Abstract
Conifers are often used as biomarkers of industrial pollution; however, little is known about the effects of heavy metals on them because only a few species have been tested. The aim of this work was to investigate the effects of cadmium (Cd2+) and lead (Pb2+) at three different concentrations (50, 250, and 500 µM) on the detoxification potential of Abies alba and Picea abies embryogenic cell masses throughout the 21-day proliferation period. Embryogenic cell masses of A. alba and P. abies responded to treatment with cadmium and lead by inducing phytochelatins and their biosynthetic intermediates. With increasing heavy metal concentrations, glutathione was used for the synthesis of phytochelatins enabling the tissues to bind to heavy metal ions and thereby avoiding the production of reactive oxygen species. Lead in A. alba and cadmium in both species caused similar increases of all antioxidative thiol compounds; thus, similar mechanisms involving a heavy metal-induced stress response can be assumed. In P. abies, the lowest lead concentration tested provoked the highest antioxidative response. Since a very low uptake of lead into the tissue was observed, the higher resistance of P. abies can be attributed to its ability to reduce lead uptake after longer exposure times. The results of cadmium treatment of both species and lead treatment of A. alba indicated the possibility of testing these coniferous species as potential phytoremediators. This is the first study to analyze the effects of heavy metals on the low-molecular-weight plant thiol content in A. alba embryogenic cell masses.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bankaji I, Caçador I, Sleimi N (2015) Physiological and biochemical responses of Suaeda fruticosa to cadmium and copper stresses: growth, nutrient uptake, antioxidant enzymes, phytochelatin, and glutathione levels. Environ Sci Pollut Res 22:13058–13069. doi:10.1007/s11356-015-4414-x
Chmielowska-Bąk J, Gzyl J, Rucińska-Sobkowiak R, Arasimowicz-Jelonek M, Deckert J (2014) The new insights into cadmium sensing. Front Plant Sci 5:245. doi:10.3389/fpls.2014.00245
Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832. doi:10.1104/pp.123.3.825
Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182. doi:10.1146/annurev.arplant.53.100301.135154
DalCorso G, Farinati S, Maistri S, Furini A (2008) How plants cope with cadmium: staking all on metabolism and gene expression. J Integr Plant Biol 50:1268–1280. doi:10.1111/j.1744-7909.2008.00737.x
DalCorso G, Farinati S, Furini A (2010) Regulatory networks of cadmium stress in plants. Plant Signal Behav 5:663–667. doi:10.4161/psb.5.6.11425
Das P, Samantaray S, Rout GR (1997) Studies on cadmium toxicity in plants: a review. Environ Pollut 98:29–36. doi:10.1016/S0269-7491(97)00110-3
Davidian JC, Kopriva S (2010) Regulation of sulfate uptake and assimilation—the same or not the same? Mol Plant 3:314–325. doi:10.1093/mp/ssq001
Đorđević B, Krajňáková J, Hampel D, Gömöry D, Havel L (2017) Effects of cadmium and lead stress on somatic embryogenesis of coniferous species. Part I: Evaluation of the genotype-dependent response. Acta Physiol Plant. doi:10.1007/s11738-017-2436-3
di Toppi SL, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130. doi:10.1016/S0098-8472(98)00058-6
di Toppi SL, Lambardi M, Pazzagli L, Cappugi G, Durante M, Gabbrielli R (1998) Response to cadmium in carrot in vitro plants and cell suspension cultures. Plant Sci 137:119–129. doi:10.1016/S0168-9452(98)00099-5
Flores-Cáceres ML, Hattab S, Hattab S, Boussetta H, Banni M, Hernández LE (2015) Specific mechanisms of tolerance to copper and cadmium are compromised by a limited concentration of glutathione in alfalfa plants. Plant Sci 233:165–173. doi:10.1016/j.plantsci.2015.01.013
Foyer CH, Theodoulou FL, Delrot S (2001) The functions of inter- and intracellular glutathione transport systems in plants. Trends Plant Sci 6:486–492. doi:10.1016/S1360-1385(01)02086-6
Gandois L, Probst A (2012) Localisation and mobility of trace metal in silver fir needles. Chemosphere 87:204–210. doi:10.1016/j.chemosphere.2011.12.020
Garrido T, Mendoza J, Riveros R, Sáez L (2010) Acute and chronic effect of copper on levels of reduced and oxidized glutathione and nutrient uptake of tomato plants. J Plant Nutr Soil Sci 173:920–926. doi:10.1002/jpln.200800306
Golubović Ćurguz V, Raičević V, Veselinović M, Tabaković-Tošić M, Vilotić D (2012) Influence of heavy metals on seed germination and growth of Picea abies L. Karst. Pol J Environ Stud 21:355–361
Gupta DK, Huang HG, Corpas FJ (2013) Lead tolerance in plants: strategies for phytoremediation. Environ Sci Pollut Res 20:2150–2161. doi:10.1007/s11356-013-1485-4
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. doi:10.1007/s11240-004-8808-6
Ha SB, Smith AP, Howden R, Dietrich WM, Bugg S, O’Connell MJ, Goldsbrough PB, Cobbett CS (1999) Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell 11:1153–1163. doi:10.1105/tpc.11.6.1153
Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11. doi:10.1093/jexbot/53.366.1
Hernández LE, Sobrino-Plata J, Montero-Palmero MB, Carrasco-Gil S, Flores-Cáceres ML, Ortega-Villasante C, Escobar C (2015) Contribution of glutathione to the control of cellular redox homeostasis under toxic metal and metalloid stress. J Exp Bot 66:2901–2911. doi:10.1093/jxb/erv063
Hoffmann T, Kutter C, Santamaría JM (2004) Capacity of Salvinia minima Baker to tolerate and accumulate As and Pb. Eng Life Sci 4:61–65. doi:10.1002/elsc.200400008
Hu Y, Liu X, Bai J, Shih K, Zeng EY, Cheng H (2013) Assessing heavy metal pollution in the surface soils of a region that had undergone three decades of intense industrialization and urbanization. Environ Sci Pollut Res 20:6150–6159. doi:10.1007/s11356-013-1668-z
Huska D, Zitka O, Krystofova O, Adam V, Babula P, Zehnalek J, Bartusek K, Beklova M, Havel L, Kizek R (2010) Effects of cadmium(II) ions on early somatic embryos of norway spruce studied by using electrochemical techniques and nuclear magnetic resonance. Int J Electrochem Sci 5:1535–1549
Kotrba P, Macek T, Ruml T (1999) Heavy metal-binding peptides and proteins in plants. A review. Collect Czechoslov Chem Commun 64:1057–1086. doi:10.1135/cccc19991057
Krajňáková J, Bertolini A, Gömöry D, Vianello A, Häggman H (2013) Initiation, long-term cryopreservation, and recovery of Abies alba Mill. embryogenic cell lines. In Vitro Cell Dev Biol Plant 49:560–571. doi:10.1007/s11627-013-9512-1
Kuroda K, Kagawa A, Tonosaki M (2013) Radiocesium concentrations in the bark, sapwood and heartwood of three tree species collected at Fukushima forests half a year after the Fukushima Dai-ichi nuclear accident. J Environ Radioact 122:37–42. doi:10.1016/j.jenvrad.2013.02.019
Li X, Cen H, Chen Y, Xu S, Peng L, Zhu H, Li Y (2016) Physiological analyses indicate superoxide dismutase, catalase, and phytochelatins play important roles in Pb tolerance in Eremochloa ophiuroides. Int J Phytoremediation 18:251–260. doi:10.1080/15226514.2015
Lin YF, Aarts MG (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69:3187–3206. doi:10.1007/s00018-012-1089-z
Liu GY, Zhang YX, Chai TY (2011) Phytochelatin synthase of Thlaspi caerulescens enhanced tolerance and accumulation of heavy metals when expressed in yeast and tobacco. Plant Cell Rep 30:1067–1076. doi:10.1007/s00299-011-1013-2
Maine MA, Duarte MV, Suñé NL (2001) Cadmium uptake by floating macrophytes. Water Res 35:2629–2634. doi:10.1016/S0043-1354(00)00557-1
Mishra S, Srivastava S, Tripathi RD, Kumar R, Seth CS, Gupta DK (2006) Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere 65:1027–1039. doi:10.1016/j.chemosphere.2006.03.033
Moudouma CFM, Riou C, Gloaguen V, Saladin G (2013) Hybrid larch (Larix × eurolepis Henry): a good candidate for cadmium phytoremediation? Environ SciPollut Res 20:1889–1894. doi:10.1007/s11356-012-1419-6
Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216. doi:10.1007/s10311-010-0297-8
Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2011) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484. doi:10.1111/j.1365-3040.2011.02400.x
Park J, Song WY, Ko D, Eom Y, Hansen TH, Schiller M, Lee TG, Martinoia E, Lee Y (2012) The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant J 69:278–288. doi:10.1111/j.1365-313X.2011.04789.x
Piechalak A, Tomaszewska B, Baralkiewicz D, Malecka A (2002) Accumulation and detoxification of lead ions in legumes. Phytochemistry 60:153–162. doi:10.1016/S0031-9422(02)00067-5
Przybysz A, Sæbø A, Hanslin HM, Gawroński SW (2014) Accumulation of particulate matter and trace elements on vegetation as affected by pollution level, rainfall and the passage of time. Sci Total Environ 481:360–369. doi:10.1016/j.scitotenv.2014.02.072
Queval G, Thominet D, Vanacker H, Miginiac-Maslow M, Gakiére B, Noctor G (2009) H2O2-activated up-regulation of glutathione in Arabidopsis involves induction of genes encoding enzymes involved in cysteine synthesis in the chloroplast. Mol Plant 2:344–356. doi:10.1093/mp/ssp002
Saladin G (2015) Phytoextraction of heavy metals: the potential efficiency of conifers. In: Sherameti I, Varma A (eds) Soil biology, vol 44. Heavy metal contamination of soils—monitoring and remediation. Springer, Switzerland, pp 333–353
Schmöger MEV, Oven M, Grill E (2000) Detoxification of arsenic by phytochelatins in plants. Plant Physiol 122:793–801. doi:10.1104/pp.122.3.793
Schröder P, Fischer C, Debus R, Wenzel A (2003) Reaction of detoxification mechanisms in suspension cultured spruce cells (Picea abies L. Karst.) to heavy metals in pure mixture and in soil eluates. Environ Sci Pollut Res 10:225–234. doi:10.1007/BF02979658
Seregin IV, Pekhov VM, Ivanov VB (2002) Plasmolysis as a tool to reveal lead localization in the apoplast of root cells. Russ J Plant Physiol 49:283–285. doi:10.1023/A:1014822127865
Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52. doi:10.1590/S1677-04202005000100004
Shukla D, Tiwari M, Tripathi RD, Nath P, Trivedi PK (2013) Synthetic phytochelatins complement a phytochelatin-deficient Arabidopsis mutant and enhance the accumulation of heavy metal(loid)s. Biochem Biophys Res Commun 434:664–669. doi:10.1016/j.bbrc.2013.03.138
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. doi:10.1007/s11240-006-9192-1
Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:364–372. doi:10.1016/j.pbi.2009.05.001
VSN International (2014) GenStat for Windows, 17th edn. VSN International, Hemel Hempstead
Wójcik M, Tukiendorf A (2014) Accumulation and tolerance of lead in two contrasting ecotypes of Dianthus carthusianorum. Phytochemistry 100:60–65. doi:10.1016/j.phytochem.2014.01.008
Xiang C, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550. doi:10.1105/tpc.10.9.1539
Zenk MH (1996) Heavy metal detoxification in higher plants—a review. Gene 179:21–30. doi:10.1016/S0378-1119(96)00422-2
Zhu YL, Pilon-Smits EAH, Tarun AS, Weber SU, Jouanin L, Terry N (1999) Cadmium tolerance and accumulation in indian mustard is enhanced by overexpressing γ-glutamylcysteine synthetase. Plant Physiol 121:1169–1177. doi:10.1104/pp.121.4.1169
Zitka O, Krystofova O, Sobrova P, Adam V, Zehnalek J, Beklova M, Kizek R (2011) Phytochelatin synthase activity as a marker of metal pollution. J Hazard Mater 192:794–800. doi:10.1016/j.jhazmat.2011.05.088
Zitka O, Krystofova O, Hynek D, Sobrova P, Kaiser J, Sochor J, Zehnalek J, Babula P, Ferrol N, Kizek R, Adam V (2013) Metal Transporters in Plants. In: Gupta DK, Corpas FJ, Palma JM (eds) Heavy metal stress in plants. Springer, Berlin, pp 19–41
Acknowledgements
This work was supported by the IGA (Internal Grant Agency) FFWT (Faculty of Forestry and Wood Technology) Mendel University in Brno (Grant Number 54/2013). We are thankful to the Write Science Right Company for linguistic editing.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J Van Huylenbroeck.
Rights and permissions
About this article
Cite this article
Đorđević, B., Prášková, M., Hampel, D. et al. Effects of cadmium and lead stress on somatic embryogenesis of coniferous species. Part II: Changes of thiol substances. Acta Physiol Plant 39, 141 (2017). https://doi.org/10.1007/s11738-017-2441-6
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-017-2441-6