Hostname: page-component-7479d7b7d-pfhbr Total loading time: 0 Render date: 2024-07-12T06:18:08.605Z Has data issue: false hasContentIssue false
  • English
  • Français

Genetic diversity and species delimitation of the zeorin-containing red-fruited Cladonia species (lichenized Ascomycota) assessed with ITS rDNA and β-tubulin data

Published online by Cambridge University Press:  23 August 2013

Jana STEINOVÁ ,
Soili STENROOS ,
Martin GRUBE  and
Pavel ŠKALOUD
Jana STEINOVÁ*
Affiliation:
Department of Botany, Faculty of Science, Charles University in Prague, Benátská 2, Praha 2, CZ-12801, Czech Republic. Email: jana.steinova@gmail.com
Soili STENROOS
Affiliation:
Botanical Museum, Finnish Museum of Natural History, P.O. Box 7, FI-00014, University of Helsinki, Finland
Martin GRUBE
Affiliation:
Institute of Plant Sciences, Karl-Franzens-University Graz, Holteigasse 6, A-8010, Graz, Austria
Pavel ŠKALOUD
Affiliation:
Department of Botany, Faculty of Science, Charles University in Prague, Benátská 2, Praha 2, CZ-12801, Czech Republic. Email: jana.steinova@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Zeorin-containing red-fruited Cladonia species, the so-called C. coccifera group, are widespread terrestrial lichens which share most of their secondary substances but differ morphologically. The main objective of this study was to explore whether the current delimitation of these species is supported by molecular data. A total of 52 European and North American specimens of C. coccifera, C. deformis, C. diversa, and C. pleurota were examined. The internal transcribed spacer regions of the nuclear ribosomal DNA and the β-tubulin gene loci were sequenced for phylogenetic analyses. Traditional morphological species circumscriptions in zeorin-containing members of the C. coccifera group are not supported by molecular data. Cladonia coccifera, C. deformis, and C. pleurota were recovered as polyphyletic in both gene topologies; C. diversa formed a lineage in the ITS phylogeny but this was not statistically supported. We detected chemical patterns of the presence/absence of porphyrilic and/or isousnic acid which may help to characterize two lineages. Our results also show incongruence between the two molecular markers studied. Therefore, we focused on possible explanations of this phenomenon. Five major evolutionary mechanisms can potentially result in phylogenetic discordance between genes: presence of pseudogenes, horizontal gene transfer, gene paralogy, incomplete lineage sorting, and hybridization. These mechanisms are briefly discussed. We consider incomplete lineage sorting and/or hybridization to best explain the incongruence.

Keywords

bootscanningCladoniaceaeCocciferaeLecanoromyceteslichenstaxonomy
Type
Articles
Information
The Lichenologist , Volume 45 , Issue 5 , September 2013 , pp. 665 - 684
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

Ahti, T. (2000) Cladoniaceae. Flora Neotropica Monograph 78: 1–362.Google Scholar
Ahti, T. & Stenroos, S. (2012) New data on nomenclature, taxonomy and distribution of some species of the lichen genus Cladonia . Botanica Complutensis 36: 31–34.Google Scholar
Asperges, M. (1983) De Cladonia's uit de sectie Cocciferae in België: morfologie, chemie, ecologie, sociologie, verspreiding en systematiek . Ph. D thesis, University of Antwerp.Google Scholar
Asperges, M. (1985) Cladonia diversa Asperges en Europe occidentale. Dumortiera 32: 24–31.Google Scholar
Begerow, D., John, B. & Oberwinkler, F. (2004) Evolutionary relationships among β-tubulin gene sequences of basidiomycetous fungi. Mycological Research 108: 1257–1263.Google Scholar
Beiggi, S. & Piercey-Normore, M. D. (2007) Evolution of ITS ribosomal RNA secondary structures in fungal and algal symbionts of selected species of Cladonia sect. Cladonia (Cladoniaceae, Ascomycotina). Journal of Molecular Evolution 64: 528–542.Google Scholar
Blanco-Pastor, J. L., Vargas, P. & Pfeil, B. E. (2012) Coalescent simulations reveal hybridization and incomplete lineage sorting in Mediterranean Linaria . Plos One 7: e39089.Google Scholar
Bloomquist, E. W. & Suchard, M. A. (2010) Unifying vertical and nonvertical evolution: a stochastic ARG-based Framework. Systematic Biology 59: 27–41.Google Scholar
Brasier, C. M., Kirk, S. A., Pipe, N. D. & Buck, K. W. (1998) Rare interspecific hybrids in natural populations of the Dutch elm disease pathogens Ophiostoma ulmi and O. novo-ulmi . Mycological research 102: 45–57.Google Scholar
Brasier, C. M., Cooke, D. E. & Duncan, J. M. (1999) Origin of a new Phytophthora pathogen through interspecific hybridization. Proceedings of the National Academy of Sciences of the United States of America 96: 5878–5883.Google Scholar
Buckler, E. S., Ippolito, A. & Holtsford, T. P. (1997) The evolution of ribosomal DNA: divergent paralogues and phylogenetic implications. Genetics 145: 821–832.Google Scholar
Christensen, S. N. & Johnsen, I. (2001) The lichen-rich coastal heath vegetation on the isle of Anholt, Denmark–description, history and development. Journal of Coastal Conservation 7: 1–12.Google Scholar
Coleman, A. W. (2000) The significance of a coincidence between evolutionary landmarks found in mating affinity and a DNA sequence. Protist 151: 1–9.Google Scholar
Coleman, A. W. (2003) ITS2 is a double-edged tool for eukaryote evolutionary comparisons. Trends in Genetics 19: 370–375.Google Scholar
Corradi, N., Kuhn, G. & Sanders, I. R. (2004) Monophyly of β-tubulin and H+-ATPase gene variants in Glomus intraradices: consequences for molecular evolutionary studies of AM fungal genes. Fungal Genetics and Biology 41: 262–273.Google Scholar
Craven, K. D., Blankenship, J. D., Leuchtmann, A., Hignight, K. & Schardl, C. L. (2001 a) Hybrid fungal endophytes symbiotic with the grass Lolium pratense . Sydowia 53: 44–73.Google Scholar
Craven, K. D., Hsiau, P. T. W., Leuchtmann, A., Hollin, W. & Schardl, C. L. (2001 b) Multigene phylogeny of Epichloë species, fungal symbionts of grasses. Annals of the Missouri Botanical Garden 88: 14–34.CrossRefGoogle Scholar
Cubero, O. F., Crespo, A., Fatehi, J. & Bridge, P. D. (1999) DNA extraction and PCR amplification method suitable for fresh, herbarium-stored, lichenized, and other fungi. Plant Systematics and Evolution 216: 243–249.Google Scholar
De Rijk, P., Wuyts, J. & De Wachter, R. (2003) RnaViz 2: an improved representation of RNA secondary structure. Bioinformatics 19: 299–300.Google Scholar
Divakar, P. K., Crespo, A., Blanco, O. & Lumbsch, H. T. (2006) Phylogenetic significance of morphological characters in the tropical Hypotrachyna clade of parmelioid lichens (Parmeliaceae, Ascomycota). Molecular Phylogenetics and Evolution 40: 448–458.Google Scholar
Edgar, R. C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792–1797.Google Scholar
Ertz, D., Miądlikowska, J., Lutzoni, F., Dessein, S., Raspe, O., Vigneron, N., Hofstetter, V. & Diederich, P. (2009) Towards a new classification of the Arthoniales (Ascomycota) based on a three-gene phylogeny focusing on the genus Opegrapha . Mycological Research 113: 141–152.CrossRefGoogle Scholar
Fehrer, J., Gemeinholzer, B., Chrtek, J. & Braeutigam, S. (2007) Incongruent plastid and nuclear DNA phylogenies reveal ancient intergeneric hybridization in Pilosella hawkweeds (Hieracium, Cichorieae, Asteraceae). Molecular Phylogenetics and Evolution 42: 347–361.Google Scholar
Fontaine, K., Ahti, T. & Piercey-Normore, M. D. (2010) Convergent evolution in Cladonia gracilis and allies. Lichenologist 42: 323–338.CrossRefGoogle Scholar
Gardes, M. & Bruns, T. (1993) ITS primers with enhanced specificity for Basidiomycetes: application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113–118.Google Scholar
Grimm, G. W. & Denk, T. (2008) ITS evolution in Platanus (Platanaceae): homoeologues, pseudogenes and ancient hybridization. Annals of Botany 101: 403–419.CrossRefGoogle ScholarPubMed
Grube, M. & Hawksworth, D. (2007) Trouble with lichen: the re-evaluation and re-interpretation of thallus form and fruit body types in the molecular era. Mycological Research 111: 1116–1132.CrossRefGoogle ScholarPubMed
Grube, M. & Kroken, S. (2000) Molecular approaches and the concept of species and species complexes in lichenized fungi. Mycological Research 104: 1284–1294.Google Scholar
Harpke, D. & Peterson, A. (2008) 5.8S motifs for the identification of pseudogenic ITS regions. Botany 86: 300–305.Google Scholar
Hasse, T. (2005) Charakterisierung der Sukzessionsstadien im Spergulo-Corynephoretum (Silbergrasfluren) unter besonderer Berücksichtigung der Flechten. Tuexenia 25: 407–424.Google Scholar
Holland, B. R., Benthin, S., Lockhart, P. J., Moulton, V. & Huber, K. T. (2008) Using supernetworks to distinguish hybridization from lineage-sorting. BMC Evolutionary Biology 8: 202.CrossRefGoogle ScholarPubMed
Huson, D. H. & Bryant, D. (2006) Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23: 254–267.Google Scholar
Jakob, S. S. & Blattner, F. R. (2006) A chloroplast genealogy of Hordeum (Poaceae): long-term persisting haplotypes, incomplete lineage sorting, regional extinction, and the consequences for phylogenetic inference. Molecular Biology and Evolution 23: 1602–1612.Google Scholar
James, P. W. (2009) Cladonia. In The Lichens of Great Britain and Ireland (Smith, C. W., Aptroot, A., Coppins, B. J., Fletcher, A., Gilbert, O. L., James, P. W. & Wolseley, P. A., eds): 309–338. London: British Lichen Society.Google Scholar
Jobb, G., von Haeseler, A. & Strimmer, K. (2004) TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evolutionary Biology 4: 18.Google Scholar
Keeling, P. J. & Palmer, J. D. (2008) Horizontal gene transfer in eukaryotic evolution. Nature Reviews Genetics 9: 605–618.Google Scholar
Kelly, L. J., Hollingsworth, P. M., Coppins, B. J., Ellis, C. J., Harrold, P., Tosh, J. & Yahr, R. (2011) DNA barcoding of lichenized fungi demonstrates high identification success in a floristic context. New Phytologist 191: 288–300.Google Scholar
Khaldi, N., Collemare, J., Lebrun, M.-H. & Wolfe, K. H. (2008) Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi. Genome Biology 9: R18.Google Scholar
Knowles, L. L. & Carstens, B. C. (2007) Delimiting species without monophyletic gene trees. Systematic Biology 56: 887–895.Google Scholar
Kotelko, R. & Piercey-Normore, M. D. (2010) Cladonia pyxidata and C. pocillum; genetic evidence to regard them as conspecific. Mycologia 102: 534–545.Google Scholar
Kumar, S., Nei, M., Dudley, J. & Tamura, K. (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Briefings in Bioinformatics 9: 299–306.Google Scholar
Leache, A. D. & Fujita, M. K. (2010) Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus). Proceedings of the Royal Society B-Biological Sciences 277: 3071–3077.Google Scholar
Lechowicz, M. J. & Adams, M. S. (1974) Ecology of Cladonia lichens. I. Preliminary assessment of the ecology of terricolous lichen–moss communities in Ontario and Wisconsin. Canadian Journal of Botany 52: 55–64.Google Scholar
Lee, J. S., Lee, H. K., Hur, J.-S., Andreev, M. & Hong, S. G. (2008) Diversity of the lichenized fungi in King George Island, Antarctica, revealed by phylogenetic analysis of partial large subunit rDNA sequences. Journal of Microbiology and Biotechnology 18: 1016–1023.Google Scholar
Linnaeus, C. (1753) Species Plantarum. Holmiae [Stockholm]: Laurentius Salvius.Google Scholar
Lole, K. S., Bollinger, R. C., Paranjape, R. S., Gadkari, D., Kulkarni, S. S., Novak, N. G., Ingersoll, R., Sheppard, H. W. & Ray, S. C. (1999) Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. Journal of Virology 73: 152–160.Google Scholar
Lopez, P., Forterre, P. & Philippe, H. (1999) The root of the tree of life in the light of the covarion model. Journal of Molecular Evolution 49: 496–508.Google Scholar
Marcet-Houben, M. & Gabaldon, T. (2010) Acquisition of prokaryotic genes by fungal genomes. Trends in Genetics 26: 5–8.Google Scholar
Martin, D. P., Lemey, P., Lott, M., Moulton, V., Posada, D. & Lefeuvre, P. (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26: 2462–2463.Google Scholar
McBreen, K. & Lockhart, P. J. (2006) Reconstructing reticulate evolutionary histories of plants. Trends in Plant Science 11: 398–404.Google Scholar
Meng, C. & Kubatko, L. S. (2009) Detecting hybrid speciation in the presence of incomplete lineage sorting using gene tree incongruence: a model. Theoretical Population Biology 75: 35–45.CrossRefGoogle ScholarPubMed
Morando, M., Avila, L. J., Baker, J. & Sites, J. W. (2004) Phylogeny and phylogeography of the Liolaemus darwinii complex (Squamata: Liolaemidae): evidence for introgression and incomplete lineage sorting. Evolution 58: 842–861.Google Scholar
Msiska, Z. & Morton, J. B. (2009) Phylogenetic analysis of the Glomeromycota by partial β-tubulin gene sequences. Mycorrhiza 19: 247–254.Google Scholar
Müller, T., Philippi, N., Dandekar, T., Schultz, J. & Wolf, M. (2007) Distinguishing species. RNA 13: 1469–1472.Google Scholar
Muschner, V. C., Lorenz, A. P., Cervi, A. C., Bonatto, S. L., Souza-Chies, T. I., Salzano, F. M. & Freitas, L. B. (2003) A first molecular phylogenetic analysis of Passiflora (Passifloraceae). American Journal of Botany 90: 1229–1238.Google Scholar
Myllys, L., Lohtander, K. & Tehler, A. (2001) β-tubulin, ITS and group I intron challenge the species pair concept in Physcia aipolia and P. caesia . Mycologia 93: 335–343.Google Scholar
Myllys, L., Stenroos, S., Thell, A. & Ahti, T. (2003) Phylogeny of bipolar Cladonia arbuscula and Cladonia mitis (Lecanorales, Euascomycetes). Molecular Phylogenetics and Evolution 27: 58–69.Google Scholar
Orange, A., James, P.W. & White, F. J. (2001) Microchemical Methods for the Identification of Lichens. London: British Lichen Society.Google Scholar
Osyczka, P. (2009) Cladonia diversa (Cladoniaceae, lichenized Ascomycota) – overlooked lichen in Poland. Acta Societatis Botanicorum Poloniae 78: 215–219.CrossRefGoogle Scholar
Osyczka, P. (2011) The genus Cladonia, group Cocciferae, in Poland. Herzogia 24: 231–249.Google Scholar
Pérez-Ortega, S., Fernández-Mendoza, F., Raggio, J., Vivas, M., Ascaso, C., Sancho, L. G., Printzen, C. & de Los Ríos, A. (2012) Extreme phenotypic variation in Cetraria aculeata (lichenized Ascomycota): adaptation or incidental modification? Annals of Botany 109: 1133–1148.Google Scholar
Piercey-Normore, M. D., Ahti, T. & Goward, T. (2010) Phylogenetic and haplotype analyses of four segregates within Cladonia arbuscula s. l. Botany 88: 397–408.Google Scholar
Pino-Bodas, R., Rosa Burgaz, A. R. & Martin, M. P. (2010) Elucidating the taxonomic rank of Cladonia subulata versus C. rei (Cladoniaceae). Mycotaxon 113: 311–326.Google Scholar
Pino-Bodas, R., Martín, M. P. & Burgaz, A. R. (2012 a) Cladonia subturgida and C. iberica (Cladoniaceae) form a single, morphologically and chemically polymorphic species. Mycological Progress 11: 269–278.Google Scholar
Pino-Bodas, R., Rosa Burgaz, A. R., Martín, M. P. & Lumbsch, H. T. (2012 b) Species delimitations in the Cladonia cariosa group (Cladoniaceae, Ascomycota). Lichenologist 44: 121–135.Google Scholar
Pollard, D. A., Iyer, V. N., Moses, A. M. & Eisen, M. B. (2006) Widespread discordance of gene trees with species tree in Drosophila: evidence for incomplete lineage sorting. Plos Genetics 2: 1634–1647.Google Scholar
Ronquist, F. & Huelsenbeck, J. P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.CrossRefGoogle ScholarPubMed
Rot, C., Goldfarb, I., Ilan, M. & Huchon, D. (2006) Putative cross-kingdom horizontal gene transfer in sponge (Porifera) mitochondria. BMC Evolutionary Biology 6: 71.Google Scholar
Salminen, M., Carr, J., Burke, D. & Mccutchan, F. (1995) Identification of breakpoints in intergenotypic recombinants of HIV type-1 by bootscanning. AIDS Research and Human Retroviruses 11: 1423–1425.Google Scholar
Schmidt, H. A., Strimmer, K., Vingron, M. & von Haeseler, A. (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502–504.Google Scholar
Seehausen, O. (2004) Hybridization and adaptive radiation. Trends in Ecology & Evolution 19: 198–207.Google Scholar
Stenroos, S. (1989) Taxonomy of the Cladonia coccifera group 1. Annales Botanici Fennici 26: 157–168.Google Scholar
Stenroos, S., Vitikainen, O. & Koponen, T. (1994) Cladoniaceae, Peltigeraceae and other lichens from northwestern Sichuan, China. Journal of the Hattori Botanical Laboratory 75: 319–344.Google Scholar
Stenroos, S., Hyvonen, J., Myllys, L., Thell, A. & Ahti, T. (2002) Phylogeny of the genus Cladonia s.lat. (Cladoniaceae, Ascomycetes) inferred from molecular, morphological, and chemical data. Cladistics 18: 237–278.Google Scholar
Stenroos, S. K. & DePriest, P. T. (1998) SSU rDNA phylogeny of cladoniiform lichens. American Journal of Botany 85: 1548–1559.Google Scholar
Strimmer, K. & von Haeseler, A. (1997) Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proceedings of the National Academy of Sciences of the United States of America 94: 6815–6819.Google Scholar
Swofford, D. L. (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4. Sunderland, Massachusetts: Sinauer Associates.Google Scholar
Taylor, J. W., Jacobson, D. J., Kroken, S., Kasuga, T., Geiser, D. M., Hibbett, D. S. & Fisher, M. C. (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genetics and Biology 31: 21–32.Google Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25: 4876–4882.Google Scholar
Vanin, E. (1985) Processed pseudogenes – characteristics and evolution. Annual Review of Genetics 19: 253–272.Google Scholar
Verbruggen, H., Maggs, C. A., Saunders, G. W., Le Gall, L., Yoon, H. S. & De Clerck, O. (2010) Data mining approach identifies research priorities and data requirements for resolving the red algal tree of life. BMC Evolutionary Biology 10: 16.Google Scholar
Walter, A. E., Turner, D. H., Kim, J., Lyttle, M. H., Muller, P., Mathews, D. H. & Zuker, M. (1994) Coaxial stacking of helixes enhances binding of oligoribonucleotides and improves predictions of RNA folding. Proceedings of the National Academy of Sciences of the United States of America 91: 9218–9222.Google Scholar
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): 315–322. San Diego: Academic Press.Google Scholar
Won, H. & Renner, S. S. (2003) Horizontal gene transfer from flowering plants to Gnetum . Proceedings of the National Academy of Sciences of the United States of America 100: 10824–10829.Google Scholar
Xu, J., Vilgalys, R. & Mitchell, T. G. (2000) Multiple gene genealogies reveal recent dispersion and hybridization in the human pathogenic fungus Cryptococcus neoformans . Molecular Ecology 9: 1471–1481.Google Scholar
Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31: 3406–3415.Google Scholar