Skip to main content
SpringerLink
Log in

Overexpression of UDP-glucose dehydrogenase from Larix gmelinii enhances growth and cold tolerance in transgenic Arabidopsis thaliana

  • Original Paper
  • Published:
Biologia Plantarum

Abstract

Uridine diphosphate glucose dehydrogenase (UGDH) plays an important role in biosynthesis of hemicellulose by catalyzing oxidation of UDP-glucose (UDP-Glc) to UDP-glucuronate (UDP-GlcA), a key sugar nucleotide involved in biosynthesis of the plant cell wall. In this study, a UGDH ortholog referred to as LgUGDH was isolated from Larix gmelinii using PCR and rapid amplification of cDNA ends techniques. Real-time PCR shows that the LgUGDH gene was expressed primarily in larch stems in addition to its roots and leaves, and Southern blot analysis indicates that UGDH is encoded by two paralogous genes in L. gmelinii. Overexpression of LgUGDH increased the content of soluble sugars and hemicelluloses and enhanced vegetative growth and cold tolerance in transgenic Arabidopsis thaliana. These results reveal that L. gmelinii UGDH participates in sucrose/polysaccharide metabolism and cell wall biosynthesis and may be a good candidate gene for enhancing plant growth, cold tolerance, and hemicellulose content.

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

Similar content being viewed by others

Abbreviations

CaMV:

cauliflower mosaic virus

CTAB:

cetyltrimethylammonium bromide

LSD:

least significant difference

MS:

Murashige and Skoog

NAD:

nicotinamide adenine dinucleotide

NPT II :

neomycin phosphotransferase IIgene

RACE:

rapid amplification of cDNA ends

RT-PCR:

reverse transcription polymerase chain reaction

UDP-Glc:

uridine diphosphate glucose

UDP-GlcA:

uridine diphosphate glucuronate

UGDH:

uridine diphosphate glucose dehydrogenase

UGPase:

uridine diphosphate glucose pyrophosphorylase

WT:

wild type

References

  • Akama, K., Shiraishi, H., Ohta, S., Nakamura, K., Okada, K., Shimura, Y.: Efficient transformation of Arabidopsis thaliana: comparison of the efficiencies with various organs, plant ecotypes and Agrobacterium strains. - Plant Cell Rep. 12: 7–11, 1992.

    Article  CAS  PubMed  Google Scholar 

  • Amino, S., Takeuchi, Y., Komamine, A.: Changes in enzyme activities involved in formation and interconversion of UDPsugars during the cell cycle in a synchronous culture of Catharanthus roseus. - Physiol. Plant 64: 111–117, 1985.

    Article  CAS  Google Scholar 

  • Bindschedler, L.V., Tuerck, J., Maunders, M., Ruel, K., Petit- Conil, M., Danoun, S., Boudet, A.M., Joseleau, J.P., Bolwell, G.P.: Modification of hemicellulose content by antisense down-regulation of UDP-glucuronate decarboxylase in tobacco and its consequences for cellulose extractability. - Phytochemistry 68: 2635–2648, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Bindschedler, L.V., Wheatley, E., Gay, E., Cole, J., Cottage, A., Bolwell, G.P.: Characterisation and regulation of the pathway from UDP-glucose to UDP-xylose in differentiating tobacco tissue. - Plant mol. Biol. 57: 285–301, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Chang, S., Puryear, T., Caimey, I.: A simple and efficient method for isolating RNA from pine trees. - Plant mol. Biol. Rep. 11: 113–116, 1993.

    Article  CAS  Google Scholar 

  • Dalessandro, G., Northcote, D.H.: Possible control sites of polysaccharide synthesis during cell growth and wall expansion of pea seedlings (Pisum sativum L.). - Planta 134: 39–44, 1977a.

    Article  CAS  PubMed  Google Scholar 

  • Dalessandro, G., Northcote, D.H.: Changes in enzymatic activities of nucleoside diphosphate sugar interconversions during differentiation of cambium to xylem in sycamore and poplar. - Biochem. J. 162: 267–279, 1977b.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delmer, D.P., Stone, B.A.: Biosynthesis of plant cell walls. - In: Stumpf, P.K., Conn, E.E. (ed.): The Biochemistry of Plants. Vol. 14. Pp. 373–420. Academic Press, San Diego 1988.

    Chapter  Google Scholar 

  • De Luca, G., Speziale, P., Rindi, S., Balduini, C., Castellani, A.A.: Effect of some nucleotides on the regulation of glycosaminoglycan biosynthesis. - Connect. Tissue Res. 4: 247–254, 1976.

    Article  PubMed  Google Scholar 

  • Gibeaut, D.M.: Nucleotide sugars and glycosyltransferases for synthesis of cell wall matrix polysaccharides. - Plant Physiol. Biochem. 38: 69–80, 2000.

    Article  CAS  Google Scholar 

  • Gibeaut, D.M., Carpita, N.C.: Biosynthesis of plant cell wall polysacharides. - FASEB J. 8: 904–915, 1994.

    CAS  PubMed  Google Scholar 

  • Griffith, C.L., Klutts, J.S., Zhang, L., Levery, S.B., Doering, T.L.: UDP-glucose dehydrogenase plays multiple roles in the biology of the pathogenic fungus Cryptococcus neoformans. - J. biol. Chem. 279: 51669–51676, 2004.

    Article  CAS  PubMed  Google Scholar 

  • He, Q.H., Qiao, D.R., Zhang, Q.L.: Cloning and expression studies of the Dunaliella salina UDP-glucose dehydrogenase cDNA. - DNA Sequence 3: 202–206, 2005.

    Google Scholar 

  • Huntley, S.K., Ellis, D., Gilbert, M., Chapple, C., Mansfield, S.D.: Significant increases in pulping efficiency in C4H–F5H-transformed poplars, improved chemical savings and reduced environmental toxins. - J. Agr. Food Chem. 51: 6178–6183, 2003.

    Article  CAS  Google Scholar 

  • Johansson, H., Sterky, F., Amini, B., Lundeberg, J., Kleczkowski, L.A.: Molecular cloning and characterization of a cDNA encoding poplar UDP-glucose dehydrogenase, a key gene of hemicellulose/pectin formation. - Biochem. biophys. Acta 1576: 53–58, 2002.

    CAS  PubMed  Google Scholar 

  • Karkonen, A., Murigneux, A., Martinant, J., Pepey, E., Tatout, C., Dudley, B., Fry, S.: UDP-glucose dehydrogenases of maize: a role in cell wall pentose biosynthesis. - Biochem. J. 391: 409–415, 2005.

    Article  PubMed  PubMed Central  Google Scholar 

  • Karkonen, A., Fry, S.: Novel characteristics of UDP-glucose dehydrogenase activities in maize: non-involvement of alcohol dehydrogenases in cell wall polysaccharide biosynthesis. - Planta 223: 858–870, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Kim, G., Tsukaya, H., Saito, Y., Uchimiya, H.: Changes in the shapes of leaves and flowers upon overexpression of the novel cytochrome P450 in Arabidopsis thaliana. - Proc. nat. Acad. Sci. USA 96: 9433–9437, 1999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kleczkowski, L.A., Geisler, M., Ciereszko, I., Johansson, H.: UDP glucose pyrophosphorylase, an old protein with new tricks. - Plant Physiol. 134: 912–918, 2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klinghammer, M., Tenhaken, R.: Genome-wide analysis of the UDP-glucose dehydrogenase gene family in Arabidopsis, a key enzyme for matrix polysaccharides in cell walls. - J. exp. Bot. 58: 3609–3621, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Labate, M.T.V., Bertolo, A.L.F., Nascimento, D.D.D., Gutmanis, G., Andrade, A.D., Rodrigues, M.J.C., Labate, C.A.: Cloning and endogenous expression of a Eucalyptus grandis UDPglucose dehydrogenase cDNA. - Genet. mol. Biol. 33: 686–695, 2010.

    Article  PubMed  PubMed Central  Google Scholar 

  • Li, N.N., Wang, L., Zhang, W.B., Takechi, K., Takano, H., Lin, X.F.: Overexpression of UDP-glucose pyrophosphorylase from Larix gmelinii enhances vegetative growth in transgenic Arabidopsis thaliana. - Plant Cell Rep. 33: 779–791, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Lin, X.F., Minamisawa, N., Takechi, K., Zhang, W.B., Sato, H., Takio, S., Tsukaya, H., Takano, H.: Isolation and characterization of the Larix gmelinii ANGUSTIFOLIA (LgAN) gene. - Planta 228: 601–608, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Liu, F., Huang, Y., Guo, Q.Q., Zhang, X.W., Li, L.Y., Deng, J., Xie, L.L.: Cloning and eExpression of UDP-glucose dehydrogenase (UDPGDH) cDNA in ramie (Boehmeria nivea L. Gaud.) - Scientia agr. sin. 41: 3542–3548, 2008.

    CAS  Google Scholar 

  • Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using realtime quantitative PCR and the 2-CT method. - Methods 25: 402–408, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Loewus, F., Chen, M.S., Loewus, M.W.: The myo-inositol oxidation pathway to cell wall polysaccharides. - In: Loewus, F. (ed.): Biogenesis of Plant Cell Wall Polysaccharides. Pp. 1–27. Academic Press, New York 1973.

    Chapter  Google Scholar 

  • Matsumoto, T., Tanaka, T., Sakai, H.: Comprehensive sequence analysis of 24 783 barley full-length cDNAs derived from 12 clone libraries. - Plant Physiol. 156: 20–28, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murashige, T., Skoog, F.: A revised medium for rapid growth and bioassays with tobacco tissue cultures. - Plant Physiol. 15: 473–497, 1962.

    Article  CAS  Google Scholar 

  • Murray, M.G., Thompson, W.F.: Rapid isolation of high molecular weight DNA. - Nucl. Acids Res. 8: 4321–4235, 1980.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelsetuen, G.L., Kirkwood, S.: The mechanism of action of uridine diphosphoglucose dehydrogenase. - J. biol. Chem. 246: 3828–3834, 1971.

    Google Scholar 

  • Pang, C.Y., Wang, H., Pang, Y.: Comparative proteomics indicates that biosynthesis of pectic precursors is important for cotton fiber and Arabidopsis root hair elongation. - Mol. cell. Proteomics 9: 2019–2033, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reiter, W.D., Vanzin, G.F.: Molecular genetics of nucleotide sugar interconversion pathways in plants. - Plant mol. Biol. 47: 95–113, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Rigg, G.P., Barrett, B.: The localization of KpsC, S and T, and KfiA, C and D proteins involved in the biosynthesis of the Escherichia coli K5 capsular polysaccharide: evidence for a membrane-bound complex. - Microbiology 144: 290–291, 1998.

    Article  Google Scholar 

  • Roberts, R.M., Cetorelli, J.J.: UDP-D-glucuronic acid pyrophosphorylase and the formation of UDP-D-glucuronic acid in plants. - In Loewus, F. (ed.): Biogenesis of Plant Cell Wall Polysaccharides. Pp. 49–68. Academic Press, New York 1973.

    Chapter  Google Scholar 

  • Roberts, R.M., Loewus, F.: The conversion of D-glucose- 6-14C to cell wall polysaccharide material in Zea mays in presence of high endogenous levels of myoinositol. - Plant Physiol. 52: 646–650, 1973.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robertson, D., Beech, I., Bolwell, G.P.: Regulation of the enzymes of UDP-sugar metabolism during differentiation of French bean. - Phytochemistry 39: 21–28, 1995.

    Article  CAS  Google Scholar 

  • Robertson, D., Smith, C., Bolwell, G.P.: Inducible UDP-glucose dehydrogenase from French bean (Phaseolus vulgaris L.) locates to vascular tissue and has alcohol dehydrogenase activity - Biochem. J. 313: 311–317, 1996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki, K., Taylor, I.E.P.: Specific labeling of cell wall polysaccharides with myo-[2-3H] inositol during germination and growth of Phaseolus vulgaris L. - Plant Cell Physiol. 25: 989–997, 1984.

    CAS  Google Scholar 

  • Sato, K., Hihara, E., Yamaguchi, M., Kanahama, K., Kanayama, Y.: Possible role of a peach homolog of UDP-glucose dehydrogenase in fruit development.- Scientia Hort. 150: 195–200, 2013.

  • Schädel, C., Blöchl, A., Richter, A., Hoch, G.: Quantification and monosaccharide composition of hemicelluloses from different plant functional types. - Plant Physiol. Biochem. 48: 1–8, 2010.

    Article  PubMed  Google Scholar 

  • Seifert, G.J.: Nucleotide sugar interconvertions and cell wall biosynthesis: How to bring the inside to the outside. - Curr. Opin. Plant Biol. 7: 277–284, 2004.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sekin, S.: Enzymatic determination of glucose, fructose and sucrose in tobacco. - Tobacco Sci. 23: 75–77, 1978.

    Google Scholar 

  • Stewart, D.C., Copeland, L.: Uridine-5’-diphosphate dehydrogenase from soybean nodules. - Plant Physiol. 116: 349–355, 1998.

    Article  CAS  PubMed Central  Google Scholar 

  • Tenhaken, R., Thulke, O.: Cloning of an enzyme that synthesizes a key nucleotide sugar precursor of hemicellulose biosynthesis from soybean: UDP-glucose dehydrogenase. - Plant Physiol. 112: 1127–1134, 1996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Updegraff, D.M.: Semi-micro determination of cellulose in biological materials. - Anal. Biochem. 32: 420–424, 1969.

    Article  CAS  PubMed  Google Scholar 

  • Van Soest, P.J.: Use of detergents in analysis of fibrous feeds. 2. A rapid method for determination of fiber and lignin. - J. Assoc. Offic. Anal. Chem. 46: 829–835, 1963.

    Google Scholar 

  • Van Soest, P.J., Wine RH: Use of detergents in analysis of fibrous feeds. 4. Determination of plant cell-wall constituents. - J. Assoc. Offic. Anal. Chem. 50: 50–55, 1967.

    Google Scholar 

  • Wegrowski, Y., Perreau, C., Bontemps, Y., Maquart, F.X.: Uridine diphosphoglucose dehydrogenase regulates proteoglycan expression: cDNA cloning and antisense study. - Biochem. biophys. Res. Commun. 250: 206–211, 1998.

    Article  CAS  PubMed  Google Scholar 

  • Winter, H., Huber, S.C.: Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. - Biochem. mol. Biol. 35: 253–289, 2000.

    CAS  Google Scholar 

  • Witt, H.J.: UDP-glucose metabolism during differentiation and dedifferentiation of Riella helicophylla. - J. Plant Physiol. 140: 276–281, 1992.

    Article  CAS  Google Scholar 

  • Zablackis, E., Huang, J., Muller, B., Darvill, A.G., Albersheim, P.: Characterization of the cell-wall polysaccharides of Arabidopsis thaliana leaves. - Plant Physiol. 107: 1129–1138, 1995.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu, W., Lin, X., Zhang, W., Xu, Y., Takano, H.: Isolation and sequence analysis of Larix gmelinii actin gene. - Biotechnol. Bull. 31: 95–100, 2011.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Life Sciences, Inner Mongolia University, Hohhot, 010021, P.R. China

    N. N. Li, L. Chen, Q. Li & X. F. Lin

  2. College of Forestry, Inner Mongolia Agricultural University, Hohhot, 010019, P.R. China

    X. H. Li & W. B. Zhang

  3. Graduate School of Science and Technology, Kumamoto University, Kurokami, Kumamoto, 860-8555, Japan

    K. Takechi & H. Takano

Authors
  1. N. N. Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. X. H. Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Q. Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. W. B. Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. K. Takechi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. H. Takano
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. X. F. Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to X. F. Lin.

Additional information

Acknowledgments: We would like to thank Prof. Nakamura Kenzo in the Chubu University for kindly providing the pBI101-35::Gus-Hm vector. This study was supported by the National Natural Science Foundation of China (No. 31160143, No. 31060106, No. 30960030, and No. 31260168), the Natural Science Foundation of Inner Mongolia (No. 2010BS0509 and 2009MS0505) and Chun-Hui project (No. Z2009-1-01009).

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, N.N., Chen, L., Li, X.H. et al. Overexpression of UDP-glucose dehydrogenase from Larix gmelinii enhances growth and cold tolerance in transgenic Arabidopsis thaliana . Biol Plant 61, 95–105 (2017). https://doi.org/10.1007/s10535-016-0657-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-016-0657-8

Additional key words

Search

Navigation