Skip to main content
Log in

Effects of combined ozone and cadmium stresses on leaf traits in two poplar clones

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

Abstract

Information on plant responses to combined stresses such as ozone (O3) and cadmium (Cd) is scarce in tree species. On the other hand, high O3 concentrations in the atmosphere and heavy metal contaminations in water and soil simultaneously affect forest ecosystems. Toxic metals may exacerbate the consequences of air pollutants. In this research, two poplar clones, differently sensitive to O3 (“I-214” O3-tolerant and “Eridano” O3-sensitive), were grown for 5 weeks in pots supplied with 0 and 150 mg Cd kg−1 soil and then exposed to a 15-day O3 fumigation (60 nl l−1, 5 h a day) or supplied with charcoal-filtered air under the same conditions (referred to as control samples). The effects of the two stressors, alone or in combination, on Cd accumulation, photosynthetic capacity, ethylene emission and oxidative state were investigated in fully expanded leaves. Cadmium accumulation in leaves caused a reduction, but not complete failure, of photosynthesis in Eridano and I-214 poplar clones. The reduction in assimilation rate was more important following O3 fumigation. Stomatal aperture after O3 treatment, instead, increased in I-214 and decreased in Eridano. Overall, Cd treatment was effective in decreasing ethylene emission, whereas O3 fumigation increased it in both clones, although interacting with the metal treatment. Again, O3 fumigation induced a significant increase in ascorbate (ASA) + dehydroascorbate (DHA) content, which was strongly oxidised by O3, thus decreasing the redox state. On the other hand, Cd treatment had a positive effect on ASA content and redox state in I-214, but not in Eridano. Although Cd and O3 are known to share some common toxicity pathways, the combined effects induced distinct clone-specific responses, underlying the complexity of plant reactions to multiple stresses.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

ACC:

1-Aminocyclopropane-1-carboxylic acid

A max :

Net photosynthesis at saturating irradiance

APX:

Ascorbate peroxidise

ASA:

Ascorbate

Cd:

Cadmium

C i :

Internal CO2 concentration

DHA:

Dehydroascorbate

G w :

Stomatal conductance

H2O2 :

Hydrogen peroxide

NADPH:

Nicotinamide adenine dinucleotide phosphate

NO:

Nitric oxide

O3 :

Ozone

[O3]:

O3 concentration

PPFD:

Photosynthetic photon flux density

ROS:

Reactive oxygen species

References

  • Andersen CP (2003) Source-sink balance and carbon allocation below ground in plants exposed to ozone. New Phytol 157:213–228

    Article  CAS  Google Scholar 

  • Anjum NA, Umar S, Ahmad A, Iqbal M (2008) Sulphur protects mustard (Brassica campestris L.) from cadmium toxicity by improving leaf ascorbate and glutathione. Plant Growth Reg 54:271–279

    Article  CAS  Google Scholar 

  • Ashmore MR (2005) Assessing the future global impacts of ozone on vegetation. Plant, Cell Environ 28:949–964

    Article  CAS  Google Scholar 

  • Bagard M, Le Thiec D, Delacote E, Hasenfratz-Sauder MP, Banvoy J, Gérard J, Dizengremel P, Jolivet Y (2008) Ozone-induced changes in photosynthesis and photorespiration of hybrid poplar in relation to the developmental stage of the leaves. Physiol Plant 134:559–574

    Article  CAS  Google Scholar 

  • Bartoli CG, Simontacchi M, Montaldi E, Puntarulo S (1996) Oxidative stress, antioxidant capacity and ethylene production during ageing of cut carnation (Dianthus caryophyllus) petals. J Exp Bot 297:595–601

    Article  Google Scholar 

  • Betz GA, Knappe C, Lapierre C, Olbrich M, Welzl G, Langebartels C, Heller W, Sandermann H, Ernst D (2009) Ozone affects shikimate pathway transcripts and monomeric lignin composition in European beech (Fagus sylvatica L.). Eur J For Res 128:109–116

    Article  CAS  Google Scholar 

  • Bohler S, Sergeant K, Jolivet Y, Hoffmann L, Hausman J-F, Dizengremel P, Renaut J (2013) A physiological and proteomic study of poplar leaves during ozone exposure combined with mild drought. Proteomics 13:1737–1754

    Article  CAS  Google Scholar 

  • Borghi M, Tognetti R, Monteforti G, Sebastiani L (2007) Responses of Populus × euramericana (P. deltoide × P. nigra) clone Adda to increasing copper concentrations. Environ Exp Bot 61:66–73

    Article  CAS  Google Scholar 

  • Borghi M, Tognetti R, Monteforti G, Sebastiani L (2008) Responses of two poplar species (Populus alba and Populus x canadensis) to high copper concentrations. Environ Exp Bot 62:290–299

    Article  CAS  Google Scholar 

  • Cabané M, Pireaux JC, Leger E, Weber E, Dizengremel P, Pollet B, Lapierre C (2004) Condensed lignins are synthesized in poplar leaves exposed to ozone. Plant Physiol 134:586–594

    Article  Google Scholar 

  • Castagna A, Ranieri A (2009) Detoxification and repair process of ozone injury: from O3 uptake to gene expression adjustment. Environ Pollut 157:1461–1469

    Article  CAS  Google Scholar 

  • Castagna A, Di Baccio D, Tognetti R, Ranieri A, Sebastiani L (2013) Differential ozone sensitivity interferes with cadmium stress in poplar clones. Biol Plant 57:313–324

    Article  CAS  Google Scholar 

  • Cocozza C, Vitullo D, Lima G, Maiuro L, Marchetti M, Tognetti R (2014) Enhancing phytoextraction of Cd by combining poplar (clone “I-214”) with Pseudomonas fluorescens and microbial consortia. Environ Sci Pollut Res 21:1796–1808

    Article  CAS  Google Scholar 

  • Conklin P, Barth C (2004) Ascorbic acid, a familiar small molecule intertwined in the response of plants to ozone, pathogens, and the onset of senescence. Plant, Cell Environ 27:959–970

    Article  CAS  Google Scholar 

  • de Silva NDG, Cholewa E, Ryser P (2012) Effects of combined drought and heavy metal stresses on xylem structure and hydraulic conductivity in red maple (Acer rubrum L.). J Exp Bot 63:5957–5966

    Article  Google Scholar 

  • Di Baccio D, Castagna A, Paoletti E, Sebastiani L, Ranieri A (2008) Could the differences in O3 sensitivity between two poplar clones be related to a difference in antioxidant defense and secondary metabolic response to O3 influx? Tree Physiol 28:1761–1772

    Article  Google Scholar 

  • Di Baccio D, Tognetti R, Minnocci A, Sebastiani L (2009) Responses of the Populus x euramericana clone I-214 to excess zinc: carbon assimilation, structural modifications, metal distribution and cellular localization. Environ Exp Bot 67:153–163

    Article  Google Scholar 

  • Di Baccio D, Galla G, Bracci T, Andreucci A, Barcaccia G, Tognetti R, Sebastiani L (2011) Transcriptome analyses of Populus × euramericana clone I-214 leaves exposed to excess zinc. Tree Physiol 31:1293–1308

    Article  Google Scholar 

  • Di Cagno R, Guidi L, De Gara L, Soldatini GF (2001) Combined cadmium and ozone treatments affect photosynthesis and ascorbate-dependent defences in sunflower. New Phytol 151:627–636

    Article  Google Scholar 

  • Diara C, Castagna A, Baldan B, Mensuali Sodi A, Sahr T, Langebartels C, Sebastiani L, Ranieri A (2005) Different kinetics and extent of signalling molecules production modulate the ozone sensitivity of hybrid poplar clones: the role of H2O2, ethylene and salicylic acid. New Phytol 168:351–364

    Article  CAS  Google Scholar 

  • Dickmann DI (1971) Photosynthesis and respiration by developing leaves of cottonwood (Populus deltoides Bartr.). Bot Gaz 132:253–259

    Article  Google Scholar 

  • Dumont J, Cohen D, Gérard J, Jolivet Y, Dizengremel P, Le Thiec D (2014) Distinct responses to ozone of abaxial and adaxial stomata in three Euramerican poplar genotypes. Plant, Cell Environ 37:2064–2076

    Article  CAS  Google Scholar 

  • Durand TC, Hausman JF, Carpin S, Alberic P, Baillif P, Label P, Morabito D (2010a) Zinc and cadmium effects on growth and ion distribution in Populus tremula x Populus alba. Biol Plant 54:191–194

    Article  CAS  Google Scholar 

  • Durand TC, Sergeant K, Planchon S, Carpin S, Label P, Morabito D, Hausman JF, Renaut J (2010b) Acute metal stress in Populus tremula x P. alba (717-1B4 genotype): leaf and cambial proteome changes induced by cadmium2+. Proteomics 10:349–368

    Article  CAS  Google Scholar 

  • Ederli L, Reale L, Ferranti F, Pasqualini S (2004) Responses induced by high concentration of cadmium in Phragmites australis roots. Physiol Plant 121:66–74

    Article  CAS  Google Scholar 

  • Elobeid M, Göbel C, Feussner I, Polle A (2012) Cadmium interferes with auxin physiology and lignification in poplar. J Exp Bot 63:1413–21

    Article  CAS  Google Scholar 

  • Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345

    Article  CAS  Google Scholar 

  • Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90

    Article  CAS  Google Scholar 

  • Gielen B, Low M, Deckmyn G, Metzger U, Franck F, Heerdt C, Matyssek R, Valcke R, Ceulemans R (2007) Chronic ozone exposure affects leaf senescence of adult beech trees: a chlorophyll fluorescence approach. J Exp Bot 58:785–795

    Article  CAS  Google Scholar 

  • Grulke NE, Preisler HK, Rose C, Kirsch J, Balduman L (2002) O-3 uptake and drought stress effects on carbon acquisition of ponderosa pine in natural stands. New Phytol 154:621–631

    Article  CAS  Google Scholar 

  • He J, Qin J, Long L, Ma Y, Li H, Li K, Jiang X, Liu T, Polle A, Liang Z, Luo ZB (2011) Net cadmium flux and accumulation reveal tissue-specific oxidative stress and detoxification in Populus × canescens. Physiol Plant 143:50–63

    Article  CAS  Google Scholar 

  • Horemans N, Raeymaekers T, Van Beek K, Nowocin A, Blust R, Broos K, Cuypers A, Vangronsveld J, Guisez Y (2007) Dehydroascorbate uptake is impaired in the early response of Arabidopsis plant cell cultures to cadmium. J Exp Bot 58:4307–4317

    Article  CAS  Google Scholar 

  • Iannone MF, Rosales EP, Groppa MD, Benavides MP (2010) Reactive oxygen species formation and cell death in catalase-deficient tobacco leaf disks exposed to cadmium. Protoplasma 245:15–27

    Article  CAS  Google Scholar 

  • Iqbal N, Nazar R, Syeed S, Masood A, Khan NA (2011) Exogenously-sourced ethylene increases stomatal conductance, photosynthesis, and growth under optimal and deficient nitrogen fertilization in mustard. J Exp Bot 62:4955–4963

    Article  CAS  Google Scholar 

  • Jin X, Yang X, Mahmood Q, Islam E, Liu D, Li H (2008) Response of antioxidant enzymes, ascorbate and glutathione metabolism towards Cd in hyperaccumulator and nonhyperaccumulator ecotypes of Sedum alfredii H. Environ Toxicol 23:517–529

    Article  CAS  Google Scholar 

  • Johnson JD, Tognetti R, Paris P (2002) Water relations and gas exchange in poplar and willow under water stress and elevated atmospheric CO2. Physiol Plant 115:93–100

    Article  CAS  Google Scholar 

  • Kangasjärvi J, Jaspers P, Kollist H (2005) Signalling and cell death in ozone-exposed plants. Plant, Cell Environ 28:1021–1036

    Article  Google Scholar 

  • Kellomäki S, Wang K-Y (1997) Effects of elevated O3 and CO2 concentrations on photosynthesis and stomatal conductance in Scots pine. Plant, Cell Environ 20:995–1006

    Article  Google Scholar 

  • Khan NA, Anjum NA, Nazar R, Iqbal N (2009) Increased activity of ATP-sulfurylase, contents of cysteine and glutathione reduce high cadmium-induced oxidative stress in high photosynthetic potential mustard (Brassica juncea L.) cultivar. Russ J Plant Physiol 56:670–677

    Article  CAS  Google Scholar 

  • Kieffer P, Schroder P, Dommes J, Hoffmann L, Renaut J, Hausman JF (2009) Proteomic and enzymatic response of poplar to cadmium stress. J Proteomics 72:379–396

    Article  CAS  Google Scholar 

  • Langebartels C, Schraudner M, Heller W, Ernst D, Sandermann H (2002) Oxidative stress and defense reactions in plants exposed to air pollutants and UV-B radiation. In: Inzé D, Van Montagu M (eds) Oxidative Stress in Plants. Taylor and Francis, London, pp 105–135

    Google Scholar 

  • Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts: the effect of hydrogen peroxide and of paraquat. Biochem J 210:899–903

    CAS  Google Scholar 

  • Li Y, Li C, Zheng Y, Wu G, Wuyun T, Xu H, He X, Jiang G (2011) Cadmium pollution enhanced ozone damage to winter wheat: biochemical and physiological evidences. J Environ Sci 23:1–11

    Article  Google Scholar 

  • Lingua G, Bona E, Todeschini V, Cattaneo C, Marsano F et al (2012) Effects of heavy metals and arbuscular mycorrhiza on the leaf proteome of a selected poplar clone: a time course analysis. PLoS One 7:e38662

    Article  CAS  Google Scholar 

  • Liu C, Guo J, Cui Y, Lu T, Zhang X, Shi G (2011) Effects of cadmium and salicylic acid on growth, spectral reflectance and photosynthesis of castor bean seedlings. Plant Soil 344:131–141

    Article  CAS  Google Scholar 

  • Marchi S, Tognetti R, Minnocci A, Borghi M, Sebastiani L (2008) Variation in mesophyll anatomy and photosynthetic capacity during leaf development in a deciduous mesophyte fruit tree (Prunus persica) and an evergreen sclerophyllous Mediterranean shrub (Olea europaea). Trees 22:559–571

    Article  CAS  Google Scholar 

  • Markovska YK, Gorinova NI, Nedkovska MP, Miteva KM (2009) Cadmium induced oxidative damage and antioxidative responses in Brassica juncea plants. Biol Plant 53:151–154

    Article  CAS  Google Scholar 

  • Marmiroli M, Pietrini F, Maestri E, Zacchini M, Marmiroli N, Massacci A (2011) Growth, physiological and molecular traits in the Salicaceae trees investigated for phytoremediation of heavy metals and organics. Tree Physiol 31:1319–1334

    Article  CAS  Google Scholar 

  • Masood A, Iqbal N, Khan NA (2012) Role of ethylene in alleviation of cadmium-induced photosynthetic capacity inhibition by sulphur in mustard. Plant, Cell Environ 35:524–533

    Article  CAS  Google Scholar 

  • Matyssek R, Sandermann H (2003) Impact of ozone on trees: an ecophysiological perspective. Progress Bot 64:349–404

    Article  CAS  Google Scholar 

  • Mensuali Sodi A, Panizza M, Tognoni F (1992) Quantification of ethylene losses in different container-seal systems and comparison of biotic and abiotic contributions to ethylene accumulation in cultured tissues. Physiol Plant 84:472–476

    Article  CAS  Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19

    Article  CAS  Google Scholar 

  • Mobin M, Khan NA (2007) Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. J Plant Physiol 164:601–610

    Article  CAS  Google Scholar 

  • Moeder W, Barry CS, Tauriainen AA, Betz C, Tuomainen J, Utriainen M, Grierson D, Sandermann H, Langebartels C, Kangasjärvi J (2002) Ethylene synthesis regulated by biphasic induction of 1-aminocyclopropane-1-carboxylic acid synthase and 1-aminocyclopropane-1-carboxylic acid oxidase genes is required for hydrogen peroxide accumulation and cell death in ozone-exposed tomato. Plant Physiol 130:1918–1926

    Article  CAS  Google Scholar 

  • Mohamed AA, Castagna A, Ranieri A, Sanità di Toppi L (2012) Cadmium tolerance in Brassica juncea roots and shoots is affected by antioxidant status and phytochelatin biosynthesis. Plant Physiol Biochem 57:15–22

    Article  CAS  Google Scholar 

  • Nikolić N, Kojić D, Pilipović A, Pajević S, Krstić B, Borišev M, Orlović S (2008) Responses of hybrid poplar to cadmium stress: photosynthetic characteristics, cadmium and proline accumulation and antioxidant enzime activity. Acta Biologica Cracoviensia Ser Bot 502:95–103

    Google Scholar 

  • Nocito FF, Lancilli C, Giacomini B, Sacchi GA (2007) Sulfur metabolism and cadmium stress in higher plants. Plant Stress 1:142–156

    Google Scholar 

  • Okamura M (1980) An improved method for determination of L-ascorbic acid and L-dehydroascorbic acid in blood plasma. Clin Chem Acta 103:259–268

    Article  CAS  Google Scholar 

  • Panek JA (2004) Ozone uptake, water loss and carbon exchange dynamics in annually drought-stressed Pinus ponderosa forests: measured trends and parameters for uptake modeling. Tree Physiol 24:277–290

    Article  CAS  Google Scholar 

  • Panek JA, Goldstein AH (2001) Response of stomatal conductance to drought in ponderosa pine: implications for carbon and ozone uptake. Tree Physiol 21:335–342

    Article  Google Scholar 

  • Pierik R, Tholen D, Poorter H, Visser EJW, Voesenek LACJ (2006) The Janus face of ethylene: growth inhibition and stimulation. Trends Plant Sci 11:176–183

    Article  CAS  Google Scholar 

  • Pietrini F, Zacchini M, Iori V, Pietrosanti L, Ferretti M, Massacci A (2010) Spatial distribution of cadmium in leaves and its impact on photosynthesis: examples of different strategies in willow and poplar clones. Plant Biol 12:355–363

    Article  CAS  Google Scholar 

  • Pilon-Smits E (2005) Phytoremediation. Biochem Biophys Res Commun 56:15–39

    CAS  Google Scholar 

  • Ranieri A, Castagna A, Padu E, Moldau H, Rahi M, Soldatini GF (1999) The decay of O3 through direct reaction with cell wall ascorbate is not sufficient to explain the different degrees of O3-sensitivity in two poplar clones. J Plant Physiol 150:250–255

    Article  Google Scholar 

  • Ranieri A, Serini R, Castagna A, Nali C, Baldan B, Lorenzini G, Soldatini GF (2000) Differential sensitivity to ozone in two poplar clones. Analysis of thylakoid pigment-protein complexes. Physiol Plant 110:181–188

    Article  CAS  Google Scholar 

  • Rao MV, Lee H-I, Davis KR (2002) Ozone-induced ethylene production is dependent on salicylic acid, and both salicylic acid and ethylene act in concert to regulate ozone-induced cell death. Plant J 32:447–456

    Article  CAS  Google Scholar 

  • Ribas A, Peñuelas J, Elvira S, Gimeno BS (2005) Ozone exposure induces the activation of leaf senescence-related processes and morphological and growth changes in seedlings of Mediterranean tree species. Environ Pollut 134:291–300

    Article  CAS  Google Scholar 

  • Rivetta A, Negrini N, Cocucci M (1997) Involvement of Ca2+-calmodulin in Cd2+ toxicity during the early phases of radish (Raphanus sativus L.) seed germination. Plant, Cell Environ 20:600–608

    Article  CAS  Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, del Río LA et al (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots: imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant, Cell Environ 29:1532–1544

    Article  Google Scholar 

  • Romero-Puertas MC, Rodríguez-Serrano M, Corpas FJ, Gómez M, del Río LA, Sandalio LM (2004) Cd-induced subcellular accumulation of O2 and H2O2 in pea leaves. Plant, Cell Environ 27:1122–1134

    Article  CAS  Google Scholar 

  • Schützendübel A, Nikolova P, Rudolf C, Polle A (2002) Cadmium and H2O2-induced oxidative stress in Populus x canescens roots. Plant Physiol Biochem 40:577–584

    Article  Google Scholar 

  • Sebastiani L, Scebba F, Tognetti R (2004) Heavy metal accumulation and growth responses in poplar clones Eridano (Populus deltoides × maximowiczii) and I-214 (P. × euramericana) exposed to industrial waste. Environ Exp Bot 52:79–88

    Article  CAS  Google Scholar 

  • Tognetti R, Sebastiani L, Minnocci A (2004) Gas exchange and foliage characteristics of two poplar clones grown in soil amended with industrial waste. Tree Physiol 24:75–82

    Article  Google Scholar 

  • Tognetti R, Massacci A, Scarascia Mugnozza G (2011) Editorial: Fifth International Poplar Symposium: ‘Poplars and willows: from research models to multipurpose trees for a bio-based society’. Tree Physiol 31:1289–1292

    Article  Google Scholar 

  • Trudić B, Kebert M, Popović BM, Štajner D, Orlović S, Galović V (2012) The level of oxidative stress in poplars due to heavy metal pollution in soil. Baltic For 18:214–227

    Google Scholar 

  • Vahala J, Ruonala R, Keinänen M, Tuominen H, Kangasjärvi J (2003) Ethylene insensitivity modulates ozone-induced cell death in Birch. Plant Physiol 132:185–195

    Article  CAS  Google Scholar 

  • Vollenweider P, Ottinger M, Gunthardt-Goerg MS (2003) Validation of leaf ozone symptoms in natural vegetation using microscopical methods. Environ Pollut 124:101–118

    Article  CAS  Google Scholar 

  • Wang KL-C, Li H, Ecker JR (2002) Ethylene biosynthesis and signalling networks. Plant Cell 14:S131–S151

    CAS  Google Scholar 

  • Wi SJ, Jang SJ, Park KY (2010) Inhibition of biphasic ethylene production enhances tolerance to abiotic stress by reducing the accumulation of reactive oxygen species in Nicotiana tabacum. Mol Cells 30:37–49

    Article  CAS  Google Scholar 

  • Wittig VE, Ainsworth EA, Long SP (2007) To what extent do current and projected increases in surface ozone affect photosynthesis and stomatal conductance of trees? A meta-analytic review of the last 3 decades of experiments. -. Plant, Cell Environ 30:1150–1162

    Article  CAS  Google Scholar 

  • Wittig VE, Ainsworth EA, Naidu SL, Karnosky DF, Long SP (2009) Quantifying the impact of current and future tropospheric ozone on tree biomass, growth, physiology and biochemistry: a quantitative meta-analysis. Glob Chang Biol 15:396–424

    Article  Google Scholar 

  • Wójcik M, Tukiendorf A (2011) Glutathione in adaptation of Arabidopsis thaliana to cadmium stress. Biol Plant 55:125–132

    Article  Google Scholar 

  • Wullschleger SD (1993) Biochemical limitations to carbon assimilation in C3 plants—a retrospective analysis of the A/C i curves from 109 species. J Exp Bot 44:907–920

    Article  CAS  Google Scholar 

  • Yoshida S, Tamaoki M, Ioki M et al (2009) Ethylene and salicylic acid control glutathione biosynthesis in ozone-exposed Arabidopsis thaliana. Physiol Plant 136:284–298

    Article  CAS  Google Scholar 

  • Zacchini M, Iori V, Scarascia Mugnozza G, Pietrini F, Massacci A (2011) Cadmium accumulation and tolerance in Populus nigra and Salix alba. Biol Plant 55:383–386

    Article  CAS  Google Scholar 

  • Zheng Y, Shimizu H, Barnes JD (2002) Limitations to CO2 assimilation in ozone-exposed leaves of Plantago major. New Phytol 155:67–78

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We kindly acknowledge Giuseppe Nervo and Lorenzo Vietto (CRA, Casale Monferrato, Italy) for having provided cuttings of the two poplar clones. The present research was supported by funds of the University of Pisa and Scuola Superiore Sant’Anna, Pisa. We also acknowledge funding by the project “Molecular, physiological, and agronomic analyses for selecting and managing Salicacee in phytoremediation” (Italian Ministry for Education, University and Research).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Antonella Castagna or Roberto Tognetti.

Additional information

Responsible editor: Elena Maestri

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 77 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Castagna, A., Di Baccio, D., Ranieri, A.M. et al. Effects of combined ozone and cadmium stresses on leaf traits in two poplar clones. Environ Sci Pollut Res 22, 2064–2075 (2015). https://doi.org/10.1007/s11356-014-3481-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3481-8

Keywords

Navigation