Abstract
Ca2+ is a critical component in signal transduction pathways that lead to stress gene expression in higher plants and regulates a wide range of physiological processes. The calcineurin B-like protein (CBL) family represents a unique group of calcium sensors in plants, and plays a key role in decoding calcium transients. Here, a CBL1 homolog gene, AmCBL1 (NCBI accession no. AY902246), was isolated from Ammopiptanthus mongolicus (Maxim.) by reverse transcriptase-polymerase chain reaction (RT-PCR) and rapid amplification of cDNA ends (RACE). Quantitative real-time PCR (QRT-PCR) experiments showed that AmCBL1 was significantly induced by drought, high salinity, heat, and CaCl2 treatments in A. mongolicus seedlings. Subcellular localization analysis suggested that AmCBL1 is a plasma membrane-localized protein. Our results suggest that AmCBL1 is not only a positive regulator of salt response but also a positive regulator of temperature stresses in A. mongolicus.
Similar content being viewed by others
Abbreviations
- ABA:
-
Abscisic acid
- CaM:
-
Calmodulin
- CAML:
-
Calmodulin like proteins
- CBL:
-
Calcineurin B-like
- CDPK:
-
Calcium dependent protein kinase
- CIPK:
-
CBL-interacting protein kinases
- CNB:
-
Calcineurin B
- GFP:
-
Green fluorescent protein
- NCS:
-
Neuronal calcium sensors
- ORF:
-
Open reading frame
- PCR:
-
Polymerase chain reaction
- qRT-PCR:
-
Quantitative real-time PCR
- RACE:
-
Rapid amplification cDNA ends
References
Albrecht V, Weinl S, Blazevic D, D’Angelo C, Batistic O, Kolukisaoglu Ü, Bock R, Schulz B, Harter K, Kudla J (2003) The calcium sensor CBL1 integrates plant response to abiotic stresses. Plant J 36:457–470
Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffman T, Tang YY, Grill E, Schroeder JI (2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053–1057
Asano T, Tanaka N, Nagao G (2005) Genome-wide identification of the rice calcium-dependent protein kinase and its closely related kinase gene families: comprehensive analysis of the CDPKs gene family in rice. Plant Cell Physiol 46:356–366
Batistic O, Kudla J (2004) Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta 219:915–924
Batisticˇ O, Sorek N, Schütke S, Yalovsky S, Kudla J (2008) Dual Fatty Acyl Modification Determines the Localization and Plasma Membrane Targeting of CBL/CIPK Ca2+ Signaling Complexes in Arabidopsis. Plant Cell 20:1346–1362
Batisticˇ O, Waadt R, Steinhorst L, Held K, Kudla J (2010) CBL-mediated targeting of CIPKs facilitates the decoding of calcium signals emanating from distinct cellular stores. Plant J 61:211–222
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
Chen JH, Xia XL, Yin WL (2009) Expression profiling and functional characterization of a DREB2-type gene from Populus euphratic. Bioche Biophys Res Commun 378:483–487
Cheong YH, Kim KN, Pandey GK, Gupta R, Grant JJ, Luan S (2003) CBL, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell 15:1833–1845
Cheong YH, Pandey GK, Grant JJ, Batisticˇ O, Li L, Kim BG, Lee SC, Kudla J, Luan S (2007) Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J 52:223–239
Guo LL, Yu YH, Xia XL, Yin WL (2010) Identification and functional characterization of the promoter of the calcium sensor gene CBL1 from the xerophyte Ammopiptanthus mongolicus. BMC Plant Biol 10:18
Harper JF (2001) Dissecting calcium oscillators in plant cells. Trends Plant Sci 6:395–397
Jiang Y, Wei LB, Fei YB, Shu NH, Gao SQ (1999) Purification and identification of antifreeze proteins in Ammopiptanthus mongolicus. Acta Bot Sin 41:967–971
Knight H, Knight MR (2001) Abiotic stress signaling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267
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 134:43–58
Kudla J, Xu Q, Harter K, Gruissem W, Luan S (1999) Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc Natl Acad Sci USA 96:4718–4723
Xu J, Li HD, Chen LQ, Wang Y, Liu LL HL, Wu WH (2006) A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125:1347–1360
Luan S (2009) The CBL-CIPK network in plant calcium signaling. Trends Plant Sci 14:37–42
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 Suppl 14:S389–S400
McCormack E, Braam J (2003) Calmodulins and related potential calcium sensors of Arabidopsis. New Phytol 159:585–598
Nozawa A, Koizumi N, Sano H (2001) An Arabidopsis SNF1-related protein kinase, AtSR1, interact with a calcium-binding protein, AtCBL2, of which transcripts respond to light. Plant Cell Physiol 42:976–981
Pandey GK, Cheong YH, Kim KN, Luan S (2004) The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. Plant Cell 16:1912–1924
Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14:S401–S417
Weinl S, Kudla J (2009) The CBL–CIPK Ca2+-decoding signaling network: function and perspectives. New Phytol 184:517–528
Yang L, Tang R, Zhu J, Liu H, Mueller-Roeber B, Xia H, Zhang H (2008) Enhancement of stress tolerance in transgenic tobacco plants constitutively expressing AtIpk2β, an inositol polyphosphate 6-/3-kinase from Arabidopsis thaliana. Plant Mol Biol 66:329–343
Yu YH, Xia XL, Yin WL, Zhang HC (2007) Comparative genomic analysis of CIPK gene family in Arabidopsis and Populus. Plant Growth Regul 52:101–110
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
Zhao CM, Wang GX (2002) Effects of drought stress on the photoprotection in Ammopiptanthus mongolicus leaves. Acta Bot Sin 44:1309–1313
Zielinski RE (1998) Calmodulin and calmodulin-binding proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 49:697–725
Zwiazek JJ, Blake TJ (1990) Effects of preconditioning on electrolyte leakage and lipid composition in black spruce (Picea mariana) stressed with polyethylene glycol. Physiol Plant 79:71–77
Acknowledgments
This work was supported by the Hi-Tech Research and Development Program of China (2007AA10Z106), National Natural Science Foundation of China (30730077, 30972339, 31070597), Program for New Century Excellent Talents in University of China (NCET-07-0083), “948” Project of State Forestry Administration of China (2007-4-01), and the Fundamental Research funds for central universities (Y×2010-17).
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Chen, JH., Sun, Y., Sun, F. et al. Tobacco plants ectopically expressing the Ammopiptanthus mongolicus AmCBL1 gene display enhanced tolerance to multiple abiotic stresses. Plant Growth Regul 63, 259–269 (2011). https://doi.org/10.1007/s10725-010-9523-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-010-9523-4