Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Study of sucrose and mannitol transport in plasma-membrane vesicles from phloem and non-phloem tissues of celery (Apium graveolens L.) petioles


The mature petiole of celery is an organ with versatile sink/source capacities where sucrose and mannitol are unloaded from and reloaded into the phloem cells. Plasma-membrane vesicles were purified by twophase partitioning either from phloem strands isolated from mature petioles of celery (Apium graveolens L.) or from mature petioles devoid of vascular bundles. Both types of vesicle were comparable in purity (more than 86% of plasma-membrane origin), size (135 nm diameter) and orientation (72% right-side-out). Plasma-membrane vesicles from phloem tissues had a higher vanadate-sensitive ATPase activity than plasma-membrane vesicles from petioles. Plasma-membrane vesicles from phloem tissues accumulated mannitol and sucrose in response to an artificial proton-motive force, in agreement with the existence of proton/substrate carriers. Plasma-membrane vesicles from petioles devoid of vascular bundles accumulated only mannitol following application of an artificial proton-motive force. The data suggest the volvement of apoplasmic transport events. The pathway for sucrose uptake in storage parenchyma cells is discussed in the light of the available physiological data.

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



carbonyl cyanide m-chlorophenylhydrazone




p-chloromercuribenzenesulfonic acid


proton-motive force


plasmamembrane vesicle


PMV from phloem strands


PMV from petioles devoid of vascular bundles


phosphotungstic acid


sieve element/companion cell


  1. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Plant Physiol 24: 1–15

  2. Bouché-Pillon S, Fleurat-Lessart P, Serrano R, Bonnemain JL (1994) Asymmetric distribution of the plasma-membrane H+ ATPase in embryo of Vicia faba L. with special reference to transfer cells. Planta 193: 392–397

  3. Bush DR (1993) Proton-coupled sugar and amino acids transporters in plants. Annu Rev Plant Physiol Plant Mol Biol 44: 513–542

  4. Daie J (1986) Kinetics of sugar transport in isolated vascular bundles and phloem tissues of celery. J Am Soc Hort Sci 111: 216–220

  5. Daie J (1987) Sucrose uptake in isolated phloem of celery is a single saturable transport system. Planta 171: 474–482

  6. Daie J, Watts M, Aloni B, Wyse R (1986) In vitro and in vivo modification of sugar transport and translocation in celery by phytohormones. Plant Sci 46: 35–41

  7. Davis JM, Loescher WH (1990) [14C]-assimilate translocation in the light and dark in celery (Apium graveolens) leaves of different ages. Physiol Plant 79: 656–662

  8. Everard JD, Franceschi VR, Loescher WH (1993) Mannose-6-phosphate reductase, a key enzyme in photoassimilate partitioning, is abundant and located in the cytosol of photosynthetically active cells of celery (Apium graveolens L.) source leaves. Plant Physiol 102: 345–356

  9. Heinz E, Weinstein AW (1984) The overshoot phenomenon in cotransport. Biochim Biophys Acta 776: 83–91

  10. Kalinin VA, Opritov VA (1989) Role of Δψ and ΔpH in protondependent sucrose transport in plasma membrane vesicles of plant phloem. Fiziol Rast 36: 901–909

  11. Keller F, Matile P (1989) Storage of sugars and mannitol in petioles of celery leaves. New Phytol 113: 291–299

  12. Larsson C (1985) Plasma membrane. In Cell components. Modern methods in plant analysis, pp. 85–104, Linkens HF, Jackson SF, eds. Springer, Berlin

  13. Lemoine R, Delrot S (1989) Proton-motive-force-driven sucrose uptake in sugar beet plasma membrane vesicles. FEBS Lett 249: 129–133

  14. Lemoine R, Bourquin S, Delrot S (1991) Active uptake of sucrose by plant plasma membrane vesicles: determination of some important physical and energitical parameters. Physiol Plant 82: 377–384

  15. Lemoine R, Gallet O, Gaillard C, Frommer W, Delrot S (1992) Plasma membrane vesicles from source and sink leaves. Plant Physiol 100: 1150–1156

  16. Loescher WH (1987) Physiology and metabolism of sugar alcohols in higher plants. Physiol Plant 70: 553–557

  17. Maurousset L, Lemoine R, Delrot S, Pichelin-Poitevin D (1992) Solute uptake in plasma membrane vesicles from broad bean (Vicia faba L.) leaves. Acta Bot Neerl 42: 151–159

  18. M'Batchi B, Elayadi R, Delrot S, Bonnemain JL (1986) Direct versus indirect effects of p-chloromercuribenzene sulphonic acid on sucrose uptake by plant tissues: the electrophysiological evidence. Physiol Plant 68: 391–395

  19. Palmgren MG, Sommarin M (1989) Lysophosphatidylcholine stimulates ATP dependent proton accumulation in isolated root PMV. Plant Physiol 90: 1009–1014

  20. Riesmeier JW, Hirner B, Frommer WB (1993) Potato sucrose transporter expression in minor veins indicates a role in phloem loading. Plant Cell 5: 1591–1598

  21. Riesmeier JW, Willmitzer L, Frommer WB (1992) Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J 11: 4705–4713

  22. Roland JC, Lembi C, Morre J (1972) Phosphotungstic acid-chromic acid as a selective electron-dense stain for plasma membranes of plant cells. Stain Technol 47: 195–200

  23. Sauer N, Friedländer K, Gräml-Wicke U (1990) Primary structure, genomic organization and heterologous expression of a glucose transporter from Arabidopsis thaliana. EMBO J 9: 3045–3050

  24. Van Bel AJE, Koops AJ (1985) Uptake of [14C]sucrose in isolated minor vein networks of Commelina benghalensis L. Planta 164: 362–369

  25. Villalba JM, Lützelschwab M, Serrano R (1991) Immunocytolocalization of plasma-membrane H+-ATPase in maize coleoptiles and enclosed leaves. Planta 185: 458–461

  26. Widell S, Larsson C (1990) A critical evaluation of markers. In: The plant plasma membrane. Structure, function and molecular biology, pp. 16–43, Lavsson C, Moller SM, eds, Springer, Berlin

Download references

Author information

Correspondence to Rémi Lemoine.

Additional information

This work was supported by the Centre National de la Recherche Scientifique (URA CNRS 574). The authors wish to thank all the people who helped in preparing phloem strands and also J.M. Perault for the pictures. We thank Professor S. Delrot for critical reading of the manuscript.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Salmon, S., Lemoine, R., Jamai, A. et al. Study of sucrose and mannitol transport in plasma-membrane vesicles from phloem and non-phloem tissues of celery (Apium graveolens L.) petioles. Planta 197, 76–83 (1995).

Download citation

Key words

  • Apium
  • Mannitol
  • Membrane transport
  • Phloem
  • Plasma membrane vesicles
  • Sucrose