Advertisement

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

Auxin transport in membrane vesicles from Cucurbita pepo L.

Abstract

Association of 14C-labelled indole-3-acetic acid (IAA) with membrane particles from zucchini (Cucurbita pepo L.) hypocotyls — previously described as “site III binding” (M. Jacobs and R. Hertel, 1978, Planta 142, 1–10) — is reinterpreted as a carrier-mediated uptake into closed and sealed vesicles driven by a pH gradient. Accumulation of the radioactive auxin is saturable, sensitive to the protonophore, carbonyl cyanide p-trifluoromethoxyphenyl hydrazone (FCCP), and to nigericin, and requires a pH gradient across the membranes with proton concentration greater outside than inside. The pH gradient decays within 1–2 h at 4°C and can be restored by re-equilibration of the particle preparation at more alkaline pH followed by return to more acidic medium. Osmotic shock and sonication release the IAA from the vesicles. 1-N-naphthylphthalamic acid (NPA) and 2,3,5-triiodobenzoic acid (TIBA), both inhibitors of auxin transport in vivo, increase the amount of net IAA accumulation in the vesicles, presumably by blocking efflux. Analogs of NPA less active or inactive in vivo are respectively less active or inactive in vitro. It is proposed that these membrane particles are outside-out plasma membrane vesicles, and that they perform the essential functions of auxin transport according to the chemiosmotic theory, with a specific, saturable proton symport uptake and an export anion carrier which is inhibited by NPA and TIBA.

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

Abbreviations

FCCP:

carbonyl cyanide p-trifluoromethoxyphenyl hydrazone

IAA:

indole-3-acetic acid

1-NAA:

1-naphthaleneacetic acid

NPA:

1-N-naphthylphthalamic acid

PM:

plasma membrane

TIBA:

2,3,5-triiodobenzoic acid

References

  1. Depta, H., Hertel, R. (1982) FCCP sensitive association of weak organic acids to membranes from Cucurbita homogenates: evidence for closed and intact plasma membrane vesicles. In: Plasmalemma and tonoplast: their functions in the plant cell, pp. 137–145, Marmé, D., Marrè, E., Hertel, R., eds. Elsevier, Amsterdam

  2. Edwards, K.L., Goldsmith, M.H.M. (1980) pH-dependent accumulation of indoleacetic acid by corn coleoptile sections. Planta 147, 457–466

  3. Goad, L.J. (1977) The biosynthesis of plant sterols. In: Lipids and lipid polymers in higher plants, pp. 146–168, Tevini, M., Lichtenthaler, H.K., eds. Springer, Berlin Heidelberg New York

  4. Goldsmith, M.H.M. (1982) A saturable site responsible for polar transport of indole-3-acetic acid in sections of maize coleoptiles. Planta 155, 68–75

  5. Goldsmith, M.H.M., Ray, P.M. (1973) Intracellular localization of the active process in polar transport of auxin. Planta 111, 297–314

  6. Goldsmith, M.H.M., Goldsmith, T.H., Martin, M.H. (1981) Mathematical analysis of the chemiosmotic polar diffusion of auxin through plant tissues. Proc. Natl. Acad. Sci. USA 78, 976–980

  7. Hartmann-Bouillon, M.-A., Ehrhardt, A., Benveniste, P. (1982) Concanavalin A binding by purified membrane fractions maize coleoptiles. In: Plasmalemma and tonoplast: their functions in the plant cell, pp. 163–169, Marmé, D., Marrè, E., Hertel, R., eds., Elsevier, Amsterdam

  8. Hertel, R. (1981) Zur Auxinproblematik: primäre Wirkung, Transport und In vitro-Bindung. Biochem. Physiol. Pflanz. 176, 495–506

  9. Hertel, R., Leopold, A.C. (1963) Versuche zur Analyse des Auxintransports in der Koleoptile vonZea mays L. Planta 59, 535–562

  10. Hertel, R., Flory, R. (1968) Auxin movement in corn coleoptiles. Planta 82, 123–144

  11. Hertel, R., Evans, M.L., Leopold, A.C., Sell, H.M. (1969) The specificity of the auxin transport system. Planta 85, 238–249

  12. Jacobs, M., Hertel, R. (1978) Auxin binding to subcellular fractions from Cucurbita hypocotyls: in vitro evidence for an auxin transport carrier. Planta 142, 1–10

  13. Katekar, G.F. (1976) Inhibitors of the geotropic response in plants: a correlation of molecular structures. Phytochemistry 15, 1421–1424

  14. Katekar, G.F., Geissler, A.E. (1980) Auxin transport inhibitors. IV. Evidence of a common mode of action for a proposed class of auxin transport inhibitors: the phytotropins. Plant Physiol. 66, 1190–1195

  15. Katekar, G.F., Navè, J.-F., Geissler, A.E. (1981) Phytotropins. III. Naphthylphthalamic acid binding sites on maize coleoptile membranes as possible receptor sites for phytotropin action. Plant Physiol. 68, 1460–1464

  16. Michalke, W. (1982) pH-shift dependent kinetics of NPA-binding in two particulate fractions from corn coleoptile homogenates. In: Plasmalemma and tonoplast: their functions in the plant cell, pp. 129–135. Marmé, D., Marrè, E., Hertel, R., eds. Elsevier, Amsterdam

  17. Raven, J.A. (1975) Transport of indoleacetic acid in plant cells in relation to pH and electrical potential gradients, and its significance for polar IAA transport. New Phytol. 74, 163–172

  18. Ray, P.M., Dohrmann, U., Hertel, R. (1977) Characterization of naphthaleneacetic acid binding to receptor sites on cellular membranes of maize coleoptile tissue. Plant Physiol. 59, 357–364

  19. Roberts, J.K.M., Ray, P.M., Wade-Jardetzky, N., Jardetzky, O. (1981) Extent of intracellular pH changes during H+ extrusion by maize root tip cells. Planta 152, 74–78

  20. Rubery, P.H. (1977) The specificity of carrier-mediated auxin uptake by suspension-cultured crown gall cells. Planta 135, 275–283

  21. Rubery, P.H. (1978) Hydrogen ion dependence of carrier-mediated auxin uptake by suspension-cultured crown gall cells. Planta 142, 203–206

  22. Rubery, P.H. (1979) The effects of 2,4-dinitrophenol and chemical modifying reagents on auxin transport by suspensioncultured crown gall cells. Planta 144, 173–178

  23. Rubery, P.H., Sheldrake, A.R. (1974) Carrier-mediated auxin transport. Planta 118, 101–121

  24. Shinkle, J.R. Jacobs, M. (1982) Correlation between in vivo and in vitro auxin transport in developing zucchini hypocotyls. (Abstr.) Plant Physiol 69, Suppl. 64

  25. Sussman, M.R., Goldsmith, M.H.M. (1981a) Auxin uptake and action of N-1-naphthylphthalamic acid in corn coleoptiles. Planta 151, 15–25

  26. Sussman, M.R., Goldsmith, M.H.M. (1981b) The action of specific inhibitors of auxin transport on uptake of auxin and binding of 1-N-naphthylphthalamic acid to a membrane site in maize coleoptiles. Planta 152, 13–18

  27. Thomson, K.-St., Hertel, R., Mueller, S., Tavares, J.E. (1973) 1-N-naphthylphthalamic acid and 2,3,5-triidobenzoic acid. In vitro binding to particulate cell fractions and action on auxin transport in corn coleoptiles. Planta 109, 337–352

  28. Trillmich, K., Michalke, W. (1979) Kinetic characteristics of N-1-naphthylphthalamic acid binding sites from maize coleoptile homogenates. Planta 145, 119–127

Download references

Author information

Additional information

Carnegie Institution of Washington, Department of Plant Biology, Publication No. 779

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Hertel, R., Lomax, T.L. & Briggs, W.R. Auxin transport in membrane vesicles from Cucurbita pepo L.. Planta 157, 193–201 (1983). https://doi.org/10.1007/BF00405182

Download citation

Key words

  • Auxin transport
  • Chemiosmotic theory
  • Cucurbita
  • pH gradient and auxin transport
  • Plasma membrane
  • Symport (IAA-/H+)
  • Transport (cellular, auxin)
  • Vesicles, sealed