Advertisement

Molecular Breeding

, 39:49 | Cite as

Root-specific expression of rice OsHMA3 reduces shoot cadmium accumulation in transgenic tobacco

  • Hailin Cai
  • Pengfei Xie
  • Weiai Zeng
  • Zhengguang Zhai
  • Wen Zhou
  • Zhong TangEmail author
Article
  • 42 Downloads

Abstract

Cadmium (Cd) is a toxic trace element released into the environment by anthropogenic activities. Its release threatens the growth of plants and contaminates the food chain. Tobacco (Nicotiana tabacum L.) is a Cd accumulator, and tobacco smoking is a major source of Cd exposure for smoking people. In the present study, we generated transgenic tobacco plants expressing the rice heavy metal P-type ATPase 3 gene (OsHMA3) in the roots under the control of a novel root-specific promoter from a tobacco root extensin-like protein-coding gene (NtREL1). Transgenic plants showed significantly reduced Cd accumulation in the shoots in both hydroponic and soil pot experiments. Analysis of Cd concentration in xylem sap showed that the transgenic plants had significantly decreased root-to-shoot translocation of Cd relative to that of wild-type plants. Moreover, a significantly lower oxidative stress level under Cd stress was observed in the shoots of transgenic plants than in wild-type shoots. These results suggest that OsHMA3 can be expressed in tobacco plants and may be useful for developing tobacco varieties with a reduced capacity to accumulate Cd in the shoots, potentially reducing the risk of Cd exposure for smoking people.

Keywords

Cadmium OsHMA3 Root-specific expression Tobacco Heavy metals 

Notes

Funding information

The study was funded by the Science Research Project of Hunan Tobacco Company (No. CYKJ2014-03) and the Fundamental Research Funds for the Central Universities (KYZ201873).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11032_2019_964_Fig7_ESM.png (45 kb)
Supplementary Figure 1

(PNG 44 kb)

11032_2019_964_MOESM1_ESM.tif (126 kb)
High resolution image (TIF 125 kb)
11032_2019_964_MOESM2_ESM.docx (22 kb)
ESM 1 (DOCX 22 kb)

References

  1. Ahmadi H, Corso M, Weber M, Verbruggen N, Clemens S (2018) CAX1 suppresses Cd-induced generation of reactive oxygen species in Arabidopsis halleri. Plant Cell Environ 41:2435–2448CrossRefGoogle Scholar
  2. Chang S, Shu H (2015) The inhibition analysis of two heavy metal ATPase genes (NtHMA3a and NtHMA3b) in Nicotiana tabacum. Biorem J 19:113–123CrossRefGoogle Scholar
  3. Chao DY, Silva A, Baxter I, Huang YS, Nordborg M, Danku J, Lahner B, Yakubova E, Salt DE (2012) Genome-wide association studies identify heavy metal Atpase3 as the primary determinant of natural variation in leaf cadmium in Arabidopsis thaliana. PLoS Genet 8:e1002923 CrossRefGoogle Scholar
  4. Clemens S, Aarts MGM, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18:92–99CrossRefGoogle Scholar
  5. Clemens S, Palmgren MG, Kramer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315CrossRefGoogle Scholar
  6. Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Lannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46CrossRefGoogle Scholar
  7. Gallois P, Marinho P (1995) Leaf disk transformation using Agrobacterium tumefaciens-expression of heterologous genes in tobacco. Methods Mol Biol (Clifton, NJ) 49:39–48Google Scholar
  8. Geiss O, Kotzias D (2007) Tobacco, cigarettes and cigarette smoke an overview. Institute for Health and Consumer Protection, European CommissionGoogle Scholar
  9. Grant CA, Clarke JM, Duguid S, Chaney RL (2008) Selection and breeding of plant cultivars to minimize cadmium accumulation. Sci Total Environ 390:301–310CrossRefGoogle Scholar
  10. Han Y, Sa G, Sun J, Shen Z, Zhao R, Ding M, Deng S, Lu Y, Zhang Y, Shen X, Chen S (2014) Overexpression of Populus euphratica xyloglucan endotransglucosylase/hydrolase gene confers enhanced cadmium tolerance by the restriction of root cadmium uptake in transgenic tobacco. Environ Exp Bot 100:74–83CrossRefGoogle Scholar
  11. He J, Qin J, Long L, Ma Y, Li H, Li K, Jiang X, Liu T, Polle A, Liang Z, Luo Z-B (2011) Net cadmium flux and accumulation reveal tissue-specific oxidative stress and detoxification in Populus x canescens. Physiol Plant 143:50–63CrossRefGoogle Scholar
  12. Hermand V, Julio E, de Borne FD, Punshon T, Ricachenevsky FK, Bellec A, Gosti F, Berthomieu P (2014) Inactivation of two newly identified tobacco heavy metal ATPases leads to reduced Zn and Cd accumulation in shoots and reduced pollen germination. Metallomics 6:1427–1440CrossRefGoogle Scholar
  13. Jana S, Choudhuri MA (1982) Glycolate metabolism of three submersed aquatic angiosperms during ageing. Aquat Bot 12:345–354CrossRefGoogle Scholar
  14. Jarup L, Akesson A (2009) Current status of cadmium as an environmental health problem. Toxicol Appl Pharmacol 238:201–208CrossRefGoogle Scholar
  15. Korenkov V, King B, Hirschi K, Wagner GJ (2009) Root-selective expression of AtCAX4 and AtCAX2 results in reduced lamina cadmium in field-grown Nicotiana tabacum L. Plant Biotechnol J 7:219–226CrossRefGoogle Scholar
  16. Liedschulte V, Laparra H, Battey JND, Schwaar JD, Broye H, Mark R, Klein M, Goepfert S, Bovet L (2017) Impairing both HMA4 homeologs is required for cadmium reduction in tobacco. Plant Cell Environ 40:364–377CrossRefGoogle Scholar
  17. Liu L, Li Y, Tang J, Hu L, Chen X (2011) Plant coexistence can enhance phytoextraction of cadmium by tobacco (Nicotiana tabacum L.) in contaminated soil. J Environ Sci 23:453–460CrossRefGoogle Scholar
  18. Lugon-Moulin N, Martin F, Krauss MR, Ramey PB, Rossi L (2006) Cadmium concentration in tobacco (Nicotiana tabacum L.) from different countries and its relationship with other elements. Chemosphere 63:1074–1086CrossRefGoogle Scholar
  19. Lugon-Moulin N, Zhang M, Gadani F, Rossi L, Koller D, Krauss M, Wagner GJ (2004) Critical review of the science and options for reducing cadmium in tobacco (Nicotiana tabacum L.) and other plants. In: Advances in agronomy, vol 83, pp 111–180Google Scholar
  20. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410CrossRefGoogle Scholar
  21. Miyadate H, Adachi S, Hiraizumi A, Tezuka K, Nakazawa N, Kawamoto T, Katou K, Kodama I, Sakurai K, Takahashi H, Satoh-Nagasawa N, Watanabe A, Fujimura T, Akagi H (2011) OsHMA3, a P-1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol 189:190–199CrossRefGoogle Scholar
  22. Morel M, Crouzet J, Gravot A, Auroy P, Leonhardt N, Vavasseur A, Richaud P (2009) AtHMA3, a P-1B-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol 149:894–904CrossRefGoogle Scholar
  23. Nesler A, DalCorso G, Fasani E, Manara A, Di Sansebastiano GP, Argese E, Furini A (2017) Functional components of the bacterial CzcCBA efflux system reduce cadmium uptake and accumulation in transgenic tobacco plants. New Biotechnol 35:54–61CrossRefGoogle Scholar
  24. Sasaki A, Yamaji N, Ma JF (2014) Overexpression of OsHMA3 enhances Cd tolerance and expression of Zn transporter genes in rice. J Exp Bot 65:6013–6021CrossRefGoogle Scholar
  25. Shah K, Kumar RG, Verma S, Dubey RS (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 161:1135–1144CrossRefGoogle Scholar
  26. Shao JF, Xia J, Yamaji N, Shen RF, Ma JF (2018) Effective reduction of cadmium accumulation in rice grain by expressing OsHMA3 under the control of the OsHMA2 promoter. J Exp Bot 69:2743–2752CrossRefGoogle Scholar
  27. Siemianowski O, Barabasz A, Kendziorek M, Ruszczynska A, Bulska E, Williams LE, Antosiewicz DM (2014) HMA4 expression in tobacco reduces Cd accumulation due to the induction of the apoplastic barrier. J Exp Bot 65:1125–1139CrossRefGoogle Scholar
  28. Smeets K, Opdenakker K, Remans T, Van Sanden S, Van Belleghem F, Semane B, Horemans N, Guisez Y, Vangronsveld J, Cuypers A (2009) Oxidative stress-related responses at transcriptional and enzymatic levels after exposure to Cd or Cu in a multipollution context. J Plant Physiol 166:1982–1992CrossRefGoogle Scholar
  29. Tamas L, Mistrik I, Zelinova V (2017) Heavy metal-induced reactive oxygen species and cell death in barley root tip. Environ Exp Bot 140:34–40CrossRefGoogle Scholar
  30. Tsadilas CD, Karaivazoglou NA, Tsotsolis NC, Stamatiadis S, Samaras V (2005) Cadmium uptake by tobacco as affected by liming, N form, and year of cultivation. Environ Pollut 134:239–246CrossRefGoogle Scholar
  31. Ueno D, Yamaji N, Kono I, Huang CF, Ando T, Yano M, Ma JF (2010) Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci U S A 107:16500–16505CrossRefGoogle Scholar
  32. Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, Ishikawa S (2009) Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J Exp Bot 60:2677–2688CrossRefGoogle Scholar
  33. Verma S, Yadav S, Singh I (2010) Trace metal concentration in different Indian tobacco products and related health implications. Food Chem Toxicol 48:2291–2297CrossRefGoogle Scholar
  34. Wagner GJ (1993) Accumulation of cadmium in crop plants and its consequences to human health. Adv Agron 51(51):173–212CrossRefGoogle Scholar
  35. Willers S, Gerhardsson L, Lundh T (2005) Environmental tobacco smoke (ETS) exposure in children with asthma-relation between lead and cadmium, and cotinine concentrations in urine. Respir Med 99:1521–1527CrossRefGoogle Scholar
  36. Williams LE, Mills RF (2005) P-1B-ATPases—an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci 10:491–502CrossRefGoogle Scholar
  37. Yan J, Wang P, Wang P, Yang M, Lian X, Tang Z, Huang C-F, Salt DE, Zhao FJ (2016) A loss-of-function allele of OsHMA3 associated with high cadmium accumulation in shoots and grain of Japonica rice cultivars. Plant Cell Environ 39:1941–1954CrossRefGoogle Scholar
  38. Zhang C, Pan S, Chen H, Cai T, Zhuang C, Deng Y, Zhuang Y, Zeng Y, Chen S, Zhuang W (2016a) Characterization of NtREL1, a novel root-specific gene from tobacco, and upstream promoter activity analysis in homologous and heterologous hosts. Plant Cell Rep 35:757–769CrossRefGoogle Scholar
  39. Zhang J, Zhang M, Shohag MJI, Tian S, Song H, Feng Y, Yang X (2016b) Enhanced expression of SaHMA3 plays critical roles in Cd hyperaccumulation and hypertolerance in Cd hyperaccumulator Sedum alfredii Hance. Planta 243:577–589CrossRefGoogle Scholar
  40. Zhao F-J, Ma Y, Zhu Y-G, Tang Z, McGrath SP (2015) Soil contamination in China: current status and mitigation strategies. Environ Sci Technol 49:750–759CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Tobacco Production Technology CenterChangsha Branch of Hunan Tobacco CompanyChangshaChina
  2. 2.State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental SciencesNanjing Agricultural UniversityNanjingChina

Personalised recommendations