Skip to main content
Log in

Sporopollenin in the cell wall of Chlorella and other algae: Ultrastructure, chemistry, and incorporation of 14C-acetate, studied in synchronous cultures

  • Published:
Planta Aims and scope Submit manuscript

Summary

Cells of Chlorella fusca var. vacuolata (Cambridge 211/8p) resisted efforts aimed at producing naked protoplasts by enzymatic degradation of the cell wall, and a study of the development and composition of the wall was therefore undertaken.

  1. 1.

    After cytokinesis has produced naked autospores within the mother cell wall, cell wall formation commences outside the autospore plasma membrane with the appearance of small trilaminar plaques. These enlarge while inter-autospore granular material diminishes in quantity, and they eventually fuse to produce a complete trilaminar sheath around each autospore.

  2. 2.

    A microfibrillar, cellulase digestible, layer is deposited between the trilaminar component and the plasma membrane. Meanwhile the corresponding microfibrillar component of the mother cell wall is digested leaving only its resistant trilaminar component.

  3. 3.

    The trilaminar component includes a substance considered to be the polymerized carotenoid, sporopollenin, on the basis of its resistance to extreme extraction procedures including acetolysis, and its infra red absorption spectrum.

  4. 4.

    Two phases of sporopollenin biosynthesis were detected by means of pulse and pulse-chase treatments with 14C-acetate at intervals during the cell cycle in synchronous cultures. One coincides with the formation of the sporopollenin-containing trilaminar wall component, and the other is 6–8 hours earlier while the cells are in karyokinesis. The former yields labelled sporopollenin directly and the latter probably represents formation of a precursor.

  5. 5.

    Of five other strains of Chlorella tested, only one possesses sporopollenin, and so does one Scenedesmus and two out of three strains of Prototheca.

  6. 6.

    Examination of the wall structure of the above algae suggest a relationship between the presence of sporopollenin and the development of an outer, trilaminar wall component.

  7. 7.

    A survey of the literature gives support to this hypothesis and further suggests that the ability to synthesise sporopollenin is related to the ability to produce secondary carotenoids.

  8. 8.

    The significance of the findings is discussed.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Atkinson, A. W., Jr., Gunning, B. E. S., John, P. C. L., McCullough, W.: Centrioles and microtubules in Chlorella. Nature New Biol. 234, 24–25 (1971).

    Google Scholar 

  • Bendix, S., Allen, M. B.: Ultra-violet induced mutants of Chlorella pyrenoidosa. Arch. Mikrobiol. 41, 115–141 (1962).

    Google Scholar 

  • Bisalputra, T.: The origin of the peptic layer of the cell wall of Scenedesmus quadricauda. Canad. J. Bot. 43, 1549–1552 (1965).

    Google Scholar 

  • Bisalputra, T., Ashton, F. M., Weier, T. E.: Role of dictyosomes in wall formation during cell division of Chlorella vulgaris. Amer. J. Bot. 53, 213–216 (1966).

    Google Scholar 

  • Bisalputra, T., Weier, T. E.: The cell wall of Scenedesmus quadricauda. Amer. J. Bot. 50, 1011–1019 (1963).

    Google Scholar 

  • Bisalputra, T., Weier, T. E., Risley, E. B., Engelbrecht, A. H. P.: The pectic layer of the cell wall of Scenedesmus quadricauda. Amer. J. Bot. 51, 548–551 (1964).

    Google Scholar 

  • Bowen, W. R.: Ultrastructural aspects of the cell boundary of Haematococcus pluvialis. Trans. Amer. microscop. Soc. 86, 36–43 (1967).

    Google Scholar 

  • Brooks, J.: Some chemical and geochemical studies on sporopollenin. In: Sporopollenin (J. Brooks, P. R. Grant, M. Muir, P. van Gijzel, and G. Shaw, eds.), p. 351–407. London: Acad. Press 1971.

    Google Scholar 

  • Brooks, J., Shaw, G.: Recent developments in the chemistry, biochemistry, geochemistry and post-tetrad ontogeny of sporopollenins derived from pollen and spore exines. In: Pollen: Development and physiology (J. Heslop-Harrison, ed.), p. 99–114. London: Butterworths 1971.

    Google Scholar 

  • Budd, T. W., Tjostem, J. L., Duysen, M. E.: Ultrastructure of Chlorella pyrenoidosa as affected by environmental changes. Amer. J. Bot. 56, 540–545 (1969).

    Google Scholar 

  • Burzyk, J., Grzybek, H., Banaś, J., Banaś, E.: Studies on the ultrastructure of the cell walls of Scenedesmus 1. Acta med. pol. 12, 143–146 (1971).

    Google Scholar 

  • Burczyk, J., Grzybek, H., Banaś, J., Banaś, E.: Presence of cellulase in the alga Scenedesmus. Exp. Cell Res. 63, 451–453 (1971).

    Google Scholar 

  • Callely, A. G., Lloyd, D.: The metabolism of acetate in the colourless alga Prototheca zopfii. Biochem. J. 90, 483–489 (1964).

    Google Scholar 

  • Chaloner, W. G., Orbell, G.: A palaeobotanical definition of sporopollenin. In: Sporopollenin (J. Brooks, P. R. Grant, M. Muir, P. van Gijzel and G. Shaw, eds.), p. 273–294. London: Acad. Press 1971.

    Google Scholar 

  • Claes, H.: Analyse der biochemischen Synthesekette für Carotinoide mit Hilfe von Chlorella-Mutanten. Z. Naturforsch. 9b, 461–470 (1954).

    Google Scholar 

  • Claes, H.: Action spectrum of light-dependent carotenoid synthesis in Chlorella vulgaris. In: Biochemistry of chloroplasts (T. W. Goodwin, ed.), vol 2, p. 441–444 London: Acad. Press 1967.

    Google Scholar 

  • Cocking, E. C.: Virus uptake, cell wall regeneration, and virus multiplication in isolated plant protoplasts. Int. Rev. Cytol. 28, 89–124 (1970).

    Google Scholar 

  • Czygan, F.-C.: Sekundär-Carotinoide in Grünalgen. 1. Chemie, Vorkommen und Faktoren, welche die Bildung dieser Polyene beeinflussen. Arch. Mikrobiol. 61, 81–102 (1968).

    Google Scholar 

  • Deason, T. R., Darden, W. H., Jr., Ely, S.: The development of sperm packets of the M5 strain of Volvox aureus. J. Ultrastruct. Res. 26, 85–94 (1969).

    Google Scholar 

  • Dickinson, H. G.: The role played by sporopollenin in the development of pollen in Pinus banksiana. In: Sporopollenin (J. Brooks, P. R. Grant, M. Muir, P. van Gijzel and G. Shaw, eds.), p. 31–67. London: Acad. Press 1971.

    Google Scholar 

  • Dickinson, H. G., Heslop-Harrsion, J.: The mode of growth of the inner layer of the pollen-grain exine in Lilium. Cytobios 4, 233–243 (1971).

    Google Scholar 

  • Eberhardt, U.: The cell wall as the site of carotenoid in the “Knallgas” bacterium. Arch. Mikrobiol. 80, 32–37 (1971).

    Google Scholar 

  • Faegri, K., Iversen, J.: Textbook of pollen analysis. Copenhagen: Munksgaard 1964.

    Google Scholar 

  • Gawlik, S. R., Millington, W. F.: Pattern formation and the fine structure of the developing cell wall in colonies of Pediastrum boryanum. Amer. J. Bot. 56, 1084–1093 (1969).

    Google Scholar 

  • Gergis, M. S.: A colourless Chlorella mutant containing thylakoids. Arch. Mikrobiol. 68, 187–190 (1969).

    Google Scholar 

  • Gergis, M. S.: The presence of microbodies in three strains of Chlorella. Planta (Berl.) 101, 180–184 (1971).

    Google Scholar 

  • Gooday, G. W.: A biochemical and autoradiographic study of the role of the Golgi bodies in thecal formation in Platymonas tetrahele. J. exp. Bot. 22, 959–971 (1971).

    Google Scholar 

  • Goulding, K. H., Merrett, M. J.: The photometabolism of acetate by Chlorella pyrenoidosa. J. exp. Bot. 17, 678–689 (1966).

    Google Scholar 

  • Griffiths, D.A., Griffiths, D. J.: The fine structure of autotrophic and heterotrophic cells of Chlorella vulgaris (Emerson strain). Pl. Cell Physiol. 10, 11–19 (1969).

    Google Scholar 

  • Hanic, L. A., Craigie, J. S.: Studies on the algal cuticle. J. Physiol. 5, 89–102 (1969).

    Google Scholar 

  • Hawkins, A. F., Leedale, G. F.: Zoospore structure and colony formation in Pediastrum spp. and Hydrodictyon reticulatum (L.) Lagerheim. Ann. Bot. 35, 201–211 (1971).

    Google Scholar 

  • Heslop-Harrison, J.: The pollen wall: structure and development. In: Pollen: Development and physiology (J. Heslop-Harrison, ed.), p. 75–98. London: Butterworths 1971.

    Google Scholar 

  • Horner, H. J., Lersten, N. R., Bowen, C. C.: Spore development in the liverwort Riccardia pinguis. Amer. J. Bot. 53, 1048–1064 (1966).

    Google Scholar 

  • Karakashian, S. J.: Morphological plasticity and the evolution of algal symbionts. Ann. N.Y. Acad. Sci. 175, 474–487 (1970).

    Google Scholar 

  • Karakashian, S. J., Karakashian, M. W., Rudzinska, M.: Electron microscopic observations on the symbiosis of Paramecium bursaria and its intracellular algae. J. Protozool. 15, 113–128 (1968).

    Google Scholar 

  • Kessler, E., Langner, W., Ludewig, I., Wiechmann, H.: Bildung von Sekundär-Carotinoiden bei Stickstoffmangel und Hydrogenase-Aktivität als taxonomische Merkmale in der Gattung Chlorella. In: Studies on microalgae and photosynthetic bacteria (Japan Soc. Plant Physiol., eds.), p. 7–20. Tokyo: Univ. of Tokyo Press 1963.

    Google Scholar 

  • Kochert, G., Olson, L. W.: Ultrastructure of Volvox Carteri 1. The asexual colony. Arch. Mikrobiol. 74, 19–30 (1970).

    Google Scholar 

  • Lang, N. J.: Electron microscopy of the Volvocaceae and Astrephomenaceae. Amer. J. Bot. 50, 280–300 (1963).

    Google Scholar 

  • Lang, N. J.: Electron microscopic studies of extraplastidic astaxanthin in Haematococcus. J. Phycol. 4, 12–19 (1968).

    Google Scholar 

  • Lewin, R. A.: The cell wall of Platymonas. J. gen. Microbiol. 19, 87–90 (1958).

    Google Scholar 

  • Lloyd, D., Turner, G.: The cell wall of Prototheca zopfii. J. gen. Microbiol. 50, 421–427 (1968).

    Google Scholar 

  • Lorenzen, H.: Synchrone Zellteilungen von Chlorella bei verschiedenen Licht-Dunkel-Wechseln. Flora (Jena) 144, 473–496 (1957).

    Google Scholar 

  • Manton, I., Parke, M.: Observations on the fine structure of two species of Platymonas with special reference to flagellar scales and the mode of origin of the theca. J. marine biol. Ass. 45, 743–754 (1965).

    Google Scholar 

  • Marchant, H. J., Pickett-Heaps, J. D.: Ultrastructure and differentiation of Hydrodictyon reticulatum. II. Formation of zooids within the coenobium. Aust. J. biol. Sci. 24, 471–486 (1971).

    Google Scholar 

  • Mayer, F., Czygan, F. C.: Änderungen der Ultrastrukturen in den Grünalgen Ankistrodesmus braunii und Chlorella fusca var. rubescens bei Stickstoffmangel. Planta (Berl.) 86, 175–185 (1969).

    Google Scholar 

  • McCullough, W., John, P. C. L.: Temporal control of the de novo synthesis of isocitrate lyase during the cell cycle of the eucaryote Chlorella pyrenoidosa. Biochim. biophys. Acta (Amst.) 269, 287–296 (1972).

    Google Scholar 

  • McLean, R. J.: Primary and secondary carotenoids of Spongiochloris typica. Physiol. Plantarum (Cbh.) 20, 41–47 (1967).

    Google Scholar 

  • McLean, R. J.: Ultrastructure of Spongiochloris typica during senescence. J. Phycol. 4, 277–283 (1968).

    Google Scholar 

  • Menke, W., Fricke, B.: Einige Beobachtungen an Prototheca ciferrii. Port. Acta biol. A 6, 243–252 (1962).

    Google Scholar 

  • Merrett, M. J., Goulding, K. H.: Short-term products of 14C-acetate assimilation by Chlorella pyrenoidosa in the light. J. exp. Bot. 18, 128–139 (1967).

    Google Scholar 

  • Millington, W. F., Gawlik, S. R.: Silica in the wall of Pediastrum. Nature (Lond.) 216, 68 (1967).

    Google Scholar 

  • Millington, W. F., Gawlik, S. R.: Ultrastructure and initiation of wall pattern in Pediastrum boryanum. Amer. J. Bot. 57, 552–561 (1970).

    Google Scholar 

  • Mollenhauer, H. H.: Plastic embedding mixtures for use in electron microscopy. Stain Technol. 39, 111–114 (1964).

    Google Scholar 

  • Mühlethaler, K.: Ultrastructure and formation of plant cell walls. Ann. Rev. Plant Physiol. 18, 1–24 (1967).

    Google Scholar 

  • Northcote, D. H., Goulding, K. J., Horne, R. W.: The chemical composition and structure of the cell wall of Chlorella pyrenoidosa. Biochem. J. 70, 391–397 (1958).

    Google Scholar 

  • O'Brien, T.P.: Further observations on hydrolysis of the cell wall in the xylem. Protoplasma (Wien) 69, 1–14 (1970).

    Google Scholar 

  • Parke, M., Manton, I.: Preliminary observations on the fine structure of Prasinocladus marinus. J. marine biol. Ass. 45, 525–536 (1965).

    Google Scholar 

  • Pearsall, W. H., Loose, L.: The growth of Chlorella vulgaris in pure culture. Proc. roy. Soc. B 121, 451–501 (1937).

    Google Scholar 

  • Pickett-Heaps, J. D.: Some ultrastructural features of Volvox, with particular reference to the phenomenon of inversion. Planta (Berl.) 90, 174–190 (1970a).

    Google Scholar 

  • Pickett-Heaps, J. D.: Mitosis and autospore formation in the green alga Kirchneriella lunaris. Protoplasma (Wien) 70, 325–347 (1970b).

    Google Scholar 

  • Reynolds, E. S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963).

    Google Scholar 

  • Rodriguéz-López, M.: Morphological and structural changes produced in Chlorella pyrenoidosa by assimilable sugars. Arch. Mikrobiol. 52, 319–324 (1965).

    Google Scholar 

  • Rowley, J. R., Flynn, J. J.: Single-stage carbon replicas of microspores. Stain Technol. 41, 287–290 (1966).

    Google Scholar 

  • Rowley, J. R., Southworth, D.: Deposition of sporopollenin on lamellae of unit membrane dimensions. Nature (Lond.) 213, 703–704 (1967).

    Google Scholar 

  • Schnepf, E., Hegewald, E., Soeder, C. J.: Elektronenmikroskopische Beobachtungen an Parasiten aus Scenedesmus-Massenkulturen. 2.. Arch. Mikrobiol. 75, 209–229 (1971a).

    Google Scholar 

  • Schnepf, E., Deichgräber, G., Hegewald, E., Soeder, C.-J.: Elektronenmikroskopische Beobachtungen an Parasiten aus Scenedesmus-Massenkulturen. 3. Arch. Mikrobiol. 75, 230–245 (1971b)

    Google Scholar 

  • Schwimmer, D., Schwimmer, M.: Algae and medicine In: Algae and man (D. F. Jackson, ed.), p. 368–412. New York: Plenum Press 1964.

    Google Scholar 

  • Sharman, B. C.: Volvox colonies and snail cytase. Nature (Lond.) 186, 90 (1960).

    Google Scholar 

  • Shaw, G.: Sporopollenin. In: Phytochemical phylogeny (J. B. Harborne, ed.), p. 31–58. London: Acad. Press 1970.

    Google Scholar 

  • Shaw, G.: The chemistry of sporopollenin. In: Sporopollenin (J. Brooks, P. R. Grant, M. Muir, P. van Gjizel and G. Shaw, eds.), p. 305–350, London: Acad. Press 1971.

    Google Scholar 

  • Shaw, G., Yeadon, A.: Chemical studies on the constitution of some pollen and spore membranes. J. chem. Soc. (C) 16-22 (1966).

  • Soeder, C. J.: Elektronenmikroskopische Untersuchungen an ungeteilten Zellen von Chlorella fusca Shihira et Krauss. Arch. Mikrobiol. 47, 311–324 (1964).

    Google Scholar 

  • Soeder, C. J.: Elektronenmikroskopische Untersuchung der Protoplastenteilung bei Chlorella fusca Shihira et Krauss. Arch. Mikrobiol. 50, 368–377 (1965).

    Google Scholar 

  • Southworth, D.: Incorporation of radioactive precursors into developing pollen walls. In: Pollen: Development and physiology (J. Heslop-Harrison, ed.), p. 115–120. London: Butterworths 1971.

    Google Scholar 

  • Southworth, D., Branton, D.: Freeze-etched pollen walls of Artemisia pycnocephala and Lilium humboldtii. J. Cell Sci. 9, 193–207 (1971).

    Google Scholar 

  • Spurr, A. J.: A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26, 31–49 (1969).

    Google Scholar 

  • Staehelin, A.: Die Ultrastruktur der Zellwand und des Chloroplasten von Chlorella. Z. Zellforsch. 74, 325–350 (1966).

    Google Scholar 

  • Sutton, J. S.: Potassium permanganate staining of ultra-thin sections for electron microscopy. J. Ultrastruct. Res. 21, 424–429 (1968).

    Google Scholar 

  • Swift, E., Remsen, C. C.: The cell wall of Pyrocystis spp. (Dinococcales). J. Phycol. 6, 79–86 (1970).

    Google Scholar 

  • Syrett, P. J.: The kinetics of isocitrate lyase formation in Chlorella: evidence for the promotion of enzyme synthesis by photophosphorylation. J. exp. Bot. 53, 641–654 (1966).

    Google Scholar 

  • Syrett, P. J., Bocks, S. M., Merrett, M. J.: The assimilation of acetate by Chlorella vulgaris. J. exp. Bot. 15, 35–47 (1964).

    Google Scholar 

  • Wanka, F.: Ultrastructural changes during normal and colchicine-inhibited cell division of Chlorella. Protoplasma (Wien) 66, 105–130 (1968).

    Google Scholar 

  • Waterkeyn, L., Bienfait, A.: Primuline induced fluorescence of the first exine elements and Ubisch bodies in Ipomoea and Lilium. In: Sporopollenin (J. Brooks, P. R. Grant, M. Muir, P. van Gijzel and G. Shaw, eds.), p. 108–129. London: Acad. Press 1971.

    Google Scholar 

  • Zetsche, F., Vicari, H.: Untersuchungen über die Membran der Sporen und Pollen II. Lycopodium clavatum L. 2. Helv. chim. Acta 14, 58–62 (1931a).

    Google Scholar 

  • Zetsche, F., Vicari, H.: Untersuchungen über die Membran der Sporen und Pollen. III. 2. Picea orientalis, Pinus sylvestris L., Corylus avellana L. Helv. chim. Acta 14, 62–67 (1931b).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Atkinson, A.W., Gunning, B.E.S. & John, P.C.L. Sporopollenin in the cell wall of Chlorella and other algae: Ultrastructure, chemistry, and incorporation of 14C-acetate, studied in synchronous cultures. Planta 107, 1–32 (1972). https://doi.org/10.1007/BF00398011

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00398011

Keywords

Navigation