Skip to main content
Log in

Enhanced cold stress tolerance of transgenic Dendrocalamus latiflorus Munro (Ma bamboo) plants expressing a bacterial CodA gene

  • Anther Culture/Haploids
  • Published:
In Vitro Cellular & Developmental Biology - Plant Aims and scope Submit manuscript

Abstract

Ma bamboo (Dendrocalamus latiflorus Munro) is a widespread culm and shoot-producing species in southern China. However, low temperatures reduce Ma bamboo shoot production and delay its development. In an attempt to enhance its cold-tolerance, a bacterial CodA gene encoding choline oxidase was introduced into Ma bamboo by Agrobacterium-mediated transformation, an approach that had not been previously utilized in bamboo. PCR and Southern blot analyses confirmed that CodA had integrated into the Ma bamboo genome. RT-PCR results showed that expression of CodA driven by the Arabidopsis Rd29A promoter was induced by cold stress in the transgenic bamboo lines. Following treatment at 4°C for 24 h, the content of glycine betaine (GB) increased to 83% and 140% in control plants (wild type (WT)) and CodA transgenic Ma bamboo plants, respectively. Superoxide dismutase, peroxidase, and catalase activities increased in both transgenic and WT plants. However, increases in these enzymes activities were much greater in the transgenic lines than in the WT plants under cold stress. The accumulation of malondialdehyde and electrolyte leakage (REL) in CodA transgenic Ma bamboo plants was less than that in control plants. Collectively, these results suggest that increased cold-tolerance induced by accumulation of GB in vivo was associated with the enhancement of antioxidant enzyme activities, which led to reduced accumulation of reactive oxygen species and stabilization of membrane integrity against extreme temperatures in transgenic plants.

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.

Figure 1.
Figure 2.
Figure 3.
Figure 4.

Similar content being viewed by others

References

  • Aebi H. Catalase in vitro. Methods Enzymol 105: 121–126; 1984.

    Article  CAS  PubMed  Google Scholar 

  • Beck E.; Fettig S.; Knake C.; Hartig K.; Bhattarai T. Specific and unspecific responses of plants to cold and drought stress. J Bioscience 32: 501–510; 2007.

    Article  CAS  Google Scholar 

  • Chen W.; Li P.; Chen T. Glycinebetaine increases chilling tolerance and reduces chilling-induced lipid peroxidation in Zea mays L. Plant Cell Environ 23: 609–618; 2000.

    Article  CAS  Google Scholar 

  • Cheng C.; Yun K.; Ressom H.; Mohanty B.; Bajic V.; Jia Y.; Yun S.; Reyes B. An early response regulatory cluster induced by low temperature and hydrogen peroxide in seedlings of chilling-tolerant japonica rice. BMC Genom 8: 175; 2007.

    Article  Google Scholar 

  • Deshnium P.; Los D.; Hayashi H.; Mustardy L.; Murata N. Transformation of Synechococcus with a gene for choline oxidase enhances tolerance to salt stress. Plant Mol Biol 29: 897–907; 1995.

    Article  CAS  PubMed  Google Scholar 

  • Doyle J. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19: 11–15; 1987.

    Google Scholar 

  • Dubouzet J.; Sakuma Y.; Ito Y.; Kasuga M.; Dubouzet E.; Miura S.; Seki M.; Shinozaki K.; Yamaguchi-Shinozaki K. OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33: 751–763; 2003.

    Article  CAS  PubMed  Google Scholar 

  • Gao Z.; Wang X.; Peng Z.; Zheng B.; Liu Q. Characterization and primary functional analysis of phenylalanine ammonia-lyase gene from Phyllostachys edulis. Plant Cell Rep 31: 1345–1356; 2012.

    Article  CAS  PubMed  Google Scholar 

  • Giannopolitis C.; Ries S. Superoxide dismutases I. Occurrence in higher plants. Plant Physiol 59: 309–314; 1977.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gorham J (1995) Betaines in higher plants-biosynthesis and role in stress metabolism. Seminar series-society for experimental biology. Cambridge University Press, pp 173–173.

  • Grieve C.; Grattan S. Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70: 303–307; 1983.

    Article  CAS  Google Scholar 

  • Hamilton E.; Heckathorn S. Mitochondrial adaptations to NaCl. Complex I is protected by anti-oxidants and small heat shock proteins, whereas complex II is protected by proline and betaine. Plant Physiol 126: 1266–1274; 2001.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hayashi H.; Mustardy L.; Deshnium P.; Ida M.; Murata N. Transformation of Arabidopsis thaliana with the CodA gene for choline oxidase; accumulation of glycinebetaine and enhanced tolerance to salt and cold stress. Plant J 12: 133–142; 1997.

    Article  CAS  PubMed  Google Scholar 

  • Hodges D.; DeLong J.; Forney C.; Prange R. Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207: 604–611; 1999.

    Article  CAS  Google Scholar 

  • Holmström K.; Somersalo S.; Mandal A.; Palva T.; Welin B. Improved tolerance to salinity and low temperature in transgenic tobacco producing glycine betaine. J Exp Bot 51: 177–185; 2000.

    Article  PubMed  Google Scholar 

  • Jiang J.; LI B.; Jiang N.; Zhu W.; Yu Y.; Chen X. Impact of the snow disaster occurred in 2008 in South China to the clump bamboo in South Sichuan. Scientia Silvae Sinicae 44: 141–144; 2008 (In Chinese with English abstract).

    Google Scholar 

  • Kasuga M.; Miura S.; Shinozaki K.; Yamaguchi-Shinozaki K. A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought-and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol 45: 346–350; 2004.

    Article  CAS  PubMed  Google Scholar 

  • Kishitani S.; Watanabe K.; Yasuda S.; Arakawa K.; Takabe T. Accumulation of glycinebetaine during cold acclimation and freezing tolerance in leaves of winter and spring barley plants. Plant Cell Environ 17: 89–95; 1994.

    Article  CAS  Google Scholar 

  • Kondo Y.; Sakamoto A.; Nonaka H.; Hayashi H.; Saradhi P.; Chen T.; Murata N. Enhanced tolerance to light stress of transgenic Arabidopsis plants that express the codA gene for a bacterial choline oxidase. Plant Mol Biol 40: 279–288; 1999.

    Article  PubMed  Google Scholar 

  • Li Z.; Dou H.; Wei D.; Meng Q.; Yang X. codA transgenic tomato plants enhance tolerance to high temperature stress. Acta Agronomica Sinica 39: 2046–2054; 2013 (In Chinese with English abstract).

    CAS  Google Scholar 

  • Lin C.; Liang C.; Hsaio H.; Lin M.; Chang W. In vitro flowering of green and albino Dendrocalamus latiflorus. New Forest 34: 177–186; 2007.

    Article  Google Scholar 

  • Liu J.; Nada K.; Honda C.; Kitashiba H.; Wen X.; Pang X.; Moriguchi T. Polyamine biosynthesis of apple callus under salt stress: importance of the arginine decarboxylase pathway in stress response. J Exp Bot 57: 2589–2599; 2006.

    Article  CAS  PubMed  Google Scholar 

  • Liu M.; Qiao G.; Jiang J.; Yang H.; Xie L.; Xie J.; Zhuo R. Transcriptome sequencing and de novo analysis for ma bamboo (Dendrocalamus latiflorus Munro) using the Illumina platform. PloS One 7: e46766; 2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mahajan S.; Tuteja N. Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444: 139–158; 2005.

    Article  CAS  PubMed  Google Scholar 

  • Park E.; Jeknić Z.; Sakamoto A.; DeNoma J.; Yuwansiri R.; Murata N.; Chen T. Genetic engineering of glycinebetaine synthesis in tomato protects seeds, plants, and flowers from chilling damage. Plant J 40: 474–487; 2004.

    Article  CAS  PubMed  Google Scholar 

  • Pellegrineschi A.; Reynolds M.; Pacheco M.; Brito R.; Almeraya R.; Yamaguchi-Shinozaki K.; Hoisington D. Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 47: 493–500; 2004.

    Article  CAS  PubMed  Google Scholar 

  • Qiao G.; Li H.; Liu M.; Jiang J.; Yin Y.; Zhang L.; Zhuo R. Callus induction and plant regeneration from anthers of Dendrocalamus latiflorus Munro. In Vitro Cell Dev Biol–Plant 49: 375–382; 2013.

    Article  CAS  Google Scholar 

  • Qiu W.; Liu M.; Qiao G.; Jiang J.; Xie L.; Zhuo R. An isopentyl transferase gene driven by the stress-Inducible rd29A promoter improves salinity stress tolerance in transgenic tobacco. Plant Mol Biol Rep 30: 519–528; 2012.

    Article  CAS  Google Scholar 

  • Sakamoto A.; Murata A. Metabolic engineering of rice leading to biosynthesis of glycinebetaine and tolerance to salt and cold. Plant Mol Biol 38: 1011–1019; 1998.

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J.; Russell D. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York; 2001.

    Google Scholar 

  • Thomashow M. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Biol 50: 571–599; 1999.

    Article  CAS  Google Scholar 

  • Xu L.; Ye M. A measurement of peroxidase activity using continuous recording method. J Nanjing Agricult Univ 12: 82–83; 1989 (In Chinese with English abstract).

    Google Scholar 

  • Xu Z.; Ni Z.; Liu L.; Nie L.; Li L.; Chen M.; Ma Y. Characterization of the TaAIDFa gene encoding a CRT/DRE-binding factor responsive to drought, high-salt, and cold stress in wheat. Mol Genet Genomics 280: 497–508; 2008.

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K.; Shinozaki K. Arabidopsis DNA encoding two desiccation-responsive rd29 genes. Plant Physiol 101: 1119; 1993.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Science Technology Department of Zhejiang province (Nos. 2012C22099, 2010C12010, and 2012C12908-3) and the National Natural Science Foundation of China (No. 31200508). The authors declare that no competing interests exist.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Yancheng Jiang or Renying Zhuo.

Additional information

Editor: J. Forster

Guirong Qiao and Huiqing Yang contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Qiao, G., Yang, H., Zhang, L. et al. Enhanced cold stress tolerance of transgenic Dendrocalamus latiflorus Munro (Ma bamboo) plants expressing a bacterial CodA gene. In Vitro Cell.Dev.Biol.-Plant 50, 385–391 (2014). https://doi.org/10.1007/s11627-013-9591-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11627-013-9591-z

Keywords

Navigation