Skip to main content
Log in

Cadmium and zinc activate adaptive mechanisms in Nicotiana tabacum similar to those observed in metal tolerant plants

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Tobacco germinated and grew in the presence of high concentrations of cadmium and zinc without toxic symptoms. Evidence suggests that these ions are sequestered into the vacuole by heavy metal/H + exchanger mechanisms.

Heavy metal hyperaccumulation and hypertolerance are traits shared by a small set of plants which show specialized physiological and molecular adaptations allowing them to accumulate and sequester toxic metal ions. Nicotiana tabacum was used to test its potential as a metal-accumulator in a glass house experiment. Seed germination was not affected in the presence of increasing concentrations of zinc and cadmium. Juvenile and adult plants could concentrate CdCl2 and ZnSO4 to levels exceeding those in the hydroponic growth medium and maintained or increased their leaf dry weight when treated with 0.5- or 1-mM CdCl2 or 1-mM ZnSO4 for 5 days. Accumulation of heavy metals did not affect the chlorophyll and carotenoid levels, while variable effects were observed in cell sap osmolarity. Heavy metal-dependent H+ transport across the vacuole membrane was monitored using quinacrine fluorescence quenching. Cadmium- or zinc-dependent fluorescence recovery revealed that increasing concentrations of heavy metals stimulated the activities of the tonoplast Cd2+ or Zn2+/H+ exchangers. Immunodetection of the V-ATPase subunits showed that the increased proton transport by zinc was not due to changes in protein amount. MTP1 and MTP4 immunodetection and semiquantitative RT-PCR of NtMTP1, NtNRAMP1, and NtZIP1 helped to identify the genes that are likely involved in sequestration of cadmium and zinc in the leaf and root tissue. Finally, we demonstrated that cadmium and zinc treatments induced an accumulation of zinc in leaf tissues. This study shows that N. tabacum possesses a hyperaccumulation response, and thus could be used for phytoremediation purposes.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

MTP:

Metal tolerance protein

NRAMP:

Natural resistance-associated macrophage protein

ZIP:

ZRT, IRT-like protein family

References

  • Ahmad I, Akhtar MJ, Zahir ZA, Jamil A (2012) Effect of cadmium on seed germination and seedling growth of four wheat (Triticum aestivum L.) cultivars. Pak J Bot 44:1569–1574

    Google Scholar 

  • Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Method Enzymol 8(115–1):18

    Google Scholar 

  • Anjum NA, Singh HP, Khan MIR, Khan Masood A, Per TS, Negi A, Batish DR, Khan NA, Duarte AC, Pereira E, Ahmad I (2015) Too much is bad-an appraisal of phytotoxicity of elevated plant-beneficial heavy metal ions. Environ Sci Pollut Res 22:3361–3382

    Article  CAS  Google Scholar 

  • Arrivault S, Senger T, Krämer U (2006) The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. Plant J 46:861–879

    Article  CAS  PubMed  Google Scholar 

  • Assunção AGL, Schat H, Aarts MGM (2003) Thaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol 159:351–360

    Article  Google Scholar 

  • Baker AJM, McGrath SP, Reeves RD, Smith JAC (2000) Metal hyperaccumulator plants: A review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils. In: Terry N, Banuelos G (eds) Phytoremediation of contaminate soil and water. Lewis Publishers, London, pp 85–107

    Google Scholar 

  • Barabasz A, Krämer U, Hanikenne M, Rudzka J, Antosiewicz DM (2010) Metal accumulation in tobacco expressing Arabidopsis halleri metal hyperaccumulation gene depends on external supply. J Exp Bot 61:3057–3067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barceló J, Poschenreider C, Andreu I, Gunsé B (1986) Cadmium-induced decreased of water stress resistance in Bush bean plants (Phaseolus vulgaris L. cv. Contender). I. Effect of Cd on water potential, relative water content, and cell wall elasticity. J Plant Physiol 125:17–25

    Article  Google Scholar 

  • Barkla BJ, Zingarelli L, Blumwald E, Smith JAC (1995) Tonoplast Na+/H+ antiport activity and its energization by the vacuolar H+-ATPase in the halophyte Mesembryanthemum crystallinum. Plant Physiol 109:549–556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belogurov GA, Lahti R (2002) A lysine substitute for K+. A460K mutation eliminates K+ dependence in H+-pyrophosphatase of Carboxydothermus hydrogenoformans. J Biol Chem 277:49651–49654

    Article  CAS  PubMed  Google Scholar 

  • Bennett AB, Spanswick RM (1983) Optical measurements of ΔpH and Δψ in corn root membrane vesicles: kinetic analysis of Cl−1 effects of proton-translocating ATPase. J Membr Biol 71:95–107

    Article  CAS  Google Scholar 

  • Bloß T, Clemens S, Nies DH (2002) Characterization of the ZAT1p zinc transporter from Arabidopsis thaliana in microbial model organisms and reconstituted proteoliposomes. Planta 214:783–791

    Article  PubMed  Google Scholar 

  • Bowman EJ, Siebers A, Altendorf K (1988) Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci USA 85:7972–7976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702

    Article  CAS  PubMed  Google Scholar 

  • Cailliatte R, Schikora A, Briat J-F, Mari S, Curie C (2010) High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell 22:904–917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen M, Shen X, Li D, Ma L, Dong J, Wang T (2009) Identification and characterization of MtMTP1, a Zn transporter of CDF family, in the Medicago truncatula. Plant Physiol Biochem 47:1089–1094

    Article  CAS  PubMed  Google Scholar 

  • Clarke BB, Brennan E (1989) Differential cadmium accumulation and phytotoxicity in sixteen tobacco cultivars. J Air Waste Manag Assoc 39:1319–1322

    CAS  Google Scholar 

  • Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719

    Article  CAS  PubMed  Google Scholar 

  • Curie C, Alonso JM, Le Jean M, Ecker JR, Briat JF (2000) Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem J 347:749–755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Desbrosses-Fonrouge AG, Voigt K, Schroder A, Arrivault S, Thomine S, Kramer U (2005) Arabidopsis thaliana MTP1 is a Zn transporter in the vacuole membrane which mediates Zn detoxification nad drives leaf Zn accumulation. FEBS Lett 579:4165–4174

    Article  CAS  PubMed  Google Scholar 

  • Dräger DB, Desbrosses-Fonrouge AG, Krach C, Chardonnens AN, Meyer RC, Saumitou-Laprade P, Krämer U (2004) Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels. Plant J 39:425–439

    Article  PubMed  Google Scholar 

  • Fodor F (2002) Physiological responses of vascular plants to heavy metals. In: Prasad MNV, Strzatka K (eds) Physiology and biochemistry of metal toxicity and tolerance in plants. Kluwer Academic Publishers-Springer, Netherlands, pp 149–177

    Chapter  Google Scholar 

  • Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46

    Article  CAS  Google Scholar 

  • Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta 1465:190–198

    Article  CAS  PubMed  Google Scholar 

  • Guerinot ML, Eide D (1999) Zeroing in ion zinc uptake in yeast and plants. Curr Opin Plant Biol 2:244–249

    Article  CAS  PubMed  Google Scholar 

  • Gustin JL, Zanis MJ, Salt DE (2011) Structure and evolution of the plant cation diffusion facilitator family of ion transporters. BMC Evol Biol 11:76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hart JJ, Welch RM, Norwell WA, Sullivan LA, Kochian LV (1998) Characterization of cadmium binding uptake and translocation in intact seedlings of bread and durum wheat cultivars. Plant Physiol 116:1413–1420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirschi KD, Korenkov VD, Wilganowski NL, Wagner GJ (2000) Expression of Arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. Plant Physiol 124:125–133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoagland DR, Arnon DI (1938) The water culture method for growing plants without soil. Calif Exp Stat Circ 347:1–39

    CAS  Google Scholar 

  • Islam MM, Hoque MA, Okuma E, Banu MN, Shimoishi Y, Nakamura Y, Murata Y (2009) Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultures tobacco cells. J Plant Physiol 166:1587–1597

    Article  CAS  PubMed  Google Scholar 

  • Kabała K, Janicka-Russak M, Anklewicz A (2013) Mechanism of Cd and Cu action on the tonoplast proton pumps in cucumber roots. Physiol Plant 147:207–217

    Article  PubMed  Google Scholar 

  • Kabała K, Janicka-Russak M, Reda M, Migocka M (2014) Transcriptional regulation of the V-ATPase subunit c and V-PPase isoforms in Cucumis sativus under heavy metal stress. Physiol Plant 150:32–45

    Article  PubMed  Google Scholar 

  • Kabir E, Ray S, Kim KH, Yoon HO, Jeon EC, Kim YS, Cho YS, Yun ST, Brown RJ (2012) Current status of trace metal pollution in soils affected by industrial activities. Sci World J 2012:916705

    Article  Google Scholar 

  • Kawasaki NS, Bowers K, Nishi T, Forgac M, Stevens TH (2003) The amino-terminal domain of the vacuolar proton-translocating ATPase a subunit controls targeting and in vivo dissociation, and the carboxyl-terminal domain affects coupling of proton transport and ATP hydrolysis. J Biol Chem 276:47411–47420

    Article  Google Scholar 

  • Kim D, Gustin JL, Lahner B, Persans MW, Baek D, Yun DJ, Salt DE (2004) The plant CDF family member TgMTP1 from the Ni/Zn hyperaccumulator Thlaspi goesingense acts to enhance efflux of Zn at the plasma membrane when expressed in Saccharomyces cerevisiae. Plant J 39:237–251

    Article  CAS  PubMed  Google Scholar 

  • Kobae Y, Uemura T, Sato MH, Ohnishi M, Mimura T, Nakagawa T, Meshima M (2004) Zinc transporter of Arabidopsis thaliana ATMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell Physiol 45:1749–1758

    Article  CAS  PubMed  Google Scholar 

  • Korenkov V, Hirschi K, Crutchfield JD, Wagner GJ (2007) Enhanced tonoplast Cd/H antiport activity increases Cd, Zn, and Mn tolerance, and impacts root/shoot Cd partitioning in Nicotiana tabacum L. Planta 226:1379–1387

    Article  CAS  PubMed  Google Scholar 

  • Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534

    Article  PubMed  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

  • Lang M, Hao M, Fan Q, Wang W, Mo S, Zaho W, Zhou J (2011) Functional characterization of BjCET3 and BjCET4, two new cation-efflux transporters from Brassica juncea L. J Exp Bot 62:4467–4480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lasat MM, Baker AJM, Kochian LV (1996) Physiological characterization of root Zn2+ absorption and translocation to shoots in Zn hyperaccumulator and nonaccumulator species of Thlaspi. Plant Physiol 112:1715–1722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu G-H, Zhang Y-X, Chai T-Y (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

    Article  CAS  PubMed  Google Scholar 

  • Löw R, Rausch T (1996) In suspension-cultured Daucus carota cells salt stress stimulates H+-transport but not ATP hydrolysis of the V-ATPase. J Exp Bot 47:1725–1732

    Article  Google Scholar 

  • Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Bot 68:1–13

    Article  CAS  Google Scholar 

  • Mäser P, Thomine S, Schroeder JI, Ward JI, Hirschi K, Sze H, Talke IN, Amtmann A, Maathius FJ, Sanders D, Harper JF, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA, Guerinot ML (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667

    Article  PubMed  PubMed Central  Google Scholar 

  • Menguer PK, Farthing E, Peaston KA, Ricachenevsky FK, Fett JP, Williams LE (2013) Functional analysis of the vacuolar zinc transporter OsMTP1. J Exp Bot 64:2871–2883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Migocka M, Kosieradzka A, Papierniak A, Maciaszczyk-Dziubinska E, Posyniak E, Garbiec A, Filleur S (2015) Two metal-tolerance proteins, MTP1 and MTP4, are involved in Zn homeostasis and Cd sequestration in cucumber cells. J Exp Bot 66:1001–1015

    Article  CAS  PubMed  Google Scholar 

  • Milner MJ, Kochian LV (2008) Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102:3–13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montanini B, Blaudez D, Jeandroz S, Sanders D, Chalot M (2007) Phylogenetic and functional analysis of the Cation Diffusion Facilitator (CDF) family: improved signature and prediction of substrate specificity. BMC Genomics 8:107

    Article  PubMed  PubMed Central  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol Plant 15:473–479

    Article  CAS  Google Scholar 

  • Musharraf SG, Shoaib M, Siddiqui AJ, Najama-ul-Haq M (2012) Quantitative analysis of some important metals and metalloids in tobacco products by inductive coupled plasma-mass spectrometry (ICP-MS). Chem Cent J 6:56

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parry RV, Turner JC, Rea PA (1989) High purity preparations of higher plant vacuolar H+-ATPase reveal additional subunits: revised subunit composition. J Biol Chem 264:20025–20032

    CAS  PubMed  Google Scholar 

  • Pomponi M, Censi V, Di Girolamo V, De Paolis A, di Toppi LS, Aromolo R, Costantino P, Cardarelli M (2006) Overexpression of Arabidopsis phytochelatin synthase in tobacco plants enhances Cd2+ tolerance and accumulation but not translocation to the shoot. Planta 223:180–190

    Article  CAS  PubMed  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll II standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Potters G, Pasternak T, Guisez Y, Jansen M (2009) Different stresses, similar morphogenic responses: integrating a plethora of pathways. Plant Cell Environ 32:158–169

    Article  PubMed  Google Scholar 

  • Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181

    Article  CAS  PubMed  Google Scholar 

  • Ratajczak R (2000) Structure, function and regulation of the plant vacuolar H+-translocating ATPase. Biochim Biophys Acta 1465:17–36

    Article  CAS  PubMed  Google Scholar 

  • Remans T, Thijs S, Truyens S, Weyens N, Schellingen K, Keunen E, Gielen H, Cuypers A, Vangronsveld J (2012) Understanding the development of roots exposed to contaminants and the potential of plant- associated bacteria for optimization of growth. Ann Bot 110:239–252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodríguez-Ortíz JC, Valdez-Cepeda RD, Lara-Mireles JL, Rodríguez-Fuentes H, Vázquez-Alvarado RE (2006) Soil nitrogen fertilization effects on phytoextraction of cadmium and lead by tobacco (Nicotiana tabacum L.). Biorem J 10:1–10

    Article  Google Scholar 

  • Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanisms of cadmium mobility and accumulation on Indian mustard. Plant Physiol 109:427–433

    Article  Google Scholar 

  • Sánchez Pineda ESE (2012) Manifiesto de impacto ambiental hidráulico. Particular. CEAMA, Modalidad

    Google Scholar 

  • Sarret G, Harada E, Choi Y-E, Isaure M-P, Geoffroy N, Fakra S, Marcus MA, Birschwilks M, Clemens S, Manceau A (2006) Trichomes of tobacco excrete zinc and zinc-substituted calcium-containing compounds. Plant Physiol 141:1021–1034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seidel T, Siek M, Marg B, Dietz KJ (2013) Energization of vacuolar transport in plant cells and its significance under stress. Int Rev Cell Mol Biol 304:57–131

    Article  CAS  PubMed  Google Scholar 

  • Sen A, Shukla KK, Singh S, Tejovathi G (2013) Impact of heavy metals on root and shoot length of indian mustard: an initial approach for phytoremediation. Sci Secure J Biotechnol 2:48–55

    CAS  Google Scholar 

  • Sharma SS, Dietz K-J, Mimura T (2016) Vacuolar compartmentalization as indispensable component of heavy metal detoxification in plants. Plant Cell Environ 39:1112–1126

    Article  CAS  PubMed  Google Scholar 

  • Sinclair SA, Sherson SM, Jarvis R, Camakaris J, Cobbett CS (2007) The use of the zinc-fluorophore, Zinpyr-1, in the study of zinc homeostasis in Arabidopsis roots. New Phytol 174:39–45

    Article  CAS  PubMed  Google Scholar 

  • Singh AK, Kumar R, Pareek A, Sopory SK, Singla-Pareek SL (2012) Overexpression of rice CBS domain containing protein improves salinity, oxidative, and heavy metal tolerance in transgenic tobacco. Mol Biotechnol 52:205–216

    Article  CAS  PubMed  Google Scholar 

  • Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI (2000) Cadmium and iron transport by members of a plant transporter gene family in Arabidopsis with homology to NRAMP genes. Proc Natl Acad Sci USA 97:4991–4996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van der Zaal BJ, Neuteboom LW, Pinas JE, Chardonnens AN, Schat H, Verkleij JA, Hooykaas PJ (1999) Overexpression of a novel Arabidopsis gene related to putative zinc-transport genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol 119:1047–1055

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Winkle LJ (1999) Biomembrane transport. Academic Press, New York

    Google Scholar 

  • Vasiliadou S, Dordas C (2009) Increased concentration of soil cadmium effects on plant growth, dry matter accumulation, Cd, and Zn uptake of different tobacco cultivars (Nicotiana tabacum L.). Int J Phytoremediat 11:115–130

    Article  CAS  Google Scholar 

  • Vera-Estrella R, Barkla BJ, Higgins VJ, Blumwald E (1994) Plant defense response to fungal pathogens: activation of host-plasma membrane H+-ATPase by elicitor induced enzyme dephosphorylation. Plant Physiol 104:209–215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vera-Estrella R, Barkla BJ, Bohnert HJ, Pantoja O (1999) Salt stress in Mesembryanthemum crystallinum L. cell suspensions activates adaptive mechanisms similar to those observed in the whole plant. Planta 207:426–435

    Article  CAS  PubMed  Google Scholar 

  • Wang J-W, Yan L, Zhang Y-X, Chai T-Y (2013) Molecular cloning of a Brassica juncea yellow stripe-like gene, BjYSL7, whose overexpression increases heavy metal tolerance of tobacco. Plant Cell Rep 32:651–662

    Article  CAS  PubMed  Google Scholar 

  • Wiseman CLS, Zereinin F, Püttmann W (2013) Traffic-related trace element fate and uptake by plant cultivated in roadside soil in Toronto Canada. Sci Total Environ 444:86–95

    Article  Google Scholar 

  • Yrela I (2013) Transition metals in plant photosynthesis. Metallomics 5:1090–1109

    Article  Google Scholar 

  • Yuan L, Yang S, Liu B, Zhang M, Wu K (2012) Molecular characterization of a rice metal tolerance protein, OsMTP1. Plant Cell Rep 31:67–79

    Article  PubMed  Google Scholar 

  • Zhang M, Senoura T, Yang X, Nishizawa NK (2011) Functional analysis of metal tolerance protein isolated from Zn/Cd hyperaccumulating ecotype and non-hyperaccumulating ecotype of Sedum alfredii Hance. FEBS Lett 585:2604–2609

    Article  CAS  PubMed  Google Scholar 

  • Zhou B, Yao W, Wang S, Wang Z, Jiang T (2014) The metallothionein gene, TaMT3, from Tamarix androssowii confers Cd2+ tolerance in tobacco. Int J Mol Sci 15:10398–10409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study has been funded by Consejo Nacional de Ciencia y Tecnología (CONACYT) 178232 and DGAPA IN202514 Grants to R. V-E. The analyses of metals were performed by the IMTA (Instituto Mexicano de Tecnología del Agua). We would like to thank an anonymous reviewer for their helpful input.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rosario Vera-Estrella.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vera-Estrella, R., Gómez-Méndez, M.F., Amezcua-Romero, J.C. et al. Cadmium and zinc activate adaptive mechanisms in Nicotiana tabacum similar to those observed in metal tolerant plants. Planta 246, 433–451 (2017). https://doi.org/10.1007/s00425-017-2700-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-017-2700-1

Keywords

Navigation