Skip to main content
SpringerLink
Log in

Two CBL genes from Populus euphratica confer multiple stress tolerance in transgenic triploid white poplar

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

Abstract

In plants, the calcineurin B-like protein (CBL) family is a unique group of calcium sensors that play a key role in decoding calcium transients by specifically interacting with and regulating a family of CBL-interacting protein kinases. In this study, two CBL genes (PeCBL6 and PeCBL10) from Populus euphratica were isolated by reverse transcription-polymerase chain reaction. To examine their functions, the corresponding cDNAs, which expression was driven by the cauliflower mosaic virus 35S promoter, were cloned into a plant expression vector pCAMBIA1301 and introduced into the triploid white poplar (Popolus tomentosa ‘YiXianCiZhu B385’). The physiological parameters, including the percentage of wilted leaves, height growth rate, chlorophyll content, malondialdehyde (MDA) content and relative electrical conductivity (REC) of transgenic lines and wild type (WT) plants, were measured and compared. The results showed that the MDA content and REC of transgenic plants were significantly lower in transgenic plants compared to WT plants when exposed to cold stress and that the presence of the PeCBL gene can induce an increase in height growth rate and a reduction in the number of wilted leaves in comparison to non-transgenic poplars under high salt, drought and cold stress. These results clearly demonstrate that transgenic plants had a greater tolerance to stresses than non-transgenic seedlings, suggesting that PeCBLs might play an important role in stress tolerance.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

CaMV:

Cauliflower mosaic virus

CBL:

Calcineurin B-like protein

CIPK:

CBL-interacting protein kinases

CPR:

Chlorophenol red

CTAB:

Cetyltriethylammnonium bromide

HPT:

Hygromycin phosphotransferase

MDA:

Malondialdehyde

MS:

Murashige and Skoog

NAA:

1-naphthaleneacetic acid

PMI:

6-phosphomannose isomerase

PFD:

Photon flux density

REC:

Relative electrical conductivity

REL:

Relative leakage

TBA:

Thiobarbituric acid

TDZ:

Thidiazuton

WT:

Wild-type

References

  • Albrecht V, Weinl S, Blazevic D, D’Angelo C, Batistic O, Kolukisaoglu U, Bock R, Schulz B, Harter K, Kudla J (2003) The calcium sensor CBL1 integrates plant responses to abiotic stresses. Plant J 36:457–470

    Article  PubMed  CAS  Google Scholar 

  • Batistič O, Kudla J (2004) Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta 219:915–924

    Google Scholar 

  • Batistič O, Kudla J (2009) Plant calcineurin B-like proteins and their interacting protein kinases. Biochim Biophys Acta 1793:985–992

    Article  PubMed  Google Scholar 

  • Boscariol RL, Almeida WAB, Derbyshire MTVC, Mourao Filho FAA, Mendes BMJ (2003) The use of the PMI/mannose selection system to recover transgenic sweet orange plants (Citrus sinensis L. Osbeck). Plant Cell Rep 22(2):122–128

    Article  PubMed  CAS  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116

    Article  CAS  Google Scholar 

  • Chen TH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257

    Article  PubMed  CAS  Google Scholar 

  • Chen JH, Xia XL, Yin WL (2009) Expression profiling and functional characterization of a DREB2-type gene from Populus euphratic. Biochem Biophys Res Commun 378:483–487

    Article  PubMed  CAS  Google Scholar 

  • Chen JH, Sun Y, Sun F, Xia XL, Yin WL (2011) Tobacco plants ectopically expressing the Ammopiptanthus mongolicus AmCBL1 gene display enhanced tolerance to multiple abiotic stresses. Plant Growth Regul 63:259–269

    Article  CAS  Google Scholar 

  • Cheong YH, Kim KN, Pandey GK, Gupta R, Grant JJ, Luan S (2003) CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell 15:1833–1845

    Article  PubMed  CAS  Google Scholar 

  • Cheong YH, Sung SJ, Kim BG, Pandey GK, Cho JS, Kim KN, Luan S (2010) Constitutive over-express ion of the calcium sensor CBL5 confers osmotic or drought stress tolerance in Arabidopsis. Mol Cells 29:159–165

    Article  PubMed  CAS  Google Scholar 

  • DeBlock M (1990) Factors influencing the tissue culture and the Agrobacterium tumefaciens-mediated transformation of hybrid aspen and poplar clones. Plant Physiol 93:1110–1116

    Article  CAS  Google Scholar 

  • Du NX, Liu X, Li Y, Chen SY, Zhang JS, Ha D, Deng WG, Sun CK, Zhang YZ, Pijut PM (2011) Genetic transformation of Populus tomentosa to improve salt tolerance. Plant Cell Tiss Organ Cult. doi:10.1007/s11240-011-0026-4

  • Duan AA, Zhang SX (1997) Progress in cold and drought-resistant breeding of poplars. J Northwest For Coll 12:94–99

    Google Scholar 

  • Gray GR, Chauvin LP, Sarhan F, Huner NPA (1997) Cold acclimation and freezing tolerance. A complex interaction of light and temperature. Plant Physiol 114:467–474

    PubMed  CAS  Google Scholar 

  • Gua ZM, Ma BJ, Jiang Y, Chen ZW, Su X, Zhang HS (2008) Expression analysis of the calcineurin B-like gene family in rice (Oryza sativa L.) under environmental stresses. Gene 415:1–12

    Article  Google Scholar 

  • Guo XH, Jiang J, Lin SJ, Wang BC, Wang YC, Liu GF, Yang CP (2009) A ThCAP gene from Tamarix hispida confers cold tolerance in transgenic Populus (P. davidiana × P. bolleana). Biotechnol Lett 31:1079–1087

    Article  PubMed  CAS  Google Scholar 

  • Guy CL (1990) Cold acclimation and freezing tolerance: role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 41:187–223

    Article  CAS  Google Scholar 

  • Hasthanasombut S, Supaibulwatana K, Mii M, Nakamura I (2011) Genetic manipulation of Japonica rice using the OsBADH1 gene from Indica rice to improve salinity tolerance. Plant Cell Tiss Organ Cult 104:79–89

    Article  CAS  Google Scholar 

  • He LX, Ban Y, Hiromichi I, Narumi M, Liu JH, Takaya M (2008) Enhancement of spermidine content and antioxidant capacity in transgenic pear shoots overexpressing apple spermidine synthase in response to salinity and hyperosmosis. Phytochemistry 69:2133–2141

    Article  PubMed  CAS  Google Scholar 

  • Jin T, Chang Q, Li W, Yin D, Li Z, Wang D, Liu B, Liu L (2010) Stress-inducible expression of GmDREB1 conferred salt tolerance in transgenic alfalfa. Plant Cell Tiss Organ Cult 100:219–227

    Article  CAS  Google Scholar 

  • Kim BG, Waadt R, Cheong YH, Pandey GK, Dominguez-Solis JR, Schültke S, Lee SC, Kudla J, Luan S (2007) The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J 52:473–484

    Article  PubMed  CAS  Google Scholar 

  • Kolukisaoglu Ü, Weinl S, Blazevic D, Batistic O, Kudla J (2004) Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL-CIPK signaling networks. Plant Physiol 134(1):43–58

    Article  PubMed  CAS  Google Scholar 

  • Lee BT, Matheson NK (1984) Phosphomanno isomerase and phophogluco isomerase in seeds of Cassia coluteoides and some other legumes that synthesize galactomannan. Phytochemistry 23:983–987

    Article  CAS  Google Scholar 

  • Li YL, Su XH, Zhang BY, Huang QJ, Zhang XH, Huang RF (2008) Expression of jasmonic ethylene responsive factor gene in transgenic poplar tree leads to increased salt tolerance. Tree Physiol 29:273–279

    Article  PubMed  CAS  Google Scholar 

  • Li YH, Zhang YZ, Feng FJ, Liang D, Cheng LL, Ma FW, Shi SG (2010) Overexpression of a Malus vacuolar Na+/H+ antiporter gene (MdNHX1) in apple rootstock M.26 and its influence on salt tolerance. Plant Cell Tiss Organ Cult 102:337–345

    Article  CAS  Google Scholar 

  • Luan S (2008) The CBL-CIPK network in plant calcium signaling. Trends Plant Sci 14:37–42

    Article  PubMed  Google Scholar 

  • Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W (2002) Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 14:S389–S400

    PubMed  CAS  Google Scholar 

  • Luan S, Lan W, Lee SC (2009) Potassium nutrition, sodium toxicity, and calcium signaling: connections through the CBL-CIPK network. Curr Opin Plant Biol 12:1–8

    Article  Google Scholar 

  • Massimo C, Gianni A, Alma B, Corrado F, Massimo D (1998) Regeneration of Populus nigra transgenic plants expressing a Kunitz proteinase inhibitor (KTi3) gene. Mol Breed 4:137–145

    Article  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 

  • Orlova IV, Serebriiskaya TS, Popov V, Merkulova N, Nosov AM, Trunova TI, Tsydendambaev VD, Los DA (2003) Transformation of tobacco with a gene for the thermophilic acyl-lipid desaturase enhances the chilling tolerance of plants. Plant Cell Physiol 44:447–450

    Article  PubMed  CAS  Google Scholar 

  • Pandey GK, Cheong YH, Kim KN, Grant JJ, Li L, Hung W, D’Angelo C, Weinl S, Kudla J, Luan S (2004) The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. Plant Cell 16:1912–1924

    Article  PubMed  CAS  Google Scholar 

  • Quan R, Lin H, Mendoza I, Zhang Y, Cao W, Yang Y, Shang M, Chen S, Pardo JM, Guo Y (2007) SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 19:1415–1431

    Article  PubMed  CAS  Google Scholar 

  • Renaut J, Hoffmann L, Hausman JF (2005) Biochemical and physiological mechanisms related to cold acclimation and enhanced freezing tolerance in poplar plantlets. Physiol Planta 125:82–94

    Article  CAS  Google Scholar 

  • Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14:S401–S417

    PubMed  CAS  Google Scholar 

  • Shen LL, Chen Y, Su XH, Zhang SG, Pan HX, Huang MR (2011) Two FT orthologs from Populus simonii Carrière induce early flowering in Arabidopsis and poplar trees. Plant Cell Tiss Organ Cult. doi:10.1007/s11240-011-0048-y

    Google Scholar 

  • Sreenivasulu N, Sopory SK, Kishor PBK (2007) Deciphering the regulatory mechanisms of abiotic stress tolerance in plants by genomic approaches. Gene 388:1–13

    Article  PubMed  CAS  Google Scholar 

  • Thomashow MF (2001) So what’s new in the field of plant cold acclimation? Lots! Plant Physiol 125:89–93

    Article  PubMed  CAS  Google Scholar 

  • Wang JY, Xia XL, Wang JP, Yin WL (2008) Stress responsive zinc-finger protein gene of Populus euphratica in tobacco enhances salt tolerance. J Integr Plant Biol 50(1):56–61

    Article  PubMed  CAS  Google Scholar 

  • Weinl S, Kudla J (2009) The CBL-CIPK Ca2+-decoding signaling network: function and perspectives. New Phytol 184:517–528

    Article  PubMed  CAS  Google Scholar 

  • Xu J, Li HD, Chen LQ, Wang Y, Liu LL, He L, Wu WH (2006) A protein kinase, interacting with two calcineurin Blike proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125:1347–1360

    Article  PubMed  CAS  Google Scholar 

  • Yang CY, Yin WL, Xia XL (2009) Establishment of positive selection system of mannose and application of genetic transformation in Arabidopsis thaliana. Mol Plant Breed 6:1120–1129

    Google Scholar 

  • Zhang F, Yang WC, Wang ZP (2002) Review on transgenic poplar and their application. Shandong For Sci Technol 4:36–38

    Google Scholar 

  • Zhang HC, Yin WL, Xia XL (2008) Calcineurin B-Like family in Populus: comparative genome analysis and expression pattern under cold, drought and salt stress treatment. Plant Growth Regul 56:129–140

    Article  CAS  Google Scholar 

  • Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    Article  PubMed  CAS  Google Scholar 

  • Zhu ZT, Kang XY, Zhang ZY (1998) Studies on selection of natural triploids of Populus tomentosa. Scientia Silvae Sinicae 34(4):22–30

    Google Scholar 

Download references

Acknowledgments

We thank Jiayang Zhang for his helpful comments on the manuscript and technical assistance. This research was supported by the National Natural Science Foundation of China (30730077,30972339,31070597), the Ministry of Science and Technology of China (2009CB119101, 2011BAD38B01), the Beijing city Joint Project (forest quality improvement and postgraduate students training base) and the 111 project (B08005).

Author information

Authors and Affiliations

  1. National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Biotechnology, Beijing Forestry University, No. 35, Tsinghua East Road, Beijing, People’s Republic of China

    Dandan Li, Shuyu Song, Xinli Xia & Weilun Yin

Authors
  1. Dandan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shuyu Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xinli Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Weilun Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xinli Xia or Weilun Yin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, D., Song, S., Xia, X. et al. Two CBL genes from Populus euphratica confer multiple stress tolerance in transgenic triploid white poplar. Plant Cell Tiss Organ Cult 109, 477–489 (2012). https://doi.org/10.1007/s11240-011-0112-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-011-0112-7

Keywords

Search

Navigation