Skip to main content
Log in

Carbohydrate metabolism during tuber initiation in potato: A transient surge in invertase activity marks the stolon to tuber transition

  • Published:
Potato Research Aims and scope Submit manuscript

Summary

The relationship between carbohydrate metabolism and tuber initiation in potato was determined by monitoring changes in the amount of starch and sugars along with the activities of sugar metabolizing enzymes upon transfer of plants to tuber-inducing conditions (TI; short days, cold nights) from non-inducing conditions (NTI: long days, warm nights). Switch to TI conditions caused an immediate slow-down in plant growth and triggered swelling of stolon tips, which went on to develop into tubers. Leaves of plants moved to TI conditions accumulated less starch and sugar while their stolon tips showed a sudden upsurge in starch content and a sharp decline in sugars even before any tip swelling was detectable. These changes were paralleled by a transient surge in the activity of cell wall invertase (74%) and soluble invertase (30%) in stolon tips of plants transferred to TI conditions in two unrelated cultivars under different experimental conditions. As the surge in invertase activity faded, it was replaced by a substantial increase in sucrose synthase activity as the tuber enlargement proceeded. The transient increase in invertase activity just prior to tuber initiation appears to mark a turning point in the transition of stolon tip to tuber.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Appeldoorn, N.J.G., S.M. de Bruijn, E.A.M. Koot-Gronsveld, R.G.F. Visser, D. Vreugdenhil & L.H.W. van der Plas, 1997. Developmental changes of enzymes involved in conversion of sucrose to hexose-phosphate during early tuberization of potato.Planta 202: 220–226.

    Article  CAS  Google Scholar 

  • Basu, P.S. & J.S. Minhas, 1991. Heat tolerance and assimilate transport in different potato genotypes.Journal of Experimental Botany 42: 861–866.

    Article  CAS  Google Scholar 

  • Chapman, H.W., 1958. Tuberization in the potato plant.Physiologia Plantarum 11: 215–224.

    Article  Google Scholar 

  • Cutter, E.G., 1978. Structure and development of the potato plant. In: P.M. Harris (Ed.), The Potato Crop. Chapman and Hall, London, pp. 70–152.

    Google Scholar 

  • Dancer, J.E.W.D. Hatzfeld & M. Stitt, 1990. Cytosolic cycles regulate the turnover of sucrose in heterotrophic cellsuspension cultures ofChenopodium rubrum.Planta 182: 223–251.

    Article  CAS  Google Scholar 

  • Davies, H.V., 1984. Sugar metabolism in the stolon tips of potato during tuberization.Zeitschrift für Pflanzenphysiologie 113: 377–381.

    CAS  Google Scholar 

  • Eschrich, W., 1980. Free space invertase, its possible role in phloem unloading.Berichte der Deutschen Botanischen Gesellschaft 93: 363–378.

    CAS  Google Scholar 

  • Ewing, E.E. & P.C. Struik, 1992. Tuber formation in potato: Induction, initiation, and growth.Horticulture Reviews 14: 89–198.

    Google Scholar 

  • Frommer, W. & U. Sonnewald, 1995. Molecular analysis of carbon partitioning in solanaceous species.Journal of Experimental Botany 46: 587–607.

    Article  CAS  Google Scholar 

  • Hajirezaei, M., Y. Takahata, R.N. Trethewey, L. Willmitzer, U. Sonnewald & J.J. Pavek, 2000. Impact of elevated cytosolic and apoplastic invertase activity on carbon metabolism during potato tuber development.Journal of Experimental Botany 51: 439–445.

    Article  PubMed  CAS  Google Scholar 

  • Heim, U., H. Weber, H. Baumlein & U. Wobus, 1993. A sucrose synthase gene ofVicia faba L.: Expression pattern in developing seeds in relation to starch synthesis and metabolic regulation.Planta 191: 394–401.

    Article  PubMed  CAS  Google Scholar 

  • Helder, J. & D. Vreugdenhil, 1999. Carbohydrate metabolism in tuberizing stolon tips of the strictly short day dependent potato speciesSolanum demissum Lindl.Plant Biology 1: 372–378.

    CAS  Google Scholar 

  • Koch, K.E., 1996. Carbohydrate modulated gene expression in plants.Annual Review of Plant Physiology and Plant Molecular Biology 47: 509–540.

    Article  PubMed  CAS  Google Scholar 

  • Lorenzen, J.H. & E.E. Ewing, 1992. Starch accumulation in leaves of potato (Solanum tuberosum L.) during the first 18 days of photoperiod treatment.Annals of Botany 69: 481–485.

    CAS  Google Scholar 

  • Madec, P., 1963. Tuber forming substances in the potato. In: J.D. Ivins & F.L. Milthorpe (Eds), Growth of the Potato. Butterworth, London, pp. 121–131.

    Google Scholar 

  • Menzel, C.M., 1980. Tuberization in potato at high temperatures: response to gibberellin and growth inhibitors.Annals of Botany 46: 259–265.

    CAS  Google Scholar 

  • Miller, M.E. & P.S. Chourey, 1992. The maize invertase-deficient miniature-1 seed mutation is associated with aberrant pedicle and endosperm development.The Plant Cell 4: 297–305.

    Article  PubMed  CAS  Google Scholar 

  • Misra, J.B., E.V. Daniel & Premchand, 1994. Sucrose synthase and sucrose phosphate synthase in potato: distribution of activities and variations in leaves.Plant Physiology and Biochemistry Paris 32: 131–136.

    CAS  Google Scholar 

  • Moorby, J., 1968. The influence of carbohydrates and mineral nutrient supply on the growth of potato tubers.Annals of Botany 32: 57–68.

    CAS  Google Scholar 

  • Moorby, J., 1978. The physiology of growth and tuber yield. In: P.M. Harris (Ed.), The Potato Crop. Chapman and Hall, London, pp. 153–195.

    Google Scholar 

  • Nagarajan, S. & K.C. Bansal, 1990. Growth and distribution of dry matter in a heat tolerant and a susceptible potato cultivar under normal and high temperature.Journal of Agronomy and Crop Science 165: 306–311.

    Google Scholar 

  • Nelson, N., 1944. A photometric adaptation of the Somogyi method for the determination of glucose.Journal of Biological Chemistry 153: 375–380.

    CAS  Google Scholar 

  • Okazawa, Y., 1967. Physiological studies on the tuberization of potato plant.Journal of the Faculty of Agriculture, Hokaido University 55: 268–336.

    Google Scholar 

  • Patrick, J.W., 1997. Phloem unloading: sieve elements unloading and post sieve element transport.Annual Review of Plant Physiology and Plant Molecular Biology 48: 191–192.

    Article  PubMed  CAS  Google Scholar 

  • Roitsch, T., 1999. Source-sink regulation by sugars and stress.Current Opinion in Plant Biology 2: 198–206.

    Article  PubMed  CAS  Google Scholar 

  • Roitsch, T., M. Goetz, R. Ehneß, B. Hause, M. Hofmann & A.K. Sinha, 2000. Regulation and function of extracellular invertase from higher plants in relation to assimilate partitioning, stress responses and sugar signaling.Australian Journal of Plant Physiology 27: 815–825.

    CAS  Google Scholar 

  • Ross, H.A., H.V. Davies, L.R. Burch, R. Viola & D. McRae, 1994. Developmental changes in carbohydrate content and sucrose degrading enzymes in tuberizing stolons of potato (Solanun tuberosum).Physiologia Plantarum 90: 748–756.

    Article  CAS  Google Scholar 

  • Sale, P.J.M., 1974. Productivity of vegetative crops in a region of high solar input. III. Carbon balance of potato crops.Australian Journal of Plant Physiology 1: 283–296.

    Article  CAS  Google Scholar 

  • Sheen, J., 1994. Feedback control of gene expression.Photosynthesis Research 39: 427–438.

    Article  CAS  Google Scholar 

  • Stitt, M. & U. Sonnewald, 1995. Regulation of metabolism in transgenic plants.Annual Review of Plant Physiology and Plant Molecular Biology 46: 341–368.

    Article  CAS  Google Scholar 

  • Sung, S.-J., D.-P. Xu & C.C. Black, 1989. Identification of actively filling sucrose sinks.Plant Physiology 89: 1117–1121.

    PubMed  CAS  Google Scholar 

  • Tang, G. & A. Sturm, 1999. Antisense repression of vacuolar and cell wall invertase in transgenic carrots alters early plant development and sucrose partitioning.The Plant Cell 11: 177–189.

    Article  PubMed  CAS  Google Scholar 

  • Tauberger, E., S. Hoffman-Benning, H. Fleischer-Notter, L. Willmitzer & J. Fisahn, 1999. Impact of invertase over-expression on cell size, starch granule formation and cell wall properties during tuber development in potatoes with modified carbon allocation patterns.Journal of Experimental Botany 50: 477–486.

    Article  CAS  Google Scholar 

  • Tsai, C.Y., F. Salamini & O.E. Nelson, 1970. Enzymes of carbohydrate metabolism in the developing endosperm of maize.Plant Physiology 46: 299–306.

    Article  PubMed  CAS  Google Scholar 

  • Viola, R., A.G. Roberts, S. Haupt, S. Gazzani, R.D. Hancock, N. Marmiroli, G.C. Machray & K.J. Oparka, 2001. Tuberization in potato involves a switch from apoplastic to symplastic phloem unloading.The Plant Cell 13: 385–398.

    Article  PubMed  CAS  Google Scholar 

  • Visser, R.F., D. Vreugdenhil, T. Hendriks & E. Jacobsen, 1994. Gene expression and carbohydrate content during stolon to tuber transition in potatoes (Solanum tuberosum).Physiologia Plantarum 90: 285–292.

    Article  CAS  Google Scholar 

  • Wang, F., A.G. Smith & M.L. Brenner, 1993. Isolation and sequencing of tomato fruit sucrose synthase cDNA.Plant Physiology 103: 1463–1464.

    Article  PubMed  CAS  Google Scholar 

  • Weber, H., L. Borisjuk, U. Heim, P. Buchner & U. Wobus, 1995. Seed coat-associated invertases of fava bean control both unloading and storage functions: Cloning of cDNAs and cell type-specific expression.The Plant Cell 7: 1835–1846.

    Article  PubMed  CAS  Google Scholar 

  • Wolf, S., 1993. Effect of leaf age on photosynthesis, carbon transport and carbon allocation in potato plants.Potato Research 36: 253–262.

    Article  CAS  Google Scholar 

  • Wolf, S., A. Marani & J. Rudich, 1990. Effect of temperature and photoperiod on assimilate partitioning in potato plants.Annals of Botany 66: 513–520.

    Google Scholar 

  • Yemm, E.W. & A.J. Willis, 1954. The estimation of carbohydrates in plant extracts by anthrone.Biochemical Journal 57: 508–514.

    PubMed  CAS  Google Scholar 

  • Zinselmeier, C., M.E. Westgate, L.R. Schussler & R.J. Jones, 1995. Low water potential disrupts carbohydrate metabolism in maize (Zea mays) L. ovaries.Plant Physiology 107: 385–391.

    PubMed  CAS  Google Scholar 

  • Zrenner, R., M. Salanoubat, L. Willmitzer & U. Sonnewald, 1995. Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.).Plant Journal 7: 97–107.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to H. S. Saini.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Minhas, J.S., Rai, V.K. & Saini, H.S. Carbohydrate metabolism during tuber initiation in potato: A transient surge in invertase activity marks the stolon to tuber transition. Potato Res. 47, 113–126 (2004). https://doi.org/10.1007/BF02735978

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02735978

Additional keywords

Navigation