Skip to main content
Log in

Expression analysis and functional characterization of a cold-responsive gene COR15A from Arabidopsis thaliana

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

The cold-responsive (COR) genes play an important role in cold acclimation of higher plants. Here, a tight correlation between chloroplast functionality and COR15A expression, and the functional characterization of Arabidopsis COR15A involved in salt/osmotic stress, were revealed. COR15A gene is light inducible and expressed in light-grown seedlings. The expression level of COR15A was reduced when chloroplasts were damaged by norflurazon treatment. By using several albino mutants, seca1, secy1, and tic20, all of which exhibited severe defects in both structure and function of chloroplast, it was shown that the accumulation of COR15A mRNA depends on chloroplast functionality. Real-time RT-PCR and GUS-staining assays demonstrated that COR15A was induced by salt/osmotic stress partially via ABA. Overexpression of COR15A in Arabidopsis resulted in the seedlings displaying hypersensitivity to salt/osmotic stress. All these results suggest that plant acquire the ability to fully express COR15A only after the development of functional chloroplasts, COR15A may be involved in response to salt/osmotic stress during early stages of plant development.

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

References

  • Alonso JM, Stepanova AN, Leisse TJ et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana corl5a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24:701–713

    CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  PubMed  Google Scholar 

  • Cartharius K, Frech K, Grote K, Klocke B, Haltmeier M, Klingebhoff A, Frisch M, Bayerlein M, Werner T (2005) MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 21:2933–2942

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    CAS  PubMed  Google Scholar 

  • Crone D, Rueda J, Martin KL, Hamilton DA, Mascarenhas JP (2001) The differential expression of a heat shock promoter in floral and reproductive tissues. Plant Cell Environ 24:869–874

    CAS  Google Scholar 

  • Di Cola A, Klostermann E, Robinson C (2005) The complexity of pathways for protein import into thylakoids: it’s not easy being green. Biochem Soc Trans 33:1024–1027

    PubMed  Google Scholar 

  • Estavillo GM, Crisp PA, Pornsiriwong W, Wirtz M, Collinge D, Carrie C, Giraud E, Whelan J, David P, Javot H, Brearley C, Hell R, Marin E, Pogson BJ (2011) Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23:3992–4012

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fernández AP, Strand A (2008) Retrograde signaling and plant stress: plastid signals initiate cellular stress responses. Curr Opin Plant Biol 11:509–513

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Gilmour SJ, Artus NN, Thomashow MF (1992) cDNA sequence analysis and expression of two cold-regulated genes of Arabidopsis thaliana. Plant Mol Biol 18:13–21

    CAS  PubMed  Google Scholar 

  • Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genom 9:118

    Google Scholar 

  • Inaba T, Schnell DJ (2008) Protein trafficking to plastids: one theme, many variations. Biochem J 413:15–28

    CAS  PubMed  Google Scholar 

  • Jefferson RA (1989) The GUS reporter gene system. Nature 342:837–838

    CAS  PubMed  Google Scholar 

  • Kakizaki T, Matsumura H, Nakayama K, Che FS, Terauchi R, Inaba T (2009) Coordination of plastid protein import and nuclear gene expression by plastid-to-nucleus retrograde signaling. Plant Physiol 151:1339–1353

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kakizaki T, Yazu F, Nakayama K, Ito-inaba Y, Inaba T (2012) Plastid signalling under multiple conditions is accompanied by a common defect in RNA editing in plastids. J Exp Bot 63:251–260

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kasmati AR, Töpel M, Patel R, Murtaza G, Jarvis P (2011) Molecular and genetic analyses of Tic20 homologues in Arabidopsis thaliana chloroplasts. Plant J 66:877–889

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316:715–719

    CAS  PubMed  Google Scholar 

  • Kurkela S, Borg-Franck M (1992) Structure and expression of kin2, one of two cold- and ABA-induced genes of Arabidopsis thaliana. Plant Mol Biol 19:689–692

    CAS  PubMed  Google Scholar 

  • Leister D (2005) Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis. Gene 354:110–116

    CAS  PubMed  Google Scholar 

  • Lescot M, Dehais P, Thijs G, Marchal K (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li B, Li Q, Xiong L, Kronzucker HJ, Krämer U, Shi W (2012) Arabidopsis plastid AMOS1/EGY1 integrates abscisic acid signaling to regulate global gene expression response to ammonium stress. Plant Physiol 160:2040–2051

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lin C, Thomashow MF (1992) DNA sequence analysis of a complementary DNA for cold-regulated Arabidopsis gene COR15 and characterization of the COR15 polypeptide. Plant Physiol 99:519–525

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu D, Gong Q, Ma Y, Li P, Li J, Yang S, Yuan L, Yu Y, Pan D, Xu F, Wang NN (2010) cpSecA, a thylakoid protein translocase subunit, is essential for photosynthetic development in Arabidopsis. J Exp Bot 61:1655–1669

    CAS  PubMed  Google Scholar 

  • López-Juez E (2007) Plastid biogenesis, between light and shadows. J Exp Bot 58:11–26

    PubMed  Google Scholar 

  • Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J (2001) Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci USA 98:2053–2058

    CAS  PubMed Central  PubMed  Google Scholar 

  • Morris ER, Chevalier D, Walker JC (2006) DAWDLE, a forkhead-associated domain genes, regulates multiple aspects of plant development. Plant Physiol 141:932–941

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nott A, Jung HS, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol 57:739–759

    CAS  PubMed  Google Scholar 

  • Oelmuller R, Mohr H (1986) Photooxidative destruction of chloroplast and its consequences for expression of nuclear genes. Planta 167:106–113

    CAS  PubMed  Google Scholar 

  • Quesada V, Ponce MR, Micol JL (2000) Genetic analysis of salt-tolerant mutants in Arabidopsis thaliana. Genetics 154:421–436

    CAS  PubMed Central  PubMed  Google Scholar 

  • Roy LM, Barkan A (1998) A SecY homologue is required for the elaboration of the chloroplast thylakoid membrane and for normal chloroplast gene expression. J Cell Biol 141:385–395

    CAS  PubMed Central  PubMed  Google Scholar 

  • Seki M, Kamei A, Yamaguchi-Shinozaki K, Shinozaki K (2003) Molecular responses to drought, salinity and frost: common and different paths for plant protection. Curr Opin Biotechnol 14:194–199

    CAS  PubMed  Google Scholar 

  • Skalitzky CA, Martin JR, Harwood JH, Beirne JJ, Adamczyk BJ, Heck GR, Cline K, Fernandez DE (2011) Plastids contain a second Sec translocase system with essential functions. Plant Physiol 155:354–369

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Susek RE, Ausubel FM, Chory J (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74:787–799

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Thomsen B, Oelze-Karow H, Schuster C, Mohr H (1993) Stimulation of appearance of extraplastidic tetrapyrroles by a photooxidative treatment of the plastids. Photochem Photobiol 58:711–717

    CAS  Google Scholar 

  • Vothknecht UC, Westhoff P (2001) Biogenesis and origin of thylakoid membranes. BBA 1541:91–101

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Wang H, Ceorges F, Pelcher LE, Saleem M, Cutler AJ (1994) A 5.3-kilobase genomic fragment from Arabidopsis thaliana containing kin1 and cor6.6. Plant Physiol 104:291–292

    CAS  PubMed Central  PubMed  Google Scholar 

  • Waters MT, Langdale JA (2009) The making of a chloroplast. EMBO J 28:2861–2873

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Wu L, Zhou M, 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 169:1408–1416

    CAS  PubMed  Google Scholar 

  • Xiong L, Ishitani M, Lee H, Zhu JK (2001) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress. Plant Cell 13:2063–2083

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1993) Characterization of the expression of a desiccation-responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants. Mol Gen Genet 236:331–340

    CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    CAS  PubMed  Google Scholar 

  • Yan K, Shao H, Shao C, Chen P, Zhao S, Brestic M, Chen X (2013) Physiological adaptive mechanisms of plants grown in saline soil and implications for sustainable saline agriculture in coastal zone. Acta Physiol Plant 35:2867–2878

    CAS  Google Scholar 

  • Yu HD, Yang XF, Chen ST, Wang YT, Li JK, Shen Q, Liu XL, Guo FQ (2012) Downregulation of chloroplast RPS1 negatively modulates nuclear heat-responsive expression of HsfA2 and its target genes in Arabidopsis. PLoS Genet 8:e1002669

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang L, Gao Y, Pan H, Hu W, Zhang Q (2013) Cloning and characterisation of a Primula heat shock protein gene, PfHSP17.1, which confers heat, salt and drought tolerance in transgenic Arabidopsis thaliana. Acta Physiol Plant 35:3191–3200

    CAS  Google Scholar 

  • Zhou M, Wu L, Liang J, Shen C, Lin J (2012) Expression analysis and functional characterization of a novel cold-responsive gene CbCOR15a from Capsella bursa-pastoris. Mol Biol Rep 39:5169–5179

    CAS  PubMed  Google Scholar 

  • Zuther E, Schulz E, Childs LH, Hincha DK (2012) Clinal variation in the non-acclimated and cold-acclimated freezing tolerance of Arabidopsis thaliana accessions. Plant Cell Environ 35:1860–1878

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to give our great thanks to Mrs. Lixia Ma for technical assistance. We are also grateful to the anonymous reviewers for constructive suggestions. This work was supported by the National Natural Science Foundation of China (NSFC) (No. 31100185) and the Science Foundation of Jiangxi Provincial Education Department (No. GJJ12243) to Dong Liu.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dong Liu.

Additional information

Communicated by M. Prasad.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 67 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, D., Li, W., Cheng, J. et al. Expression analysis and functional characterization of a cold-responsive gene COR15A from Arabidopsis thaliana . Acta Physiol Plant 36, 2421–2432 (2014). https://doi.org/10.1007/s11738-014-1615-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-014-1615-8

Keywords

Navigation