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Analysis of the region in between two closely linked patatin genes: class II promoter activity in tuber, root and leaf

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Abstract

From a potato genomic library a phage lambda clone was isolated that carried nucleotide sequences of two patatin genes, thus demonstrating a close physical linkage between these two members of the patatin gene family. Sequence and restriction analysis showed the genes to be oriented in tandem. The more upstream gene was a pseudogene truncated at the 3′ end, whereas the downstream gene was a class II patatin gene. In addition to a 208 bp fragment also present in patatin class I promoters, the region in between both genes contained various direct repeats also found in other patatin genes. To study the promoter activity of this intergenic region, a 2.78 kb fragment was transcriptionally fused to the β-glucuronidase gene and reintroduced into potato cultivar Bintje. Histochemical analysis revealed expression in the outermost layer of cells of the cortex, in the tuber phellogen, in or around the root vascular system, and also in the abaxial phloem layer of the vascular bundle in leaves.

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References

  1. Andrews DL, Beames B, Summers MD, Park WD: Characterisation of the lipid acyl hydrolase activity of the major potato tuber protein, patatin, by cloning and abundant expression in a baculovirus vector. Biochem J 252: 199–206 (1988).

    Google Scholar 

  2. Bevan MW: Binary Agrobacterium vectors for plant transformation. Nucl Acids Res 12: 8711–8721 (1984).

    Google Scholar 

  3. Bevan MW: Gene activity during tuber formation in the potato (Solanum tuberosum). In: Grierson D (ed) Developmental Regulation of Plant Gene Expression, pp. 75–93. Chapman and Hall, New York (1991).

    Google Scholar 

  4. Bevan M, Barker R, Goldsbrough A, Jarvis M, Kavanagh T, Iturriaga G: The structure and transcription start site of a major potato tuber protein gene. Nucl Acids Res 14: 4625–4638 (1986).

    Google Scholar 

  5. Blundy KS, Blundy MAC, Carter D, Wilson F, Park WD, Burrell MM: The expression of class I patatin gene fusions in transgenic potato varies with both gene and cultivar. Plant Mol Biol 16: 153–160 (1991).

    Google Scholar 

  6. Bonierbale MW, Plaisted RL, Tanksley SD: RFLP maps based on a common set of clones reveal modes of chromosomal evolution in potato and tomato. Genetics 120: 1095–1103 (1988).

    Google Scholar 

  7. Bradford M: A rapid and sensitive method for the quantitation of microgram amounts of protein using the principle of dye binding. Anal Biochem 72: 248–252 (1976).

    Google Scholar 

  8. Cutter EG: Structure and development of the potato plant. In: Harris PM (ed) The Potato Crop, pp. 70–152. Chapman and Hall, New York (1982).

    Google Scholar 

  9. Dellaporta SL, Wood J, Hicks JB: A plant DNA minipreparation: version II. Plant Mol Biol Rep 1: 19–21 (1983).

    Google Scholar 

  10. Devereux J, Haeberli P, Smithies O: A comprehensive set of sequence analysis programs for the VAX. Nucl Acids Res 12: 387–395 (1984).

    Google Scholar 

  11. Ditta G, Stanfield S, Corbin D, Helinski DR: Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc Natl Acad Sci USA 77: 7347–7351 (1980).

    Google Scholar 

  12. Frischauf AM, Lehrach H, Poustka A, Murray N: Lambda replacement vectors carrying polylinker sequences. J Mol Biol 170: 827–842 (1983).

    Google Scholar 

  13. Ganal MW, Bonierbale MW, Roeder MS, Park WD, Tanksley SD: Genetic and physical mapping of the patatin genes in potato and tomato. Mol Gen Genet 225: 501–509 (1991).

    Google Scholar 

  14. Gebhardt C, Ritter E, Debener T, Schachtschabel U, Walkemeier B, Uhrig H, Salamini F: RFLP analysis and linkage mapping in Solanum tuberosum. Theor Appl Genet 78: 65–75 (1989).

    Google Scholar 

  15. Gebhardt C, Ritter E, Barone A, Debener T, Walkemeier B, Schachtschabel U, Kaufmann H, Thompson R, Bonierbale MW, Ganal MW, Tanksley SD, Salamini F: RFLP maps of potato and their alignment with the homoeologous tomato genome. Theor Appl Genet 83: 49–57 (1991).

    Google Scholar 

  16. Heidekamp F, Dirkse WG, Hille J, van Ormondt H: Nucleotide sequence of the Agrobacterium tumefaciens octopine Ti plasmid-encoded tmr gene. Nucl Acids Res 11: 6211–6223 (1983).

    Google Scholar 

  17. Hoekema A, Hirsch PR, Hooykaas PJJ, Schilperoort RA: A binary plant vector strategy based on separation of vir and T region of the Agrobacterium tumefaciens Ti-plasmid. Nature 303: 179–180 (1983).

    Google Scholar 

  18. Jefferson RA: Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5: 387–405 (1988).

    Google Scholar 

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

    Google Scholar 

  20. Jefferson R, Goldsbrough A, Bevan M: Transcriptional regulation of a patatin-1 gene in potato. Plant Mol Biol 14: 995–1006 (1990).

    Google Scholar 

  21. Köster-Töpfer M, Frommer WB, 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 219: 390–396 (1989).

    Google Scholar 

  22. Köster-Töpfer M, Frommer WB, Rocha-Sosa M, Willmitzer L: Presence of a transposon-like element in the promoter region of an inactive patatin gene in Solanum tuberosum L. Plant Mol Biol 14: 239–247 (1990).

    Google Scholar 

  23. Lelievre J-M, Oliveira LO, Nielsen NC: 5′-CATGCAT-3′ elements modulate the expression of glycinin genes. Plant Physiol 98: 387–391 (1992).

    Google Scholar 

  24. Liu XJ, Prat S, Willmitzer L, Frommer WB: Cis regulatory elements directing tuber-specific and sucrose-inducible expression of a chimeric class I patatin promoter/GUS gene fusion. Mol Gen Genet 223: 401–406 (1990).

    Google Scholar 

  25. Liu XY, Rocha-Sosa M, Hummel S, Willmitzer L, Frommer WB: A detailed study of the regulation and evolution of the two classes of patatin genes in Solanum tuberosum L. Plant Mol Biol 17: 1139–1154 (1991).

    Google Scholar 

  26. Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1982).

    Google Scholar 

  27. Maxam AM, Gilbert W: Sequencing end-labeled DNA with base specific chemical cleavages. Meth Enzymol 65: 499–450 (1980).

    Google Scholar 

  28. Mignery GA, Pikaard CS, Hannapel DJ, Park WD: Isolation and sequence analysis of cDNAs for the major potato tuber protein, patatin. Nucl Acids Res 21: 7987–8000 (1984).

    Google Scholar 

  29. Mignery GA, Pikaard CS, Park WD: Molecular characterization of the patatin multigene family of potato. Gene 62: 27–44 (1988).

    Google Scholar 

  30. Murashige T, Skoog F: A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15: 473–497 (1962).

    Google Scholar 

  31. Pikaard CS, Mignery GA, Ma DP, Stark VJ, Park WD: Sequence of two apparent pseudogenes of the major potato tuber protein patatin. Nucl Acids Res 14: 5564–5566 (1986).

    Google Scholar 

  32. Pikaard CS, Brusca JS, Hannapel DJ, Park WD: The two classes of genes for the major potato tuber protein, patatin, are differentially expressed in tubers and roots. Nucl Acids Res 15: 1979–1994 (1987).

    Google Scholar 

  33. Plegt L, Bino RJ: β-Glucuronidase activity during development of the male gametophyte from transgenic and non-transgenic plants. Mol Gen Genet 216: 321–327 (1989).

    Google Scholar 

  34. Racusen D: Lipid acyl hydrolase of patatin. Can J Bot 62: 1640–1644 (1984).

    Google Scholar 

  35. Racusen D, Foote M: A major soluble glycoprotein of potato tubers. J Food Biochem 4: 43–52 (1980).

    Google Scholar 

  36. Rocha-Sosa M, Sonnewald U, Frommer W, Stratmann M, Schell J, Willmitzer L: Both developmental and metabolic signals activate the promoter of a class 1 patatin gene. EMBO J 8: 23–29 (1989).

    Google Scholar 

  37. Rosahl S, Schmidt R, Schell J, Willmitzer L: Isolation and characterization of a gene from Solanum tuberosum encoding patatin, the major storage protein of potato tubers. Mol Gen Genet 203: 214–220 (1986).

    Google Scholar 

  38. Rosahl S, Eckes P, Schell J, Willmitzer L: Organ-specific gene expression in potato: isolation and characterization of tuber-specific cDNA sequences. Mol Gen Genet 202: 308–373 (1986).

    Google Scholar 

  39. Rosahl S, Schell J, Willmitzer L: Expression of a tuberspecific storage protein in transgenic tobacco plants: demonstration of an esterase activity. EMBO J 6: 1155–1159 (1987).

    Google Scholar 

  40. Sonnewald U, Studer D, Rocha-Sosa M, Willmitzer L: Immunochemical localization of patatin, the major glycoprotein in potato (Solanum tuberosum) tubers. Planta 178: 176–183 (1989).

    Google Scholar 

  41. Sonnewald U, von Schaewen A, Willmitzer L: Expression of mutant patatin protein in transgenic tobacco plants: role of glycans and intracellular location. Plant Cell 2: 345–355 (1990).

    Google Scholar 

  42. Staden R: An interactive graphics program for comparing and aligning nucleic aicd and amino acid sequences. Nucl Acids Res 10: 2951–2961 (1982).

    Google Scholar 

  43. Stiekema WJ, Heidekamp F, Louwerse JD, Verhoeven HA, Dijkhuis P: Introduction of foreign genes into potato cultivars Bintje and Desiree using an Agrobacterium tumefaciens binary vector. Plant Cell Rep 7: 47–50 (1988).

    Google Scholar 

  44. Stiekema WJ, Heidekamp F, Dirkse WG, van Beckum J, de Haan P, ten Bosch C, Louwerse JD: Molecular cloning and analysis of four potato tuber mRNAs. Plant Mol Biol 11: 255–269 (1988).

    Google Scholar 

  45. Twell D, Ooms G: The 5′ flanking DNA of a patatin gene directs tuber specific expression of a chimaeric gene in potato. Plant Mol Biol 9: 345–375 (1987).

    Google Scholar 

  46. Twell D, Ooms G: Structural diversity of the patatin gene family in potato cv. Desiree. Mol Gen Genet 212: 325–336 (1988).

    Google Scholar 

  47. Vancanneyt G, Sonnewald U, Höfgen R, Willmitzer L: Expression of a patatin-like protein in the anthers of potato and sweet pepper flower. Plant Cell 1: 533–540 (1989).

    Google Scholar 

  48. Visser RGF, Hergersberg M, van der Leij FR, Jacobsen E, Witholt B, Feenstra WJ: Molecular cloning and partial characterization of the gene for granulebound starch synthase from a wild-type and an amylose-free potato (Solanum tuberosum L.) Plant Sci 64: 185–192 (1989).

    Google Scholar 

  49. Wenzler HC, Mignery GA, Fisher LM, Park WD: Analysis of a chimeric class-I patatin-GUS gene in transgenic potato plants: high-level expression in tubers and sucrose-inducible expression in cultured leaf and stem explants. Plant Mol Biol 12: 41–50 (1989).

    Google Scholar 

  50. Wenzler H, Mignery G, Fisher L, Park WD: Sucroseregulated expression of a chimeric potato tuber gene in leaves of transgenic tobacco plants. Plant Mol Biol 13: 347–354 (1989).

    Google Scholar 

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Author notes

  1. Jeanine Louwerse

    Present address: Centre for Phytotechnology RUL/TNO, Leiden, Netherlands

  2. Joke Onstenk

    Present address: KeyGene NV, Wageningen, Netherlands

Authors and Affiliations

  1. Department of Molecular Biology, DLO-Centre for Plant Breeding and Reproduction Research (CPRO-DLO), P.O. Box 16, 6700 AA, Wageningen, Netherlands

    Jan Peter Nap, Wim G. Dirkse, Jeanine Louwerse, Joke Onstenk, Annelies Loonen, Freek Heidekamp & Willem J. Stiekema

  2. Department of Plant Breeding, Agricultural University, Wageningen, Netherlands

    Richard Visser

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  1. Jan Peter Nap
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Nap, J.P., Dirkse, W.G., Louwerse, J. et al. Analysis of the region in between two closely linked patatin genes: class II promoter activity in tuber, root and leaf. Plant Mol Biol 20, 683–694 (1992). https://doi.org/10.1007/BF00046453

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  • DOI: https://doi.org/10.1007/BF00046453

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