Log in

Enhancement of cadmium tolerance and accumulation by introducing Perilla frutescens (L.) Britt var. frutescens genes in Nicotiana tabacum L. plants

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

Abstract

The tobacco has the genetic potential to remove toxic metals from the soil. To develop hyperaccumulating tobacco plants, distant hybridization between tobacco (Nicotiana tabacum L.), a high-biomass crop, and Perilla frutescens (L.) Britt var. frutescens, a newfound Cd-hyperaccumulator species, was carried out using a novel method viz. pollination following grafting. Their hybrid nature was preliminarily confirmed by phenotype, isozyme pattern, random amplified polymorphic DNA (RAPD) and metabolites analysis. About 120 putative F2 hybrids derived from the cross-combination [(N. sylvestris Speg. & Comes rootstock + N. tabacum L. var. 78–04 scion) × P. frutescens (L.) Britt var. frutescens] were then subjected to up to 300 μM CdCl2 in hydroponic conditions for 10 days. Results showed five seedlings were more resistant to Cd than female parent and accumulated 314.6 ± 99.9 mg kg−1 Cd in their aerial biomass, which was 5.7 times greater than that in "78-04" tobacco (47.2 ± 3.56 mg kg−1) (P ≤ 0.05). Two of these seedlings exceeded male parent P. frutescens in the Cd concentration of shoots and reached 424 and 396 mg kg−1, which was 13 % and 6 % greater for that of perilla (374.2 ± 10.38 mg kg−1), respectively. Compared with parents, two other F2 hybrids tended to accumulate more Cd in the root with bioconcentration factor (BCF) 7.05 and 5.17, respectively. Only one hybrid showed lower Cd concentration but transferred Cd more effectively from the root to the shoot than parents and other F2 hybrids, with the maximum translocation factor (TF) value 1.37. These indicated that the introduction of P. frutescens genes could obviously enhance the cadmium tolerance and accumulation of superior individuals.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Andrianov V, Borisjuk N, Pogrebnyak N, Brinker A, Dixon J, Spitsin S, Flynn J, Matyszczuk P, Andryszak K, Laurelli M, Golovkin M, Koprowski H (2010) Tobacco as a production platform for biofuel: overexpression of Arabidopsis DGAT and LEC2 genes increases accumulation and shifts the composition of lipids in green biomass. Plant Biotechnol J 3:277–287

    Article  Google Scholar 

  • Assunção AG, Pieper B, Vromans J, Lindhout P, Aarts MG, Schat H (2006) Construction of a genetic linkage map of Thlaspi caerulescens and quantitative trait loci analysis of zinc accumulation. New Phytol 1:21–32

    Article  Google Scholar 

  • Barceló J, Poschenrieder C (2003) Phytoremediation: principles and perspectives. Contrib Sci 3:333–334

    Google Scholar 

  • Bhargava A, Carmona FF, Bhargava M, Srivastava S (2012) Approaches for enhanced phytoextraction of heavy metals. J Environ Manage 105:103–120

    Article  CAS  Google Scholar 

  • Carolina TM, Alesso M, Acosta M, Olsina R, Fernández LP (2013) Determination of cadmium in tobacco by solid surface fluorescence using nylon membranes coated with carbon nanotubes. Talanta 107:61–66

    Article  Google Scholar 

  • Chen GG, Zhang JY, Guo YL (2004) Analysis of volatile components of fresh Perilla frutescens (L.) Britt. var. acuta (Thunb.) Kudo by headspace GC/MS. J Essent Oil Res 5:435–436

    Article  Google Scholar 

  • Deniau AX, Pieper B, Ten Bookum WM, Lindhout P, Aarts MG, Schat H (2006) QTL analysis of cadmium and zinc accumulation in the heavy metal hyperaccumulator Thlaspi caerulescens. Theor Appl Genet 113:907–920

    Article  CAS  Google Scholar 

  • Douchiche O, Chaibi W, Morvan C (2012) Cadmium tolerance and accumulation characteristics of mature flax, cv. Hermes: Contribution of the basal stem compared to the root. J Hazard Mater 235–236:101–107

    Article  Google Scholar 

  • Dushenkov S, Skarzhinskaya M, Glimelius K, Gleba D, Raskin I (2002) Bioengineering of a phytoremediation plant by means of somatic hybridization. Int J Phytoremed 4:117–126

    Article  CAS  Google Scholar 

  • Gorinova N, Nedkovska M, Todorovska E, Simova-Stoilova L, Stoyanova Z, Georgieva K, Demirevska-Kepova K, Atanassov A, Herzig R (2007) Improved phytoaccumulation of cadmium by genetically modified tobacco plants (Nicotiana tabacum L.). Physiological and biochemical response of the transformants to cadmium toxicity. Environ Pollut 145:161–170

    Article  CAS  Google Scholar 

  • Grant CA, Clarke JM, Duguid S, Chaney RL (2008) Selection and breeding of plant cultivars to minimize cadmium accumulation. Sci Total Environ 2–3:301–310

    Article  Google Scholar 

  • Grispen VMJ, Hakvoort HWJ, Bliek T, Verkleij JAC, Schat H (2011) Combined expression of the Arabidopsis metallothionein MT2b and the heavy metal transporting ATPase HMA4 enhances cadmium tolerance and the root to shoot translocation of cadmium and zinc in tobacco. Environ Exp Bot 72:71–76

    Article  CAS  Google Scholar 

  • Hertstein U, Jager HJ (1986) Tolerances of different populations of three grass species to cadmium and other metals. Environ Exp Bot 26:309–319

    Article  CAS  Google Scholar 

  • Kang XW, Wei ZZ (1986) Cross breeding of tobacco. Shanxi Science and Education Publishing House, Taiyuan, pp 118–120 (in Chinese)

    Google Scholar 

  • Khoudi H, Maatar Y, Gouiaa S, Masmoudi K (2012) Transgenic tobacco plants expressing ectopically wheat H+-pyrophosphatase (H+-PPase) gene TaVP1 show enhanced accumulation and tolerance to cadmium. J Plant Physiol 169:98–103

    Article  CAS  Google Scholar 

  • Kim KH, Lee YH, Kim D, Park YH, Lee JY, Hwang YS, Kim YH (2004) Agrobacterium-mediated genetic transformation of Perilla frutescens. Plant Cell Rep 6:386–390

    Article  Google Scholar 

  • Kramer U (2005) Phytoremediation: novel approaches to clearing up polluted soils. Curr Opin Biotechnol 16:133–141

    Article  Google Scholar 

  • Krystofova O, Zitka O, Krizkova S, Hynek D, Shestivska V, Adam V, Hubalek J, Mackova M, Macek T, Zehnalek J, Babula P, Havel L, Kizek R (2012) Accumulation of cadmium by transgenic tobacco plants (Nicotiana tabacum L.) carrying yeast metallothionein gene revealed by electrochemistry. Int J Electrochem Sci 8:886–907

    Google Scholar 

  • Kusano M, Fukushima A, Arita M, Jonsson P, Moritz T, Kobayashi M, Hayashi N, Tohge T, Saito K (2007) Unbiased characterization of genotype-dependent metabolic regulations by metabolomic approach in Arabidopsis thaliana. BMC Syst Biol 1:53–69

    Article  Google Scholar 

  • Lewis RS, Nicholson JS (2007) Aspects of the evolution of Nicotiana tabacum L. and the status of the United States Nicotiana germplasm collection. Genet Resour Crop Ev 54:727–740

    Article  Google Scholar 

  • Li HF, Fan WH, Wang XD, Xue XG (2006a) The survey and analysis of copper contents in two species plants growing on the copper mining spoils. J Shanxi Agric Univ 4:391–392 (in Chinese)

    Google Scholar 

  • Li JC, Guo JB, Xu WZ, Ma M (2006b) Enhanced cadmium accumulation in transgenic tobacco expressing the phytochelatin synthase gene of Cynodon dactylon L. J Integr Plant Biol 8:928–937

    Article  Google Scholar 

  • Liu JG, Zhu QS, Zhang ZJ, Xu JK, Yang JC, Wong MH (2005) Variations in cadmium accumulation among rice cultivars and types and the selection of cultivars for reducing cadmium in the diet. J Sci Food Agric 85:147–153

    Article  CAS  Google Scholar 

  • Liu X, Zhang SR, Zhu R, Xu XX, Fan XW (2009) Effect of cadmium and copper stress on the growth response and accumulation characteristics of Perilla frutescens (L.) Britt. J Agro-Environ Sci 11:2264–2269 (in Chinese)

    Google Scholar 

  • Liu L, Li YF, Tang JJ, Hu LL, Chen X (2011) Plant coexistence can enhance phytoextraction of cadmium by tobacco (Nicotiana tabacum L.) in contaminated soil. J Environ Sci 3:453–460

    Article  Google Scholar 

  • Macnair MR, Bert V, Huitson SB, Saumitou-Laprade P, Petit D (1999) Zn tolerance and hyperaccumulation are genetically independent characters. Proc Royal Soc Biol Sci B 266:2175–2179

    Article  CAS  Google Scholar 

  • Majdi S, Barzegar M, Jabbari A, AghaAlikhani M (2012) Supercritical fluid extraction of tobacco seed oil and its comparison with solvent extraction methods. J Agr Sci Tech 5:1053–1065

    Google Scholar 

  • Marmiroli M, Pietrini F, Maestri E, Zacchini M, Marmiroli N, Massacci A (2011) Growth, physiological and molecular traits in Salicaceae trees investigated for phytoremediation of heavy metals and organics. Tree Physiol 12:1319–1334

    Article  Google Scholar 

  • Moon H, Nicholson JS (2007) AFLP and SCAR markers linked to tomato spotted wilt virus resistance in tobacco. Crop Sci 47:1887–1894

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nitta M, Lee JK, Kang CW, Katsuta M, Yasumoto S, Liu DJ, Nagamine T, Ohnishi O (2005) The distribution of Perilla species. Genet Resour Crop Ev 52:797–804

    Article  Google Scholar 

  • Nitta M, Kobayashi H, Ohnishi-Kameyama M, Nagamine T, Yoshida M (2006) Essential oil variation of cultivated and wild Perilla analyzed by GC/MS. Biochem Syst Ecol 1:25–37

    Article  Google Scholar 

  • Nouri J, Lorestani B, Yousefi N, Khorasani N, Hasani AH, Seif F, Cheraghi M (2011) Phytoremediation potential of native plants grown in the vicinity of Ahangaran lead–zinc mine (Hamedan, Iran). Environ Earth Sci 62:639–644

    Article  CAS  Google Scholar 

  • Oh K, Li T, Cheng HY, He XY, Yonemochi S (2013) Study on tolerance and accumulation potential of biofuel crops for phytoremediation of heavy metals. Int J Environ Sci Develop 2:152–156

    Article  Google Scholar 

  • Ohara K, Ujihara T, Endo T, Sato F, Yazaki K (2003) Limonene production in tobacco with Perilla limonene synthase cDNA. J Exp Bot 393:2635–2642

    Article  Google Scholar 

  • Richau KH, Schat H (2009) Intraspecific variation of nickel and zinc accumulation and tolerance in the hyperaccumulator Thlaspi caerulescens. Plant Soil 314:253–262

    Article  CAS  Google Scholar 

  • Ruiz JM, Blasco B, Rivero RM, Romero L (2005) Nicotine-free and salt-tolerant tobacco plants obtained by grafting to salinity-resistant rootstocks of tomato. Physiol Plant 124:465–475

    Article  CAS  Google Scholar 

  • Sa KJ, Kim JA, Lee JK (2012) Comparison of seed characteristics between the cultivated and the weedy types of Perilla species. Hort Environ Biotechnol 4:310–315

    Article  Google Scholar 

  • Schat H, Llugany M, Bernhard R (1999) Metal-specific patterns of tolerance, uptake and transport of heavy metals in hyperaccumulating and non-hyperaccumulating metallophytes. In: Terry N, Bañuelos G (eds) Phytoremediation of contaminated soils and water. CRC Press LLC, Boca Raton, FL, USA, pp 171–188

    Google Scholar 

  • Shah K, Nongkynrih JM (2007) Metal hyperaccumulation and bioremediation. Biol Plantarum 4:618–634

    Article  Google Scholar 

  • Taylor J, King RD, Altmann T, Fiehn O (2002) Application of metabolomics to plant genotype discrimination using statistics and machine learning. Bioinformatics Suppl 2:241–248

    Article  Google Scholar 

  • Wang P, Liang Z, Zeng J, Li W, Sun X, Miao Z, Tang K (2008) Generation of tobacco lines with widely different reduction in nicotine levels via RNA silencing approaches. J Biosci 2:177–184

    Article  Google Scholar 

  • Wang FY, Shi ZY, Xu XF, Wang XG, Li YJ (2013) Contribution of AM inoculation and cattle manure to lead and cadmium phytoremediation by tobacco plants. Environ Sci: Processes Impacts 15:794–801

    CAS  Google Scholar 

  • Wawrzynski A, Kopera E, Wawrzynska A, Kaminska J, Bal W, Sirko A (2006) Effects of simultaneous expression of heterologous genes involved in phytochelatin biosynthesis on thiol content and cadmium accumulation in tobacco plants. J Exp Bot 10:2173–2182

    Article  Google Scholar 

  • Wei ZZ (1993) Study on the variation of the number of chromosome and character of the hybrid of tobacco and medical plant. J Shanxi Agric Univ 13:195–198 (in Chinese)

    Google Scholar 

  • Wei ZZ, Wei KQ (2008) Distant hybridization breeding of tobacco. China Agricultural Science and Technology Press, Bei**g, pp 99–105 (in Chinese)

    Google Scholar 

  • Wei ZZ, Yan XP, Deng ZF, Yang JX, Wang YT (2005) Research on distance hybridization between tobacco and stramonium. Chinese Tobacco Science 26:1–5 (in Chinese)

    Google Scholar 

  • Wei KQ, Yang JX, Wei ZZ (2008a) The primary research of chemical components and medicine ingredients from new-type tobacco. Nat Prod Res Dev 20:652–656 (in Chinese)

    CAS  Google Scholar 

  • Wei SH, Teixeira da Silva JA, Zhou QX (2008b) Agro-improving method of phytoextracting heavy metal contaminated soil. J Hazard Mater 150:662–668

    Article  CAS  Google Scholar 

  • Wei KQ, Yang JX, Wei ZZ (2010) Chemical components and medicine ingredients in the hybrid of families between tobacco and medicinal plant Perilla frutescens (L.) Britt. Nat Prod Res Dev 22:801–806 (in Chinese)

    CAS  Google Scholar 

  • Wei KQ, Yang JX, Wei ZZ (2013) Pollination following grafting introduces efficiently Ocimum basilicum L. genes into Nicotiana tabacum L. Span J Agric Res 4:1068–1077

    Article  Google Scholar 

  • **e HL, Chen AP, Zhang FY, **ong Y, Chen YL, Liu J, Zhou LY, Lin RY (2011) Physiological response of Perilla frutescens (L.) Britt. to cadmium. Chin J Eco-Agr 3:672–675 (in Chinese)

    Article  Google Scholar 

  • Yang X, Feng Y, He Z, Stoffella PJ (2005) Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation. J Trace Elem Med Biol 4:339–353

    Article  Google Scholar 

  • Yasinok AE, Sahin FI, Eyidogan F, Kuru M, Haberal M (2009) Grafting tomato plant on tobacco plant and its effect on tomato plant yield and nicotine content. J Sci Food Agric 89:1122–1128

    Article  CAS  Google Scholar 

  • Zhang QH, Yang FJ, Li BX, Zhou GZ (2007) Analysis and evaluation of heavy metals in the soil and plant system in some mining area of southwest China. J Shandong Univ Sci Technol 3:15–18 (in Chinese)

    Google Scholar 

  • Zhang HY, Liu XZ, He CS, Yang YM (2008a) Genetic diversity among flue-cured tobacco cultivars based on RAPD and AFLP markers. Braz Arch Biol Technol 51:1097–1101

    Article  CAS  Google Scholar 

  • Zhang ZJ, Wang YM, Long LK (2008b) Tomato rootstock effects on gene expression patterns in eggplant scions. Russ J Plant Physiol 55:93–100

    Article  CAS  Google Scholar 

  • Zhang X, Wu W, Zheng YL, Chen L, Cai QR (2009) Essential oil variations in different Perilla L. accessions: chemotaxonomic implications. Plant Syst Evol 281:1–10

    Article  CAS  Google Scholar 

  • Zhao XL, Li YE (2007) Variation of cadmium tolerance and accumulation in different tobacco cultivars. J Southwest Univ (Nat Sci Edit) 2:110–114 (in Chinese)

    Google Scholar 

Download references

Acknowledgments

This work was the Research Project Supported by Shanxi Scholarship Council of China and the Shanxi Provincial Key Technologies Research and Development Program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Keqiang Wei.

Additional information

Responsible editor: Elena Maestri

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 2583 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wei, K., Pang, S., Yang, J. et al. Enhancement of cadmium tolerance and accumulation by introducing Perilla frutescens (L.) Britt var. frutescens genes in Nicotiana tabacum L. plants. Environ Sci Pollut Res 22, 5405–5416 (2015). https://doi.org/10.1007/s11356-014-4048-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-4048-4

Keywords

Navigation