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Element uptake and physiological responses of Lactuca sativa upon co-exposures to tourmaline and dissolved humic acids

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Abstract

Element migration and physiological response in Lactuca sativa upon co-exposure to tourmaline (T) and dissolved humic acids (DHAs) were investigated. Different fractions of DHA1 and DHA4 and three different doses of T were introduced into Hoagland’s solution. The results indicated that T enhanced the contents of elements such as N and C, Si and Al in the roots and shoots. The correlation between TF values of Si and Al (R2 = 0.7387) was higher than that of Si and Mn (R2 = 0.4961) without the presence of DHAs. However, both DHA1 and DHA4 increased the correlation between Si and Mn, but decreased the one between Si and Al. CAT activities in T treatments were positively correlated to the contents of N and Al in the shoots, whose R2 was 0.9994 and 0.9897, respectively. In the co-exposure of DHAs and tourmaline, DHA4 exhibited more impacts on element uptake, CAT activities, as well as ABA contents in comparison with the presence of DHA1, regardless of the T exposure doses. These results suggested that DHAs have effects on mineral element behaviors and physiological response in Lactuca sativa upon exposure to tourmaline for the first time, which had great use in guiding soil remediation.

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References

  • Atiyeh RM, Lee S, Edwards CA, Arancon NQ, Metzger JD (2002) The influence of humic acids derived from earthworm processed organic wastes on plant growth. Bioresour Technol 84:7–14

    Article  CAS  Google Scholar 

  • Birchall JD (1990) The role of silicon in biology. Chem Britain 26:141–144

    CAS  Google Scholar 

  • Borlotti A, Vigani G, Zocchi G (2012) Iron deficiency affects nitrogen metabolism in cucumber (Cucumis sativus L.) plants. Plant Biol 12:189–204

    CAS  Google Scholar 

  • Chan MT, Selvam A, Wong JWC (2016) Reducing nitrogen loss and salinity during ‘struvite’ food waste composting by zeolite amendment. Bioresour Technol 200:838–844

    Article  CAS  Google Scholar 

  • Christl I, Milne CJ, Kinniburgh DG, Kretzschmar R (2001) Relating ion binding by fulvic and humic acids to chemical composition and molecular size 2 metal binding. Environ Sci Technol 35:2512–2517

    Article  CAS  Google Scholar 

  • Cordeiro FC, Santa-Catarina C, Silveira V, de Souza SR (2011) Humic acid effect on catalase activity and the generation of reactive oxygen species in corn (Zea Mays L). Biosci Biotechnol Biochem 75:70–74

    Article  CAS  Google Scholar 

  • Desouky MM, Powell JJ, Jugdaohsingh R, White KN, McCrohan CR (2002) Influence of oligomeric silicic and humic acids on aluminum accumulation in a freshwater grazing invertebrate. Ecotoxicol Environ Saf 53:382–387

    Article  CAS  Google Scholar 

  • Dobranskyte A, Jugdaohsingh R, McCrohan CR, Stuchlik E, Powell JJ, White KN (2006) Effect of humic acid on water chemistry, bioavailability and toxicity of aluminium in the freshwater snail, Lymnaea stagnalis, at neutral pH. Environ Pollut 140:340–347

    Article  CAS  Google Scholar 

  • Frankowski M (2014) Aluminium and its complexes in teas and fruity brew samples, speciation and ions determination by ion chromatography and high performance liquid chromatography-fluorescence analytical methods. Food Anal Method 27:1109–1117

    Article  Google Scholar 

  • Ghanati F, Moritam A, Yokota H (2005) Effects of aluminum on the growth of tea plant and activation of antioxidant system. Plant Soil 276:133–141

    Article  CAS  Google Scholar 

  • Guo LD, Hunt BJ, Santschi PH (2001) Ray S.M. effect of dissolved organic matter on the uptake of trace metals by American oysters. Environ Sci Technol 35:885–893

    Article  CAS  Google Scholar 

  • González MA, Pavlovic I, Rojas-Delgado R, Barriga C (2014) Removal of Cu2+, Pb2+ and Cd2+ by layered double hydroxide-humate hybrid, sorbate and sorbent comparative studies. Chem Eng J 254:605–611

    Article  CAS  Google Scholar 

  • Han N, Thompson ML (1999) Copper-binding ability of dissolved organic matter derived from anaerobically digested biosolids. J Environ Qual 5-6:939–944

    Article  Google Scholar 

  • Hao Y, Yu FF, Lv RT, Ma CX, Zhang ZT, Rui YK, Liu LM, Cao WD, Xing BS (2016) Carbon nanotubes filled with different ferromagnetic alloys affect the growth and development of rice seedlings by changing the C:N ratio and plant hormones concentrations. PLoS One 11:1–19

    CAS  Google Scholar 

  • Hofman G, Cleemput OV (2004) Soil and plant nitrogen. Internat Fertiliz Indust Associat Paris

  • Imtiaz M, Rizwan MS, Mushtaq MA, Ashraf M, Shahzad SM, Yousaf B, Saeed DA, Rizwan M, Nawaz MA, Mehmood S, Tu SX (2016) Silicon occurrence, uptake, transport and mechanisms of heavy metals, minerals and salinity enhanced tolerance in plants with future prospects: a review. J Environ Manag 183:521–529

    Article  CAS  Google Scholar 

  • Iwasaki K, Matsumura A (1999) Effect of silicon on alleviation of manganese toxicity in pumpkin (Cucurbita moschata Duch cv Shintosa). Soil Sci Plant Nutr 45:909–920

    Article  CAS  Google Scholar 

  • Iwasaki K, Maier P, Fecht M, Horst WJ (2002a) Effects of silicon supply on apoplastic manganese concentrations in leaves and their relation to manganese tolerance in cowpea (Vigna unguiculata (L) Walp). Plant Soil 238:281–288

    Article  CAS  Google Scholar 

  • Iwasaki K, Maier P, Fecht M, Horst WJ (2002b) Leaf apoplastic silicon enhances manganese tolerance of cowpea (Vigna unguiculata). J Plant Physiol 159:167–173

    Article  CAS  Google Scholar 

  • Jarosz Z (2013) The effect of silicon application and type of substrate on yield and chemical composition of leaves and fruit of cucumber. J Elem 3:403–414

    Google Scholar 

  • Jiang F, Hartung W (2008) Long-distance signalling of abscisic acid (ABA): the factors regulating the intensity of the ABA signal. J Exp Bot 59:37–43

    Article  CAS  Google Scholar 

  • Kang S, Xing B (2005) Phenanthrene sorption to sequentially extracted soil humic acids and humin. Environ Sci Technol 39:134–140

    Article  CAS  Google Scholar 

  • Kidd PS, Llugany M, Poschenrieder C, Gunse B, Barcelo J (2001) The role of root exudates in aluminium resistance and silicon-induced amelio ration of aluminium toxicity in three varieties of maize (Zea mays L.) J Exp Bot 52:1339–1352

    CAS  Google Scholar 

  • Kleiber T, Calomme M, Borowiak K (2015) The effect of choline-stabilized orthosilicic acid on microelements and silicon concentration, photosynthesis activity and yield of tomato grown under Mn stress. Plant Physiol Biochem 96:180–188

    Article  CAS  Google Scholar 

  • Kupper H, Parameswaran A, Leitenmaier B, Trtilek M, Setlik I (2007) Cadmium-induced inhibition of photosynthesis and long-term acclimation to cadmium stress in the hyperaccumulator. New Phytol 175:655–674

    Article  Google Scholar 

  • Lazo DE, Dyer LG, Alorro RD (2017) Silicate, phosphate and carbonate mineral dissolution behaviour in the presence of organic acids: a review. Miner Eng 100:115−123

    Article  CAS  Google Scholar 

  • Lee TJ, Luitel BP, Kang WH (2011) Growth and physiological response to manganese toxicity in Chinese cabbage (Brassica rapa L. ssp. campestris). Hortic Environ Biotechnol 52:252–258

    Article  CAS  Google Scholar 

  • Li J, Wang CP, Wang D, Zhou ZY, Sun HW, Zhai S (2016) A novel technology for remediation of PBDEs contaminated soils using tourmaline-catalyzed Fenton-like oxidation combined with P. chrysosporium. Chem Eng J 296:319–328

    Article  CAS  Google Scholar 

  • Liang Y, Sun W, Zhu YG, Christie P (2007) Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: a review. Environ Pollut 147:422–428

    Article  CAS  Google Scholar 

  • Liang YC, Hua HX, Zhu YG, Zhang J, Cheng CM, Römheld V (2006) Importance of plant species and external silicon concentration to active silicon uptake and transport. New Phytol 172:63–72

    Article  CAS  Google Scholar 

  • Liu X, Han HM, Liu HB, Xiao SJ (2010) Enhanced protain loading on planar Si-H with second generation NTA. Surf Sci 604:1315–1319

    Article  CAS  Google Scholar 

  • Lydersen E, Poleo ABS, Muniz IP, Salbu B, Bjørnstad HE (1990) The effects of naturally occurring high and low molecular weight inorganic and organic species on the yolk-sack larvae of Atlantic salmon (Salmo salar L) exposed to acidic aluminium-rich lake water. Aquat Toxicol 18:219–230

    Article  CAS  Google Scholar 

  • Ma CX, Chhikara S, Xing BS, Musante C, White JC, Dhankher OP (2013) Physiological and molecular response of arabidopsis thaliana (L) to nanoparticle cerium and indium oxide exposure. ACS Sustain Chem Eng 1:768–778

    Article  CAS  Google Scholar 

  • Ma CX, Chhikara S, Minocha R, Long S, Musante C, White JC, Xing BS, Dhankher OP (2015) Reduced silver nanoparticle phytotoxicity in crambe abyssinica with enhanced glutathione production by overexpressing bacterial γ-Glutamylcysteine synthase. Environ Sci Technol 49:10117–10126

    Article  CAS  Google Scholar 

  • Ma CX, Liu H, Guo HY, Musante C, Coskun SH, Nelson BC, White JC, Xing BS, Dhankher OP (2016) Defense mechanisms and nutrient displacement in Arabidopsis thaliana upon exposure to CeO2 and In2O3 nanoparticles. Environ Sci: Nano 3:1369–1379

    CAS  Google Scholar 

  • Ma JF, Takahashi E (1989) Effect of silicic acid on phosphorus uptake by rice plant. Soil Sci Plant Nutr 35:227–234

    Article  CAS  Google Scholar 

  • Maji D, Misra P, Singh S, AKalra A (2017) Humic acid rich vermicompost promotes plant growth by improving microbial community structure of soil as well as root nodulation and mycorrhizal colonization in the roots of Pisum sativum. Appl Soil Ecol 110:97–108

    Article  Google Scholar 

  • Mazeika R, Dambrauskas T, Baltakys K (2016) Molecular and morphological structure of poultry manure derived organo-mineral fertilizers (OMFs). ACS Sustain Chem Eng 4:4788−4796

    Google Scholar 

  • Mora V, Bacaicoa E, Zamarreno AM (2010) Action of humic acid on promotion of cucumber shoot growth involves nitrate-related changes associated with the root-to-shoot distribution of cytokinins, polyamines and mineral nutrients. J Plant Physiol 167:633–642

    Article  CAS  Google Scholar 

  • Murthy TC, Weinberger P (1984) Measures MP uranium effects on the growth of soybean (Glycine max (L) Merr). Bull Environ Contam Toxicol 32:580–586

    Article  CAS  Google Scholar 

  • Nakamura T, Kubo T (1992) Tourmaline group crystals reaction water. Ferroelectrics 137:13–31

    Article  CAS  Google Scholar 

  • Nardi S, Pizzeghello D, Muscolo A, Vianello A (2002) Physiological effects of humic substances on higher plants. Soil Biol Biochem 34:1527–1536

    Article  CAS  Google Scholar 

  • Pellet DM, Papernik LA, Jones DL, Darrah PR, Grunes DL, Kochian LV (1997) Involvement of multiple aluminium exclusion mechanisms in aluminium tolerance in wheat. Plant Soil 192:63–68

    Article  CAS  Google Scholar 

  • Rezaee F, Ghanati F, Behmanesh M (2013) Antioxidant activity and expression of catalase gene of (Eustoma grandiflorum L) in response to boron and aluminum. South Afr J Bot 84:13–18

    Article  CAS  Google Scholar 

  • Rogalla H, Römheld V (2002) Role of leaf apoplast in silicon-mediated manganese tolerance of Cucumis sativus L. Plant Cell Environ 25:549–555

    Article  CAS  Google Scholar 

  • Ryan PR, Ditomaso JM, Kochian LV (1993) Aluminium toxicity in roots: an investigation of spatial sensitivity and the role of the root cap. J Exp Bot 44:437–446

    Article  CAS  Google Scholar 

  • Saminathan T, Malkaram SA, Taylor K, Patel D, Hass A, Nimmakayala P, Huber DH, Reddy UK (2015) Transcriptome analysis of ivasive plants in response to mineral toxicity of reclaimed coal-mine soil in the appalachian region. Environ Sci Technol 49:10320–10329

    Article  CAS  Google Scholar 

  • Sauvant MP, Pepin D, Guillot J (1999) Effects of humic substances and phenolic compounds on the in vitro toxicity of aluminium. Ecotoxicol Environ Saf 44:47–55

    Article  CAS  Google Scholar 

  • Schnitzer M, Khan SU (1972) Humic substances in the environment. Marcel Dekker, Inc, New York

    Google Scholar 

  • Shi QH, Bao ZY, Zhu ZJ, He Y, Qian QQ, Yu JQ (2005) Siliconmediated alleviation of Mn toxicity in Cucumis sativus in relation to activities of superoxide dismutase and ascorbate peroxidase. Phytochemistry 66:1551–1559

    Article  CAS  Google Scholar 

  • Shi Y, Huang ZB, Liu XJ, Imran S, Peng LC, Dai RJ, Deng Y (2016) Environmental materials for remediation of soils contaminated with lead and cadmium using maize (Zea mays L) growth as a bioindicator. Environ Sci Pollut Res 23:6168–6178

    Article  CAS  Google Scholar 

  • Valdrighi MM, Pera A, Agnolucci M, Frassinetti S, Lunardi D, Vallini G (1996) Effects of compost-derived humic acids on vegetable biomass production and microbial growth within a plant (Cichorium intybus)-soil system: a comparative study. Agric Ecosyst Environ 58:133–144

    Article  Google Scholar 

  • Wang BL, Wang CP, Li J, Sun HW, Xu Z (2014a) Remediation of alkaline soil with heavy metal contamination using tourmaline as a novel amendment. J Environ Chem Eng 2:1281–1286

    Article  CAS  Google Scholar 

  • Wang CP, Yu L, Zhang ZY, Wang BL, Sun HW (2014b) Tourmaline combined with Phanerochaete chrysosporium to remediate agricultural soil contaminated with PAHs and OCPs. J Hazard Mater 264:439–448

    Article  CAS  Google Scholar 

  • Welch SA, Ullman WJ (1993) The effect of organic acids on plagioclase dissolution rates and stoichiometry. Geochim Cosmochim Acta 157:2725–2736

    Article  Google Scholar 

  • Weng L, Van Riemsdijk WH, Koopal LK, Hiemstra T (2006) Adsorption of humic substances on goethite: comparison between humic acids and fulvic acids. Environ Sci Technol 40:7494–7500

    Article  CAS  Google Scholar 

  • Williams DE, Vlamis J (1975) The effect of silicon on yield and manganese-54 uptake and distribution in the leaves of barley plants grown in culture solutions. Plant Physiol 32:404–409

    Article  Google Scholar 

  • Wong JWC, Fung SO, Selvam A (2009) Coal fly ash and lime addition enhances the rate and efficiency of decomposition of food waste during composting. Bioresour Technol 100:3324–3331

    Article  CAS  Google Scholar 

  • Yamaji N, Mitatni N, Ma JF (2008) A transporter regulating silicon distributionin rice shoots. Plant Cell 20:1381–1389

    Article  CAS  Google Scholar 

  • Yue Q, Li Y, Gao B (2009) Impact factors and thermodynamic characteristics of aquatic humic acid loaded onto kaolin. Colloids Surf B 72:241–247

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Ministry of Science and Technology of China (2014CB441104) and Natural Science Foundation of China (41673104) and Tianjin Science and Technology Committee (17JCZDJC39600), Science and Technology Commission of Tianjin Binhai New Area (BHXQKJXM-PT-ZJSHJ-2017002), the Fundamental Research Funds for the Central Universities, and 111 program, Ministry of Education, China (T2017002).

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Correspondence to Cuiping Wang or Chuanxin Ma.

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Responsible editor: Philippe Garrigues

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Additional information including experimental design, characterization of DHAs, element analysis result, biomass of plant tissues and contents of total chlorophyll were provided in the supplementary document.

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Jia, W., Wang, C., Ma, C. et al. Element uptake and physiological responses of Lactuca sativa upon co-exposures to tourmaline and dissolved humic acids. Environ Sci Pollut Res 25, 15998–16008 (2018). https://doi.org/10.1007/s11356-018-1751-6

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