Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-24T14:52:42.711Z Has data issue: false hasContentIssue false
  • English
  • Français

Green-algal photobiont diversity (Trebouxia spp.) in representatives of Teloschistaceae (Lecanoromycetes, lichen-forming ascomycetes)

Published online by Cambridge University Press:  11 February 2014

Shyam NYATI ,
Sandra SCHERRER ,
Silke WERTH  and
Rosmarie HONEGGER
Shyam NYATI
Affiliation:
Institute of Plant Biology, University of Zürich, Zollikerstrasse 107, CH-8008, Zürich, Switzerland. Email: [email protected] Department of Radiation Oncology, University of Michigan, 109 Zina Pitcher Place, Ann Arbor, Michigan 48109, USA
Sandra SCHERRER
Affiliation:
Institute of Plant Biology, University of Zürich, Zollikerstrasse 107, CH-8008, Zürich, Switzerland. Email: [email protected] Natural History Museum Winterthur, 8402 Winterthur, Switzerland
Silke WERTH
Affiliation:
Faculty of Life- and Environmental Sciences, University of Iceland, Sturlugata 7, 101 Reykjavik, Iceland
Rosmarie HONEGGER*
Affiliation:
Institute of Plant Biology, University of Zürich, Zollikerstrasse 107, CH-8008, Zürich, Switzerland. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The green algal photobionts of 12 Xanthoria, seven Xanthomendoza, two Teloschistes species and Josefpoeltia parva (all Teloschistaceae) were analyzed. Xanthoria parietina was sampled on four continents. More than 300 photobiont isolates were brought into sterile culture. The nuclear ribosomal internal transcribed spacer region (nrITS; 101 sequences) and the large subunit of the RuBiSco gene (rbcL; 54 sequences) of either whole lichen DNA or photobiont isolates were phylogenetically analyzed. ITS and rbcL phylogenies were congruent, although some subclades had low bootstrap support. Trebouxia arboricola,T. decolorans and closely related, unnamed Trebouxia species, all belonging to clade A, were found as photobionts of Xanthoria species. Xanthomendoza species associated with either T. decolorans (clade A), T. impressa, T. gelatinosa (clade I) or with an unnamed Trebouxia species. Trebouxia gelatinosa genotypes (clade I) were the photobionts of Teloschistes chrysophthalmus,T. hosseusianus and Josefpoeltia parva. Only weak correlations between distribution patterns of algal genotypes and environmental conditions or geographical location were observed.

Keywords

AsterochlorisJosefpoeltia parvanrITSrbcLTeloschistesXanthomendozaXanthoria
Type
Articles
Information
The Lichenologist , Volume 46 , Issue 2 , March 2014 , pp. 189 - 212
Copyright
Copyright © British Lichen Society 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmadjian, V. (1958) A guide for the identification of algae occurring as lichen symbionts. Botaniska Notiser 111: 632–644.Google Scholar
Ahmadjian, V. (1960) Some new and interesting species of Trebouxia, a genus of lichenized algae. American Journal of Botany 47: 677–683.CrossRefGoogle Scholar
Ahmadjian, V. (1967) A guide to the algae occurring as lichen symbionts: isolation, culture, cultural physiology, and identification. Phycologia 6: 127–160.Google Scholar
Ahmadjian, V. (1988) The lichen alga Trebouxia: does it occur free-living? Plant Systematics and Evolution 158: 243–247.Google Scholar
Ahmadjian, V. (2002 a) Lingering lichen myths are hard to dispel. International Symbiosis Society Newsletter 2: 1–2.Google Scholar
Ahmadjian, V. (2002 b) Trebouxia: reflections on a perplexing and controversial lichen photobiont. In Symbiosis: Mechanisms and Model Systems (Seckbach, J., ed.): 373–383. Dordrecht, Netherlands: Kluwer Academic Publishers.Google Scholar
Altermann, S. (2009) Geographic structure in a symbiotic mutualism. Ph.D. thesis, University of California at Santa Cruz.Google Scholar
Aoki, M., Nakano, T., Kanda, H. & Deguchi, H. (1998) Photobionts isolated from Antarctic lichens. Journal of Marine Biotechnology 6: 39–43.Google Scholar
Archibald, P. A. (1975) Trebouxia de Puymaly (Chlorophyceae, Chlorococcales) and Pseudotrebouxia gen. nov. (Chlorophyceae, Chlorosarcinales). Phycologia 14: 125–137.CrossRefGoogle Scholar
Ascaso, C., Valladares, F. & De Los Rios, A. (1995) New ultrastructural aspects of pyrenoids of the lichen photobiont Trebouxia (Microthamniales, Chlorophyta). Journal of Phycology 31: 114–119.Google Scholar
Beck, A. (2002) Selektivität der Symbionten schwermetalltoleranter Flechten. D.Phil thesis, Ludwig-Maximilians-Universität München.Google Scholar
Beck, A. & Peršoh, D. (2009) Flechten und ihre Stellung im Reich der Pilze. Rundgespräche der Kommission für Ökologie. Ökologische Rolle der Flechten 36: 13–24.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.Google 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
Bhattacharya, D., Friedl, T. & Damberger, S. (1996) Nuclear-encoded rDNA group I introns: origin and phylogenetic relationships of insertion site lineages in the green algae. Molecular Biology and Evolution 13: 978–989.CrossRefGoogle Scholar
Bhattacharya, D., Friedl, T. & Helms, G. (2002) Vertical evolution and intragenic spread of lichen-fungal group I introns. Journal of Molecular Evolution 55: 74–84.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 the Linnean Society 88: 283–293.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 parientina (L.) Th. Fr. can be found free-living in nature. New Phytologist 97: 455–462.Google Scholar
Dahlkild, A., Kallersjo, M., Lohtander, K. & Tehler, A. (2001) Photobiont diversity in the Physciaceae (Lecanorales). Bryologist 104: 527–536.Google Scholar
Dal Grande, F., Widmer, I., Wagner, H. H. & Scheidegger, C. (2012) Vertical and horizontal photobiont transmission within populations of a lichen symbiosis. Molecular Ecology 21: 3159–3172.Google Scholar
Deason, T. R. & Bold, H. C. (1960) Phycological Studies: Exploratory Studies of Texas Soil Algae. Austin: University of Texas.Google Scholar
Domaschke, S., Fernandez-Mendoza, F., Garcia, M. A., Martin, M. P. & Printzen, C. (2012) Low genetic diversity in Antarctic populations of the lichen-forming ascomycete Cetraria aculeata and its photobiont. Polar Research 31: doi: 10.3402/polar.v31i0.17353.Google Scholar
Eichenberger, C. (2007) Molecular phylogenies of representatives of Xanthoria and Xanthomendoza (lichen-forming Ascomycetes) . Ph.D. thesis, University of Zürich.Google Scholar
Ettl, H. & Gärtner, G. (1995) Syllabus der Boden-, Luft-und Flechtenalgen. Stuttgart: Gustav Fischer.Google Scholar
Francisco De Oliveira, P. M. F., Timsina, B. & Piercey-Normore, M. D. (2012) Diversity of Ramalina sinensis and its photobiont in local populations. Lichenologist 44: 649–660.Google Scholar
Friedl, T. (1987) Thallus development and phycobionts of the parasitic lichen Diploschistes muscorum . Lichenologist 19: 183–191.Google Scholar
Friedl, T. (1989) Systematik und biologie von Trebouxia (Microthamniales, Chlorophyta) als phycobiont der Parmeliaceae (lichenisierte Ascomyceten). Ph.D. thesis, University of Bayreuth.Google Scholar
Friedl, T. (1995) Inferring taxonomic positions and testing genus level assignments in coccoid green lichen algae: a phylogenetic analysis of 18S ribosomal RNA sequences from Dictyochloropsis reticulata and from members of the genus Myrmecia (Chlorophyta, Trebouxiophyceae cl. nov.). Journal of Phycology 31: 632–639.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
Friedl, T., Besendahl, A., Pfeiffer, P. & Bhattacharya, D. (2000) The distribution of group I introns in lichen algae suggests that lichenization facilitates intron lateral transfer. Molecular Phylogenetics and Evolution 14: 342–352.CrossRefGoogle Scholar
Galloway, D. J. (1985) Flora of New Zealand: Lichens. Wellington, New Zealand: PD Hasselberg, Government Printer.Google Scholar
Gärtner, G. (1985 a) The culture collection of algae at the Botanical Institute of the University of Innsbruck (Austria). Berichte des Naturwissenschaftlich-medizinischen Vereins in Innsbruck 72: 33–52.Google Scholar
Gärtner, G. (1985 b) Die Gattung Trebouxia Puymaly (Chlorellales, Chlorophyceae). Archiv für Hydrobiologie—Supplement 71: 495–548.Google Scholar
Gärtner, G. (1985 c) Taxonomische Probleme bei den Flechtenalgengattungen Trebouxia und Pseudotrebouxia (Chlorophyceae, Chlorellales). Phyton (Austria) 25: 101–111.Google Scholar
Guzow-Krzeminska, B. (2006) Photobiont flexibility in the lichen Protoparmeliopsis muralis as revealed by ITS rDNA analyses. Lichenologist 38: 469–476.Google Scholar
Handa, S., Ohmura, Y., Nakano, T. & Nakahara-Tsubota, M. (2007) Airborne green microalgae (Chlorophyta) in snowfall. Hikobia 15: 109–120.Google Scholar
Hedenås, H., Blomberg, P. & Ericson, L. (2007) Significance of old aspen (Populus tremula) trees for the occurrence of lichen photobionts. Biological Conservation 135: 380–387.Google Scholar
Helms, G. (2003) Taxonomy and symbiosis in associations of Physciaceae and Trebouxia. Ph.D. thesis, Georg-August Universität Göttingen (unpublished, but accessible at: http://hdl.handle.net/11858/00-1735-0000-0006-AE69-7).Google 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.Google Scholar
Honegger, R. (1993) Developmental biology of lichens. New Phytologist 125: 659–677.Google Scholar
Honegger, R. (2003) The impact of different long-term storage conditions on the viability of lichen-forming ascomycetes and their green algal photobiont, Trebouxia spp. Plant Biology 5: 324–330.CrossRefGoogle Scholar
Honegger, R. (2004) Fine structure of the interaction of Leprocaulon microscopicum with its green algal photobiont, Dictyochloropsis symbiontica . Bibliotheca Lichenologica 88: 201–210.Google Scholar
Honegger, R. (2008) Morphogenesis. In Lichen Biology (Nash, T. H. III, ed.): 69–93. Cambridge: Cambridge University Press.Google Scholar
Honegger, R. & Peter, M. (1994) Routes of solute translocation and the location of water in heteromerous lichens visualized with cryotechniques in light and electron microscopy. Symbiosis 16: 167–186.Google Scholar
Honegger, R., Conconi, S. & Kutasi, V. (1996) Field studies on growth and regenerative capacity in the foliose macrolichen Xanthoria parietina (Teloschistales, Ascomycotina). Botanica Acta 109: 187–193.Google Scholar
Honegger, R., Zippler, U., Scherrer, S. & Dyer, P. S. (2004) Genetic diversity in Xanthoria parietina (L.) Th. Fr. (lichen-forming ascomycete) from worldwide locations. Lichenologist 36: 381–390.Google Scholar
Itten, B. & Honegger, R. (2010). Population genetics in the homothallic lichen-forming ascomycete Xanthoria parietina . Lichenologist 42: 751–761.CrossRefGoogle Scholar
John, D. M., Whitton, B. A. & Brook, A. J. (2002) The Freshwater Algal Flora of the British Isles: an Identification Guide to Freshwater and Terrestrial Algae. Cambridge: Cambridge University Press.Google Scholar
Kroken, S. & Taylor, J. W. (2000) Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia . Bryologist 103: 645–660.Google Scholar
Maddison, W. P. & Maddison, D. R. (2002) MacClade. Sunderland, Massachusetts: Sinauer Associates.Google Scholar
McCourt, R. M., Karol, K. G., Kaplan, S. & Hoshaw, R. W. (1995) Using rbcL sequences to test hypotheses of chloroplast and thallus evolution in conjugating green algae (Zygnematales, Charophyceae). Journal of Phycology 31: 989–995.Google Scholar
Muggia, L., Grube, M. & Tretiach, M. (2008) Genetic diversity and photobiont associations in selected taxa of the Tephromela atra group (Lecanorales, lichenised Ascomycota). Mycological Progress 7: 147–160.Google Scholar
Muggia, L., Zellnig, G., Rabensteiner, J. & Grube, M. (2010) Morphological and phylogenetic study of algal partners associated with the lichen-forming fungus Tephromela atra from the Mediterranean region. Symbiosis 51: 149–160.Google 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
Nozaki, H., Ito, M., Sano, R., Uchida, H., Watanabe, M. M., Takahashi, H. & Kuroiwa, T. (1997) Phylogenetic analysis of Yamagishiella and Platydorina (Volvocaceae, Chlorophyta) based on rbcL gene sequences. Journal of Phycology 33: 272–278.Google Scholar
Nozaki, H., Onishi, K. & Morita, E. (2002) Differences in pyrenoid morphology are correlated with differences in the rbcL genes of members of the Chloromonas lineage (Volvocales, Chlorophyceae). Journal of Molecular Evolution 55: 414–430.Google Scholar
Nyati, S., Werth, S. & Honegger, R. (2013 a) Genetic diversity of sterile cultured Trebouxia photobionts associated with the lichen-forming fungus Xanthoria parietina visualized with RAPD-PCR fingerprinting techniques. Lichenologist 45: 825–840.CrossRefGoogle Scholar
Nyati, S., Bhattacharya, D., Werth, S. & Honegger, R. (2013 b) Phylogenetic analysis of LSU and SSU rDNA group I introns of lichen photobionts associated with the genera Xanthoria and Xanthomendoza (Teloschistaceae, lichenized ascomycetes). Journal of Phycology (in press).Google Scholar
Ohmura, Y., Kawachi, M., Kasai, 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 a) Reproductive strategies in lichens. Bibliotheca Lichenologica 25: 81–93.Google Scholar
Ott, S. (1987 b) Sexual reproduction and developmental adaptations in Xanthoria parietina . Nordic Journal of Botany 7: 219–228.Google Scholar
Ott, S., Schröder, T. & Jahns, H. M. (2000) Colonization strategies and interactions of lichens on twigs. Bibliotheca Lichenologica 75: 445–455.Google Scholar
Peksa, O. & Skaloud, P. (2011) Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Molecular Ecology 20: 3936–3948.Google Scholar
Pérez-Ortega, S., Ortiz-Álvarez, R., Allan Green, T. G. & de los Ríos, A. (2012) Lichen myco- and photobiont diversity and their relationships at the edge of life (McMurdo Dry Valleys, Antarctica). FEMS Microbiology Ecology 82: 429–448.Google Scholar
Peršoh, D., Beck, A. & Rambold, G. (2004) The distribution of ascus types and photobiontal selection in Lecanoromycetes (Ascomycota) against the background of a revised SSU nrDNA phylogeny. Mycological Progress 3: 103–121.Google Scholar
Piercey-Normore, M. D. (2004) Selection of algal genotypes by three species of lichen fungi in the genus Cladonia . Canadian Journal of Botany 82: 947–961.Google Scholar
Piercey-Normore, M. D. (2006) The lichen-forming ascomycete Evernia mesomorpha associates with multiple genotypes of Trebouxia jamesii . New Phytologist 169: 331–344.Google Scholar
Piercey-Normore, M. D. & DePriest, P. T. (2001) Algal switching among lichen symbioses. American Journal of Botany 88: 1490–1498.Google Scholar
Rambold, G., Friedl, T. & Beck, A. (1998) Photobionts in lichens: possible indicators of phylogenetic relationships? Bryologist 101: 392–397.Google Scholar
Reis, R. A., Iacomini, M., Gorin, P. A. J., de Souza, L. M., Grube, M., Cordeiro, L. M. C. & Sassaki, G. L. (2005) Fatty acid composition of the tropical lichen Teloschistes flavicans and its cultivated symbionts. Fems Microbiology Letters 247: 1–6.CrossRefGoogle ScholarPubMed
Rindi, F. & Guiry, M. D. (2003) Composition and distribution of subaerial algal assemblages in Galway City, western Ireland. Cryptogamie Algologie 24: 245–267.Google Scholar
Rogers, R. W. (1992) Lichen ecology and biogeography. Flora of Australia 54: 30–42.Google Scholar
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.Google Scholar
Sanders, W. B. (2005) Observing microscopic phases of lichen life cycles on transparent substrata placed in situ . Lichenologist 37: 373–382.Google Scholar
Scherrer, S. & Honegger, R. (2003) Inter- and intraspecific variation of homologous hydrophobin (H1) gene sequences among Xanthoria spp. (lichen-forming ascomycetes). New Phytologist 158: 375–389.Google Scholar
Schroeter, B. & Sancho, L. G. (1996) Lichens growing on glass in Antarctica. Lichenologist 28: 385–390.Google Scholar
Sherwood, A. R., Garbary, D. J. & Sheath, R. G. (2000) Assessing the phylogenetic position of the Prasiolales (Chlorophyta) using rbcL and 18S rRNA gene sequence data. Phycologia 39: 139–146.CrossRefGoogle Scholar
Swofford, D. L. (1998) PAUP: Phylogenetic Analysis Using Parsimony (*and Other Methods), version 4. Sunderland, Massachusetts: Sinauer Associates.Google Scholar
Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596–1599.Google Scholar
Thomas, E. A. (1939) Über die Biologie von Flechtenbildnern. Beiträge zur Kryptogamenflora der Schweiz 9: 1–108.Google Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25: 4876–4882.Google Scholar
Tibell, L. (2001) Photobiont association and molecular phylogeny of the lichen genus Chaenotheca . Bryologist 104: 191–198.Google Scholar
Tibell, L. & Beck, A. (2002) Morphological variation, photobiont association and ITS phylogeny of Chaenotheca phaeocephala and C. subroscida (Coniocybaceae, lichenized ascomycetes). Nordic Journal of Botany 21: 651–660.Google Scholar
Tomaselli, R. (1956) Primi dati su ecotipi italiani di Cystococcus Xanthoriae parietinae . Aarchivo Botanico e Biogeografico Italiano 32: 1–8.Google Scholar
Tschermak-Woess, E. (1978) Myrmecia reticulata as a phycobiont and free-living Trebouxia—the problem of Stenocybe septata . Lichenologist 10: 69–79.Google Scholar
Tschermak-Woess, E. (1988) The algal partner. In Handbook of Lichenology (Galun, M., ed.): 39–92. Boca Raton, Florida: CRC Press.Google Scholar
Vargas Castillo, R. & Beck, A. (2012) Photobiont selectivity and specificity in Caloplaca species in a fog-induced community in the Atacama Desert, northern Chile. Fungal Biology 116: 665–676.Google Scholar
Werner, R. G. (1954) La gonidie marocaine du Xanthoria parietina (L.) Beltr. Bulletin de la Société de Sciences de Nancy 13: 8–26.Google Scholar
Werth, S. (2012) Fungal-algal interactions in Ramalina menziesii and its associated epiphytic lichen community. Lichenologist 44: 543–560.Google Scholar
Werth, S. & Scheidegger, C. (2012) Congruent genetic structure in the lichen-forming fungus Lobaria pulmonaria and its green-algal photobiont. Molecular Plant-Microbe Interactions 25: 220–230.Google Scholar
Werth, S. & Sork, V. L. (2010) Identity and genetic structure of the photobiont of the epiphytic lichen Ramalina menziesii on three oak species in southern California. American Journal of Botany 97: 821–830.Google Scholar
White, T. J., Bruns, T., Lee, S. & Taylor, J. W. (1990) Amplification and direct sequencing for 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. San Diego: Academic Press.Google Scholar
Widmer, I., Dal Grande, F., Excoffier, L., Holderegger, R., Keller, C., Mikryukov, V. S. & Scheidegger, C. (2013) European phylogeography of the epiphytic lichen fungus Lobaria pulmonaria and its green algal symbiont. Molecular Ecology (in press).Google Scholar
Wirtz, N., Lumbsch, H. T., Green, T. G. A., Türk, R., Pintado, A., Sancho, L. & Schroeter, B. (2003) Lichen fungi have low cyanobiont selectivity in maritime Antarctica. New Phytologist 160: 177–183.Google Scholar
Yahr, R., Vilgalys, R. & DePriest, P. T. (2004) Strong fungal specificity and selectivity for algal symbionts in Florida scrub Cladonia lichens. Molecular Ecology 13: 3367–3378.CrossRefGoogle ScholarPubMed
Yahr, R., Vilgalys, R. & DePriest, P. T. (2006) Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytologist 171: 847–860.Google Scholar