Skip to main content
NCBI home page
Plant Physiology logoLink to Plant Physiology
. 1994 May;105(1):19–33. doi: 10.1104/pp.105.1.19

Nonvascular, Symplasmic Diffusion of Sucrose Cannot Satisfy the Carbon Demands of Growth in the Primary Root Tip of Zea mays L.

M S Bret-Harte 1, W K Silk 1
PMCID: PMC159325  PMID: 12232183

Abstract

Nonvascular, symplasmic transport of sucrose (Suc) was investigated theoretically in the primary root tip of maize (Zea mays L. cv WF9 x Mo 17) seedlings. Symplasmic diffusion has been assumed to be the mechanism of transport of Suc to cells in the root apical meristem (R.T. Giaquinta, W. Lin, N.L. Sadler, V.R. Franceschi [1983] Plant Physiol 72: 362-367), which grow apical to the end of the phloem and must build all biomass with carbon supplied from the shoot or kernel. We derived an expression for the growth-sustaining Suc flux, which is the minimum longitudinal flux that would be required to meet the carbon demands of growth in the root apical meristem. We calculated this flux from data on root growth velocity, area, and biomass density, taking into account construction and maintenance respiration and the production of mucilage by the root cap. We then calculated the conductivity of the symplasmic pathway for diffusion, from anatomical data on cellular dimensions and the frequency and dimensions of plasmodesmata, and from two estimates of the diffusive conductance of a plasmodesma, derived from independent data. Then, the concentration gradients required to drive a growth-sustaining Suc flux by diffusion alone were calculated but were found not to be physiologically reasonable. We also calculated the hydraulic conductivity of the plasmodesmatal pathway and found that mass flow of Suc solution through plasmodesmata would also be insufficient, by itself, to satisfy the carbon demands of growth. However, much of the demand for water to cause cell expansion could be met by the water unloaded from the phloem while unloading Suc to satisfy the carbon demands of growth, and the hydraulic conductivity of plasmodesmata is high enough that much of that water could move symplasmically. Either our current understanding of plasmodesmatal ultrastructure and function is flawed, or alternative transport mechanisms must exist for Suc transport to the meristem.

Full Text

The Full Text of this article is available as a PDF (1.6 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baron-Epel O., Hernandez D., Jiang L. W., Meiners S., Schindler M. Dynamic continuity of cytoplasmic and membrane compartments between plant cells. J Cell Biol. 1988 Mar;106(3):715–721. doi: 10.1083/jcb.106.3.715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blake J. R. On the hydrodynamics of plasmodesmata. J Theor Biol. 1978 Sep 20;74(1):33–47. doi: 10.1016/0022-5193(78)90288-6. [DOI] [PubMed] [Google Scholar]
  3. Blum J. J., Lawler G., Reed M., Shin I. Effect of cytoskeletal geometry on intracellular diffusion. Biophys J. 1989 Nov;56(5):995–1005. doi: 10.1016/S0006-3495(89)82744-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cosgrove D. Biophysical control of plant cell growth. Annu Rev Plant Physiol. 1986;37:377–405. doi: 10.1146/annurev.pp.37.060186.002113. [DOI] [PubMed] [Google Scholar]
  5. Horowitz S. B. The permeability of the amphibian oocyte nucleus, in situ. J Cell Biol. 1972 Sep;54(3):609–625. doi: 10.1083/jcb.54.3.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Koch K. E., Nolte K. D., Duke E. R., McCarty D. R., Avigne W. T. Sugar Levels Modulate Differential Expression of Maize Sucrose Synthase Genes. Plant Cell. 1992 Jan;4(1):59–69. doi: 10.1105/tpc.4.1.59. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. LEHMAN R. C., POLLARD E. DIFFUSION RATES IN DISRUPTED BACTERIAL CELLS. Biophys J. 1965 Jan;5:109–119. doi: 10.1016/s0006-3495(65)86705-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Lin W., Schmitt M. R., Hitz W. D., Giaquinta R. T. Sugar transport in isolated corn root protoplasts. Plant Physiol. 1984 Dec;76(4):894–897. doi: 10.1104/pp.76.4.894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Luby-Phelps K., Lanni F., Taylor D. L. The submicroscopic properties of cytoplasm as a determinant of cellular function. Annu Rev Biophys Biophys Chem. 1988;17:369–396. doi: 10.1146/annurev.bb.17.060188.002101. [DOI] [PubMed] [Google Scholar]
  10. Mastro A. M., Babich M. A., Taylor W. D., Keith A. D. Diffusion of a small molecule in the cytoplasm of mammalian cells. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3414–3418. doi: 10.1073/pnas.81.11.3414. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Meiners S., Xu A., Schindler M. Gap junction protein homologue from Arabidopsis thaliana: evidence for connexins in plants. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4119–4122. doi: 10.1073/pnas.88.10.4119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Pahlavanian A. M., Silk W. K. Effect of temperature on spatial and temporal aspects of growth in the primary maize root. Plant Physiol. 1988 Jun;87(2):529–532. doi: 10.1104/pp.87.2.529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Paull R. E., Johnson C. M., Jones R. L. Studies on the secretion of maize root cap slime: I. Some properties of the secreted polymer. Plant Physiol. 1975 Aug;56(2):300–306. doi: 10.1104/pp.56.2.300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Paull R. E., Jones R. L. Studies on the Secretion of Maize Root Cap Slime: II. Localization of Slime Production. Plant Physiol. 1975 Aug;56(2):307–312. doi: 10.1104/pp.56.2.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Penning de Vries F. W., Brunsting A. H., van Laar H. H. Products, requirements and efficiency of biosynthesis: a quantitative approach. J Theor Biol. 1974 Jun;45(2):339–377. doi: 10.1016/0022-5193(74)90119-2. [DOI] [PubMed] [Google Scholar]
  16. RENKIN E. M. Filtration, diffusion, and molecular sieving through porous cellulose membranes. J Gen Physiol. 1954 Nov 20;38(2):225–243. [PMC free article] [PubMed] [Google Scholar]
  17. Schmalstig J. G., Cosgrove D. J. Coupling of solute transport and cell expansion in pea stems. Plant Physiol. 1990;94:1625–1633. doi: 10.1104/pp.94.4.1625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Schmalstig J. G., Geiger D. R. Phloem Unloading in Developing Leaves of Sugar Beet : I. Evidence for Pathway through the Symplast. Plant Physiol. 1985 Sep;79(1):237–241. doi: 10.1104/pp.79.1.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Sharp R. E., Silk W. K., Hsiao T. C. Growth of the maize primary root at low water potentials : I. Spatial distribution of expansive growth. Plant Physiol. 1988 May;87(1):50–57. doi: 10.1104/pp.87.1.50. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Silk W. K., Erickson R. O. Kinematics of plant growth. J Theor Biol. 1979 Feb 21;76(4):481–501. doi: 10.1016/0022-5193(79)90014-6. [DOI] [PubMed] [Google Scholar]
  21. Spollen W. G., Sharp R. E. Spatial distribution of turgor and root growth at low water potentials. Plant Physiol. 1991 Jun;96(2):438–443. doi: 10.1104/pp.96.2.438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Steudle E. Water-relation Parameters of Individual Mesophyll Cells of the Crassulacean Acid Metabolism Plant Kalanchoë daigremontiana. Plant Physiol. 1980 Dec;66(6):1155–1163. doi: 10.1104/pp.66.6.1155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Tyree M. T. The symplast concept. A general theory of symplastic transport according to the thermodynamics of irreversible processes. J Theor Biol. 1970 Feb;26(2):181–214. doi: 10.1016/s0022-5193(70)80012-1. [DOI] [PubMed] [Google Scholar]
  24. Wolf S., Deom C. M., Beachy R. N., Lucas W. J. Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science. 1989 Oct 20;246(4928):377–379. doi: 10.1126/science.246.4928.377. [DOI] [PubMed] [Google Scholar]
  25. Wyse R. Sucrose uptake by sugar beet tap root tissue. Plant Physiol. 1979 Nov;64(5):837–841. doi: 10.1104/pp.64.5.837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Yahalom A., Warmbrodt R. D., Laird D. W., Traub O., Revel J. P., Willecke K., Epel B. L. Maize mesocotyl plasmodesmata proteins cross-react with connexin gap junction protein antibodies. Plant Cell. 1991 Apr;3(4):407–417. doi: 10.1105/tpc.3.4.407. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES