Skip to main content
SpringerLink
Log in

Antioxidative and antifungal response of woody species to environmental conditions in the urban area

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

The complexity of ecological conditions in urban areas imposes the plant species need for the development of various biochemical and physiological adaptive strategies. The aim of our research was to examine the antioxidative and antifungal metabolism of species Pinus nigra, Picea omorika, Tilia cordata and Betula pendula from the area of Banja Luka City (urban area) during two vegetation seasons (spring and autumn) and compared with the same species from forest habitats. Changes in the protein concentration, activity and isoenzyme profiles of peroxidases (POD, EC 1.11.1.7), content and antioxidative activity of total phenols and antifungal activity in leaves and needles of the plants from the urban area and forest habitats were monitored. The obtained results indicate that urban areas induce changes in antioxidative metabolism in all examined species, but that the response is species specific. The most sensitive parameter that indicates different adaptation strategy of Pinus nigra, Picea omorika, Tilia cordata and Betula pendula to environment conditions in the urban area were peroxidase isoenzyme patterns. Less specific parameter was phenol content even though there are some indications for role of their antioxidative capacity in the adjustment to specific habitat. In addition, each species had different metabolic strategy to cope with the changes caused by the urban environment.

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
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Aboul-Enein HY, Kruk I, Kladna A, Lichsztof K, Michalska T (2007) Scavenging effects of phenolic compounds on reactive oxygen species. Biopolymers 86:222–230

    Article  CAS  Google Scholar 

  • Aguiar-Silva C, Brandao SE, Domingos M, Bulbovas P (2016) Antioxidant responses of Atlantic Forest native tree species as indicators of increasing tolerance to oxidative stress when they are exposed to air pollutants and seasonal tropical climate. Ecol Indic 63:154–164

    Article  CAS  Google Scholar 

  • Akbari H, Pomerantz M, Taha H (2001) Cool surfaces and shade trees to reduce energy use and improve air quality in urban areas. Sol Energy 70:295–310

    Article  Google Scholar 

  • Alfredsen G, Solheim H, Slimestad R (2008) Antifungal effect of bark extract from some European tree species. Eur J For Res 127:387–393

    Article  Google Scholar 

  • Anttila AK, Pirttila AM, Haggman H, Julkunen-Tiitto R (2013) Condensed conifers tannins as antifungal agents in liquid culture. Holzforschung 67:825–832

    Article  CAS  Google Scholar 

  • Begum A, Harikrishna S (2010) Evaluation of some tree species to absorb air pollutants in three industrial locations of South Bengaluru, India. E-J Chem 7:51–56

    Article  Google Scholar 

  • Bogdanovic' J, Miloševic' N, Prodanovic' R, Duc(ic' T, Radotic' K (2007) Variability of antioxidant enzyme activity and isoenzyme profile in needles of Serbian spruce (Picea omorika (Panc(.) Purkinye). Biochem Syst Ecol 35:263–273

    Article  CAS  Google Scholar 

  • Calfapietra C, Penuelas J, Niinemets U (2015) Urban plant physiology: adaptation- mitigation strategies under permanent stress. Trends Plant Sci 20:72–75

    Article  CAS  Google Scholar 

  • Carreras HA, Canas MS, Pignata ML (1996) Differences in responses to urban air pollutants by Ligustrum lucidum Ait. and Ligustrum lucidum Ait. f. tricolor (Rehd.) Rehd. Environ Pollut 93:211–218

    Article  CAS  Google Scholar 

  • Chandawat DK, Verma PU, Solanki HA (2011) Air pollution tolerance index (APTI) of tree species at cross roads of Ahmedabad city. Life Sci Leafl 20:935–943

    Google Scholar 

  • Chow JC, Watson JG, Kuhns H, Etyemezian V, Lowenthal DH, Crow D, Kohl SD, Engelbrecht JP, Green MC (2004) Sourse profiles for industrial, mobile, and area sources in the Big Bend Regional Aerosol Visibility and Observational study. Chemosphere 54:185–208

    Article  CAS  Google Scholar 

  • Constantinidou HA, Kozlowski TT (1979) Effect of SO2 and O3 on Ulmus americana seedling. 1. Visible injury and growth 2. Carbohydrate, proteins and lipids. Can J Bot 57:170–184

    Article  CAS  Google Scholar 

  • Cowan MM (1999) Plant products as antimicrobial agents. Clin Microbiol Rev 12:564–582

    CAS  Google Scholar 

  • Czaja M, Kołton A, Baran A, Muszyńska E, Muras P (2015) Physiological responses of Betula pendula Roth growing in polluted areas. Ecol Quest 22:39–46

    Article  Google Scholar 

  • Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS- scavengers during environmental stress in plants. Front Environ Sci 2:1–13

    Article  CAS  Google Scholar 

  • Dellavalle PD, Cabrera A, Alem D, Larranaga P, Ferreira F, Dalla Rizza M (2011) Antifungal activity of medicinal plant extracts against phytopathogenic fungi Alternaria sp. Chil JAR 71:231–239

    Google Scholar 

  • Demidchik V (2014) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environ Exp Bot 109:212–228

    Article  CAS  Google Scholar 

  • Dudonne S, Vitrac X, Coutiere P, Woillez M, Merillon JM (2009) Comparative study of antioxidant properties and total phenolic content of 30 plant extracts of industrial interest using DPPH, ABTS, FRAP, SOD, and ORAC assays. J Agric Food Chem 57:1768–1774

    Article  CAS  Google Scholar 

  • Elloumi N, Zouari M, Mezghani I, Abdallah FB, Woodward S, Kallel M (2017) Adaptive biochemical and physiological responses of Eriobotrya japonica to fluoride air pollution. Ecotoxicol 26:991–1001

    Article  CAS  Google Scholar 

  • Ferrini F, Bussotti F, Tattini M, Fini A (2014) Trees in urban environment: response mechanisms and benefits for the ecosystem should guide plant selection for future plantings. Agrochimica 58:234–246

    Google Scholar 

  • Ferrini F, Fini A (2011) Sustainable management techniques for trees in the urban areas. JBES 1(1):20

    Google Scholar 

  • Fitriansyah SN, Fidrianny I, Ruslan K (2017) Correlation of total phenolic, flavonoid and carotenoid content of Sesbania sesban (L. Merr) leaves extract with DPPH scavenging activities. IJPPR 9:89–94

    Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Red Signal 11:181–905

    Google Scholar 

  • Giertych MJ, Karolewski P (1993) Changes in phenolic compounds content in needles of Scot pine (Pinus sylvestris L.) seedlings following short term exposition to sulphur dioxide. Arbor Korn 38:43–51

    CAS  Google Scholar 

  • Govindaraju M, Ganeshkumar RS, Suganthi P, Muthukumaran VR, Visvanathan P (2010) Impact Assessment of Air Pollution Stress on Plant Species through Biochemical Estimations. International Journal of Environmental, Chemical, Ecological, Geological and Geophysical Engineering4:696–699

    Google Scholar 

  • Gupta MC, Ghouse AKM, (1986) The effects of coal-smoke pollutants on the leaf epidermal architecture in Solanum molengena L. variety Pusa purble long. Environ Poll 41:315–321

    Article  Google Scholar 

  • Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322

    Article  CAS  Google Scholar 

  • Hematy K, Cherk C, Somerville S (2009) Host-pathogen warfare at the plant cell wall. Curr Opin Plant Biol 12:406–413

    Article  CAS  Google Scholar 

  • Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H (2001) A large family of class III plant peroxidases. Plant Cell Physiol 42:462–468

    Article  CAS  Google Scholar 

  • Hrdlic(ka P, Kula E (2011) Changes in element content of birch leaves (Betula pendula Roth) in polluted air. Pol J Environ Stud 20:661–670

    CAS  Google Scholar 

  • Husain SR, Collard J, Collard P (1987) Hydroxyl radical scavenging activity of flavonoids. Phytochem 26:2489–2491

    Article  CAS  Google Scholar 

  • Iriti M, Faoro F (2009) Chemical diversity and defence metabolism: how plants cope with pathogens and ozone pollution. Int J Mol Sci 10:3371–3399

    Article  CAS  Google Scholar 

  • Jager HJ, Bender J, Grunhage L (1985) Metabolic responses of plants differing in SO2 sensitivity towards SO2 fumigation. Environ Pollut 39:317–335

    Article  Google Scholar 

  • Jansen MAK, van den Noort RE, Tan MYA, Prinsen E, Lagrimini LM, Thornley RNF (2001) Phenol-oxidizing peroxidases contribute to the protection of plants from ultraviolet radiation stress. Plant Physiol 126:1012–1023

    Article  CAS  Google Scholar 

  • Kang MK, Kim SH, Kim KS, Kang Y-H (2017) Correlation analysis between antioxidant activity and phytochemicals in Korean colored corns using principal component analysis. J Agr Sci 6:1–9

    Google Scholar 

  • Kasprzyk I, Rodinkova V, Šauliene I, Ritenberga O, Grinn-Gofron A, Nowak M, Sulborska A, Kaczmarek J, Weryszko-Chmielewska E, Bilous E, Jedryczka M (2015) Air pollution by allergenic spores of the genus Alternaria in the air of central and eastern Europe. Environ Sci Pollut Res 22:9260–9274

    Article  CAS  Google Scholar 

  • Khan AA, Malhotra SS (1982) Peroxidase activity as an indicator of SO2 injury in jack pine and white birch. Biochem Physiol Pflanz 177:643–650

    Article  CAS  Google Scholar 

  • Khan AM, Pandey V, Shukla J, Singh N, Yunus M, Singh SN, Ahmad KJ (1990) Effect of thermal power plant emission on Catharanthus roseus L. Bull Environ Cont Toxicol 44:865–870

    Article  CAS  Google Scholar 

  • Klumpp A, Domingos M, de Moraes RM, Klumpp G (1998) Effects of complex air pollution on trees species of the Atlantic rain forest near Cubatao, Brazil. Chemosphere 36:989–994

    Article  CAS  Google Scholar 

  • Lattanzio V, Lattanzio VMT, Cardinali A, (2006) Role of phenolics in the resistance mechanisms of plant against fungal pathogens and insects. Phytochem 37:23–6

    Google Scholar 

  • Li MH (2003) Peroxidase and superoxide dismutase activities in fig leaves in response to ambient air pollution in a subtropical city. Arch Environ Cont Toxicol 45:168–176

    Article  CAS  Google Scholar 

  • Liyana-Pathirana CM, Shahidi F (2005) Antioxidant activity of commercial soft and hard wheat (Triticum aestivum L.) as affected by gastric pH conditions. J Agr Food Chem 53:2433–2440

    Article  CAS  Google Scholar 

  • Lohe NR, Tyagi B, Singh V, Kumar Tyagi P, Khanna DR, Bhutiani R (2015) A comparative study for air pollution tolerance index of some terrestrial plant species. Global J Sci Environ Manag 1:315–324

    CAS  Google Scholar 

  • Lomeli-Ramirez MG, Davila-Soto H, Silva-Guzman JA, Ruiz HGO, Garcia-Enriquez S (2016) Fungitoxic potential of extract of four Pinus spp. bark to inhibit fungus Trametes versicolor (L. ex Fr) Pilát. BioResources 11:10575–10584

    Article  Google Scholar 

  • Lowry ΟH, Rosebrough ΝJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265

    CAS  Google Scholar 

  • Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol J Environ Stud 15:523–530

    CAS  Google Scholar 

  • Michalowicz J, Duda W (2007) Phenols – Sources and Toxicity. Pol J Environ Stud 16:347–362

    CAS  Google Scholar 

  • Moraes RM, Klumpp A, Furlan CM, Klumpp G, Domingos M, Rinaldi MCS, Modesto IF (2002) Tropical fruit trees as bioindicators of industrial air pollution in southeast Brazil. Environ Int 28:367–374

    Article  CAS  Google Scholar 

  • Oksanen E, Haikio E, Sober J, Karnosky DF (2004) Ozone-induced H2O2 accumulation in field-grown aspen and birch is linked to foliar ultrastructure and peroxisomal activity. New Phytol 161:791–799

    Article  CAS  Google Scholar 

  • Oliveira VM, Carraro E, Auler ME, Khali NM (2016) Quercetin and rutin as potential agents antifungal against Cryptococcus spp. Braz J Biol 76:1029–1034

    Article  CAS  Google Scholar 

  • Oztetik E (2015) Biomarkers of ecotoxicological oxidative stress in an urban environment: using evergreen plant in industrial areas. Ecotoxicol 24:903–914

    Article  CAS  Google Scholar 

  • Pandey DK, Tripathi NN, Tripathi RD, Dixit SN (1982) Fungi-toxic and phytotoxic properties of the essential oil of Hyptis suaveolens. J Plant Dis Prot 89:344–349

    Google Scholar 

  • Pasqualini V, Robles C, Garzino S, Greff S, Bousquet-Melou A, Bonin G (2003) Phenolic compounds content in Pinus halepensis Mill. needles a bioindicator of air pollution. Chemosphere 52:239–248

    Article  CAS  Google Scholar 

  • Pell EJ, Eckardt NA, Glick RE (1994) Biochemical and molecular basis for impairment of photosynthetic potential. Photosynth Res 39:453–462

    Article  CAS  Google Scholar 

  • Pourkhabbaz A, Rastin N, Olbrich A, Langenfeld-Heyser R, Polle A (2010) Influence of environmental pollution on leaf properties of urban plane trees, Platanus orientalis L. Bull Environ Contam Toxicol 85:251–255

    Article  CAS  Google Scholar 

  • Rabe R, Kreeb KH (1979) Enzyme activities and chlorophyll and protein content in plants as indicators of air pollution. Enviroment Pollut 19:119–137

    Article  CAS  Google Scholar 

  • Rai PK (2016) Impact of particulate matter pollution on plants: Implications for environmental biomonitoring. Ecotoxicol Environ Saf 129:120–136

    Article  CAS  Google Scholar 

  • Ramirez-Briones E, Rodriguez-Macias R, Salcedo-Perez E, Martinez-Gallardo N, Tiessen A, Molina-Torres J, Delano-Frier JP, Zanudo-Hernandez J (2017) Seasonal variation in non-structural carbohydrates, sucrolytic activity and secondary metabolites in deciduous and perennial Diospyros species sampled in Western Mexico. PLoS ONE 12:1–24

    Article  CAS  Google Scholar 

  • Rao MN, Rao HVN (1989) Air pollution. Tata McGraw-Hill publishing company limited. New Delhi. 271–272

  • Rezanejad F (2008) The structure and ultra structure of anther epidermis and pollen in Lagerstroemia indica L. (Lythraceae) in response to air pollution. Turk J Bot 32:35–42

    Google Scholar 

  • Robak J, Shridi F, Wolbis M, Krolikowska M (1998) Screening of the influence of flavonoids on lipoxygenase and cyclooxygenase activity, as well as on non enzymatic lipid oxidation. Pol J Pharmacol Pharm 40:451–458

    Google Scholar 

  • Simonova ZA, Chemarkin DA (2013) Peroxidase activity Betula pendula used as indicators of the urban enviroment (by the example of Saratov). Biol Sci 8:1097–1101

    Google Scholar 

  • Tegelberg R, Julkunen-Tiitto R, Vartiainen M, Paunonen R, Rousi M, Kellomaki S (2008) Exposures to elevated CO2, elevated temperature and enhanced UV-B radiation modify activities of polyphenol oxidase and guaiacol peroxidase and concentrations of chlorophylls, polyamines and soluble proteins in the leaves of Betula pendula seedlings. Environ Exp Bot 62:308–315

    Article  CAS  Google Scholar 

  • Tripathi AK, Gautam M (2007) Biochemical parametars of plants as indicators of air pollution. J Enviromen Biol 28:127–132

    CAS  Google Scholar 

  • Uka UN, Hogar J, Belford EJD (2017) Morpho-anatomical and biochemical responses of plants to air pollution. Int J Mod Bot 7:1–11

    Google Scholar 

  • Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human Domination of Earths Ecosystems. Science 277:494–499

    Article  CAS  Google Scholar 

  • Wolfe K, Wu X, Liu RH (2003) Antioxidant activity of apple peels. J Agric Food Chem 51:609–614

    Article  CAS  Google Scholar 

  • Zobel AM, Nighswander JE (1990) Accumulation of phenolic compounds in the necrotic areas of Austrian and red pine needles due to salt spray. Ann Bot 6:629–640

    Article  Google Scholar 

  • Zuccarini P (2009) Troposferic ozone as a fungal elicitor. J Biosci 34:125–138

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was financed by the Ministry of Science and Technology of the Republika Srpska through project no. 19/6-020/961-46/12. For statistical data processing we owe our thanks to colleague Borut Bosanc(ic' M.Sc. from the Faculty of Agriculture of the University of Banja Luka.

Author information

Author notes

  1. These authors contributed equally: Nevena Šuškalo, Dino Hasanagić.

Authors and Affiliations

  1. University of Banja Luka, Faculty of Natural Sciences and Mathematics, Banja Luka, Bosnia and Herzegovina

    Nevena Šuškalo, Dino Hasanagić, Ivan Samelak & Biljana Kukavica

  2. University of Banja Luka, Faculty of Technology, Banja Luka, Bosnia and Herzegovina

    Ljiljana Topalić-Trivunović, Zoran Kukrić & Aleksandar Savić

Authors
  1. Nevena Šuškalo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dino Hasanagić
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ljiljana Topalić-Trivunović
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zoran Kukrić
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ivan Samelak
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Aleksandar Savić
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Biljana Kukavica
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dino Hasanagić.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Šuškalo, N., Hasanagić, D., Topalić-Trivunović, L. et al. Antioxidative and antifungal response of woody species to environmental conditions in the urban area. Ecotoxicology 27, 1095–1106 (2018). https://doi.org/10.1007/s10646-018-1963-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-018-1963-z

Keywords

Search

Navigation