Brazilian Journal of Botany

, Volume 42, Issue 1, pp 97–105 | Cite as

A CkDREB1 gene isolated from Caragana korshinskii Kom. enhances Arabidopsis drought and cold tolerance

  • Ziyi Zhang
  • Qi Yang
  • Chunlin Zhang
  • Lili Wei
  • Rong Yue
  • Guojing Li
  • Xiaofei LinEmail author
  • Ruigang WangEmail author
Original Article


Caragana korshinskii Kom., an arbuscular legume with important economic and ecological value in feed, processing industry, and environmental protection, also has great tolerance potential to abiotic stress conditions. An AP2 domain-containing gene was isolated from the suppression subtractive hybridization library of C. korshinskii under drought stress. In addition, the isolated gene was also found to be responsive to cold and ABA treatment. Phylogenetic analysis indicates that the deduced protein belongs to the DREB A-1 subfamily and is designated as CkDREB1. Overexpression of CkDREB1 in Arabidopsis thaliana (L.) Heynh increased drought and cold tolerance compared with the wild type. The drought responsive genes RD29A, RD29B, KIN1, and KIN2, as well as cold-responsive marker genes COR15A and COR47, were also highly induced in the overexpression lines under drought and cold conditions. These results should shed light on our understanding on the mechanisms of abiotic resistance of C. korshinskii.


AP2 DNA-binding motif DREB Drought stress Transcription activator 



We thank Dr. Mark Goettel, the Editor-in-Chief of Biocontrol Science and Technology, for polishing the manuscript carefully. This work was supported by the National Natural Science Foundation of China (No. 31060105 and No. 31360169), grants from Chinese National Programs for High Technology Research and Development (No. 2011AA100203), and Inner Mongolia Natural Science Foundation (2010Zd13).

Author contributions

RW and XL conceived of the research, and RW designed the study and wrote the manuscript. ZZ, QY, and CZ conducted the most of the experiments. LW performed all of the plasmid construction. RY completed the plant transformation and provide plant materials. GL did bioinformatics analysis.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

40415_2018_509_MOESM1_ESM.doc (1.8 mb)
Supplementary material 1 (DOC 1882 kb)


  1. Abu-Romman S (2016) Genotypic response to heat stress in durum wheat and the expression of small HSP genes. Rend Lincei-Sci Fis 27:261–267. CrossRefGoogle Scholar
  2. Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274. CrossRefGoogle Scholar
  3. Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24:701–713CrossRefGoogle Scholar
  4. Bhardwaj PK, Ahuja PS, Kumar S (2010) Characterization of gene expression of QM from Caragana jubata, a plant species that grows under extreme cold. Mol Biol Rep 37:1003–1010. CrossRefGoogle Scholar
  5. Bhardwaj PK, Kaur J, Sobti RC, Ahuja PS, Kumar S (2011) Lipoxygenase in Caragana jubata responds to low temperature, abscisic acid, methyl jasmonate and salicylic acid. Gene 483:49–53. CrossRefGoogle Scholar
  6. Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12:2383–2394CrossRefGoogle Scholar
  7. Bouaziz D et al (2012) Ectopic expression of dehydration responsive element binding proteins (StDREB2) confers higher tolerance to salt stress in potato. Plant Physiol Biochem 60:98–108. CrossRefGoogle Scholar
  8. Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1:37–52. CrossRefGoogle Scholar
  9. Buttner 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 94:5961–5966CrossRefGoogle Scholar
  10. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefGoogle Scholar
  11. Drews GN, Bowman JL, Meyerowitz EM (1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65:991–1002CrossRefGoogle Scholar
  12. Dubouzet JG et al (2003a) 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. CrossRefGoogle Scholar
  13. Dubouzet JG et al (2003b) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33:751–763CrossRefGoogle Scholar
  14. 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 124:1854–1865CrossRefGoogle Scholar
  15. Hsieh TH, Lee JT, Yang PT, Chiu LH, Charng YY, Wang YC, Chan MT (2002) Heterology expression of the Arabidopsis C-repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. Plant Physiol 129:1086–1094. CrossRefGoogle Scholar
  16. Ito Y et al (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47:141–153. CrossRefGoogle Scholar
  17. Jiang C, Iu B, Singh J (1996) Requirement of a CCGAC cis-acting element for cold induction of the BN115 gene from winter Brassica napus. Plant Mol Biol 30:679–684CrossRefGoogle Scholar
  18. Jinhuan C, Xinli X, Weilun Y (2009) Expression profiling and functional characterization of a DREB2-type gene from Populus euphratica. Biochem Biophys Res Commun 378:483–487CrossRefGoogle Scholar
  19. Jofuku KD, den Boer BG, Van Montagu M, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–1225CrossRefGoogle Scholar
  20. Jofuku KD, Omidyar PK, Gee Z, Okamuro JK (2005) Control of seed mass and seed yield by the floral homeotic gene APETALA2. Proc Natl Acad Sci USA 102:3117–3122. CrossRefGoogle Scholar
  21. Khedr AHA, Serag MS, Nemat-Alla MM, Abo-Elnaga AZ, Nada RM, Quick WP, Abogadallah GM (2011) A DREB gene from the xero-halophyte Atriplex halimus is induced by osmotic but not ionic stress and shows distinct differences from glycophytic homologues. Plant Cell, Tissue Organ Cult 106:191–206. CrossRefGoogle Scholar
  22. Klucher KM, Chow H, Reiser L, Fischer RL (1996) The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8:137–153. CrossRefGoogle Scholar
  23. Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62:4731–4748. CrossRefGoogle Scholar
  24. Lee JY, Baum SF, Alvarez J, Patel A, Chitwood DH, Bowman JL (2005) Activation of CRABS CLAW in the nectaries and carpels of Arabidopsis. Plant Cell 17:25–36. CrossRefGoogle Scholar
  25. 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 10:1391–1406CrossRefGoogle Scholar
  26. Moose SP, Sisco PH (1996) Glossy15, an APETALA2-like gene from maize that regulates leaf epidermal cell identity. Genes Dev 10:3018–3027CrossRefGoogle Scholar
  27. Nakashima K, Shinwari ZK, Sakuma Y, Seki M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol Biol 42:657–665CrossRefGoogle Scholar
  28. Navarro M, Ayax C, Martinez Y, Laur J, El Kayal W, Marque C, Teulieres C (2011) Two EguCBF1 genes overexpressed in Eucalyptus display a different impact on stress tolerance and plant development. Plant Biotechnol J 9:50–63. CrossRefGoogle Scholar
  29. Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182. CrossRefGoogle Scholar
  30. Okamuro JK, Caster B, Villarroel R, Van Montagu M, Jofuku KD (1997) The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc Natl Acad Sci USA 94:7076–7081CrossRefGoogle Scholar
  31. Perveen S, Al-Musayeib N, Malik A, Tareen RB (2014) Brachysides A and B, new lignan glucosides from Caragana brachyantha. J Chem Res. Google Scholar
  32. Ren XZ et al (2010) ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J 63:417–429. CrossRefGoogle Scholar
  33. Shi Y, Tian S, Hou L, Huang X, Zhang X, Guo H, Yang S (2012) Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis. Plant Cell 24:2578–2595. CrossRefGoogle Scholar
  34. Shinwari ZK, Nakashima K, Miura S, Kasuga M, Seki M, Yamaguchishinozaki K, Shinozaki K (1998) An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. Biochem Biophys Res Commun 250:161CrossRefGoogle Scholar
  35. Siminovitch D, Cloutier Y (1983) Drought and freezing tolerance and adaptation in plants: some evidence of near equivalences. Cryobiology 20:487–503CrossRefGoogle Scholar
  36. 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 94:1035–1040CrossRefGoogle Scholar
  37. Wang Z, Gao HW, Wu YQ, Han JG (2007) Genetic diversity and population structure of Caragana korshinskii revealed by AFLP. Crop Sci 47:1737–1743. CrossRefGoogle Scholar
  38. Wang X, Wang Z, Dong J, Wang M, Gao H (2009) Cloning of a 9-cis-epoxycarotenoid dioxygenase gene and the responses of Caragana korshinskii to a variety of abiotic stresses. Genes Genet Syst 84:397–405CrossRefGoogle Scholar
  39. Wang XM, Dong J, Liu Y, Gao HW (2010) A novel dehydration-responsive element-binding protein from Caragana korshinskii is involved in the response to multiple abiotic stresses and enhances stress tolerance in transgenic tobacco. Plant Mol Biol Rep 28:664–675. CrossRefGoogle Scholar
  40. Wang XM, Chen XF, Liu Y, Gao HW, Wang Z, Sun GZ (2011) CkDREB gene in Caragana korshinskii is involved in the regulation of stress response to multiple abiotic stresses as an AP2/EREBP transcription factor. Mol Biol Rep 38:2801–2811. CrossRefGoogle Scholar
  41. Wilson K, Long D, Swinburne J, Coupland G (1996) A dissociation insertion causes a semidominant mutation that increases expression of TINY, an Arabidopsis gene related to APETALA2. Plant Cell 8:659–671. CrossRefGoogle Scholar
  42. Wu YP, Hu XW, Wang YR (2009) Growth, water relations, and stomatal development of Caragana korshinskii Kom. and Zygophyllum xanthoxylum (Bunge) Maxim. seedlings in response to water deficits. N Z J Agric Res 52:185–193. CrossRefGoogle Scholar
  43. Xu ZS, Ni ZY, Liu L, Nie LN, Li LC, Chen M, Ma YZ (2008) Characterization of the TaAIDFa gene encoding a CRT/DRE-binding factor responsive to drought, high-salt, and cold stress in wheat. Mol Genet Genom 280:497–508CrossRefGoogle Scholar
  44. Xu ZS et al (2009) Isolation and functional characterization of HvDREB1-a gene encoding a dehydration-responsive element binding protein in Hordeum vulgare. J Plant Res 122:121–130. CrossRefGoogle Scholar
  45. 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. CrossRefGoogle Scholar
  46. Yoo SH, Kim BY, Weon HY, Kwon SW, Go SJ, Stackebrandt E (2007) Burkholderia soli sp. nov., isolated from soil cultivated with Korean ginseng. Int J Syst Evol Microbiol 57:122–125. CrossRefGoogle Scholar
  47. Zandalinas SI, Mittler R, Balfagon D, Arbona V, Gomez-Cadenas A (2018) Plant adaptations to the combination of drought and high temperatures. Physiol Plant 162:2–12. CrossRefGoogle Scholar
  48. Zhang Y et al (2010) Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proc Natl Acad Sci USA 107:18220–18225. CrossRefGoogle Scholar
  49. Zhou ML, Ma JT, Zhao YM, Wei YH, Tang YX, Wu YM (2012) Improvement of drought and salt tolerance in Arabidopsis and Lotus corniculatus by overexpression of a novel DREB transcription factor from Populus euphratica. Gene 506:10–17. CrossRefGoogle Scholar
  50. Zou JJ, Wei FJ, Wang C, Wu JJ, Ratnasekera D, Liu WX, Wu WH (2010) Arabidopsis calcium-dependent protein kinase CPK10 functions in abscisic acid- and Ca2+-mediated stomatal regulation in response to drought stress. Plant Physiol 154:1232–1243. CrossRefGoogle Scholar

Copyright information

© Botanical Society of Sao Paulo 2019

Authors and Affiliations

  1. 1.Inner Mongolia Key Laboratory of Plant Stress Physiology and Molecular Biology, College of Life SciencesInner Mongolia Agricultural UniversityHohhotPeople’s Republic of China
  2. 2.Key Laboratory of Forage and Endemic Crop Biotechnology, Ministry of Education, School of Life SciencesInner Mongolia UniversityHohhotPeople’s Republic of China

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