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

• Autorzy: Liu D. , Li W. , Cheng J. , Hou L.
• Języki publikacji: EN

Abstrakty

EN

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.

Słowa kluczowe

EN

functional characteristics; cold response; COR15A gene; Arabidopsis thaliana; chloroplast; functionality; salt stress; osmotic stress

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2014
• Tom: 36
• Numer: 09
• Opis fizyczny: p.2421-2432,fig.,ref.

Twórcy

autor

Liu D.

• College of Agronomy, Jiangxi Agricultural University, 330045 Nanchang, China

autor

Li W.

• College of Agronomy, Jiangxi Agricultural University, 330045 Nanchang, China

autor

Cheng J.

• College of Agronomy, Jiangxi Agricultural University, 330045 Nanchang, China

autor

Hou L.

• College of Agronomy, Jiangxi Agricultural University, 330045 Nanchang, China

Bibliografia

• Alonso JM, Stepanova AN, Leisse TJ et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657
• 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
• 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
• 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
• 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
• Cattivelli L, Bartels D (1990) Molecular cloning and characterization of cold-regulated genes in barley. Plant Physiol 93:1504–1510
• 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
• Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
• 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
• 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
• 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
• Fernández AP, Strand A (2008) Retrograde signaling and plant stress: plastid signals initiate cellular stress responses. Curr Opin Plant Biol 11:509–513
• Gilmour SJ, Thomashow MF (1991) Cold acclimation and cold-regulated gene expression in ABA mutants of Arabidopsis thaliana. Plant Mol Biol 17:1233–1240
• 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
• Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genom 9:118
• Inaba T, Schnell DJ (2008) Protein trafficking to plastids: one theme, many variations. Biochem J 413:15–28
• Jefferson RA (1989) The GUS reporter gene system. Nature 342:837–838
• 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
• 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
• 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
• 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
• 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
• 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
• Leister D (2005) Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis. Gene 354:110–116
• 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
• 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
• 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
• 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
• López-Juez E (2007) Plastid biogenesis, between light and shadows. J Exp Bot 58:11–26
• 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
• Morris ER, Chevalier D, Walker JC (2006) DAWDLE, a forkhead-associated domain genes, regulates multiple aspects of plant development. Plant Physiol 141:932–941
• 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
• Nott A, Jung HS, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol 57:739–759
• Oelmuller R, Mohr H (1986) Photooxidative destruction of chloroplast and its consequences for expression of nuclear genes. Planta 167:106–113
• Quesada V, Ponce MR, Micol JL (2000) Genetic analysis of salttolerant mutants in Arabidopsis thaliana. Genetics 154:421–436
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• Vothknecht UC, Westhoff P (2001) Biogenesis and origin of thylakoid membranes. BBA 1541:91–101
• 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
• 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
• Waters MT, Langdale JA (2009) The making of a chloroplast. EMBO J 28:2861–2873
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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

Identyfikatory

DOI

10.1007/s11738-014-1615-8