Skip to main content
SpringerLink
Log in

Biochemical modifications in Pinus pinaster Ait. as a result of environmental pollution

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Exposure to chemical pollution can cause significant damage to plants by imposing conditions of oxidative stress. Plants combat oxidative stress by inducing antioxidant metabolites, enzymatic scavengers of activated oxygen and heat shock proteins. The accumulation of these proteins, in particular heat shock protein 70 and heme oxygenase, is correlated with the acquisition of thermal and chemical adaptations and protection against oxidative stress. In this study, we used Pinus pinaster Ait. collected in the areas of Priolo and Aci Castello representing sites with elevated pollution and reference conditions, respectively. The presence of heavy metals and the levels of markers of oxidative stress (lipid hydroperoxide levels, thiol groups, superoxide dismutase activity and expression of heat shock protein 70, heme oxygenase and superoxide dismutase) were evaluated, and we measured in field-collected needles the response to environmental pollution. P. pinaster Ait. collected from a site characterized by industrial pollution including heavy metals had elevated stress response as indicated by significantly elevated lipid hydroperoxide levels and decreased thiol groups. In particular, we observed that following a chronic chemical exposure, P. pinaster Ait. showed significantly increased expression of heat shock protein 70, heme oxygenase and superoxide dismutase. This increased expression may have protective effects against oxidative stress and represents an adaptative cellular defence mechanism. These results suggest that evaluation of heme oxygenase, heat shock protein 70 and superoxide dismutase expression in P. pinaster Ait. could represent a useful tool for monitoring environmental contamination of a region and to better understand mechanisms involved in plant defence and stress tolerance.

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

Similar content being viewed by others

References

  • Ali MB, Hahn EJ, Paek KY (2005) Effects of temperature on oxidative stress defense systems, lipid peroxidation and lipoxygenase activity in Phalaenopsis. Plant Physiol Biochem 43:213–223. doi:10.1016/j.plaphy.2005.01.007

    Article  CAS  Google Scholar 

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutase (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341. doi:10.1093/jexbot/53.372.1331

    Article  CAS  Google Scholar 

  • Arduini I, Godbold DL, Onnis A (1996) Influence of copper on root growth and morphology of Pinus pinea L. and Pinus pinaster Ait. seedlings. Tree Physiol 15:411–415

    Google Scholar 

  • Balestrasse KB, Noriega GO, Batlle A, Tomaro ML (2005) Involvement of heme oxigenase as antioxidant defense in soybean nodules. Free Rad Res 39:145–151. doi:10.1080/10715760400022319

    Article  CAS  Google Scholar 

  • Bowler C, Fluhr R (2000) The role of calcium and activated oxygens as signals for controlling cross-tolerance. Trends Plant Sci 5:241–246. doi:10.1016/S1360-1385(00)01628-9

    Article  CAS  Google Scholar 

  • 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. doi:10.1016/0003-2697(76)90527-3

    Article  CAS  Google Scholar 

  • Bytnerowicz A, Omasa K, Paoletti E (2006) Integrated effects of air pollution and climate change on forests: a northern hemisphere perspective. Environ Pollut 147:438–445. doi:10.1016/j.envpol.2006.08.028

    Article  Google Scholar 

  • Casano LM, Gómez LD, Lascano HR, González CA, Trippi VS (1997) Inactivation and degradation of CuZn-SOD by active oxygen species in wheat chloroplasts exposed to photooxidative stress. Plant Cell Physiol 38:433–440

    Article  CAS  Google Scholar 

  • Chauhan H, Khurana N, Agarwal P, Khurana P (2011) Heat shock factors in rice (Oryza sativa L.): genome-wide expression analysis during reproductive development and abiotic stress. Mol Genet Genomics 286:171–187. doi:10.1007/s00438-011-0638-8

    Article  CAS  Google Scholar 

  • Di Giacomo C, Acquaviva R, Lanteri R, Licata F, Licata A, Vanella A (2003) Non proteic antioxidant status in plasma of subjects with colon cancer. Exp Med Biol 228:525–528. doi:10.1016/j.envpol.2006.08.028

    Google Scholar 

  • Dias de Azevedo Neto N, Prisco JT, Enèas-Filho J, Medeiros JR, Gomes-Filho E (2005) Hydrogen peroxide pre-treatment induces salt-stress acclimation in maize plants. J Plant Physiol 162:1114–1122. doi:10.1016/j.jplph.2005.01.007

    Article  Google Scholar 

  • Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Ann Rev Physiol 61:243–282. doi:10.1146/annurev.physiol.61.1.243

    Article  CAS  Google Scholar 

  • Foyer CH, Lopez-Delgado H, Dat JE, Scott IM (1997) Hydrogen peroxide- and glutathione-associated mechanism of acclimatory stress tolerance and signalling. Plant Physiol 100:241–254. doi:10.1111/j.1399-3054.1997.tb04780.x

    Article  CAS  Google Scholar 

  • Gallego SM, Benavides MP, Tomaro ML (1996) Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. Plant Sci 121:151–159. doi:10.1016/S0168-9452(96)04528-1

    Article  CAS  Google Scholar 

  • Giertych MJ, De Temmerman LO, Rachwal L (1997) Distribution of elements along the length of Scots pine needles in a heavily polluted and a control environment. Tree Physiol 17:697–703

    Article  CAS  Google Scholar 

  • Gifford DJ, Taleisnk E (1994) Heat-shock response of Pinus and Picea seedlings. Tree Physiol 14:103–110

    Google Scholar 

  • Godbold DL, Huttermann A (1985) Effect of zinc, cadmium and mercury on root elongation of Picea abies (Karst.) seedlings, and the significance of these metals to forest die-back. Environ Pollut 38:375–381. doi:10.1016/0143-1471(85)90108-4

    Article  CAS  Google Scholar 

  • Goycoolea C, Cardemil L (1991) Expression of heat shock proteins in seeds and during seedling growth of Araucaria araucana as a response to thermal stress. Plant Physiol Biochem 29:213–222

    CAS  Google Scholar 

  • Gozzelino R, Jenev V, Soares MP (2010) Mechanisms of cells protection by heme oxygenase-1. Annu Rev Pharmacol Toxicol 50:323–354

    Article  CAS  Google Scholar 

  • Grulke NE, Paoletti E, Heath R (2007) Chronic vs. short-term acute O3 exposure effects on nocturnal transpiration in two Californian oaks. ScientificWorldJournal 7:134–140

    Article  CAS  Google Scholar 

  • Gurriero C, Bianchi F, Cairns J, Cori L (2011) Policies to clean up toxic industrial contaminated sites of Gela and Priolo: a cost-benefit analysis. Environ Health 10:68–78. doi:10.1186/1476-069X-10-68

    Article  Google Scholar 

  • Heikkila JJ (1993) Heat shock gene expression and development. I. An overview of fungal, plant and poikilothermic animal development systems. Dev Genetics 14:1–5

    Article  CAS  Google Scholar 

  • Helmisaari HS, Derome J, Nöjd P, Kukkola M (2007) Fine root biomass in relation to site and stand characteristics in Norway spruce and Scots pine stands. Tree Physiol 27:1493–1504

    Article  CAS  Google Scholar 

  • Hernandez LD, Vierling E (1993) Expression of low molecular weight heat-shock proteins under field conditions. Plant Physiol 101:1209–1216

    CAS  Google Scholar 

  • Kovtun Y, Chiu WL, Tena G, Shenn J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. PNAS 97:2940–2945. doi:10.1073/pnas.97.6.2940

    Article  CAS  Google Scholar 

  • Kupcinskienea E, Stiklieneb A, Judzentienec A (2008) The essential oil qualitative and quantitative composition in the needles of Pinus sylvestris L. growing along industrial transects. Environ Pollut 155:481–491. doi:10.1016/j.envpol.2008.02.001

    Article  Google Scholar 

  • Lai LS, Chang PC, Chang CT (2008) Isolation and characterization of superoxide dismutase from wheat seedlings. J Agric Food Chem 56:8121–8129. doi:10.1021/jf800859f

    Article  CAS  Google Scholar 

  • Lin CT, Lin MT, Chen YT, Shaw JF (1995) Subunit interaction enhances enzymatic activity and stability of sweet potato cytosolic Cu/Zn superoxide dismutase purified by a His-tagged recombinant protein method. Plant Mol Biol 28:305–311. doi:10.1007/BF00020249

    Article  Google Scholar 

  • Lozano-Rodriguez E, Hernandez LE, Bonay P, Carpena-Ruiz RO (1997) Distribution of cadmium in shoot and root tissues of maize and pea plants: physiological disturbances. J Exp Bot 306:123–128

    Article  Google Scholar 

  • Mandre M, Kask R, Pikk J, Ots K (2008) Assessment of growth and stemwood quality of Scots pine on territory influenced by alkaline industrial dust. Environ Monit Assess 138:51–63. doi:10.1007/s10661-007-9790-3

    Article  CAS  Google Scholar 

  • Manitatsevic S, Dunderski J, Matic G, Tuci B (2007) Seasonal variation in heat shock proteins Hsp70 and Hsp90 expression in an exposed and a shaded habitat of Iris pumila. Plant Cell Environ 30:1–11

    Article  Google Scholar 

  • Manninen S, Huttunen S (1995) Scots pine needles as bioindicators of sulphur deposition. Can J Forest Res 25:1559–1569. doi:10.1139/x95-170

    Article  CAS  Google Scholar 

  • Mansfield MA, Key JL (1987) Synthesis of the low molecular weight heat shock proteins in plants. Plant Physiol 84:1007–1017

    Article  CAS  Google Scholar 

  • Mazorra LM, Numez M, Hechavarria M, Coll F, Sanchez-Blanco MJ (2002) Influence of brassinosteroids on antioxidant enzymes activity in tomato under different temperatures. Plant Biol 45:593–596. doi:10.1023/A:1022390917656

    Article  CAS  Google Scholar 

  • Mehra RK, Tripathi RD (2000) Phytochelatins and metal tolerance. In: Agrawal SB, Agrawal M (eds) Environmental pollution and plant responses. CRC Press, Boca Raton

    Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. doi:10.1016/S1360-1385(02)02312-9

    Article  CAS  Google Scholar 

  • National Environment Agency APAT (2010) Rilevamento di metalli in aghi di pino nella città di Gela e nella zona di Siracusa-Augusta. National Health Institute

  • Neill SJ, Desikan R, Hancock JT (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5:388–395

    Article  CAS  Google Scholar 

  • Nerg A, Kainulainen P, Vuorinen M, Hanso M, Holopainen JK, Kurkela T (1994) Seasonal and geographical variation of terpenes, resin acid and total phenolics in nursery grown seedlings of Scots pine (Pinus sylvestris L.). New Phytol 128:703–713. doi:10.1111/j.1469-8137.1994.tb04034.x

    Article  CAS  Google Scholar 

  • Nieminen T, Helmisaari HS (1996) Nutrient retranslocation in the foliage of Pinus sylvestris L. growing along a heavy metal pollution gradient. Tree Physiol 16:825–831

    Article  CAS  Google Scholar 

  • Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biot 51:730–750. doi:10.1007/s002530051457

    Article  CAS  Google Scholar 

  • Noriega GO, Tomaro ML, Batlle A (2003) Bilirubin is highly effective in preventing in vivo δ-aminolevulinic acid-induced oxidative cell damage. Biochim Biophys Acta 1638:173–178

    Article  CAS  Google Scholar 

  • Noriega GO, Balestrasse KB, Batlle A, Tomaro ML (2004) Heme oxygenase exerts a protective role against oxidative stress in soybean leaves. Biochem Bioph Res Co 323:1003–1008. doi:10.1016/j.bbrc.2004.08.199

    Article  CAS  Google Scholar 

  • Noriega GO, Yannarelli GG, Balestrasse KB, Batlle A, Tomaro ML (2007) The effect of nitric oxide on heme oxigenase gene expression in soybean leaves. Planta 226:1155–1163. doi:10.1007/s00425-007-0561-8

    Article  CAS  Google Scholar 

  • Palta JP (1990) Stress interaction at the cellular and membranes levels. HortSci 25:1377–1381

    CAS  Google Scholar 

  • Rascio N, Dalla Vecchia F, La Rocca N, Barbato R, Pagliano C, Raviolo M, Gonnelli C, Gabbrielli R (2008) Metal accumulation and damage in rice (cv. Vialone nano) seedlings exposed to cadmium. Environ Exp Bot 62:267–278

    Article  CAS  Google Scholar 

  • Reiter SW, Tyrrell RM (2000) The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties. Free Radic Biol Med 28:289–309. doi:10.1016/S0891-5849(99)00223-3

    Article  Google Scholar 

  • Reyes MA, Corcurea LJ, Cardemil L (2003) Accumulation of HSP70 in Deschampsia antarctica Desv. leaves under thermal stress. Antarct Sci 15:345–352. doi:10.1017/S0954102003001366

    Article  Google Scholar 

  • Schöffl F, Prändl R, Reindl A (1998) Regulation of the heat-shock response. Plant Physiol 117:1135–1141. doi:10.1104/pp. 117.4.1135

    Article  Google Scholar 

  • Schutzendubel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365. doi:10.1093/jexbot/53.372.1351

    Article  CAS  Google Scholar 

  • 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 127:887–898

    Article  Google Scholar 

  • Slooten L, Capiau K, Van Camp W, Van Montagu M, Sybesma C, Inze D (1995) Factors affecting the enhancement of oxidative stress tolerance in transgenic tobacco overexpressing manganese superoxide dismutase in the chloroplasts. Plant Physiol 107:737–750

    CAS  Google Scholar 

  • Sorger PK (1991) Heat shock factor and the heat shock response. Cell 65:363–366. doi:10.1016/0092-8674(91)90452-5

    Article  CAS  Google Scholar 

  • Sung DY, Vierling E, Guy CL (2001) Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiol 126:789–800

    Article  CAS  Google Scholar 

  • Terry MJ, Linely PJ, Kochi T (2002) Making light of it: the role of plants haem oxygenases in phytochrome chromophore synthesis. Biochem Soc Trans 30:604–609. doi:10.1042/BST0300604

    Article  Google Scholar 

  • Van Breusegem F, Vranovà E, Dat JF, Inzè D (2001) The role of active oxygen species in plant signal transduction. Plant Sci 161:405–414. doi:10.1016/S0168-9452(01)00452-6

    Article  Google Scholar 

  • Vierling E (1991) The roles the heat-shock proteins in plants. Ann Rev Plant Phys 42:229–233. doi:10.1146/annurev.pp.42.060191.003051

    Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:246–252. doi:10.1016/j.tplants.2004.03.006

    Google Scholar 

  • Xiang C, Oliver DJ (1998) Glutathione metabolic genes co-ordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550

    CAS  Google Scholar 

  • Yamamoto Y, Hachia A, Matsumoto H (1997) Oxidative damage to membranes by a combination of aluminium and iron in suspension-cultured tobacco cells. Plant Cell Physiol 38:1333–1339

    Article  CAS  Google Scholar 

  • Zenk HM (1996) Heavy metal detoxification in higher plants—a review. Gene 179:21–30. doi:10.1016/S0378-1119(96)00422-2

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Mike Wilkinson for proofreading the manuscript. This work was financed through grants by MURST (Ministero dell’Università e della Ricerca Scientifica e Tecnologica), Italy.

Author information

Authors and Affiliations

  1. Department of Drug Science—Biochemistry Section, University of Catania, V.le A. Doria, 6, 95125, Catania, Italy

    Rosaria Acquaviva, Valeria Sorrenti, Rosa Santangelo, Alessandra Russo, Ignazio Barbagallo & Claudia Di Giacomo

  2. Department of Physiology and Pharmacology, Health Education Building, College of Medicine, University of Toledo, 3000 Arlington Ave., Toledo, OH, 43614-2598, USA

    Luca Vanella

  3. Department of Bio-Medical Sciences, University of Catania, Via Androne 81, 95124, Catania, Italy

    Liliana Iauk

  4. Department of Botany, University of Catania, Via A. Longo 19, 95125, Catania, Italy

    Francesca Savoca

Authors
  1. Rosaria Acquaviva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luca Vanella
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Valeria Sorrenti
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rosa Santangelo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Liliana Iauk
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alessandra Russo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Francesca Savoca
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ignazio Barbagallo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Claudia Di Giacomo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luca Vanella.

Additional information

Responsible editor: Markus Hecker

Rights and permissions

Reprints and permissions

About this article

Cite this article

Acquaviva, R., Vanella, L., Sorrenti, V. et al. Biochemical modifications in Pinus pinaster Ait. as a result of environmental pollution. Environ Sci Pollut Res 19, 3850–3858 (2012). https://doi.org/10.1007/s11356-012-1030-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-012-1030-x

Keywords

Search

Navigation