Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1994 May;6(5):737–749. doi: 10.1105/tpc.6.5.737

Phosphate Modulates Transcription of Soybean VspB and Other Sugar-Inducible Genes.

A Sadka 1, D B DeWald 1, G D May 1, W D Park 1, J E Mullet 1
PMCID: PMC160472  PMID: 12244255

Abstract

The soybean vegetative storage protein genes VspA and VspB encode vacuolar glycoprotein acid phosphatases. Transcription of the Vsp is synergistically activated by jasmonic acid or methyl jasmonate (MeJA) and soluble sugars. The action of these modulators is mediated by two different DNA domains in the VspB promoter. In this study, we present new data regarding VspB regulation by sucrose and inorganic phosphate, which suggest a common mechanism of transcriptional control for Vsp and other sugar-inducible genes. We found that the sugar-mediated activation of VspB expression was inhibited by phosphate. Deletion analysis and transient assays in tobacco protoplasts identified a 130-bp DNA domain in the VspB promoter that mediates both sucrose induction and phosphate inhibition. Transcription mediated by this DNA domain was induced by phosphate elimination from the protoplast incubation medium, even in the absence of sucrose. The effect of sucrose and phosphate on VspB expression was studied in vivo in several ways. Depletion of phosphate from soybean cell cultures by the addition of mannose stimulated VspB expression, even in the absence of sucrose or MeJA. In illuminated soybean leaves treated with MeJA, inhibition of photosynthetic electron transport by DCMU decreased VspB expression. In contrast, VspB expression in soybean leaves stimulated by phosphate depletion was not influenced by DCMU. Moreover, sucrose-stimulated expression of the sugar-responsive genes lipoxygenase A and chalcone synthase of soybean and proteinase inhibitor II and class I patatin of potato was inhibited by phosphate. Like VspB, these genes were stimulated by phosphate depletion in the absence of exogenous sucrose. We propose that sugar-responsive genes are activated, in part, by accumulation of sugar-phosphates and concomitant reduction of cellular phosphate levels. These data may help explain recruitment of the Vsp, which encode acid phosphatases, as vegetative storage proteins.

Full Text

The Full Text of this article is available as a PDF (1.9 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aarts J. M., Hontelez J. G., Fischer P., Verkerk R., van Kammen A., Zabel P. Acid phosphatase-1(1), a tightly linked molecular marker for root-knot nematode resistance in tomato: from protein to gene, using PCR and degenerate primers containing deoxyinosine. Plant Mol Biol. 1991 Apr;16(4):647–661. doi: 10.1007/BF00023429. [DOI] [PubMed] [Google Scholar]
  2. Bell E., Mullet J. E. Lipoxygenase gene expression is modulated in plants by water deficit, wounding, and methyl jasmonate. Mol Gen Genet. 1991 Dec;230(3):456–462. doi: 10.1007/BF00280303. [DOI] [PubMed] [Google Scholar]
  3. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  4. Datla R. S., Hammerlindl J. K., Pelcher L. E., Crosby W. L., Selvaraj G. A bifunctional fusion between beta-glucuronidase and neomycin phosphotransferase: a broad-spectrum marker enzyme for plants. Gene. 1991 May 30;101(2):239–246. doi: 10.1016/0378-1119(91)90417-a. [DOI] [PubMed] [Google Scholar]
  5. DeWald D. B., Mason H. S., Mullet J. E. The soybean vegetative storage proteins VSP alpha and VSP beta are acid phosphatases active on polyphosphates. J Biol Chem. 1992 Aug 5;267(22):15958–15964. [PubMed] [Google Scholar]
  6. DeWald D. B., Sadka A., Mullet J. E. Sucrose Modulation of Soybean Vsp Gene Expression Is Inhibited by Auxin. Plant Physiol. 1994 Feb;104(2):439–444. doi: 10.1104/pp.104.2.439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Duff S. M., Lefebvre D. D., Plaxton W. C. Purification, characterization, and subcellular localization of an acid phosphatase from black mustard cell-suspension cultures: comparison with phosphoenolpyruvate phosphatase. Arch Biochem Biophys. 1991 Apr;286(1):226–232. doi: 10.1016/0003-9861(91)90033-f. [DOI] [PubMed] [Google Scholar]
  8. Duff S. M., Moorhead G. B., Lefebvre D. D., Plaxton W. C. Phosphate Starvation Inducible ;Bypasses' of Adenylate and Phosphate Dependent Glycolytic Enzymes in Brassica nigra Suspension Cells. Plant Physiol. 1989 Aug;90(4):1275–1278. doi: 10.1104/pp.90.4.1275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Duff S. M., Plaxton W. C., Lefebvre D. D. Phosphate-starvation response in plant cells: de novo synthesis and degradation of acid phosphatases. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9538–9542. doi: 10.1073/pnas.88.21.9538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Franceschi V. R., Grimes H. D. Induction of soybean vegetative storage proteins and anthocyanins by low-level atmospheric methyl jasmonate. Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6745–6749. doi: 10.1073/pnas.88.15.6745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Franceschi V. R., Wittenbach V. A., Giaquinta R. T. Paraveinal Mesophyll of Soybean Leaves in Relation to Assimilate Transfer and Compartmentation : III. Immunohistochemical Localization of Specific Glycopeptides in the Vacuole after Depodding. Plant Physiol. 1983 Jun;72(2):586–589. doi: 10.1104/pp.72.2.586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Goldstein A. H., Baertlein D. A., McDaniel R. G. Phosphate Starvation Inducible Metabolism in Lycopersicon esculentum: I. Excretion of Acid Phosphatase by Tomato Plants and Suspension-Cultured Cells. Plant Physiol. 1988 Jul;87(3):711–715. doi: 10.1104/pp.87.3.711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Huber S. C., Huber J. L. Role of sucrose-phosphate synthase in sucrose metabolism in leaves. Plant Physiol. 1992 Aug;99(4):1275–1278. doi: 10.1104/pp.99.4.1275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jefferson R., Goldsbrough A., Bevan M. Transcriptional regulation of a patatin-1 gene in potato. Plant Mol Biol. 1990 Jun;14(6):995–1006. doi: 10.1007/BF00019396. [DOI] [PubMed] [Google Scholar]
  15. Kim S. R., Costa M. A., An G. H. Sugar response element enhances wound response of potato proteinase inhibitor II promoter in transgenic tobacco. Plant Mol Biol. 1991 Nov;17(5):973–983. doi: 10.1007/BF00037137. [DOI] [PubMed] [Google Scholar]
  16. Lefebvre D. D., Duff S. M., Fife C. A., Julien-Inalsingh C., Plaxton W. C. Response to Phosphate Deprivation in Brassica nigra Suspension Cells : Enhancement of Intracellular, Cell Surface, and Secreted Phosphatase Activities Compared to Increases in Pi-Absorption Rate. Plant Physiol. 1990 Jun;93(2):504–511. doi: 10.1104/pp.93.2.504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mason H. S., DeWald D. B., Mullet J. E. Identification of a methyl jasmonate-responsive domain in the soybean vspB promoter. Plant Cell. 1993 Mar;5(3):241–251. doi: 10.1105/tpc.5.3.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mason H. S., Mullet J. E. Expression of two soybean vegetative storage protein genes during development and in response to water deficit, wounding, and jasmonic acid. Plant Cell. 1990 Jun;2(6):569–579. doi: 10.1105/tpc.2.6.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Müller-Röber B. T., Kossmann J., Hannah L. C., Willmitzer L., Sonnewald U. One of two different ADP-glucose pyrophosphorylase genes from potato responds strongly to elevated levels of sucrose. Mol Gen Genet. 1990 Oct;224(1):136–146. doi: 10.1007/BF00259460. [DOI] [PubMed] [Google Scholar]
  20. Oshima Y. Impact of the Douglas-Hawthorne model as a paradigm for elucidating cellular regulatory mechanisms in fungi. Genetics. 1991 Jun;128(2):195–201. doi: 10.1093/genetics/128.2.195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ryan C. A. Oligosaccharide signalling in plants. Annu Rev Cell Biol. 1987;3:295–317. doi: 10.1146/annurev.cb.03.110187.001455. [DOI] [PubMed] [Google Scholar]
  22. Salanoubat M., Belliard G. The steady-state level of potato sucrose synthase mRNA is dependent on wounding, anaerobiosis and sucrose concentration. Gene. 1989 Dec 7;84(1):181–185. doi: 10.1016/0378-1119(89)90153-4. [DOI] [PubMed] [Google Scholar]
  23. Schulze-Lefert P., Dangl J. L., Becker-André M., Hahlbrock K., Schulz W. Inducible in vivo DNA footprints define sequences necessary for UV light activation of the parsley chalcone synthase gene. EMBO J. 1989 Mar;8(3):651–656. doi: 10.1002/j.1460-2075.1989.tb03422.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Spilatro S. R., Anderson J. M. Characterization of a soybean leaf protein that is related to the seed lectin and is increased with pod removal. Plant Physiol. 1989 Aug;90(4):1387–1393. doi: 10.1104/pp.90.4.1387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Staswick P. E. Developmental regulation and the influence of plant sinks on vegetative storage protein gene expression in soybean leaves. Plant Physiol. 1989 Jan;89(1):309–315. doi: 10.1104/pp.89.1.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Staswick P. E., Huang J. F., Rhee Y. Nitrogen and methyl jasmonate induction of soybean vegetative storage protein genes. Plant Physiol. 1991 May;96(1):130–136. doi: 10.1104/pp.96.1.130. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Staswick P. E. Novel Regulation of Vegetative Storage Protein Genes. Plant Cell. 1990 Jan;2(1):1–6. doi: 10.1105/tpc.2.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Staswick P. E. Soybean vegetative storage protein structure and gene expression. Plant Physiol. 1988 May;87(1):250–254. doi: 10.1104/pp.87.1.250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Theodorou M. E., Elrifi I. R., Turpin D. H., Plaxton W. C. Effects of Phosphorus Limitation on Respiratory Metabolism in the Green Alga Selenastrum minutum. Plant Physiol. 1991 Apr;95(4):1089–1095. doi: 10.1104/pp.95.4.1089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Theodorou M. E., Plaxton W. C. Metabolic Adaptations of Plant Respiration to Nutritional Phosphate Deprivation. Plant Physiol. 1993 Feb;101(2):339–344. doi: 10.1104/pp.101.2.339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Tranbarger T. J., Franceschi V. R., Hildebrand D. F., Grimes H. D. The soybean 94-kilodalton vegetative storage protein is a lipoxygenase that is localized in paraveinal mesophyll cell vacuoles. Plant Cell. 1991 Sep;3(9):973–987. doi: 10.1105/tpc.3.9.973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Uesono Y., Tokai M., Tanaka K., Tohe A. Negative regulators of the PHO system of Saccharomyces cerevisiae: characterization of PHO80 and PHO85. Mol Gen Genet. 1992 Feb;231(3):426–432. doi: 10.1007/BF00292712. [DOI] [PubMed] [Google Scholar]
  33. Ullah A. H., Gibson D. M. Purification and characterization of acid phosphatase from cotyledons of germinating soybean seeds. Arch Biochem Biophys. 1988 Feb 1;260(2):514–520. doi: 10.1016/0003-9861(88)90476-6. [DOI] [PubMed] [Google Scholar]
  34. Vogel K., Hinnen A. The yeast phosphatase system. Mol Microbiol. 1990 Dec;4(12):2013–2017. doi: 10.1111/j.1365-2958.1990.tb00560.x. [DOI] [PubMed] [Google Scholar]
  35. Vogel K., Hörz W., Hinnen A. The two positively acting regulatory proteins PHO2 and PHO4 physically interact with PHO5 upstream activation regions. Mol Cell Biol. 1989 May;9(5):2050–2057. doi: 10.1128/mcb.9.5.2050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Walker-Simmons M., Ryan C. A. Immunological Identification of Proteinase Inhibitors I and II in Isolated Tomato Leaf Vacuoles. Plant Physiol. 1977 Jul;60(1):61–63. doi: 10.1104/pp.60.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Weiner H., McMichael R. W., Huber S. C. Identification of factors regulating the phosphorylation status of sucrose-phosphate synthase in vivo. Plant Physiol. 1992 Aug;99(4):1435–1442. doi: 10.1104/pp.99.4.1435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wenzler H., Mignery G., Fisher L., Park W. Sucrose-regulated expression of a chimeric potato tuber gene in leaves of transgenic tobacco plants. Plant Mol Biol. 1989 Oct;13(4):347–354. doi: 10.1007/BF00015546. [DOI] [PubMed] [Google Scholar]
  39. Wittenbach V. A. Effect of pod removal on leaf senescence in soybeans. Plant Physiol. 1982 Nov;70(5):1544–1548. doi: 10.1104/pp.70.5.1544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wittenbach V. A. Purification and characterization of a soybean leaf storage glycoprotein. Plant Physiol. 1983 Sep;73(1):125–129. doi: 10.1104/pp.73.1.125. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES