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Environmental Science and Pollution Research

, Volume 25, Issue 5, pp 4739–4749 | Cite as

Indicators of environmental contamination by heavy metals in leaves of Taraxacum officinale in two zones of the metropolitan area of Mexico City

  • Sandra Gómez-ArroyoEmail author
  • Arisbel Barba-García
  • Francisco Arenas-Huertero
  • Josefina Cortés-Eslava
  • Michel Grutter de la Mora
  • Rocío García-Martínez
Research Article

Abstract

The present study was designed to detect the effect of heavy metals in two zones of the Metropolitan Area of Mexico City (MAMC), the Centro de Ciencias de la Atmósfera (CCA), and the Altzomoni station in the Iztaccíhuatl-Popocatépetl National Park. Taraxacum officinale was selected as the indicator organism of responses to atmospheric contamination by heavy metals. Determinations of heavy metals were performed, and total mRNA was extracted to quantify the expression of microRNA398 (miR398), superoxide dismutase 2 (CSD2), and the amounts of free radicals using the bromide of 3-(4,5-dimethylthiazole-2-ilo)-2,5-diphenyltetrazole (MTT) salts reduction assay. Results from the Altzomoni station showed high concentrations of five heavy metals, especially Aluminum, while three heavy metals were identified in the CCA-UNAM zone, most importantly, Vanadium, both in the dry season; miR398 expression presented subtle changes but was greater in the leaves from the stations with higher concentrations of heavy metals. Observations included a significant expression of CSD2, mainly in the dry season in both study zones, where levels were significant with respect to controls (p < 0.05). Reduced MTT was also higher in the dry season than in the rainy season (p < 0.05). In conclusion, the increase in heavy metals on the leaves of Taraxacum officinale induces increased expression of the CSD2 gene and reduced MTT; thus, they can be used as indicators for biomonitoring heavy metal concentrations.

Keywords

MicroRNAs Atmospheric pollution Dry and rainy seasons Taraxacum officinale Heavy metals 

Notes

Acknowledgments

The authors would like to thank the Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT-DGAPA), Universidad Nacional Autónoma de México for financial support through the project IN225114, to Ana Rosa Flores Márquez for her technical assistance, to Claudio Amescua for his editing assistance, and to Dirección de Investigación of Hospital Infantil de México Federico Gómez.

References

  1. Alptekin B, Langridge P, Budak H (2017) Abiotic stress miRNomes in the Triticeae. Funct Integr Genomics 17(2):145–170.  https://doi.org/10.1007/s10142-016-0525-9 CrossRefGoogle Scholar
  2. An J, Jeong S, Moon H, Jho E, Nam K (2012) Prediction of Cd and Pb toxicity to Vibrio fischeri using biotic ligand-based models in soil. J Hazard Mater 203-204:69–76.  https://doi.org/10.1016/j.jhazmat.2011.11.085 CrossRefGoogle Scholar
  3. Bartel D (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297.  https://doi.org/10.1016/S0092-8674(04)00045-5 CrossRefGoogle Scholar
  4. Bretzel F, Benvenuti S, Pistelli L (2014) Metal contamination in urban street sediment in Pisa (Italy) can affect the production of antioxidant metabolites in Taraxacum officinale Weber. Environ Sci Pollut Res 21(3):2325–2333.  https://doi.org/10.1007/s11356-013-2147-2 CrossRefGoogle Scholar
  5. Calderón de Rzedowski G, Rzedowski J (2005) Flora fanerogámica del Valle de México. Instituto de Ecología, A.C. and Comisión Nacional para el Conocimiento y uso de la Biodiversidad, Pátzcuaro, Michoacán, 1406pGoogle Scholar
  6. Choudhury S, Panda P, Sahoo L, Panda SK (2013) Reactive oxygen species signaling in plants under abiotic stress. Reactive oxygen species signaling in plants under abiotic stress. Plant Signal Behav 8(4):e23681.  https://doi.org/10.4161/psb.23681 CrossRefGoogle Scholar
  7. CONAPO (2012) Proyecciones de la población 2010–2050. Disponible en: http://www.conapo.gob.mx/es/CONAPO/Proyecciones_Datos. Accessed Jun 14 2016
  8. Cortés N, Mora C, Muñoz K, Díaz J, Serna R, Castro D, Osorio E (2014) Microscopical descriptions and chemical analysis by HPTLC of Taraxacum officinale in comparison to Hypochaeris radicata: a solution for mis-identification. Rev Bras Farmacogn 24(4):381–388.  https://doi.org/10.1016/j.bjp.2014.07.018
  9. Djingova R, Kovacheva P, Wagner G, Markert B (2003) Distribution of platinum group elements and other traffic related elements among different plants a ling some highways in Germany. Sci Total Environ 308:235–246.  https://doi.org/10.1016/S0048-9697(02)00677-0 CrossRefGoogle Scholar
  10. Doran J, Abbott S, Archuleta J, Bian X, Chow J, Coulter R, Wekker S, Edgerton S, Elliott S, Fernández A, Fast D, Hubbe J, King C, Langley D, Leach J, Lee J, Martin T, Martinez D, Martinez J, Mercado G, Mora V, Mulhearn M, Pena J, Petty R, Porch W, Russell C, Salas R, Shannon J, Shaw W, Sosa G, Tellier L, Templeman B, Watson J, White R, Whiteman C, Wolfe D (1998) The IMADA-AVER boundary layer experiment in the Mexico City area. Am Meteorol Soc 79(11):2497–2508.  https://doi.org/10.1175/1520-0477(1998)079<2497:TIABLE>2.0.CO;2 CrossRefGoogle Scholar
  11. Floris M, Mahgoub H, Lanet E, Robaglia C, Menand B (2009) Post-transcriptional regulation of gene expression in plants during abiotic stress. Int J Mol Sci 10(7):3168–3185.  https://doi.org/10.3390/ijms10073168 CrossRefGoogle Scholar
  12. Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64(1):97–112.  https://doi.org/10.1146/annurev.bi.64.070195.000525 CrossRefGoogle Scholar
  13. Gjorgieva D, Kadifkova-Panovska T, Baceva K, Stafilov T (2011) Assessment of heavy metal pollution in republic of Macedonia using a plant assay. Arch Environ Contam Toxicol 60(2):233–240.  https://doi.org/10.1007/s00244-010-9543-0 CrossRefGoogle Scholar
  14. Grant WF (1988) Higher plant assays for the detection of genotoxicity in air polluted environments. Ecosyst Health 4(4):210–229.  https://doi.org/10.1046/j.1526-0992.1998.98097.x CrossRefGoogle Scholar
  15. Grant WF (1994) The present status of higher bioassays for the detection of environmental mutagens. Mutat Res Fundam Mol Mech Mutagen 310(2):175–185.  https://doi.org/10.1016/0027-5107(94)90112-0 CrossRefGoogle Scholar
  16. He H, He L, Gu M (2014) Role of microRNAs in aluminum stress in plants. Plant Cell Rep 33(6):831–836.  https://doi.org/10.1007/s00299-014-1565-z CrossRefGoogle Scholar
  17. Holm L, Doll J, Holm E, Pancho J, Herberger J (1997) World weeds: natural histories and distribution. John Wiley and Sons, New York 1129 pGoogle Scholar
  18. Jagadeeswaran G, Saini A, Sunkar R (2009) Biotic and abiotic stress down regulate miR398 expression in Arabidopsis. Planta 229(4):1009–1014.  https://doi.org/10.1007/s00425-009-0889-3 CrossRefGoogle Scholar
  19. Jones-Rhoades M, Bartel D (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14(6):787–799.  https://doi.org/10.1016/j.molcel.2004.05.027 CrossRefGoogle Scholar
  20. Kabata-Pendias A, Dudka S (1991) Trace metal contents of Taraxacum officinale (dandelion) as a convenient environmental indicator. Environ Geochem Health 13(2):108–113.  https://doi.org/10.1007/BF01734301 CrossRefGoogle Scholar
  21. Keane B, Collier MH, Shann JR, Rogstad SH (2001) Metal content of dandelion (Taraxacum officinale) leaves in relation to soil contamination and airborne particulate matter. Sci Total Environ 281(1-3):63–78.  https://doi.org/10.1016/S0048-9697(01)00836-1 CrossRefGoogle Scholar
  22. Keane B, Matthew H, Collier MH, Steven H, Rogstad SH (2005) Pollution and genetic structure of North American populations of the common dandelion (Taraxacum officinale). Environ Monit Assess 105(1-3):341–357.  https://doi.org/10.1007/s10661-005-4333-2 CrossRefGoogle Scholar
  23. Kováčik J, Dudáš M, Hedbavny J, Mártonfi P (2016) Dandelion Taraxacum linearisquameum does not reflect soil metal content in urban localities. Environ Pollut 218:160–167  doi.org/10.1016/j.envpol.2016.08.030 CrossRefGoogle Scholar
  24. Kovalchuc I, Bokyo A (2008) Epigenetic control of stress response. Environ Mol Mutagen 49(1):61–72.  https://doi.org/10.1002/em.20347 CrossRefGoogle Scholar
  25. Lee SH, Ahsan N, Lee KW, Kim DH, Lee DG, Kwak SS, Kwon SY, Kim TH, Lee BH (2007) Simultaneous overexpression of both Cu Zn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. J Plant Physiol 164(12):1626–1638.  https://doi.org/10.1016/j.jplph.2007.01.003 CrossRefGoogle Scholar
  26. Liu Y, Muraleedharan N (2010) An efficient and economical MTT assay for determining the antioxidant activity of plant natural product extracts and pure compounds. J Nat Prod 73(7):1193–1195.  https://doi.org/10.1021/np1000945 CrossRefGoogle Scholar
  27. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 25(4):402–408.  https://doi.org/10.1006/meth.2001.1262 CrossRefGoogle Scholar
  28. Madany I, Ali S, Akhter M (1990) Assessment of lead in roadside vegetation in Bahrain. Environ Int 16(2):123–126.  https://doi.org/10.1016/0160-4120(90)90152-V CrossRefGoogle Scholar
  29. Malinowska E, Jankowski K, Wisniewska-Kadzajan B, Sosnowski J, Kolczarek R, Jankowska J, Ciepiela GA (2015) Content of zinc and cooper in selected plants growing along a motorway. Bull Environ Contam Toxicol 95(5):638–643.  https://doi.org/10.1007/s00128-015-1648-8 CrossRefGoogle Scholar
  30. Mendoza-Soto AB, Sánchez F, Hernández G (2012) MicroRNAs as regulators in plant metal toxicity response. Front Plant Sci 3:1–6.  https://doi.org/10.3389/fpls.2012.00105 CrossRefGoogle Scholar
  31. Moeder W, Del Pozo O, Navarre DA, Martin GB, Klessing DF (2007) Aconitase plays a role in regulating resistance to oxidative stress and cell death in Arabidopsis and Nicotiana benthamiana. Plant Mol Biol 63(2):273–287.  https://doi.org/10.1007/s11103-006-9087-x CrossRefGoogle Scholar
  32. Molina L, Molina M (2005) La calidad del aire en la megaciudad de México. Un enfoque integral. México: Fondo de Cultura Económica. 463 pGoogle Scholar
  33. Müller KJ, He X, Fischer R, Prüfer D (2006) Constitutive knox1 gene expression in dandelion (Taraxacum officinale, web.) changes leaf morphology from simple to compound. Planta 224(5):1023–1027.  https://doi.org/10.1007/s00425-006-0288-y CrossRefGoogle Scholar
  34. Naya L, Paul S, Valdés-López O, Mendoza-Soto AB, Nova-Franco B, Sosa-Valencia G, Reyes JL, Hernández G (2014) Regulation of copper homeostasis and biotic interactions by microRNA 398b in common bean. PLoS One 9(1):e84416.  https://doi.org/10.1371/journal.pone.0084416 CrossRefGoogle Scholar
  35. Normandin L, Kennedy G, Zayed J (1999) Potential of dandelion (Taraxacum officinale) as a bioindicator of manganese arising from the use of methylcyclopentadienyl manganese tricarbonyl in unleaded gasoline. Sci Total Environ 239(1):165–171.  https://doi.org/10.1016/S0048-9697(99)00292-2 CrossRefGoogle Scholar
  36. Pandey C, Raghuram B, Sinha AK, Gupta M (2015) miRNA plays a role in the antagonistic effect of selenium on arsenic in rice seedlings. Matallomics 7(5):857–866.  https://doi.org/10.1039/c5mt00013k CrossRefGoogle Scholar
  37. Pourrut B, Pohu A, Pruvot C, Garçon G, Verdin A, Waterlot C, Bidar G, Shirali P, Douay F (2011) Assessment of fly ash-aided phytostabilisation of highly contaminated soils after an 8 year field trial part 2. Influence on plants. Sci Total Environ 409(21):4504–4510.  https://doi.org/10.1016/j.scitotenv.2011.07.047 CrossRefGoogle Scholar
  38. Qiu Z, Hai B, Guo J, Li Y, Zhang L (2016) Characterization of wheat miRNAs and their target genes responsive to cadmium stress. Plant Physiol Biochem 101:60–67.  https://doi.org/10.1016/j.plaphy.2016.01.020 CrossRefGoogle Scholar
  39. Quintana R, Serrano J, Gómez V, de Foy B, Miranda J, García-Cuellar C, Vega E, Vázquez-López I, Molina LT, Manzano-León N, Rosas I, Osornio-Vargas AR (2011) The oxidative potential and biological effects induced by PM10 obtained in Mexico City and at a receptor site during the MILAGRO campaign. Environ Pollut 159(12):3446–3454.  https://doi.org/10.1016/j.envpol.2011.08.022 CrossRefGoogle Scholar
  40. Rao M, Dubey P (1992) Occurrence of heavy metals in air and their accumulation by tropical plants growing around an industrial area. Sci Total Environ 126(1–6):1–16.  https://doi.org/10.1016/0048-9697(92)90479-C CrossRefGoogle Scholar
  41. Romero-Puertas MC, Corpas FJ, Rodríguez-Serrano M, Gómez M, del Río LA, Sandalio LM (2007) Differential expression and regulation of antioxidative enzymes by cadmium in pea plants. J Plant Physiol 164(10):1346–1357.  https://doi.org/10.1016/j.jplph.2006.06.018 CrossRefGoogle Scholar
  42. Rosas-Pérez I, Serrano J, Alfaro-Moreno E, Baumgardner D, García-Cuellar C, Martín Del Campo JM, Raga GB, Castillejos M, Colín RD, y Osornio-Vargas AR (2007) Relations between PM10 composition and cell toxicity: a multivariate and graphical approach. Chemosphere 67(6):1218–1228.  https://doi.org/10.1016/j.chemosphere.2006.10.078 CrossRefGoogle Scholar
  43. Sarma H, Deka S, Deka H, Saikia R (2011) Accumulation of heavy metals in selected medicinal plants. Rev Environ Contam Toxicol 214:63–86.  https://doi.org/10.1007/978-1-4614-0668-6_4 Google Scholar
  44. Schreck E, Foucault Y, Sarret G, Sobanska S, Cécillon L, Castrec-Rouelle M, Uzu G, Dumat C (2012) Metal and metalloid foliar uptake by various plant species exposed to atmospheric industrial fallout: Mechanisms involved for lead. Sci Total Environ 427-428:253–262.  https://doi.org/10.1016/j.scitotenv.2012.03.051 CrossRefGoogle Scholar
  45. Schützendübel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R, Godbold DL, Polle A (2001) Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in scots pine roots. Plant Physiol 127(3):887–898.  https://doi.org/10.1104/pp.010318 CrossRefGoogle Scholar
  46. SEDEMA-GDF (Secretaría de Medio Ambiente del Gobierno del Distrito Federal) (2013) Inventario de Emisiones Contaminantes y de Efecto Invernadero de la Zona Metropolitana del Valle de México 2012. Available in: http://www.aire.df.gob.mx/default.php?opc=Z6BhnmI=&dc=Zg==. Accessed Jun 14 2016
  47. Shahid M, Pourrut B, Dumat C, Nadeem M, Aslam M, Pinelli E (2014) Heavy-metal-induced reactive oxygen species: phytotoxicity and physicochemical changes in plants. Rev Environ Contam Toxicol 232:1–44.  https://doi.org/10.1007/978-3-319-06746-9_1 Google Scholar
  48. Shengben L, Lin L, Xiaohong Z, Yu Y, Xigang L, Xia C, Lijuan J, Zhiqiang P, Xiaofeng C, Beixin M, Fuchun Z, Natasha R, Liwen J, Xuemei C (2013) MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 153(3):562–574.  https://doi.org/10.1016/j.cell.2013.04.005 CrossRefGoogle Scholar
  49. Singh RP, Agrawa M (2010) Variations in heavy metal accumulation, growth and yield of rice plants grown at different sewage sludge amendment rates. Ecotoxicol Environ Saf 73(4):632–641.  https://doi.org/10.1016/j.ecoenv.2010.01.020 CrossRefGoogle Scholar
  50. Sunkar R (2010) MicroRNAs with macro effects on plant stress responses. Semin Cell Dev Biol 21(8):805–811.  https://doi.org/10.1016/j.semcdb.2010.04.001 CrossRefGoogle Scholar
  51. Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16(8):2001–2019.  https://doi.org/10.1105/tpc.104.022830 CrossRefGoogle Scholar
  52. Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by down regulation of miR398 and important for oxidative stress tolerance. Plant Cell 18(8):2051–2065.  https://doi.org/10.1105/tpc.106.041673 CrossRefGoogle Scholar
  53. Tzintzun-Cervantes G, Rojas-Bracho L, Fernández-Bremauntz A (2005) Las partículas suspendidas en tres grandes ciudades mexicanas. Gaceta Ecol 74:29–44Google Scholar
  54. Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136(4):669–687.  https://doi.org/10.1016/j.cell.2009.01.046 CrossRefGoogle Scholar
  55. Ward NI (1990) Lead contamination of the London orbital (M25) motorway (since it's opening in 1986). Sci Total Environ 93:277–284.  https://doi.org/10.1016/0048-9697(90)90117-D CrossRefGoogle Scholar
  56. Whiteside J, Box C, McMillan T, Allinson S (2010) Cadmium and copper inhibit both DNA repair activities of polynucleotide kinase. DNA Repair 9(1):83–89.  https://doi.org/10.1016/j.dnarep.2009.11.004 CrossRefGoogle Scholar
  57. Zhou Z, Huang S, Yang Z (2008) Bioinformatic identification and expression analysis of new microRNAs from Medicago truncatula. Biochem Biophys Res Commun 374(3):538–542.  https://doi.org/10.1016/j.bbrc.2008.07.083 CrossRefGoogle Scholar
  58. Zhu C, Ding Y, Liu H (2011) MiR398 and plant stress responses. Physiol Plant 143(1):1–9.  https://doi.org/10.1111/j.1399-3054.2011.01477 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Laboratorio de Genotoxicología Ambiental, Centro de Ciencias de la AtmósferaUniversidad Nacional Autónoma de MéxicoCiudad de MéxicoMexico
  2. 2.Laboratorio de Investigación en Patología ExperimentalHospital Infantil de México Federico GómezCiudad de MéxicoMexico
  3. 3.Laboratorio de Espectroscopía y Percepción Remota, Centro de Ciencias de la AtmósferaUniversidad Nacional Autónoma de MéxicoCiudad de MéxicoMexico
  4. 4.Laboratorio de Aerosoles Atmosféricos, Centro de Ciencias de la AtmósferaUniversidad Nacional Autónoma de MéxicoCiudad de MéxicoMexico

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