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Expression analysis and functional characterization of a novel cold-responsive gene CbCOR15a from Capsella bursa-pastoris

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Abstract

The cold-responsive (COR) genes involved in C-repeat binding factor signaling pathway function essentially in cold acclimation of higher plants. A novel COR gene CbCOR15a from shepherd’s purse (Capsella bursa-pastoris) was predicted to be a homolog of COR15 in Arabidopsis. The analysis of tissue specific expression pattern as well as characterization of the CbCOR15a promoter revealed that the expression of CbCOR15a was induced by coldness not only in leaves and stem but also in roots. Sequence analysis showed that a 909 bp promoter region of CbCOR15a contained two CRT/DRE elements, two ABRE elements, one auxin-responsive TGA-element and one MeJA-responsive CGTCA-motif. In young seedlings the expression of CbCOR15a could be apparently increased by SA, ABA, MeJA and IAA, and transiently increased by GA3 accompanied by obvious feedback suppression. According to the altered physiological index values in tobacco under cold treatments, the overexpression of CbCOR15a significantly increased the cold tolerance of transgenic tobacco plants. It can be suggested that CbCOR15a was involved in cold response of Capsella bursa-pastoris associated with SA, ABA, MeJA, IAA and GA3 regulation and confers enhanced cold acclimation in transgenic plants.

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Abbreviations

ABA:

Abscisic acid

COR:

Cold-responsive

EV:

Empty vector control

GA3 :

Gibberllic acid

IAA:

Indole-3-acetic acid

MeJA:

Methyl jasmonate

qRT-PCR:

Quantitative real-time PCR

RACE:

Rapid amplification of cDNA ends

SA:

Salicylic acid

WT:

Wild type

References

  1. Zhou MQ, Shen C, Wu LH, Tang KX, Lin J (2011) CBF-dependent signaling pathway: a key responder to low temperature stress in plants. Crit Rev Biotechnol 31:186–192

    Article  PubMed  CAS  Google Scholar 

  2. 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

    Article  PubMed  CAS  Google 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 24:701–713

    Article  PubMed  CAS  Google Scholar 

  4. 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

    Article  PubMed  CAS  Google Scholar 

  5. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599

    Article  PubMed  CAS  Google Scholar 

  6. 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 

  7. Breton G, Danyluk J, Charron JF, Sarhan F (2003) Expression profiling and bioinformatic analyses of a novel stress-regulated multispanning transmembrane protein family from cereals and Arabidopsis. Plant Physiol 132:64–74

    Article  PubMed  CAS  Google Scholar 

  8. Okawa K, Nakayama K, Kakizaki T, Yamashita T, Inaba T (2008) Identification and characterization of Cor413im proteins as novel components of the chloroplast inner envelope. Plant Cell Environ 31:1470–1483

    Article  PubMed  CAS  Google Scholar 

  9. Artus NN, Uemura M, Steponkus PL, Gilmour SJ, Lin C, 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 93:13404–13409

    Article  PubMed  CAS  Google Scholar 

  10. Nakayama K, Okawa K, Kakizaki T, Honma T, Itoh H, Inaba T (2007) Arabidopsis Cor15am is a chloroplast stromal protein that has cryoprotective activity and forms oligomers. Plant Physiol 144:513–523

    Article  PubMed  CAS  Google Scholar 

  11. Lin C, Thomashow MF (1992) DNA sequence analysis of a complementary of the COR15 polypeptide. Plant Physiol 115:171–180

    Google Scholar 

  12. Cattivelli L, Bartels D (1990) Molecular cloning and characterization of cold-regulated genes in barley. Plant Physiol 93:1504–1510

    Article  PubMed  CAS  Google Scholar 

  13. Weretilnyk E, Orr W, White TC, Iu B, Singh J (1993) Characterization of three related low-temperature-regulated cDNAs from winter Brassica napus. Plant Physiol 101:171–177

    Article  PubMed  CAS  Google Scholar 

  14. Chauvin LP, Houde M, Sarhan F (1993) A leaf-specific gene stimulated by light during wheat acclimation to low temperature. Plant Mol Biol 23:255–265

    Article  PubMed  CAS  Google Scholar 

  15. Lee YP, Fleming JA, Korner C, Meins F Jr (2009) Differential expression of the CBF pathway and cell cycle-related genes in Arabidopsis accessions in response to chronic low-temperature exposure. Plant Biol 11:273–283

    Article  PubMed  CAS  Google Scholar 

  16. 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 104:21002–21007

    Article  PubMed  CAS  Google Scholar 

  17. Guiltinan MJ, Marcotte WJ, Quatrano RS (1990) A plant leucine zipper protein that recognizes an abscisic acid response element. Science 250:267–271

    Article  PubMed  CAS  Google Scholar 

  18. Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94

    Article  PubMed  CAS  Google Scholar 

  19. Olof E, Henrik N, Gunnar VH (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8:978–984

    Article  Google Scholar 

  20. Geourjon C, Deleage G (1995) SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Comput Appl Biosci 11:681–684

    PubMed  CAS  Google Scholar 

  21. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  22. Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5:387–405

    Article  CAS  Google Scholar 

  23. Weatherley PE (1950) Studies in the water relations of cotton plants: 1. The field measurement of water deficit in leaves. New Phytol 49:81–97

    Article  Google Scholar 

  24. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  PubMed  CAS  Google Scholar 

  25. Liu S, Wang X, Fan Z, Pang Y, Sun X, Wang X, Tang K (2004) Molecular cloning and characterization of a novel cold-regulated gene from Capsella bursa-pastoris. DNA Seq 15:262–268

    Article  PubMed  CAS  Google Scholar 

  26. Si J, Wang JH, Zhang LJ, Zhang H, Liu YJ, An LZ (2009) CbCOR15, a cold-regulated gene from alpine Chorispora bungeana, confers cold tolerance in transgenic tobacco. J Plant Biol 52:593–601

    Article  CAS  Google Scholar 

  27. Wilhelm KS, Thomashow MF (1993) Arabidopsis thaliana cor15b, an apparent homologue of cor15a, is strongly responsive to cold and ABA, but not drought. Plant Mol Biol 23:1073–1077

    Article  PubMed  CAS  Google Scholar 

  28. Thalhammer A, Hundertmark M, Popova AV, Seckler R, Hincha DK (2010) Interaction of two intrinsically disordered plant stress proteins (COR15A and COR15B) with lipid membranes in the dry state. Biochim Biophys Acta Biomembr 1798:1812–1820

    Article  CAS  Google Scholar 

  29. Gavel Y, Heijine GV (1990) A conserved cleavage-site motif in chloroplast transit peptide. FEBS Lett 261:455–458

    Article  PubMed  CAS  Google Scholar 

  30. Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183

    Article  PubMed  CAS  Google Scholar 

  31. Wang Y, Hua J (2009) A moderate decrease in temperature induces COR15a expression through the CBF signaling cascade and enhances freezing tolerance. Plant J 60:340–349

    Article  PubMed  CAS  Google Scholar 

  32. Steponkus PL, Uemura M, Joseph RA, Gilmour SJ, Thomashow MF (1998) Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana. Proc Natl Acad Sci USA 95:14570–14575

    Article  PubMed  CAS  Google Scholar 

  33. Hara M, Terashima S, Fukaya T, Kuboi T (2003) Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta 217:290–298

    PubMed  CAS  Google Scholar 

  34. Houde M, Dallaire S, N’dong D, Sarhan F (2004) Overexpression of the acidic dehydrin WCOR410 improves freezing tolerance in transgenic strawberry leaves. Plant Biotechnol J 2:381–387

    Article  PubMed  CAS  Google Scholar 

  35. Shimamura C, Ohno R, Nakamura C, Takumi S (2006) Improvement of freezing tolerance in tobacco plants expressing a cold-responsive and chloroplast-targeting protein WCOR15 of wheat. J Plant Physiol 163:213–219

    Article  PubMed  CAS  Google Scholar 

  36. Hajela RK, Horvath DP, Gilmour SJ, Thomashow MF (1990) Molecular cloning and expression of cor (cold-regulated) genes in Arabidopsis thaliana. Plant Physiol 93:1246–1252

    Article  PubMed  CAS  Google Scholar 

  37. Ghassemian M, Nambara E, Cutler S, Kawaide H, Kamiya Y, McCourt P (2000) Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. Plant Cell 12:1117–1126

    Article  PubMed  CAS  Google Scholar 

  38. Venketesh S (2008) Properties, potentials, and prospects of antifreeze proteins. Crit Rev Biotechnol 28:57–82

    Article  PubMed  CAS  Google Scholar 

  39. Gilmour SJ, Thomashow MF (1991) Cold acclimation and cold-regulated gene expression in ABA mutants of Arabidopsis thaliana. Plant Mol Biol 17:1233–1240

    Article  PubMed  CAS  Google Scholar 

  40. Knight H, Zarka DG, Okamoto H, Thomashow MF, Knight MR (2004) Abscisic acid induces CBF gene transcription and subsequent induction of cold-regulated genes via the CRT promoter element. Plant Physiol 135:1710–1717

    Article  PubMed  CAS  Google Scholar 

  41. Bao F, Li JY (2002) Evidence that the auxin signaling pathway interacts with plant stress response. Acta Bot Sin 44:532–536

    CAS  Google Scholar 

  42. Chong JJ, Yang DD (2003) Methyl jasmonate as vital substance in plants. Trends Genet 19:409–413

    Article  Google Scholar 

  43. Malamy J, Carr JP, Klessig DF, Raskin I (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:1002–1004

    Article  PubMed  CAS  Google Scholar 

  44. Senaratna T, Touchell D, Bunn E, Dixon K (2000) Acetyl salicylic acid (aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Regul 30:157–161

    Article  CAS  Google Scholar 

  45. Richards DE, King KE, Ait-Ali T, Harberd NP (2001) How gibberellin regulates plant growth and development: a molecular genetic analysis of gibberellin signaling. Annu Rev Plant Physiol Plant Mol Biol 52:67–88

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was financially supported by The Major Program for the Fundamental Research of Shanghai, China (09JC1401700), The National High Technology Research and Development Program of China (863 Program) (2008AA10Z105), The National Key Technology R&D Program (2009BADA8B04).

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Authors and Affiliations

  1. State Key Laboratory of Genetic Engineering, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, 200433, People’s Republic of China

    Mingqi Zhou, Lihua Wu, Jing Liang, Chen Shen & Juan Lin

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  1. Mingqi Zhou
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  2. Lihua Wu
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  3. Jing Liang
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  4. Chen Shen
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  5. Juan Lin
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Correspondence to Juan Lin.

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Zhou, M., Wu, L., Liang, J. et al. Expression analysis and functional characterization of a novel cold-responsive gene CbCOR15a from Capsella bursa-pastoris . Mol Biol Rep 39, 5169–5179 (2012). https://doi.org/10.1007/s11033-011-1313-1

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