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Development of microsatellite markers in Protoparmeliopsis muralis (lichenized Ascomycete) – a common lichen species

Published online by Cambridge University Press:  31 October 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; and Department of Organismic Biology, University of Salzburg, Hellbrunnerstr. 34, 5020 Salzburg, Austria. Email: [email protected]
Elfie STOCKER-WÖRGÖTTER
Affiliation:
Department of Organismic Biology, University of Salzburg, Hellbrunnerstr. 34, 5020 Salzburg, Austria
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Abstract

Lichen-forming fungi are symbiotic organisms forming a thallus with autotrophic green algae and/or cyanobacteria. Protoparmeliopsis muralis (Schreb.) Choisy is a green-algal lichen-forming fungus associating with Trebouxia photobionts. It is known as one of the most successful urban lichens in the world. In this paper, the development of microsatellite markers specific for the mycobiont of Protoparmeliopsis muralis is reported. In order to avoid algal contaminations, the pure mycobiont culture was obtained and subsequently used for DNA isolation. For DNA enrichment, the Fast Isolation by AFLP of Sequences Containing Repeats (FIASCO) method was applied. Of the 380 clones sequenced, 62 contained repeats. In total, 38 primer pairs were designed and tested, and finally 7 primer pairs were polymorphic based on 21 specimens of P. muralis.

Keywords

FIASCOlichenmycobiontpopulation
Type
Articles
Information
The Lichenologist , Volume 45 , Issue 6 , November 2013 , pp. 791 - 798
Copyright
Copyright © British Lichen Society 2013 

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References

Ahmadjian, V. (1993) The Lichen Symbiosis. New York: John Wiley & Sons.Google Scholar
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.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
Bikandi, J. (2006) Microsatellite Repeats Finder. Available online: http://www.biophp.org/minitools/microsatellite_repeats_finder/demo.php (accessed 2008–2009).Google 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
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.Google Scholar
Dal Grande, F., Widmer, I., Beck, A. & Scheidegger, C. (2010) Microsatellite markers for Dictyochloropsis reticulata (Trebouxiophyceae), the symbiotic alga of the lichen Lobaria pulmonaria (L.). Conservation Genetics 11: 1147–1149.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 13: 3159–3172.CrossRefGoogle Scholar
Dal Grande, F., Beck, A., Singh, G. & Schmitt, I. (2013) Microsatellite primers in the lichen symbiotic alga Trebouxia decolorans (Trebouxiophyceae). Applications in Plant Sciences 1: 1200400.Google 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
Dutech, C., Enjalbert, J., Fournier, E., Delmotte, F., Barrès, B., Carlier, J., Tharreau, D. & Giraud, T. (2007) Challenges of microsatellite isolation in fungi. Fungal Genetics and Biology 44: 33–49.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
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.Google Scholar
Guzow-Krzemińska, B. (2006) Photobiont flexibility in the lichen Protoparmeliopsis muralis as revealed by ITS rDNA analyses. Lichenologist 38: 469–476.Google Scholar
Guzow-Krzemińska, B. & Węgrzyn, G. (2000) Potential use of restriction analysis of PCR-amplified DNA fragments in taxonomy of lichens. Mycotaxon 76: 305–313.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. (1991) Functional aspects of the lichen symbiosis. Annual Review of Plant Physiology and Plant Molecular Biology 42: 553–578.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
Jones, T. C., Green, T. G. A., Hogg, I. D. & Wilkins, R. J. (2012) Isolation and characterization of microsatellites in the lichen Buellia frigida (Physciaceae), an Antarctic endemic. American Journal of Botany 99: e131–e133.Google Scholar
Laudon, J. A. (2010) Lecanora antiqua, a new saxicolous species from Great Britain and the nomenclatural and authorship of L. albescens, L. conferta and L. muralis . Lichenologist 42: 631–636.Google Scholar
Leach, R. (2000) Perfect microsatellite repeat finder (based on Tandyman). Computer program by the author. http://sgdp.iop.kcl.ac.uk/nikammar/repeatfinder.html (accessed 2008–2009).Google Scholar
Lim, S., Notley-McRobb, L., Lim, M. & Carter, D. A. (2004) A comparison of the nature and abundance of microsatellites in 14 fungal genomes. Fungal Genetics and Biology 41: 1025–1036.Google Scholar
Lindblom, L. & Ekman, S. (2006) Genetic variation and population differentiation in the lichen-forming ascomycete Xanthoria parietina on the island Storfosna, central Norway. Molecular Ecology 15: 1545–1559.Google Scholar
Lindblom, L. & Ekman, S. (2012) RAPDs distinguish the lichens Xanthoria aureola and X. parietina in a mixed seashore population. Nova Hedwigia 94: 279–285.Google Scholar
Magain, N., Forrest, L. L., Sérusiaux, E. & Goffinet, B. (2010) Microsatellite primers in the Peltigera dolichorhiza complex (lichenized ascomycete, Peltigerales). American Journal of Botany 97: e102–e104.Google Scholar
Mansournia, M. R., Wu, B., Matsushita, N. & Hogetsu, T. (2012) Genotypic analysis of the foliose lichen Parmotrema tinctorum using microsatellite markers: association of mycobiont and photobiont, and their reproductive modes. Lichenologist 44: 419–440.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.CrossRefGoogle Scholar
Murtagh, G. J., Dyer, P. S. & Crittenden, P. D. (2000) Reproductive systems: sex and the single lichen. Nature 404: 564.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.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
Rozen, S. & Skaletsky, H. J. (2000) Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics Methods and Protocols: Methods in Molecular Biology (Krawetz, S. & Misener, S., eds): 365–386. Totowa, New Jersey: Humana Press.Google Scholar
Seymour, F. A., Crittenden, P. D., Dickinson, M., 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
Smit, A. F. A., Hubley, R. & Green, P. (1996–2010) RepeatMasker Open-3.0. <http://www.repeatmasker.org>. Used Version: open-3.2.8 (RMLib: 20090604)..+Used+Version:+open-3.2.8+(RMLib:+20090604).>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
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 24: 4876–4882.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
Walser, J. C., Gugerli, F., Holderegger, R., Kuonen, D. & Scheidegger, C. (2004) Recombination and clonal propagation in different populations of the lichen Lobaria pulmonaria . Heredity 93: 322–329.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
Werth, S. (2010) Population genetics of lichen-forming fungi – a review. Lichenologist 42: 499–519.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
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. San Diego: Academic Press.Google Scholar
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.Google Scholar
Zane, L., Bargelloni, L. & Patarnello, T. (2002) Strategies for microsatellite isolation: a review. Molecular Ecology 11: 1–16.Google Scholar
Zoller, S., Scheidegger, C. & Sperisen, C. (1999) PCR primers for the amplification of mitochondrial small subunit ribosomal DNA of lichen-forming ascomycetes. Lichenologist 31: 511–516.Google Scholar