Abstract
The translationally controlled tumor protein (TCTP) is an important component of the target of rapamycin (TOR) signaling pathway, the major regulator of cell growth in animals and fungi. Despite its relevance, knowledge on plant TCTP homologs is still limited. In the present study, the full-length BoTCTP cDNA was isolated from a cabbage (Brassica oleracea L.) cDNA library. The BoTCTP cDNA encodes a polypeptide of 168 amino acids and shared the highly conserved GTPase binding surface in all of the species analyzed. Northern blotting analysis showed that BoTCTP was specifically expressed in the root and stem. Furthermore, the expression of BoTCTP could be obviously enhanced by stress stimuli, including high temperature and salt stresses, while no significant changes in the BoTCTP expression were observed under ABA stress. Functional analysis of BoTCTP was performed by the silencing of BoTCTP using RNA interference (RNAi) and the BoTCTP RNAi plants exhibited reduced vegetative growth rate and decreased tolerance of the cold, high temperature, and salt stresses. The reported results clearly suggest that the BoTCTP gene is involved in the regulation of both growth and stress response in cabbage.
Similar content being viewed by others
References
Aoki K, Suzui N, Fujimaki S, Dohmae N, Yonekura-Sakakibara K, Fujiwara T, Hayashi H, Yamaya T, Sakakibara H (2005) Destination-selective long-distance movement of phloem proteins. Plant Cell 17:1801–1814
Berkowitz O, Jost R, Pollmann S, Masle J (2008) Characterization of TCTP, the translationally controlled tumor protein, from Arabidopsis thaliana. Plant Cell 20:3430–3447
Bommer UA, Thiele BJ (2004) The translationally controlled tumour protein (TCTP). Int J Biochem Cell Biol 36:379–385
Cans C, Passer BJ, Shalak V, Nancy-Portebois V, Crible V, Amzallag N, Allanic D, Tufino R, Argentini M, Moras D, Fiucci G, Goud B, Mirande M, Amson R, Telerman A (2003) Translationally controlled tumor protein acts as a guanine nucleotide dissociation inhibitor on the translation elongation factor eEF1A. Proc Natl Acad Sci USA 100:13892–13897
Cao B-H, Lei J-J, Song H-Y, Song M, Yang Z-H, Xiang C-B, Oliver DJ, Li D-Q (2002) cDNA library construction and identification of cabbage. Acta Horticulturae Sinica 29:579–580
Cao B-H, Lei J-J, Xiang C-B, Chen G-J, Zeng G-P, Oliver DJ, Zhao S, Lu L-L (2008) The function identification of the candidate disease-resistant gene in cabbage. Agric Sci China 7:101–105
Chapman HD, Pratt PF (1982) Methods of plant analysis. In: Methods of analysis for soils, plants and water. Chapman Publishers, Riverside
Chen SH, Wu PS, Chou CH, Yan YT, Liu H, Weng SY, Yang-Yen HF (2007) A knockout mouse approach reveals that TCTP functions as an essential factor for cell proliferation and survival in a tissue- or cell type-specific manner. Mol Biol Cell 18:2525–2532
Chitpatima ST, Makrides S, Bandyopadhyay R, Brawerman G (1988) Nucleotide sequence of a major messenger RNA for a 21 kilodalton polypeptide that is under translational control in mouse tumor cells. Nucleic Acids Res 16:2350
De Virgilio C, Loewith R (2006) Cell growth control: little eukaryotes make big contributions. Oncogene 25:6392–6415
Deprost D, Yao L, Sormani R, Moreau M, Leterreux G, Nicolaï M, Bedu M, Robaglia C, Meyer C (2007) The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Rep 8:864–870
Ermolayev V, Weschke W, Manteuffel R (2003) Comparison of Al-induced gene expression in sensitive and tolerant soybean cultivars. J Exp Bot 54:2745–2756
Gachet Y, Lee M, Sawitzki B, Tournier S, Poulton T, Bommer UA (1997) Intracellular colocalisation of the translationally controlled protein P23 with cytoskeletal structures. Biochem Soc Trans 25:269S
Gachet Y, Tournier S, Lee M, Lazaris-Karatzas A, Poulton T, Bommer UA (1999) The growth-related, translationally controlled protein P23 has properties of a tubulin binding protein and associates transiently with microtubules during the cell cycle. J Cell Sci 112:1257–1271
Hsu YC, Chern JJ, Cai Y, Liu M, Choi KW (2007) Drosophila TCTP is essential for growth and proliferation through regulation of dRheb GTPase. Nature 445:785–788
Ingram GC, Waites R (2006) Keeping it together: co-ordinating plant growth. Curr Opin Plant Biol 9:12–20
Itzen A, Pylypenko O, Goody RS, Alexandrov K, Rak A (2006) Nucleotide exchange via local protein unfolding—structure of Rab8 in complex with MSS4. EMBO J 25:1445–1455
John PC, Qi R (2008) Cell division and endoreduplication: doubtful engines of vegetative growth. Trends Plant Sci 13:121–127
Lee JY, Lee DH (2003) Use of serial analysis of gene expression technology to reveal changes in gene expression in Arabidopsis pollen undergoing cold stress. Plant Physiol 132:517–529
Li F, Zhang D, Fujise K (2001) Characterization of fortilin, a novel antiapoptotic protein. J Biol Chem 276:47542–47549
Liu H, Peng HW, Cheng YS, Yuan HS, Yang-Yen HF (2005) Stabilization and enhancement of the antiapoptotic activity of mcl-1 by TCTP. Mol Cell Biol 25:3117–3126
Lopez AP, Franco AR (2006) Cloning and expression of cDNA encoding translationally controlled tumor protein from strawberry fruits. Biol Plantarum 50:447–449
Rual JF, Ceron J, Koreth J, Hao T, Nicot AS, Hirozane-Kishikawa T, Vandenhaute J, Orkin SH, Hill DE, van den Heuvel S, Vidal M (2004) Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res 14:2162–2168
Sage-Ono K, Ono M, Harada H, Kamada H (1998) Dark-induced accumulation of mRNA for a homolog of translationally controlled tumor protein (TCTP) in Pharbitis. Plant Cell Physiol 39:357–360
Sánchez JC, Schaller D, Ravier F, Golaz O, Jaccoud S, Belet M, Wilkins MR, James R, Deshusses J, Hochstrasser D (1997) Translationally controlled tumor protein: a protein identified in several nontumoral cells including erythrocytes. Electrophoresis 18:150–155
Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37:501–506
Sönnichsen B, Koski LB, Walsh A, Marschall P, Neumann B, Brehm M, Alleaume AM, Artelt J, Bettencourt P, Cassin E, Hewitson M, Holz C, Khan M, Lazik S, Martin C, Nitzsche B, Ruer M, Stamford J, Winzi M, Heinkel R, Röder M, Finell J, Häntsch H, Jones SJM, Jones M, Piano F, Gunsalus KC, Oegema K, Gönczy P, Coulson A, Hyman AA, Echeverri CJ (2005) Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434:462–469
Sprunck S, Baumann U, Edwards K, Langridge P, Dresselhaus T (2005) The transcript composition of egg cells changes significantly following fertilization in wheat (Triticum aestivum L.). Plant J 41:660–672
Stürzenbaum SR, Kille P, Morgan AJ (1998) Identification of heavy metal induced changes in the expression patterns of the translationally controlled tumour protein (TCTP) in the Earthworm Lumbricus rubellus. Biochim Biophys Acta 1398:294–304
Thaw P, Baxter NJ, Hounslow AM, Price C, Waltho JP, Craven CJ (2001) Structure of TCTP reveals unexpected relationship with guanine nucleotide-free chaperones. Nat Struct Biol 8:701–704
Tuynder M, Susini L, Prieur S, Besse S, Fiucci G, Amson R, Telerman A (2002) Biological models and genes of tumor reversion: cellular reprogramming through tpt1/TCTP and SIAH-1. Proc Natl Acad Sci USA 99:14976–14981
Ulrich-Axel B, Bernd-Joachim T (2004) Molecules in focus. The translationally controlled tumour protein (TCTP). Int J Biochem Cell Biol 36:379–385
Veena, Jiang H, Doerge RW, Gelvin SB (2003) Transfer of T-DNA and Vir proteins to plant cells by Agrobacterium tumefaciens induces expression of host genes involved in mediating transformation and suppresses host defense gene expression. Plant J 35:219–236
Vernoud V, Horton AC, Yang Z, Nielsen E (2003) Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol 131:1191–1208
Vincent D, Ergül A, Bohlman MC, Tattersall EAR, Tillett RL, Wheatley MD, Woolsey R, Quilici DR, Joets J, Schlauch K, Schooley DA, Cushman JC, Cramer GR (2007) Proteomic analysis reveals differences between Vitis vinifera L. cv. Chardonnay and cv. Cabernet Sauvignon and their responses to water deficit and salinity. J Exp Bot 58:1873–1892
Woo HH, Hawes MC (1997) Cloning of genes whose expression is correlated with mitosis and localized in dividing cells in root caps of Pisum sativum L. Plant Mol Biol 35:1045–1051
Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124:471–484
Yarm FR (2002) Plk phosphorylation regulates the microtubule-stabilizing protein TCTP. Mol Cell Biol 22:6209–6221
Acknowledgments
This work was financially supported in part by grants from the National Natural Science Foundation of China (30871716).
Author information
Authors and Affiliations
Corresponding author
Additional information
Bihao Cao and Yaqing Lu contributed equally to this work.
Rights and permissions
About this article
Cite this article
Cao, B., Lu, Y., Chen, G. et al. Functional characterization of the translationally controlled tumor protein (TCTP) gene associated with growth and defense response in cabbage. Plant Cell Tiss Organ Cult 103, 217–226 (2010). https://doi.org/10.1007/s11240-010-9769-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11240-010-9769-6