 130:317–323

    Article  CAS  Google Scholar 

  • Gorinova N, Nedkovska M, Todorovska E, Simova-Stoilova L, Stoyanova Z, Georgieva K, Demirevska-Kepova K, Atanassov A, Herzig R (2007) Improved phytoaccumulation of cadmium by genetically modified tobacco plants (Nicotiana tabacum L.). Physiological and biochemical response of the transformants to cadmium toxicity. Environ Pollut 145:161–170

    Article  CAS  Google Scholar 

  • Groppa MD, Rosales EP, Iannone MF, Benavides MP (2008) Nitric oxide, polyamines and Cd-induced phytotoxicity in wheat roots. Phytochem 69:2609–2615

    Article  CAS  Google Scholar 

  • Gururani M, Mohanta T, Bae H (2015) Current understanding of the interplay between phytohormones and photosynthesis under environmental stress. Int J Mol Sci 16:19055–19085

    Article  CAS  Google Scholar 

  • Hattab NM, Soubrand R, Guégan M, Motelica-Heino X, Bourrat O, Faure J, Buchardon L (2014) Effect of organic amendments on the mobility of trace elements in phytoremediated techno-soils: role of the humic substances. Environ Sci Pollut Res 21:10470-10480

  • He PP, Lv XZ, Wang GY (2004) Effects of Se and Zn supplementation on the antagonism against Pb and Cd in vegetables. Environ Int 30:167–172

  • Herzig R, Guadagnini M, Rehnert A, Erismann KH (2003) Phytoextraction efficiency of in vitro-bred tobacco variants using a non-GMO approach. In: Vanek T, Schwitzguébel JP (eds) Phytoremediation Inventory—COST Action 837 View, Prague, UOCHB AVCR, p 73, ISBN 80-86241-19-X

  • Herzig R, Nehnevajova E, Pfistner C, Schwitzguebel JP, Ricci A, Keller C (2014) Feasibility of labile Zn phytoextraction using enhanced tobacco and sunflower: Results of five- and one-year field- scale experiments in Switzerland. Int J Phytorem 16:735–754

    Article  CAS  Google Scholar 

  • Hornburg V, Brummer G (1993) Heavy metals in soils: experiments on heavy metal mobility. J Plant Nutr Soil Sci 156:467–477

    CAS  Google Scholar 

  • Houtz RL, Ross O, Nable A, George M, Cheniae S (1988) Evidence for effects on the in vivo activity of ribulose-bisphosphate carboxylase/ oxygenase during development of Mn toxicity in tobacco. Plant Physiol 86:1143–1149

    Article  CAS  Google Scholar 

  • Hovsepyan AS, Greipsson S (2004) Effect of arbuscular mycorrhizal fungi on phytoextraction by corn (Zea mays) of lead- contaminated soil. Int J Phytorem 6:305–321

    Article  CAS  Google Scholar 

  • Hu L, Zhang Z, Xiang Z, Yang Z (2016) Exogenous application of citric acid ameliorates the adverse effect of heat stress in tall fescue (Lolium arundinaceum). Front Plant Sci 7:179

    Google Scholar 

  • Hui F, Liu J, Gao Q, Lou B (2015) Piriformospora indica confers cadmium tolerance in Nicotiana tabacum. J Environ Sci 37:184–191

    Article  CAS  Google Scholar 

  • Hussain A, Ali S, Rizwan M, Rehman MZ, Javed MR, Imran M, Chatha SA, Nazir R (2018) Zinc oxide nanoparticles alter the wheat physiological response and reduce the cadmium uptake by plants. Environ Pollut 242:1518–1526

    Article  CAS  Google Scholar 

  • Hussain A, Rizwan M, Ali Q, Ali S (2019) Seed priming with silicon nanoparticles improved the biomass and yield while reduced the oxidative stress and cadmium concentration in wheat grains. 26:7579–7588

  • Iqbal N, Umar S, Khan NA, Khan MIR (2014) A new perspective of phyto- hormones in salinity tolerance: regulation of proline metabolism. Environ Exp Bot 100:34–42

    Article  CAS  Google Scholar 

  • Iqbal M, Iqbal N, Bhatti IA, Ahmad N, Zahid M (2016) Response surface methodology application in optimization of cadmium adsorption by shoe waste: a good option of waste mitigation by waste. Ecol Eng 88:265–275

    Article  Google Scholar 

  • Janoš P, Vávrová J, Herzogová L, Pilarová V (2010) Effects of inorganic and organic amendments on the mobility (leachability) of heavy metals in contaminated soil: a sequential extraction study. Geoderm 159:335–341

    Article  CAS  Google Scholar 

  • Janoušková M, Vosátka M, Rossi L, Lugon-Moulin N (2007) Effects of arbuscular mycorrhizal inoculation on cadmium accumulation by different tobacco (Nicotiana tabacum L.) types. Appl Soil Ecol 35:502–510

    Article  Google Scholar 

  • Janssen J, Weyens N, Croes S, Beckers B, Meiresonne L, Van Peteghem P, Carleer R, Vangronsveld J (2015) Phytoremediation ofmetal con- taminated soil using willow: exploiting plant-associated bacteria to improve biomass production and metal uptake. Int J Phytorem 17:1123–1136

    Article  CAS  Google Scholar 

  • Jin HQ, Liu HB, Xie YY, Zhang YG, Xu QQ, Mao LJ, Li XJ, Chen J, Lin FC, Zhang CL (2018) Effect of the dark septate endophytic fungus Acrocalymma vagum on heavy metal content in tobacco leaves. Symbiosis 74:89–95

    Article  CAS  Google Scholar 

  • Jorgensen SE (1993) Removal of heavy metals from compost and soil by ecotechnological methods. Ecol Eng 2:89–100

    Article  Google Scholar 

  • Kaya A, Doganlar ZB (2016) Exogenous jasmonic acid induces stress tolerance in tobacco (Nicotiana tabacum) exposed to imazapic. Ecotoxicol Environ Saf 124:470–479

    Article  CAS  Google Scholar 

  • Keller C, Hammer D, Kayser A, Richner W, Brodbeck M, Sennhauser M (2003) Root development and heavy metal phytoextraction efficiency: com- parison of different plant species in the field. Plant Soil 249:67–81

    Article  CAS  Google Scholar 

  • Keller C, Marchetti M, Rossi L, Lugon-Moulin N (2005) Reduction of cadmium availability to tobacco (nicotiana tabacum) plants using soil amendments in low cadmium-contaminated agricultural soils: a pot experiment. Plant Soil 276:69–84

    Article  CAS  Google Scholar 

  • Keller C, Rizwan M, Davidian JC, Pokrovsky OS, Bovet N, Chaurand P, Meunier JD (2015) Effect of silicon on wheat seedlings (Triticum turgidum L.) grown in hydroponics and exposed to 0 to 30 μM Cu. Planta 241:847–860

    Article  CAS  Google Scholar 

  • Khairy AIH, Oh MJ, Lee SM, Kim DS, Roh KS (2016) Nitric oxide overcomes Cd and Cu toxicity in in vitro-grown tobacco plants through increasing contents and activities of rubisco and rubisco activase. Biochim Open 2:41–51

    Article  Google Scholar 

  • Khan AG (2005) Rote of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. J Trace Elem Med Biol 18:355–364

    Article  CAS  Google Scholar 

  • Khan MU, Shahbaz N, Waheed S, Mahmood A, Shinwari ZK, Malik RN (2016) Comparative health risk surveillance of heavy metals via dietary foodstuff con- sumption in different land-use types of Pakistan. Hum Ecol Risk Assess 22:168–186

    Article  CAS  Google Scholar 

  • Kidd P, Mench M, Alvarez-López V, Bert V, Dimitriou I, Friesl-Hanl W, Herzig R, Janssen JO, Kolbas A, Müller I, Neu S, Renella G, Ruttens A, Vangronsveld J, Puschenreiter M (2015) Agronomic practices for improving gentle remediation of trace element-contaminated soils. Int J Phytorem 17:1005–1037

    Article  CAS  Google Scholar 

  • Kim KR, Kim JG, Park JS, Kim MS, Owens G, Youn GH, Lee JS (2012) Immobilizer-assisted management of metal-contaminated agricultural soils for safer food production. J Environ Manag 102:88–95

    Article  CAS  Google Scholar 

  • Kim YO, Bae HJ, Cho E, Kang H (2017) Exogenous Glutathione enhances mercury tolerance by inhibiting mercury entry into plant cells. Front Plant Sci 8:1–10

    Google Scholar 

  • Kolbas A (2012) Phenotypic traits and development of plants exposed to trace elements; use for phytoremediation and biomonitoring. In: Sciences & Environnements, spécialité Ecologie Evolutive, Fonctionnelle et des Communautés. Université Bordeaux 1 Talence, France

    Google Scholar 

  • Konvacs H, Szemmelveisz K (2017) Disposal options for polluted plants grown on heavy metal contaminated brownfield lands-a review. Chemosphere 166:8–20

    Article  CAS  Google Scholar 

  • Krystofova O, Zitka O, Krizkova S, Hynek D, Shestivska V, Adam V, Hubalek J, Mackova M, Macek T, Zehnalek J, Babula P, Havel L, Kizek R (2012) Accumulation of cadmium by transgenic tobacco plants (Nicotiana tabacum L.) carrying yeast metallothionein gene revealed by electrochemistry. Int J Electrochem Sci 7:886–907

    CAS  Google Scholar 

  • Kumpiene J, Lagerkvist A, Maurice C (2008) Stabilization of As, Cr, Cu, Pb, and Zn in soil using amendments: a review. Waste Manag 28:215–225

    Article  CAS  Google Scholar 

  • Kumpiene J, Mench M, Bes CM, Fitts JP (2011) Assessment of aided phytostabilization of copper-contaminated soil by X-ray absorption spectroscopy and chemical extractions. Environ Pollut 159:1536–1542

    Article  CAS  Google Scholar 

  • Kayser A, Wenger K, Keller A, Attinger W, Felix HR, Gupta SK, Schulin R (2000) Enhancement of phytoextraction of Zn, Cd, and Cu from calcareous soil: the use of NTA and sulfur amendments. Environ Sci Technol 34:1778–1783

    Article  CAS  Google Scholar 

  • Labanowski J, Monna F, Bermond A, Cambier P, Fernandez C, Lamy I, van Oort F (2008) Kinetic extractions to assess mobilization of zn, pb, cu, and cd in a metal-contaminated soil: Edta vs. citrate. Environ Pollut 152:693–701

    Article  CAS  Google Scholar 

  • Lasat MM (2000) Phytoextraction of metals from contaminated soil: a review of plant/soil/metal interaction and assessment of pertinent agronomic issues. J Hazardous Substance Res 2:1–25

    Google Scholar 

  • Lasat MM (2002) Phytoextraction of toxic metals. J Environ Qual 31:109–120

    Article  CAS  Google Scholar 

  • Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330

    Article  CAS  Google Scholar 

  • Le Bot J, Goss MJ, Carvalho MJGPR, Van Beusichem ML, Kirkby EA (1990) The significance of the magnesium to manganese toxicity in tomato (Lycopersicon esculentum) and wheat (Triticum aestivum) plants. In plant Nutrition – Phyiology and applications 223-228. Springer, Dordrecht

    Google Scholar 

  • Lee BR, Hwang S (2015) Over-expression of NtHb1 encoding a non-symbiotic class 1 hemoglobin of tobacco enhances a tolerance to cadmium by decreasing NO (Nitric Oxide) and Cd levels in Nicotiana tabacum. Environ Exp Bot 113:18–27

    Article  CAS  Google Scholar 

  • Leyval C, Turnau K, Haselwandter K (1997) Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological, and applied aspects. Mycorrhiza 7:139–153

    Article  CAS  Google Scholar 

  • Li YJ, Wang ZK, Qin FX, Fang ZQ, Li XL, Li G (2018) Potentially toxic elements and health risk assessment in farmland systems around high-concentrated arsenic coal mining in Xingren, China. J Chemom 2018:1–10

    Google Scholar 

  • Lin D, Xing B (2007) Phytotoxicity of nanoparticles: inhibition of seed germination and root growth. Environ Pollut 150:243–250

    Article  CAS  Google Scholar 

  • Lin L, Zhou WH, Dai HX, Cao FB, Zhang GB, Wu FB (2012) Selenium reduces cadmium uptake and mitigates cadmium toxicity in rice. J. Hazard. Mater 235:343–351

    Article  CAS  Google Scholar 

  • Liu L, Chen H, Cai P, Liang W, Huang Q (2009) Immobilization and phytotoxicity of Cd in contaminated soil amended with chicken manure compost. J Hazard Mater 163:563–567

    Article  CAS  Google Scholar 

  • Liu L, Li Y, Tang J, Hu L, Chen X (2011) Plant coexistence can enhance phytoextraction of cadmium by tobacco (Nicotiana tabacum L.) in contaminated soil. J Environ Sci 23:453–460

    Article  CAS  Google Scholar 

  • Liu XY, Zhang AF, Ji CY, Joseph S, Bian RJ, Li LQ, Pan GX, Paz-Ferreiro J (2013) Biochar’s effect on crop productivity and the dependence on experimental conditions—a meta-analysis of literature data. Plant Soil 373:583–594

    Article  CAS  Google Scholar 

  • Lugon-Moulin N, Zhang M, Gadani F, Rossi L, Koller D, Krauss M, Wagner GJ (2004) Critical review of the science and options for reducing cadmium in tobacco (Nicotiana tabacum L.) and other plants. Adv Agron 83:111–180

    Article  CAS  Google Scholar 

  • Lugon-Moulin N, Rossi L, Vosatka M, Janouskova M (2007) Effects of absuscular mycorrhizal inoculation on cadmium accumulation by different tobacco (Nicotiana tabacum) types. Appl Soil Ecol 35:502–510

    Article  Google Scholar 

  • Ma W, Xu W, Xu H, Chen Y, He Z, Ma M (2010) Nitric oxide modulates cadmium influx during cadmium-induced programmed cell death in tobacco BY-2 cells. Planta 232:325–335

    Article  CAS  Google Scholar 

  • Ma Y, Prasad MN, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metallif- erous soils. Biotechnol Adv 29:248–258

    Article  CAS  Google Scholar 

  • Mao C, Feng Y, Wang X, Ren G (2015) Review on research achievements of biogas from anaerobic digestion. Renewable Sus Energy Rev 45:540–555

    Article  CAS  Google Scholar 

  • Maodzeka A, Hussain N, Wei L, Zvobgo G, Mapodzeke JM, Adil MF, Jabeen S, Wang F, Jiang L, Shamsi IH (2017) Elucidating the physiological and biochemical responses of different tobacco (Nicotiana tabacum) genotypes to lead toxicity. Environ Toxicol Chem 3:175–181

    Article  CAS  Google Scholar 

  • Maqbool A, Ali S, Rizwan M, Ishaque W, Rasool N, ur Rehman MZ, Bashir A, Abid M, Wu L (2018) Management of tannery wastewater for improving growth attributes and reducing chromium uptake in spinach through citric acid application. Environ Sci Pollut Res 25:10848–10856

    Article  CAS  Google Scholar 

  • Mastretta C, Taghavi S, Van Der Lelie D, Mengoni A, Galardi F, Gonnelli C, Barac T, Boulet J, Weyens N, Vangronsveld J (2009) Endophytic bacteria from seeds of Nicotiana tabacum can reduce cadmium phytotoxicity. Int J Phytorem 11:251–267

    Article  CAS  Google Scholar 

  • McNeil SE (2005) Nanotechnology for the biologist. J Leukoc Biol 78:585–594

    Article  CAS  Google Scholar 

  • Mench M, Tancogne J, Gomez A, Juste C (1989) Cadmium bioavailability to Nicotiana tabacum L., Nicotiana rustica L., and Zea mays L. grown in soil amended or not amended with cadmium nitrate. Biol Fertil Soils 8:48–53

    Article  CAS  Google Scholar 

  • Mench MJ, Didier VL, Lo Ёffler M, Gomez A, Masson P (1994) A mimicked in-situ remediation study of metalcontaminated soils with emphasis on cadmium and lead. J Environ Qual 23:58–63

    Article  CAS  Google Scholar 

  • Mench MJ, Manceau A, Vangronsveld J, Clijsters H, Mocquot B (2000) Capacity of soil amendments in lowering the phytoavailability of sludge-borne zinc. Agronomie 20:383–397

    Article  Google Scholar 

  • Mench M, Lepp N, Bert V, Schwitzguébel JP, Gawronski S, Schröder P, Vangronsveld J (2010) Successes and limitations of phytotechnologies at field scale: outcomes, assessment and outlook from COST Action 859. J Soils Sediments 10:1039–1070

    Article  CAS  Google Scholar 

  • Millar AH, MittovaV KG, Heazlewood JL, Bartoli CG, Theodoulou FL, Foyer CH (2003) Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol 133:443–447

    Article  CAS  Google Scholar 

  • Misra S, Gedamu L (1989) Heavy-metal tolerant transgenic Brassica napus L and Nicotiana tabacum L plants. Theor Appl Genet 78:161–168

    Article  CAS  Google Scholar 

  • Molas J (1996) Changes in morphological and anatomical structure of cabbage outer leaves and in ultrastructure of their chloroplasts caused by an in vitroexcess of nickel. Photosynthetica 34:513–522

    Article  Google Scholar 

  • Mora MDLL, Pinilla L, Rosas A, Cartes P (2008) Selenium uptake and its influence on the antioxidative system of white clover as affected by lime and phosphorus fertilization. Plant Soil 303:139–149

    Article  CAS  Google Scholar 

  • Moraghan JT (1993) Accumulation of cadmium and selected elements in flax seed grown on a calcareous soil. Plant Soil 150:61–68

    Article  CAS  Google Scholar 

  • Mullineaux P, Rausch T (2005) Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynth Res 86:459–474

    Article  CAS  Google Scholar 

  • Murakami M, Ae N, Ishikawa S (2007) Phytoextraction of cad- mium by rice (Oryza sativa L.), soybean (Glycine max (L.) Merr.), and maize (Zea mays L.). Environ Pollut 145:96–103

    Article  CAS  Google Scholar 

  • Naeem S, Ingram JC, Varga A, Agardy T, Barten P, Bennett G, Bloomgardan E, Bremer LL, Burkill P, Cattau M, Ching C (2015) Get the science right when paying for nature’s services. Sci 347:1206–1207

    Article  CAS  Google Scholar 

  • Naeem A, Badshah S, Muska M, Ahma N, Khan K (2016) The current case of quinolones: synthetic approaches and antibacterial activity. Molecules 21:268

    Article  CAS  Google Scholar 

  • Naeem A, Saifullah Rehman MZ, Akhtar T, Zia MH, Aslam M (2018) Silicon nutrition lowers cadmium content of wheat cultivars by regulating transpiration rate and activity of antioxidant enzymes. Environ Pollut 242:126–135

    Article  CAS  Google Scholar 

  • Nedkovska M, Atanassov AI (1998) Metallothionein genes and expression for heavy metal resistance. Biotechnol Biotechnol Equip 12:11–16

    Article  Google Scholar 

  • Nehnevajova E, Herzig R, Federer G, Erismann K, Schwitzgu’ebel J (2005) Screening of sunflower cultivars for metal phytoextraction in a contaminated field prior to mutagenesis. Int J Phytoremediation 7:337–349

    Article  CAS  Google Scholar 

  • Nehnevajova E, Herzig R, Federer G, Erismann KH, Schwitzguebel JP (2007) Chemical mutagenesis–a promising technique to increase metal concen- tration and extraction in sunflowers. Int J Phytorem 9:149–165

    Article  CAS  Google Scholar 

  • Ngorwe EN, Nyambaka HN, Murungi JI (2014) Use of low cost soil amendments reduces uptake of cadmium and lead by tobacco (Nicotiana tabacum) grown in medially polluted soils. J Environ Human 1:104–113

    Google Scholar 

  • Nouri J, Khorasani N, Lorestani B, Karami M, Hassani A, Yousefi N (2009) Accumulation of heavy metals in soil and uptake by plant species with phytoremediation potential. Environ Earth Sci 59:315–323

    Article  CAS  Google Scholar 

  • Okhi K (1984) Manganese deficiency and toxicity effects on growth, development, and nutrient composition in wheat 1. Agron J 76:213–218

    Article  Google Scholar 

  • Olowe VIO, Adeyemo AY (2009) Enhanced crop productivity and compatibility through intercropping of sesame and sunflower varieties. Ann Appl Biol 155:285–291

    Article  Google Scholar 

  • Park JH, Choppala GK, Bolan NS, Chung JW, Chuasavathi T (2011a) Biochar reduces the bioavailability and phytotoxicity of heavy metals. Plant Soil 348:439–451

    Article  CAS  Google Scholar 

  • Park JH, Lamb D, Paneerselvam P, Choppala G, Bolan N, Chung JW (2011b) Role of organic amendments on enhanced bioremediation of heavy metal(loid) contaminated soils. J Hazard Mater 185:549–574

    Article  CAS  Google Scholar 

  • Parraga-Aguado I, González-Alcaraz MN, Schulin R, Conesa HM (2015) The potential use of Piptatherum miliaceum for the phytomanagement of mine tailings in semiarid areas: role of soil fertility and plant competition. J Environ Manag 158:74–84

    Article  CAS  Google Scholar 

  • Pilon-Smits E, Pilon M (2002) Phytoremediation of metals using transgenic plants. CRC Crit Rev Plant Sci 21:439–456

    Article  CAS  Google Scholar 

  • Qayyum MF, Rehman MZ, Ali S, Rizwan M, Naeem A, Maqsood MA, Khalid H, Rinklebe J, Ok YS (2017) Residual effects of monoammonium phosphate, gypsum and elemental sulfur on cadmium phytoavailability and translocation from soil to wheat in an effluent irrigated field. Chemosphere 174:515–523

    Article  CAS  Google Scholar 

  • Rafique N, Tariq SR (2016) Distribution and source apportionment studies of heavy metals in soil of cotton/wheat fields. Environ Monit Assess 188:309

    Article  CAS  Google Scholar 

  • Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181

    Article  CAS  Google Scholar 

  • Rausch T, Gromes R, Liedschulte V, Muller I, Bogs J, Galovic V, Wachter A (2007) Novel insight into the regulation of GSH biosynthesis in higher plants. Plant Biol (Stuttg) 9:565–572

    Article  CAS  Google Scholar 

  • Rehman MZ, Rizwan M, Ghafoor A, Naeem A, Ali S, Sabir M, Qayyum MF (2015) Effect of inorganic amendments for in situ stabilization of cadmium in contaminated soils and its phyto-availability to wheat and rice under rotation. Environ Sci Pollut Res 22:16897–16906

    Article  CAS  Google Scholar 

  • Rehman MZ, Rizwan M, Ali A, Fatima N, Yousaf B, Naeem A, Sabir M, Ahmad HR, Ok YS (2016) Contrasting effects of biochar, compost and farm manure on alleviation of nickel toxicity in maize (Zea mays L.) in relation to plant growth, photosynthesis and metal uptake. Ecotoxicol Environ Saf 133:218–225

    Article  CAS  Google Scholar 

  • Rehman MZ, Khalid H, Akmal F, Ali S, Rizwan M, Qayyum MF, Iqbal M, Khalid MU, Azhar M (2017a) Effect of limestone, lignite and biochar applied alone and combined on cadmium uptake in wheat and rice under rotation in an effluent irrigated field. Environ Pollut 227:560–568

    Article  CAS  Google Scholar 

  • Rehman MZ, Rizwan M, Ali S, Ok YS, Ishaque W, Nawaz MF, Akmal F, Waqar M (2017b) Remediation of heavy metal contaminated soils by using Solanum nigrum: a review. Ecotoxicol Environ Saf 143:236–248

    Article  CAS  Google Scholar 

  • Rehman MZ, Rizwan M, Rauf A, Ayub MA, Ali S, Qayyum MF, Waris AA, Naeem A, Sanaullah M (2019) Split application of silicon in cadmium (Cd) spiked alkaline soil plays a vital role in decreasing Cd accumulation in rice (Oryza sativa L.) grains. Chemosphere 226:454–462

    Article  CAS  Google Scholar 

  • Rizwan M, Ali S, Adrees M, Rizvi H, Rehman MZ, Hannan F, Qayyum MF, Hafeez F, OK YS (2016) Cadmium stress in rice: toxic effects, tolerance mechanisms and management: a critical review. Environ Sci Pollut Res 23:17859–17879

    Article  CAS  Google Scholar 

  • Rizwan M, Ali S, Qayyum MF, Ok YS, Adrees M, Ibrahim M, Rehman MZ, Farid M, Abbas F (2017a) Effect of metal and metal oxide nanoparticles on growth and physiology of globally important food crops: a critical review. J Hazard Mater 322:2–16

    Article  CAS  Google Scholar 

  • Rizwan M, Ali S, Adrees M, Ibrahim M, Tsang DC, Rehman MZ, Zahir ZA, Rinklebe J, Tack FM, Ok YS (2017b) A critical review on effects, tolerance mechanisms and management of cadmium in vegetables. Chemosphere 182:90–105

    Article  CAS  Google Scholar 

  • Rizwan M, Ali S, Rehman MZ, Rinklebe J, Tsang DC, Bashir A, Maqbool A, Tack FM, Ok YS (2018) Cadmium phytoremediation potential of Brassica crop species: a review. Sci Total Environ 631:1175–1191

    Article  CAS  Google Scholar 

  • Rizwan M, Ali S, Rehman MZ, Maqbool A (2019) A critical review on the effects of zinc at toxic levels of cadmium in plants. Environ Sci Pollut Res 26:6279–6289

    Article  CAS  Google Scholar 

  • Rocco C, Agrelli D, Tafuro M, Caporale AG, Adamo P (2018) Assessing the bioavailability of potentially toxic elements in soil: a proposed approach. Ital J Agron 13:16–22

    Google Scholar 

  • Rodríguez-Ortíz JC, Valdez-Cepeda RD, Lara-Mireles JL, Rodríguez-Fuentes H, Vázquez-Alvarado RE, Magallanes-Quintanar R, García-Hernández JL (2006) Soil nitrogen fertilization effects on phytoextraction of cadmium and lead by tobacco (Nicotiana tabacum L.). Bioremediat J 10:105–114

    Article  CAS  Google Scholar 

  • Rufty TW, Miner GS, Raper CD (1979) Temperature effects on growth and manganese tolerance in tobacco 1. Agron J 71:638–644

    Article  CAS  Google Scholar 

  • Rufyikiri G, Thiry Y, Wang L, Delvaux B, Declerck S (2002) Uranium uptake and translocation by the arbuscular mycor- rhizal fungus, Glomus intraradices, under root-organ culture conditions. New Phytol 156:275–281

    Article  CAS  Google Scholar 

  • Ruotolo R, Maestri E, Pagano L, Marmiroli M, White JC, Marmiroli N (2018) Plant response to metal-containing engineered nanomaterials: an omics-based perspective. Environ Sci Technol 52:2451–2467

    Article  CAS  Google Scholar 

  • Ruso J, Zapata J, Hernandez M, Ojeda MA (2001) Toxic metals accumulation and total soluble phenolics in sunflower and tobacco plants. Minerva Biotechnol 13:93

    Google Scholar 

  • Sabir S (2015) Approach of cost effective absorbents for oil removal from oily water. Crit Rev Environ Sci Technol 45(17):1916–1945

    Article  CAS  Google Scholar 

  • Sabo-Attwood T, Unrine JM, Stone JW, Murphy CJ, Ghoshroy S, Blom D, Bertsch PM, Newman LA (2012) Uptake, distribution and toxicity of gold nanoparticles in tobacco (Nicotiana xanthi) seedlings. Nanotoxicology 6:353–360

    Article  CAS  Google Scholar 

  • Salt DE, Blaylock M, Kumar NPBA, Dushenkov V, Ensley BD, Chet I, Raskin I (1995) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Nat Biotechnol 13:468–474

    Article  CAS  Google Scholar 

  • Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M (2013) The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194

    Article  CAS  Google Scholar 

  • Shuman LM (1991) Chemical forms of micronutrient in soils. Micronutrients in Agriculture. Soil Sci Soc Am J:113–144

  • Silveira ML, Alleoni LFA, Chang A (2008) Soil amendments and heavy metal retention and distribution in oxisols treated with biosolids. Revista Brasileira de Ciencia do Solo 32:1087–1098

    Article  CAS  Google Scholar 

  • Singh HP, Batish DR, Kaur G, Arora K, Kohli RK (2008) Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environ Exp Bot 63:158–167

    Article  CAS  Google Scholar 

  • Singh HP, Kaur S, Batish DR, Sharma VP, Sharma N, Kohli PK (2009) Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the roots of Oryza sativa (rice). Nitric Oxide 20:289–297

    Article  CAS  Google Scholar 

  • Singla-Pareek SL, Yadav SK, Pareek A, Reddy MK, Sopory SK (2006) Transgenic tobacco overexpressing glyoxalase pathway enzymes grow and set viable seeds in zinc-spiked soils. Plant Physiol 140:613–623

    Article  CAS  Google Scholar 

  • Son JA, Narayanankutty DP, Roh KS (2014) Influence of exogenous application of glutathione on rubisco and rubisco activase in heavy metal-stressed tobacco plant grown in vitro. Saudi J Biol Sci 21:89–97

    Article  CAS  Google Scholar 

  • Soudek P, Kufner D, Petrová S, Mihaljevič M, Vaněk T (2013) Composition of hydroponic medium affects thorium uptake by tobacco plants. Chemosphere 92:1090–1098

    Article  CAS  Google Scholar 

  • Štefanić PP, Šikić S, Cvjetko P, Balen B (2012) Cadmium and zinc induced similar changes in protein and glycoprotein patterns in tobacco (Nicotiana tabacum L.) seedlings and plants. Arch Ind Hyg Toxicol 63:321–335

    Google Scholar 

  • Štefanić PP, Cvjetko P, Biba R, Domijan AM, Letofsky-Papst I, Tkalec M, Šikić S, Cindrić M, Balen B (2018) Physiological, ultrastructural and proteomic responses of tobacco seedlings exposed to silver nanoparticles and silver nitrate. Chemosphere 209:640–653

    Article  CAS  Google Scholar 

  • Stoger E, Ma JK, Fischer R, Christou P (2005) Sowing the seeds of success: pharmaceutical proteins from plants. Curr Opin Biotechnol 16:167–173

    Article  CAS  Google Scholar 

  • Sudova E, Machova J, Svobodova Z, Vesely T (2007) Negative effects of malachite green and possibilities of its replacement in the treatment of fish eggs and fish: a review. Vet Med (Praha) 52:527

    Article  CAS  Google Scholar 

  • Sun Y, Li Y, Xu Y, Liang X, Wang L (2015) In situ stabilization remedi- ation of cadmium (Cd) and lead (Pb) co-contaminated paddy soil using bentonite. Appl Clay Sci 105:200–206

    Article  CAS  Google Scholar 

  • Tancogne J, Lich NP, Schildz P, Truhaut JR, Ckaude JR, Chouteau J (1989) Influence of some factors of the growth medium on the adsorption of cadmium by tobacco L., variety PB D6. Ann Du Tabac:135–144

  • Tandy S, Healey JR, Nason MA, Williamson JC, Jones DL (2009) Remediation of metal polluted mine soil with compost: cocomposting versus incorporation. Environ Pollut 157:690–697

    Article  CAS  Google Scholar 

  • Tauqeer HM, Ali S, Rizwan M, Ali Q, Saeed R, Iftikhar U, Ahmad R, Farid M, Abbasi GH (2016) Phytoremediation of heavy metals by Alternanthera bett- zickiana: growth and physiological response. Ecotoxicol Environ Saf 126:138–146

    Article  CAS  Google Scholar 

  • Temperton VM, Mwangi PN, Scherer-Lorenzen M, Schmid B, Buchmann N (2007) Positive interactions between nitrogen- fixing legumes and four different neighbouring species in a biodiversity experiment. Oecologia 151:190–205

    Article  Google Scholar 

  • Tichy R, Fajtl J, Kuzel S, Kolar L (1996) Use of elemental Sulphur to enhance a cadmium solubilization and its vegetative removal from contaminated soil. Nutri Cycl Agroecosys 46:249–255

    Article  CAS  Google Scholar 

  • Tichy R, Nydl V, Kuzel S, Kolar L (1997) Increased cadmium availability to crops on a sewage sludge amended soil. Water Air Soil Pollut 94:361–372

    CAS  Google Scholar 

  • Tripathi DK, Tripathi A, Shweta SS, Singh Y, Vishwakarma K, Yadav G, Sharma S, Singh VK, Mishra RK, Upadhyay RG, Dubey NK, Lee Y, Chauhan DK (2017) Uptake, accumulation and toxicity of silver nanoparticle in autotrophic plants, and heterotrophic microbes: a concentric review. Front Microbiol 8:1–12

    CAS  Google Scholar 

  • Vamerali T, Marchiol L, Bandiera M, Fellet G, Dickinson NM, Lucchini P, Mosca G, Zerbi G (2012) Advances in agronomic management of phytoremediation: methods and results from a 10-year study of metal-polluted soils. Ital J Agron 7:323–330

    Google Scholar 

  • Vanessa ÁL, Ángeles PF, Sergio R, Beatriz RG, Rolf H, Markus P, Susan KP (2017) Evaluating phytoextraction efficiency of two high-biomass crops after soil amendment and inoculation with rhizobacterial strains. Environ Sci Pollut Res Int 24:7591–7606

    Article  CAS  Google Scholar 

  • Vannini C, Domingo G, Onelli E, De Mattia F, Bruni I, Marsoni M, Bracale M (2014) Phytotoxic and genotoxic effects of silver nanoparticles exposure on germinating wheat seedlings. J Plant Physiol 171:1142–1148

    Article  CAS  Google Scholar 

  • Vasiliadou S, Dordas C (2009) Increased concentration of soil cadmium affects on plant growth, dry matter accumulation, Cd, and Zn uptake of different tobacco cultivars (Nicotiana tabacum L.). Int J Phytorem 11:115–130

    Article  CAS  Google Scholar 

  • Vera-Estrella R, Gomez-Mendez MF, Amezcua-Romero JC, Barkla BJ, Rosas-Santiago P, Pantoja O (2017) Cadmium and zinc activate adaptive mechanisms in Nicotiana tabacum similar to those observed in metal tolerant plants. Planta 246:433–451

    Article  CAS  Google Scholar 

  • Wagner GJ, Yeargan R (1986) Variation in cadmium accumulation potential and tissue distribution of cadmium in tobacco. Plant Physiol 82:274–279

    Article  CAS  Google Scholar 

  • Walker DJ, Clemente R, Roig A, Bernal MP (2003) The effect of soil amendments on heavy metal bioavailability in two contaminated Mediterranean soils. Environ Pollut 122:303–312

    Article  CAS  Google Scholar 

  • Walker DJ, Clemente R, Bernal MP (2004) Contrasting effects of manure and compost on soil pH, heavy metal availability and growth of Chenopodium album L. in a soil contaminated by pyritic mine waste. Chemosphere 57:215–224

    Article  CAS  Google Scholar 

  • Wang J, Evangelou VP (1994) Metal tolerance aspects of plant cell wall and vacuole. In: Pessarakli M (ed) Handbook of Plant and Crop Physiology. Marcel Dekker, Inc., New York

    Google Scholar 

  • Wang FL, Ouyang W, Hao FH, Lin CY, Song NN (2014) In situ remediation of cadmium-polluted soil reusing four byproducts individually and in combination. J Soils Sediments 14:451–461

    Article  CAS  Google Scholar 

  • Wang M, Duan S, Zhou Z, Chen S, Wang D (2019) Foliar spraying of melatonin confers cadmium tolerance in Nicotiana tabacum L. EcotoxicolEnviron Safe 170:68–76

  • Wasay SA, Barrington SF, Tokunaga S (1998) Remediation of soils polluted by heavy metals using salts of organic acids and chelating agents. Environ Technol 19:369–379

    Article  CAS  Google Scholar 

  • Wenger K, Kayser A, Gupta SK, Furrer G, Schulin R (2002) Comparison of NTA and elemental sulfur as potential soil amendments in phytoremediation. Soil Sediment Contam 11:655–672

    Article  CAS  Google Scholar 

  • Wojas S, Clemens S, Hennig J, Skłodowska A, Kopera E, Schat H, Bal W, Antosiewicz DM (2008) Overexpression of phytochelatin synthase in tobacco: distinctive effects of AtPCS1 and CePCS genes on plant response to cadmium. J Exp Bot 59:2205–2219

    Article  CAS  Google Scholar 

  • Xiong J, Lu H, Lu K, Duan Y, An L, Zhu C (2009) Cadmium decreases crown root number by decreasing endogenous nitric oxide, which is indispensable for crown root primordia initiation in rice seedlings. Planta 230:599–610

    Article  CAS  Google Scholar 

  • Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. South Afr J Bot 76:167–179

    Article  CAS  Google Scholar 

  • Yadav SK, Singla-Pareek SL, Ray M, Reddy MK, Sopory SK (2005a) Methylglyoxal levels in plants under salinity stress are dependent on glyoxalase I and glutathione. Biochem Biophys Res Commun 337:61–67

    Article  CAS  Google Scholar 

  • Yadav SK, Singla-Pareek SL, Reddy MK, Sopory SK (2005b) Methyl- glyoxal detoxification by glyoxalase system: a survival strategy during environmental stresses. Physiol Mol Biol Plants 11:1–11

    CAS  Google Scholar 

  • Yadav SK, Singla-Pareek SL, Reddy MK, Sopory SK (2005c) Transgenic tobacco plants overexpressing glyoxalase enzymes resist an increase in methylglyoxal and maintain higher reduced glutathione levels under salinity stress. FEBS Lett 579:6265–6271

    Article  CAS  Google Scholar 

  • Yang RY, Tang JJ, Chen X, Hu SJ (2007) Effects of coexisting plant species on soil microbes and soil enzymes in metal lead contaminated soils. Appl Soil Ecol 37:240–246

    Article  Google Scholar 

  • Yang X, Stoffella PJ, Baligar VC (2015) Soil biogeochemistry, plant physiology, and phytoremediation of cadmium-contaminated soils. Adv Agron. https://doi.org/10.1016/bs.agron.2015.06.005

  • Yang X, Lu K, McGrouther K, Che L, Hu G, Wang Q, Liu X, Shen L, Huang H, Ye Z, Wang H (2017a) Bioavailability of Cd and Zn in soils treated with biochars derived from tobacco stalk and dead pigs. J Soils Sediments 17:751–762

    Article  CAS  Google Scholar 

  • Yang Y, Ge Y, Zeng H, Zhou X, Peng L, Zeng Q (2017b) Phytoextraction of cadmium-contaminated soil and potential of regenerated tobacco biomass for recovery of cadmium. Sci Rep 7:1–10

    Article  CAS  Google Scholar 

  • Yeh TY, Lin CF, Chuang CC, Pan CT (2012) The effect of varying soil organic levels on phytoextraction of Cu and Zn uptake, enhanced by chelator EDTA, DTPA, EDDS and citric acid, in sunflower (Helianthus annuus), Chinese cabbage (Brassica campestris), cattail (Typha latifolia), and reed (Phragmites communis). Environ Anal Toxicol 2:1–10

    Google Scholar 

  • Yin L, Cheng Y, Espinass B, Colman BP, Auffan M, Wiesner M, Rose J, Liu J, Bernhardt ES (2011) More than the ions: the effects of silver nanoparticles on Lolium multiflorum. Environ Sci Technol 45:2360–2367

    Article  CAS  Google Scholar 

  • Younis U, Malik SA, Rizwan M, Qayyum MF, Ok YS, Shah MH, Rehman RA, Ahmad N (2016) Biochar enhances the cadmium tolerance in spinach (Spinacia oleracea) through modification of Cd uptake and physiological and biochemical attributes. Environ Sci Pollut Res 23:21385–21394

    Article  CAS  Google Scholar 

  • Yousaf B, Liu G, Wang R, Rehman MZ, Rizwan MS, Imtiaz M, Murtaza G, Shakoor A (2016) Investigating the potential influence of biochar and tradi- tional organic amendments on the bioavailability and transfer of Cd in the soil–plant system. Environ Earth Sci 75:1–10

    Article  CAS  Google Scholar 

  • Yu CC, Hung KT, Kao CH (2005) Nitric oxide reduces Cu toxicity and Cu-induced NH4+ accumulation in rice leaves. J Plant Physiol 162:1319–1330

    Article  CAS  Google Scholar 

  • Yu Y, Wan Y, Wang Q, Li H (2017) Effect of humic acid-based amendments with foliar application of Zn and Se on Cd accumulation in tobacco. Ecotoxicol Environ Saf 138:286–291

    Article  CAS  Google Scholar 

  • Yuan X, Huang H, Zeng G, Li H, Wang J, Zhou C, Zhu H, Pei X, Liu Z, Liu Z (2011) Total concentrations and chemical speciation of heavy metals in liquefaction residues of sewage sludge. Bioresour Technol 102:4104–4110

    Article  CAS  Google Scholar 

  • Yurekli F, Porgalı ZB, Turkan I (2004) Variations in absisic acid, indol-3-asetic acid, giberellic acid and zeatin concentrations in two ban species subjected to salt stress. Acta Biol Crov Bot 46:201–212

    Google Scholar 

  • Zembala M, Filek M, Walas S, Mrowiec H, Kornas A, Miszalski Z, Hartikainen H (2010) Effect of selenium on macro- and microelement distribution and physiological parameters of rape and wheat seedlings exposed to cadmium stress. Plant Soil 329:457–468

    Article  CAS  Google Scholar 

  • Zeng WA, Li F, Zhou H, Qin XL, Zou ZJ, Tian T, Zeng M, Liao BH (2016) Effect of calcium carbonate on cadmium and nutrients uptake in tobacco (Nicotiana tabacum L) planted on contaminated soil. J Environ Biol 37:163–168

    CAS  Google Scholar 

  • Zeng WA, Hu Q, Li F, Gu S, Huang Y, Cai H, Zeng M, Li Q, Tan L (2018) Effects of application of silicon and zeolite on chemical speciation of cadmium in soil and its uptake by Tobacco. Int J Agric Biol 20:452–456

    Article  CAS  Google Scholar 

  • Zhang L, Liu N, Ma X, Jiang L (2013) The transcriptional control machinery as well as the cell wall integrity and its regulation are involved in the detoxification of the organic solvent dimethyl sulfoxide in Saccharomyces cerevisiae. FEMS Yeast Res 13:200–218

    Article  CAS  Google Scholar 

  • Zhang Y, He X, Liang H, Zhao J, Zhang Y, Xu C, Shi X (2016a) Long-term tobacco plantation induces soil acidification and soil base cation loss. Environ Sci Pollut Res 23:5442–5450

    Article  CAS  Google Scholar 

  • Zhang Y, He X, Zhao J, Zhang Y, Shi X (2016b) Soil acidification under long-term tobacco plantation results in alterations of mineralogical properties in an Alisol. Arch Agron Soil Sci 62:1033–1040

    Article  CAS  Google Scholar 

  • Zhao CH, Yuan GA, Yanliang ZH, Qisheng YI (2013) Effects of soil amendments on cadmium uptake of tobacco plants. Tobacco Sci Technol 3:72–76

    Google Scholar 

  • Zhu YG, Zhao ZQ, Li HY, Smith SE, Smith FA (2003) Effect of zinc-cadmium interactions on the uptake of zinc and cadmium by winter wheat (Triticum aestivum) grown in pot culture. Bull Environ Contam Toxicol 71:1289–1296

    Article  CAS  Google Scholar 

  • Zou ZJ (2015) Heavy metal translocation and accumulation in iron plaques and plant tissues for 32 hybrid rice (Oryza sativa L.) culti- vars. Plant Soil 386:317–329

    Article  CAS  Google Scholar 

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This research work was financially supported by the University of Agriculture, Faisalabad, and Higher Education Commission of Pakistan.

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Rehman, M., Rizwan, M., Sohail, M.I. et al. Opportunities and challenges in the remediation of metal-contaminated soils by using tobacco (Nicotiana tabacum L.): a critical review. Environ Sci Pollut Res 26, 18053–18070 (2019). https://doi.org/10.1007/s11356-019-05391-9

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