Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-10T22:00:19.120Z Has data issue: false hasContentIssue false
  • English
  • Français

Convergent evolution in Cladonia gracilis and allies

Published online by Cambridge University Press:  25 March 2010

Kyle M. FONTAINE ,
Teuvo AHTI  and
Michele D. PIERCEY-NORMORE
Kyle M. FONTAINE
Affiliation:
Department of Biological Sciences, University of Manitoba, Winnipeg, Manitoba, Canada, R3T 2N2. Email: pierceyn@cc.umanitoba.ca
Teuvo AHTI
Affiliation:
Botanical Museum, P. O. Box 7, FI-00014, Helsinki University, Finland.
Michele D. PIERCEY-NORMORE
Affiliation:
Department of Biological Sciences, University of Manitoba, Winnipeg, Manitoba, Canada, R3T 2N2. Email: pierceyn@cc.umanitoba.ca
Get access Rights & Permissions [Opens in a new window]

Abstract

Members of the Cladonia gracilis group of lichen fungi are common terrestrial lichens where morphological features are more similar between members of the C. gracilis species complex and allied species outside the complex than they are between subspecies within the complex. The objectives of this study were to examine whether the Cladonia gracilis species complex is monophyletic, to determine whether morphological similarity is supported by genetic variation, and to examine the utility of the polyketide synthase (PKS) gene for phylogenetic studies among closely related species. Two loci, the ketosynthase region of the PKS gene and the internal transcribed spacer (ITS) region of nuclear ribosomal DNA, were sequenced and analysed by Maximum Parsimony, Bayesian and haplotype network analyses. Functional differences were also inferred through ITS2 RNA secondary structures and non-synonymous changes in translated PKS amino acid sequences. The monophyly of the C. gracilis complex is supported by 71% bootstrap in the ITS phylogeny, and 92% bootstrap with greater than 95% posterior probability in the PKS phylogeny. Morphological similarity is not always supported by genetic similarity. The PKS gene is less variable than the ITS but the PKS supports species hypotheses that are reflected in the ITS2 RNA model. We conclude that monophyly of the C. gracilis complex can be supported if C. cornuta, C. coniocraea and C. ochrochlora are included in the complex. In addition, C. maxima, C. phyllophora and C. subchordalis are supported as monophyletic species outside the C. gracilis complex. Cladonia maxima may form a separate species and variation among podetial morphology may be explained by convergent evolution.

Keywords

Cladonia maximaCladonia phyllophoracompensatory base changesITS rDNA sequencesnon-synonymous substitutions, polyketide synthase gene
Type
Research Article
Information
The Lichenologist , Volume 42 , Issue 3 , May 2010 , pp. 323 - 338
Copyright
Copyright © British Lichen Society 2010

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. (1980) Taxonomic revision of Cladonia gracilis and its allies. Annales Botanica Fennici 17: 195–243.Google Scholar
Ahti, T. (2000) Cladoniaceae, Flora Neotropica Monograph 78. New York: The New York Botanical Garden.Google Scholar
Ahti, T., Parnmen, S. & Mongkolsuk, P. (2008) Three new species of Cladonia from Thailand. Sauteria 15: 15–19.Google Scholar
Armaleo, D. & Clerc, P. (1991) Lichen chimeras: DNA analysis suggests that one fungus forms two morphotypes. Experimental Mycology 15: 1–10.CrossRefGoogle Scholar
Bailey, R. H. (1966) Studies on the dispersal of lichen soredia. Journal of the Linnean Society, Botany 59: 479–490.CrossRefGoogle Scholar
Beard, K. H. & DePriest, P. T. (1996) Genetic variation within and among mats of the reindeer lichen, Cladina subtenuis. Lichenologist 28: 171–182.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Bingle, L. E. H., Simpson, T. J. & Lazarus, C. M. (1999) Ketosynthase domain probes identify two subclasses of fungal polyketide synthase genes. Fungal Genetics and Biology 26: 209–223.CrossRefGoogle ScholarPubMed
Brodie, H. J. (1951) The splash-cup dispersal mechanism in plants. Canadian Journal of Botany 29: 224–234.CrossRefGoogle Scholar
Castolloe, J. & Templeton, A. R. (1994) Root probabilities for intraspecific gene trees under neutral coalescent theory. Molecular Phylogenetics and Evolution 3: 102–113.CrossRefGoogle Scholar
Clement, M., Posada, D. & Crandall, K. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1660.CrossRefGoogle ScholarPubMed
Coleman, A. W. (2003) ITS2 is a double-edged tool for eukaryote evolutionary comparisons. Trends in Genetics 19: 370–375.CrossRefGoogle ScholarPubMed
Culberson, C. F. (1972) Improved conditions and new data for the identification of lichen products by a standardized thin-layer chromatographic method. Journal of Chromatography 72: 113–125.CrossRefGoogle ScholarPubMed
Culberson, C. F. (1986) Biogenetic relationships of the lichen substances in the framework of systematics. Bryologist 89: 91–98.CrossRefGoogle Scholar
Culberson, C. F. & Armaleo, D. (1992) Induction of a complete secondary-product pathway in a cultured lichen fungus. Experimental Mycology 16: 52–63.CrossRefGoogle Scholar
Culberson, C. F., Culberson, W. L. & Johnson, A. (1988) Gene flow in lichens. American Journal of Botany 75: 1135–1139.CrossRefGoogle Scholar
DePriest, P. T. (2004) Early molecular investigations of lichen-forming symbionts: 1986–2001. Annual Review of Microbiology 58: 273–301.CrossRefGoogle ScholarPubMed
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.CrossRefGoogle ScholarPubMed
Gowan, S. P. (1989) A character analysis of the secondary products of the Porpidiaceae (lichenized Ascomycotina). Systematic Botany 14: 77–90.CrossRefGoogle Scholar
Grube, M. & Blaha, J. (2003) On the phylogeny of some polyketide synthase genes in the lichenized genus Lecanora. Mycological Research 107: 1419–1426.CrossRefGoogle ScholarPubMed
Grube, M. & Hawksworth, D. L. (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., DePriest, P. T., Gargas, A. & Hafellner, J. (1995) DNA isolation from lichen ascomata. Mycological Research 99: 1321–1324.CrossRefGoogle Scholar
Guo, S. & Kashiwadani, H. (2004) Recent study on the phylogeny of the genus Cladonia (s. lat.) with the emphasis on the integrative biology. National Science Museum Monographs, Tokyo 24: 207–225.Google Scholar
Hawksworth, D. L. (1976) Lichen chemotaxonomy. In Lichenology: Progress and Problems (Brown, D. H., Hawksworth, D. L. & Bailey, R. H., eds): 139–184. London: Academic Press.Google Scholar
Hawksworth, D. L. & LaGreca, S. (2007) New bottles for old wine: fruit body types, phylogeny, and classification. Mycological Research 111: 999–1000.CrossRefGoogle ScholarPubMed
Hinds, J. W. & Hinds, P. L. (2007) The Macrolichens of New England. New York: New York Botanical Garden Press.Google Scholar
Huelsenbeck, J. P., Ronquist, F., Nielsen, R. & Bollback, J. P. (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294: 2310–2314.CrossRefGoogle ScholarPubMed
Hur, J. S., Wang, L. S., Oh, S. O., Kim, G. H., Lim, K. M., Jung, J. S. & Koh, Y. J. (2005) Highland macrolichen flora of northwestern Yunnan, China. The Journal of Microbiology 43: 228–236.Google ScholarPubMed
Hyvönen, J., Ahti, T., Stenroos, S. & Gowan, S. P. (1995) Genus Cladina and the section Unciales of the genus Cladonia (Cladoniaceae, lichenized Ascomycotina), a preliminary phylogenetic analysis. Journal of the Hattori Botanical Laboratory 78: 243–253.Google Scholar
Kearney, M. & Clark, J. M. (2003) Problems due to missing data in phylogenetic analyses including fossils: a critical review. Journal of Vertebrate Paleontology 23: 263–274.CrossRefGoogle Scholar
Keller, N. P. & Hohn, T. M. (1997) Metabolic pathway gene clusters in filamentous fungi. Fungal Genetics and Biology 21: 17–29.CrossRefGoogle ScholarPubMed
Kishino, H. & Hasagawa, M. (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. Journal of Molecular Evolution. 29: 170–179.CrossRefGoogle ScholarPubMed
Leuckert, C., Ahmadjian, V., Culberson, C. F. & Johnson, A. (1990) Xanthones and depsidones of the lichen Lecanora dispersa in nature and of its mycobiont in culture. Mycologia 82: 370–378.CrossRefGoogle Scholar
Müller, T., Philippi, N., Dandekar, T., Schultz, J. & Wolf, M. (2007) Distinguishing species. RNA 13: 1469–1472.CrossRefGoogle ScholarPubMed
Nakanishi, H. (2004) Splash seed dispersal by raindrops. Ecological Research 17: 663–671.CrossRefGoogle Scholar
Opanowicz, M., Blaha, J. & Grube, M. (2005) Detection of paralogous polyketide synthase genes in Parmeliaceae by specific primers. Lichenologist 38: 47–54.CrossRefGoogle Scholar
Piercey-Normore, M. D. & DePriest, P. T. (2001) Algal switching among lichen symbioses. American Journal of Botany 88: 1490–1498.CrossRefGoogle ScholarPubMed
Posada, D. & Crandall, K. A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818.CrossRefGoogle ScholarPubMed
Rambaut, A. (2001) Se-Al: Sequence Alignment Editor V2.0. Oxford: University of Oxford.Google Scholar
Reimer, J. D., Takishita, K., Ono, S., Maruyama, T. & Tsukahara, J. (2006) Latitudinal and intracolony ITS-rDNA sequence variation in the symbiotic dinoflagellate genus Symbiodinium (Dinophyceae) in Zoanthus sansibaricus (Anthozoa: Hexacorallia). Phycological Research 54: 122–132.CrossRefGoogle Scholar
Ronquist, F. & Huelsenbeck, J. P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.CrossRefGoogle ScholarPubMed
Schaschl, H., Kaulfus, D., Hammer, S. & Suchentrunk, F. (2003) Spatial patterns of mitochondrial and nuclear gene pools in chamois (Rupicarpra r. rupicapra) from the Eastern Alps. Heredity 91: 125–135.CrossRefGoogle ScholarPubMed
Schmitt, I., Martin, M. P., Kautz, S. & Lumbsch, H. T. (2005) Diversity of non-reducing polyketide synthase genes in the Pertusariales (lichenized Ascomycota): a phylogenetic perspective. Phytochemistry 66: 1241–1253.CrossRefGoogle ScholarPubMed
Schümann, J. & Hertwech, C. (2006) Advances in cloning, functional analysis and heterologous expression of fungal polyketide synthase genes. Journal of Biotechnology 124: 690–703.CrossRefGoogle ScholarPubMed
Shwab, E. K. & Keller, N. P. (2008) Regulation of secondary metabolite production in filamentous ascomycetes. Mycological Research 112: 225–230.CrossRefGoogle ScholarPubMed
Stenroos, S. K. & DePriest, P. T. (1998) SSU DNA phylogeny of cladoniiform lichens. American Journal of Botany 85: 1548–1559.CrossRefGoogle Scholar
Stenroos, S., Ahti, T. & Hyvönen, J. (1997) Phylogenetic analysis of the genera Cladonia and Cladina (Cladoniaceae, lichenized Ascomycota). Plant Systematics and Evolution 207: 43–58.CrossRefGoogle Scholar
Stenroos, S., Hyvönen, 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.CrossRefGoogle ScholarPubMed
Stocker-Wörgötter, E. (2001) Experimental studies of the lichen symbiosis: DNA-analyses, differentiation and secondary chemistry of selected mycobionts, artificial resynthesis of two- and tripartite symbioses. Symbiosis 30: 207–227.Google Scholar
Swofford, D. L. (2003) PAUP*: Phylogenetic Analysis Using Parsimony (* and Other Methods), Version 4.0., Sunderland, MA: Sinauer Associates.Google Scholar
Tibell, L. (1998) Crustose mazaediate lichens and the Mycocaliciaceae in temperate South America. Bibliotheca Lichenologica 71: 1–107.Google Scholar
Verseghy, K. (1965) Effect of dry periods on the spore production of lichens. Acta Biologica Hungarica 16: 85–104.Google 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): 315–322. New York: Academic Press, Inc.Google Scholar
Wiens, J. J. (2006) Missing data and the design of phylogenetic analyses. Journal of Biomedical Informatics 39: 34–42.CrossRefGoogle ScholarPubMed
Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31: 3406–3415.CrossRefGoogle ScholarPubMed