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.
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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
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
Ashmore MR (2005) Assessing the future global impacts of ozone on vegetation. Plant, Cell Environ 28:949–964
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
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
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
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
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
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
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
Castagna A, Ranieri A (2009) Detoxification and repair process of ozone injury: from O3 uptake to gene expression adjustment. Environ Pollut 157:1461–1469
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
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
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
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
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
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
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
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
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
Dickmann DI (1971) Photosynthesis and respiration by developing leaves of cottonwood (Populus deltoides Bartr.). Bot Gaz 132:253–259
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
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
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
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
Elobeid M, Göbel C, Feussner I, Polle A (2012) Cadmium interferes with auxin physiology and lignification in poplar. J Exp Bot 63:1413–21
Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345
Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90
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
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
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
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
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
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
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
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
Kangasjärvi J, Jaspers P, Kollist H (2005) Signalling and cell death in ozone-exposed plants. Plant, Cell Environ 28:1021–1036
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
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
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
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
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
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
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
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
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
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
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
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
Matyssek R, Sandermann H (2003) Impact of ozone on trees: an ecophysiological perspective. Progress Bot 64:349–404
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
Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19
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
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
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
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
Nocito FF, Lancilli C, Giacomini B, Sacchi GA (2007) Sulfur metabolism and cadmium stress in higher plants. Plant Stress 1:142–156
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
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
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
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
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
Pilon-Smits E (2005) Phytoremediation. Biochem Biophys Res Commun 56:15–39
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
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
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
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
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
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
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
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
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
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
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
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
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
Vollenweider P, Ottinger M, Gunthardt-Goerg MS (2003) Validation of leaf ozone symptoms in natural vegetation using microscopical methods. Environ Pollut 124:101–118
Wang KL-C, Li H, Ecker JR (2002) Ethylene biosynthesis and signalling networks. Plant Cell 14:S131–S151
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
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
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
Wójcik M, Tukiendorf A (2011) Glutathione in adaptation of Arabidopsis thaliana to cadmium stress. Biol Plant 55:125–132
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
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
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
Zheng Y, Shimizu H, Barnes JD (2002) Limitations to CO2 assimilation in ozone-exposed leaves of Plantago major. New Phytol 155:67–78
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).
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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
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DOI: https://doi.org/10.1007/s11356-014-3481-8