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.
Similar content being viewed by others
References
Aebi H. Catalase in vitro. Methods Enzymol 105: 121–126; 1984.
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.
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.
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.
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.
Doyle J. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19: 11–15; 1987.
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.
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.
Giannopolitis C.; Ries S. Superoxide dismutases I. Occurrence in higher plants. Plant Physiol 59: 309–314; 1977.
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.
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.
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.
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.
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.
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).
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.
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.
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.
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).
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.
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.
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.
Mahajan S.; Tuteja N. Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444: 139–158; 2005.
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.
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.
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.
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.
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.
Sambrook J.; Russell D. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York; 2001.
Thomashow M. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Biol 50: 571–599; 1999.
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).
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.
Yamaguchi-Shinozaki K.; Shinozaki K. Arabidopsis DNA encoding two desiccation-responsive rd29 genes. Plant Physiol 101: 1119; 1993.
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
Corresponding authors
Additional information
Editor: J. Forster
Guirong Qiao and Huiqing Yang contributed equally to this work.
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11627-013-9591-z