Skip to main content
SpringerLink
Log in

The biological response chain to pollution: a case study from the “Italian Triangle of Death” assessed with the liverwort Lunularia cruciata

  • (E)merging directions on air pollution and climate change research in Mediterranean Basin ecosystems
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The liverwort Lunularia cruciata, known for being a species tolerant to pollution able to colonize urban areas, was collected in the town of Acerra (South Italy) to investigate the biological effects of air pollution in one of the three vertices of the so-called Italian Triangle of Death. The ultrastructural damages observed by transmission electron microscopy in specimens collected in Acerra were compared with samples collected in the city center of Naples and in a small rural site far from sources of air pollution (Riccia, Molise, Southern Italy). The biological response chain to air pollution was investigated considering vitality, photosynthetic efficiency, heat shock protein 70 (Hsp70) induction and gene expression levels, and chlorophyll degradation and related ultrastructural alterations. Particularly, a significant increment in Hsp70 expression and occurrence, and modifications in the chloroplasts’ ultrastructure can be strictly related to the environmental pollution conditions in the three sites. The results could be interpreted in relation to the use of these parameters as biomarkers for environmental pollution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adamo P, Giordano S, Vingiani S, Castaldo Cobianchi R, Violante P (2003) Trace elements accumulation by moss and lichen bags in the city of Naples (Italy). Environ Pollut 122:91–103

    Article  CAS  Google Scholar 

  • Basile A, Cogoni AE, Bassi P, Fabrizi E, Sorbo S, Giordano S, Castaldo Cobianchi R (2001) Accumulation of Pb and Zn in gametophytes and sporophytes of the moss Funaria hygrometrica (Funariales). Ann Bot London 87:537–543

    Article  CAS  Google Scholar 

  • Basile A, di Nuzzo RA, Capasso C, Sorbo S, Capasso A, Carginale V (2005) Effect of cadmium on gene expression in the liverwort Lunularia cruciata. Gene 356:153–159

    Article  CAS  Google Scholar 

  • Basile A, Sorbo S, Aprile G, Conte B, Castaldo Cobianchi R (2008) Comparison of the heavy metal bioaccumulation capacity of an epiphytic moss and an epiphytic lichen. Environ Pollut 151:401–407

    Article  CAS  Google Scholar 

  • Basile A, Sorbo S, Aprile G, Conte B, Castaldo Cobianchi R, Pisani T, Loppi S (2009) Heavy metal deposition in the Italian “Triangle of death” determined with the moss Scorpiurium circinatum. Environ Pollut 157:2255–2260

    Article  CAS  Google Scholar 

  • Basile A, Sorbo S, Conte B, Golia B, Montanari S, Castaldo Cobianchi R, Esposito S (2011) Antioxidant activity in extracts from Leptodyctium riparium (Bryophyta), stressed by heavy metals, heat shock, salinity. Plant Biosyst 175:77–80. doi:10.1080/11263504-2010-509935

    Article  Google Scholar 

  • Basile A, Sorbo S, Pisani T, Paoli L, Munzi S, Loppi S (2012) Bioaccumulation and ultrastructural effects of Cd, Cu, Pb and Zn in the moss Scorpiurum circinatum (Brid.) Fleisch. & Loeske. Environ Pollut 166:208–211

    Article  CAS  Google Scholar 

  • Basile A, Sorbo S, Conte B, Cardi M, Esposito S (2013) Ultrastructural changes and heat shock proteins 70 induced by atmospheric pollution are similar to the effects observed under in vitro heavy metals stress in Conocephalum conicum (Marchantiales—Bryophyta). Environ Pollut 182:209–216. doi:10.1016/j.envpol.2013.07.014

    Article  CAS  Google Scholar 

  • Basile A, Sorbo S, Cardi M, Lentini M, Castiglia D, Cianciullo P, Conte B, Loppi S, Esposito S (2015) Effects of heavy metals on ultrastructure and Hsp70 induction in Lemna minor L. exposed to water along the Sarno River, Italy. Ecotox Environ Safe 114:93–101

    Article  CAS  Google Scholar 

  • Basile A, Sorbo S, Lentini M, Conte B, Esposito S (2016) Water pollution causes ultrastructural and functional damages in Pellia neesiana (Gottsche) Limpr. J Trace Elem Med Biol. doi:10.1016/j.jtemb.2016.11.014

  • Bassham DC, Laporte M, Marty F, Moriyasu Y, Ohsumi Y, Olsen LJ, Yoshimoto K (2006) Autophagy in development and stress responses of plants. Autophagy 2:2–11. doi:10.4161/auto.2092

    Article  CAS  Google Scholar 

  • Cardi M, Castiglia D, Ferrara M, Guerriero G, Chiurazzi M, Esposito S (2015) The effects of salt stress cause a diversion of basal metabolism in barley roots: possible different roles for glucose-6-phosphate dehydrogenase isoforms. Plant Physiol Bioch 86:44–54. doi:10.1016/j.plaphy.2014.11.001

    Article  CAS  Google Scholar 

  • Carginale V, Sorbo S, Capasso C, Trinchella F, Cafiero G, Basile A (2004) Accumulation, localisation, and toxic effects of cadmium in the liverwort Lunularia cruciata. Protoplasma 223:53–61

    Article  CAS  Google Scholar 

  • Chiaiese P, Minutolo M, Arciello A, Guglielmini F, Piccoli R, Filippone E (2011) Expression of human apolipoprotein A-I in Nicotiana tabacum. Biotechnol Lett 33:159. doi:10.1007/s10529-010-0388-4

    Article  CAS  Google Scholar 

  • Esposito S, Castaldo Cobianchi R, Sorbo S, Conte B, Basile A (2007) Ultrastructural alterations and HSP70 induction in Elodea canadensis Michx. exposed to heavy metals. Caryologia 60:115–120. doi:10.1080/00087114.2007.10589557

    Article  Google Scholar 

  • Esposito S, Sorbo S, Conte B, Basile A (2012) Effects of heavy metals on ultrastructure and HSP70s induction in the aquatic moss Leptodictyum riparium Hedw. Int J Phytorem 14:443–455. doi:10.1080/15226514.2011.620904

    Article  CAS  Google Scholar 

  • Harmens H, Norris D, the participants of the Moss Survey (2008) Spatial and temporal trends in heavy metal accumulation in mosses in Europe (1990–2005). Centre for ecology and hydrology, environment centre wales, Bangor, UK. http://nora.nerc.ac.uk/id/eprint/3928

  • Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381:571–580. doi:10.1038/381571a0

    Article  CAS  Google Scholar 

  • Galano E, Arciello A, Piccoli R, Monti DM, Amoresano A (2014) A proteomic approach to investigate the effects of cadmium and lead on human primary renal cells. Metallomics 6:587. doi:10.1039/c3mt00344b

    Article  CAS  Google Scholar 

  • Giordano S, Castaldo-Cobianchi R, Basile A, Spagnuolo V (1989) The structure and the role of hyaline parenchyma in the liverwort Lunularia cruciata (L.) Dum. G Bot Ital 123:169–176

    Article  Google Scholar 

  • Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494

    Article  CAS  Google Scholar 

  • Kukkola E, Rautio P, Huttunen S (2000) Stress indications in copper- and nickel exposed Scots pine seedlings. Environ Exp Bot 43:197–210. doi:10.1016/s0098-8472(99)00057-x

    Article  CAS  Google Scholar 

  • Lage-Pinto F, Oliveira JG, Da Cunha M, Souza CMM, Rezende CE, Azevedo RA, Vitória AP (2008) Chlorophyll a fluorescence and ultrastructural changes in chloroplast of water hyacinth as indicators of environmental stress. Environ Exp Bot 64:307–313

    Article  CAS  Google Scholar 

  • Landi S, Nurcato R, De Lillo A, Lentini M, Grillo S, Esposito S (2016) Glucose-6 phosphate dehydrogenase plays a central role in the response of tomato (Solanum lycopersicum) plants to short and long-term drought. Plant Physiol Bioch 105:79–89. doi:10.1016/j.plaphy.2016.04.013

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)). Methods 25:402–408

    Article  CAS  Google Scholar 

  • Liu D, Kottke I (2004) Subcellular localization of copper in the root cells of Allium sativum by electron energy spectroscopy (EELS). Bioresour Technol 94:153–158

    Article  CAS  Google Scholar 

  • Miernyk JA (1997) The 70 kDa stress-related proteins as molecular chaperones. Tr Plant Sci 2:180–187. doi:10.1016/j.tplants.2004.03.006

    Article  CAS  Google Scholar 

  • Nassiri Y, Ginsburger-Vogel T, Mansot JL, Wéry J (1996) Effects of heavy metals on Tetraselmis suecica: ultrastructural and energy-dispersive x-ray spectroscopy studies. Biol Cell 86:151–160

    Article  CAS  Google Scholar 

  • Paoli L, Fiorini E, Munzi S, Sorbo S, Basile A, Loppi S (2014) Uptake and acute toxicity of cerium in the lichen Xanthoria parietina. Ecotoxicol Environ Saf 104:379–385. doi:10.1016/j.ecoenv.2014.02.028

    Article  CAS  Google Scholar 

  • Qu C, Albanese S, Chen W, Lima A, Doherty A, Piccolo A, Arienzo M, Qi S, De Vivo B (2016) The status of organochlorine pesticide contamination in the soils of the Campania plain, Southern Italy, and correlations with soil properties and cancer risk. Environ Pollut 216:500–511

    Article  CAS  Google Scholar 

  • Ronen R, Galun M (1984) Pigment extraction from lichens with dimethylsulfoxide (DMSO) and estimation of chlorophyll degradation. Environ Exp Bot 24:239–245

    Article  CAS  Google Scholar 

  • Romieu I, Castro-Giner F, Kunzli N, Sunyer J (2008) Air pollution, oxidative stress and dietary supplementation: a review. Eur Respir J 31:179–197. doi:10.1183/09031936.00128106

    Article  CAS  Google Scholar 

  • Schwartzman RA, Cidlowski JA (1993) Apoptosis: the biochemistry and molecular biology programmed cell death. Endocr Rev 14:133–151

    CAS  Google Scholar 

  • Senior K, Mazza A (2004) Italian “Triangle of death” linked to waste crisis. Lancet Oncol 5:525–527

    Article  Google Scholar 

  • Shailasree S, Venkataramana M, Niranjana SR, Prakash HS (2015) Cytotoxic effect of p-coumaric acid on neuroblastoma, N2a cell via generation of reactive oxygen species leading to dysfunction of mitochondria inducing apoptosis and autophagy. Mol Neurobiol 51:119–130

    Article  CAS  Google Scholar 

  • Sorbo S, Aprile G, Strumia S, Castaldo Cobianchi R, Leone A, Basile A (2008) Trace element accumulation in Pseudevernia furfuracea (L.) Zopf exposed in Italy’s so called Triangle of Death. Sci Tot Environ 407:647–654

    Article  CAS  Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterise and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanisms, regulation and adaptation. Taylor & Francis, London, pp 445–483

    Google Scholar 

  • Taylor NL, Day DA, Millar AH (2002) Environmental stress causes oxidative damage to plant mitochondria leading to inhibition of glycine decarboxylase. J Biol Chem 277:42663–42668

    Article  CAS  Google Scholar 

  • Thompson AR, Vierstra RD (2005) Autophagic recycling: lessons from yeast help define the process in plants. Curr Op Plant Biol 8:165–173. doi:10.1016/j.pbi.2005.01.013

    Article  CAS  Google Scholar 

  • Todeschini V, Lingua G, D'Agostino G, Carniato F, Roccotiello E, Berta G (2011) Effects of high zinc concentration on poplar leaves: a morphological and biochemical study. Environ Exp Bot 71:50–56

    Article  CAS  Google Scholar 

  • Tyler G (1990) Bryophytes and heavy metals: a literature review. Bot J Linn Soc 104:231–253

    Article  Google Scholar 

  • Zhang X, Gao B, Xia H (2014) Effect of cadmium on growth, photosynthesis, mineral nutrition and metal accumulation of bana grass and vetiver grass. Ecotoxicol Environ Saf 106:102–108. doi:10.1016/j.ecoenv.2014.04.025

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors want to thank Dr. Vivana Maresca (Naples) for the statistical analysis of HM accumulation and vitality data. This work was supported by a grant from MIUR, PROGETTO TIDe, Obiettivo realizzativo: 1.9; Bioaccumulo. The authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Dipartimento di Biologia, Università di Napoli “Federico II”—Complesso Universitario di Monte Sant’Angelo, Via Cinthia 4, I-80126, Naples, Italy

    Adriana Basile, Marina Piscopo, Marco Lentini & Sergio Esposito

  2. Dipartimento di Scienze della Vita, Università di Siena, Via Pier Andrea Mattioli, 453100, Siena, Italy

    Stefano Loppi, Luca Paoli, Andrea Vannini & Fabrizio Monaci

  3. Ce.S.M.A, University of Naples “Federico II”—Complesso Universitario Monte Sant’Angelo, Via Cinthia 4, I-80126, Naples, Italy

    Sergio Sorbo

Authors
  1. Adriana Basile
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stefano Loppi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marina Piscopo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luca Paoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrea Vannini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fabrizio Monaci
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sergio Sorbo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Marco Lentini
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Sergio Esposito
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sergio Esposito.

Additional information

Responsible editor: Philippe Garrigues

Highlights

• Severe alterations were observed in chloroplasts of Lunularia cruciata exposed to pollution.

• A strong increase in the expression and occurrence of heat shock protein 70 was detected.

• The results suggest L. cruciata could be possibly used as a bioindicator organism.

• Hsp70 could be useful biomarkers to measure the effects and the extent of anthropic pollution.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Basile, A., Loppi, S., Piscopo, M. et al. The biological response chain to pollution: a case study from the “Italian Triangle of Death” assessed with the liverwort Lunularia cruciata . Environ Sci Pollut Res 24, 26185–26193 (2017). https://doi.org/10.1007/s11356-017-9304-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-9304-y

Keywords

Search

Navigation