UDP-glucose pyrophosphorylase is not rate limiting, but is essential in arabidopsis

Plant and Cell Physiology

Volumn 50, Issue 5, 2009, Pages 998-1011

  Meng, Meng ^a   Geisler, Matt ^b   Johansson, Henrik ^a   Harholt, Jesper ^c   Scheller, Henrik V ^c,e   Mellerowicz, Ewa J ^d   Kleczkowski, Leszek A ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b SOUTHERN ILLINOIS UNIVERSITY   (United States)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^e JOINT BIOENERGY INSTITUTE   (United States)

Author keywords

Callose; Cell wall synthesis; Cellulose; Seed fitness; Sucrose synthesis

Indexed keywords

ARABIDOPSIS;

ARABIDOPSIS PROTEIN; STARCH; SUCROSE; URIDINE TRIPHOSPHATE GLUCOSE 1 PHOSPHATE URIDYLYLTRANSFERASE;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; CELL WALL; CLUSTER ANALYSIS; DNA MICROARRAY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; PLANT GENE; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL WALL; CLUSTER ANALYSIS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; MUTAGENESIS, INSERTIONAL; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANTS, GENETICALLY MODIFIED; STARCH; SUCROSE; UTP-GLUCOSE-1-PHOSPHATE URIDYLYLTRANSFERASE;

EID: 66149096644     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcp052     Document Type: Article

References (67)

1. Alexander, R.D. and Morris, P.C. (2006) A proteomic analysis of 14: 3: 3 binding proteins from developing barley grains. Proteomics 6: 1886-1896.
2. Baud, S. and Graham, I.A. (2006) A spatiotemporal analysis of enzymatic activities associated with carbon metabolism in wild-type and mutant embryos of Arabidopsis using in situ histochemistry. Plant J. 46: 155-169.
3. Borovkov, A.Y., McClean, P.E., Sowokinos, J.R., Ruud, S.H. and Secor, G.A. (1996) Effect of expression of UDP-glucose pyrophosphorylase ribozyme and antisense RNAs on the enzyme activity and carbohydrate composition of field-grown transgenic potato plants. J. Plant Physiol. 147: 644-652.
4. Carpentier, S.C., Witters, E., Laukens, K., Van Onckelen, H., Swennen, R. and Panis, B. (2007) Banana (Musa spp.) as a model to study the meristem proteome: acclimation to osmotic stress. Proteomics 7: 92-105.
5. Chen, R., Zhao, X., Shao, Z., Wei, Z., Wang, Y., Zhu, L., et al. (2007b) Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition, and its cosuppression results in a new type of thermosensitive genic male sterility. Plant Cell 19: 847-861.
6. Chen, R., Zhao, X., Shao, Z., Zhu, L. and He, G. (2007a) Multiple isoforms of UDP-glucose pyrophosphorylase in rice. Physiol. Plant. 129: 725-736.
7. Ciereszko, I., Janonis, A. and Kociakowska, M. (2002) Growth and metabolism of cucumber in phosphate-deficient conditions. J. Plant Nutr. 25: 1115-1127.
8. Ciereszko, I., Johansson, H., Hurry, V. and Kleczkowski, L.A. (2001a) Phosphate status affects the gene expression, protein content and enzymatic activity of UDP-glucose pyrophosphorylase in wild-type and pho mutants of Arabidopsis. Planta 212: 598-605.
9. Ciereszko, I., Johansson, H. and Kleczkowski, L.A. (2001b) Sucrose and light regulation of a cold-inducible UDP-glucose pyrophosphorylase gene via a hexokinase-independent and abscisic acid-insensitive pathway in Arabidopsis. Biochem. J. 354: 67-72.
10. Ciereszko, I., Johansson, H. and Kleczkowski, L.A. (2005) Interactive effects of phosphate deficiency, sucrose and light/dark conditions on gene expression of UDP-glucose pyrophosphorylase in Arabidopsis. J. Plant Physiol. 162: 343-353.
11. Coleman, H.D., Ellis, D.D., Gilbert, M. and Mansfield, S.D. (2006) Up-regulation of sucrose synthase and UDP-glucose pyrophosphorylase impacts plant growth and metabolism. Plant Biotechnol. J. 4: 87-101.
12. Coleman, H.D., Canam, T., Kang, K.Y., Ellis, D.D. and Mansfield, S.D. (2007) Over-expression of UDP-glucose pyrophosphorylase in hybrid poplar affects carbon allocation. J. Exp. Bot. 58: 4257-4268.
13. Doblin, M.S., Kurek, I., Jacob-Wilk, D. and Delmer, D.P. (2002) Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol. 43: 1407-1420.
14. Edwards, G.E. and Walker, D.A. (1983) C3, C4: Mechanisms, and Cellular and Environmental Regulation, of Photosynthesis. Blackwell Scientific, Oxford.
15. Eimert, K., Villand, P., Kilian, A. and Kleczkowski, L.A. (1996) Cloning and characterization of several cDNAs for UDP-glucose pyrophosphorylase from barley (Hordeum vulgare) tissues. Gene 170: 227-232.
16. Eisen, M.B., Spellman, P.T., Brown, P.O. and Botstein, D. (2008) Cluster analysis and display of genome-wide expression patterns. Proc. Natl Acad. Sci. USA 95: 14863-14868.
17. Elling, L. (1996) Kinetic characterization of UDP-glucose pyrophosphorylase from germinated barley (malt). Phytochemistry 42: 955-960.
18. Fernando, D.D. (2005) Characterization of pollen tube development in Pinus strobus (Eastern white pine) through proteomic analysis of differentially expressed proteins. Proteomics 5: 4917-4926.
19. Frenkel, M., Bellafiore, S., Rochaix, J.D. and Jansson, S. (2007) Hierarchy amongst photosynthetic acclimation responses for plant fitness. Physiol. Plant. 129: 455-459.
20. Fry, S. (1988) The Growing Plant Cell Wall: Chemical and Metabolic Analysis. The Blackburn Press, Caldwell, NJ.
21. Geisler, M., Jablonska, B. and Springer, P.S. (2002) Enhancer trap expression patterns provide a novel teaching resource. Plant Physiol. 130: 1747-1753.
22. Geisler, M., Kleczkowski, L.A. and Karpinski, S. (2006) A universal algorithm for genome-wide in silico identification of biologically significant gene promoter putative cis-regulatory-elements; identification of new elements for reactive oxygen species and sucrose signaling in Arabidopsis. Plant J. 45: 384-398.
23. Geisler, M., Wilczynska, M., Karpinski, S. and Kleczkowski, L.A. (2004) Toward a blueprint for UDP-glucose pyrophosphorylase structure/ function properties: homology-modeling analyses. Plant Mol. Biol. 56: 783-794.
24. Gibeaut, D.M. (2000) Nucleotide sugars and glucosyltransferases for synthesis of cell wall matrix polysaccharides. Plant Physiol. Biochem. 38: 69-80.
25. Harholt, J., Jensen, J.K., Sørensen, S.O., Orfi la, C., Pauly, M. and Scheller, H.V. (2006) ARABINAN DEFICIENT 1 is a putative arabinosyltransferase involved in biosynthesis of pectic arabinan in Arabidopsis. Plant Physiol. 140: 49-58.
26. Hertzberg, M., Aspeborg, H., Schrader, J., Andersson, A., Erlandsson, R., Blomqvist, K., et al. (2001) A transcriptional roadmap to wood formation. Proc. Natl Acad. Sci. USA 98: 14732-14737.
27. Johansson, H., Sterky, F., Amini, B., Lundeberg, J. and Kleczkowski, L.A. (2002) Molecular cloning and characterization of a cDNA encoding poplar UDP-glucose dehydrogenase, a key gene of hemicellulose/ pectin formation. Biochim. Biophys. Acta 1576: 53-58.
28. Karthikeyan, A.S., Varadarajan, D.K., Jain, A., Held, M.A., Carpita, N.C. and Raghothama, K.G. (2007) Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 225: 907-918.
29. Katsube, T., Kazuta, Y., Tanizawa, K. and Fukui, T. (1991) Expression in Escherichia coli of UDP-glucose pyrophosphorylase cDNA from potato tuber and functional assessment of the lysyl residues located at the substrate-binding site. Biochemistry 30: 8546-8551.
30. Kleczkowski, L.A. (1994) Glucose activation and metabolism through UDP-glucose pyrophosphorylase in plants. Phytochemistry 37: 1507-1515.
31. Kleczkowski, L.A., Geisler, M., Ciereszko, I. and Johansson, H. (2004) UDP-glucose pyrophosphorylase - an old protein with new tricks. Plant Physiol. 134: 912-918.
32. Komatsu, S., Yamada, E. and Furukawa, K. (2009) Cold stress changes the concavalin A-positive glycosylation pattern of proteins expressed in the basal parts of rice leaf sheaths. Amino Acids 36: 115-123.
33. Koncz, C., Martini, N., Mayerhofer, R., Koncz-Kalman, Z., Körber, H., Rédei, G.P., et al. (1989) High frequency T-DNA-mediated gene tagging in plants. Proc. Natl Acad. Sci. USA 86: 8467-8471.
34. Kotake, T., Hojo, S., Yamaguchi, D., Aohara, T., Konishi, T. and Tsumuraya, Y. (2007) Properties and physiological functions of UDP-sugar pyrophosphorylase in Arabidopsis. Biosci. Biotechnol. Biochem. 71: 761-771.
35. Kuipers, A.G.J., Soppe, W.J.J., Jacobsen, E. and Visser, R.G.F. (1995) Factors affecting the inhibition by antisense RNA of granule-bound starch synthase gene-expression in potato. Mol. Gen. Genet. 246: 745-755.
36. Külheim, C., Agren, J. and Jansson, S. (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297: 91 -93.
37. Lee-Ho, E., Walton, L.J., Reid, D.M., Yeung, E.C. and Kurepin, L.V. (2007) Effects of elevated carbon dioxide and sucrose concentrations on Arabidopsis thaliana root architecture and anatomy. Can.J. Bot. 85: 324-330.
38. Litterer, L.A., Schnurr, J A, Plaisance, K.L., Storey, K.K., Gronwald, J.W. and Somers, D.A. (2006) Characterization and expression of Arabidopsis UDP-sugar pyrophosphorylase. Plant Physiol. Biochem. 44: 171-180.
39. Martz, F., Wilczynska, M. and Kleczkowski, L.A. (2002) Oligomerization status, with the monomer as active species, defines catalytic efficiency of UDP-glucose pyrophosphorylase. Biochem. J. 367: 295-300.
40. McCoy, J.G., Bitto, E., Bingman, C.A., Wesenberg, G.E., Bannen, R.M., Kondrashov, D.A., et al. (2007) Structure and dynamics of UDP-glucose pyrophosphorylase from Arabidopsis thaliana with bound UDP-glucose and UTP. J. Mol. Biol. 366: 830-841.
41. Meng, M., Geisler, M., Johansson, H., Mellerowicz, E.J., Karpinski, S. and Kleczkowski, L.A. (2007) Differential tissue/organ-dependent expression of two sucrose- and cold-responsive genes for UDP-glucose pyrophosphorylase in Populus. Gene 389: 186-195.
42. Meng, M., Wilczynska, M. and Kleczkowski, L.A. (2008) Molecular and kinetic characterization of two UDP-glucose pyrophosphorylases, products of distinct genes, from Arabidopsis. Biochim. Biophys. Acta 1784: 967-972.
43. Mikami, S., Hori, H. and Mitsui, T. (2002) Separation of distinct compartments of rice Golgi complex by sucrose density gradient centrifugation. Plant Sci. 161: 665-675.
44. Mouille, C, Witucka-Wall, H., Bruyant, M.P., Loudet, O., Pelletier, S., Rihouey, C., et al. (2006) Quantitative trait loci analysis of primary cell wall composition in Arabidopsis. Plant Physiol. 141: 1035-1044.
45. Mu, H., Ke, J., Liu, W., Zhuang, C. and Yip, W. (2009) UDP-glucose pyrophosphorylase2 (OsUgp2), a pollen-preferential gene in rice, plays a critical role in starch accumulation during pollen maturation. Chinese Sci. Bull. 54: 234-243.
46. Nakano, K., Omura, Y., Tagaya, M. and Fukui, T. (1989) UDP-glucose pyrophosphorylase from potato tuber - purification and characterization. J. Biochem. 106: 528-532.
47. Nakata, P.A. and Okita, T.W. (1996) Cis-elements important for the expression of the ADP-glucose pyrophosphorylase small subunit are located both upstream and downstream from its structural gene. Mol. Gen. Genet. 250: 581-592.
48. Nishikawa, S., Zinkl, G.M., Swansson, R.J., Maruyama, D. and Preuss, D. (2005) Callose (β-1,3 glucan) is essential for Arabidopsis pollen wall patterning, but not tube growth. BMC Plant Biol. 5: 22.
49. Øbro, J., Harholt, J., Scheller, H.V. and Orfila, C. (2004) Rhamnogalacturonan I in Solanum tuberosum tubers contains complex arabinogalactan structures. Phytochemistry 65: 1429-1438.
50. Pina, A. and Errea, P. (2008) Influence of graft incompatibility on gene expression and enzymatic activity of UDP-glucose pyrophosphorylase. Plant Sci. 174: 502-509.
51. Pua, E.C., Lim, S.S.W., Liu, P. and Liu, J.Z. (2000) Expression of UDPglucose pyrophosphorylase cDNA during fruit ripening of banana. Austr. J. Plant Physiol. 27: 1151 -1159.
52. Repetto, O., Bestel-Corre, C, Dumas-Gaudot, E., Berta, C, Gianinazzi-Pearson, V. and Gianinazzi, S. (2003) Targeted proteomics to identify cadmium-induced modifications in Glomus mosseae-inoculated pea roots. New Phytol. 157: 555-567.
53. Ruban, A.V., Wentworth, M., Yakushevska, A.E., Andersson, J., Lee, P.J., Keegstra, W., et al. (2003) Plants lacking the main light-harvesting complex retain photosystem II macro-organization. Nature 421: 648-652.
54. Rutter, J., Probst, B.L. and McKnight, S.L. (2002) Coordinate regulation of sugar flux and translation by PAS kinase. Cell 111: 17-28.
55. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., et al. (2005) A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37: 501 -506.
56. Spychalla, J.P., Scheffler, B.E., Sowokinos, J.R. and Bevan, M.W. (1994) Cloning, antisense RNA inhibition and the coordinated expression of UDP-glucose pyrophosphorylase with starch biosynthetic genes in potato tubers. J. Plant Physiol. 144: 444-453.
57. Strand, A., Zrenner, R., Trevanion, S., Stitt, M., Gustafsson, P. and Gardeström, P. (2000) Decreased expression of two key enzymes in the sucrose biosynthesis pathway, cytosolic fructose-1,6-bisphosphatase and sucrose phosphate synthase, has remarkably different consequences for photosynthetic carbon metabolism in transgenic Arabidopsis thaliana. Plant J. 23: 759-770.
58. Taylor, J.S. and Raes, J. (2004) Duplication and divergence: the evolution of new genes and old ideas. Annu. Rev. Genet. 38: 615-643.
59. Wells, L., Whalen, S.A. and Hart, G.W. (2003) O-GlcNAc: a regulatory post-translational modification. Biochem. Biophys. Res. Commun. 302: 435-441.
60. Winter, H. and Huber, S.C. (2000) Regulation of sucrose metabolism in higher plants. Localization and regulation of activity of key enzymes. Crit. Rev. Plant Sci. 19: 31 -67.
61. Woo, M.O., Ham, T.H., Ji, H.S., Choi, M.S., Jiang, W., Chu, S.H., et al. (2008) Inactivation of the UGPase1 gene causes genic male sterility and endosperm chalkiness in rice (Oryza sativa L.). Plant J. 54: 190-204.
62. Zablackis, E., Huang, J., Müller, B., Darvill, A.G.and Albersheim, P. (1995) Characterization of the cell-wall polysaccharides of Arabidopsis thaliana leaves. Plant Physiol. 107: 1129-1138.
63. Zhang, H. and Forde, B.G. (1998) An Arabidopsis MADS box gene that controls nutrient induced changes in root architecture. Science 279: 407-409.
64. Zhong, R., Peña, M.J., Zhou, G.K., Nairn, C.J., Wood-Jones, A., Richardson, E.A., et al. (2005) Arabidopsis fragile fiber8, which encodes a putative glucuronyltransferase, is essential for normal secondary wall synthesis. Plant Cell 17: 3390-408.
65. Zhu, J., Alvarez, S., Marsh, E.L., LeNoble, M.E., Cho, I.J., Sivaguru, M., et al. (2007) Cell wall proteome in the maize primary root elongation zone. II. Region-specific changes in water soluble and lightly ionically bound proteins under water deficit. Plant Physiol. 145: 1533-1548.
66. Zrenner, R., Krause, K.P., Apel, P. and Sonnewald, U. (1996) Reduction of the cytosolic fructose-1,6-bisphosphatase in transgenic potato plants limits photosynthetic sucrose biosynthesis with no impact on plant growth and tuber yield. Plant J. 9: 671-681.
67. Zrenner, R., Willmitzer, L. and Sonnewald, U. (1993) Analysis of the expression of potato uridinediphosphate-glucose pyrophosphorylase and its inhibition by antisense RNA. Planta 190: 247-252.