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

다국어 초록 (Multilingual 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 129 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 14introns and exhibits high similarities with OsCSTLP2.
Asearch 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, VvCSTLP1expression was induced in response to 1-naphthaleneacetic acid, salicylic acid (SA), and boric acid treatments, but was decreased by drought stress. The regulation of VvCSTLP1expression 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.

참고문헌 (Reference)

1 Hirsch AM, "Ultrastructural changes in sunflower root cells in relation to boron deficiency and added auxin" 58 : 856-866, 1980

2 Goto S, "UDP-sugar transporter implicated in glycosylation and processing of Notch" 3 : 816-822, 2002

3 Hirschberg CB, "Transporters of nucleotide sugars, ATP, and nucleotide sulfate in the endoplasmic reticulum and Golgi apparatus" 67 : 49-69, 1998

4 Norambuena L, "Transport of UDP-galactose in plants. Identi- fication and functional characterization of AtUTr1, an Arabidopsis thaliana UDP galactose/UDP-glucose transporter" 277 : 32923-32929, 2002

5 Caffall KH, "The structure, function, and biosynthesis of plant cell wall pectic polysaccharides" 344 : 1879-1900, 2009

6 Martinez-Duncker I, "The nucleotide-sugar transporter family: a phylogenetic approach" 85 : 245-260, 2003

7 Reyes F, "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" 61 : 423-435, 2010

8 Burget EG, "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" 15 : 523-531, 2003

9 Molhoj M, "The biosynthesis of D-galacturonate in plants. Functional cloning and characterization of a membrane-anchored UDP-D-glucuronate 4-epimerase from Arabidopsis" 135 : 1221-1230, 2004

10 Tabuchi M, "The Schizosaccharomyces pombe gms1? gene encodes an UDPgalactose transporter homologue required for protein galactosylation" 232 : 121-125, 1997

11 Hong K, "The Leishmania GDPmannose transporter is an autonomous, multi-specific, hexameric complex of LPG2 subunits" 39 : 2013-2022, 2000

12 Daskalova SM, "The Arabidopsis thaliana putative sialyltransferase resides in the Golgi apparatus but lacks the ability to transfer sialic acid" 11 : 284-299, 2009

13 Davies C, "Sugar accumulation in grape berries (cloning of two putative vacuolar invertase cDNAs and their expression in grapevine tissues)" 111 : 275-283, 1996

14 Aoki K, "Substrate recognition by nucleotide sugar transporters: further characterization of substrate recognition regions by analyses of UDP galactose/CMPsialic acid transporter chimeras and biochemical analysis of the substrate specificity of parental and chimeric transporters" 278 : 22887-22893, 2003

15 Aoki K, "Substrate recognition by UDPgalactose and CMPsialic acid transporters. Different sets of transmembrane helices are utilized for the specific recognition of UDP-galactose and CMP-sialic acid" 276 : 21555-21561, 2001

16 Xiao H, "Stress- and development-induced expression of spliced and unspliced transcripts from two highly similar dehydrin 1 genes in V. riparia and V. vinifera" 25 : 968-977, 2006

17 Hu H, "Species variability in boron requirement is correlated with cell wall pectin" 47 : 227-232, 1996

18 Shah MM, "Sialylated endogenous glycoconjugates in plant cells" 21 : 1470-1471, 2003

19 Zeleny R, "Sialic acid concentrations in plants are in the range of inadvertent contamination" 5 : 1-6, 2006

20 Bӧttcher C, "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" 61 : 3615-3625, 2010

21 Berninsone PM, "SQV-7, a protein involved in Caenorhabditis elegans epithelial invagination and early embryogenesis, transports UDP-glucuronic acid, UDP-N-acetyl galactosamine, and UDPgalactose" 98 : 3738-3743, 2001

22 O’Neill MA, "Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide" 55 : 109-139, 2004

23 Cawton DL, "Relationship of seed number and maturity to berry development, fruit maturation, hormonal changes, and uneven ripening of ‘Concord’ (Vitis labrusca L.) grapes" 107 : 1099-1104, 1982

24 Segawa H, "Reconstitution of GDP-mannose transport activity with purified Leishmania LPG2 protein in liposomes" 280 : 2028-2035, 2005

25 Findeklee P, "Rapid effects of boron deficiency on cell wall elasticity modulus in Cucurbita pepo roots" 109 : 463-465, 1996

26 Nagels B, "Production of complex multiantennary N-glycans in Nicotiana benthamiana plants" 155 : 1103-1112, 2011

27 Yuan Z, "Prediction of Golgi Type II membrane proteins based on their transmembrane domains" 18 : 1109-1115, 2002

28 Cervilla CM, "Oxidative stress and antioxidants in tomato (Solanum lycopersicum) plants subjected to boron toxicity" 100 : 747-756, 2007

29 Kainuma M, "Overexpression of HUT1 gene stimulates in vivo galactosylation by enhancing UDP-galactose transport activity in Saccharomyces cerevisiae" 18 : 533-541, 2001

30 Gerardy-Schahn R, "Nucleotide sugar transporters: biological and functional aspects" 83 : 775-782, 2001

31 Berninsone PM, "Nucleotide sugar transporters of the Golgi apparatus" 10 : 542-547, 2000

32 Bakker H, "Molecular cloning of two Arabidopsis UDP-galactose transporters by complementation of a deficient Chinese hamster ovary cell line" 15 : 193-201, 2005

33 Abeijon C, "Molecular cloning of the Golgi apparatus uridine diphosphate-N-acetylglucosamine transporter from Kluyveromyces lactis" 93 : 5963-5968, 1996

34 Ishida N, "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" 120 : 1074-1078, 1996

35 Muraoka M, "Molecular characterization of human UDP glucuronic acid/UDP-N-acetylgalactosamine transporter, a novel nucleotide sugar transporter with dual substrate specificity" 495 : 87-93, 2001

36 Eckhardt M, "Membrane topology of the mammalian CMP-sialic acid transporter" 274 : 8779-8787, 1999

37 Seitz B, "Matrix polysaccharide precursor in Arabidopsis cell wall are synthesized by alternate pathways with organ-specific expression patterns" 21 : 537-546, 2000

38 Münster AK, "Mammalian cytidine 50-monophosphate N-acetylneuraminic acid synthetase: a nuclear protein with evolutionarily conserved structural motifs" 95 : 9140-9145, 1998

39 Guillen E, "Mammalian Golgi apparatus UDP-N-acetylglucosamine transporter: molecular cloning by phenotypic correction of a yeast mutant" 95 : 7888-7892, 1998

40 Kumar S, "MEGA: a biologistcentric software for evolutionary analysis of DNA and protein sequences" 9 : 299-306, 2008

41 Hu H, "Localization of boron in cell walls of squash and tobacco and its association with pectin" 105 : 681-689, 1994

42 Garcia O, "Inventory and comparative analysis of rice and Arabidopsis ATP-binding cassette (ABC) systems" 343 : 249-265, 2004

43 Enyedi AJ, "Induction of UDP-glucose:salicylic acid glucosyltransferase activity in tobacco mosaic virus-inoculated tobacco (Nicotiana tabacum) leaves" 101 (101): 1375-1380, 1993

44 Baldwin TC, "Identification and characterization of GONST1, a Golgi-localized GDP mannose transporter in Arabidopsis" 13 : 2283-2295, 2001

45 Nakanishi H, "Hut1 proteins identified in Saccharomyces cerevisiae and Schizosaccharomyces pombe are functional homologues involved in the protein-folding process at the endoplasmic reticulum" 18 : 543-554, 2001

46 Zhang X, "Growth and development responses of seeded and seedless grape berries to shoot girdling" 128 : 316-323, 2003

47 Zhang B, "Golgi nucleotide sugar transporter modulates cell wall biosynthesis and plant growth in rice" 108 : 5110-5115, 2011

48 Ma D, "Golgi GDPmannose uptake requires Leishmania LPG2. A member of a eukaryotic family of putative nucleotide-sugar transporters" 272 : 3799-3805, 1997

49 Seveno M, "Glycoprotein sialylation in plants?" 22 : 1351-1352, 2004

50 Lee H-I, "Glucosylation of salicylic acid in Nicotiana tabacum cv. Xanthi-nc" 88 : 692-697, 1998

51 Bakker H, "Functional UDP-xylose transport across the endoplasmic reticulum/Golgi membrane in a Chinese hamster ovary cell mutant defective in UDP-xylose Synthase" 284 : 2576-2583, 2009

52 Eckhardt M, "Expression cloning of the Golgi CMP-sialic acid transporter" 93 : 7572-7576, 1996

53 Capasso JM, "Effect of nucleotides on translocation of sugar nucleotides and adenosine 30 -phosphate 50 -phosphosulfate into Golgi apparatus vesicles" 777 : 133-139, 1984

54 Selva EM, "Dual role of the fringe connection gene in both heparan sulphate and fringe-dependent signalling events" 3 : 809-815, 2001

55 Edwards R, "Conjugation and metabolism of salicylic acid in tobacco" 143 : 609-614, 1994

56 Oriol R, "Common origin and evolution of glycosyltransferases using Dol-P-monosaccharides as donor substrates" 19 : 1451-1463, 2002

57 Seino J, "Characterization of rice nucleotide sugar transporters capable of transporting UDP-galactose and UDPglucose" 148 : 35-46, 2010

58 Roy SK, "Characterization of Yeast Yea4p, a uridine diphosphate-N-acetylglucosamine transporter localized in the endoplasmic reticulum and required for chitin synthesis" 275 : 13580-13587, 2000

59 Inaba A, "Changes in endogenous hormone concentrations during berry development in relation to ripening of Delaware grapes" 45 : 245-252, 1976

60 Han S, "CO2 assimilation, photosystem II photochemistry, carbohydrate metabolism and antioxidant system of citrus leaves in response to boron stress" 176 : 143-153, 2009

61 Matoh T, "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" 33 : 1135-1141, 1992

62 Loomis WD, "Boron and cell walls, In Current topics in plant biochemistry and physiology, vol 10" University of Missouri 149-178, 1991

63 Altschul SF, "Basic local alignment search tool" 215 : 403-410, 1990

64 Norambuena L, "AtUTr2 is an Arabidopsis thaliana nucleotide sugar transporter located in the Golgi apparatus capable of transporting UDP-galactose" 222 : 521-529, 2005

65 Kouchi H, "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" 22 : 53-71, 1976

66 Knappe S, "Analysis of the plastidic phosphate translocator gene family in Arabidopsis and identi- fication of new phosphate translocator-homologous transporters, classified by their putative substrate-binding site" 131 : 1178-1190, 2003

67 Takashima S, "Analysis of sialyltransferase-like proteins from Oryza sativa" 139 : 279-287, 2006

68 Takashima S, "Analysis of CMP-sialic acid transporterlike proteins in plants" 70 : 1973-1981, 2009

69 Descoteaux A, "A specialized pathway affecting virulence glycoconjugates of Leishmania" 269 : 1869-1872, 1995

70 Kyte J, "A simple method for displaying the hydropathic character of a protein" 157 : 105-132, 1982

71 Bakker H, "A CMP-sialic acid transporter cloned from Arabidopsis thaliana" 343 : 2148-2152, 2008