Skip to main content

Advertisement

Log in

Overexpression of the Tamarix hispida ThMT3 gene increases copper tolerance and adventitious root induction in Salix matsudana Koidz.

  • Original Paper
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

In this work, transgenic Salix matsudana expressing the Tamarix hispida ThMT3 gene, which encodes encoding a type 3 metallothionein, showed increased tolerance to copper (Cu) stress. Exposure to 50 μM Cu completely inhibited rooting of wild-type (WT) plants, but induced numerous adventitious roots in the transgenic plants. The nitric oxide (NO) content in the transgenic plants was higher than that in WT plants. The application of an NO inhibitor, 2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide, decreased superoxide dismutase, catalase and ascorbate peroxidase activities under Cu stress. Auxin application-related genes that are known to improve adventitious roots, such as Auxin response factor 8, auxin resistant 1 and pinformed, were highly expressed in transgenic plants under Cu and sodium nitroprusside treatments. These results suggested that the expression of the ThMT3 gene increased Cu tolerance and NO production, and the higher NO release contributed to the induction of adventitious roots under Cu stress.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /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 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
Fig. 9

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Adamis PDB, Panek AD, Leite SGF, Eleutherio ECA (2003) Factors involved with cadmium absorption by a wild-type strain of Saccharomyces cerevisiae. Braz J Mirobiol 34:55–60

    CAS  Google Scholar 

  • An Z, Li C, Zu Y, Du Y, Wachter A, Gromes R, Rausch T (2006) Expression of BjMT2, a metallothionein 2 from Brassica juncea, increases copper and cadmium tolerance in Escherichia coli and Arabidopsis thaliana, but inhibits root elongation in Arabidopsis thaliana seedlings. J Exp Bot 57:3575–3582

    Article  CAS  Google Scholar 

  • Bellion M, Courbot M, Jacob C, Guinet F, Blaudez D, Chalot M (2007) Metal induction of a Paxillus involutus metallothionein and its heterologous expression in Hebeloma cylindrosporum. New Phytol 174:151–158

    Article  CAS  PubMed  Google Scholar 

  • Benatt MR, Yookongkaew N, Meetam M, Guo WJ, Punyasuk N, AbuQamar S, Goldsbrough P (2014) Metallothionein deficiency impacts copper accumulation and redistribution in leaves and seeds of Arabidopsis. New Phytol 202:940–951

    Article  Google Scholar 

  • Cai F, Mei L, An X, Gao S, Tang L, Chen F (2011) Lipid peroxidation and antioxidant responses during seed germination of Jatropha curcas. Int J Agric Biol 13:25–30

    CAS  Google Scholar 

  • Chen PY, Wang CK, Soong SC, To KY (2003) Complete sequence of the binary vector pBI121 and its application in cloning T-DNA insertion from transgenic plants. Mol Breed 11:287–293

    Article  CAS  Google Scholar 

  • Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    Article  CAS  PubMed  Google Scholar 

  • Dos Santos Utmazian MN, Wieshammer G, Vega R, Wenzel WW (2007) Hydroponic screening for metal resistance and accumulation of cadmium and zinc in twenty clones of willows and poplars. Environ Pollut 148:155–165

    Article  PubMed  Google Scholar 

  • Dowling DN, Doty SL (2009) Improving phytoremediation through biotechnology. Curr Opin Biotechnol 20:204–206

    Article  CAS  PubMed  Google Scholar 

  • Freeman JL, Tamaoki M, Stushnoff C, Quinn CF, Cappa JJ, Devonshire J, Fakra SC, Marcus MA, McGrath SP, Van Hoewyk D, Pilon-Smits EA (2010) Molecular mechanisms of selenium tolerance and hyperaccumulation in Stanleya pinnata. Plant Physiol 153:1630–1652

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Geldner N, Frim J, Stierhof YD, Juergens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428

    Article  CAS  PubMed  Google Scholar 

  • Groppa MD, Rosales EP, Lannone MF, Benavides MP (2008) Nitric oxide, polyamines and Cd-induced phytotoxicity in wheat roots. Phytochemistry 69:2609–2615

    Article  CAS  PubMed  Google Scholar 

  • Guo Z, Ou W, Lu S, Zhong Q (2006) Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol Biochem 44:828–836

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez L, Bussell JD, Pacurar DI, Schwambach J, Pacurar M, Bellini C (2009) Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell 21:3119–3132

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hung KT, Chang CJ, Kao CH (2002) Paraquat toxicity is reduced by nitric oxide in rice leaves. J Plant Physiol 159:159–166

    Article  CAS  Google Scholar 

  • Jaakola L, Pirttilä AM, Halonen M, Hohtola A (2001) Isolation of high quality RNA from bilberry (Vaccinium myrtillus L.) fruit. Mol Biotechnol 19:201–213

    Article  CAS  PubMed  Google Scholar 

  • Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330

    Article  CAS  Google Scholar 

  • Lee J, Shim D, Song WY, Hwang I, Lee Y (2004) Arabidopsis metallothioneins 2a and 3 enhance resistance to cadmium when expressed in Vicia faba guard cells. Plant Mol Biol 54:805–815

    Article  CAS  PubMed  Google Scholar 

  • Lei YB, Korpelainen H, Li CY (2007) Physiological and biochemical responses to high Mn concentrations in two contrasting Populus cathayana populations. Chemosphere 68:686–694

    Article  CAS  PubMed  Google Scholar 

  • Lewis DR, Negi S, Sukumar P, Muday GK (2011) Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. Development 138:3485–3495

    Article  CAS  PubMed  Google Scholar 

  • Malamy JE (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant, Cell Environ 28:67–77

    Article  CAS  Google Scholar 

  • Marchant A, Bhalerao R, Casimiro I, Eklöf J, Casero PJ, Bennett M, Sandberg G (2002) AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. Plant Cell 14:589–597

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Muday GK, Murphy AS (2002) An emerging model of auxin transport regulation. Plant Cell 14:293–299

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plantarum 15:495–497

    Article  Google Scholar 

  • Shi SY, Wang G, Wang YD, Zhang LG, Zhang LX (2005) Protective effect of nitric oxide against oxidative stress under ultraviolet-B radiation. Nitric Oxide 13:1–9

    Article  CAS  PubMed  Google Scholar 

  • Singh HP, Kaur S, Batish DR, Sharma VP, Sharma N, Kohli RK (2009) Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the roots of Oryza sativa (rice). Nitric Oxide 20:289–297

    Article  CAS  PubMed  Google Scholar 

  • Sridhar BBM, Diehl SV, Han FX, Monts DL, Su Y (2005) Anatomical changes due to uptake and accumulation of Zn and Cd in Indian mustard (Brassica juncea). Environ Exp Bot 54:131–141

    Article  Google Scholar 

  • Sukumar P, Maloney GS, Muday GK (2013) Localized induction of the ATP-Binding cassette B19 auxin transporter enhances adventitious root formation in Arabidopsis. Plant Physiol 162:1392–1405

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Swarup K, Benková E, Swarup R, Casimiro I, Péret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, Levesque MP, Carrier D, James N, Calvo V, Ljung K, Kramer E, Roberts R, Graham N, Marillonnet S, Patel K, Jones JD, Taylor CG, Schachtman DP, May S, Sandberg G, Benfey P, Friml J, Kerr I, Beeckman T, Laplaze L, Bennett MJ (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10:946–954

    Article  CAS  PubMed  Google Scholar 

  • Wang LN, Yang LM, Yang FJ, Li XG, Song YP (2010) Involvements of H2O2 and metallothionein in NO-mediated tomato tolerance to copper toxicity. J Plant Physiol 167:1298–1306

    Article  CAS  PubMed  Google Scholar 

  • Wilmoth JC, Wang S, Tiwari SB, Joshi AD, Hagen G, Guilfoyle TJ, Alonso JM, Ecker JR, Reed JW (2005) NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J 43:118–130

    Article  CAS  PubMed  Google Scholar 

  • Xiong J, Lu H, Lu K, Duan Y, An L, Zhu C (2009) Cadmium decreases crown root number by decreasing endogenous nitric oxide, which is indispensable for crown root primordia initiation in rice seedlings. Planta 230:599–610

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Yin H, Li Y, Liu X (2010) Nitric oxide is associated with long-term zinc tolerance in Solanum nigrum. Plant Physiol 154:1319–1334

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang JL, Wang YC, Liu GF, Yang CP, Li CH (2011) Tamarix hispida metallothionein-like ThMT3, a reactive oxygen species scavenger, increases tolerance against Cd2+, Zn2+, Cu2+, and NaCl in transgenic yeast. Mol Biol Rep 38:1567–1574

    Article  CAS  PubMed  Google Scholar 

  • Yang JL, Yi JS, Yang CP, Li CH (2013) Agrobacterium tumefaciens-mediated genetic transformation of Salix matsudana Koidz. using mature seeds. Tree Physiol 33:628–639

    Article  PubMed  Google Scholar 

  • Yu CC, Hung KT, Kao CH (2005) Nitric oxide reduces Cu toxicity and Cu-induced NH4+ accumulation in rice leaves. J Plant Physiol 162:1319–1330

    Article  CAS  PubMed  Google Scholar 

  • Zazímalová E, Murphy AS, Yang HB, Hoyerová K, Hosek P (2010) Auxin transporters–why so many? CSH Perspect Biol 2:a001552

    Google Scholar 

  • Zhang F, Wang Y, Yang Y, Wu H, Wang D, Liu J (2007) Involvement of hydrogen peroxide and nitric oxide in salt resistance in the calluses from Populus euphratica. Plant, Cell Environ 30:775–785

    Article  Google Scholar 

  • Zhang Y, Tan J, Guo Z, Lu S, He S, Shu W, Zhou B (2009) Increased abscisic acid levels in transgenic tobacco over-expressing 9 cis-epoxycarotenoid dioxygenase influence H2O2 and NO production and antioxidant defences. Plant, Cell Environ 32:509–519

    Article  Google Scholar 

  • Zhou B, Guo Z, Xing J, Huang B (2005) Nitric oxide is involved in abscisic acid-induced antioxidant activities in Stylosanthes guianensis. J Exp Bot 56:3223–3228

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the the Innovation Project of State Key Laboratory of Tree Genetics and Breeding (Northeast Forestry University) (2014B02), National High Technology Research and Development Program of China (863 Program, 2013AA102704), the Fundamental Research Funds for the Central Universities (DL11EA02), and China Postdoctoral Science Foundation (2014M560242).

Conflict of Interest

The authors declare no competing financial interests.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Chuanping Yang or Chenghao Li.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, J., Chen, Z., Wu, S. et al. Overexpression of the Tamarix hispida ThMT3 gene increases copper tolerance and adventitious root induction in Salix matsudana Koidz.. Plant Cell Tiss Organ Cult 121, 469–479 (2015). https://doi.org/10.1007/s11240-015-0717-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-015-0717-3

Keywords