Hostname: page-component-848d4c4894-4hhp2 Total loading time: 0 Render date: 2024-05-14T07:34:23.856Z Has data issue: false hasContentIssue false

Genotypic analysis of the foliose lichen Parmotrema tinctorum using microsatellite markers: association of mycobiont and photobiont, and their reproductive modes

Published online by Cambridge University Press:  29 March 2012

Mohammad Reza MANSOURNIA
Affiliation:
Laboratory of Forest Botany, Department of Forest Science, Graduate School of Agricultural and Life Sciences, The University of Tokyo. 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan. Email: mrmansournia@yahoo.com
Bingyun WU
Affiliation:
Laboratory of Forest Botany, Department of Forest Science, Graduate School of Agricultural and Life Sciences, The University of Tokyo. 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan. Email: mrmansournia@yahoo.com
Norihisa MATSUSHITA
Affiliation:
Laboratory of Forest Botany, Department of Forest Science, Graduate School of Agricultural and Life Sciences, The University of Tokyo. 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan. Email: mrmansournia@yahoo.com
Taizo HOGETSU
Affiliation:
Laboratory of Forest Botany, Department of Forest Science, Graduate School of Agricultural and Life Sciences, The University of Tokyo. 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan. Email: mrmansournia@yahoo.com

Abstract

To investigate the association between, and the reproductive modes of, mycobiont and photobiont in the lichen Parmotrema tinctorum, microsatellite markers (SSR markers) were developed for both bionts and genotypic analysis was performed for thalli in a Pinus thunbergii forest. In a within-thallus analysis, tissue pieces were sampled from many portions within each of five thalli. Within-thallus variation for both mycobiont and photobiont differed among the thalli investigated, suggesting that a single thallus can be derived from either a single mycobiont origin with or without occasional changes in the photobiont, or fusion of several independent thalli. In the within-tree analysis, thalli with the same genotypes were found on individual trees, suggesting the presence of short-distance isidium dispersal. In the within-stand analysis, genotypically similar photobionts tended to be associated with the same mycobiont genotype, suggesting the participation of local dispersal via isidia. The overall index of association (IA) for the mycobiont in the stand probably indicates the dominance of sexual reproduction, in contrast to that of the photobiont, where dominance of asexual reproduction is suggested. IA's of mycobiont and photobiont were also calculated for thalli collected from larger areas, where there is a signature for sexual reproduction for photobiont.

Type
Research Article
Copyright
Copyright © British Lichen Society 2012

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

Agapow, P. M. & Burt, A. (2001) Indices of multilocus linkage disequilibrium. Molecular Ecology Notes 1: 101102.CrossRefGoogle Scholar
Ahmadjian, V. (1987) The lichen alga Trebouxia: does it occur free-living? Plant Systematics and Evolution 158: 243247.CrossRefGoogle Scholar
Armstrong, R. A. (1984) Growth of experimentally reconstructed thalli of the lichen Parmelia conspersa. New Phytologist 98: 497502.CrossRefGoogle Scholar
Bischoff, H. W. & Bold, H. C. (1963) Phycological Studies IV. Some soil algae from enchanted rocks and related species. University of Texas Publication 6318: 195.Google Scholar
Bridge, P. D. & Hawksworth, D. L. (1998) What molecular biology has to tell us at the species level in lichenized fungi. Lichenologist 30: 307320.CrossRefGoogle Scholar
Casano, L. M., Del Campo, E. M., García-Breijo, F. J., Reig-Armiñana, J., Gasulla, F., Del Hoyo, A., Guéra, 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: 806818.CrossRefGoogle ScholarPubMed
Cordeiro, L. M. C., Reis, R. A., Cruz, L. M., Stocker- Wörgötter, E., Grube, M. & Iacomini, M. (2005) Molecular studies of photobionts of selected lichens from the coastal vegetation of Brazil. FEMS Microbiology Ecology 54: 381390.CrossRefGoogle ScholarPubMed
Culberson, C. F., Culberson, W. L. & Johnson, A. (1988) Gene flow in lichens. American Journal of Botany 75: 11351139.CrossRefGoogle Scholar
Culberson, W. L., Culberson, C. F. & Johnson, A. (1993) Speciation in lichens of the Ramalina siliquosa complex (Ascomycotina, Ramalinaceae): gene flow and reproductive isolation. American Journal of Botany 80: 14721481.CrossRefGoogle 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: 11471149.CrossRefGoogle Scholar
del Campo, E. M., Casanoa, L. M., Gasullab, F. & Barrenob, E. (2010) Suitability of chloroplast LSU rDNA and its diverse group I introns for species recognition and phylogenetic analyses of lichen-forming Trebouxia algae. Molecular Phylogenetics and Evolution 54: 437444.CrossRefGoogle 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: 213229.Google Scholar
Fahselt, D. (1988) Measurement of intrapopulational enzyme variation in five species of epiphytic lichens. Lichenologist 20: 377384.CrossRefGoogle Scholar
Fahselt, D., Alstrup, V. & Tavares, S. (1995) Enzyme polymorphism in Umbilicaria cylindrica in Northwest Greenland. Bryologist 98: 118122.CrossRefGoogle Scholar
Friedl, T. & Büdel, B. (2008) Photobionts. In Lichen Biology (Nash, T. H. III, ed): 926. Cambridge: Cambridge University Press.CrossRefGoogle 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: 125148.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: 113118.CrossRefGoogle Scholar
Hageman, C. & Fahselt, D. (1992) Geographical distribution of enzyme polymorphisms in the lichen Umbilicaria mammulata. Bryologist 95: 316323.CrossRefGoogle Scholar
Hawksworth, D. L. (1988) The variety of fungal-algal symbioses, their evolutionary significance, and the nature of lichens. Botanical Journal of the Linnean Society 96: 320.CrossRefGoogle Scholar
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: 753757.CrossRefGoogle ScholarPubMed
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: 7386.CrossRefGoogle Scholar
Högberg, N., Kroken, S., Thor, G. & Taylor, J. W. (2002) Reproductive mode and genetic variation suggest a North American origin of European Letharia vulpina. Molecular Ecology 11: 11911196.CrossRefGoogle ScholarPubMed
Holm, S. (1979) A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics 6: 6570.Google Scholar
Honegger, R. (1991) Fungal evolution: symbiosis and morphogenesis. In Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis (Margulis, L. & Fester, R., eds): 319340. Cambridge: The MIT Press.Google Scholar
Honegger, R. & Scherrer, S. (2008) Sexual reproduction in lichen-forming ascomycetes. In Lichen Biology (Nash, T. H. III, ed): 94103. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Kotelko, R., Doering, M. & Piercey-Normore, M. D. (2008) Species diversity and genetic variation of terrestrial lichens and bryophytes in a boreal jack pine forest of central Canada. Bryologist 111: 594606.CrossRefGoogle 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: 645660.CrossRefGoogle Scholar
Kroken, S. & Taylor, J. W. (2001) Outcrossing and recombination in the lichenized fungus Letharia. Fungal Genetics and Biology 34: 8392.CrossRefGoogle ScholarPubMed
Langella, O. (1999) Populations version 1.2.30. http://bioinformatics.org/~tryphon/populations/Google Scholar
Lewis, D. H. (1987) Evolutionary aspects of mutualistic associations between fungi and photosynthetic organisms. In Evolutionary Biology of the Fungi (Rayner, A. D. M., Brasier, C. M. & Moore, D., eds): 161178. New York: Cambridge University Press.Google Scholar
Lian, C., Hogetsu, T., Matsushita, N., Guerin-Laguette, A., Suzuki, K. & Yamada, A. (2003) Development of microsatellite markers from an ectomycorrhizal fungus, Tricholoma matsutake, by an ISSR-suppression-PCR method. Mycorrhiza 13: 2731.CrossRefGoogle ScholarPubMed
Lutzoni, F., Pagel, M. & Reeb, V. (2001) Major fungal lineages are derived from lichen symbiotic ancestors. Nature 411: 937940.CrossRefGoogle ScholarPubMed
Maynard-Smith, J., Smith, N. H., O'Rourke, M. & Spratt, B. G. (1993) How clonal are bacteria? Proceeding of the National Academy of Sciences of the United States of America 90: 43844388.CrossRefGoogle Scholar
Moxham, T. H. (1981) Fusion of a detached lobe onto the parent thallus in the lichen Xanthoria parietina. Bryologist 84: 363364.CrossRefGoogle Scholar
Nash, T. H. III (2008) Introduction. In Lichen Biology (Nash, T. H. III, ed): 18. Cambridge: Cambridge University 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: 4359.CrossRefGoogle Scholar
Peakall, R. & Smouse, P. E. (2005) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6: 288295.CrossRefGoogle Scholar
Powell, W., Morgante, M., Andre, C., Hanafey, M., Vogel, J., Tingey, S. & Rafalski, A. (1996) The comparison of RFLP, RAPD, AFLP and SSR (microsatellite) markers for germplasm analysis. Molecular Breeding 2: 225238.CrossRefGoogle Scholar
Robertson, J. & Piercey-Normore, M. D. (2007) Gene flow in symbionts of Cladonia arbuscula. Lichenologist 39: 6982.CrossRefGoogle Scholar
Saitou, N. & Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406425.Google Scholar
Sanders, W. B. (2005) Observing microscopic phases of lichen life cycles on transparent substrata placed in situ. Lichenologist 37: 373382.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: 425435.CrossRefGoogle ScholarPubMed
Schneider, S., Roessli, D. & Excoffier, L. (2000) Arlequin, version 2.000: a software for population genetics data analysis. Genetics and Biometry Laboratory. University of Geneva, Geneva, Switzerland.Google Scholar
Schuster, G., Ott, S. & Jahns, H. M. (1985) Artificial cultures of lichens in the natural environment. Lichenologist 17: 247253.CrossRefGoogle Scholar
Shen, S. (2008) Genetic diversity analysis with ISSR PCR on green algae Chlorella vulgaris and Chlorella pyrenoidosa. Chinese Journal of Oceanology and Limnology 26: 380384.CrossRefGoogle 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: 15961599.CrossRefGoogle ScholarPubMed
Tehler, A. & Wedin, M. (2008) Systematics of lichenized fungi. In Lichen Biology (Nash, T. H. III, ed): 336363. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Thompson, J. D., Higgins, D. G. & Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 46734680.CrossRefGoogle ScholarPubMed
Vilgalys, R. & Hester, M. (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172: 42384246.CrossRefGoogle ScholarPubMed
Walser, J. C., Zoller, S., Büchler, U. & Scheidegger, C. (2001) Species-specific detection of Lobaria pulmonaria (lichenized ascomycete) diaspores in litter samples trapped in snow cover. Molecular Ecology 10: 21292138.CrossRefGoogle ScholarPubMed
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: 7282.CrossRefGoogle ScholarPubMed
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: 28072815.CrossRefGoogle ScholarPubMed
White, T. J., Bruns, T., Lee, S. & Taylor, J. (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): 315322. London: 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: 538544.CrossRefGoogle ScholarPubMed
Wornik, S. & Grube, M. (2010) Joint dispersal does not imply maintenance of partnerships in lichen symbioses. Microbial Ecology 59: 150157.CrossRefGoogle Scholar
Wu, B. Y., Kurokochi, H. & Hogetsu, T. (2009) Development of 12 microsatellite markers in Euptelea polyandra by a random tailed genome-walking method using Phi29 DNA polymerase. Conservation Genetics Resources 1: 5961.CrossRefGoogle Scholar
Zhou, Z., Miwa, M. & Hogetsu, T. (1999) Analysis of genetic structure of a Suillus grevillei population in a Larix kaempferi stand by polymorphism of inter-simple sequence repeat (ISSR). New Phytologist 144: 5563.CrossRefGoogle Scholar
Zoller, S., Lutzoni, F. & Scheidegger, C. (1999) Genetic variation within and among populations of the threatened lichen Lobaria pulmonaria in Switzerland and implications for its conservation. Molecular Ecology 8: 20492059.CrossRefGoogle ScholarPubMed