The Histochemical Journal

, Volume 18, Issue 11–12, pp 647–657 | Cite as

Preliminary evidence for a cholinergic-like system in lichen morphogenesis

  • Margherita Raineri
  • Paolo Modenesi


Membrane acetylcholinesterase activity is considered to be a marker for a cholinergic system. When temporarily expressed in differentiating cells other than the nervous or muscular ones, it may play a role in morphogenesis. In the lichenParmelia caperata (L.) Ach., acetylcholinesterase is histochemically localized mainly in the cell walls and/or membranes of both symbionts just where they proliferate and form well-organized propagation structures, the soredia. The enzyme activity is first detected in a few algae undergoing aplanosporogenesis and later in medullary hyphae that reach the dividing algae by elongating perpendicularly to the thallus surface. This histochemical pattern that is associated with algal proliferation and oriented hyphal growth is characteristic of early morphogenesis of the soredia; when fully differentiated, they consist of an inner dividing alga and an outer hyphal envelope, both showing cholinesterase activity. Substrate specificity and inhibitor sensitivity of the histochemical staining indicate an acetylcholinesterase-like activity. However, extracts of the thallus areas where soredia develop give four bands of cholinesterase activity on disc electrophoresis: the two cathodal bands have the characteristics of acetylcholinesterase, the others of pseudocholinesterase. One of the latter hydrolyses propionylthiocholine very rapidly. The findings suggest that in lichen symbiosis, a cholinergic-like system participates in regulating morphogenetic processes such as cell division, oriented tip growth and alga-fungus membrane interactions. Environmental stimuli, particularly light, might trigger the development of soredia by modulating the activity of the cholinergic mechanism.


Acetylcholinesterase Cholinergic System Hyphal Growth Cholinesterase Activity Acetylcholinesterase Activity 
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  1. AHMADJIAN, V. (1982) Algal/fungal symbioses. InProgress of Phycological Research, Vol. 1. (Edited by ROUND, F. E. and CHAPMAN, D. S.). pp. 179–223. Amsterdam: Elsevier Biomedical.Google Scholar
  2. ARMBRUSTER, B. L. & WEISENSEEL, M. H. (1983) Ionic currents traverse growing hyphae and sporangia of the mycelian water moldAchlya debaryana.Protoplasma 115, 65–9.Google Scholar
  3. BEHRENS, H. M., WEISENSEEL, M. H. & SIEVERS, A. (1982) Rapid changes in the pattern of electric current around the root tip ofLepidium sativum (L.) following gravistimulation.Plant Physiol. 70, 1079–83.Google Scholar
  4. BLATT, M. R., WEISENSEEL, M. H. & HAUPT, W. (1981) A light-dependent current associated with chloroplast aggregation in the algaVaucheria sessilis.Planta 152, 513–26.Google Scholar
  5. BORGENS, R. B. (1982) What is the role of naturally produced electric current in vertebrate regeneration and healing?Int. Rev. Cytol. 76, 245–98.Google Scholar
  6. BORGENS, R. B., ROULEAU, M. F. & DELANNEY, L. E. (1983) A steady efflux of ionic current predicts hind limb development in the axolotl.J, Exp. Zool. 228, 491–503.Google Scholar
  7. BURNS, C. P. & ROZENGURT, E. (1984) Extracellular Na+ and initiation of DNA synthesis: role of intracellular pH and K+.J. Cell Biol. 98, 1082–9.Google Scholar
  8. BUZNIKOV, G. A. (1980) Biogenic monoamines and acetylcholine in Protozoa and metazoan embryos. InNeurotransmitters: Comparative Aspects (Edited by SALÁNKI, J. and TURPAEV, T. M.) pp. 7–29. Budapest: Akadémiai Kiadó.Google Scholar
  9. BUZNIKOV, G. A. & SHMUKLER, Y. B. (1981) Possible role of ‘prenervous’ neurotransmitters in cellular interactions of early morphogenesis: a hypothesis.Neurochem. Res. 6, 55–68.Google Scholar
  10. CHEN, T-H. & JAFFE, L. F. (1979) Forced calcium entry and polarized growth ofFunaria spores.Planta 144, 401–6.Google Scholar
  11. DARBISHIRE, O. V. (1897) Die deutschen Pertusariaceen mit besondered Berücksichtigung ihrer Sorredien bildung.Engl. Bot, Jahr. 22, 593–671.Google Scholar
  12. DETTBARN, W. D. (1962) Acetylcholinesterase activity inNitella.Nature 194, 1175–6.Google Scholar
  13. DREWS, U. Cholinesterase in embryonic development.Prog. Histochem. Cytochem. 7, 1–52.Google Scholar
  14. ERICKSON, C. A. & NUCCITELLI, R. (1984) Embryonic fibroblast motility and orientation can be influenced by physiological electric fields.J. Cell Biol. 98, 296–307.Google Scholar
  15. ERNST, M. & HARTMANN, E. (1980) Biochemical characterization of an acetylcholine-hydrolyzing enzyme from bean seedlings.Plant Physiol. 65, 447–50.Google Scholar
  16. EVANS, M. L. (1972) Promotion of cell elongation inAvena coleoptiles by acetylcholine.Plant Physiol. 50, 414–16.Google Scholar
  17. FALUGI, C. (1985) Histochemical localization of acetylcholinesterase in blood cells.Bas. Appl. Histochem. 29, 105–13.Google Scholar
  18. FALUGI, C. & RAINERI, M. (1985) Acetylcholinesterase (AChE) and pseudocholinesterase (BuChE) activity distribution pattern in early developing chick limb.J. Embryol. Exp. Morphol. 86, 89–108.Google Scholar
  19. FLUCK, R. A. & JAFFE, M. J. (1975) Cholinesterases from plant tissues. I. Purification and characterization of enzymes fromSolanum melogena andZea mays.Biochim. Biophys. Acta,410, 130–4.Google Scholar
  20. GOLDSWORTHY, A. & RATHORE, K. S. (1985) The electrical control of growth in plant tissues cultures: the polar transport of auxin.J. Exp. Bot. 36, 1134–41.Google Scholar
  21. GOODWIN, B. C. & PATEROMICHELAKIS, S. (1979) The role of electrical fields, ions, and the cortex in the morphogenesis ofAcetabularia.Planta 145, 427–35.Google Scholar
  22. GUPTA, R. & MAHESHWARI, S. C. (1980) Preliminary characterization of a cholinesterase from roots of Bengal gram -Cicer arietinum L.Plant & Cell Physiol. 21, 1675–9.Google Scholar
  23. HARTMANN, E. (1975) Influence of light on the bioelectric potential of the bean (Phaseolus vulgaris) hypocotyl hook.Physiol. Plant. 33, 266–75.Google Scholar
  24. HARTMANN, E. (1977) Influence of acetylcholine and light on the bioelectric potential of bean (Phaseolus vulgaris) hypocotyl hook.Plant & Cell Physiol. 18, 1203–7.Google Scholar
  25. HARTMANN, E. & KIBLINGER, H. (1974a) Gas-liquid chromatographic determination of light-dependent acetylcholine concentration in moss callus.Biochem. J. 137, 249–52.Google Scholar
  26. HARTMANN, E. & KIBLINGER, H. (1974b) Occurrence of lightdependent acetylcholine concentrations in higher plants.Experientia 30, 1387–8.Google Scholar
  27. HESKETH, T. R., MOORE, J. P., MORRIS, J. D. H., TAYLOR, M. V., ROGERS, J., SMITH, G. A. & METCALFE, J. C. (1985) A common sequence of calcium and pH signals in the mitogenic stimulation of eukaryotic cells.Nature 313, 481–4.Google Scholar
  28. HOITINK, A. W. & DIJK, G. V. (1965) The influence of neurohumoral transmitter substances on protoplasmic streaming in the MyxomycetePhysarella oblonga.J. Cell. Physiol. 67, 133–40.Google Scholar
  29. HOSHINO, T. (1983a) Effects of acetylcholine on the growth of theVigna seedlings.Plant & Cell Physiol. 24, 551–6.Google Scholar
  30. HOSHINO, T. (1983b) Identification of acetylcholine as a natural constituent ofVigna seedlings.Plant & Cell Physiol. 24, 829–34.Google Scholar
  31. JAFFE, M. J. (1970) Evidence for the regulation of phytochrome-mediated processes in bean roots by the neurohumor, acetylcholine.Plant Physiol. 46, 768–77.Google Scholar
  32. JAFFE, M. J. (1972) Acetylcholine as a native metabolic regulator of phytochrome-mediated processes in bean roots. InRecent Advances in Phytochemistry. Vol. 5, (Edited by RUNECKLES, V. C. and TSO, T. C.) pp. 81–104. New York, Academic Press.Google Scholar
  33. JAFFE, L. F. (1982) Developmental currents, voltages and gradients. InDevelopmental Order: its Origin and Regulation. (Edited by SUBTELNY, S. and GREEN, P. B.) pp. 183–215. New York: Alan R. Liss.Google Scholar
  34. JAMIESON, JR, G. A., FRAZIER, W. A. & SCHLESINGER, P. H. (1984) Transient increase in intracellular pH duringDictyostelium differentiation.J. Cell Biol. 99, 1883–7.Google Scholar
  35. KARNOVSKY, M. J. & ROOTS, L. (1964) A ‘direct-coloring’ thiocholine method for cholinesterases.J. Histochem. Cytochem. 12, 219–21.Google Scholar
  36. KEYHANI, E. & MAIGNE, J. (1981) Acetylcholinesterase in mammalian erythroid cells.J. Cell Sci. 52, 327–39.Google Scholar
  37. KROPF, D. L., LUPA, M. D. A., CALDWELL, J. H. & HAROLD, F. M. (1983) Cell polarity: endogenous ion currents precede and predict branching in the water moldAchlya.Science 220, 1385–7.Google Scholar
  38. KROPF, D. L., CALDWELL, J. H., GOW, N. A. R. & HAROLD, F. M. (1984) Transcellular ion currents in the water moldAchlya. Amino acid proton symport as a mechanism of current entry.J. Cell Biol. 99, 486–96.Google Scholar
  39. LALLEMANT, R. (1972) Etude de la formation des sorédies chez le DiscolichenBuellia canescens (Dicks.) D. Notrs.Bull. Soc. Bot. Fr. 119, 463–76.Google Scholar
  40. LEES, G. L. & THOMPSON, J. E. (1975) The effects of germination on the subcellular distribution of cholinesterase in cotyledons ofPhaseolus vulgaris.Physiol. Plant. 34, 230–7.Google Scholar
  41. MCMAHON, D. (1974) Chemical messengers in development: a hypothesis.Science 185, 1012–21.Google Scholar
  42. MINGANTI, A., FALUGI, C., RAINERI, M. & PESTARINO, M. (1981) Acetylcholinesterase in the embryonic development: an invitation to a hypothesis.Acta Embryol. Morph. Exper. 2, 30–31.Google Scholar
  43. MITCHELL, P. (1976) Vectorial chemistry and the molecular mechanism of chemiosmotic coupling: power transmission by proticity.Trans. Biochem. Soc. 4, 399–430.Google Scholar
  44. MIURA, G. A. & SHIH, T-M. (1984) Cholinergic constituents in plants: characterization and distribution of acetylcholine and choline.Physiol. Plant. 61, 417–21.Google Scholar
  45. MOREAU, F. (1928) Les Lichens: morphologie, biologie, systématique. InEnciclopédie biologique, Vol. 2, pp. 77–80. Paris: Paul Lechevalier.Google Scholar
  46. MUKHERJEE, I. (1980) The effect of acetylcholine on hypocotyl elongation in soybean.Plant & Cell Physiol. 21, 1657–60.Google Scholar
  47. MÜLLER, W. A. & EL-SHERSHABY, E. (1981) Electrical current and cAMP induce lateral branching in the stolon of hydroids.Devel. Biol. 87, 24–9.Google Scholar
  48. NAKAJIMA, H. & HATANO, S. (1962) Acetylcholinesterase in the plasmodium of the myxomycete,Physarum polycephalum.J. Cell. Comp. Physiol. 59, 259–64.Google Scholar
  49. NEUMANN, E. & NACHMANSOHN, D. (1975) Nerve excitability. Towards an integrating concept. InBiomembranes, Vol. 7 (edited by MANSON, L. A.) pp. 99–166. New York: Plenum Press.Google Scholar
  50. ORNSTEIN, L. & DAVIS, B. (1962)Disk Electrophoresis. Parts I and II. Distillation Products Industries, Rochester, New York.Google Scholar
  51. OZAKI, H. (1976) Molecular properties and differentiation of acetylcholinesterase in sea urchin embryos.Devel. Growth Diff. 18, 245–57.Google Scholar
  52. RAINERI, M. & FALUGI, C. (1983) Acetylcholinesterase activity in embryonic and larval development ofArtemia salina Leach (Crustaceae Phyllopoda).J. Exp. Zool. 227, 229–46.Google Scholar
  53. RAINERI, M. & MODENESI, P. (1984) The cholinergic system: a hypothesis of its general role in living cells. InCellular and Molecular Control of Direct Cell Interactions in Developing Systems, pp. 49–50. Banyuls-sur-Mer, France: NATO—ASI.Google Scholar
  54. RATHORE, K. S. & GOLDSWORTHY, A. (1985) Electrical control of growth in plant tissue cultures.Biotechnology 3, 253–4.Google Scholar
  55. RIOV, J. & JAFFE, M. J. (1973a) Cholinesterases from plant tissues. I. Purification and characterization of a cholinesterase from mung bean roots.Plant Physiol. 51, 520–8.Google Scholar
  56. RIOV, J. & JAFFE, M. J. (1973b) A cholinesterase from bean roots and its inhibition by plant growth retardants.Experientia 29, 264–5.Google Scholar
  57. SCHWENDENER, S. (1860) Untersuchungen über der Flechtenthallus.Beitr. Wiss. Bot. (Leipzig)2, 108–86.Google Scholar
  58. SMITH, D. C. (1974) Transport from symbiotic algae and symbiotic chloroplast to host cells.Symp. Soc. Exper. Biol. 28, 485–520.Google Scholar
  59. SMITH, D. C. (1975) Symbiosis and the biology of lichenized fungi. InSymbiosis. 29th Symposium of the Society for Experimental Biology. pp. 373–405. London: Cambridge University Press.Google Scholar
  60. SUN, I. L., CRANE, F. L., GREBIG, C. & LOW, H. (1985) Transmembrane redox in control of cell growth. Stimulation of HeLa cell growth by ferricyanide and insulin.Exp. Cell Res. 156, 528–36.Google Scholar
  61. TAPPER, R. C. (1981) Direct measurement of translocation of carbohydrate in the lichen,Cladonia convoluta, by quantitative autoradiography.New Phytol. 89, 429–37.Google Scholar
  62. THEIDEMANN, K-U., VANITTANAKOM, P., SCHWEERS, F-M. & DREWS, U. (1986) Embryonic cholinesterase activity during morphogenesis of the mouse genital tract.Cell Tiss. Res. 244, 153–64.Google Scholar
  63. TOPILKO, A. & CAILLOU, B. (1985) Fine structural localization of acetylcholinesterase activity in rat submandibular gland.J. Histochem. Cytochem. 33, 439–45.Google Scholar
  64. TREWAVAS, A. J., SEXTON, R. & KELLY, P. (1984) Polarity, calcium and abscission: molecular bases for developmental plasticity in plants.J. Embryol. Exper. Morph. 83, (suppl.) 179–95.Google Scholar
  65. TSUJI, S. (1974) On the chemical basis of thiocholine methods for demonstration of acetylcholinesterase activity.Histochemistry 42, 99–105.Google Scholar
  66. VANITTANAKOM, P. & DREWS, U. (1985) Ultrastructural localization of cholinesterase during chondrogenesis and myogenesis in the chick limb bud.Anat. Embryol. 172, 183–94.Google Scholar
  67. WAALAND, S. D. & LUCAS, W. J. (1984) An investigation of the role of transcellular ion currents in morphogenesis ofGriffithsia pacifica Kylin.Protoplasma 123, 184–91.Google Scholar
  68. WEINBERGER, C., PENNER, P. L. & BRICK, I. (1984) Polyingression, an important morphogenetic movement in chick gastrulation.Am. Zool. 24, 545–54.Google Scholar
  69. WEISENSEEL, M. H., DORN, A. & JAFFE, L. F. (1979) Natural H+ currents traverse growing roots and root hairs of barley (Hordeum vulgare L.)Plant Physiol. 64, 512–18.Google Scholar
  70. YUNGHANS, H. & JAFFE, M. J. (1972) Rapid respiratory changes due to red light or acetylcholine during the early events of phytochrome-mediated photomorphogenesis.Plant Physiol. 49, 1–7.Google Scholar

Copyright information

© Chapman and Hall Ltd. 1986

Authors and Affiliations

  • Margherita Raineri
    • 1
  • Paolo Modenesi
    • 2
  1. 1.Institute of Comparative AnatomyUniversity of GenovaGenovaItaly
  2. 2.Institute of Botany "Hanbury"University of GenovaGenovaItaly

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