Skip to main content
Log in

Heterologous expression of Arabidopsis C-repeat binding factor 3 (AtCBF3) and cold-regulated 15A (AtCOR15A) enhanced chilling tolerance in transgenic eggplant (Solanum melongena L.)

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Our study shows that the expression of AtCBF3 and AtCOR15A improved the chilling tolerance in transgenic eggplant.

Abstract

In an attempt to improve chilling tolerance of eggplant (Solanum melongena L) plants, Arabidopsis C-repeat binding factor 3 (AtCBF3) and cold-regulated 15A (AtCOR15A) genes both driven by an Arabidopsis RESPONSIVE TO DESSICATION 29A promoter (AtRD29A) were transferred into the plants of eggplant cultivar Sanyueqie. Two independent homozygous transgenic lines were tested for their cold tolerance. The leaves of the transgenic plants in both lines withered much slower and slighter than the wild-type plants after exposure to cold stress treatment at 2 ± 1 °C. The gene expression of AtCBF3 and AtCOR15A was significantly increased as well as the proline content and the levels of catalase and peroxidase activities, while the relative electrical conductivity and the malondialdehyde content were remarkably decreased in the transgenic plants compared with the wild type at 4 ± 0.5 °C. The results showed that the expression of the exogenous AtCBF3 and AtCOR15A could promote the cold adaptation process to protect eggplant plants from chilling stress.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

AtRD29A:

RESPONSIVE TO DESSICATION 29A promoter of Arabidopsis thaliana

6-BA:

6-benzyladenine

CaMV 35S:

Cauliflower mosaic virus 35S promoter

CAT:

Catalase

CBF:

C-repeat-binding factor

EL:

Electrolyte leakage

FW:

Fresh weight

MDA:

Malondialdehyde

NAA:

α-Naphthaleneacetic acid

POD:

Peroxidase

ROS:

Reactive oxygen species

RT:

Room temperature

RT-PCR:

Real-time PCR

TBA:

2-thiobarbituric acid

Tnos:

The terminator of nopaline synthase gene

ZT:

Zeatin

References

  • Acciarri N, Restaino F, Vitelli G, Perrone D, Zottini M, Pandolfini T, Spena A, Rotino GL (2002) Genetically modified parthenocarpic eggplants: improved fruit productivity under both greenhouse and open field cultivation. BMC Biotechnol 2(1):4–11

    Article  PubMed Central  PubMed  Google Scholar 

  • 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(12):1263–1274

    Article  CAS  PubMed  Google Scholar 

  • Arbona V, Gomez-Cadenas A (2008) Hormonal modulation of citrus responses to flooding. J Plant Growth Regul 27(3):241–250

    Article  CAS  Google Scholar 

  • Artus NN, Uemura M, Steponkus PL, Gilmour SJ, Lin CT, Thomashow MF (1996) Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. Proc Natl Acad Sci USA 93(23):13404–13409

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207

    Article  CAS  Google Scholar 

  • Behnam B, Kikuchi A, Celebi-Toprak F, Kasuga M, Yamaguchi-Shinozaki K, Watanabe KN (2007) Arabidopsis rd29A : DREB1A enhances freezing tolerance in transgenic potato. Plant Cell Rep 26(8):1275–1282

    Article  CAS  PubMed  Google Scholar 

  • Cao B, Huang Z, Chen G, Lei J (2010) Restoring pollen fertility in transgenic male-sterile eggplant by Cre/loxp-mediated site-specific recombination system. Genet Mol Biol 33(2):298–307

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen M, Xu Z, Xia L, Li L, Cheng X, Dong J, Wang Q, Ma Y (2009) Cold-induced modulation and functional analyses of the DRE-binding transcription factor gene, GmDREB3, in soybean (Glycine max L.). J Exp Bot 60:121–135

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK (2006) Gene regulation during cold acclimation in plants. Physiol Plant 126(1):52–61

    Article  CAS  Google Scholar 

  • Concellon A, Anon MC, Chaves AR (2005) Effect of chilling on ethylene production in eggplant fruit. Food Chem 92(1):63–69

    Article  CAS  Google Scholar 

  • Dong C, Zhang Z, Ren JP, Qin Y, Huang JF, Wang Y, Cai BH, Wang BL, Tao JM (2013) Stress-responsive gene ICE1 from Vitis amurensis increases cold tolerance in tobacco. Plant Physiol Biochem 71:212–217

    Article  CAS  PubMed  Google Scholar 

  • Gantasala NP, Papolu PK, Thakur PK, Kamaraju D, Sreevathsa R, Rao U (2013) Selection and validation of reference genes for quantitative gene expression studies by real-time PCR in eggplant (Solanum melongena L). BMC Res Notes 6:312–323

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gao HB, Chen GL, Han LH, Lin HA (2004) Calcium influence on chilling resistance of grafting eggplant seedlings. J Plant Nutr 27(8):1327–1339

    Article  CAS  Google Scholar 

  • 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(4):1854–1865

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Goggin FL, Jia L, Shah G, Hebert S, Williamson VM, Ullman DE (2006) Heterologous expression of the Mi-1.2 gene from tomato confers resistance against nematodes but not aphids in eggplant. Mol Plant. Microbe 19(4):383–388

    CAS  Google Scholar 

  • Groeneveld RA, Ansink E, Van de Wiel C, Wesseler J (2011) Benefits and costs of biologically contained genetically modified tomatoes and eggplants in Italy and Spain. Sustainability 3:1265–1281

    Article  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1):189–198

    Article  CAS  PubMed  Google Scholar 

  • 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(3):1086–1094

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Huang J, Sun SJ, Xu DQ, Yang X, Bao YM, Wang ZF, Tang HJ, Zhang HS (2009) Increased tolerance of rice to cold, drought and oxidative stresses mediated by the overexpression of a gene that encodes the zinc finger protein ZFP245. Biochem Biophys Res Commun 389(3):556–561

    Article  CAS  PubMed  Google Scholar 

  • Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47(1):141–153

    Article  CAS  PubMed  Google Scholar 

  • Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280(5360):104–106

    Article  CAS  PubMed  Google Scholar 

  • Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2004) 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(3):346–350

    Article  CAS  PubMed  Google Scholar 

  • Li X, Cheng XX, Liu J, Zeng HM, Han LB, Tang W (2011) Heterologous expression of the Arabidopsis DREB1A/CBF3 gene enhances drought and freezing tolerance in transgenic Lolium perenne plants. Plant Biotechnol Rep 5(1):61–69

    Article  Google Scholar 

  • Liu JH, Nada K, Honda C, Kitashiba H, Wen XP, Pang XM, Moriguchi T (2006) Polyamine biosynthesis of apple callus under salt stress: importance of the arginine decarboxylase pathway in stress response. J Exp Bot 57(11):2589–2599

    Article  CAS  PubMed  Google Scholar 

  • Maestrelli A, Lo Scalzo R, Rotino GL, Acciarri N, Spena A, Vitelli G, Bertolo G (2003) Freezing effect on some quality parameters of transgenic parthenocarpic eggplants. J Food Eng 56(2–3):285–287

    Article  Google Scholar 

  • Medina J, Catala R, Salinas J (2011) The CBFs: three arabidopsis transcription factors to cold acclimate. Plant Sci 180(1):3–11

    Article  CAS  PubMed  Google Scholar 

  • Morsy MR, Almutairi AM, Gibbons J, Yun SJ, de los Reyes BG (2005) The OsLti6 genes encoding low-molecular-weight membrane proteins are differentially expressed in rice cultivars with contrasting sensitivity to low temperature. Gene 344:171–180

    Article  CAS  PubMed  Google Scholar 

  • Novillo F, Medina J, Salinas J (2007) Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon. Proc Natl Acad Sci USA 104(52):21002–21007

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Novillo F, Medina J, Rodriguez-Franco M, Neuhaus G, Salinas J (2012) Genetic analysis reveals a complex regulatory network modulating CBF gene expression and Arabidopsis response to abiotic stress. J Exp Bot 63(1):293–304

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, Kim M, Kim YK, Nahm BH, Kim JK (2005) Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138(1):341–351

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Oh SJ, Kwon CW, Choi DW, Song SI, Kim JK (2007) Expression of barley HvCBF4 enhances tolerance to abiotic stress in transgenic rice. Plant Biotechnol J 5(5):646–656

    Article  CAS  PubMed  Google Scholar 

  • Oraby H, Ahmad R (2012) Physiological and biochemical changes of CBF3 transgenic oat in response to salinity stress. Plant Sci 185:331–339

    Article  PubMed  Google Scholar 

  • Pellegrineschi A, Reynolds M, Pacheco M, Brito RM, Almeraya R, Yamaguchi-Shinozaki K, Hoisington D (2004) Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 47:493–500

    Article  CAS  PubMed  Google Scholar 

  • Pino MT, Skinner JS, Park EJ, Jeknic Z, Hayes PM, Thornashow MF, Chen THH (2007) Use of a stress inducible promoter to drive ectopic AtCBF expression improves potato freezing tolerance while minimizing negative effects on tuber yield. Plant Biotechnol J 5(5):591–604

    Article  CAS  PubMed  Google Scholar 

  • Prabhavathi VR, Rajam MV (2007) Polyamine accumulation in transgenic eggplant enhances tolerance to multiple abiotic stresses and fungal resistance. Plant Biotechnol Nar 24:273–282

    Article  CAS  Google Scholar 

  • Prabhavathi V, Yadav JS, Kumar PA, Rajam MV (2002) Abiotic stress tolerance in transgenic eggplant (Solanum melongena L.) by introduction of bacterial mannitol phosphodehydrogenase gene. Mol Breed 9(2): 137-147

  • Rotino GL, Perri E, Zottini M, Sommer H, Spena A (1997) Genetic engineering of parthenocarpic plants. Nat Biotechnol 15(13):1398–1401

    Article  CAS  PubMed  Google Scholar 

  • Sanghera GS, Wani SH, Hussain W, Singh NB (2011) Engineering cold stress tolerance in crop plants. Curr Genomics 12(1):30–43

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shi J, Fu XZ, Peng T, Huang XS, Fan QJ, Liu JH (2010) Spermine pretreatment confers dehydration tolerance of citrus in vitro plants via modulation of antioxidative capacity and stomatal response. Tree Physiol 30(7):914–922

    Article  CAS  PubMed  Google Scholar 

  • Sidhu A, Bal S, Behera T, Rani M (2005) An outlook in hybrid eggplant breeding. J New Seeds 6:15–29

    Article  Google Scholar 

  • Thomashow MF (2010) Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol 154(2):571–577

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thomashow MF, Gilmour SJ, Stockinger EJ, Jaglo-Ottosen KR, Zarka DG (2001) Role of the Arabidopsis CBF transcriptional activators in cold acclimation. Physiol Plant 112(2):171–175

    Article  CAS  Google Scholar 

  • Wisniewski M, Norelli J, Bassett C, Artlip T, Macarisin D (2011) Ectopic expression of a novel peach (Prunus persica) CBF transcription factor in apple (Malus × domestica) results in short-day induced dormancy and increased cold hardiness. Planta 233(5):971–983

    Article  CAS  PubMed  Google Scholar 

  • Wu LH, Zhou MQ, Shen C, Liang J, Lin J (2012) Transgenic tobacco plants over expressing cold regulated protein CbCOR15b from Capsella bursa-pastoris exhibit enhanced cold tolerance. J Plant Physiol 169(14):1408–1416

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Hung B, Chen Z, Liu Y (2000) Low temperature injury and cold resistance mechanism of eggplant. Fujian J Agric Sci 15(1):40–42

    Google Scholar 

  • Zeller G, Henz SR, Widmer CK, Sachsenberg T, Ratsch G, Weigel D, Laubinger S (2009) Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. Plant J 58(6):1068–1082

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Fowler SG, Cheng HM, Lou YG, Rhee SY, Stockinger EJ, Thomashow MF (2004) Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis. Plant J 39(6):905–919

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2000) Genetic analysis of plant salt tolerance using arabidopsis. Plant Physiol 124(3):941–948

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the National High Technology Research and Development Program of China (863 Program, Grant No. 2009AA10Z104-7), the Transgenic Engineering Crops Breeding Special Funds from China’s Ministry of Agriculture (Grant No. 2009ZX08010-005B) and China Postdoctoral Science Foundation (Grant No. 2013M540692).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xingguo Zhang.

Additional information

Communicated by Kinya Toriyama.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 43 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wan, F., Pan, Y., Li, J. et al. Heterologous expression of Arabidopsis C-repeat binding factor 3 (AtCBF3) and cold-regulated 15A (AtCOR15A) enhanced chilling tolerance in transgenic eggplant (Solanum melongena L.). Plant Cell Rep 33, 1951–1961 (2014). https://doi.org/10.1007/s00299-014-1670-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-014-1670-z

Keywords

Navigation