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In vitro culturing and resynthesis of the mycobiont Protoparmeliopsis muralis with algal bionts

Published online by Cambridge University Press:  08 January 2013

Beata GUZOW-KRZEMIŃSKA  and
Elfie STOCKER-WÖRGÖTTER
Beata GUZOW-KRZEMIŃSKA
Affiliation:
Department of Molecular Biology, University of Gdańsk, Wita Stwosza 59, 80-308 Gdańsk, Poland. Email: beatagk@biotech.ug.gda.pl Department of Organismic Biology, University of Salzburg, Hellbrunner Str. 34, 5020 Salzburg, Austria
Elfie STOCKER-WÖRGÖTTER
Affiliation:
Department of Organismic Biology, University of Salzburg, Hellbrunner Str. 34, 5020 Salzburg, Austria
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Abstract

The widespread and ubiquitous lichen-forming fungus Protoparmeliopsis muralis is able to form a thallus with Trebouxia species. In this study, several photobiont strains were isolated from different specimens of P. muralis and cultured in vitro. The compatibility of Trebouxia spp. and Asterochloris algae with P. muralis were investigated in in vitro resynthesis experiments and the re-lichenized bionts were observed with the scanning electron microscope. It was found that, in addition to compatible photobionts, also a presumably incompatible Asterochloris sp. was able to interact with the mycobiont. The life strategy that enables the mycobiont to form associations with a wider range of photobionts could be advantageous for the survival of the lichen and successful colonization of new habitats.

Keywords

compatibility of biontsITS rDNA sequencinglichenphotobiontscanning electron microscopy
Type
Articles
Information
The Lichenologist , Volume 45 , Issue 1 , January 2013 , pp. 65 - 76
Copyright
Copyright © British Lichen Society 2013

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References

Ahmadjian, V. (1988) The lichen alga Trebouxia: does it occur free-living? Plant Systematics and Evolution 158: 243–247.CrossRefGoogle Scholar
Ahmadjian, V. (1993) The Lichen Symbiosis. New York: John Wiley & Sons.Google Scholar
Ahmadjian, V., Jacobs, J. B. & Russell, L. A. (1978) Scanning electron microscope study of early lichen synthesis. Science 200: 1062–1064.CrossRefGoogle ScholarPubMed
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. (1990) Basic local alignment search tool. Journal of Molecular Biology 215: 403–410.CrossRefGoogle ScholarPubMed
Armaleo, D. & Clerc, P. (1995) A rapid and inexpensive method for the purification of DNA from lichens and their symbionts. Lichenologist 27: 207–213.CrossRefGoogle Scholar
Beck, A. & Koop, H.-U. (2001) Analysis of the photobiont population in lichens using a single-cell manipulator. Symbiosis 31: 57–67.Google Scholar
Beck, A., Friedl, T. & Rambold, G. (1998) Selectivity of photobiont choice in a defined lichen community: inferences from cultural and molecular studies. New Phytologist 139: 709–720.CrossRefGoogle Scholar
Beck, A., Kasalicky, T. & Rambold, G. (2002) Myco-photobiontal selection in a Mediterranean cryptogam community with Fulgensia fulgida . New Phytologist 153: 317–326.CrossRefGoogle Scholar
Bischoff, H. W. & Bold, H. C. (1963) Phycological Studies IV. Some soil algae from enchanted rock and related algal species. University of Texas Publication 6318: 1–95.Google Scholar
Blaha, J., Baloch, E. & Grube, M. (2006) High photobiont diversity associated with the euryoecious lichen-forming ascomycete Lecanora rupicola (Lecanoraceae, Ascomycota). Biological Journal of Linnean Society 88: 283–293.CrossRefGoogle Scholar
Brunauer, G., Hager, A., Grube, M., Türk, R. & Stocker-Wörgötter, E. (2007) Alterations in secondary metabolism of aposymbiotically grown mycobionts of Xanthoria elegans and cultured resynthesis stages. Plant Physiology and Biochemistry 45: 146–151.CrossRefGoogle ScholarPubMed
Bubrick, P. & Galun, M. (1986) Spore to spore resynthesis of Xanthoria parietina . Lichenologist 18: 47–49.CrossRefGoogle Scholar
Bubrick, P., Galun, M. & Frensdorff, A. (1984) Observations on free-living Trebouxia de Puymaly and Pseudotrebouxia Archibald, and evidence that both symbionts from Xanthoria parietina (L.) Th. Fr. can be found free-living in nature. New Phytologist 97: 455–462.CrossRefGoogle Scholar
Deason, T. R. & Bold, H. C. (1960) Phycological studies. I. Exploratory studies of Texas soil algae. University of Texas Publication 6022: 1–72.Google Scholar
Ettl, H. & Gärtner, G. (1995) Syllabus der Boden-, Luft- und Flechtenalgen. Stuttgart: Gustav Fischer.Google Scholar
Friedl, T. (1989) Comparative ultrastructure of pyrenoids in Trebouxia (Microthamniales, Chlorophyta). Plant Systematics and Evolution 164: 145–159.Google Scholar
Friedl, T. & Büdel, B. (1996) Photobionts. In Lichen Biology (Nash, T. H. III, ed.): 8–23. Cambridge: Cambridge University Press.Google Scholar
Friedl, T. & Rokitta, C. (1997) Species relationships in the lichen alga Trebouxia (Chlorophyta, Trebouxiophyceae): molecular phylogenetic analyses of nuclear-encoded large subunit rRNA gene sequences. Symbiosis 23: 125–148.Google Scholar
Galun, M. (1988) Lichenization. In CRC Handbook of Lichenology, vol. II. (Galun, M., ed.): 153–169. Boca Raton: CRC Press.Google Scholar
Galun, M. & Bubrick, P. (1984) Physiological interactions between the partners of the lichen symbiosis. In Encyclopedia of Plant Physiology. Cellular Interactions. (Linskens, H. F. & Heslop-Harrison, J., eds): 362–401. Berlin: Springer.CrossRefGoogle Scholar
Gardes, M. & Bruns, T. D. (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113–118.CrossRefGoogle Scholar
Guzow-Krzemińska, B. (2006) Photobiont flexibility in the lichen Protoparmeliopsis muralis as revealed by ITS rDNA analyses. Lichenologist 38: 469–476.CrossRefGoogle Scholar
Hauck, M., Helms, G. & Friedl, T. (2007) Photobiont selectivity in the epiphytic lichens Hypogymnia physodes and Lecanora conizaeoides . Lichenologist 39: 195–204.CrossRefGoogle Scholar
Helms, G., Friedl, T., Rambold, G. & Mayrhofer, H. (2001) Identification of photobionts from the lichen family Physciaceae using algal-specific ITS rDNA sequencing. Lichenologist 33: 73–86.CrossRefGoogle Scholar
Honegger, R. (1996) Morphogenesis. In Lichen Biology (Nash, T. H. III, ed.): 65–87. Cambridge: Cambridge University Press.Google Scholar
Honegger, R. (2008) Morphogenesis. In Lichen Biology, 2nd edition. (Nash, T. H. III, ed.): 69–93. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Honegger, R. (2009) Lichen-forming fungi and their photobionts. In Plant Relationships. The Mycota V, 2nd Edition (Deising, H., ed.): 307–333. Berlin, Heidelberg: Springer-Verlag.Google Scholar
Joneson, S. & Lutzoni, F. (2009) Compatibility and thigmotropism in the lichen symbiosis: a reappraisal. Symbiosis 47: 109–115.CrossRefGoogle Scholar
Joneson, S., Armaleo, D. & Lutzoni, F. (2011) Fungal and algal gene expression in early developmental stages of lichen-symbiosis. Mycologia 103: 291–306.CrossRefGoogle ScholarPubMed
Laundon, J. R. (2010) Lecanora antiqua, a new saxicolous lichen from Great Britain, and the nomenclature and authorship of L. albescens, L. conferta and L. muralis . Lichenologist 42: 631–636.CrossRefGoogle Scholar
Meessen, J. & Ott, S. (2010) Identification of six up-regulated mycobiont genes by initial biont interaction studies of the lichen Fulgensia bracteata . In Abstracts of the 9th International Mycological Congress: The Biology of Fungi, 1–6 August, 2010, Edinburgh, Scotland, p 1.161.Google Scholar
Muggia, L., Grube, M. & Tretiach, M. (2008) Genetic diversity and photobiont associations in selected taxa of the Tephromela atra group (Lecanorales, lichenized Ascomycota). Mycological Progress 7: 147–160.CrossRefGoogle Scholar
Mukhtar, A., Garty, J. & Galun, M. (1994) Does the lichen alga Trebouxia occur free-living in nature: further immunological evidence. Symbiosis 17: 247–253.Google Scholar
Ohmura, Y., Kawachi, M., Kasaie, F., Watanabe, M. M. & Takeshita, S. (2006) Genetic combinations of symbionts in a vegetatively reproducing lichen, Parmotrema tinctorum, based on ITS rDNA sequences. Bryologist 109: 43–59.CrossRefGoogle Scholar
Ott, S. (1987) The juvenile development of lichen thalli from vegetative diaspores. Symbiosis 3: 57–74.Google Scholar
Pérez-Ortega, S., Spribille, T., Palice, Z., Elix, J. A. & Printzen, C. (2010) A molecular phylogeny of the Lecanora varia group, including a new species from western North America. Mycological Progress 9: 523–535.CrossRefGoogle Scholar
Piercey-Normore, M. D. (2006) The lichen-forming ascomycete Evernia mesomorpha associates with multiple genotypes of Trebouxia jamesii . New Phytologist 169: 331–344.CrossRefGoogle ScholarPubMed
Piercey-Normore, M. D. & DePriest, P. T. (2001) Algal switching among lichen symbioses. American Journal of Botany 88: 1490–1498.CrossRefGoogle ScholarPubMed
Romeike, J., Friedl, T., Helms, G. & Ott, S. (2002) Genetic diversity of algal and fungal partners in four species of Umbilicaria (lichenized Ascomycetes) along a transect of the Antarctic Peninsula. Molecular Biology and Evolution 19: 1209–1217.CrossRefGoogle ScholarPubMed
Sanders, W. (2005) Observing microscopic phases of lichen life cycles on transparent substrata placed in situ . Lichenologist 37: 373–382.CrossRefGoogle Scholar
Sanders, W. B. & Lücking, R. (2002) Reproductive strategies, relichenization and thallus development observed in situ in leaf-dwelling lichen communities. New Phytologist 155: 425–435.CrossRefGoogle ScholarPubMed
Schaper, T. & Ott, S. (2003) Photobiont selectivity and interspecific interactions in lichen communities. I. Culture experiments with the mycobiont Fulgensia bracteata . Plant Biology 5: 441–450.CrossRefGoogle Scholar
Skaloud, P. & Peksa, O. (2010) Evolutionary inferences based on ITS rDNA and actin sequences reveal extensive diversity of the common lichen alga Asterochloris (Trebouxiophyceae, Chlorophyta). Molecular Phylogenetics and Evolution 54: 36–46.CrossRefGoogle ScholarPubMed
Smith, D. C. & Douglas, A. E. (1987). The Biology of Symbiosis. London: Edward Arnold.Google Scholar
Stenroos, S., Stocker-Wörgötter, E., Yoshimura, I., Myllys, L., Thell, A. & Hyvönen, J. (2003) Culture experiments and DNA sequence data confirm the identity of Lobaria photomorphs. Canadian Journal of Botany 81: 232–247.CrossRefGoogle Scholar
Stocker-Wörgötter, E. (2001 a) Experimental lichenology and microbiology of lichens: culture experiments, secondary chemistry of cultured mycobionts, resynthesis and thallus morphogenesis. Bryologist 104: 576–581.CrossRefGoogle Scholar
Stocker-Wörgötter, E. (2001 b) Experimental studies of the lichen symbiosis: DNA-analyses, differentiation and secondary chemistry of selected mycobionts, artificial resynthesis of two- and tripartite symbioses. Symbiosis 30: 207–227.Google Scholar
Stocker-Wörgötter, E. (2002) Resynthesis of photosymbiodemes. In Protocols in Lichenology – Culturing, Biochemistry, Ecophysiology and Use in Biomonitoring (Kranner, I., Beckett, R. P., Varma, A., eds): 47–60. Berlin, Heidelberg: Springer-Verlag.Google Scholar
Stocker-Wörgötter, E. (2010) Stress and developmental strategies in lichens. Symbioses and Stress: Joint Ventures in Biology, Cellular Origin, Life in Extreme Habitats and Astrobiology 17: 525–546.CrossRefGoogle Scholar
Stocker-Wörgötter, E. & Elix, J. (2006) Morphogenetic strategies and induction of secondary metabolite biosynthesis in cultured lichen-forming Ascomycota, as exemplified by Cladia retipora (Labill.) Nyl. and Dactylina arctica (Richards) Nyl. Symbiosis 41: 9–20.Google Scholar
Stocker-Wörgötter, E. & Türk, R. (1991) Artificial resynthesis of thalli of the cyanobacterial lichen Peltigera praetextata under laboratory conditions. Lichenologist 23: 127–138.CrossRefGoogle Scholar
Stocker-Wörgötter, E. & Türk, R. (1993) Redifferentiation of the lichen Cladonia furcata ssp. furcata from cultivated lichen tissue. Cryptogamic Botany 3: 283–289.Google Scholar
Tschermak-Woess, E. (1978) Myrmecia reticulate as a phycobiont and free-living Trebouxia – the problem of Stenocybe septata . Lichenologist 10: 69–79.CrossRefGoogle Scholar
White, T. J., Bruns, T., Lee, S. & Taylor, J. W. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols: A Guide to Methods and Applications (Innis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T. J., eds): 315–322. New York: Academic Press.Google Scholar
Wornik, S. & Grube, M. (2010) Joint dispersal does not imply maintenance of partnership in lichen symbioses. Microbial Ecology 59: 150–157.CrossRefGoogle Scholar
Yahr, R., Vilgalys, R. & DePriest, P. T. (2006) Geographic variation in algal partners in Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytologist 171: 847–860.CrossRefGoogle ScholarPubMed
Yamamoto, Y. (1990) Studies of Cell Aggregates and the Production of Natural Pigments in Plant Cell Culture. Neyagawa: Nippon Paint Public.Google Scholar