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Response of uptake and translocation of phenanthrene to nitrogen form in lettuce and wheat seedlings

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Abstract

Polycyclic aromatic hydrocarbons (PAHs) are widespread chemicals that are potentially carcinogenic and toxic to human due to dietary intake of food crops contaminated by PAHs. To date, the mechanisms underlying root uptake and acropetal translocation of PAHs in crops are poorly understood. Here we describe uptake and translocation of phenanthrene (a model PAH) in relation to nitrogen form and concentration in wheat and lettuce seedlings. At concentrations of 0–15 mM, phenanthrene uptake by roots is enhanced with an increase in ammonium and inhibited with an increment of nitrate. Phenanthrene concentration in shoots is much lower than in roots, suggesting that the direction of phenanthrene transport is acropetal. Ammonium reduces both phenanthrene accumulation and bioconcentration factor in shoots, as well as translocation factor, but nitrate elevates them. Phenanthrene uptake increases nutrient solution pH in the treatments with either nitrate or ammonium. Thus, it is concluded that the root uptake and acropetal translocation of phenanthrene in crops are associated with nitrogen form. Our results provide both a novel insight into the mechanism on PAH transport in higher plants and a promising agronomic strategy to minimize PAH contamination in crops or to improve phytoremediation of PAH-contaminated soils or water via nitrogen management.

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References

  • Adler PR, Wilcox GE, Markhart AH (1996) Ammonium decreases muskmelon root system hydraulic conductivity. J Plant Nutr 19(10–11):1395–1403

    Article  CAS  Google Scholar 

  • Cai Q, Mo C, Wu Q, Katsoyiannisc A, Zeng Q (2008) The status of soil contamination by semivolatile organic chemicals (SVOCs) in China: a review. Sci Total Environ 389:209–224

    Article  CAS  Google Scholar 

  • Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351–368

    Article  CAS  Google Scholar 

  • Chapin FS, Vitousek PM, Vancleve K (1986) The nature of nutrient limitation in plant-communities. Am Nat 127(1):48–58

    Article  Google Scholar 

  • Chapin FS, Moilanen L, Kielland K (1993) Preferential use of organic nitrogen for growth by a non-mycorrhizal article sedge. Nature 361:150–153

    Article  CAS  Google Scholar 

  • Chiou CT, McGroddy SE, Kile DE (1998) Partition characteristics of polycyclic aromatic hydrocarbons on soils and sediments. Environ Sci Technol 32:264–268

    Article  CAS  Google Scholar 

  • Collins CD, Finnegan E (2010) Modeling the plant uptake of organic chemicals, including the soil-air-plant pathway. Environ Sci Technol 44(3):998–1003

    Article  CAS  Google Scholar 

  • Duan Y, Zhang Y, Shen Q, Wang S (2006) Nitrate effect on rice growth and nitrogen absorption and assimilation at different growth stages. Pedosphere 16(6):707–717

    Article  Google Scholar 

  • Falco G, Doming JL, Llobet JM, Teixido A, Casas C, Muller L (2003) Polycyclic aromatic hydrocarbons in foods: human exposure through the diet in Catalonia, Spain. J Food Prot 66(12):2325–2331

    CAS  Google Scholar 

  • Gao Y, Zhu L (2004) Plant uptake, accumulation and translocation of phenanthrene and pyrene in soils. Chemosphere 55:1169–1178

    Article  CAS  Google Scholar 

  • Gent MPN, White JC, Parrish ZD, Isleyen M, Eitzer BD, Mattina MI (2007) Uptake and translocation of p,p-dichlorodiphenyldichloroethylene supplied in hydroponics solution to Cucurbita. Environ Toxicol Chem 26(12):2467–2475

    Article  CAS  Google Scholar 

  • Greenway H, Kulichikhin KY, Cawthray GR, Colmer TD (2012) pH regulation in anoxic rice coleoptiles at pH 3.5: biochemical pHstats and net H+ influx in the absence and presence of NO3 −. J Exp Bot 63(5):1969–1983

    Article  CAS  Google Scholar 

  • Guo S, Brük H, Sattelmacher B (2002) Effects of supplied nitrogen from on growth and water uptake of French bean (Phaseolus vulgaris L.) plants. Plant Soil 239:267–275

    Article  CAS  Google Scholar 

  • Guo F, Young J, Crawford NM (2003) The nitrate transporter AtNRT1.1 (CHL1) functions in stomatal opening and contributes to drought susceptibility in Arabidopsis. Plant Cell 15:107–117

    Article  CAS  Google Scholar 

  • Hartmann R (1996) Polycyclic aromatic hydrocarbons (PAHs) in forest soils: critical evaluation of a new analytical procedure. Int J Environ Anal Chem 62:161–173

    Article  CAS  Google Scholar 

  • Helali SM, Nebli H, Kaddour R, Mahmoudi H, Lachaâl M, Ouerghi Z (2010) Influence of nitrate-ammonium ratio on growth and nutrition of Arabidopsis thaliana. Plant Soil 336(1–2):65–74

    Article  Google Scholar 

  • Hinsinger P, Plassard C, Tang C, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248(1–2):43–59

    Article  CAS  Google Scholar 

  • Howard JW, Fazio T (1970) A review of polycyclic aromatic hydrocarbons in foods. Ind Med Surg 39(10):435–440

    CAS  Google Scholar 

  • Huang W, Yu H, Weber JWJ (1998) Hysteresis in the sorption and desorption of hydrophobic organic contaminants by soil and sediments: 1. A comparative analysis of experimental protocols. J Contam Hydrol 31:129–148

    Article  CAS  Google Scholar 

  • Jiao X, Xu F, Dawson R, Chen S, Tao S (2007) Adsorption and absorption of polycyclic aromatic hydrocarbons to rice roots. Environ Pollut 148:230–235

    Article  CAS  Google Scholar 

  • Jing J, Zhang F, Rengel Z, Shen J (2012) Localized fertilization with P plus N elicits an ammonium-dependent enhancement of maize root growth and nutrient uptake. Field Crop Res 133:176–185

    Article  Google Scholar 

  • Kipopoulou AM, Manoli E, Samara C (1999) Bioconcentration of polycyclic aromatic hydrocarbons in vegetables grown in industrial area. Environ Pollut 106:369–380

    Article  CAS  Google Scholar 

  • Lu Y, Li C, Zhang F (2005) Transpiration, potassium uptake and flow in tobacco as affected by nitrogen forms and nutrient levels. Ann Bot 95:991–998

    Article  CAS  Google Scholar 

  • Nadal M, Schunhmacher M, Domingo JL (2004) Levels of PAHs in soil and vegetation samples from Tarragona County, Spain. Environ Pollut 132:1–11

    Article  CAS  Google Scholar 

  • Schwab AP, Al-Assi AA, Banks MK (1998) Adsorption of naphthalene onto plant roots. J Environ Qual 27:220–224

    Article  CAS  Google Scholar 

  • Su Y, Zhu Y (2008) Uptake of selected PAHs from contaminated soils by rice seedlings (Oryza sativa) and influence of rhizosphere on PAH distribution. Environ Pollut 155:359–365

    Article  CAS  Google Scholar 

  • Tang C, Conyers MK, Nuruzzaman M, Poile GJ, Liu D (2011) Biological amelioration of subsoil acidity through managing nitrate uptake by wheat crops. Plant Soil 338(1–2):383–397

    Article  CAS  Google Scholar 

  • Thomson CJ, Marschner H, Römheld V (1993) Effect of nitrogen-fertilizer form on pH of the bulk soil and rhizosphere, and on the growth, phosphorus, and micronutrient uptake of bean. J Plant Nutr 16(3):493–506

    Article  CAS  Google Scholar 

  • Voutsa D, Samara C (1998) Dietary intake of trace elements and polycyclic aromatic hydrocarbons via vegetables grown in an industrial Greek area. Sci Total Environ 218:203–216

    Article  CAS  Google Scholar 

  • Wang G, Li C, Zhang F (2003) Effects of different nitrogen forms and combination with foliar spraying with 6-benzylaminopurine on growth, transpiration, and water and potassium uptake and flow in tobacco. Plant Soil 256:169–178

    Article  CAS  Google Scholar 

  • Wang S, Zhu Y, Jiang H, Cao W (2006a) Positional differences in nitrogen and sugar concentrations of upper leaves relate to plant N status in rice under different N rates. Field Crop Res 96:224–234

    Article  Google Scholar 

  • Wang X, Liu R, Wang K, Hu J, Ye Y, Zhang S, Xu F, Tao S (2006b) Application of multivariate spatial analysis in scale-based distribution and source study of PAHs in the topsoil: an example from Tianjin, China. Environ Geol 49:1208–1216

    Article  CAS  Google Scholar 

  • Weligama C, Tang C, Sale PWG, Conyers MK, Liu D (2010) Application of nitrogen in NO3 − form increases rhizosphere alkalization in the subsurface soil layers in an acid soil. Plant Soil 333(1–2):403–416

    Article  CAS  Google Scholar 

  • Whitfield Åslund ML, Rutter A, Reimer KJ, Zeeb BA (2008) The effects of repeated planting, planting density, and specific transfer pathways on PCB uptake by Cucurbita pepo grown in field conditions. Sci Total Environ 405:14–25

    Article  Google Scholar 

  • Wild SR, Jones KC (1992) Organic chemicals entering agricultural soils in sewage sludges: screening for their potential to transfer to crop plants and livestock. Sci Total Environ 119:85–119

    Article  CAS  Google Scholar 

  • Wild SR, Jones KC (1995) Polynuclear aromatic hydrocarbons in the United Kingdom environment: a preliminary source in inventory and budget. Environ Pollut 88:91–108

    Article  CAS  Google Scholar 

  • Wild E, Dent J, Thomas GO, Jones KC (2005) Direct observation of organic contaminant uptake, storage, and metabolism within plant roots. Environ Sci Technol 39:3695–3702

    Article  CAS  Google Scholar 

  • Win T, Luther W, Jacob J, Vaessen HAMG, Boenke A (1998) Reference materials for PAHs in foodstuffs: results of the certification exercise of two coconut oil reference materials. Fresenius J Anal Chem 360:640–644

    Article  CAS  Google Scholar 

  • Xiao B, Yu Z, Huang W, Song J, Peng P (2004) Black carbon and kerogen in soils and sediments. 2. Their roles in equilibrium sorption of less-polar organic pollutants. Environ Sci Technol 38:5842–5852

    Article  CAS  Google Scholar 

  • Xie H, Jiang R, Zhang F, McGrath SP, Zhao F (2009) Effect of nitrogen form on the rhizosphere dynamics and uptake of cadmium and zinc by the hyperaccumulator Thlaspi caerulescens. Plant Soil 318:205–215

    Article  CAS  Google Scholar 

  • Xu S, Chen Y, Wu W, Wang K, Lin Q, Liang X (2006) Enhanced dissipation of phenanthrene and pyrene in spiked soils by combined plants cultivation. Sci Total Environ 363:206–215

    Article  CAS  Google Scholar 

  • Yang Z, Zhu L (2007) Performance of the partition-limited model on predicting ryegrass uptake of polycyclic aromatic hydrocarbons. Chemosphere 67:402–409

    Article  CAS  Google Scholar 

  • Yin X, Liang X, Xu G, Zhan X (2014) Effect of phenanthrene uptake on membrane potential in roots of soybean, wheat and carrot. Environ Exp Bot 99:53–58

    Article  CAS  Google Scholar 

  • Zaccheo P, Crippa L, Pasta VDM (2006) Ammonium nutrition as a strategy for cadmium mobilization in the rhizosphere of sunflower. Plant Soil 283(1–2):43–56

    Article  CAS  Google Scholar 

  • Zhan X, Ma H, Zhou L, Liang J, Jiang T, Xu G (2010) Accumulation of phenanthrene by roots of intact wheat (Triticum aestivum L.) seedlings: passive or active uptake? BMC Plant Biol 10:52

    Article  Google Scholar 

  • Zhan X, Zhang X, Yin X, Ma H, Liang J, Zhou L, Jiang T, Xu G (2012) H+/phenanthrene symporter and aquaglyceroporin are implicated in phenanthrene uptake by wheat (Triticum aestivum L.). J Environ Qual 41:188–196

    Article  CAS  Google Scholar 

  • Zhan X, Liang X, Jiang T, Xu G (2013a) Interaction of phenanthrene and potassium uptake by wheat roots: a mechanistic model. BMC Plant Biol 13:168

    Article  Google Scholar 

  • Zhan X, Liang X, Xu G, Zhou L (2013b) Influence of plant root morphology and tissue composition on phenanthrene uptake: stepwise multiple linear regression analysis. Environ Pollut 179:294–300

    Article  CAS  Google Scholar 

  • Zhang Y, Tao S (2008) Seasonal variation of polycyclic aromatic hydrocarbons (PAHs) emissions in China. Environ Pollut 156:657–663

    Article  CAS  Google Scholar 

  • Zhou Q, Sun T (2004) Effects of environmental pollution on terrestrial ecosystem. In: Ye C, Wang C, Jin L (eds) Environmental chemistry for the 21st century. Science, Beijing, pp 219–227

    Google Scholar 

  • Zhou Y, Zhang Y, Wang X, Cui J, Xia X, Shi K, Yu J (2011) Effects of nitrogen form on growth, CO2 assimilation, chlorophyll fluorescence, and photosynthetic electron allocation in cucumber and rice plants. J Zhejiang Univ Sci B 12(2):126–134

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by the National Natural Science Foundation of China (31370521), the Fundamental Research Funds for the Central Universities (KYZ201145), and the Open Fund of the State Key Laboratory of Soil and Sustainable Agriculture (Institute of Soil Science, Chinese Academy of Sciences, 0812201223).

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Authors and Affiliations

  1. College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, Jiangsu, 210095, People’s Republic of China

    Xinhua Zhan, Jiahan Yuan, Le Yue & Guohua Xu

  2. State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, Jiangsu, 210008, People’s Republic of China

    Xinhua Zhan & Renkou Xu

  3. College of Life Sciences, Nanjing Agricultural University, Nanjing, Jiangsu, 210095, People’s Republic of China

    Bing Hu

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  1. Xinhua Zhan
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  2. Jiahan Yuan
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  4. Guohua Xu
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  5. Bing Hu
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  6. Renkou Xu
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Correspondence to Xinhua Zhan.

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Responsible editor: Philippe Garrigues

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Zhan, X., Yuan, J., Yue, L. et al. Response of uptake and translocation of phenanthrene to nitrogen form in lettuce and wheat seedlings. Environ Sci Pollut Res 22, 6280–6287 (2015). https://doi.org/10.1007/s11356-014-3834-3

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  • DOI: https://doi.org/10.1007/s11356-014-3834-3

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