Abstract
Callus cultures of two parental clones of Populus nigra L., Poli and 58-861, originating from contrasting environments, were exposed to different cadmium concentrations (0, 150 and 250 μM CdSO4). Clones showed different growth responses to cadmium, evaluated by the tolerance index (Ti), with Poli being more tolerant to the metal at both concentrations. The cadmium concentration at the end of the treatment was very similar between clones at 150 μM CdSO4, while a higher value in 58-861 compared to Poli was detected at 250 μM CdSO4. The bioconcentration factor evidenced the lowest value in Poli at 250 μM CdSO4. Unlike 58-861, cadmium provoked a strong induction of thiols and phytochelatins in clone Poli. In both clones, organic acid concentration differed notably in untreated calli and cadmium treatment induced a general lowering of these compounds. A notably higher antioxidant enzyme activity (ascorbate peroxidase, APX; catalase, CAT; guaiacol peroxidase, GPX) was measured in control calli of clone Poli compared to 58-861. Cadmium induced a remarkable enhancement of APX and CAT, but not GPX, activity at 150 μM CdSO4 in Poli. Conversely, in 58-861 at 150 μM CdSO4, and in both clones at 250 μM CdSO4, a decrease in the antioxidant activity occurred. This investigation provided evidence that these two contrasting genotypes of P. nigra are characterised by a different response to cadmium in callus cultures. In particular, in Poli, the higher tolerance to cadmium is associated with a higher activity of antioxidative enzymes and the ability to strongly increase thiol and PC concentration in response to metal exposure.
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Abbreviations
- APX:
-
Ascorbate peroxidase
- BCF:
-
Bioconcentration factor
- CAT:
-
Catalase
- Cys:
-
Cysteine
- γ-EC:
-
γ-Glutamylcysteine
- GPX:
-
Guaiacol peroxidase
- GSH:
-
Glutathione
- MS:
-
Murashige and Skoog
- OAs:
-
Organic acids
- PCs:
-
Phytochelatins
- Ti:
-
Tolerance index
References
Aina R, Labra M, Fumagalli P, Vannini C, Marsoni M, Cucchi U, Bracale M, Sgorbati S, Citterio S (2007) Thiol-peptide level and proteomic changes in response to cadmium toxicity in Oryza sativa L. roots. Environ Exp Bot 59:381–392
Alscher RG, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants: relationship in green cells. Physiol Plant 100:224–233
Azevedo H, Pinto CGG, Santos C (2005a) Cadmium effects in sunflower: nutritional imbalances in plants and calluses. J Plant Nutr 28:2221–2231
Azevedo H, Pinto CGG, Santos C (2005b) Cadmium effects in sunflower: membrane permeability and changes in catalase and peroxidase activity in leaves and calluses. J Plant Nutr 28:2233–2241
Baker AJM (1987) Metal tolerance. New Phytol 106:93–111
Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17:21–34
Bhatia NP, Walsh KB, Baker AJM (2005) Detection and quantification of ligands involved in nickel detoxification in a herbaceous Ni hyperaccumulator Stackousia tryonii Bailey. J Exp Bot 56:1343–1349
Bittsánsky A, Komives T, Gullner G, Gyulai G, Kiss J, Heszky L, Radimszky L, Rennemberg H (2005) Ability of transgenic poplars with elevated glutathione content to tolerate zinc (2+) stress. Environ Int 31:251–254
Boominathan R, Doran PM (2003) Organic acid complexation, heavy metal distribution and the effect of ATPase inhibition in hairy roots of hyperaccumulator plant species. J Biotechnol 101:131–146
Bosela MJ (2009) Effects of β-lactam antibiotics, auxins, and cytokinins on shoot regeneration from callus cultures of two hybrid aspens, Populus tremuloides × P. tremula and P. canescens × P. grandidentata. Plant Cell Tissue Organ Cult 98:249–261
Chance B, Maehly C (1955) Assay of catalase and peroxidases. Methods Enzymol 11:764–775
Chardonnens AN, Bookum WM, Kujper LDJ, Verkleij JAC, Ernst WHO (1998) Distribution of cadmium in leaves of cadmium tolerant and sensitive ecotypes of Silene vulgaris. Physiol Plant 104:75–80
Chen YX, Lin Q, Luo YM, He YF, Zhen SJ, Yu YL, Tian GM, Wong MH (2003) The role of citric acid on the phytoremediation of heavy metal contaminated soil. Chemosphere 50:807–811
Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719
Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182
Cocozza C, Minnocci A, Tognetti R, Iori V, Zacchini M, Scarascia Mugnozza G (2008) Distribution and concentration of cadmium in root tissue of Populus alba determined by scanning electron microscopy and energy-dispersive X-ray microanalysis. iForest 1:96–103
Cocozza C, Cherubini P, Regier N, Saurer M, Frey B, Tognetti R (2010) Early effects of water deficit on two parental clones of Populus nigra L. grown under different environmental conditions. Funct Plant Biol 37:244–254
Confalonieri M, Balestrazzi A, Bisoffi S, Carbonera D (2003) In vitro culture and genetic engineering of Populus spp.: synergy for forest tree improvement. Plant Cell Tissue Organ Cult 73:109–138
Di Lonardo S, Capuana M, Arnetoli M, Gabbrielli R, Gonnelli C (2011) Exploring the metal phytoremediation potential of three Populus alba L. clones using an in vitro screening. Environ Sci Pollut Res 18:82–90
Dominguez-Solis JR, Lopez-Martin MC, Ager FJ, Ynsa MD, Romero LC, Gotor C (2004) Increased cysteine availability is essential for cadmium tolerance and accumulation in Arabidopsis thaliana. Plant Biotechnol J 2:469–476
Edge R, McGarvey DJ, Truscott TG (1997) The carotenoids as anti-oxidants—a review. J Photochem Photobiol B Biol 41:189–200
Ferreira S, Batista D, Serrazina S, Pais MS (2009) Morphogenesis induction and organogenic nodule differentiation in Populus euphratica Oliv. leaf explants. Plant Cell Tissue Organ Cult 96:35–43
Fornazier RF, Ferreira RR, Pereira GJG, Molina SMG, John Smith R, Lea PJ, Azevedo RA (2002) Cadmium stress in sugar cane callus cultures: effect on antioxidant enzymes. Plant Cell Tissue Organ Cult 71:125–131
Gaudet M, Jorge V, Paolucci I, Beritognolo I, Scarascia Mugnozza G, Sabatti M (2008) Genetic linkage maps of Populus nigra L. including AFLPs, SSRs, SNPs, and sex traits. Tree Genet Genome 4:25–36
Ghnaya AB, Hourmant A, Cerantola S, Kervarec N, Cabon JY, Branchard M, Charles G (2010) Influence of zinc on soluble carbohydrate and free amino acid levels in rapeseed plants regenerated in vitro in the presence of zinc. Plant Cell Tissue Organ Cult 102:191–197
Gullner G, Kömives T, Rennemberg H (2005) Enhanced tolerance of transgenic poplar plants overexpressing g-glutamylcysteine synthetase towards chloroacetanilide herbicides. J Exp Bot 52:971–979
Gzyl J, Gwóźdź EA (2005) Selection in vitro and accumulation of phytochelatins in cadmium tolerant cell line of cucumber (Cucumis sativus). Plant Cell Tissue Organ Cult 80:59–67
Gzyl J, Przymusiski R, Gwóźdź EA (2009) Ultrastructure analysis of cadmium-tolerant and—sensitive cell lines of cucumber (Cucumis sativus L.). Plant Cell Tissue Organ Cult 99:227–232
Han F, Shan X, Zhang S, Wein B, Owens G (2006) Enhanced cadmium accumulation in maize roots—the impact of organic acids. Plant Soil 289:355–368
Harada E, Yamaguchi Y, Koizumi N, Hiroshi S (2002) Cadmium stress induces production of thiol compounds and transcripts for enzymes involved in sulfur assimilation pathways in Arabidopsis. J Plant Physiol 159:445–448
Harmens H, Koevoets PLM, Verkleij JAC, Ernst WHO (1994) The role of low molecular weight organic acids in the mechanism of increased zinc tolerance in Silene vulgaris (Moench) Garcke. New Phytol 126:615–621
Havir EA, McHale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455
Jones DL (1998) Organic acid in the rhizosphere—a critical review. Plant Soil 205:25–44
Joshi MK, Mohanty P (2004) Chlorophyll a fluorescence as a probe of heavy metal ion toxicity in plants. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration, vol 19. Springer, Dordrecht, pp 637–661
Kang B-G, Osburn L, Kopsell D, Tuskan GA, Cheng Z-M (2009) Micropropagation of Populus trichocarpa Nisqually-1: the genotype deriving the Populus reference genome. Plant Cell Tissue Organ Cult 99:251–257
López-Bucio J, Martínez de la Vega O, Guevara-García A, Herrera-Estrella L (2000) Enhanced phosphorus uptake in tobacco transgenic plants that overproduce citrate. Nat Biotechnol 18:450–453
Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278
Meister A (1995) Glutathione metabolism. Methods Enzymol 251:3–13
Mendoza-Cózatl DG, Moreno-Sanchez R (2006) Control of glutathione and phytochelatin synthesis under cadmium stress. Pathway modeling for plants. J Theor Biol 238:919–936
Metwally A, Safronova VI, Belinov AA, Dietz KJ (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 56:167–178
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Nawrot T, Plusquin M, Hogervorst J, Roels HA, Celis H, Thijs L, Vangronsveld J, Van Hecke E, Staessen JA (2006) Environmental exposure to cadmium and risk of cancer: a prospective population-based study. Lancet Oncol 7:119–126
Nehnevajova E, Herzig R, Erismann KH, Schwitzguébel JP (2007) In vitro breeding of Brassica juncea L. to enhance metal accumulation and extraction properties. Plant Cell Rep 26:429–437
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279
Pietrini F, Iannelli MA, Montanari R, Bianconi D, Massacci A (2005) Cadmium interaction with thiols and photosynthesis in higher plants. In: Hemantaranjan A (ed) Advances in plant physiology. Scientific Publishers (India), Jodhpur, pp 313–326
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
Prasad MNV (1995) Cadmium toxicity and tolerance in vascular plants. Environ Exp Bot 25:525–545
Regier N, Streb S, Cocozza C, Schaub M, Cherubini P, Zeeman SC, Frey B (2009) Drought tolerance of two black poplar (Populus nigra L.) clones: contribution of carbohydrates and oxidative stress defence. Plant Cell Environ 32:1724–1736
Rennemberg H, Will B (2000) Phytochelatin production and cadmium accumulation in transgenic poplar (Populus tremula × P. alba). In: Brunold C, Rennemberg H, De Koh LJ, Stulen I, Davidian J-C (eds) Sulfur nutrition and sulfur assimilation in higher plants. Paul Haupt, Bern, pp 393–398
Salt DE, Prince RC, Pickering JI, Raskin I (1995) Mechanism of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109:1427–1433
Samac DA, Tesfaye M (2003) Plant improvement for tolerance to aluminium in acid soils—a review. Plant Cell Tissue Organ Cult 75:189–207
Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726
Shekhawat GS, Verma K, Jana S, Singh K, Teotia P, Prasad A (2010) In vitro biochemical evaluation of cadmium tolerance mechanism in callus and seedlings of Brassica juncea. Protoplasma 239:31–38
Shützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365
Smeets K, Ruytinx J, Semane B, Van Belleghem F, Remans T, Van Sanden S, Vangronsveld J, Cuypers A (2008) Cadmium-induced transcriptional and enzymatic alterations related to oxidative stress. Environ Exp Bot 63:1–8
Sun J, Li L, Liu M, Wang M, Ding M, Deng S, Lu C, Zhou X, Shen X, Zheng X, Chen S (2010) Hydrogen peroxide and nitric oxide mediate K+/Na+ homeostasis and antioxidant defense in NaCl-stressed callus cells of two contrasting poplars. Plant Cell Tissue Organ Cult 103:205–215
Thangavel P, Long S, Minocha R (2007) Changes in phytochelatins and their biosynthetic intermediates in red spruce (Picea rubens Sarg.) cell suspension cultures under cadmium and zinc stress. Plant Cell Tissue Organ Cult 88:201–216
Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:1–9
Zacchini M, Rea E, Tullio M, de Agazio M (2003) Increased antioxidative capacity in maize calli during and after oxidative stress induced by a long lead treatment. Plant Physiol Biochem 41:49–54
Zacchini M, Pietrini F, Scarascia Mugnozza G, Iori V, Pietrosanti L, Massacci A (2009) Metal tolerance, accumulation and translocation in poplar and willow clones treated with cadmium in hydroponics. Water Air Soil Pollut 197:23–34
Zorrig W, Rouached A, Shahzad Z, Abdelly C, Davidian JC, Berthomieu P (2010) Identification of three relationships linking cadmium accumulation to cadmium tolerance and zinc and citrate accumulation in lettuce. J Plant Physiol 167:1239–1247
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Iori, V., Pietrini, F., Massacci, A. et al. Induction of metal binding compounds and antioxidative defence in callus cultures of two black poplar (P. nigra) clones with different tolerance to cadmium. Plant Cell Tiss Organ Cult 108, 17–26 (2012). https://doi.org/10.1007/s11240-011-0006-8
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DOI: https://doi.org/10.1007/s11240-011-0006-8