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Application of carotenoid to alleviate the oxidative stress caused by phenanthrene in wheat

  • Yu Shen
  • Jinfeng Li
  • Shengnan Shi
  • Ruochen Gu
  • Xinhua Zhan
  • Baoshan Xing
Research Article

Abstract

It is reported that the accumulated polycyclic aromatic hydrocarbons (PAHs) can cause wheat leaf chlorosis, and we identified that carotenoid (Car) and superoxide dismutase (SOD) are the two most active factors in antioxidant system in the previous study. Herein, we applied Car as an exogenous chemical added to alleviate the toxicity triggered by phenanthrene (a model PAH) in wheat seedlings. In the exogenous Car addition groups, we found that the leaf number would grow three, and the relative biomass and the relative root length of 20 mg L−1 Car added would take positive changes that increased by 171.35% and 108.08% of the phenanthrene-treated group at day 9, respectively. Under the subcellular structure, vacuole would be clear and clean, chloroplast and mitochondria shapes turned normal in the exogenous Car addition groups, and their osmophilic particle densities were much lower than the phenanthrene-treated group. Chlorophyll a, chlorophyll b, and total chlorophyll concentrations also recovered after Car was added in the phenanthrene treatments for 9 days. The activity of SOD, another active factor, also decreased when Car was added, and the values dropped to 16.54 and 24.61 U g−1 for the 10 and 20 mg L−1 Car addition groups, respectively. Like the SOD activity, malondialdehyde (MDA) concentrations of the two Car addition groups decreased to 26.50% and 26.87% of the phenanthrene treatment. The relative concentrations of 5 kinds of amino acids (valine, alanine, proline, aspartic acid, and lysine) recovered significantly, and the principal component analysis suggested that amino acid concentrations were in recovery progress when Car was added in phenanthrene treatments. Therefore, it is concluded that Car is an effective PAH toxicity relief. Our result offers a new way to improve the plant resistance to PAH pollution in the environment.

Graphical abstract

Keywords

Polycyclic aromatic hydrocarbons, Carotenoid, Detoxification, Wheat, Phenanthrene 

Notes

Funding information

This work was supported jointly by the National Natural Science Foundation of China (31770546, 31370521), the Key Talent-Inviting Project of Nanjing Agricultural University (X2017024), and the Graduate Student Training Innovation Project of Jiangsu Province (KYZZ16_0378). Yu Shen thanks the China Scholarship Council (CSC) for the financial support to study at the University of Massachusetts, Amherst.

References

  1. Allison MJ, Baetz AL, Wiegel J (1984) Alternative pathways for biosynthesis of leucine and other amino acids in Bacteroides ruminicola and Bacteroides fragilis. Appl Environ Microbiol 48:1111–1117Google Scholar
  2. Armstrong GA, Hearst JE (1996) Carotenoids 2: genetics and molecular biology of carotenoid pigment biosynthesis. FASEB J 10:228–237CrossRefGoogle Scholar
  3. Bozzola JJ (2007) Conventional specimen preparation techniques for transmission electron microscopy of cultured cells. In: Bozzola J (ed) Electron microscopy. Humana Press, New YorkGoogle Scholar
  4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254.  https://doi.org/10.1016/0003-2697(76)90527-3 CrossRefGoogle Scholar
  5. Burg SP, Burg EA (1966) The interaction between auxin and ethylene and its role in plant growth. P Natl Acad Sci USA 55:262–269CrossRefGoogle Scholar
  6. Chou K (2001) Prediction of protein cellular attributes using pseudo-amino acid composition. Proteins 43:246–255.  https://doi.org/10.1002/prot.1035 CrossRefGoogle Scholar
  7. Claessens M, Saris WH, Bouwman FG, Evelo CT, Hul GB, Blaak EE, Mariman EC (2007) Differential valine metabolism in adipose tissue of low and high fat-oxidizing obese subjects. Proteomics Clin Appl 1:1306–1315.  https://doi.org/10.1002/prca.200700049 CrossRefGoogle Scholar
  8. Dassot M, Constant T, Ningre F, Fournier M (2014) Impact of stand density on tree morphology and growth stresses in young beech (Fagus sylvatica L.) stands. Trees 29:583–591.  https://doi.org/10.1007/s00468-014-1137-4 CrossRefGoogle Scholar
  9. Dazy M, Jung V, Ferard JF, Masfaraud JF (2008) Ecological recovery of vegetation on a coke-factory soil: role of plant antioxidant enzymes and possible implications in site restoration. Chemosphere 74:57–63.  https://doi.org/10.1016/j.chemosphere.2008.09.014 CrossRefGoogle Scholar
  10. del Rio D, Stewart AJ, Pellegrini N (2005) A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardiovasc Dis 15:316–328.  https://doi.org/10.1016/j.numecd.2005.05.003 CrossRefGoogle Scholar
  11. Drozdov KA, Drozdov AL (2015) Variation in the contents of lactate and alanine in the coelomic fluid of the sea urchin Mesocentrotus nudus (A. Agassiz, 1863) indicates anaerobic glycolysis. Russ J Mar Biol 41:311–314.  https://doi.org/10.1134/S1063074015040069 CrossRefGoogle Scholar
  12. Du H, Liu H, Xiong L (2013) Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice. Front Plant Sci 4:397.  https://doi.org/10.3389/fpls.2013.00397 CrossRefGoogle Scholar
  13. Eagle H (1955) Nutrition needs of mammalian cells in tissue culture. Science 122:501–504CrossRefGoogle Scholar
  14. Farooq MA, Ali S, Hameed A, Ishaque W, Mahmood K, Iqbal Z (2013) Alleviation of cadmium toxicity by silicon is related to elevated photosynthesis, antioxidant enzymes; suppressed cadmium uptake and oxidative stress in cotton. Ecotox Environ Saf 96:242–249.  https://doi.org/10.1016/j.ecoenv.2013.07.006 CrossRefGoogle Scholar
  15. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930.  https://doi.org/10.1016/j.plaphy.2010.08.016 CrossRefGoogle Scholar
  16. Gorton HL, Williams WE, Vogelmann TC (1997) Chloroplast movement and whole leaf photosynthesis. Plant Physiol 114:390Google Scholar
  17. Guly MF (1980) Regulatory role of amino acids in protein biosynthesis 398 effect of various factors. Arch Anim Nutr 30:55–62CrossRefGoogle Scholar
  18. Guo WQ, Zhang PT, Li CH, Yin JM, Han X (2015) Recovery of root growth and physiological characters in cotton after salt stress relief. Chil J Agr Res 75:85–91.  https://doi.org/10.4067/S0718-58392015000100012 CrossRefGoogle Scholar
  19. Harding HP, Zhang Y, Zeng H, Novoa I, Lu P, Calfon M, Sadri N, Yun C, Popko B, Paules R, Stojdl DF, Bell JC, Hettmann T, Leiden JM, Ron D (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11:619–633CrossRefGoogle Scholar
  20. Hildebrandt TM, Nunes Nesi A, Araujo WL, Braun HP (2015) Amino acid catabolism in plants. Mol Plant 8:1563–1579.  https://doi.org/10.1016/S1097-2765(03)00105-9 CrossRefGoogle Scholar
  21. Hong Y, Liao D, Chen J, Khan S, Su J, Li H (2015) A comprehensive study of the impact of polycyclic aromatic hydrocarbons (PAHs) contamination on salt marsh plants Spartina alterniflora: 410 implication for plant-microbe interactions in phytoremediation. Environ Sci Pollut Res 22:7071–7081.  https://doi.org/10.1007/s11356-014-3912-6 CrossRefGoogle Scholar
  22. Hudson AO, Bless C, Macedo P, Chatterjee SP, Singh BK, Gilvarg C, Leustek T (2005) Biosynthesis of lysine in plants: evidence for a variant of the known bacterial pathways. Biochim Biophys Acta 1721:27–36.  https://doi.org/10.1016/j.bbagen.2004.09.008 CrossRefGoogle Scholar
  23. Jiang S, Lu H, Zhang Q, Liu J, Yan C (2016) Effect of enhanced reactive nitrogen availability on plant-sediment mediated degradation of polycyclic aromatic hydrocarbons in contaminated mangrove sediment. Mar Pollut Bull 103:151–158.  https://doi.org/10.1016/j.marpolbul.2015.12.027 CrossRefGoogle Scholar
  24. Kholova J, Hash C, Kocova M, Vadez V (2011) Does a terminal drought tolerance QTL contribute to differences in ROS scavenging enzymes and photosynthetic pigments in pearl millet exposed to drought? Environ Exp Bot 71:99–106.  https://doi.org/10.1016/j.envexpbot.2010.11.001 CrossRefGoogle Scholar
  25. Kosugi H, Kikugawa K (1985) Thiobarbituric acid reaction of aldehydes and oxidized lipids in glacial acetic acid. Lipids 20:915–921CrossRefGoogle Scholar
  26. Lee DH, Kim YS, Lee CB (2001) The inductive responses of the antioxidant enzymes by salt stress in the rice (Oryza sativa L.). J Plant Physiol 158:737–745.  https://doi.org/10.1078/0176-1617-00174 CrossRefGoogle Scholar
  27. Li J, Gao Y, Wu S, Cheung K, Wang X, Wong M (2008) Physiological and biochemical responses of rice (Oryza SativaL.) to phenanthrene and pyrene. Int J Phytoremediation 10:106–118.  https://doi.org/10.1080/15226510801913587 CrossRefGoogle Scholar
  28. Li W, Xu L, Wu J, Ma L, Liu M, Jiao J, Li H, Hu F (2015) Effects of indole-3-acetic acid (IAA), a plant hormone, on the ryegrass yield and the removal of fluoranthene from soil. Int J Phytoremediation 17:422–428.  https://doi.org/10.1080/15226514.2014.910172 CrossRefGoogle Scholar
  29. Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry–based metabolite profiling in plants. Nat Protoc 1(1):387–396.  https://doi.org/10.1038/nprot.2006.59 CrossRefGoogle Scholar
  30. Liu H, Weisman D, Ye Y, Cui B, Huang Y, Colón-Carmona A, Wang Z (2009) An oxidative stress response to polycyclic aromatic hydrocarbon exposure is rapid and complex in Arabidopsis thaliana. Plant Sci 176:375–382.  https://doi.org/10.1016/j.plantsci.2008.12.002 CrossRefGoogle Scholar
  31. Moran R (1982) Formulae for determination of chlorophyllous pigments extracted with N,N-Dimethylformamide. Plant Physiol 69:1376–1381.  https://doi.org/10.1104/pp.69.6.1376 CrossRefGoogle Scholar
  32. Nam JJ, Thomas GO, Jaward FM, Steinnes E, Gustafsson O, Jones KC (2008) PAHs in background soils from Western Europe: influence of atmospheric deposition and soil organic matter. Chemosphere 70:1596–1602.  https://doi.org/10.1016/j.chemosphere.2007.08.010 CrossRefGoogle Scholar
  33. Nam YS, Her JY, Hwang J, Lee KG (2015) Pesticide residues in yuza (Citrus junos) cultivated using ordinary and environmentally friendly cultures. J Pestic Sci 40:60–64.  https://doi.org/10.1584/jpestics.D14-074 CrossRefGoogle Scholar
  34. Nelson DL, Cox MM, Lehninger AL (2000) Lehninger principles of biochemistry. Worth Publishers, New YorkGoogle Scholar
  35. Ong S, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, Pandey A, Mann M (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 1:376–386CrossRefGoogle Scholar
  36. Orecchio S (2010) Contamination from polycyclic aromatic hydrocarbons (PAHs) in the soil of a botanic garden localized next to a former manufacturing gas plant 442 in Palermo (Italy). J Hazard Mater 180:443590–443601.  https://doi.org/10.1016/j.jhazmat.2010.04.074 CrossRefGoogle Scholar
  37. Peng YL, Wang Y, Fei J, Sun C, Cheng H (2015) Ecophysiological differences between three mangrove seedlings (Kandelia obovata, Aegiceras corniculatum, and Avicennia marina) exposed to chilling stress. Ecotoxicology 24:1722–1732.  https://doi.org/10.1007/s10646-015-1488-7 CrossRefGoogle Scholar
  38. Pilon C, Soratto R, Broetto F, Fernandes AM (2014) Foliar or soil applications of silicon alleviate water-deficit stress of potato plants. Agron J 106(6):2325–2334.  https://doi.org/10.2134/agronj14.0176 CrossRefGoogle Scholar
  39. Pompelli MF, Barata-Luís R, Vitorino HS, Gonçalves ER, Rolim EV, Santos MG, Almeida-Cortez JS, Ferreira VM, Lemos EE, Endres L (2010) Photosynthesis, photoprotection and antioxidant activity of purging nut under drought deficit and recovery. Biomass Bioenergy 34:1207–1215.  https://doi.org/10.1016/j.biombioe.2010.03.011 CrossRefGoogle Scholar
  40. Sakami W, Harrington H (1963) Amino acid metabolism. Annu Rev Biochem 32:355–398CrossRefGoogle Scholar
  41. Shan G, Ye M, Zhu L (2014) Protective effects of epigallocatechin gallate (EGCG) against the cytotoxicity of tetrachloro-1,4-benquinone (TCBQ). Asian J Ecotoxicology 3:585–592Google Scholar
  42. Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726.  https://doi.org/10.1093/jxb/erj073 CrossRefGoogle Scholar
  43. Shen Y (2014) Studies on the physiological response of Cyclosorus acuminatus to Cu and Zn Pollution. Nanjing Forestry University, Nanjing, ChinaGoogle Scholar
  44. Shen Y, Li J, Gu R, Yue L, Zhan X, Xing B (2017) Phenanthrene-triggered chlorosis is caused by elevated chlorophyll degradation and leaf moisture. Environ Pollut 220:1311–1321.  https://doi.org/10.1016/j.envpol.2016.11.003 CrossRefGoogle Scholar
  45. Shen Y, Li J, Gu R, Yue L, Wang H, Zhan X, Xing B (2018) Carotenoid and superoxide dismutase are the most effective antioxidants participating in ROS scavenging in phenanthrene accumulated wheat leaf. Chemosphere 197:513–525.  https://doi.org/10.1016/j.chemosphere.2018.01.036 CrossRefGoogle Scholar
  46. Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759.  https://doi.org/10.1007/s00726-008-0061-6 CrossRefGoogle Scholar
  47. Wang J, Geng N, Xu Y, Zhang W, Tang X, Zhang R (2014) PAHs in PM2.5 in Zhengzhou: concentration, carcinogenic risk analysis, and source apportionment. Environ Monit Assess 186:7461–7473.  https://doi.org/10.1007/s10661-014-3940-1 CrossRefGoogle Scholar
  48. Wang C, Wang X, Wang P, Chen B, Hou J, Qian J, Yang Y (2016a) Effects of iron on growth, antioxidant enzyme activity, bound extracellular polymeric substances and microcystin production of Microcystis aeruginosa FACHB-905. Ecotoxicol Environ Saf 132:231–239.  https://doi.org/10.1016/j.ecoenv.2016.06.010 CrossRefGoogle Scholar
  49. Wang S, Li Q, Fang C, Zhou C (2016b) The relationship between economic growth, energy consumption, and CO2 emissions: empirical evidence from China. Sci Total Environ 542:360–371.  https://doi.org/10.1016/j.scitotenv.2015.10.027 CrossRefGoogle Scholar
  50. Wania F, Mackay D (1996) Tracking the distribution of persistent organic pollutants. Environ Sci Technol 30:390A–396ACrossRefGoogle Scholar
  51. Wu G, Fang Y, Yang S, Lupton JR, Turner ND (2004) Glutathione metabolism and its implications for health. J Nutr 134:489–492.  https://doi.org/10.1093/jn/134.3.489 CrossRefGoogle Scholar
  52. Yang W, Lang Y, Li G (2014) Cancer risk of polycyclic aromatic hydrocarbons (PAHs) in the soils from Jiaozhou Bay wetland. Chemosphere 112:289–295.  https://doi.org/10.1016/j.chemosphere.2014.04.074 CrossRefGoogle Scholar
  53. Yeh SM, Sherman DG, Meares CF (1979) A new route to “bifunctional” chelating agents: conversion of amino acids to analogs of ethylenedinitrilotetraacetic 486 acid. Anal Biochem 100:152–487,159.  https://doi.org/10.1016/0003-2697(79)90125-8 CrossRefGoogle Scholar
  54. Zhan X, Zhu M, Shen Y, Yue L, Li J, Gardea-Torresdey TL, Xu G (2018) Apoplastic and symplastic uptake of phenanthrene in wheat roots. Environ Pollut 233:331–339.  https://doi.org/10.1016/j.envpol.2017.10.056 CrossRefGoogle Scholar
  55. Zhang Y, Rock CO (2004) Evaluation of epigallocatechin gallate and related plant polyphenols as inhibitors of the FabG and FabI reductases of bacterial type II fatty-acid synthase. J Biol Chem 279:30994–31001CrossRefGoogle Scholar
  56. Zhang W, Yan W, Wang Z (1978) Chemically induced plant senescence and its application in accelerating maturation of cereals. J Integr Plant Biol 3:21–28Google Scholar
  57. Zhang Z, Rengel Z, Meney K, Pantelic L, Tomanovic R (2011) Polynuclear aromatic hydrocarbons (PAHs) mediate cadmium toxicity to an emergent wetland species. J Hazard Mater 189:119–126.  https://doi.org/10.1016/j.jhazmat.2011.02.007 CrossRefGoogle Scholar
  58. Zhang J, Decmh C, Torres-Jerez I, Kang Y, Allen SN, Huhman DV, Tang Y, Murray J, Sumner LW, Udvardi MK (2014) Global reprogramming of transcription and metabolism in Medicago truncatula during progressive drought and after rewatering. Plant Cell Environ 37:2553–2576.  https://doi.org/10.1111/pce.12328 CrossRefGoogle Scholar
  59. Zhao O, Zhang X, Feng S, Zhang L, Shi W, Yang Z, Chen M, Fang X (2017) Starch-enhanced degradation of HMW PAHs by Fusarium sp. in an aged polluted soil from a coal mining area. Chemosphere 174:774–780.  https://doi.org/10.1016/j.chemosphere.2016.12.026 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Yu Shen
    • 1
    • 2
  • Jinfeng Li
    • 1
  • Shengnan Shi
    • 1
  • Ruochen Gu
    • 1
  • Xinhua Zhan
    • 1
  • Baoshan Xing
    • 2
  1. 1.College of Resources and Environmental SciencesNanjing Agricultural UniversityJiangsu ProvinceChina
  2. 2.Stockbridge School of AgricultureUniversity of MassachusettsAmherstUSA

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