Skip to main content
SpringerLink
Log in

Identification of a UDP-glucose pyrophosphorylase from cotton (Gossypium hirsutum L.) involved in cellulose biosynthesis in Arabidopsis thaliana

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

UDP-glucose pyrophosphorylase is an important regulatory enzyme for the development of plants and a critical enzyme in synthesis of glycogen. Here, we reported the cloning of a full-length UGP cDNA from cotton, named GhUGP. Real-time PCR analysis indicated the GhUGP expression in root, stem, leaf and flower of cotton, with a higher level in flower and root. The transcription level of GhUGP depended on sucrose and light in short time and increased under low temperature, but decreased in O2 deficiency. Interestingly, the expression of GhUGP was significantly up-regulated after ethylene induction in cotton ovules. The over-expression of the GhUGP in Arabidopsis showed discrepant phenotype: increase in height and growth rate when compared with control lines. What is more, the transgenic Arabidopsis had increased contents of soluble sugars, starch and cellulose, but not in lignin content. Collectively, these results indicate that cotton UGPase participates in sucrose/polysaccharides metabolism and cell wall biosynthesis and provide theoretical deduction supporting GhUGP as a good candidate gene for improving the development of cotton fibers cell.

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

Similar content being viewed by others

Abbreviations

UDP:

Uridine diphosphate

UGPase:

UDP-glucose pyrophosphorylase

UDPG:

Uridine diphosphate glucose

UTP:

Uridine triphosphate

Glc-1-P:

Glucose 1-phosphate

PPi:

Pyrophosphate

SPS:

Sucrose phosphate synthase

SS:

Sucrose synthase

AGPase:

ADP-glucose pyrophosphorylase

ADP:

Adenosine diphosphate

SuSy:

Sucrose synthase

NADP:

Nicotinamide adenine dinucleotide phosphate

HXK:

Hexokinase

OKA:

Okadaic acid

USPase:

UDP-sugar pyrophosphorylase

NB:

Nucleotide binding

References

  • Abe T, Niiyama H, Sasahara T (2002) Cloning of cDNA for UDP-glucose pyrophosphorylase and the expression of mRNA in rice endosperm. Theor Appl Genet 105:216–221. doi:10.1007/s00122-002-0927-z

    Article  PubMed  CAS  Google Scholar 

  • Amor Y, Haigler CH, Johnson S, Wainscott M, Delmer DP (1995) A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc Natl Acad Sci USA 92:9353–9357

    Article  PubMed  CAS  Google Scholar 

  • Beasley CA, Ting IP (1973) The effect of plant growth substances on in vitro fiber development from fertilized cotton ovules. Am J Bot 60:130–139

    Article  CAS  Google Scholar 

  • Borovkov AY, McClean PE, Sowokinos JR, Ruud SH, Secor GA (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. Plant Physiol 147:644–652

    CAS  Google Scholar 

  • Chang CW, Moseley JL, Wykoff D, Grossman AR (2005) The LPB1 gene is important for acclimation of Chlamydomonas reinhardtii to phosphorus and sulfur deprivation. Plant Physiol 138:319–329

    Article  PubMed  CAS  Google Scholar 

  • Chen RZ, Zhao X, Shao Z, Zhu LL, He G (2007) Multiple isoforms of UDP-glucose pyrophosphorylase in rice. Physiol Plant 129:725–736. doi:10.1111/j.1399-3054.2007.00865.x

    Article  CAS  Google Scholar 

  • Ciereszko I, Johansson H, Hurry V, Kleczkowski LA (2001a) Phosphate status affects the gene expression, protein content and enzymatic activity of UDP-glucose pyrophosphorylase gene in wild-type and pho mutants of Arabidopis. Planta 212:598–605. doi:10.1007/s004250000424

    Article  PubMed  CAS  Google Scholar 

  • Ciereszko I, Johansson H, Kleczkowski LA (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

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Coleman HD, Ellis DD, Gilbert M, Mansfield SD (2006) Up-regulation of sucrose synthase and UDP-glucose pyrophosphorylase impacts plant growth and metabolism. Plant Biotechnol J 4:87–101. doi:10.1111/j.1467-7652.2005.00160.x

    Article  PubMed  CAS  Google Scholar 

  • Coleman HD, Canam T, Kang KY, Ellis DD, Mansfield SD (2007) Over-expression of UDP-glucose pyrophosphorylase in hybrid poplar affects carbon allocation. J Exp Bot 58:4257–4268. doi:10.1093/jxb/erm287

    Article  PubMed  CAS  Google Scholar 

  • Dai N, Petreikov M, Portnoy V, Katzir N, Pharr DM, Schaffer AA (2006) Cloning and expression analysis of a UDP-galactose/glucose pyrophosphorylase from Melon fruit provides evidence for the major metabolic pathway of galactose metabolism in raffinose oligosaccharide metabolizing plants. Plant Physiol 142:294–304. doi:10.1104/pp.106.083634

    Article  PubMed  CAS  Google Scholar 

  • Eimert K, Villand P, Kilian A, Kleczkowski LA (1996) Cloning and characterization of several cDNAs for UDP-glucose pyrophosphorylase from barley (Hordeum vulgare) tissues. Gene 170:227–232. doi:0378-1119(95)00873-X

    Article  PubMed  CAS  Google Scholar 

  • Hertzberg M, Aspeborg H, Schrader J, Andersson A, Erlandsson R, Blomqvist K, Bhalerao R, Uhlen M, Teeri TT, Lundeberg J, Sundberg B, Peter Nilsson, Sandberg G (2001) A transcriptional roadmap to wood formation. Proc Natl Acad Sci USA 98:14732–14737. doi:10.1037/pnas.261293398

    Article  PubMed  CAS  Google Scholar 

  • Huntley SK, Ellis D, Gilbert M, Chapple C, Mansfield SD (2003) Significant increases in pulping efficiency in C4H–F5H-transformed poplars; improved chemical savings and reduced environmental toxins. J Agric Food Chem 51:6178–6183. doi:10.1021/jf034320

    Article  PubMed  CAS  Google Scholar 

  • Johansson H (2003) Gene regulation of UDP-glucose synthesis and metabolism in plants. PhD thesis, Umeå University, Umeå

  • Katsube T, Kazuta Y, Mori H, Nakano K, Tanizawa K, Toshio Fukui (1990) UDP-glucose pyrophosphorylase from potato tuber: cDNA cloning and sequencing. J Biochem 108:321–332

    PubMed  CAS  Google Scholar 

  • Katsube T, Kazuta Y, Tanizawa K, Fukui T (1991) Expression in Escherichia coli of UDP-glucose pyrophosphorylase cDNA from potato tuber and functional assessment of the five lysyl residues located at the substrate-binding site. Biochemistry 30:8456–8661. doi:10.1021/bi00099a008

    Article  Google Scholar 

  • Kiyosumi D, Ishimizu T, Nakanishi T, Norioka S (2002) Pollen UDP-glucose pyrophosphorylase showing polymorphism well-correlated to the S genotype of Pyrus pyrifolia. Sex Plant Reprod 14:315–323. doi:10.1007/s00497-001-0125-1

    Article  Google Scholar 

  • Kleczkowski LA (1994) Glucose activation and metabolism through UDP-glucose pyrophosphorylase in plants. Phytochemistry 37:1507–1515. doi:10.1016/S0031-9422(00)89568-0

    Article  CAS  Google Scholar 

  • Kleczkowski LA, Geisler M, Ciereszko I, Johansson H (2004) UDP-glucose pyrophosphorylase. An old protein with new tricks. Plant Physiol 134:912–918. doi:10.1104/pp.103.036053

    Article  PubMed  CAS  Google Scholar 

  • Kleczkowski LA, Kunz S, Wilczynska M (2010) Mechanisms of UDP-glucose synthesis in plants. Crit Rev Plant Sci 29:191–203. doi:10.1080/07352689.2010.483578

    Article  CAS  Google Scholar 

  • Kotake T, Yamaguchi D, Ohzono H, Hojo S, Kaneko S, Ishida HK, Tsumuraya Y (2004) UDP-sugar pyrophosphorylase with broad substrate specificity toward various monosaccharide 1-phosphates from pea sprouts. Biol Chem 279:45728–45736

    Article  CAS  Google Scholar 

  • Loreti E, De Bellis L, Alpi A, Perata P (2001) Why and how do plant cells sense sugars? Ann Bot 88:803–812

    Article  CAS  Google Scholar 

  • Martz F, Wilczynska M, Kleczkowski LA (2002) Oligomerization status, with the monomer as active species, defines catalytic efficiency of UDP-glucose pyrophosphorylase. Biochem J 367:295–300

    Article  PubMed  CAS  Google Scholar 

  • McCoy JG, Bitto E, Bingman CA, Wesenberg GE, Bannen RM, Kondrashov DA, Phillips GN (2007) Structure and dynamics of UDP-glucose pyrophosphorylase from Arabidopsis thaliana with bound UDP-glucose and UTP. Mol Biol 366:830–841

    Article  CAS  Google Scholar 

  • Meng M, Geisler M, Johansson H, Mellerowicz EJ, Karpinski S, Kleczkowski LA (2007) Differential tissue/organ-dependent expression of two sucrose and cold-responsive genes for UDP-glucose pyrophosphorylase in Populus. Gene 389:186–195. doi:10.1016/j.gene.2006.11.006

    Article  PubMed  CAS  Google Scholar 

  • Meng M, Fitzek E, Gajowniczek A, Wilczynska M, Kleczkowski LA (2009a) Domain-specific determinants of catalysis/substrate binding and the oligomerization status of barley UDP-glucose pyrophosphorylase. Biochim Biophys Acta 1794:1734–1742. doi:10.1016/j.bbapap.2009.08.009

    PubMed  CAS  Google Scholar 

  • Meng M, Geisler M, Johansson H, Harholt J, Scheller HV, Mellerowicz EJ, Kleczkowski LA (2009b) UDP-glucose pyrophosphorylase is not rate-limiting, but is essential in Arabidopsis. Plant Cell Physiol 50:998–1011

    Article  PubMed  CAS  Google Scholar 

  • Mu H, Ke JH, Liu W, Zhang CX, Yip WK (2009) UDP-glucose pyrophosphorylase 2 (OsUgp2), a pollen-preferential gene in rice, plays a critical role in starch accumulation during pollen maturation. Chin Sci Bull 54:234–243. doi:10.1007/s11434-008-0568-y

    Article  CAS  Google Scholar 

  • Okazaki Y, Shimojima M, Sawada Y, Toyooka K, Narisawa T, Mochida K, Tanaka H, Matsuda F, Hirai A, Yokota Hirai M, Ohta H, Saito K (2009) A chloroplastic UDP-glucose pyrophosphorylase from Arabidopsis is the committed enzyme for the first step of sulfolipid biosynthesis. Plant Cell 21:892–909

    Article  PubMed  CAS  Google Scholar 

  • Park JI, Ishimizu T, Suwabe K, Sudo K, Masuko H, Hakozaki H, Nou IS, Suzuki G, Watanabe M (2010) UDP-glucose pyrophosphorylase is rate limiting in vegetative and reproductive phases in Arabidopsis thaliana. Plant Cell Physiol 56:981–996. doi:10.1093/pcp/pcq057

    Article  Google Scholar 

  • Pua EC, Lim SSW, Liu JZ (2000) Expression of a UDP-glucose pyrophosphorylase cDNA during fruit ripening of banana (Musa acuminata). Aust J Plant Physiol 27:1151–1159. doi:10.1071/PP00016

    CAS  Google Scholar 

  • Rook F, Gerrits N, Kortstee A, van Kampen M, Borrias M, Weisbeek P, Smeekens S (1998) Sucrose-specific signaling represses translation of the Arabidopsis ATB 2b ZIP transcription factor gene. Plant J 15:253–263

    Article  PubMed  CAS  Google Scholar 

  • Ruan YL, Llewellyn DJ, Furbank RT (2003) Suppression of sucrose synthase gene expression represses cotton fiber cell initiation, elongation, and seed development. Plant Cell 15:952–964. doi:10.1105/tpc.010108

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Shi YH, Zhu SW, Mao XZ, Feng JX, Qin YM, Zhang L, Cheng J, Wei LP, Wang ZY, Zhu YX (2006) Transcriptome profiling, molecular biological and physiological studies reveal a major role for ethylene in cotton fiber cell elongation. Plant Cell 18:651–664. doi:10.1105/tpc.105.040303

    Article  PubMed  CAS  Google Scholar 

  • Sowokinos JR, Thomas C, Burrell MM (1997) Allelic polymorphism of UDP-glucose pyrophosphorylase in potato cultivars and its association with tuber resistance to sweetening in the cold. Plant Physiol 113:511–517

    Article  PubMed  CAS  Google Scholar 

  • Spychalla JP, Scheffler BE, Sowokinos JR, Bevan MW (1994) Cloning, antisense RNA inhibition and the coordinated expression of UDP-glucose pyrophosphorylase with starch biosynthetic genes in potato tubers. Plant Physiol 144:444–453

    CAS  Google Scholar 

  • Updegraff DM (1969) Semi-micro determination of cellulose in biological materials. Anal Biochem 32:420–424

    Article  PubMed  CAS  Google Scholar 

  • Weng CJ, Deng JY, Lin DG, Jeang CL (2009) Cloning, expression and characterization of UDP-glucose pyrophosphorylase from shoots of Bambusa oldhamii. J Biochem. doi:10.1093/jb/mvp084

  • Woo MO, Ham TH, Ji HS, Choi MS, Jiang W, Chu SH, Piao R, Chin JH, Kim JA, Park BS, Seo HS, Jwa NS, McCouch S, Koh HJ (2008a) Inactivation of the UGPase1 gene causes genic male sterility and endosperm chalkiness in rice (Oryza sativa L.). Plant J 54:190–204. doi:10.1111/j.1365-313X.2008.03405.x

    Article  PubMed  CAS  Google Scholar 

  • Woo MO, Ham TH, Ji HS, Choi MS, Jiang W, Chu SH, Piao R, Chin JH, Kim JA, Park BS, Seo HS, Jwa NS, McCouch S, Koh HJ (2008b) Inactivation of the UGPase1 gene causes genic male sterility and endosperm chalkiness in rice (Oryza sativa L.). Plant J 54:190–204. doi:10.1111/j.1365-313X.2008.03405.x

    Article  PubMed  CAS  Google Scholar 

  • Wu XJ, Du M, Weng YQ, Liu D, Hu ZB (2002) UGPase of Astragalus membranaceus: cDNA clone, analyzing and expressing in Escherichia coli. Bot Sin 44:689–693. doi:0577-7496(2002)06-0689-05

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Genetically Modified Organism Breeding Major Project (Grant no. 2008ZX08005-002), the Program of National Nature Science Foundation of China (Grant no. 31071751) and State 863 Project funded by Ministry of Science and Technology (Grant no. 2008AA10Z127) P. R. China.

Author information

Authors and Affiliations

  1. College of Science, China Agricultural University, 2 West Rd, Yuanmingyuan, Haidian District, Beijing, 100193, China

    Qinghua Wang, Xue Zhang, Yuxia Hou & Xingliang Liu

  2. Cotton Research Institute, Chinese Academy of Agricultural Sciences, Development Zone, Anyang, 455000, Henan, China

    Fuguang Li & Xueyan Zhang

Authors
  1. Qinghua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xue Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fuguang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yuxia Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xingliang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xueyan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Fuguang Li or Yuxia Hou.

Additional information

Communicated by L. Jouanin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, Q., Zhang, X., Li, F. et al. Identification of a UDP-glucose pyrophosphorylase from cotton (Gossypium hirsutum L.) involved in cellulose biosynthesis in Arabidopsis thaliana . Plant Cell Rep 30, 1303–1312 (2011). https://doi.org/10.1007/s00299-011-1042-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-011-1042-x

Keywords

Search

Navigation