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Reassessing evolutionary relationships in the filamentous cyanolichen genus Spilonema (Peltigerales, Lecanoromycetes)

Published online by Cambridge University Press:  12 May 2014

Toby SPRIBILLE ,
Tor TØNSBERG ,
Edith STABENTHEINER  and
Lucia MUGGIA
Toby SPRIBILLE
Affiliation:
Department of Biological Sciences, University of Montana, 32 Campus Drive, Missoula, MT 59812, USA; and Institute of Plant Sciences, University of Graz, Holteigasse 6, A-8010 Graz, Austria. Email: toby.spribille@mso.umt.edu
Tor TØNSBERG
Affiliation:
Museum of Natural History, University of Bergen, Allégaten 41, P. O. Box 7800, N-5020 Bergen, Norway
Edith STABENTHEINER
Affiliation:
Institute of Plant Sciences, University of Graz, Schubertstr. 51, A-8010 Graz, Austria
Lucia MUGGIA
Affiliation:
Institute of Plant Sciences, University of Graz, Holteigasse 6, A-8010 Graz, Austria; and Department of Life Sciences, University of Trieste, via Giorgieri 10, 34127 Trieste, Italy
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Abstract

Spilonema was originally described to accommodate an unusual group of cyanolichens with thread-like, cushion-forming thalli, and has long been placed in Coccocarpiaceae based on ascomatal development. However, Spilonema is the only genus of Peltigerales to include species lichenized with the cyanobacterial genus Stigonema, and the evolutionary relationships of Spilonema to other genera in the family have yet to be tested using molecular data. We present evidence from combined nuclear 28S, 18S and mitochondrial 12S rDNA to confirm the placement of the core species of Spilonema (S. paradoxum and S. revertens) in Coccocarpiaceae. Our data further show that despite possessing a different genus of photobiont (Scytonema), the north Pacific endemic genus Spilonemella must be included within Spilonema, suggesting that closely related species of the genus have changed photobionts in the course of evolution. However, we recovered Spilonema dendroides, one of the only lichens known to associate with the cyanobacterial genus Hyphomorpha, as only distantly related to the Coccocarpiaceae. The evolutionary relationships of this species are as yet unclear but it may occupy a basal position in the Peltigerales. We create for this species the new genus Erinacellus T. Sprib., Muggia & Tønsberg.

Keywords

body plancyanobacteriaErinacelluslichenizationphotobiontphylogenetics
Type
Articles
Information
The Lichenologist , Volume 46 , Issue 3 , May 2014 , pp. 373 - 388
Copyright
Copyright © British Lichen Society 2014 

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References

Bornet, E. (1856) Descriptions de trois lichens nouveaux. Mémoires de la Société Impériale des Sciences Naturelles de Cherbourg 4: 225–234.Google Scholar
Brodo, I. M. & Tønsberg, T. (1994) A new species of Micarea with stalked pycnidia from the west coast of North America. Acta Botanica Fennica 150: 1–4.Google Scholar
Buckley, P. T. R., Arensburger, C. S. & Chambers, G. K. (2002) Combined data, Bayesian phylogenetics, and the origin of the New Zealand Cicada genera. Systematic Biology 51: 4–18.CrossRefGoogle ScholarPubMed
Cubero, O. F., Crespo, A., Fatehi, J. & Bridge, P. D. (1999) DNA extraction and PCR amplification method suitable for fresh, herbarium stored and lichenized fungi. Plant Systematics and Evolution 217: 243–249.Google Scholar
Eriksson, O. & Hawksworth, D. L. (1986) Outline of the Ascomycetes—1986. Systema Ascomycetum 5: 185–324.Google Scholar
Fries, E. (1825) Systema Orbis Vegetabilis. Primas lineas novae constrictionis periclitatur Elias Fries. Pars I. Plantae homonemeae. Lundae.: e typographia Academica.Google Scholar
Gardes, M. & Bruns, T. D. (1993) ITS primers with enhanced specificity for basidiomycetes. Application for the identification of mycorrhizae and rust. Molecular Ecology 2: 113–118.CrossRefGoogle Scholar
Gargas, A. & Taylor, J. W. (1992) Polymerase chain reaction (PCR) primers for amplifying and sequencing nuclear 18S rDNA from lichenized fungi. Mycologia 84: 589–592.Google Scholar
Goward, T. (1999) The lichens of British Columbia. Illustrated keys. Part 2—Fruticose species. British Columbia Ministry of Forest Research Program Special Report 9: 1–319.Google Scholar
Hall, T. A. (1999) BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symposium Series 41: 95–98.Google Scholar
Henssen, A. (1963) Eine Revision der Flechtenfamilien Lichinaceae und Ephebaceae . Symbolae Botanicae Upsalienses 18(1): 1–123.Google Scholar
Henssen, A. (1981) Hyphomorpha als Phycobiont in Flechten. Plant Systematics and Evolution 137: 139–143.Google Scholar
Henssen, A. & Jahns, H. M. (1973) [‘1974’] Lichenes. Stuttgart: Georg Thieme Verlag.Google Scholar
Henssen, A. & Tønsberg, T. (2000) Spilonemella, a new genus of cyanophilic lichens with species from North America and Japan (Coccocarpiaceae). Bryologist 103: 108–116.CrossRefGoogle Scholar
Henssen, A., Keuck, G., Renner, B. & Vobis, G. (1981) The Lecanoralean centrum. In Ascomycete Systematics: The Luttrellian Concept (Reynolds, D. R., ed.): 138–234. New York, Heidelberg, Berlin: Springer-Verlag.Google Scholar
Huelsenbeck, J. P. & Ronquist, F. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.Google Scholar
Kauff, F. & Lutzoni, F. (2002) Phylogeny of the Gyalectales and Ostropales (Ascomycota, Fungi): among and within order relationships based on nuclear ribosomal RNA small and large subunits. Molecular Phylogenetics and Evolution 25: 138–156.Google Scholar
Kershaw, K. A. (1985) Physiological Ecology of Lichens. Cambridge: Cambridge University Press.Google Scholar
Keuck, G. (1977) Ontogenetisch-systematische Studie über Erioderma . Bibliotheca Lichenologica 6: 1–175.Google Scholar
Miądlikowska, J. & Lutzoni, F. (2004) Phylogenetic classification of Peltigeralean fungi (Peltigerales, Ascomycota) based on ribosomal RNA small and large subunits. American Journal of Botany 91: 449–464.Google Scholar
Miądlikowska, J., Kauff, F., Hofstetter, V., Fraker, E., Grube, M., Hafellner, J., Reeb, V., Hodkinson, B. P., Kukwa, M., Lücking, R., et al. (2006) New insights into classification and evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota) from phylogenetic analyses of three ribosomal RNA- and two protein-coding genes. Mycologia 98: 1088–1103.Google Scholar
Muggia, L., Gueidan, C. & Grube, M. (2010) Phylogenetic placement of some morphologically unusual members of Verrucariales . Mycologia 102: 835–846.CrossRefGoogle ScholarPubMed
Muggia, L., Nelson, P., Wheeler, T., Yakovchenko, L. S., Tønsberg, T. & Spribille, T. (2011) Convergent evolution of a symbiotic duet: the case of the lichen genus Polychidium (Peltigerales, Ascomycota). American Journal of Botany 98: 1647–1656.Google Scholar
Nylander, W. (1865) Addenda nova ad Lichenographiam europaeam. Flora (Regensburg) 48: 601–606.Google Scholar
Otálora, M. & Wedin, M. (2013) Collema fasciculare belongs in Arctomiaceae . Lichenologist 45: 295–304.Google 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 Scholar
Rambaut, A. & Drummond, A. (2007) Tracer v1.4. Available from: beast.bio.ed.ac.uk/Tracer Google Scholar
Rodriguez, F., Oliver, J. L., Marin, A. & Medina, J. R. (1990) The general stochastic model of nucleotide substitution. Journal of Theoretical Biology 142: 485–501.Google Scholar
Ronquist, F., Huelsenbeck, J. P. & van der Mark, P. (2005) MrBayes 3.1 Manual. Available from: http://mrbayes.csit.fsu.edu/mb3.1_manual.pdf.Google Scholar
Spribille, T. & Muggia, L. (2013) Expanded taxon sampling disentangles evolutionary relationships and reveals a new family in Peltigerales (Lecanoromycetidae, Ascomycota). Fungal Diversity 58: 171–184.Google Scholar
Stabentheiner, E., Zankel, A. & Pölt, P. (2010) Environmental scanning electron microscopy (ESEM)—a versatile tool in studying plants. Protoplasma 246: 89–99.Google Scholar
Stamatakis, A., Ludwig, T. & Meier, H. (2005) RAxML-iii: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21: 456–463.Google Scholar
Vilgalys, R. & Hester, M. (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172: 4238–4246.Google Scholar
Wedin, M., Jørgensen, P. M. & Wiklund, E. (2007) Massalongiaceae fam. nov., an overlooked monophyletic group among the cyanobacterial lichens (Peltigerales, Lecanoromycetes, Ascomycota). Lichenologist 39: 61–67.Google Scholar
Wedin, M., Wiklund, E., Jørgensen, P. M. & Ekman, S. (2009) Slippery when wet: phylogeny and character evolution in the gelatinous cyanobacterial lichens (Peltigerales, Ascomycetes). Molecular Phylogenetics and Evolution 53: 862–871.Google Scholar
Wedin, M., Jørgensen, P. M. & Ekman, S. (2011) Vahliellaceae, a new family of cyanobacterial lichens (Peltigerales, Ascomycetes). Lichenologist 43: 67–72.CrossRefGoogle 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