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Comparative ultrastructure of pyrenoids inTrebouxia (Microthamniales, Chlorophyta)

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Pyrenoid ultrastructure has been investigated from cultures of all 26 species ofTrebouxia with the aim of establishing pyrenoids as a taxonomic character. Different arrangements and forms of thylakoid lamellae within the pyrenoid matrix allow eight pyrenoid types to be distinguished. Each type is characteristic of a group of species. Thegigantea- andimpressa-type are similar, differing only in the form of the tubules: short, branched tubules mark thegigantea-type; ± long and straight invaginations theimpressa-type. Thearboricola-type is characterized by meandering pyrenoid membranes developing from lamellae parallel with each other in young autospores. Pyrenoids of thegelatinosa-type are traversed by thin parallel-arranged tubules. Few thylakoids with a curved profile are typical of theirregularis-type. Thecorticola-type is different from all others in having a distinct starch sheath closely connected with the pyrenoid matrix and no pyrenoglobuli being associated with the pyrenoid membranes. No true pyrenoids have been found inT. magna andT. erici. Within the chloroplast, they have indistinct areas with pyrenoglobuli, but without differentiated thylakoids. Pyrenoid morphology is stable in culture on different media as well as in phycobionts within lichen thalli. Comparing the pyrenoid of a lichenizedTrebouxia with that from cultured species, the identification of the phycobiont within the lichen thallus is possible, without the need of culturing the algae. This has been shown in species ofParmelia andHypogymnia. New aspects for the taxonomy and systematics ofTrebouxia are discussed.

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  1. Ahmadjian, V., 1967: A guide to the algae occurring as lichen symbionts. Isolation, culture, cultural physiology and identification. — Phycologia6: 129–160.

  2. —, 1988: The lichen algaTrebouxia: does it occur free-living? — Pl. Syst. Evol.158: 243–247.

  3. Archibald, P., 1975:Trebouxia De Puymaly (Chlorophyceae, Chlorococcales) andPseudotrebouxia gen. nov. (Chlorophyceae, Chlorosarcinales). — Phycologia14: 125–137.

  4. Ascaso, C., Brown, D. H., Rapsch, S., 1988: The effect of desiccation on pyrenoid structure in the oceanic lichenParmelia laevigata. — Lichenologist20: 31–39.

  5. Berger-Perrot, Y., Thomas, J. C., 1982: Étude ultrastructurale comparée du pyrénoide et des parois dans les genresUlothrix, Chlorothrix etUrospora. — Phycologia21: 355–369.

  6. Bischoff, H. W., Bold, H. C., 1963: Phycological studies 4. Some soil algae from Enchanted Rock and related algal species. — Univ. Texas Publ.6318: 1–95.

  7. Brown, D. H., Ascaso, C., Rapsch, S., 1987: Ultrastructural changes in the pyrenoid of the lichenParmelia sulcata stored under controlled conditions. — Protoplasma136: 136–144.

  8. Brown, R. M., Wilson, R., 1968: Electron microscopy of the lichenPhyscia aipolia (Ehrh.)Nyl. — J. Phycol4: 230–240.

  9. Büdel, B., Rhiel, E., 1987: Studies on the ultrastructure of some cyanolichen haustoria. — Protoplasma139: 145–152.

  10. Ettl, H., 1980: Grundriß der allgemeinen Algologie. — Jena: G. Fischer.

  11. —, 1988: Zellteilung und Sporulation als wichtige Unterscheidungsmerkmale bei Grünalgen (Chlorophyta). — Arch. Protistenk:135: 103–118.

  12. —, 1984: Über die Bedeutung der Cytologie für die Algentaxonomie, dargestellt anTrebouxia (Chlorellales, Chlorophyceae). — Pl. Syst. Evol.148: 135–147.

  13. Fiechter, E., Honegger, R., 1988: Seasonal variations in the fine structure ofHypogymnia physodes (lichenizedAscomycetes) and itsTrebouxia photobiont. — Pl. Syst. Evol.158: 249–263.

  14. Fisher, K. A., Lang, N. J., 1971a: Ultrastructure of the pyrenoid ofTrebouxia inRamalina menziesii Tuck. — J. Phycol.7: 25–37.

  15. —, 1971b: Comparative ultrastructure of cultured species ofTrebouxia. — J. Phycol.7: 155–165.

  16. Friedl, T., 1987: Thallus development and phycobionts of the parasitic lichenDiploschistes muscorum. — Lichenologist19: 183–191.

  17. —, 1988:Trebouxia (Pleurastrales, Chlorophyta) as a phycobiont in the lichen genusDiploschistes. — Arch. Protistenk.135: 147–158.

  18. Fujita, M., 1968: Fine structure of lichens. — Misc. Bryol. Lichenol.4: 157–160.

  19. Galun, M., Paran, M., Ben-Shaul, Y., 1970: Structural modifications of the phycobiont in the lichen thallus. — Protoplasma69: 85–96.

  20. Gärtner, G., 1985a: Die GattungTrebouxia Puymaly (Chlorellales, Chlorophyceae). — Arch. Hydrobiol., Suppl.71, Algol. Stud.41: 495–548.

  21. —, 1985b: The culture collection of algae at the Botanical Institute of the University of Innsbruck (Austria). — Ber. nat. med. Ver. Innsbruck72: 33–52.

  22. Geitler, L., 1926: Zur Morphologie und Entwicklungsgeschichte der Pyrenoide. — Arch. Protistenk.56: 128–144.

  23. Griffiths, D. J., 1980: The pyrenoid and its role in algal metabolism. — Sci. Prog. Oxf.66: 537–553.

  24. Hayes, W. C., Wujek, D. E., 1974: Ultrastructure of the lichenXanthoria fallax. — Trans. Kansas Acad. Sci.76: 234–243.

  25. Holopainen, T., 1982: Summer versus winter condition of the ultrastructure of the epiphytic lichensBryoria capillaris andHypogymnia physodes in central Finland. — Ann. Bot. Fennici19: 39–52.

  26. Jacobs, J. B., Ahmadjian, V., 1969: The ultrastructure of lichens. 1. A general survey. — J. Phycol.5: 227–240.

  27. —, 1971: The ultrastructure of lichens. 2.Cladonia cristatella: the lichen and its isolated symbionts. — J. Phycol.7: 71–81.

  28. Kattner, E., Lorch, D., Weber, A., 1977: Die Bausteine der Zellwand und der Gallerte eines Stammes vonNetrium digitus (Ehrbg.)Itzigs. & Rothe. — Mitt. Inst. Allg. Bot. Hamburg15: 33–39.

  29. Kies, L., 1967: Über die Zellteilung und Zygotenbildung beiRoya obtusa (Breb.)West & West. — Mitt. Staatsinst. Allg. Bot. Hamburg12: 35–42.

  30. Komárek, J., 1987: Species concept in coccal green algae. — Arch. Hydrobiol.73 (4), Algol. Stud.45: 437–471.

  31. Lawrey, J. D., 1984: Biology of lichenized fungi. — New York: Praeger.

  32. Mattox, K. R., Stewart, K. D., 1984: Classification of the green algae: a concept based on comparative cytology. — InIrvine, D. E. G., John, D. M., (Eds.): Systematics of green algae, pp. 29–72. — London, Orlando: Academic Press.

  33. McFadden, G. I., Melkonian, M., 1986: Use of HEPES buffer for microalgal cutlure media and fixation for electron microscopy. — Phycologia25: 551–557.

  34. Melkonian, M., 1981: Fate of eyespot lipid globules after zoospore settlement in the green algaPleurastrum terrestre Fritsch & John. — Brit. Phycol. J.16: 247–255.

  35. —, 1982: Two different types of motile cells within theChlorococcales and theChlorosarcinales: taxonomic implications. — Brit. Phycol. J.17: 236.

  36. —, 1983: Zoospore ultrastructure in the green algaFriedmannia israeliensis: an absolute configuration analysis. — Protoplasma114: 67–84.

  37. —, 1988: Zoospore ultrastructure in species ofTrebouxia andPseudotrebouxia (Chlorophyta). — Pl. Syst. Evol.158: 183–210.

  38. Molnar, K. E., Stewart, K. D., Mattox, K. R., 1975: Cell division in the filamentousPleurastrum and its comparision with the unicellularPlatymonas (Chlorophyceae). — J. Phycol.11: 287–296.

  39. Peveling, E., 1968: Pyrenoidstrukturen in symbiontisch lebendenTrebouxia-Arten. — Z. Pflanzenphysiol.59: 393–396.

  40. —, 1969: Elektronenoptische Untersuchungen an Flechten. 2. Die Feinstrukitur vonTrebouxia-Phycobionten. — Planta87: 69–85.

  41. —, 1970: Das Vorkommen von Stärke inChlorophyceen-Phycobionten. — Planta93: 82–85.

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

  43. Sluiman, H. J., Lokhorst, G. M., 1988: The ultrastructure of ceilular division (auto-sporogenesis) in the coccoid green alga,Trebouxia aggregata, revealed by rapid freeze fixation and freeze substitution. — Protoplasma144: 149–159.

  44. Spurr, A. R., 1969: A low viscosity epoxy resin embedding medium for electron microscopy. — J. Ultrastruct. Res.26: 31–43.

  45. Tschermak-Woess, E., 1978: Über die Phycobionten der SektionCystophora vonChaenotheca, insbesondereDictyochloropsis splendida undTrebouxia simplex, spec. nova. — Pl. Syst. Evol.129: 185–208.

  46. Warén, H., 1920 (1918–1919): Reinkulturen von Flechtengonidien. — Finska Vet. Soc. Förh.61: 1–79.

  47. Watson, M. L., 1958: Staining of tissue sections for electron microscopy with heavy metals. — J. Biophys. Biochem. Cytol.4: 475–478.

  48. Wujek, D., 1975: Some ultrastructural aspects of the pyrenoid of the chaetophoracean algaPleurastrum. — Trans. Kansas Acad. Sci.3–4: 133–137.

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Dedicated to Prof. DrLothar Geitler on the occasion of the 90th anniversary of his birthday.

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Friedl, T. Comparative ultrastructure of pyrenoids inTrebouxia (Microthamniales, Chlorophyta). Plant Syst Evol 164, 145–159 (1989). https://doi.org/10.1007/BF00940435

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Key words

  • Algae
  • Chlorophyta
  • Trebouxia
  • Pseudotrebouxia
  • lichens
  • Parmelia
  • Hypogymnia
  • Pyrenoid
  • ultrastructure
  • systematics
  • taxonomy
  • phycobionts
  • freeze fixation
  • freeze substitution