Skip to main content
SpringerLink
Log in

Sugar acts as a regulatory signal on the wound-inducible expression of SbHRGP3::GUS in transgenic plants

  • Genetics and Genomics
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

SbHRGP3 encodes an HRGP whose expression is correlated with the cessation of root elongation in soybean. The wound-inducible expression of SbHRGP3 interestingly requires sucrose although wounding alone induces the expression of many HRGP genes. To examine whether sugar serves as a specific signal on the wound-inducible expression or whether sugar is required to provide ATP, we examined SbHRGP3::GUS expression in transgenic tobacco plants. Various oligosaccharides including non-metabolizable sugar induced SbHRGP3::GUS expression in transgenic plants. The inhibitors of photosynthesis and of cellular respiration did not affect the wound-inducible expression of SbHRGP3::GUS. However, the induction was significantly affected by PCMBS, an inhibitor of active apoplastic phloem loading of sucrose, suggesting that SbHRGP3::GUS expression in phloem tissues requires translocated sucrose. We therefore propose that sugar acts as a specific regulatory signal on the wound-inducible expression of SbHRGP3, rather than acting as a simple provider of ATP.

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.
Fig. 6.

Similar content being viewed by others

Abbreviations

ATP:

Adenosine triphosphate

DCMU:

3-(3,4-Dichlorophenyl)-1,1-dimethylurea

DTT:

Dithiothreitol

HRGP:

Hydroxyproline-rich glycoprotein

GUS:

β-Glucuronidase

MU:

4-Methylumbelliferone

MUG:

4-Methylumbelliferyl ß-glucuronide

PCMBS:

p-Chloromercuribenzenesulphonic acid

References

  • Ahn JH, Choi Y, Kwon YM, Kim SG, Choi YD, Lee JS (1996) A novel extensin gene encoding a hydroxyproline-rich glycoprotein requires sucrose for its wound-inducible expression in transgenic plants. Plant Cell 8:1477–1490

    Google Scholar 

  • Ahn JH, Choi Y, Kim SG, Kwon YM, Choi YD, Lee JS (1998) Expression of a soybean hydroxyproline-rich glycoprotein gene is correlated with maturation of roots. Plant Physiol 116:671–679

    Article  CAS  PubMed  Google Scholar 

  • An G, Ebert PR, Mitra A, Ha SB (1988) Binary vectors. In: Gelvin SB, Schilperoort RA (eds) Plant molecular biology manual. Kluwer, Dordrecht, pp 1–19

  • Aqvist J, Mowbray SL (1995) Sugar recognition by a glucose/galactose receptor. Evaluation of binding energetics from molecular dynamics simulations. J Biol Chem 270:9978–9981

    CAS  PubMed  Google Scholar 

  • Barker L, Kuhn C, Weise A, Schulz A, Gebhardt C, Hirner B, Hellmann H, Schulze W, Ward JM, Frommer WB (2000) SUT2, a putative sucrose sensor in sieve elements. Plant Cell 12:1153–1164

    Article  CAS  PubMed  Google Scholar 

  • Berger S, Bell E, Sadka A, Mullet JE (1995) Arabidopsis thaliana Atvsp is homologous to soybean VspA and VspB, genes encoding vegetative storage protein acid phosphatases, and is regulated similarly by methyl jasmonate, wounding, sugars, light and phosphate. Plant Mol Biol 27:933–942

    CAS  PubMed  Google Scholar 

  • Borisjuk L, Rolletschek H, Wobus U, Weber H (2003) Differentiation of legume cotyledons as related to metabolic gradients and assimilate transport into seeds. J Exp Bot 54:503–512

    Article  CAS  PubMed  Google Scholar 

  • Brumback RA (1980) Iodoacetate inhibition of glyceraldehyde-3-phosphate dehydrogenase as a model of human myophosphorylase deficiency (McArdle's disease) and phosphofructokinase deficiency (Tarui's disease). J Neurol Sci 48:383–398

    Article  CAS  PubMed  Google Scholar 

  • Bush DR (1993) Inhibitors of the proton-sucrose symport. Arch Biochem Biophys 307:355–360

    Article  CAS  PubMed  Google Scholar 

  • Dijkwel PP, Huijser C, Weisbeek PJ, Chua NH, Smeekens SC (1997) Sucrose control of phytochrome A signaling in Arabidopsis. Plant Cell 9:583–595

    Article  CAS  PubMed  Google Scholar 

  • Elliott KA, Shirsat AH (1998) Promoter regions of the extA extensin gene from Brassica napus control activation in response to wounding and tensile stress. Plant Mol Biol 37:675–687

    CAS  PubMed  Google Scholar 

  • Gibson SI, Laby RJ, Kim D (2001) The sugar-insensitive1 (sis1) mutant of Arabidopsis is allelic to ctr1. Biochem Biophys Res Commun 280:196–203

    Article  CAS  PubMed  Google Scholar 

  • Hall Q, Cannon MC (2002) The cell wall hydroxyproline-rich glycoprotein RSH is essential for normal embryo development in Arabidopsis. Plant Cell 14:1161–1172

    Google Scholar 

  • Hanson J, Johannesson H, Engstrom P (2001) Sugar-dependent alterations in cotyledon and leaf development in transgenic plants expressing the HDZhdip gene ATHB13. Plant Mol Biol 45:247–262

    Article  CAS  PubMed  Google Scholar 

  • Hong JC, Cheong YH, Nagao RT, Bahk JD, Cho MJ, Key JL (1994) Isolation and characterization of three soybean extensin cDNAs. Plant Physiol 104:793–796

    Article  CAS  PubMed  Google Scholar 

  • Horsch RB, Klee HJ, Stachel S, Winans SC, Nester EW, Rogers SG, Fraley RT (1986) Analysis of Agrobacterium tumefaciens virulence mutants in leaf discs. Proc Natl Acad Sci USA 83:2571–2575

    CAS  PubMed  Google Scholar 

  • Hsu BD, Lee JY, Pan RL (1986) The two binding sites for DCMU in photosystem II. Biochem Biophys Res Commun 141:682–688

    CAS  PubMed  Google Scholar 

  • Igamberdiev AU, Popov VN, Falaleeva MI (1995) Alternative system of succinate oxidation in glyoxysomes of higher plants. FEBS Lett 367:287–290

    Article  CAS  PubMed  Google Scholar 

  • Jang JC, Sheen J (1994) Sugar sensing in higher plants. Plant Cell 6:1665–1679

    Article  CAS  PubMed  Google Scholar 

  • Jang JC, Leon P, Zhou L, Sheen J (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell 9:5–19

    Article  CAS  PubMed  Google Scholar 

  • Kane MT, Buckley NJ (1977) The effects of inhibitors of energy metabolism on the growth of one-cell rabbit ova to blastocysts in vitro. J Reprod Fertil 49:261–266

    CAS  PubMed  Google Scholar 

  • Kim SR, Costa MA, An GH (1991) Sugar response element enhances wound response of potato proteinase inhibitor II promoter in transgenic tobacco. Plant Mol Biol 17:973–983

    CAS  PubMed  Google Scholar 

  • Koch KE, Ying Z, Wu Y, Avigne WT (2000) Multiple paths of sugar-sensing and a sugar/oxygen overlap for genes of sucrose and ethanol metabolism. J Exp Bot 51:417–427

    Article  CAS  PubMed  Google Scholar 

  • Leon J, Rojo E, Sanchez-Serrano JJ (2001) Wound signalling in plants. J Exp Bot 52:1–9

    Article  Google Scholar 

  • Loreti E, Alpi A, Perata P (2000) Glucose and disaccharide-sensing mechanisms modulate the expression of alpha-amylase in barley embryos. Plant Physiol 123:939–948

    CAS  PubMed  Google Scholar 

  • Memelink J, Swords KM, de Kam RJ, Schilperoort RA, Hoge JH, Staehelin LA (1993) Structure and regulation of tobacco extensin. Plant J 4:1011–1022

    Article  CAS  PubMed  Google Scholar 

  • Merkouropoulos G, Barnett DC, Shirsat AH (1999) The Arabidopsis extensin gene is developmentally regulated, is induced by wounding, methyl jasmonate, abscisic and salicylic acid, and codes for a protein with unusual motifs. Planta 208:212–219

    Article  CAS  PubMed  Google Scholar 

  • Narvaez-Vasquez J, Orozco-Cardenas ML, Ryan CA (1994) A Sulfhydryl reagent modulates systemic signaling for wound-induced and systemin-induced proteinase inhibitor synthesis. Plant Physiol 105:725–730

    CAS  PubMed  Google Scholar 

  • Ni M, Cui D, Gelvin SB (1996) Sequence-specific interactions of wound-inducible nuclear factors with mannopine synthase 2′ promoter wound-responsive elements. Plant Mol Biol 30:77–96

    CAS  PubMed  Google Scholar 

  • Parmentier Y, Durr A, Marbach J, Hirsinger C, Criqui MC, Fleck J, Jamet E (1995) A novel wound-inducible extensin gene is expressed early in newly isolated protoplasts of Nicotiana sylvestris. Plant Mol Biol 29:279–292

    CAS  PubMed  Google Scholar 

  • Ringli C, Keller B, Ryser U (2001) Glycine-rich proteins as structural components of plant cell walls. Cell Mol Life Sci 58:1430–1441

    CAS  PubMed  Google Scholar 

  • Salisbury FB, Ross CW (1992) Plant physiology, 4th edn. Wadsworth, Belmont, Calif.

  • Sheen J, Zhou L, Jang JC (1999) Sugars as signaling molecules. Curr Opin Plant Biol 2:410–418

    CAS  PubMed  Google Scholar 

  • Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5:9–23

    CAS  PubMed  Google Scholar 

  • Smeekens S (1998) Sugar regulation of gene expression in plants. Curr Opin Plant Biol 1:230–234

    CAS  PubMed  Google Scholar 

  • Strasser H, Matern V (1986) Minimal time requirement for lasting elicitor effects in cultured parsley cells. Z Naturforsch 41c:222-227

    Google Scholar 

  • Suzuki H, Wagner T, Tierney ML (1993) Differential expression of two soybean (Glycine max L.) proline-rich protein genes after wounding. Plant Physiol 101:1283–1287

    CAS  PubMed  Google Scholar 

  • Turgeon R, Medville R (1998) The absence of phloem loading in willow leaves. Proc Natl Acad Sci USA 95:12055–12060

    Article  CAS  PubMed  Google Scholar 

  • Van Oosten JJ, Gerbaud A, Huijser C, Dijkwel PP, Chua NH, Smeekens SC (1997) An Arabidopsis mutant showing reduced feedback inhibition of photosynthesis. Plant J 12:1011–1020

    Article  PubMed  Google Scholar 

  • Vasilyeva EA, Minkov IB, Fitin AF, Vinogradov AD (1982) Kinetic mechanism of mitochondrial adenosine triphosphatase. Inhibition by azide and activation by sulphite. Biochem J 202:15–23

    CAS  PubMed  Google Scholar 

  • Wobus U, Weber H (1999) Sugars as signal molecules in plant seed development. Biol Chem 380:937–944

    CAS  PubMed  Google Scholar 

  • Wu H, de Graaf B, Mariani C, Cheung AY (2001) Hydroxyproline-rich glycoproteins in plant reproductive tissues: structure, functions and regulation. Cell Mol Life Sci 58:1418–1429

    CAS  PubMed  Google Scholar 

  • Wycoff KL, Powell PA, Gonzales RA, Corbin DR, Lamb C, Dixon RA (1995) Stress activation of a bean hydroxyproline-rich glycoprotein promoter is superimposed on a pattern of tissue-specific developmental expression. Plant Physiol 109:41–52

    Article  CAS  PubMed  Google Scholar 

  • Ye ZH, Varner JE (1991) Tissue-specific expression of cell wall proteins in developing soybean tissues. Plant Cell 3:23–37

    Google Scholar 

  • Ye ZH, Song YR, Marcus A, Varner JE (1991) Comparative localization of three classes of cell wall proteins. Plant J 1:175–183

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Seung Kwan Yoo and Jeong Hwan Lee for their comments on this manuscript. We are also grateful to two anonymous reviewers for their perceptive comments. This research was supported by a grant from the Plant Metabolism Research Centre of Kyung Hee University (J. S. L.), a grant from Plant Signalling Network Research Centre of Korea University (J. H. A), and a grant from the Crop Functional Genomics Centre of the 21C Frontier Program of the Ministry of Science and Technology of Korea (J. H. A. and J. S. L.).

Author information

Authors and Affiliations

  1. School of Life Sciences and Biotechnology, Korea University, 136–701, Seoul , Korea

    J. H. Ahn

  2. School of Biological Sciences, Seoul National University, 152–742, Seoul, Korea

    J. S. Lee

Authors
  1. J. H. Ahn
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. S. Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. H. Ahn.

Additional information

Communicated by I.S. Chung

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ahn, J.H., Lee, J.S. Sugar acts as a regulatory signal on the wound-inducible expression of SbHRGP3::GUS in transgenic plants. Plant Cell Rep 22, 286–293 (2003). https://doi.org/10.1007/s00299-003-0685-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-003-0685-7

Keywords

Search

Navigation