Planta

, Volume 136, Issue 1, pp 77–89 | Cite as

Distribution and structure of the plasmodesmata in mesophyll and bundle-sheath cells of Zea mays L.

  • R. F. Evert
  • W. Eschrich
  • W. Heyser
Article

Abstract

In leaf blades of Zea mays L. plasmodesmata between mesophyll cells are aggregated in numerous thickened portions of the walls. The plasmodesmata are unbranched and all are characterized by the presence of electron-dense structures, called sphincters by us, near both ends of the plasmodesmatal canal. The sphincters surround the desmotubule and occlude the cytoplasmic annulus where they occur. Plasmodesmata between mesophyll and bundle-sheath cells are aggregated in primary pit-fields and are constricted by a wide suberin lamella on the sheath-cell side of the wall. Each plasmodesma contains a sphincter on the mesophyll-cell side of the wall. The outer tangential and radial walls of the sheath cells exhibit a continuous suberin lamella. However, on the inner tangential wall only the sites of plasmodesmatal aggregates are consistently suberized. Apparently the movement of photosynthetic intermediates between mesophyll and sheath cells is restricted largely or entirely to the plasmodesmata (symplastic pathway) and transpirational water movement to the cell walls (apoplastic pathway).

Key words

Apoplast Bundle sheath Mesophyll Plasmodesmata Suberin lamella Symplast Zea 

Abbreviation

ER

endoplasmic reticulum

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References

  1. Anderson, J.M., Boardman, N.K., Spencer, D.: Phosphorylation by intact bundle sheath chloroplasts from maize. Biochim. Biophys. Acta 245, 253–258 (1971)PubMedGoogle Scholar
  2. Bil', K.Ya., Belobrodskaya, L.K., Karpilov, Yu.S.: Localization of ATPases in cellular structures of assimilating tissues in amaranth leaves. Dokl. Akad. Nauk SSSR (Engl. transln.) Bot. Sci. 226, 16–19 (1976)Google Scholar
  3. Black, C.C., Jr.: Photosynthetic carbon fixation in relation to net CO2 uptake. Ann. Rev. Plant Physiol. 24, 253–286 (1973)Google Scholar
  4. Chapman, E.A., Bain, J.M., Gove, D.W.: Mitochondria and chloroplast peripheral reticulum in the C4 plants Amaranthus edulis and Atriplex spongiosa. Aust. J. Plant Physiol. 2, 207–223 (1975)Google Scholar
  5. Chollet, R., Ogren, W.L.: Photosynthetic carbon metabolism in isolated maize bundle sheath strands. Plant Physiol. 51, 787–792 (1973)Google Scholar
  6. Chollet, R., Ogren, W.L.: Regulation of photorespiration in C3 and C4 species. Bot. Rev. 41, 137–179 (1975)Google Scholar
  7. Crowdy, S.H., Tanton, T.W.: Water pathways in higher plants. I. Free space in wheat leaves. J. exp. Bot. 21, 102–111 (1970)Google Scholar
  8. Esau, K.: Ontogeny of the vascular bundle in Zea mays. Hilgardia 15, 327–368 (1943)Google Scholar
  9. Evert, R.F., Eschrich, W., Neuberger, D.S., Eichhorn, S.E.: Tubular extensions of the plasmalemma in leaf cells of Zea mays L. Planta 1977Google Scholar
  10. Farineau, J.: Photoassimilation of CO2 by isolated bundle-sheath strands of Zea mays. I. Stimulation of CO2 assimilation by adding various intermediates of the phtosynthetic cycle; evidence for a deficient photosystem II activity. Physiol. Plantarum 33, 300–309 (1975a)Google Scholar
  11. Farineau, J.: Photoassimilation of CO2 by isolated bundle-sheath strands of Zea mays. II. Role of malate as a source of CO2 and reducing power for photosynthetic activity of isolated bundle-sheath cells of Zea mays. Physiol. Plantarum 33, 310–315 (1975b)Google Scholar
  12. Geiger, D.R.: Phloem loading in source leaves. In: Transport and transfer processes in plants, pp. 167–183, Wardlaw, I.F., Passioura, J.B., eds. New York-San Francisco-London: Academic Press 1976Google Scholar
  13. Giles, K.L., Beardsell, M.F., Cohen, D.: Cellular and ultrastructural changes in mesophyll and bundle sheath cells of maize in response to water stress. Plant Physiol. 54, 208–212 (1974)Google Scholar
  14. Giles, K., Cohen, D., Beardsell, M.F.: Effects of water stress on the ultrastructure of leaf cells of Sorghum bicolor. Plant Physiol. 57, 11–14 (1976)Google Scholar
  15. Gracen, V.E., Jr., Hilliard, J.H., Brown, R.H., West, S.H.: Peripheral reticulum in chloroplasts of plants differing in CO2 fixation pathways and photorespiration. Planta (Berl.) 107, 189–204 (1972)Google Scholar
  16. Gunning, B.E.S.: Introduction to plasmodesmata. In: Intercellular communication in plants: Studies on plasmodesmata, pp. 1–13, Gunning, B.E.S., Robards, A.W., eds. Berlin-Heidelberg-New York: Springer 1976Google Scholar
  17. Gunning, B.E.S., Robards, A.W.: Plasmodesmata: current knowledge and outstanding problems. In: Intercellular communications in plants: Studies on plasmodesmata, pp. 297–311, Gunning, B.E.S., Robards, A.W., eds. Berlin-Heidelberg-New York: Springer 1976 (a)Google Scholar
  18. Gunning, B.E.S., Robards, A.W.: Plasmodesmata and symplastic transport. In: Transport and transfer processes in plants, pp. 15–41, Wardlaw, I.F., Passioura, J.B., eds. New York-San Francisco-London: Academic Press 1976 (b)Google Scholar
  19. Gutierrez, M., Gracen, V.E., Edwards, G.E.: Biochemical and cytological relationships in C4 plants. Planta (Berl.) 119, 279–300 (1974)Google Scholar
  20. Hatch, M.D., Kagawa, T.: Photosynthetic activities of isolated bundle sheath cells in relation to differing mechanisms of C4 pathway photosynthesis. Arch. Biochem. Biophys. 175, 39–53 (1976)PubMedGoogle Scholar
  21. Hatch, M.D., Kagawa, T., Craig, S.: Subdivision of C4-pathway species based on differing C4 acid decarboxylating systems and ultrastructural features. Aust. J. Plant Physiol. 2, 111–128 (1975)Google Scholar
  22. Hattersley, P.W., Watson, L.: Anatomical parameters for predicting photosynthetic pathways of grass leaves: the “maximum lateral cell count” and the “maximum cells distant count”. Phytomorphology 25, 325–333 (1975)Google Scholar
  23. Hattersley, P.W., Watson, L., Osmond, C.B.: Metabolite transport in leaves of C4 plants: specification and speculation. In: Transport and transfer processes in plants, pp. 191–201, Wardlaw, I.F., Passioura, J.B., eds. New York-San Francisco-London: Academic Press 1976Google Scholar
  24. Heyser, W., Leonard, O., Heyser, R., Fritz, E., Eschrich, W.: The influence of light, darkness, and the lack of CO2 on phloem translocation in detached maize leaves. Planta (Berl.) 122, 143–154 (1975)Google Scholar
  25. Heyser, W., Heyser, R., Eschrich, W., Leonard, O.A., Rautenberg, M.: The influence of externally applied organic substances on phloem translocation in detached maize leaves. Planta (Berl.) 132, 269–277 (1976)Google Scholar
  26. Karas, I., McCully, M.E.: Further studies of the histology of lateral root development in Zea mays. Protoplasma 77, 243–269 (1973)Google Scholar
  27. Karpilov, Yu.S., Bil', K.Ya.: Transport of intermediate photosynthesis products through the cytoplasm of cells assimilating tissues in C4 plants. Dokl. Akad. Nauk SSSR (Engl. transln.) Bot. Sci. 226, 24–27 (1976)Google Scholar
  28. Kirchanski, S.J.: The ultrastructural development of the dimorphic plastids of Zea mays L. Amer. J. Bot. 62, 695–705 (1975)Google Scholar
  29. Ku, S.B., Edwards, G.E.: Photosynthesis in mesophyll protoplasts and bundle sheath cells of various types of C4 plants. IV. Enzymes of respiratory metabolism and energy utilizing enzymes of photosynthetic pathways. Z. Pflanzenphysiol. 77, 16–32 (1975)Google Scholar
  30. Ku, S.B., Gutierrez, M., Kanai, R., Edwards, G.E.: Photosynthesis in mesophyll protoplasts and bundle sheath cells of various types of C4 plants. II. Chlorophyll and Hill reaction studies. Z. Pflanzenphysiol. 72, 320–337 (1974)Google Scholar
  31. Kuo, J., O'Brien, T.P., Canny, M.J.: Pit-field distribution, plasmodesmatal frequency, and assimilate flux in the mestome sheath cells of wheat leaves. Planta (Berl.) 121, 97–118 (1974)Google Scholar
  32. Laetsch, W.M.: Chloroplast structural relationships in leaves of C4 plants. In: Photosynthesis and photorespiration, pp. 323–349, Hatch, M.D., Osmond, C.B., Slatyer, R.O., eds. New York: Wiley-Interscience 1971Google Scholar
  33. Läuchli, A.: Apoplastic transport in tissues. In: Transport in plants, pp. 3–34, Lüttge, U., Pitman, M.G., eds. Berlin-Heidelberg-New York: Springer 1976Google Scholar
  34. Lush, W.M., Evans, L.T.: Translocation of photosynthetic assimilate from grass leaves, as influenced by environment and species. Aust. J. Plant Physiol. 1, 417–431 (1974)Google Scholar
  35. Metcalfe, C.R.: Anatomy of the monocotyledons. I. Gramineae. Oxford: Clarendon Press 1960Google Scholar
  36. Miyake, H., Maeda, E.: Development of bundle sheath chloroplasts in rice seedlings. Canad. J. Bot. 54, 556–565 (1976)Google Scholar
  37. O'Brien, T.P., Carr, D.J.: A suberized layer in the cell walls of the bundle sheath of grasses. Aust. J. biol. Sci. 23, 275–287 (1970)Google Scholar
  38. Olesen, P.: Plasmodesmata between mesophyll and bundle sheath cells in relation to the exchange of C4-acids. Planta (Berl.) 123, 199–202 (1975)Google Scholar
  39. Osmond, C.B.: Metabolite transport in C4 photosynthesis. Aust. J. biol. Sci. 24, 159–163 (1971)PubMedGoogle Scholar
  40. Osmond, C.B.: Carbon reduction and photosystem II deficiency in leaves of C4 plants. Aust. J. Plant Physiol. 1, 41–50 (1974)Google Scholar
  41. Osmond, C.B., Smith, F.A.: Symplastic transport of metabolites during C4-photosynthesis. In: Intercellular communication in plants: Studies on plasmodesmata, pp. 229–240, Gunning, B.E.S., Robards, A.W., eds. Berlin-Heidelberg-New York: Springer 1976Google Scholar
  42. Robards, A.W.: Plasmodesmata in higher plants. In: Intercellular communication in plants: Studies on plasmodesmata, pp. 15–57, Gunning, B.E.S., Robards, A.W., eds. Berlin-Heidelberg-New York: Springer 1976Google Scholar
  43. Slack, C.R., Hatch, M.D., Goodchild, D.J.: Distribution of enzymes in mesophyll and parenchyma-sheath chloroplasts of maize leaves in relation to the C4-dicarboxylic acid pathway of photosynthesis. Biochem. J. 114, 489–498 (1969)PubMedGoogle Scholar
  44. Troughton, J.H.: Carbon isotope fractionation by plants. In: Proc VIII Int. Radiocarbon Dating Conf., held at Lower Hutt, N.Z., 18–25 October; organized by the Roy. Soc. N.Z.; compiled by T.A. Rafter, T. Grant-Taylor, vol. 2, pp. 420–438 (1972)Google Scholar
  45. Usuda, H., Kanai, R., Miyachi, S.: Carbon dioxide assimilation and photosystem H deficiency in bundle sheath strands isolated from C4 plants. Plant Cell Physiol. 16, 485–494 (1975)Google Scholar
  46. Weatherley, P.E.: Some aspects of water relations. Adv. Bot. Res. 3, 171–206 (1970)Google Scholar
  47. Whelan, T., Sackett, W.M., Benedict, C.R.: Enzymatic fractionation of carbon isotopes by phosphoenolpyruvate carboxylase from C4 plants. Plant Physiol. 51, 1051–1054 (1973)Google Scholar

Copyright information

© Springer-Verlag 1977

Authors and Affiliations

  • R. F. Evert
    • 1
    • 2
  • W. Eschrich
    • 1
    • 2
  • W. Heyser
    • 1
    • 2
  1. 1.Department of BotanyUniversity of WisconsinMadisonUSA
  2. 2.Forstbotanisches Institut der Universität GöttingenGöttingen-WeendeFederal Republic of Germany

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