Skip to main content
SpringerLink
Log in

Distinct cis-acting elements direct the germination and sugar responses of the cucumber malate synthase gene

  • Original Paper
  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Abstract

The malate synthase gene (ms) promoter in cucumber (Cucumis sativus L.) was investigated with the aim of distinguishing DNA sequences mediating regulation of gene expression by sugar, and expression following seed germination. Promoter deletions were constructed and their ability to direct expression of theβ-glucuronidase (gus) reporter gene was investigated in transgenicNicotiana plumbaginifolia. Gene expression was assayed in germinating seeds and developing seedlings (the germination response) and in seedlings transferred from light into darkness with and without sucrose (the sugar response). As progressively more of the promoter was deleted from the 5′ end, first the sugar response and then the germination response was lost. Thus, distinct regions of the promoter are required for carbohydrate control and for regulation of gene expression in response to germination. Sequence comparisons of thems promoter with that of the isocitrate lyase gene (icl) of cucumber have previously identified four IMH (ICL-MS Homology) sequences. One such sequence, IMH2, is shown here to be implicated in the sugar response of thems gene. The 17 bp sequence, which when deleted from thems gene results in loss of the germination response, contains a 14 bp sequence which is similar to a sequence in theicl promoter, which we refer to as IMH5. Furthermore, this sequence has similarity withamdI9-like sequences in filamentous fungi, which conferfacB-mediated acetate inducibility on several genes, including those encoding ICL and MS.

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

References

  • Beevers H (1980) The role of the glyoxylate cycle. In: Stumpf PK (ed) The biochemistry of plants. A comprehensive treatise, vol 4. Academic Press, New York, pp 117–130

    Google Scholar 

  • Beevers H (1979) Microbodies in higher plants. Ann Rev Plant Physiol 30:159–193

    Article  Google Scholar 

  • Birkhan R, Kindl H (1990) Re-activation of the expression of glyoxysomal genes in green plant tissue. Z Naturforsch 45:107–111

    Google Scholar 

  • Comai L, Dietrich RA, Maslyar DJ, Baden CS, Harada JJ (1989) Coordinate expression of transcriptionally regulated isocitrate lyase and malate synthase genes inBrassica napus L. Plant Cell 1:293–300

    Article  PubMed  Google Scholar 

  • De Bellis L, Picciarelli P, Pistelli L, Alpi A (1990) Localisation of glyoxylate-cycle marker enzymes in peroxisomes of senescent leaves and green cotyledons. Planta 180:435–439

    Article  Google Scholar 

  • De Bellis L, Tsugeki R, Nishimura M (1991) Glyoxylate cycle enzymes in peroxisomes isolated from petals of pumpkin (Cucurbita sp.) during senescence. Plant Cell Physiol. 32:1227–1235

    Google Scholar 

  • Draper J, Scott R, Armitage P, Walden P (1988) Plant genetic transformation and gene expression: a laboratory manual. Blackwell Scientific Publications, Oxford

    Google Scholar 

  • Goldsbrough AP, Albrecht H, Stratford R (1993) Salicylic acid-inducible binding of a tobacco nuclear protein to a 10 bp sequence which is highly conserved amongst stress-inducible genes. Plant J 3:563–571

    Article  PubMed  Google Scholar 

  • Graham IA, Smith LS, Brown JWS, Leaver CJ, Smith SM (1989) The malate synthase gene of cucumber. Plant Mol Biol 13:673–684

    Article  PubMed  Google Scholar 

  • Graham IA, Smith LM, Leaver CJ, Smith SM (1990) Developmental regulation of expression of the malate synthase gene in transgenic plants. Plant Mol Biol 15:539–549

    Article  PubMed  Google Scholar 

  • Graham IA, Leaver CJ, Smith SM (1992) Induction of malate synthase gene expression in senescent and detached organs of cucumber. Plant Cell 4:349–357

    Article  PubMed  Google Scholar 

  • Graham IA, Denby KJ, Leaver CJ (1994a) Carbon catabolite repression regulates glyoxylate cycle gene expression in cucumber. Plant Cell 6:761–772

    Article  PubMed  Google Scholar 

  • Graham IA, Baker CJ, Leaver CJ (1994b) Analysis of the cucumber malate synthase gene promoter by transient expression and gel retardation assays. Plant J 6:893–902

    Article  PubMed  Google Scholar 

  • Grierson C, Du J-S, de Torres Zabala M, Beggs K, Smith C, Holdsworth M, Bevan M (1994) Separatecis sequences andtrans factors direct metabolic and developmental regulation of a potato tuber storage protein gene. Plant J 5:815–826

    Article  PubMed  Google Scholar 

  • Grotewold E, Drummond BJ, Bowen B, Peterson T (1994) Themyb-homologousP gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell 76:543–553

    Article  PubMed  Google Scholar 

  • Gut H, Matile P (1988) Apparent induction of key enzymes of the glyoxylic acid cycle in senescent barley leaves. Planta 176:548–550

    Article  Google Scholar 

  • Hoekema A, Hirsch PR, Hooykaas PJJ, Schilperoort RA (1983) A binary plant vector strategy based on separation ofvir- and T-regions of theAgrobacterium tumefaciens Ti-plasmid. Nature 303:179–180

    Article  Google Scholar 

  • Hynes MJ (1977) Induction of the acetamidase gene ofAspergillus nidulans by acetate metabolism. J Bacteriol 131:770–775

    PubMed  Google Scholar 

  • Huang AHC, Telease RN, Moore TS (1983) Plant peroxisomes. Academic Press, New York

    Google Scholar 

  • Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5:387–405

    Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions:β-glucuronidase as a sensitive gene fusion marker in higher plants. EMBO J 6:3901–3907

    PubMed  Google Scholar 

  • Jones DSC, Schofield JP (1991) A rapid method for isolating high quality plasmid DNA suitable for sequencing. Nucleic Acids Res 18:7463–7464

    Google Scholar 

  • Kim D-J, Smith SM (1994a) Molecular cloning of cucumber phosphoenolpyruvate carboxykinase and developmental regulation of gene expression. Plant Mol Biol 26:423–434

    Article  PubMed  Google Scholar 

  • Kim D-J, Smith SM (1994b) Expression of a single gene encoding microbody NAD-malate dehydrogenase during glyoxysome and peroxisome development in cucumber. Plant Mol Biol 26:1833–1841

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Kudielka RA, Theimer RR (1983a) Derepression of glyoxylate cycle enzyme activities in anise suspension culture cells. Plant Sci Lett 31:237–244

    Article  Google Scholar 

  • Kudielka RA, Theimer RR (1983b) Repression of glyoxysomal enzyme activities in anise (Pimpinella anisum L.) suspension cultures. Plant Sci Letts 31:245–252

    Article  Google Scholar 

  • McLaughlin JC, Smith SM (1994) Metabolic regulation of glyoxylate-cycle enzyme synthesis in detached cucumber cotyledons and protoplasts. Planta 195:22–28

    Article  Google Scholar 

  • McLaughlin JC, Smith SM (1995) Glyoxylate cycle enzyme synthesis during the irreversible phase of senescence of cucumber cotyledons. J Plant Physiol 146:133–138

    Google Scholar 

  • Pistelli L, De Bellis L, Alpi A (1991) Peroxisomal enzyme activities in attached senescing leaves. Planta 184:151–153

    Article  Google Scholar 

  • Reynolds SJ, Smith SM (1995) The isocitrate lyase gene of cucumber: isolation, characterisation and expression in cotyledons following seed germination. Plant Mol Biol 27:487–497

    Article  PubMed  Google Scholar 

  • Rocha-Sosa M, Sonnewald U, Frommer W, Stratmann M, Schell J, Willmitzer L (1989) Both developmental and metabolic signals activate the promoter of a class I patatin gene. EMBO J 8:23–31

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual (2nd edn). Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Sandeman RA, Hynes MJ (1989) Isolation of thefacA (acetyl-CoenzymeA synthetase) andacuE (malate synthase) genes ofAspergillus nidulans. Mol Gen Genet 218:87–92

    Article  PubMed  Google Scholar 

  • Sandeman RA, Hynes MJ, Fincham JRS, Connerton IF (1991) Molecular organisation of the malate synthase genes ofAspergillus nidulans andNeurospora crassa. Mol Gen Genet 228:445–452

    Article  PubMed  Google Scholar 

  • Sheen J (1990) Metabolic repression of transcription in higher plants. Plant Cell 2:1027–1038

    PubMed  Google Scholar 

  • Tolbert NE (1980) Microbodies — peroxisomes and glyoxysomes. In: Stumpf PK (ed) The biochemistry of plants: a comprehensive treatise. Vol 1 359–388

  • Turley RB, Trelease RN (1990) Development and regulation of three glyoxylate cycle enzymes during cotton seed maturation and growth. Plant Mol Biol 14:137–146

    Article  PubMed  Google Scholar 

  • Wanner L, Keller F, Matile P (1991) Metabolism of radio-labelled galactolipids in senescent barley leaves. Plant Sci 78:199–206

    Article  Google Scholar 

  • Weir EM, Riezman H, Grienenberger J-M, Becker WM, Leaver CJ (1980) Regulation of glyoxysomal enzymes during germination of cucumber. Eur J Biochem 112:469–477

    PubMed  Google Scholar 

  • Zhang JZ, Laudencia-Chingcuanco DL, Comai L, Li M, Harada JJ (1994) Isocitrate lyase and malate synthase genes fromBrassica napus L. are active in pollen. Plant Physiol 104:857–864

    Article  PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Caroline J. Sarah

    Present address: Department of Biological Sciences, University of Durham, South Road, DH1 3LE, Durham, UK

  2. Ian A. Graham

    Present address: Division of Biochemistry and Molecular Biology, University of Glasgow, G12 8QQ, Glasgow, UK

Authors and Affiliations

  1. Institute of Cell and Molecular Biology, The University of Edinburgh, The King's Buildings, Mayfield Road, EH9 3JH, Edinburgh, UK

    Caroline J. Sarah, Susan J. Reynolds & Steven M. Smith

  2. Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB, Oxford, UK

    Ian A. Graham & Christopher J. Leaver

Authors
  1. Caroline J. Sarah
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ian A. Graham
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Susan J. Reynolds
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christopher J. Leaver
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Steven M. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by J. Schell

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sarah, C.J., Graham, I.A., Reynolds, S.J. et al. Distinct cis-acting elements direct the germination and sugar responses of the cucumber malate synthase gene. Molec. Gen. Genet. 250, 153–161 (1996). https://doi.org/10.1007/BF02174174

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02174174

Key words

Search

Navigation