Skip to main content
SpringerLink
Log in

Molecular cloning, phylogenetic analysis, and expression profiling of a grape CMP-sialic acid transporter-like gene induced by phytohormone and abiotic stress

  • Research Article
  • Published:
Genes & Genomics Aims and scope Submit manuscript

Abstract

Nucleotide sugars are synthesized in the cytosol and nucleus and transported into the lumen of the endoplasmic reticulum and the Golgi apparatus via nucleotide sugar transporters (NSTs). Because NSTs exhibit high similarities with triose phosphate translocators (TPTs), they are classified into the NST/TPT superfamily. Here, we identified 38 members of the NST/TPT family by screening the grapevine genome and proteome 12× database. Vitis vinifera NST/TPT proteins can be classified into two groups on the basis of their phylogenetic relationships. From these, we isolated a full-length cDNA encoding a putative NST and named it VvCSTLP1. VvCSTLP1 comprises 15 exons and 14 introns and exhibits high similarities with OsCSTLP2. A search for cis-regulatory elements in the promoter region of VvCSTLP1 revealed that this protein is probably regulated by phytohormones and abiotic stresses. The VvCSTLP1 cDNA encodes an open reading frame of 1065 bp, and the predicted polypeptide is 354 amino acids long with a molecular mass of 39.11 kDa. Expression of VvCSTLP1 was elevated during early berry development, and dramatically decreased after the initiation of ripening. VvCSTLP1 was highly expressed in old leaves and mature leaves, and at low levels in young leaves, pollen, roots, and tendrils. Finally, VvCSTLP1 expression was induced in response to 1-naphthaleneacetic acid, salicylic acid (SA), and boric acid treatments, but was decreased by drought stress. The regulation of VvCSTLP1 expression led us to conclude that it may play a role in cell wall composition and structure and in the cross-talk between the auxin, SA, and abiotic stress signaling pathways.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abeijon C, Robbins PW, Hirschberg CB (1996) Molecular cloning of the Golgi apparatus uridine diphosphate-N-acetylglucosamine transporter from Kluyveromyces lactis. Proc Natl Acad Sci USA 93:5963–5968

    Article  PubMed  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Aoki K, Ishida N, Kawakita M (2001) Substrate recognition by UDP-galactose and CMPsialic acid transporters. Different sets of transmembrane helices are utilized for the specific recognition of UDP-galactose and CMP-sialic acid. J Biol Chem 276:21555–21561

    Article  PubMed  CAS  Google Scholar 

  • Aoki K, Ishida N, Kawakita M (2003) Substrate recognition by nucleotide sugar transporters: further characterization of substrate recognition regions by analyses of UDP galactose/CMP-sialic acid transporter chimeras and biochemical analysis of the substrate specificity of parental and chimeric transporters. J Biol Chem 278:22887–22893

    Article  PubMed  CAS  Google Scholar 

  • Bakker H, Routier F, Oelmann S, Jordi W, Lommen A, Gerardy-Schahn R, Bosch D (2005) Molecular cloning of two Arabidopsis UDP-galactose transporters by complementation of a deficient Chinese hamster ovary cell line. Glycobiology 15:193–201

    Article  PubMed  CAS  Google Scholar 

  • Bakker H, Routier F, Ashikov A, Neumann D, Bosch D, Gerardy-Schahn R (2008) A CMP-sialic acid transporter cloned from Arabidopsis thaliana. Carbohydr Res 343:2148–2152

    Article  PubMed  CAS  Google Scholar 

  • Bakker H, Oka T, Ashikov A, Yadav A, Berger M, Rana NA, Bai X, Jigami Y, Haltiwanger RS, Esko JD, Gerardy-Schahn R (2009) Functional UDP-xylose transport across the endoplasmic reticulum/Golgi membrane in a Chinese hamster ovary cell mutant defective in UDP-xylose Synthase. J Biol Chem 284:2576–2583

    Article  PubMed  CAS  Google Scholar 

  • Baldwin TC, Handford MG, Yuseff MI, Orellana A, Dupree P (2001) Identification and characterization of GONST1, a Golgi-localized GDP mannose transporter in Arabidopsis. Plant Cell 13:2283–2295

    PubMed  CAS  Google Scholar 

  • Berninsone PM, Hirschberg CB (2000) Nucleotide sugar transporters of the Golgi apparatus. Curr Opin Struct Biol 10:542–547

    Article  PubMed  CAS  Google Scholar 

  • Berninsone PM, Hwang HY, Zemtseva I, Horvitz HR, Hirschberg CB (2001) SQV-7, a protein involved in Caenorhabditis elegans epithelial invagination and early embryogenesis, transports UDP-glucuronic acid, UDP-N-acetyl galactosamine, and UDP-galactose. Proc Natl Acad Sci USA 98:3738–3743

    Article  PubMed  CAS  Google Scholar 

  • Böttcher C, Keyzers RA, Boss PK, Davies C (2010) Sequestration of auxin by the indole-3-acetic acid-amido synthetase GH3-1 in grape berry (Vitis vinifera L.) and the proposed role of auxin conjugation during ripening. J Exp Bot 61:3615–3625

    Article  PubMed  Google Scholar 

  • Burget EG, Verma R, Mølhøj M, Reiter W-D (2003) The biosynthesis of l-arabinose in plants: molecular cloning and characterization of a Golgi-localized UDP-d-xylose 4-epimerase encoded by the MUR4 gene of Arabidopsis. Plant Cell 15:523–531

    Article  PubMed  CAS  Google Scholar 

  • Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344:1879–1900

    Article  PubMed  CAS  Google Scholar 

  • Capasso JM, Hirschberg CB (1984) Effect of nucleotides on translocation of sugar nucleotides and adenosine 3′-phosphate 5′-phosphosulfate into Golgi apparatus vesicles. Biochim Biophys Acta 777:133–139

    Article  PubMed  CAS  Google Scholar 

  • Cawton DL, Morris JR (1982) Relationship of seed number and maturity to berry development, fruit maturation, hormonal changes, and uneven ripening of ‘Concord’ (Vitis labrusca L.) grapes. J Am Soc Hortic Sci 107:1099–1104

    Google Scholar 

  • Cervilla CM, Blasco B, Rios JJ, Romero L, Ruiz JM (2007) Oxidative stress and antioxidants in tomato (Solanum lycopersicum) plants subjected to boron toxicity. Ann Bot 100:747–756

    Article  PubMed  CAS  Google Scholar 

  • Daskalova SM, Pah AR, Baluch DP, Lopez LC (2009) The Arabidopsis thaliana putative sialyltransferase resides in the Golgi apparatus but lacks the ability to transfer sialic acid. Plant Biol 11:284–299

    Article  PubMed  CAS  Google Scholar 

  • Davies C, Robinson SP (1996) Sugar accumulation in grape berries (cloning of two putative vacuolar invertase cDNAs and their expression in grapevine tissues). Plant Physiol 111:275–283

    Article  PubMed  CAS  Google Scholar 

  • Descoteaux A, Luo Y, Turco SJ, Beverley SM (1995) A specialized pathway affecting virulence glycoconjugates of Leishmania. Science 269:1869–1872

    Article  PubMed  CAS  Google Scholar 

  • Eckhardt M, Muhlenhoff M, Bethe A, Gerardy-Schahn R (1996) Expression cloning of the Golgi CMP-sialic acid transporter. Proc Natl Acad Sci USA 93:7572–7576

    Article  PubMed  CAS  Google Scholar 

  • Eckhardt M, Gotza B, Gerardy-Schahn R (1999) Membrane topology of the mammalian CMP-sialic acid transporter. J Biol Chem 274:8779–8787

    Article  PubMed  CAS  Google Scholar 

  • Edwards R (1994) Conjugation and metabolism of salicylic acid in tobacco. J Plant Physiol 143:609–614

    Article  CAS  Google Scholar 

  • Enyedi AJ, Raskin I (1993) Induction of UDP-glucose:salicylic acid glucosyltransferase activity in tobacco mosaic virus-inoculated tobacco (Nicotiana tabacum) leaves. Plant Physiol 101(4):1375–1380

    PubMed  CAS  Google Scholar 

  • Findeklee P, Goldbach HE (1996) Rapid effects of boron deficiency on cell wall elasticity modulus in Cucurbita pepo roots. Botanica Acta 109:463–465

    CAS  Google Scholar 

  • Garcia O, Bouige P, Forestier C, Dassa E (2004) Inventory and comparative analysis of rice and Arabidopsis ATP-binding cassette (ABC) systems. J Mol Biol 343:249–265

    Article  PubMed  CAS  Google Scholar 

  • Gerardy-Schahn R, Oelmann S, Bakker H (2001) Nucleotide sugar transporters: biological and functional aspects. Biochimie 83:775–782

    Article  PubMed  CAS  Google Scholar 

  • Goto S, Taniguchi M, Muraoka M, Toyoda H, Sado Y, Kawakita M, Hayashi S (2002) UDP-sugar transporter implicated in glycosylation and processing of Notch. Nat Cell Biol 3:816–822

    Article  Google Scholar 

  • Guillen E, Abeijon C, Hirschberg CB (1998) Mammalian Golgi apparatus UDP-N-acetylglucosamine transporter: molecular cloning by phenotypic correction of a yeast mutant. Proc Natl Acad Sci USA 95:7888–7892

    Article  PubMed  CAS  Google Scholar 

  • Han S, Tang N, Jiang H-X, Yang L-T, Li Y, Chen L-S (2009) CO2 assimilation, photosystem II photochemistry, carbohydrate metabolism and antioxidant system of citrus leaves in response to boron stress. Plant Sci 176:143–153

    Article  CAS  Google Scholar 

  • Hirsch AM, Torrey JG (1980) Ultrastructural changes in sunflower root cells in relation to boron deficiency and added auxin. Can J Bot 58:856–866

    Article  CAS  Google Scholar 

  • Hirschberg CB, Robbins PW, Abeijon C (1998) Transporters of nucleotide sugars, ATP, and nucleotide sulfate in the endoplasmic reticulum and Golgi apparatus. Annu Rev Biochem 67:49–69

    Article  PubMed  CAS  Google Scholar 

  • Hong K, Ma D, Beverley SM, Turco SJ (2000) The Leishmania GDP-mannose transporter is an autonomous, multi-specific, hexameric complex of LPG2 subunits. Biochem 39:2013–2022

    Article  CAS  Google Scholar 

  • Hu H, Brown PH (1994) Localization of boron in cell walls of squash and tobacco and its association with pectin. Plant Physiol 105:681–689

    PubMed  CAS  Google Scholar 

  • Hu H, Brown PH, Labavitch JH (1996) Species variability in boron requirement is correlated with cell wall pectin. J Exp Bot 47:227–232

    Article  CAS  Google Scholar 

  • Inaba A, Ishida M, Sobajima Y (1976) Changes in endogenous hormone concentrations during berry development in relation to ripening of Delaware grapes. J Jpn Soc Hortic Sci 45:245–252

    Article  Google Scholar 

  • Ishida N, Miura N, Yoshioka S, Kawakita M (1996) Molecular cloning and characterization of a novel isoform of the human UDP-galactose transporter, and of related complementary DNAs belonging to the nucleotide-sugar transporter gene family. J Biochem 120:1074–1078

    Article  PubMed  CAS  Google Scholar 

  • Kainuma M, Chiba Y, Takeuchi M, Jigami Y (2001) Overexpression of HUT1 gene stimulates in vivo galactosylation by enhancing UDP-galactose transport activity in Saccharomyces cerevisiae. Yeast 18:533–541

    Article  PubMed  CAS  Google Scholar 

  • Knappe S, Flügge U-I, Fischer K (2003) Analysis of the plastidic phosphate translocator gene family in Arabidopsis and identification of new phosphate translocator-homologous transporters, classified by their putative substrate-binding site. Plant Physiol 131:1178–1190

    Article  PubMed  CAS  Google Scholar 

  • Kouchi H, Kumazawa K (1976) Anatomical responses of root tips to boron deficiency. III. Effect of boron deficiency on sub-cellular structure of root tips, particularly on morphology of cell wall and its related organelles. Soil Sci Plant Nutr 22:53–71

    Article  CAS  Google Scholar 

  • Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Briefings in Bioinformatics. 9:299–306

    Article  PubMed  CAS  Google Scholar 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132

    Article  PubMed  CAS  Google Scholar 

  • Lee H-I, Raskin I (1998) Glucosylation of salicylic acid in Nicotiana tabacum cv. Xanthi-nc. Phytopathology 88:692–697

    Article  PubMed  CAS  Google Scholar 

  • Loomis WD, Durst RW (1991) Boron and cell walls. In: Randall DD, Blevins DG, Miles CD (eds) Current topics in plant biochemistry and physiology, vol 10. University of Missouri, Columbia, pp 149–178

    Google Scholar 

  • Ma D, Russell DG, Beverley SM, Turco SJ (1997) Golgi GDP-mannose uptake requires Leishmania LPG2. A member of a eukaryotic family of putative nucleotide-sugar transporters. J Biol Chem 272:3799–3805

    Article  PubMed  CAS  Google Scholar 

  • Martinez-Duncker I, Mollicone R, Codogno P, Oriol R (2003) The nucleotide-sugar transporter family: a phylogenetic approach. Biochimie 85:245–260

    Article  PubMed  CAS  Google Scholar 

  • Matoh T, Ishigaki K, Mizutani M, Matsunaga W, Takabe K (1992) Boron nutrition of cultured tobacco BY-2 cells. I. Requirement for and intracellular localization of boron and selection of cells that tolerate low levels of boron. Plant Cell Physiol 33:1135–1141

    CAS  Google Scholar 

  • Molhoj M, Verma R, Reiter WD (2004) The biosynthesis of d-galacturonate in plants. Functional cloning and characterization of a membrane-anchored UDP-d-glucuronate 4-epimerase from Arabidopsis. Plant Physiol 135:1221–1230

    Article  PubMed  CAS  Google Scholar 

  • Münster AK, Eckhardt M, Potvin B, Muhlenhoff M, Stanley P, Gerardy-Schahn R (1998) Mammalian cytidine 50-monophosphate N-acetylneuraminic acid synthetase: a nuclear protein with evolutionarily conserved structural motifs. Proc Natl Acad Sci USA 95:9140–9145

    Article  PubMed  Google Scholar 

  • Muraoka M, Kawakita M, Ishida N (2001) Molecular characterization of human UDP glucuronic acid/UDP-N-acetylgalactosamine transporter, a novel nucleotide sugar transporter with dual substrate specificity. FEBS Lett 495:87–93

    Article  PubMed  CAS  Google Scholar 

  • Nagels B, Van Damme EJM, Pabst M, Callewaert N, Weterings K (2011) Production of complex multiantennary N-glycans in Nicotiana benthamiana plants. Plant Physiol 155:1103–1112

    Article  PubMed  CAS  Google Scholar 

  • Nakanishi H, Nakayama K, Yokota A, Tachikawa H, Takahashi N, Jigami Y (2001) Hut1 proteins identified in Saccharomyces cerevisiae and Schizosaccharomyces pombe are functional homologues involved in the protein-folding process at the endoplasmic reticulum. Yeast 18:543–554

    Article  PubMed  CAS  Google Scholar 

  • Norambuena L, Marchant L, Berninsone P, Hirschberg CB, Silva H, Orellana A (2002) Transport of UDP-galactose in plants. Identification and functional characterization of AtUTr1, an Arabidopsis thaliana UDP galactose/UDP-glucose transporter. J Biol Chem 277:32923–32929

    Article  PubMed  CAS  Google Scholar 

  • Norambuena L, Nilo R, Handford M, Reyes F, Marchant L, Meisel L, Orellana A (2005) AtUTr2 is an Arabidopsis thaliana nucleotide sugar transporter located in the Golgi apparatus capable of transporting UDP-galactose. Planta 222:521–529

    Article  PubMed  CAS  Google Scholar 

  • O’Neill MA, Ishii T, Albersheim P, Darvill AG (2004) Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annu Rev Plant Biol 55:109–139

    Article  PubMed  Google Scholar 

  • Oriol R, Martinez-Duncker I, Chantret I, Mollicone R, Codogno P (2002) Common origin and evolution of glycosyltransferases using Dol-P-monosaccharides as donor substrates. Mol Biol Evol 19:1451–1463

    Article  PubMed  CAS  Google Scholar 

  • Reyes F, León G, Donoso M, Brandizzí F, Weber APM, Orellana A (2010) The nucleotide sugar transporters AtUTr1 and AtUTr3 are required for the incorporation of UDP-glucose into the endoplasmic reticulum, are essential for pollen development and are needed for embryo sac progress in Arabidopsis thaliana. Plant J 61:423–435

    Article  PubMed  CAS  Google Scholar 

  • Roy SK, Chiba Y, Takeuchi M, Jigami Y (2000) Characterization of Yeast Yea4p, a uridine diphosphate-N-acetylglucosamine transporter localized in the endoplasmic reticulum and required for chitin synthesis. J Biol Chem 275:13580–13587

    Article  PubMed  CAS  Google Scholar 

  • Segawa H, Soares RP, Kawakita M, Beverley SM, Turco SJ (2005) Reconstitution of GDP-mannose transport activity with purified Leishmania LPG2 protein in liposomes. J Biol Chem 280:2028–2035

    Article  PubMed  CAS  Google Scholar 

  • Seino J, Ishii K, Nakano T, Ishida N, Tsujimoto M, Hashimoto Y, Takashima S (2010) Characterization of rice nucleotide sugar transporters capable of transporting UDP-galactose and UDP-glucose. J Biochem 148:35–46

    Article  PubMed  CAS  Google Scholar 

  • Seitz B, Klos C, Wurm M, Tenhaken R (2000) Matrix polysaccharide precursor in Arabidopsis cell wall are synthesized by alternate pathways with organ-specific expression patterns. Plant J 21:537–546

    Article  PubMed  CAS  Google Scholar 

  • Selva EM, Hong K, Baeg GH, Beverley SM, Turco SJ, Perrimon N, Hacker U (2001) Dual role of the fringe connection gene in both heparan sulphate and fringe-dependent signalling events. Nat Cell Biol 3:809–815

    Article  PubMed  CAS  Google Scholar 

  • Seveno M, Bardor M, Paccalet T, Gomord V, Lerouge P, Faye L (2004) Glycoprotein sialylation in plants? Nat Biotechnol 22:1351–1352

    Article  PubMed  CAS  Google Scholar 

  • Shah MM, Fujiyama K, Flynn CR, Joshi L (2003) Sialylated endogenous glycoconjugates in plant cells. Nat Biotechnol 21:1470–1471

    Article  PubMed  CAS  Google Scholar 

  • Tabuchi M, Tanaka N, Iwahara S, Takegawa K (1997) The Schizosaccharomyces pombe gms1+ gene encodes an UDP-galactose transporter homologue required for protein galactosylation. Biochem Biophys Res Commun 232:121–125

    Article  PubMed  CAS  Google Scholar 

  • Takashima S, Abe T, Yoshida S, Kawahigashi H, Saito T, Tsuji S, Tsujimoto M (2006) Analysis of sialyltransferase-like proteins from Oryza sativa. J Biochem 139:279–287

    Article  PubMed  CAS  Google Scholar 

  • Takashima S, Seino J, Nakano T, Fujiyama K, Tsujimoto M, Ishida N, Hashimoto Y (2009) Analysis of CMP-sialic acid transporter-like proteins in plants. Phytochemistry 70:1973–1981

    Article  PubMed  CAS  Google Scholar 

  • Xiao H, Nassuth A (2006) Stress- and development-induced expression of spliced and unspliced transcripts from two highly similar dehydrin 1 genes in V. riparia and V. vinifera. Plant Cell Rep 25:968–977

    Article  PubMed  CAS  Google Scholar 

  • Yuan Z, Teasdale RD (2002) Prediction of Golgi Type II membrane proteins based on their transmembrane domains. Bioinformatics 18:1109–1115

    Article  PubMed  CAS  Google Scholar 

  • Zeleny R, Kolarich D, Strasser R, Altmann F (2006) Sialic acid concentrations in plants are in the range of inadvertent contamination. Planta 5:1–6

    Google Scholar 

  • Zhang X, Luo G, Wang R, Wang J, Himelrick D (2003) Growth and development responses of seeded and seedless grape berries to shoot girdling. J Am Soc Hortic Sci 128:316–323

    Google Scholar 

  • Zhang B, Liu X, Qian Q, Liu L, Dong G, Xiong G, Zeng D, Zhou Y (2011) Golgi nucleotide sugar transporter modulates cell wall biosynthesis and plant growth in rice. Proc Natl Acad Sci USA 108:5110–5115

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a TUBITAK (The Scientific and Technological Research Council of Turkey) Grant (107O687).

Author information

Authors and Affiliations

  1. Department of Horticulture, Faculty of Agriculture, Ege University, Izmir, Turkey

    Birsen Çakır

  2. Department of Horticulture, Graduate School of Natural and Applied Sciences, Ege University, Izmir, Turkey

    Ahmet Can Olcay

Authors
  1. Birsen Çakır
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ahmet Can Olcay
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Birsen Çakır.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 156 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Çakır, B., Olcay, A.C. Molecular cloning, phylogenetic analysis, and expression profiling of a grape CMP-sialic acid transporter-like gene induced by phytohormone and abiotic stress. Genes Genom 35, 225–238 (2013). https://doi.org/10.1007/s13258-013-0074-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13258-013-0074-8

Keywords

Search

Navigation