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Effect of different amendments on rice (Oryza sativa L.) growth, yield, nutrient uptake and grain quality in Ni-contaminated soil

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Abstract

Rice ( Oryza sativa L.) is one of the main staple food crops which is inherently low in micronutrients, especially iron (Fe), and can lead to severe Fe deficiency in populations having higher consumption of rice. Soils polluted with nickel (Ni) can cause toxicity to rice and decreased Fe uptake by rice plants. We investigated the potential role of biochar (BC) and gravel sludge (GS), alone and in combination, for in situ immobilization of Ni in an industrially Ni-contaminated soil at original and sulfur-amended altered soil pH. Our further aim was to increase Fe bioavailability to rice plants by the exogenous application of ferrous sulfate to the Ni-immobilized soil. Application of the mixture of both amendments reduced grain Ni concentration, phytate, Phytate/Fe, Phyt/Zn molar ratios, and soil DTPA-extractable Ni. In addition, the amendment mixture increased 70 % Fe and 229 % ferritin concentrations in rice grains grown in the soil at original pH. The Fe and ferritin concentrations in S-treated soil was increased up to 113 and 383 % relative to control respectively. This enhanced Fe concentration and corresponding ferritin in rice grains can be attributed to Ni/Fe antagonism where Ni has been immobilized by GS and BC mixture. This proposed technique can be used to enhance growth, yield, and Fe biofortification in rice by reducing soil pH while in parallel in situ immobilizing Ni in polluted soil.

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References

  • Adrees M, Ali S, Rizwan M, Ibrahim M, Abbas F, Farid M, Rehman MZ, Irshad MK, Bharwana SA (2015a) The effect of excess copper on growth and physiology of important food crops: a review. Environ Sci Pollut Res 22:8148–8162

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ahmad M, Rajapaksha AU, Lim JE, Zhang M, Bolan N, Mohan D, Vithanage M, Lee SS, Ok YS (2014) Biochar as a sorbent for contaminant management in soil and water: a review. Chemosphere 99:19–33

    Article  CAS  Google Scholar 

  • Ali S, Bharwana SA, Rizwan M, Farid M, Kanwal S, Ali Q, Ibrahim M, Gill RA, Khan MD (2015) Fulvic acid mediates chromium (Cr) tolerance in wheat (Triticum aestivum L.) through lowering of Cr uptake and improved antioxidant defense system. Environ Sci Pollut Res 22:10601–10609

    Article  CAS  Google Scholar 

  • Allison LE, Moodie CD (1965) Carbonate. In: Black CA (ed) Methods soil analysis part 2: chemical and microbiological properties. Am Soc Agron Madison USA, p 1379–1396

  • Almaroai YA, Usman ARA, Mahtab A, Deok HM, Ju-Sik C, Young KJ, Choong J, Sang SL, Ok YS (2014) "Effects of biochar, cow bone, and eggshell on Pb availability to maize in contaminated soil irrigated with saline water. Environ Earth Sci 71:1289–1296

    Article  CAS  Google Scholar 

  • AOAC (2003) Official methods of analysis of the association of official’s analytical chemists, 17th edn. Association of official analytical chemists, Arlington, Virginia. Application on mycorrhizal root colonisation, growth and nutrition of wheat. Aust J Soil Res 48:546–554

    Google Scholar 

  • Barcelo F, Miralles F, Arean CO (1997) Purification and characterization of ferritin from alfalfa seeds. J Inorg Biochem 66:23–27

    Article  CAS  Google Scholar 

  • Bertrand J, Mars A, Boyle C, Bove F, Yeargin-Allsopp M, Decoufle P (2001) Prevalence of autism in a United States population: the Brick Township, New Jersey, investigation. Pediatrics 108:1155–1161

    Article  CAS  Google Scholar 

  • Bingham FT, Pereyea FJ, Jarrell WM (1986) Metal toxicity to agricultural crops. Met Ions Biol Syst 20:119–156

    CAS  Google Scholar 

  • Borrell AK, Hammer GL, Douglas ACL (2000) Does maintaining green leaf area in sorghum improve yield under drought? I. Leaf growth and senescence. Crop Sci J 40:1026–1037

    Article  Google Scholar 

  • Bouis HE, Welch RM (2010) Biofortification: a sustainable agricultural strategy for reducing micronutrient malnutrition in the global south. Crop Sci 50:20–32

    Article  Google Scholar 

  • Bremner JM, Mulvaney CS (1982) Nitrogen total. p. 595–624. In A. L. Page (ed.), Methods of soil analysis. Agron. No. 9, part 2: chemical and microbiological properties, 2nd ed., Am Soc Agron Madison WI USA

  • Cao XD, Ma LN, Gao B, Harris W (2009) Dairy-manure derived biochar effectively sorbs lead and atrazine. Environ Sci Technol 43:3285–3291

    Article  CAS  Google Scholar 

  • Cataldo DA, Garland TR, Wildung RE (1978) Nickel in plants. I. Uptake kinetics using intact soybean seedling. Plant Physiol 62:563

    Article  CAS  Google Scholar 

  • Chen Z, Watanabe TT, Shinano T, Exawa J, Washaki K, Kimura T, Osaki M, Xhu Y (2009) Element interconnections in Lotus japonicas: a systematic study of the effects of element additions on different natural variants. Soil Sci Plant Nutr 55:91–101

    Article  CAS  Google Scholar 

  • Cook JD, Dassenko SA, Lynch SR (1991) Assessment of the role of nonheme-iron availability in iron balance. Am J Clin Nutr 54:717–722

    CAS  Google Scholar 

  • Friesl W, Friedl J, Platzer K, Horak O, Gerzabek MH (2006) Remediation of contaminated agricultural soils near a former Pb/Zn smelter in Austria: batch, pot and field experiments. Environ Pollut 144:40–50

    Article  CAS  Google Scholar 

  • Friesl-Hanl W, Platzer K, Horak O, Gerzabek MH (2009) Immobilising of Cd, Pb, and Zn contaminated arable soils close to a former Pb/Zn smelter: a field study in Austria over 5 years. Environ Geochem Health 31:581–594

    Article  CAS  Google Scholar 

  • Gajewska E, Sklodowska M, Slaba M, Mazur J (2006) Effect of nickel on antioxidative enzyme activities, proline and chlorophyll content in wheat shoots. Biol Plant 50:653–659

    Article  CAS  Google Scholar 

  • Gajewska E, Wielanek M, Bergier K, Skłodowska M (2009) Nickel-induced depression of nitrogen assimilation in wheat roots. Acta Physiol Plant 31:1291–1300

    Article  CAS  Google Scholar 

  • Gee GW, Bauder JW (1986) Particle-size analysis. In: Klute A (ed) Methods soil anal. Part 1: physical and mineralogical methods. Agron Monogr 9. Soil Sci Soc Am. Madison, USA, p 383–409

  • Ghasemi R, Ghaderian SM, Kramer U (2009) Interference of nickel with copper and iron homeostasis contributes to metal toxicity symptoms in the nickel hyperaccumulator plant Alyssum inflatum. New Phytol 184:566–580

    Article  CAS  Google Scholar 

  • Gray CW, Dunham SJ, Dennis PG, Zhao FJ, McGrath SP (2006) Field evaluation of in situ remediation of a heavy metal contaminated soil using lime and red-mud. Environ Pollut 142:530–539

    Article  CAS  Google Scholar 

  • Guo Y, Marschner H (1995) Uptake, distribution, and binding of cadmium and nickel in different plant species. J Plant Nutr 18:2691–2706

    Article  CAS  Google Scholar 

  • Hambidge KM, Miller LV, Westcott JE, Sheng X, Krebs NF (2010) Zinc bioavailability and homeostasis. Am J Clin Nutr 91:1478–1483

    Article  Google Scholar 

  • Haug W, Lantzsch H (1983) Sensitive method for the rapid determination of phytate in cereals and cereal products. J Sci Food Agric 34:1423–1426

    Article  CAS  Google Scholar 

  • Herath I, Kumarathilaka P, Navaratne A, Rajakaruna N, Vithanage M (2015) Immobilization and phytotoxicity reduction of heavy metals in serpentine soil using biochar. J Soils Sediments 15:126–138

    Article  CAS  Google Scholar 

  • Houben D, Evrard L, Sonnet P (2013a) Mobility, bioavailability and pH-dependent leaching of cadmium, zinc and lead in a contaminated soil amended with biochar. Chemosphere 92:1450–1457

    Article  CAS  Google Scholar 

  • Houben D, Evrard L, Sonnet P (2013b) Beneficial effects of biochar application to contaminated soils on the bioavailability of Cd, Pb and Zn and the biomass production of rapeseed (Brassica napus L.). Biomass Bioenergy 57:196–204

    Article  CAS  Google Scholar 

  • Hussain S, Maqsood MA, Aziz T, Basra SMA (2013) Zinc bioavailability response curvature in wheat grains under incremental zinc applications. Arch Agron Soil Sci 59:1001–1016

    Article  CAS  Google Scholar 

  • Ippolito JA, Barbarick KA, Elliott HA (2011) Drinking water treatment residuals: a review of recent uses. J Environ Qual 40:1–12

    Article  CAS  Google Scholar 

  • Iqbal M, Puschenreiter M, Oburger E, Santner J, Wenzel WW (2012) Sulfur-aided phytoextraction of Cd and Zn by Salix smithiana combined with in situ metal immobilization by gravel sludge and red mud. Environ Pollut 170:222–231

    Article  CAS  Google Scholar 

  • Jackson ML (1973) Soil chemical analysis. Prentice-hall of India Pvt. Ltd., New Delhi

    Google Scholar 

  • Kaplan M, Orman S (1998) Effect of elemental sulfur and sulfur containing waste in a calcareous soil in Turkey. J Plant Nutr 21:1655–1665

    Article  CAS  Google Scholar 

  • Khaliq A, Ali S, Hameed A, Farooq MA, Farid M, Shakoor MB, Mahmood K, Ishaque W, Rizwan M (2016) Silicon alleviates nickel toxicity in cotton seedlings through enhancing growth, photosynthesis and suppressing Ni uptake and oxidative stress. Arch Agron Soil Sci 62:633–647

    Article  CAS  Google Scholar 

  • Khanmohammadi Z, Afyuni M, Mosaddeghi MR (2015) Effect of pyrolysis temperature on chemical and physical properties of sewage sludge biochar. Waste Manag Res 33:275–283

    Article  CAS  Google Scholar 

  • Kimetu JM, Lehmann J, Ngoze S, Mugendi DN, Kinyangi JM, Riha S, Verchot L, Recha JW, Pell A (2008) Reversibility of soil productivity decline with organic matter of differing quality along a degradation gradient. Ecosystems 11:726–739

    Article  CAS  Google Scholar 

  • Krebs R, Gupta SK, Furrer G, Schulin R (1999) Gravel sludge as an immobilising agent in soils contaminated by heavy metals: a field study. Water Air Soil Pollut 115:465–479

    Article  CAS  Google Scholar 

  • Laulhere JP, Lescure AM, Briat JF (1988) Purification and characterization of ferritins from maize, pea, and soybean seeds distribution in various pea organs. J Biol Chem 263:10289–10294

    CAS  Google Scholar 

  • Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese and copper. Soil Sci Soc Am J 42:421–428

    Article  CAS  Google Scholar 

  • Loneragan JF, Grunes DL, Welch RM, Aduayi EA, Tengah A, Lazar VA, Cary EE (1982) Phosphorus accumulation and toxicity in leaves in relation to zinc supply. Soil Sci Soc Am J 46:345–352

    Article  CAS  Google Scholar 

  • Lonnerdal B (2007) The importance and bioavailability of phytoferritin- bound iron in cereals and legume foods. Int J Vitam Nutr Res 77:152–157

    Article  CAS  Google Scholar 

  • Lothenbach B, Krebs R, Furrer G, Gupta SK, Schulin R (1998) Immobilization of cadmium and zinc in soil by Al-montmorillonite and gravel sludge. Eur J Soil Sci 49:141–148

    Article  CAS  Google Scholar 

  • Lott JNA, Greenwood JS, Batten GD (1995) Mechanisms and regulation of mineral nutrient storage during seed development. In: Kigel J, Galili G (eds) Seed development and germination. Marcel Dekker, New York, pp. 215–235

    Google Scholar 

  • Lukac RJ, Aluru MA, Reddy MB (2009) Quantification of ferritin from staple food crops. J Agric Food Chem 57:2155–2161

    Article  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press Inc., San Diego

    Google Scholar 

  • Meng F, Wei Y, Yang X (2005) Iron content and bioavailability in rice. J Trace Elem Med Biol 18:333–338

    Article  CAS  Google Scholar 

  • Michael B, Zink E, Lantzsch HJ (1980) Effect of phosphate application on phytin-phosphorus and other phosphate fractions in developing wheat grains. Z Pflanzenernaehr Bodenkd 143:369–376

    Article  CAS  Google Scholar 

  • Modaihsh S, Al-mustafa WA, Metwally AE (1989) Effect of elemental sulfur on chemical changes and nutrient availability in calcareous soils. Plant Soil 116:95–101

    Article  CAS  Google Scholar 

  • Mulligan CN, Yong RN, Gibbs BF (2001) Surfactant-enhanced remediation of contaminated soil: a review. Eng Geol 60:371–380

    Article  Google Scholar 

  • Namgay T, Singh B, Singh BP (2010) Influence of biochar application to soil on the availability of As, Cd, Cu, Pb and Zn to maize (Zea mays L.). Aust J Soil Res 48:638–647

    Article  CAS  Google Scholar 

  • Nelson DW, Sommers LE (1982) Total carbon, organic carbon and organic matter. In: Klute A (ed) Methods of soil analysis, part 2: chemical and microbiological properties. Soil Science Society of America, Madison, pp. 570–571

    Google Scholar 

  • Nishida S, Aisu A, Mizuno T (2012) Induction of IRT1 by the nickel-induced iron-deficient response in Arabidopsis. Plant Signal Behav 7:13–19

    Article  Google Scholar 

  • Ogawa M, Tanaka K, Kasai Z (1977) Note on the phytin containing particles isolated from rice scutellum. Cereal Chem 54:1029–1034

    CAS  Google Scholar 

  • Olaniran AO, Balgobind A, Pillay B (2013) Bioavailability of heavy metals in soil: impact on microbial biodegradation of organic compounds and possible improvement strategies. Int J Mol Sci 14:10197–10228

    Article  Google Scholar 

  • Ouzounidou G, Moustakas M, Symeonidis L, Karataglis S (2006) Response of wheat seedlings to Ni stress: effects of supplemental calcium. Arch Environ Contam Toxicol 50:346–352

    Article  CAS  Google Scholar 

  • Panda BB, Sharma S, Mohapatra PK, Das A (2014) Iron nutrition vis-à-vis aconitase activity and ferritin accumulation in tropical indica rice cultivars differing in grain iron concentration. Am J Plant Sci 5:2829–2841

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Prom-u-thai C, Glahn PR, Cheng Z, Fukai S, Rerkasem B, Huang L (2009) The bioavailability of iron fortified in whole grain parboiled rice. Food Chem 89:2565–2571

    CAS  Google Scholar 

  • Qureshi S, Richards BK, Steenhuis TS, McBride MB, Baveye P, Dousset S (2004) Microbial acidification and pH effects on trace element release from sewage sludge. Environ Pollut 132:61–71

    Article  CAS  Google Scholar 

  • Raboy V, Dickinson DB (1993) Phytic acid levels in seeds of Glycine max and G. soja as influenced by phosphorus status. Crop Sci 33:1300–1305

    Article  CAS  Google Scholar 

  • Rahman H, Sabreen S, Alam S, Kawai S (2005) Effects of nickel on growth and composition of metal micronutrients in barley plants grown in nutrient solution. J Plant Nutr 28:393–404

    Article  CAS  Google Scholar 

  • Rajkumar M, Freitas H (2008) Effects of inoculation of plant-growth promoting bacteria on Ni uptake by Indian mustard. Bioresour Technol 99:3491–3498

    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 soil and its phyto-availability to wheat and rice under rotation. Environ Sci Pollut Res 22:16897–16906

    Article  CAS  Google Scholar 

  • Rengel Z, Graham RD (1995) Wheat genotypes differ in zinc efficiency when grown in the chelate-buffered nutrient solution. II. Nutrient uptake. Plant Soil 176:317–324

    Article  CAS  Google Scholar 

  • Rizwan M, Ali S, Adrees M, Rizvi H, Rehman MZ, Hannan F, Qayyum MF, Hafeez F, Ok YS (2016a) Cadmium stress in rice: toxic effects, tolerance mechanisms and management: a critical review. Environ Sci Pollut Res. doi:10.1007/s11356-016-6436-4

    Google Scholar 

  • Rizwan M, Ali S, Qayyum MF, Ibrahim M, Rehman MZ, Abbas T, Ok YS (2016c) Mechanisms of biochar-mediated alleviation of toxicity of trace elements in plants: a critical review. Environ Sci Pollut Res 23:2230–2248

    Article  CAS  Google Scholar 

  • Rizwan M, Meunier JD, Davidian JC, Pokrovsky OS, Bovet N, Keller C (2016b) Silicon alleviates Cd stress of wheat seedlings (Triticum turgidum L. cv. Claudio) grown in hydroponics. Environ Sci Pollut Res 23:1414–1427

    Article  CAS  Google Scholar 

  • Rizwan M, Ali S, Abbas T, Rehman MZ, Hannan F, Keller C, Al-Wabel MI, Ok YS (2016d) Cadmium minimization in wheat: a critical review. Ecotoxicol Environ Saf 130:43–53

  • Rizwan M, Meunier JD, Hélène M, Keller C (2012) Effect of silicon on reducing cadmium toxicity in durum wheat (Triticum turgidum L. cv. Claudio W.) grown in a soil with aged contamination. J Hazard Mater 209-210:326–334

    Article  CAS  Google Scholar 

  • Roitto M, Rautio P, Julkunen-Tiitto R, Kukkola E, Huttunen S (2005) Changes in the concentrations of phenolics and photosynthates in Scots pine (Pinus sylvestris L.) seedlings exposed to nickel and copper. Environ Pollut 137:603–609

    Article  CAS  Google Scholar 

  • Rubio MI, Escrig I, Martínez-Cortina C, López-Benet F, Sanz A (1994) Cadmium and nickel accumulation in rice plants. Effects on mineral nutrition and possible interactions of abscisic and gibberellic acids. Plant Growth Regul 14:151–157

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Solaiman ZM, Blackwell P, Abbott LK, Storer P (2010) Direct and residual effect of biochar application on mycorrhizal root colonisation, growth and nutrition of wheat. Aust J Soil Res 48:546–554

    Article  CAS  Google Scholar 

  • Sruthy OA, Jayalekshmi S (2014) Electrokinetic remediation of heavy metal contaminated soil. Int J Struct Civil Eng Res 3:103–111

    Google Scholar 

  • Steel RGD, Torrie JH, Dickey DA (1997) Principles and procedures of statistics: a biometrical approach, 3rd edn. McGraw-Hill Publishing Co., New York

    Google Scholar 

  • Theil EC, Briat JF (2004) Plant ferritin and non-heme iron nutrition in humans; harvest plus technical monograph 1; International Food Policy Research Institute and International Center for Tropical. Agriculture, Washington DC

    Google Scholar 

  • Thiel J, Riewe D, Rutten T, Melzer M, Friedel S, Bollenbeck F, Weschke W, Weber H (2012) Differentiation of endosperm transfer cells of barley: a comprehensive analysis at the micro-scale. Plant J 71:639–655

    Article  CAS  Google Scholar 

  • Usman ARA, Alkredaa RS, Al-Wabel MI (2013) Heavy metal contamination in sediments and mangroves from the coast of RedSea: Avicennia marina as potential metal bioaccumulator. Ecotoxicol Environ Saf 97:263–270

    Article  CAS  Google Scholar 

  • Velikova V, Tsonev T, Loreto F, Centritto M (2010) Changes in photosynthesis, mesophyll conductance to CO2, and isoprenoid emissions in Populus nigra plants exposed to excess nickel. Environ Pollut 1–9

  • Wang J, Pan X, Liu Y, Zhang X, Xiong Z (2012) Effects of biochar amendment in two soils on greenhouse gas emissions and crop production. Plant Soil 360:287–298

    Article  CAS  Google Scholar 

  • Wang K, Gao F, Ji YX, Liu Y, Dan ZW, Yang PF, Zhu YG, Li SQ (2013a) ORFH79 impairs mitochondrial function via interaction with a subunit of electron transport chain complex III in Honglian cytoplasmic male sterile rice. New Phytol 198:408–418

    Article  CAS  Google Scholar 

  • Watanabe FS, Olsen SR (1965) Test of an ascorbic acid method for determining phosphorus in water and NaHCO3 extracts. Soil Sci Soc Am Proc 29:677–678

    Article  CAS  Google Scholar 

  • Welch RM, Graham RD (2004) Breeding for micronutrients in staple food crops from a human nutrition perspective. J Exp Bot 55:353–364

    Article  CAS  Google Scholar 

  • Wood BW (2013) Iron-induced nickel deficiency in pecan. Hortic Sci 48:1145–1153

    CAS  Google Scholar 

  • Yang X, Baligar VC, Martens DC, Clark PB (1996) Plant tolerance to nickel toxicity. II Nickel effect on influx and transport of mineral nutrients in four plant species. J Plant Nutr 19:265–279

    Article  CAS  Google Scholar 

  • Zhou JR, Erdman JW Jr (1995) Phytic acid in health and disease. Crit Rev Food Sci Nutr 35:495–508

    Article  CAS  Google Scholar 

  • Zielińska-Dawidziak M (2015) Plant ferritin—a source of iron to prevent its deficiency. Nutrients 7:1184–1201

    Article  Google Scholar 

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We are highly thankful to the Higher Education Commission (HEC), Pakistan, and Government College University, Faisalabad, Pakistan, for their financial support.

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Correspondence to Muhammad Iqbal.

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Communicated by: Elena Maestri

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Ramzani, P.M.A., Khan, WuD., Iqbal, M. et al. Effect of different amendments on rice (Oryza sativa L.) growth, yield, nutrient uptake and grain quality in Ni-contaminated soil. Environ Sci Pollut Res 23, 18585–18595 (2016). https://doi.org/10.1007/s11356-016-7038-x

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