biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 64:667-678, 2020 | DOI: 10.32615/bp.2020.099

Cloning and characterization of a UDP-glucose dehydrogenase gene from mulberry Broussonetia kazinoki × Broussonetia papyifera

R.H. JI1,2, Z. ZHANG3, X. GUO2, Y.L. BAO1, W.B. ZHANG1,*, X.F. LIN2, S.L. BAI1,*
1 College of Forestry, Inner Mongolia Agricultural University, Hohhot 010019, P.R. China
2 School of Life Sciences, Inner Mongolia University, Hohhot 010070, P.R. China
3 College of Biological Science, China Agriculture University, Beijing 100083, P.R. China

Uridine diphosphate glucose dehydrogenase (UGDH) is a key enzyme in the hemicellulose and pectin biosynthesis pathway and participates in the regulation of growth and development in plants. In this study, we isolated a BpUGDH gene from paper mulberry (Broussonetia kazinoki × Broussonetia papyifera) and analyzed its function and expression characteristics. The results show that the BpUGDH was expressed in all organs of paper mulberry with a higher expression in stems than in leaves and roots. A pBpUGDH::GUS gene construct was highly expressed in transgenic Arabidopsis thaliana seedlings, and its expression was induced by a low temperature, methyl jasmonate, gibberellin A3, ethylene, and auxin. The overexpression of BpUGDH increased the soluble sugar content, promoted the accumulation of hemicellulose, and enhanced the vegetative growth of transgenic plants. These results provide a basis for regulating the growth and adaptability of paper mulberry and improving its utilization value via genetic modification of the BpUGDH gene.

Keywords: UGDH, hemicellulose, RACE, sugars, UDP-GlcA.

Received: November 17, 2019; Revised: June 24, 2020; Accepted: June 26, 2020; Published online: September 29, 2020  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
JI, R.H., ZHANG, Z., GUO, X., BAO, Y.L., ZHANG, W.B., LIN, X.F., & BAI, S.L. (2020). Cloning and characterization of a UDP-glucose dehydrogenase gene from mulberry Broussonetia kazinoki × Broussonetia papyifera. Biologia plantarum64, Article 667-678. https://doi.org/10.32615/bp.2020.099
Download citation

Supplementary files

Download fileJi6365_Suppl.pdf

File size: 657.26 kB

References

  1. Aubertin, C.: Paper mulberry (Broussonetia papyrifera) in Lao PDR: a successful example of forest product domestication. - In: Kusters, K., Belcher, B.: Forest Products, Livelihoods and Conservation: Case-studies of Non-timber Forest Product Systems. Vol. 1. Pp. 227-246. CIFOR, Bogor 2004.
  2. Campbell, R.E., Mosimann, S.C., Rijn, I.V.D., Tanner, M.E., Strynadka, N.C.: The first structure of UDP-glucose dehydrogenase reveals the catalytic residues necessary for the two-fold oxidation. - Biochemistry 39: 7012-7023, 2000. Go to original source...
  3. Delmer, D.P., Stone, B.A., Preiss, J.: Biosynthesis of plant cell walls. - Biochem. Plants 14: 373-420, 1988. Go to original source...
  4. Gibeaut, D.M.: Nucleotide sugars and glycosyltransferases for synthesis of cell wall matrix polysaccharides. - Plant Physiol. Biochem. 38: 69-80, 2000. Go to original source...
  5. Gibeaut, D.M., Carpita, N.C.: Biosynthesis of plant cell wall polysaccharides. - FASEB J. 8: 904-915, 1994. Go to original source...
  6. Griffith, C.L., Klutts, J.S., Zhang, L.J., 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. Go to original source...
  7. He, Q.H., Qiao, D.R., Zhang, Q.L., He, S.J., Li, Y., Bai, L.H., Yang, Z.R., Cao, Y.: Cloning and expression studies of the Dunaliella salina UDP-glucose dehydrogenase cDNA. - DNA Sequence 16: 202-206, 2005. Go to original source...
  8. 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. - Biochim. Biophys. Acta. 1576: 53-58, 2002. Go to original source...
  9. Kärkönen, A., Fry, S.C.: Novel characteristics of UDP-glucose dehydrogenase activities in maize: non-involvement of alcohol dehydrogenases in cell wall polysaccharide biosynthesis. - Planta 223: 858-870, 2006. Go to original source...
  10. Kärkönen, 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. Go to original source...
  11. Kleczkowski, L.A., Geisler, M., Ciereszko, I., Johansson, H.: UDP-glucose pyrophosphorylase. An old protein with new tricks. - Plant Physiol. 134: 912-918, 2004. Go to original source...
  12. Kim, G.T., Tsukaya, H., Saito, Y., Uchimiya, H.: Changes in the shapes of leaves and flowers upon overexpression of cytochrome P450 in Arabidopsis. - Proc. nat. Acad. Sci. USA 96: 9433-9437, 1999. Go to original source...
  13. 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: 3609-3021, 2007. Go to original source...
  14. Kuang, Y., Xi, D., Li, J., Zhu, X., Zhang, L.: Traffic pollution influences leaf biochemistries of Broussonetia papyrifera. - Open J. Forestry 2: 71-76, 2012. Go to original source...
  15. Labate, M.T.V., Bertolo, A.L.F., Nascimento, D.D.D., Gutmanis, G., Andrade, A.D., Rodrigues, M.J.C., Camargo, E.L.O., Boaretto, L.F., Moon, D.H., Bragatto, J., Labate, C.A.: Cloning and endogenous expression of a Eucalyptus grandis UDP-glucose dehydrogenase cDNA. - Gene. mol. Biol. 33: 686-695, 2010. Go to original source...
  16. Lai, X.J., Gu, Y.H., Tao, X., Zhang, Y.Z., Wang, H.Y.: Cloning and characterization of uridine diphosphate glucose dehydrogenase gene from Ipomoea batatas. - Russ. J. Plant Physiol. 61: 298-308, 2014. Go to original source...
  17. Lescot, M., Déhais, P., Thijs, G., Marchal, K., Moreau, Y., Peer Y.V.D., Rouzé, P., Rombauts, S.: Plant CARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. - Nucl. Acids Res. 30: 325-327, 2002. Go to original source...
  18. Li, G.Y., Hu, N., Ding, D.X., Zheng, J.F., Liu, Y.L., Wang, Y.D., Nie, X.Q.: Screening of plant species for phytoremediation of uranium, thorium, barium, nickel, strontium and lead contaminated soils from a uranium mill tailings repository in South China. - Bull. environ. Contam. Toxicol. 86: 646-652, 2011. Go to original source...
  19. Li, M.R., Li, H.Q., Jiang, H.W., Wu, G.J.: Establishment of a highly efficient Agrobacterium tumefaciens-mediated leaf disc transformation method for Broussonetia papyrifera. - Plant Cell Tissue Organ Cult. 93: 249-255, 2008. Go to original source...
  20. Li, M.R., Li, Y., Li, H.Q., Wu, G.J.: Overexpression of AtNHX5 improves tolerance to both salt and drought stress in Broussonetia papyrifera (L.) Vent. - Tree Physiol. 31: 349-357, 2011. Go to original source...
  21. Li, N.N., Chen, L., Li, X.H., Li, Q., Lin, X.F., Zhang, W.B., Takechi, K., Takano, H.: Overexpression of UDP-glucose dehydrogenase from Larix gmelinii enhances growth and cold tolerance in transgenic Arabidopsis thaliana. - Biol. Plant. 61: 95-105, 2017. Go to original source...
  22. 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. Go to original source...
  23. Li, Y., Li, G.: [Cloning and sequence analysis of actin gene from Broussonetia papyrifera.] - Biotechnology 17: 1-3, 2007. [In Port.]
  24. 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. Go to original source...
  25. Liu, F., Huang, Y., Guo, Q.Q., Zhang, X.W., Li, L.Y., Deng, J., Xie, L.L.: [Cloning and expression of UDP-glucose dehydrogenase (UDPGDH) cDNA in ramie (Boehmeria nivea (Linn.) Gaud).] - Sci. agr. sin. 41: 3542-3548, 2008. [In Chin.]
  26. 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. Go to original source...
  27. Matsumoto, T., Tanaka, T., Sakai, H., Amano, N., Kanamori, H., Kurita, K., Kikuta, A., Kamiya, K., Yamamoto, M., Ikawa, H., Fujii, N., Hor, K., Itoh, T., Sato, K.: Comprehensive sequence analysis of 24783 barley full-length cDNAs derived from 12 clone libraries. - Plant Physiol. 156: 20-28, 2011. Go to original source...
  28. Mithra, S.V.A., Kulkarni, K., Srinivasan, R.: Plant promoters: characterization and applications in transgenic technology. - In: Abdin, M.Z., Kiran, U., Kamaluddin, A.A. (ed.): Plant Biotechnology: Principles and Applications. Pp. 117-172. Springer, Singapore 2017. Go to original source...
  29. Nagpal, U.M., Bankar, A.V., Pawar, N.J., Kapadnis, B.P., Zinjarde, S.S.: Equilibrium and kinetic studies on biosorption of heavy metals by leaf powder of paper mulberry (Broussonetia papyrifera). - Water Air Soil Pollut. 215: 177-188, 2011. Go to original source...
  30. Pang, C.Y., Wang, H., Pang, Y., Xu, C., Jiao, Y., Qin, Y.M., Western, T.L., Yu, S.X., Zhu, Y.X.: 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. Go to original source...
  31. Peng, X.J., Teng, L.H., Yan, X.Q., Zhao, M.L., Shen, S.H.: The cold responsive mechanism of the paper mulberry: decreased photosynthesis capacity and increased starch accumulation. - BMC Genomics 16: 898, 2015. Go to original source...
  32. Reiter, W.D., Vanzin, G.F.: Molecular genetics of nucleotide sugar interconversion pathways in plants. - Plant mol. Biol. 47: 95-113, 2001. Go to original source...
  33. Rigg, G.P., Barrett, B., Roberts, I.S.: 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: 2905-2914, 1998. Go to original source...
  34. 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. Go to original source...
  35. 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. Go to original source...
  36. Seifert, G.J.: Nucleotide sugar interconversions and cell wall biosynthesis: how to bring the inside to the outside. - Curr. Opin. Plant Biol. 7: 277-284, 2004. Go to original source...
  37. Seitz, B., Klos, C., Wurm, M., Tenhaken, R.: Matrix polysaccharide precursors in Arabidopsis cell walls are synthesized by alternate pathways with organ-specific expression patterns. - Plant J. 21: 537-546, 2000. Go to original source...
  38. Stewart, D.C., Copeland, L.: Uridine 5'-diphosphate-glucose dehydrogenase from soybean nodules. - Plant Physiol. 116: 349-355, 1998. Go to original source...
  39. Strominger, J.L., Kalckar, H.M., Axelrod, J., Maxwell, E.S.: Enzymatic oxidation of uridine diphosphate glucose to uridine disphosphate glucuronic acid. - J. amer. chem. Soc. 76: 6411-6412, 1954. Go to original source...
  40. Sun, J., Liu, S.F., Zhang, C.S., Yu, L.N., Bi, J., Zhu, F., Yang, Q.L.: Chemical composition and antioxidant activities of Broussonetia papyrifera fruits. - PLoS ONE 7: e32021, 2012. Go to original source...
  41. Sun, J.W., Peng, X.J., Fan, W.H., Tang, M.J., Liu, J., Shen, S.H.: Functional analysis of BpDREB2 gene involved in salt and drought response from a woody plant Broussonetia papyrifera. - Gene 535: 140-149, 2014. Go to original source...
  42. 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. Go to original source...
  43. Turner, W., Botha, F.C.: Purification and kinetic properties of UDP-glucose dehydrogenase from sugarcane. - Arch. Biochem. Biophys. 407: 209-216, 2002. Go to original source...
  44. Wang, J., Li, A., Wang, C.G., Song, W.Q., Chen, C.B.: [Cloning and expression of UDP-glucose dehydrogenase cDNA in larix kaempferi.] - Forest Res. 26: 76-81, 2013. [In Chin.]
  45. Winter, H., Huber, S.C.: Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. - Crit. Rev. Plant Sci. 19: 253-289, 2000. Go to original source...
  46. Witt, H.J.: UDP-glucose metabolism during differentiation and dedifferentiation of Riella helicophylla. - J. Plant Physiol. 140: 276-281, 1992. Go to original source...
  47. Yan, J., Wu, P., Du, H., Zhang, Q.: First report of black spot caused by Colletotrichum gloeosporioides on paper mulberry in China. - Plant Dis. 95: 880-880, 2011. Go to original source...