Russian Journal of Plant Physiology

, Volume 54, Issue 3, pp 350–359 | Cite as

Organ-specificity and inducibility of patatin class I promoter from potato in transgenic arabidopsis plants

  • E. M. Naumkina
  • Yu. P. Bolyakina
  • G. A. Romanov
Research Papers

Abstract

Patatin class I promoter (B33 promoter) is a tissue-specific potato (Solanum tuberosum L.) promoter expressing the patatin gene mainly in tubers. However, it can be induced in other organs by sucrose or light. We compared the activity of this promoter fused with the reporter gene during heterological expression in B33::GUS transgenic arabidopsis (Arabidopsis thaliana L.) plants and homological expression of the same DNA construct in potato. Promoter activity was estimated from quantification of β-glucuronidase (GUS) activity. It was shown that, during heterological expression in arabidopsis seedlings, B33 promoter manifested a tissue-specificity and inducibility, although in a different manner than during homological expression in potato. In noninduced arabidopsis seedlings, B33 promoter was most active in the roots, whereas, after induction with sucrose treatment, it became most active in cotyledons. 10 mM sucrose was sufficient for a manifold activation of B33 promoter in intact seedlings. The degree of B33 promoter induction by sucrose in arabidopsis seedlings was strictly organ-specific and increased in the following sequence: root < hypocotyl < cotyledons. 150–200 mM sucrose enhanced B33 promoter activity in cotyledons by 200 to 300 times, i.e., much stronger than in potato organs. Glucose and fructose were less efficient than sucrose. Phytohormones affecting tuber formation in potato (gibberellins, auxins, and cytokinins) did not affect significantly B33 promoter activity in arabidopsis. A lag period of approximately 6 h preceded sucrose-induced B33 promoter activation. This indicates that the patatin promoter is not the primary target for the sucrose signal. The quantitative examination of heterological expression of patatin class I promoter further clarifies its basic functional characteristics and permits a better prognosis of its behavior after transferring into other plant species.

Key words

Arabidopsis thaliana Solanum tuberosum patatin B33 promoter heterological gene expression sugar inducibility light inducibility sucrose GUS 

Abbreviations

BA

benzyladenine

GUS

β-glucuronidase

MU

4-methylumbelliferone

MUG

4-methylumbelliferyl-β-glucuronide

X-Gluc

5-bromo-4-chloro-3-indolyl-β-D-glucuronic acid

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Bur’yanov, Ya.I., Advances in Plant Gene Engineering Biotechnology, Russ. J. Plant Physiol., 1999, vol. 46, pp. 818–830.Google Scholar
  2. 2.
    Romanov, G.A., Plant Genetic Engineering and the Biosafety Problem, Russ. J. Plant Physiol., 2000, vol. 47, pp. 303–311.Google Scholar
  3. 3.
    Piruzyan, E.S., Kobets, N.S., Mett, V.L., Serebriiskaya, T.S., Neumyvakin, L.V., Alizade, Kh., Lenets, A.A., Simonova, M.L., Shevelukha, V.S., and Goldenkova, I.V., Transgenic Plants Expressing Foreign Genes as a Model for Studying Plant Stress Responses and a Source for Resistant Plant Forms, Russ. J. Plant Physiol., 2000, vol. 47, pp. 327–336.Google Scholar
  4. 4.
    Mignery, G.A., Pikaard, C.S., and Park, W.D., Molecular Characterization of the Patatin Multigene Family of Potato, Gene, 1988, vol. 62, pp. 27–41.PubMedCrossRefGoogle Scholar
  5. 5.
    Stupar, R.M., Beaubien, K.A., Jin, W., Song, J., Lee, M.-K., Wu, C., Zhang, H.-B., Han, B., and Jiang, J., Structural Diversity and Differential Transcription of the Patatin Multicopy Gene Family during Potato Tuber Development, Genetics, 2006, vol. 172, pp. 1263–1275.PubMedCrossRefGoogle Scholar
  6. 6.
    Paiva, E., Lister, R.M., and Park, W.D., Induction and Accumulation of Major Tuber Proteins of Potato in Stems and Petioles, Plant Physiol., 1983, vol. 71, pp. 161–168.PubMedCrossRefGoogle Scholar
  7. 7.
    Pikaard, C.S., Brusca, J.S., Hannapel, D.J., and Park, W.D., The Two Classes of Genes for the Major Potato Tuber Protein, Patatin, Are Differentially Expressed in Tubers and Roots, Nucleic Acids Res., 1987, vol. 15, pp. 1979–1994.PubMedCrossRefGoogle Scholar
  8. 8.
    Rocha-Sosa, M., Sonnewald, U., Frommer, W., Stratmann, M., Schell, J., and Willmitzer, L., Both Developmental and Metabolic Signals Activate the Promoter of a Class I Patatin Gene, EMBO J., 1989, vol. 8, pp. 23–29.PubMedGoogle Scholar
  9. 9.
    Jefferson, R., Goldsbrough, A., and Bevan, M., Transcriptional Regulation of a Patatin-1 Gene in Potato, Plant Mol. Biol., 1990, vol. 14, pp. 995–1006.PubMedCrossRefGoogle Scholar
  10. 10.
    Liu, X.J., Prat, S., Willmitzer, L., and Frommer, W.B., Cis Regulatory Elements Directing Tuber-Specific and Sucrose-Inducible Expression of a Chimeric Class I Patatin Promoter/GUS-Gene Fusion, Mol. Gen. Genet., 1990, vol. 223, pp. 401–406.PubMedCrossRefGoogle Scholar
  11. 11.
    Grierson, C., Du, J.-S., de Torres-Zabala, M., Beggs, K., Smith, C., Holdsworth, M., and Bevan, M., Separate Cis Sequences and Trans Factors Direct Metabolic and Developmental Regulation of a Potato Tuber Storage Protein Gene, Plant J., 1994, vol. 5, pp. 815–826.PubMedCrossRefGoogle Scholar
  12. 12.
    Kim, S.Y., May, G.D., and Park, W.D., Nuclear Protein Factors Binding to a Class I Patatin Promoter Region Are Tuber-Specific and Sucrose-Inducible, Plant Mol. Biol., 1994, vol. 26, pp. 603–615.PubMedCrossRefGoogle Scholar
  13. 13.
    Zourelidou, M., de Torres-Zabala, M., Smith, C., and Bevan, M.V., Storekeeper Defines a New Class of Plant-Specific DNA-Binding Proteins and a Putative Regulator of Patatin Expression, Plant J., 2002, vol. 30, pp. 489–497.PubMedCrossRefGoogle Scholar
  14. 14.
    Koster-Topfer, M., Frommer, W.B., Rocha-Sosa, M., Rosahl, S., Schell, J., and Willmitzer, L., A Class II Patatin Promoter Is under Developmental Control in Both Transgenic Potato and Tobacco Plants, Mol. Gen. Genet., 1989, vol. 219, pp. 390–396.PubMedCrossRefGoogle Scholar
  15. 15.
    Zvereva, S.D. and Romanov, G.A., Reporter Genes for Plant Genetic Engineering: Characteristics and Detection, Russ. J. Plant Physiol., 2000, vol. 47, pp. 424–432.Google Scholar
  16. 16.
    Swartzberg, D., Dai, N., Gan, S., Amasino, R., and Granot, D., Effects of Cytokinin Production under Two SAG Promoters on Senescence and Development of Tomato Plants, Plant Biol., 2006, vol. 8, pp. 579–586.PubMedCrossRefGoogle Scholar
  17. 17.
    Cazzonelli, C.I., McCallum, E.J., Lee, R., and Botella, J.R., Characterization of a Strong, Constitutive Mung Bean (Vigna radiata L.) Promoter with a Complex Mode of Regulation In Planta, Transgen. Res., 2005, vol. 14, pp. 941–967.CrossRefGoogle Scholar
  18. 18.
    Martin, T., Hellmann, H., Schmidt, R., Willmitzer, L., and Frommer, W.B., Identification of Mutants in Metabolically Regulated Gene Expression, Plant J., 1997, vol. 11, pp. 53–62.PubMedCrossRefGoogle Scholar
  19. 19.
    Hellmann, H., Funck, D., Rentsch, D., and Frommer, W.B., Hypersensitivity of an Arabidopsis Sugar Signalling Mutant toward Exogenous Proline Application, Plant Physiol., 2000, vol. 123, pp. 779–790.PubMedCrossRefGoogle Scholar
  20. 20.
    Mirzabekov, A.D., Gryadunov, D.A., Mikhailovich, V.M., Zasedatelev, A.C., Romanov, G.A., Kusnetsov, V.V., Tsydendambaev, V.D., and Krylova, E.M., Technique for Identification of Transgenic DNA Sequences in Plant Material and in Its Basic Products, Oligonucleotide Kit, and Biochip of This Method, RF Patent no. 2270254, Byull. Izobret., 2006, no. 5.Google Scholar
  21. 21.
    Aksenova, N.P., Konstantinova, T.N., Golyanovskaya, S.A., Kossmann, J., Willmitzer, L., and Romanov, G.A., Transformed Potato Plants as a Model for Studying the Hormonal and Carbohydrate Regulation of Tuberization, Russ. J. Plant Physiol., 2000, vol. 47, pp. 370–379.Google Scholar
  22. 22.
    Romanov, G.A., Kieber, J.J., and Schmülling, T.A., A Rapid Cytokinin Response Assay in Arabidopsis Indicates a Role for Phospholipase D in Cytokinin Signalling, FEBS Lett., 2002, vol. 515, pp. 39–43.PubMedCrossRefGoogle Scholar
  23. 23.
    Bradford, M.M., A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding, Anal. Biochem., 1976, vol. 72, pp. 248–254.PubMedCrossRefGoogle Scholar
  24. 24.
    Vreugdenhil, D. and Sergeeva, L.I., Gibberellins and Tuberization in Potatoes, Potato Res., 1999, vol. 42, pp. 192–201.CrossRefGoogle Scholar
  25. 25.
    Romanov, G.A., Aksenova, N.P., Konstantinova, T.N., Golyanovskaya, S.A., Kossmann, J., and Willmitzer, L., Effect of Indole-3-Acetic Acid and Kinetin on Tuberization Parameters of Different Cultivars and Transgenic Lines of Potato In Vitro, Plant Growth Regul., 2000, vol. 32, pp. 245–251.CrossRefGoogle Scholar
  26. 26.
    Deryabin, A.N., Trunova, T.I., Dubinina, I.M., Burakhanova, E.A., Sabel’nikova, E.P., Krylova, E.M., and Romanov, G.A., Chilling Tolerance of Potato Plants Transformed with a Yeast-Derived Invertase Gene under the Control of the B33 Patatin Promoter, Russ. J. Plant Physiol., 2003, vol. 50, pp. 449–454.CrossRefGoogle Scholar
  27. 27.
    Song, D.G., Zhou, J., Huang, D.Q., Ma, H., Situ, J.F., Wang, G.Q., and Wang, X.M., 1.4 kb 5′Flanking Region of Class I Patatin Directs Tuber-Specific GUS Expression in Potato (Solanum tuberosum L.), Shi Yan Sheng Wu Xue Bao, 2001, vol. 34, pp. 5–10.PubMedGoogle Scholar
  28. 28.
    Perl, A., Aviv, D., Willmitzer, L., and Galun, E., In Vitro Tuberization in Transgenic Potatoes Harboring β-Glucuronidase Linked to a Patatin Promoter: Effects of Sucrose Levels and Photoperiods, Plant Sci., 1991, vol. 73, pp. 87–95.CrossRefGoogle Scholar
  29. 29.
    Koch, K.E., Carbohydrate-Modulated Gene Expression in Plants, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1996, vol. 47, pp. 509–540.PubMedCrossRefGoogle Scholar
  30. 30.
    Smeekens, S., Sugar-Induced Signal Transduction in Plant, Annu. Rev. Plant Phys. Plant Mol. Biol., 2000, vol. 51, pp. 49–81.CrossRefGoogle Scholar
  31. 31.
    Gibson, S.I., Control of Plant Development and Gene Expression by Sugar Signaling, Curr. Opin. Plant Biol., 2005, vol. 8, pp. 93–102.PubMedCrossRefGoogle Scholar
  32. 32.
    Gonzali, S., Loreti, E., Solfanelli, C., Novi, G., Alpi, A., and Perata, P., Identification of Sugar-Modulated Genes and Evidence for in vivo Sugar Sensing in Arabidopsis, J. Plant Res., 2006, vol. 119, pp. 115–123.PubMedCrossRefGoogle Scholar
  33. 33.
    Vanyushin, B.F., Enzymatic DNA Methylation — Epigenetic Control of Genetic Functions in the Cells, Biokhimiya, 2005, vol. 70, pp. 598–611.Google Scholar
  34. 34.
    Ewing, E.E., The Role of Hormones in Potato (Solanum tuberosum L.) Tuberization, Plant Hormones, Physiology, Biochemistry and Molecular Biology, Davies, P.J., Ed., Dordrecht: Kluwer, 1995, pp. 698–724.Google Scholar
  35. 35.
    Chailakhyan, M.Kh., Fotoperiodicheskaya i gormonal’naya regulyatsiya tuberizatsii u rastenii (Photoperiodic and Hormonal Regulation of Tuberization in Plants), Moscow: Nauka, 1984.Google Scholar
  36. 36.
    Vreugdenhil, D. and Struik, P.C., An Integrated View of the Hormonal Regulation of Tuber Formation in Potato (Solanum tuberosum L.), Physiol. Plant., 1989, vol. 75, pp. 525–531.CrossRefGoogle Scholar
  37. 37.
    Hannapel, D.J., Miller, J.C., and Park, W.D., Regulation of Potato Tuber Protein Accumulation by Gibberellic Acid, Plant Physiol., 1985, vol. 78, pp. 700–703.PubMedGoogle Scholar
  38. 38.
    Park, W.D., Molecular Approaches to Tuberization in Potato, The Molecular and Cellular Biology of the Potato, Vayda, M.E. and Park, W.D., Eds., Melksam (UK): C.A.B. Int. Redwood Press, 1990, pp. 43–56.Google Scholar
  39. 39.
    Ganal, M.W., Bonierbale, M.W., Roeder, M.S., Park, W.D., and Tanksley, S.D., Genetic and Physical Mapping of the Patatin Genes in Potato and Tomato, Mol. Gen. Genet., 1991, vol. 225, pp. 501–509.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2007

Authors and Affiliations

  • E. M. Naumkina
    • 1
  • Yu. P. Bolyakina
    • 1
  • G. A. Romanov
    • 1
  1. 1.Timiryazev Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia

Personalised recommendations