Skip to main content
SpringerLink
Log in

Patatin and four serine proteinase inhibitor genes are differentially expressed during potato tuber development

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

A highly efficient and synchronousin vitro tuberization system is described. One-node stem pieces from potato (Solanum tuberosum cv. Bintje) plants grown under short day-light conditions containing an axillary bud were cultured in the dark on a tuber-inducing medium. After 5 or 6 days all axillary buds started to develop tubers. To study gene expression during tuber development, RNA isolated from tuberizing axillary buds was used for bothin vitro translation and northern blot hybridizations. The genes encoding the proteinase inhibitors I and II (PI-I and PI-II), a Kunitz-and a Bowman-Birk-type proteinase inhibitor were already expressed in uninduced axillary buds. The length of the day-light conditions differently influenced the expression level of the individual genes. In addition, the expression of each of these genes changed specifically during the development of the axillary bud to tuber. In contrast to the expression of these proteinase inhibitor genes, patatin gene expression was only detectable from the day tuberization was manifested as a radial expansion of the axillary bud.

These results are discussed with respect to the regulation of the expression of the genes studied in relation to the regulation of tuber development.

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

  1. Artschwager E: Studies on the potato tuber. J Agric Res 27: 809–835 (1924).

    Google Scholar 

  2. Bourque JE, Miller JC, Park WD: Use of anin vitro tuberization system to study tuber protein gene expression. In Vitro Cell Dev Biol 23: 381–386 (1987).

    Google Scholar 

  3. Chapman HW: Tuberization in the potato plant. Physiol Plant 11: 215–224 (1958).

    Google Scholar 

  4. Cleveland TE, Thornburg RW, Ryan CA: Molecular characterization of a wound-inducible inhibitor I gene from potato and the processing of its mRNA and protein. Plant Mol Biol 8: 199–207 (1987).

    Google Scholar 

  5. Cutter EG: Structure and development of the potato plant. In: Harris PM (ed) The Potato Crop, pp. 70–152. Chapman and Hall, London (1978).

    Google Scholar 

  6. Ewing EE: Cuttings as simplified models of the potato plant. In: Li PH (ed) Potato Physiology, pp. 153–207. Academic Press, Orlando, FL (1985).

    Google Scholar 

  7. Ewing EE: The role of hormones in potato (Solanum tuberosum L.) tuberization. In: Davies PJ (ed) Plant Hormones and their Roles in Plant Growth and Development, pp. 515–538. Kluwer Academic Publishers, Dordrecht (1987).

    Google Scholar 

  8. Ewing EE, Wareing PF: Shoot, stolon, and tuber formation on potato (Solanum tuberosum L.) cuttings in response to photoperiod. Plant Physiol 61: 348–353 (1978).

    Google Scholar 

  9. Farmer EE, Ryan CA: Interplant communication: Airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci USA 87: 7713–7716 (1990).

    Google Scholar 

  10. Graham JS, Hall G, Pearce G, Ryan CA: Regulation of proteinase inhibitors I and II mRNAs in leaves of wounded tomato plants. Planta 169: 399–405 (1986).

    Google Scholar 

  11. Gregory LE: Some factors for tuberization in the potato plant. Am J Bot 43: 281–288 (1956).

    Google Scholar 

  12. Hannapel JD, Creighton-Miller J, Park WD: Regulation of potato tuber protein accumulation by gibberellic acid. Plant Physiol 78: 700–703 (1985).

    Google Scholar 

  13. Hendriks T, De Jong A, Wijsman HJW, Van Loon LC: Antigenic relationships between petunia peroxidase a and specific peroxidase isoenzymes in other Solanaceae. Theor Appl Genet 80: 113–120 (1990).

    Google Scholar 

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

    Google Scholar 

  15. Johnson R, Ryan CA: Wound-inducible potato inhibitor II genes: enhancement of expression by sucrose. Plant Mol Biol 14: 527–536 (1990).

    Google Scholar 

  16. Keil M, Sanchez-Serrano JJ, Willmitzer L: Both wound-inducible and tuber-specific expression are mediated by the promoter of a single member of the proteinase inhibitor II gene family. EMBO J 8: 1323–1330 (1989).

    Google Scholar 

  17. Kernan A, Thornburg RW: Auxin levels regulate the expression of a wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusionin vitro andin vivo. Plant Physiol 91: 73–78 (1989).

    Google Scholar 

  18. Koda Y, Okazawa Y: Influences of environmental, hormonal and nutritional factors on potato tuberizationin vitro. Jpn J Crop Sci 52: 582–591 (1983).

    Google Scholar 

  19. Koda Y, Omer E-SA, Yoshihara T, Shibata H, Sakamura S, Okazawa Y: Isolation of a tuber-inducing substance from potato leaves. Plant Cell Physiol 29: 1047–1051 (1988).

    Google Scholar 

  20. Koster-Topfer M, Frommer WB, Rocha-Sosa M, Rosahl S, Schell J, Willmitzer L. A class II patain promoter is under developmental control in both transgenic potato and tobacco plants. Mol Gen Genet 219: 390–396 (1989).

    Google Scholar 

  21. Krauss A: Interaction of nutrition, phytohormones, and tuberization. In: Li PH (ed) Potato Physiology, pp. 209–230. Academic Press, Orlando, FL (1985).

    Google Scholar 

  22. Logemann J, Schell J, Willmitzer L: Improved method for the isolation of RNA from plant tissues. Anal Biochem 163: 16–20 (1987).

    Google Scholar 

  23. Menzel CM: Tuberization at high temperatures: Responses to gibberellin and growth inhibitors. Ann Bot 47: 727–733 (1980).

    Google Scholar 

  24. Menzel CM: Tuberization at high temperatures: promotion by disbudding. Ann Bot 47: 727–733 (1981).

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  27. Okazawa Y: Physiological studies on the tuberization of potato plants. J Fac Agric Hokkaido Univ 55: 267–347 (1967).

    Google Scholar 

  28. Paiva E, Lister RM, Park WD: Comparison of the protein in axillary bud tubers and underground stolon tubers in potato. Am Potato J 59: 425–433 (1982).

    Google Scholar 

  29. Paiva EP, Lister RM, Park WD: Induction and accumulation of major tuber proteins of potato in stems and petiole. Plant Physiol 71: 161–168 (1983).

    Google Scholar 

  30. Palm CJ, Costa MA, An G, Ryan CA: Wound-inducible nuclear gene binds DNA fragments that regulate a proteinase inhibitor II gene from potato. Proc Natl Acad Sci USA 87: 603–607 (1990).

    Google Scholar 

  31. Palmer CE, Smith OE: Cytokinins and tuber initiation in the potatoSolanum tuberosum L. Nature 221: 279–280.

  32. Park WD: Tuber proteins of potato — a new and surprising molecular system. Plant Mol Biol Rep 1: 61–66 (1983).

    Google Scholar 

  33. Park WD, Hannapel DJ, Mignery GA, Pikaard CS: Molecular approaches to the study of the major tuber proteins. In: Li PH (ed) Potato Physiology, pp. 261–278. Academic Press, Orlando, FL (1985).

    Google Scholar 

  34. Pena-Cortes H, Sanchez-Serrano JJ, Rocha-Sosa M, Willmitzer L: Systemic induction of proteinase-inhibitor-II gene expression in potato plants by wounding. Planta 174: 84–89 (1988).

    Google Scholar 

  35. Pena-Cortes H, Sanchez-Serrano JJ, Mertens R, Willmitzer L, Prat S: Abscisic acid is involved in the wound-induced expression of the proteinase inhibitor II gene in potato and tomato. Proc Natl Acad Sci USA 86: 9851–9855 (1989).

    Google Scholar 

  36. Peterson RL, Barker WG, Howarth MJ: Development and structure of tubers. In: Li PH (ed) Potato Physiology, pp. 123–152. Academic Press, Orlanda, FL (1985).

    Google Scholar 

  37. 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 

  38. Pont Lezica RF: Evolution des substances de type gibbérelines chez la pomme de terre pendant la tubérisaton, en relation avec la longueur du jour et la température. Potato Res 13: 323–231 (1970).

    Google Scholar 

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

    Google Scholar 

  40. Railton ID, Wareing PF: Effects of daylength on endogenous gibberellins in leaves ofSolanum andigena. Physiol Plant 28: 88–94 (1973).

    Google Scholar 

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

    Google Scholar 

  42. 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: 368–373 (1986).

    Google Scholar 

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

    Google Scholar 

  44. Ryan C, Kuo, Pearce G, Kunkel R: Variability in the concentration of three heat stable proteinase inhibitor proteins in potato tubers. Am Potato J 53: 443–455 (1976).

    Google Scholar 

  45. Sanchez-Serrano JJ, Schmidt R, Schell J, Willmitzer L: Nucleotide sequence of proteinase inhibitor II encoding cDNA of potato (Solanum tuberosum) and its mode of expression. Mol Gen Genet 203: 15–20 (1986).

    Google Scholar 

  46. Sanches-Serrano JJ, Keil M, O'Connor A, Schell J, Willmitzer L: Wound-inducible expression of a potato proteinase inhibitor II gene in transgenic tobacco plants. EMBO J 6: 303–306 (1987).

    Google Scholar 

  47. Stiekema WJ, Heidekamp F, Dikse WG, Van Beckum J, De Haan, Ten Bosch C, Louwerse JD: Molecular cloning and analysis of four potato tuber mRNAs. Plant Mol Biol 11: 255–269 (1988).

    Google Scholar 

  48. Suh S-G, Peterson JE, Stiekema WJ, Hannapel DJ: Purification and characterization of the 22-kilodalton potato tuber proteins. Plant Physiol 94: 40–45 (1990).

    Google Scholar 

  49. Tamal IA: Hormonal regulation of apical dominance. In: Davies PJ (ed) Plant Hormones and their Role in Plant Growth and Development, pp. 393–410. Kluwer Academic Publishers, Dordrecht (1987).

    Google Scholar 

  50. Thornburg RW, An G, Cleveland TE, Johnson R, Ryan CA: Wound-inducible expression of a potato inhibitor II-chloramphenicol acetyltransferase gene fusion in transgenic tobacco plants. Proc Natl Acad Sci USA 84: 744–748 (1987).

    Google Scholar 

  51. Twell D, Ooms G: Structural diversity of the patatin gene family in potato cv Désirée. Mol Gen Genet 212: 325–336 (1983).

    Google Scholar 

  52. Vreugdenhill D, Struik PC: An integrated view of the hormonal regulation of tuber formation in potato (Solanum tuberosum). Physiol Plant 75: 525–531 (1989).

    Google Scholar 

  53. 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 

  54. Wenzler HC, Mignery GA, Fisher LM, Park WD: Sucrose-regulated expression of a chimeric potato tuber gene in leaves of transgenic tobacco plants. Plant Mol Biol 13: 347–354 (1989).

    Google Scholar 

  55. Yoshihara T, Omer E-SA, Koshino H, Sakamura S, Kikuta Y, Koda Y: Structure of a tuber-inducing stimulus from potato leaves (Solanum tuberosum L.). Agric Biol Chem 53: 2835–2837 (1989).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular Biology, Centre for Plant Breeding Research CPO, P.O. Box 16, 6700 AA, Wageningen, Netherlands

    Theo Hendriks & Willem J. Stiekema

  2. Department of Plant Physiology, Agricultural University, Arboretumlaan 4, 6703 DB, Wageningen, Netherlands

    Dick Vreugdenhil

Authors
  1. Theo Hendriks
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dick Vreugdenhil
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Willem J. Stiekema
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hendriks, T., Vreugdenhil, D. & Stiekema, W.J. Patatin and four serine proteinase inhibitor genes are differentially expressed during potato tuber development. Plant Mol Biol 17, 385–394 (1991). https://doi.org/10.1007/BF00040633

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00040633

Key words

Search

Navigation