Abstract
Many plants increase in freezing tolerance upon exposure to low non-freezing temperatures, a phenomenon known as cold acclimation. Cold acclimation in Arabidopsis involves rapid cold-induced expression of the inducer of C-repeat/dehydration-responsive element-binding factor (CBF) expression (ICE) transcriptional activators followed by expression of the CBF; subsequently, CBF-targeted genes that increase freezing tolerance. Here, we present evidence for a CBF cold-response pathway in non-heading Chinese cabbage (Brassica campestris ssp. chinensis L. Makino). We show that non-heading Chinese cabbage encodes ICE1-like gene BrICE1 that bracket an open reading frame of 1,491 bp encoding a protein with a potential bHLH domain, which accumulates rapidly in response to low temperature followed closely by expression of the BrCBF gene, an ortholog of the Arabidopsis CBF3-like gene, and then BrCOR14 gene, an ortholog of the Arabidopsis CBF-targeted COR15b gene. An alignment of the later two genes from Arabidopsis, Brassica napus revealed the presence of conserved CANNTG core element and AP2 domain in BrCBF and a CCG core element in BrCOR14. In addition, BrCBF and BrCOR14 showed increased expression induced by low temperature as well as salt and drought, but not by ABA stress which are similar to those of Arabidopsis. We conclude that components of the CBF cold-response pathway are highly conserved in non-heading Chinese cabbage.
Similar content being viewed by others
Abbreviations
- ICE :
-
Inducer of CBF expression
- CBF :
-
CRT-binding factors
- COR :
-
Cold-regulated genes
References
Altus NN, Uemura M, Steponkus PL, Gilmour SJ, Lin C, Thomashow MF (1996) Constiutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. Plant Biol 93:13404–13409
Büttner M, Singh KB (1997) Arabidopsis thaliana ethylene responsive element binding protein (AtEBP), an ethylene inducible, GCC box DNA-binding protein interacts with an ocs element binding protein. Proc Natl Acad Sci USA 94:5961–5966
Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong XH, Agarwal M, Zhu JK (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17:1043–1054
Chinnusamy V, Zhu JH, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451
Chinnusamy V, Zhu JK, Sunkar R (2010) Gene regulation during cold stress acclimation in plants. Methods Mol Biol 639:39–55
Fowler DB, Limin AE, Wang S, Ward RW (1996) Relationship between low-temperature tolerance and vernalization response in wheat and rye. Can J Plant Sci 76:37–42
Gao MJ, Allard G, Byass L, Flanagan AM, Singh J (2002) Regulation and characterization of four CBF transcription factors from Brassica napus. Plant Mol Biol 49:459–471
Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16:433–442
Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124:1854–1865
Goulas E, Dily FL, Ozouf J, Ourry A (2003) Effects of a cold treatment of the root system on white clover (Trifolium repens L.) morphogenesis and nitrogen reserve accumulation. J Plant Physiol 160:893–902
Guiltinan MJ, Marcotte WR, Quatrano RS (1990) A plant leucine zipper protein that recognizes an abscisic acid response element. Science 250:267–271
Huang H, Tudor M, Su T, Zhang Y, Hu Y, Ma H (1996) DNA binding properties of two Arabidopsis MADS domain proteins: binding consensus and dimer formation. Plant Cell 8:81–94
Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106
Jaglo-Ottosen KR, Kleff S, Amundsen KL, Zhang X, Haake V, Zhang JZ, Deits T, Thomashow MF (2001) Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol 127:910–917
Jiang FL, Hou XL, Shi GJ, Cui XM (2007a) Cloning and characterization of full length cDNA of BrCBF gene from Brassica campestris ssp. chinensis. J Nanjing Agri Uni 30:18–22 (in chinensis)
Jiang FL, Hou XL, Shi GJ, Cui XM (2007b) Cloning and characterization of full length cDNA of BrCOR14 gene from Brassica campestris ssp. chinensis. Jiangsu J of Agr Sci 23:34–38 (in Chinese)
Jiang FL, Hou XL, Shi GJ, Cui XM (2007c) Cloning and characterization of full length cDNA of BrLOS2 gene from Brassica campestris ssp. chinensis. J Nanjing Agri Uni 30:27–32 (in Chinese)
Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291
Lee B, Henderson DA, Zhu JK (2005) The arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17:3155–3175
Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406
Medina J, Bargues M, Terol J, Pérez-Alonso M, Salinas J (1999) The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiol 119:463–470
Meng SS, Dane F, Si Y, Ebel R, Zhang CK (2008) Gene expression analysis of cold treated versus cold acclimated Poncirus trifoliata. Euphytica 164(1):209–219
Meshi T, Iwabuchi M (1995) Plant transcription factors. Plant Cell Physiol 36:1405–1420
Riechmann JL, Meyerowitz EM (1997) Domain proteins in plant development. Biol Chem 10:1079–1101
Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040
Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599
Thomashow MF (2001) So what’s new in the field of plant cold acclimation? Lots! Plant Physiol 125:89–93
Wang XL, Sun XQ, Liu SX, Liu L, Liu XJ, Sun XF, Tang KX (2005) Molecular cloning and characterization of a novel ice gene from Capsella bursa-pastoris. Mol Biol 39:18–25
Wang L, Li XW, Zhao Q, Jing SL, Chen SF, Yuan HY (2009) Identification of genes induced in response to low-temperature treatment in tea leaves. Plant Mol Biol Rep 27:257–265
Williams ME, Foster R, Chua NH (1992) Sequences flanking the hexameric G-box core CACGTG affect the specificity of protein binding. Plant Cell 4:485–496
Wilson CL, Hubbard SJ, Doig AJ (2002) A critical assessment of the secondary structure α-helices and their termini in proteins. Protein Eng 15(7):545–554
Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6:251–264
Yang TW, Zhang LJ, Zhang TG, Zhang H, Xu SJ, An LZ (2005) Transcriptional regulation network of cold-responsive genes in higher plants. Plant Sci 169:987–995
Zhou N, Robinson SJ, Huebert T, Bate NJ, Parkin IAP (2007) Comparative genome organization reveals a single copy of CBF in the freezing tolerant crucifer Thlaspi arvense. Plant Mol Biol 65:693–705
Acknowledgements
This research was partially supported by the Natural Science Foundation of Jiangsu Province (BK2009311) and National Science and Technology Support Program (2009BADB8B03-1).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Jiang, F., Wang, F., Wu, Z. et al. Components of the Arabidopsis CBF Cold-Response Pathway Are Conserved in Non-heading Chinese Cabbage. Plant Mol Biol Rep 29, 525–532 (2011). https://doi.org/10.1007/s11105-010-0256-3
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-010-0256-3