Hostname: page-component-848d4c4894-jbqgn Total loading time: 0 Render date: 2024-06-29T10:24:05.990Z Has data issue: false hasContentIssue false
  • English
  • Français

Genetic diversity of sterile cultured Trebouxia photobionts associated with the lichen-forming fungus Xanthoria parietina visualized with RAPD-PCR fingerprinting techniques

Published online by Cambridge University Press:  31 October 2013

Shyam NYATI ,
Silke WERTH  and
Rosmarie HONEGGER
Shyam NYATI
Affiliation:
Institute of Plant Biology, University of Zürich, Zollikerstrasse 107, CH 8008, Zürich, Switzerland. Email: rhonegg@botinst.uzh.ch Department of Radiation Oncology, University of Michigan, Ann Arbor, MI-48109, USA
Silke WERTH
Affiliation:
Faculty of Life- and Environmental Sciences, University of Iceland, Sturlugata 7, IS-101 Reykjavik, Iceland
Rosmarie HONEGGER*
Affiliation:
Institute of Plant Biology, University of Zürich, Zollikerstrasse 107, CH 8008, Zürich, Switzerland. Email: rhonegg@botinst.uzh.ch
Get access Rights & Permissions [Opens in a new window]

Abstract

Photobiont diversity within populations of Xanthoria parietina was studied at the species level by means of ITS analyses and at the subspecific level with fingerprinting techniques (RAPD-PCR) applied to sterile cultured algal isolates. Populations from coastal, rural and urban sites from NW, SW and central France and from NE Switzerland were investigated. Between 8 and 63 samples per population, altogether 150 isolates, were subjected to phenetic and ordination analyses. Epiphytic samples of X. parietina associated with different genotypes of Trebouxia decolorans but saxicolous samples contained T. arboricola. For comparison the T. gelatinosa photobiont of a small population of Teloschistes chrysophthalmus (4 samples) was investigated. ITS sequences of T. decolorans isolates from different geographic locations were largely similar. In all populations a surprisingly high diversity of genotypes was observed in Trebouxia isolated from lichen thalli growing side by side. As Trebouxia spp. are assumed to be asexually reproducing haplonts, the genetic background of this diversity is discussed. Fingerprinting techniques are a powerful tool for obtaining valuable insights into the genetic diversity within the algal partner of lichen-forming fungi at the population level, provided that sterile cultured isolates are available.

Keywords

Internal Transcribed Spacer (ITS)population geneticsTeloschistes chrysophthalmusTrebouxia arboricolaTrebouxia decoloransTrebouxia gelatinosa
Type
Articles
Information
The Lichenologist , Volume 45 , Issue 6 , November 2013 , pp. 825 - 840
Copyright
Copyright © British Lichen Society 2013 

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

REFERENCES

Ahmadjian, V. (1967) A guide to the algae occurring as lichen symbionts: isolation, culture, cultural physiology, and identification. Phycologia 6: 127–160.CrossRefGoogle Scholar
Ahmadjian, V. (1988) The lichen alga Trebouxia – does it occur free-living? Plant Systematics and Evolution 158: 243–247.Google Scholar
Beck, A. (1999) Photobiont inventory of a lichen community growing on heavy-metal-rich rock. Lichenologist 31: 501–510.CrossRefGoogle 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.Google 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
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
Casano, L. M., del Campo, E. M., Garcia-Breijo, F. J., Reig-Arminana, J., Gasulla, F., del Hoyo, A., Guera, A. & Barreno, E. (2011) Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus competition? Environmental Microbiology 13: 806–818.Google Scholar
Cox, T. F. & Cox, M. A. A. (2001) Multidimensional Scaling. CRC Press.Google Scholar
Dahlkild, A., Kallersjo, M., Lohtander, K. & Tehler, A. (2001) Photobiont diversity in the Physciaceae (Lecanorales). Bryologist 104: 527–536.CrossRefGoogle 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., Fernández-Mendoza, F., García, 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: 1–13 Google Scholar
Dyer, P. S., Murtagh, G. J. & Crittenden, P. D. (2001) Use of RAPD-PCR DNA fingerprinting and vegetative incompatibility tests to investigate genetic variation within lichen-forming fungi. Symbiosis 31: 213–229.Google Scholar
Fahselt, D. (1989) Enzyme polymorphism in sexual and asexual umbilicate lichens from Sverdrup Pass, Ellesmere Island, Canada. Lichenologist 21: 279–285.Google Scholar
Fernández-Mendoza, F., Domaschke, S., García, M. A., Jordan, P., Martín, M. P. & Printzen, C. (2011) Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata . Molecular Ecology 20: 1208–1232.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., 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.Google Scholar
Friedl, T. & Büdel, B. (1996) Photobionts. In Lichen Biology (Nash, T. H., 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
Guzow-Krzeminska, B. (2006) Photobiont flexibility in the lichen Protoparmeliopsis muralis as revealed by ITS rDNA analyses. Lichenologist 38: 469–476.Google Scholar
Hampl, V., Pavlicek, A. & Flegr, J. (2001) Construction and bootstrap analysis of DNA fingerprinting-based phylogenetic trees with the freeware program FreeTree: application to trichomonad parasites. International Journal of Systematic and Evolutionary Microbiology 51: 731–735.CrossRefGoogle ScholarPubMed
Heibel, E., Lumbsch, H. T. & Schmitt, I. (1999) Genetic variation of Usnea filipendula (Parmeliaceae) populations in western Germany investigated by RAPDs suggests reinvasion from various sources. American Journal of Botany 86: 753–757.CrossRefGoogle ScholarPubMed
Helms, G. (2003) Taxonomy and symbiosis in associations of Physciaceae and Trebouxia. PhD thesis, Georg-August Universität Göttingen.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.CrossRefGoogle Scholar
Hijri, M. & Sanders, I. R. (2004) The arbuscular mycorrhizal fungus Glomus intraradices is haploid and has a small genome size in the lower limit of eukaryotes. Fungal Genetics and Biology 41: 253–261.Google Scholar
Honegger, R. (1996) Experimental studies of growth and regenerative capacity in the foliose lichen Xanthoria parietina . New Phytologist 133: 573–581.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.Google 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. & Zippler, U. (2007) Mating systems in representatives of Parmeliaceae, Ramalinaceae and Physciaceae (Lecanoromycetes, lichen-forming ascomycetes). Mycological Research 111: 424–432.Google Scholar
Honegger, R., Zippler, U., Gansner, H. & Scherrer, S. (2004a) Mating systems in the genus Xanthoria (lichen-forming ascomycetes). Mycological Research 108: 480–488.CrossRefGoogle ScholarPubMed
Honegger, R., Zippler, U., Scherrer, S. & Dyer, P. S. (2004b) 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.Google Scholar
Kilias, H. (1988) Isoenzyme patterns as a tool in taxonomy of chlorococcal algae. Electrophoresis 9: 613–617.Google Scholar
Kilias, H., Gelfi, C. & Righetti, P. G. (1988) Isoenzyme analysis of lichen algae in immobilized pH gradients. Electrophoresis 9: 187–191.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, USA: Sinauer Associates.Google Scholar
Mansournia, M. R., Wu, B., Matsushita, N. & Hogetsu, T. (2011) Genotypic analysis of the foliose lichen Parmotrema tinctorum using microsatellite markers: association of mycobiont and photobiont, and their reproductive modes. Lichenologist 44: 1–22.Google Scholar
Meier, F. A., Scherrer, S. & Honegger, R. (2002) Faecal pellets of lichenivorous mites contain viable cells of the lichen-forming ascomycete Xanthoria parietina and its green algal photobiont, Trebouxia arboricola . Biological Journal of the Linnean Society 76: 259–268.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.CrossRefGoogle Scholar
Murtagh, G. J., Dyer, P. S. & Crittenden, P. D. (2000) Reproductive systems – sex and the single lichen. Nature 404: 564.Google Scholar
Murtagh, G. J., Dyer, P. S., McClure, P. C. & Crittenden, P. D. (1999) Use of randomly amplified polymorphic DNA markers as a tool to study variation in lichen-forming fungi. Lichenologist 31: 257–267.Google Scholar
Nyati, S., Bhattacharya, D., Werth, S. and Honegger, R. (in press) Phylogenatic analysis of LSU and SSU rDNA group 1 introns associated with the genera Xanthoria and Xanthomendoza (Teloschistaceae, lichenized ascomycetes). Journal of Phycology.Google Scholar
Nyati, S., Schaerer, S., Werth, S. and Honegger, R. (2014) Green algal photobiont diversity (Trebouxia spp.) in representatives of the Teloschistaceas (Lecanoromycetes, lichen-forming Ascomycetes). Lichenologist 46: (in press).CrossRefGoogle 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.Google Scholar
Opanowicz, M. & Grube, M. (2004) Photobiont genetic variation in Flavocetraria nivalis from Poland (Parmeliaceae, lichenized Ascomycota). Lichenologist 36: 125–131.Google Scholar
Oppermann, B., Karlovsky, P. & Reisser, W. (1997) M13 DNA fingerprinting in unicellular and filamentous green algae. European Journal of Phycology 32: 103–110.CrossRefGoogle Scholar
Page, R. D. M. (1996) TreeView: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12: 357–358.Google ScholarPubMed
Pavlicek, A., Hrda, S. & Flegr, J. (1999) FreeTree-freeware program for construction of phylogenetic trees on the basis of distance data and bootstrap jackknife analysis of the tree robustness. Application in the RAPD analysis of genus Frenkelia . Folia Biologica 45: 97–99.Google ScholarPubMed
Peakall, R. & Smouse, P. E. (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6: 288–295.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
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.CrossRefGoogle ScholarPubMed
Piercey-Normore, M. D. (2009) Vegetatively reproducing fungi in three genera of the Parmeliaceae share divergent algal partners. Bryologist 112: 773–785.Google Scholar
Piercey-Normore, M. D. & DePriest, P. T. (2001) Algal switching among lichen symbioses. American Journal of Botany 88: 1490–1498.Google Scholar
Printzen, C., Lumbsch, H. T., Schmitt, I. & Feige, G. B. (1999) A study on the genetic variability of Biatora helvola using RAPD markers. Lichenologist 31: 491–499.CrossRefGoogle Scholar
Rasmussen, U. & Svenning, M. M. (1998) Fingerprinting of cyanobacteria based on PCR with primers derived from short and long tandemly repeated repetitive sequences. Applied and Environmental Microbiology 64: 265–272.Google Scholar
Rohlf, F. J. (2000) NTSYS-PC: numerical taxonomy and multivairate analysis system, version 2.1. Setauket, New York, USA: Exeter Software.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
Scherrer, S., Zippler, U. & Honegger, R. (2005) Characterisation of the mating-type locus in the genus Xanthoria (lichen-forming ascomycetes, lecanoromycetes). Fungal Genetics and Biology 42: 976–988.Google Scholar
Schmitt, I., Mangold, A. & Lumbsch, H. T. (2002) Potential use of tRNA primers for fingerprinting in molecular lichen ecology and biogeography. Nova Hedwigia 74: 69–74.Google Scholar
Seymour, F. A., Crittenden, P. D., Dickinson, M. J., Paoletti, M., Montiel, D., Cho, L. & Dyer, P. S. (2005) Breeding systems in the lichen-forming fungal genus Cladonia . Fungal Genetics and Biology 42: 554–563.Google Scholar
Søchting, U. (1997) Two major anthraquinone chemosyndromes in Teloschistaceae . Bibliotheca Lichenologica 68: 135–144.Google Scholar
Swofford, D. L. (1998) PAUP: Phylogenetic Analysis using Parsimony (*and Other Methods), Version 4. Sunderland, Massachusetts, USA: Sinauer Associates.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
Tschermak-Woess, E. (1988) The algal partner. In Handbook of Lichenology (Galun, M., ed.): 39–92. Boca Raton, Florida, USA: 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
Walser, J. C., Holderegger, R., Gugerli, F., Hoebee, S. E. & Scheidegger, C. (2005) Microsatellites reveal regional population differentiation and isolation in Lobaria pulmonaria, an epiphytic lichen. Molecular Ecology 14: 457–467.Google Scholar
Walser, J. C., Sperisen, C., Soliva, M. & Scheidegger, C. (2003) Fungus-specific microsatellite primers of lichens: application for the assessment of genetic variation on different spatial scales in Lobaria pulmonaria . Fungal Genetics and Biology 40: 72–82.Google Scholar
Werth, S., Gugerli, F., Holderegger, R., Wagner, H. H., Csencsics, D. & Scheidegger, C. (2007) Landscape-level gene flow in Lobaria pulmonaria, an epiphytic lichen. Molecular Ecology 16: 2807–2815.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
Werth, S., Wagner, H. H., Holderegger, R., Kalwij, J. M. & Scheidegger, C. (2006) Effect of disturbances on the genetic diversity of an old-forest associated lichen. Molecular Ecology 15: 911–921.CrossRefGoogle ScholarPubMed
Widmer, I., Dal Grande, F., Cornejo, C. & Scheidegger, C. (2010) Highly variable microsatellite markers for the fungal and algal symbionts of the lichen Lobaria pulmonaria and challenges in developing biont-specific molecular markers for fungal associations. Fungal Biology 114: 538–544.CrossRefGoogle ScholarPubMed
Widmer, I., Dal Grande, F., Excoffier, L., Holderegger, R., Keller, C., Mikryukov, V. S. & Scheidegger, C. (2012) European phylogeography of the epiphytic lichen fungus Lobaria pulmonaria and its green algal symbiont. Molecular Ecology 21: 5827–5844.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, N., Gelfand, D., Sninsky, J. & White, T., eds): 315–322.Google Scholar
Wornik, S. & Grube, M. (2010) Joint dispersal does not imply maintenance of partnerships in lichen symbioses. Microbial Ecology 59: 150–157.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.Google Scholar
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