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The genus Endocena (Icmadophilaceae): DNA evidence suggests the same fungus forms different morphologies

Published online by Cambridge University Press:  24 July 2017

Alan M. FRYDAY ,
Imke SCHMITT  and
Sergio PÉREZ-ORTEGA
Alan M. FRYDAY
Affiliation:
Herbarium, Department of Plant Biology, Michigan State University, East Lansing, MI 48824-1312, USA. Email: [email protected]
Imke SCHMITT
Affiliation:
Senckenberg Biodiversity and Climate Research Centre (BiK-F), Senckenberganlage 25, D-60325 Frankfurt, Germany Institute of Ecology, Evolution and Diversity, Goethe Universität, Max-von-Laue-Str. 13, D-60438 Frankfurt, Germany
Sergio PÉREZ-ORTEGA
Affiliation:
Real Jardín Botánico de Madrid (RJB-CSIC), c/ Claudio Moyano 1, E-28014, Madrid, Spain
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Abstract

Numerous recent studies of lichenized fungi have uncovered hidden genetic diversity within a single phenotypic entity (so-called ‘cryptic species’). Here we report the opposite situation with vastly different morphologies apparently deriving from the same genotype. Endocena is a monotypic genus known only from southern South America. The single reported species, the terricolous E. informis, is morphologically variable; the type and other collections from the west coast of Chile being subfruticose, whereas specimens from further south and east are almost crustose in form. A sorediate terricolous lichen that is frequent on the Falkland Islands was confirmed by phylogenetic analysis of ITS rDNA and mtSSU rDNA sequences as being congeneric with E. informis and, surprisingly, both taxa were recovered as congeneric with the recently described genus and species Chirleja buckii, which is morphologically distinct from both E. informis and the sorediate taxon. Consequently, the genus Chirleja is included in the synonymy of Endocena and the new combination Endocena buckii is proposed. Because E. informis and the sorediate specimens have a similar thallus structure that differs radically from that of E. buckii, the name E. informis var. falklandica is proposed for the sorediate taxon. Poorly developed, incipient apothecia are also described from both varieties of E. informis, the first time that these have been reported for Endocena. We also report two lichenicolous fungi from E. informis var. informis, which are the first reports of lichenicolous fungi occurring on this genus.

Keywords

Chirlejalichenized fungilichensmolecular systematicsphenotypic plasticitysouthern South Americatypification
Type
Articles
Information
The Lichenologist , Volume 49 , Issue 4 , July 2017 , pp. 347 - 363
Copyright
© British Lichen Society, 2017 

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References

Al-Hatmi, A. M., Van Den Ende, A. G., Stielow, J. B., Van Diepeningen, A. D., Seifert, K. A., McCormick, W., Assabgui, R., Gräfenhan, T., De Hoog, G. S. & Levesque, C. A. (2016) Evaluation of two novel barcodes for species recognition of opportunistic pathogens in Fusarium . Fungal Biology 120: 231–245.CrossRefGoogle ScholarPubMed
AVH (2017) Australia’s Virtual Herbarium, Council of Heads of Australasian Herbaria. http://avh.chah.org.au; accessed 25 January 2017.Google Scholar
Calvelo, S. & Liberatore, S. (2002) Catálogo de los líquenes de la Argentina. Kurtziana 29: 7–170.Google Scholar
Cao, S., Wei, X., Zhou, Q. & Wei, J. (2013) Phyllobaeis crustacea sp. nov. from China. Mycotaxon 126: 31–36.CrossRefGoogle Scholar
Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17: 540–552.CrossRefGoogle ScholarPubMed
Crespo, A. & Pérez-Ortega, S. (2009) Cryptic species and species pairs in lichens: a discussion on the relationship between molecular phylogenetics and morphological characters. Anales del Jardín Botánico de Madrid 66S1: 71–81.CrossRefGoogle Scholar
Crombie, J. M. (1876) [1877] On the Lichens collected by Prof. R.O. Cunningham in the Falkland Islands, Fuegia, Patagonia and the Island of Chiloe during the voyage of H.M.S. Nassau 1867–1869. Journal of the Linnean Society 15: 222–234.Google Scholar
Cunningham, R. O. (1871) Notes of the Natural History of the Strait of Magellan and West Coast of Patagonia. Edinburgh: Edmonston & Douglas.Google Scholar
Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772.CrossRefGoogle ScholarPubMed
Filson, R. B. (1981) Studies on Macquarie Island lichens 1: general. Muelleria 4: 305–316.CrossRefGoogle Scholar
Fryday, A. M. & Coppins, B. J. (2007) A second species of Lithographa with submuriform ascospores. Lichenologist 39: 245–250.CrossRefGoogle Scholar
Fryday, A. M. & Prather, L. A. (2001) The lichen collection of Henry Imshaug at the Michigan State University Herbarium (MSC). Bryologist 104: 464–467.CrossRefGoogle 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.CrossRefGoogle Scholar
GBIF (2017) Endocena informis. Global Biodiversity Information Facility, GBIF Secretariat. http://www.gbif.org/species/3412462; accessed 25 January 2017.Google Scholar
Global Plants (2017 a) Endocena informis. JStor Global Plants, ITHAKA. http://plants.jstor.org/search?filter=name&so=ps_group_by_genus_species+asc&Query=Endocena; accessed 25 January 2017.Google Scholar
Global Plants (2017 b) Isotype of Endocena informis Cromb. [family ICMADOPHILACEAE]. JStor Global Plants, ITHAKA. http://plants.jstor.org/stable/10.5555/al.ap.specimen.bm001097291; accessed 25 January 2017.Google Scholar
Global Plants (2017 c) Isotype of Endocena informis Cromb. [family ICMADOPHILACEAE]. JStor Global Plants, ITHAKA. http://plants.jstor.org/stable/10.5555/al.ap.specimen.e00429965; accessed 25 January 2017.Google Scholar
Global Plants (2017 d) Isotype of Endocena informis Cromb. [family ICMADOPHILACEAE]. JStor Global Plants, ITHAKA. http://plants.jstor.org/stable/10.5555/al.ap.specimen.m0103214; accessed 25 January 2017.Google Scholar
Grassi, M. M. (1950) Contribucion al catalogo de liquenes argentinos, I. Lilloa 24: 5–296.Google Scholar
Grube, M. & Kantvilas, G. (2006) Siphula represents a remarkable case of morphological convergence in sterile lichens. Lichenologist 38: 241–249.CrossRefGoogle Scholar
Grube, M., Baloch, E. & Lumbsch, H. T. (2004) The phylogeny of Porinaceae (Ostropomycetidae) suggests a neotenic origin of perithecia in Lecanoromycetes. Mycological Research 108: 1111–1118.CrossRefGoogle ScholarPubMed
Huelsenbeck, J. P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.CrossRefGoogle ScholarPubMed
James, T. Y., Kauff, F., Schoch, C., Matheny, P. B., Hofstetter, V., Cox, C. J., Celio, G., Gueidan, C., Fraker, E., Miadlikowska, J. et al. (2006) Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443: 818–822.CrossRefGoogle ScholarPubMed
Kantvilas, G. & Seppelt, R. D. (1992?) The lichen flora of Macquarie Island: introduction and an annotated checklist of species . ANARE Research Notes 87: 1–20.Google Scholar
Kraichak, E., Lücking, R., Aptroot, A., Beck, A., Dornes, P., John, V., Lendemer, J. C., Nelsen, M. P., Neuwirth, G., Nutakki, A. et al. (2015) Hidden diversity in the morphologically variable script lichen (Graphis scripta) complex (Ascomycota, Ostropales, Graphidaceae). Organisms Diversity and Evolution 15: 447–458.CrossRefGoogle Scholar
Leavitt, S. D., Esslinger, T. L., Divakar, P. K., Crespo, A. & Lumbsch, H. T. (2016) Hidden diversity before our eyes: delimiting and describing cryptic lichen-forming fungal species in camouflage lichens (Parmeliaceae, Ascomycota). Fungal Biology 120: 1374–1391.CrossRefGoogle ScholarPubMed
Lendemer, J. C. & Hodkinson, B. P. (2012) Chirleja buckii, a new genus and species of lichenized fungi from Tierra del Fuego, southern South America. New Zealand Journal of Botany 50: 449–456.CrossRefGoogle Scholar
Lord, J. M., Knight, A., Bannister, J. M., Ludwig, L. R., Malcolm, W. M. & Orlovich, D. O. (2013) Rediscovery of pycnidia in Thamnolia vermicularis: implications for chemotype occurrence and distribution. Lichenologist 45: 397–411.CrossRefGoogle Scholar
Lowry, J. K., Horning, D. S., Poore, G. C. B. & Ricker, R. W. (1978) The Australian Museum Macquarie Island Expedition, Summer 1977–78. Sydney: Australian Museum Trust.Google Scholar
Lücking, R., Hodkinson, B. P. & Leavitt, S. D. (2016) The 2016 classification of lichenized fungi in the Ascomycota and Basidiomycota – approaching one thousand genera. Bryologist 119: 361–416.CrossRefGoogle Scholar
Ludwig, L. R. (2015) The reproductive ecology of Icmadophila splachnirima, including aspects of the reproduction in additional members of Icmadophilaceae. Ph.D. thesis, University of Otago. Online access via http://hdl.handle.net/10523/5824 Google Scholar
Lumbsch, H. T., Schmitt, I., Palice, Z., Wiklund, E., Ekman, S. & Wedin, M. (2004) Supraordinal phylogenetic relationships of Lecanoromycetes based on a Bayesian analysis of combined nuclear and mitochondrial sequences. Molecular Phylogenetics and Evolution 31: 822–832.CrossRefGoogle ScholarPubMed
Lutzoni, F., Kauff, F., Cox, C., McLaughlin, D., Celio, G., Dentinger, B., Padamsee, M., Hibbett, D., James, T. Y., Baloch, E. et al. (2004) Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. American Journal of Botany 91: 1446–1480.CrossRefGoogle ScholarPubMed
McNeill, J. (2014) Holotype specimens and type citations: general issues. Taxon 63: 1112–1113.CrossRefGoogle Scholar
McNeill, J., Barrie, F. R., Buck, W. R., Demoulin, V., Greuter, W., Hawksworth, D. L., Herendeen, P. S., Knapp, S., Marhold, K., Prado, J. et al. (2012) International Code of Nomenclature for Algae, Fungi, and Plants (Melbourne Code). Königstein: Koeltz Scientific Books.Google Scholar
Miadlikowska, 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.CrossRefGoogle ScholarPubMed
Miadlikowska, J., Kauff, F., Högnabba, F., Oliver, J. C., Molnár, K., Fraker, E., Gaya, E., Hafellner, J., Hofstetter, V., Gueidan, C. et al. (2014) A multigene phylogenetic synthesis for the class Lecanoromycetes (Ascomycota): 1307 fungi representing 1139 infrageneric taxa, 317 genera and 66 families. Molecular Phylogenetics and Evolution 79: 132–168.CrossRefGoogle ScholarPubMed
Núñez-Zapata, J., Divakar, P. K., Del-Prado, R., Cubas, P., Hawksworth, D. L. & Crespo, A. (2011) Conundrums in species concepts: the discovery of a new cryptic species segregated from Parmelina tiliacea (Ascomycota: Parmeliaceae). Lichenologist 43: 603–616.CrossRefGoogle Scholar
Ohmura, Y. (2011) Notes on eight threatened species of lichens in Japan. Bulletin of the National Museum of Nature and Science Series B 37 (2): 55–61.Google Scholar
Orange, A., James, P. W. & White, F. J. (2001) Microchemical Methods for the Identification of Lichens. London: British Lichen Society.Google Scholar
Platt, J. L. & Spatafora, J. W. (2000) Evolutionary relationships of nonsexual lichenized fungi: molecular phylogenetic hypotheses for the genera Siphula and Thamnolia from SSU and LSU rDNA. Mycologia 92: 475–487.CrossRefGoogle Scholar
RBGE (2017) Herbarium Catalogue. Royal Botanic Garden Edinburgh. http://data.rbge.org.uk/herb/E00429965; accessed 25 January 2017.Google Scholar
Resl, P., Schneider, K., Westberg, M., Printzen, C., Palice, Z., Thor, G., Fryday, A., Mayrhofer, H. & Spribille, T. (2015) Diagnostics for a troubled backbone: testing topological hypotheses of trapelioid lichenized fungi in a large-scale phylogeny of Ostropomycetidae (Lecanoromycetes). Fungal Diversity 73: 239–258.CrossRefGoogle Scholar
Samson, R. A., Visagie, C. M., Houbraken, J., Hong, S.-B., Hubka, V., Klaassen, C. H., Perrone, G., Seifert, K. A., Susca, A., Tanney, J. B. et al. (2014) Phylogeny, identification and nomenclature of the genus Aspergillus . Studies in Mycology 78: 141–173.CrossRefGoogle ScholarPubMed
Schmitt, I., Messuti, M. I., Feige, G. B. & Lumbsch, H. T. (2001) Molecular data support rejection of the generic concept in the Coccotremataceae (Ascomycota). Lichenologist 33: 315–321.CrossRefGoogle Scholar
Schmull, M., Miadlikowska, J., Pelzer, M., Stocker-Wörgötter, E., Hofstetter, V., Fraker, E., Hodkinson, B. P., Reeb, V., Kukwa, M., Lumbsch, H. T. et al. (2011) Phylogenetic affiliations of members of the heterogeneous lichen-forming fungi of the genus Lecidea sensu Zahlbruckner (Lecanoromycetes, Ascomycota). Mycologia 103: 983–1003.CrossRefGoogle ScholarPubMed
Schoch, C. L., Seifert, K. A., Huhndorf, S., Robert, V., Spouge, J. L., Levesque, C. A. & Chen, W., Fungal Barcoding Consortium (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences of the United States of America 109: 6241–6246.CrossRefGoogle ScholarPubMed
Seppelt, R. D. (1980) Bryophytes and lichens collected by the visit of Australian Museum personnel to Macquarie Island, summer 1977–78. Antarctic Division Technical Memorandum 94: 1–11.Google Scholar
Singh, G., Dal Grande, F., Divakar, P. K., Otte, J., Leavitt, S. D., Szczepanska, K., Crespo, A., Rico, V. J., Aptroot, A., Cáceres, M. E. S. et al. (2015) Coalescent-based species delimitation approach uncovers high cryptic diversity in the cosmopolitan lichen-forming fungal genus Protoparmelia (Lecanorales, Ascomycota). PLoS ONE 10: e0124625.CrossRefGoogle ScholarPubMed
Spribille, T., Resl, P., Ahti, T., Pérez-Ortega, S., Tønsberg, T., Mayrhofer, H. & Lumbsch, H. T. (2014) Molecular systematics of the wood-inhabiting, lichen-forming genus Xylographa (Baeomycetales, Ostropomycetidae) with eight new species. Acta Universitatis Upsaliensis, Symbolae Botanicae Upsalienses 37 : 1–87.Google ScholarPubMed
Spribille, T., Tuovinen, V., Resl, P., Vanderpool, D., Wolinski, H., Aime, M. C., Schneider, K., Stabentheiner, E., Toome-Heller, M., Thor, G. et al. (2016) Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353: 488–492.CrossRefGoogle ScholarPubMed
Stenroos, S., Myllys, L., Thell, A. & Hyvönen, J. (2002) Phylogenetic hypotheses: Cladoniaceae, Stereocaulaceae, Baeomycetaceae, and Icmadophilaceae revisited. Mycological Progress 1: 267–282.CrossRefGoogle Scholar
Sugiura, N. (2007) Further analysis of the data by Akaike’s information criterion and the finite corrections. Communications in Statistics-Theory and Methods 7: 13–26.CrossRefGoogle Scholar
U’Ren, J. M., Lutzoni, F., Miadlikowska, J., Laetsch, A. D. & Arnold, A. E. (2012) Host and geographic structure of endophytic and endolichenic fungi at a continental scale. American Journal of Botany 99: 898–914.CrossRefGoogle Scholar
U’Ren, J. M., Riddle, J. M., Monacell, J. T., Carbone, I., Miadlikowska, J. & Arnold, A. E. (2014) Tissue storage and primer selection influence pyrosequencing-based inferences of diversity and community composition of endolichenic and endophytic fungi. Molecular Ecology Resources 14 : 1032–1048.CrossRefGoogle ScholarPubMed
Vondrák, J., Říha, P., Arup, U. & Søchting, U. (2009) The taxonomy of the Caloplaca citrina group (Teloschistaceae) in the Black Sea region; with contributions to the cryptic species concept in lichenology. Lichenologist 41: 571–604.CrossRefGoogle Scholar
Wedin, M., Wiklund, E., Crewe, A., Döring, H., Ekman, S., Nyberg, Å., Schmitt, I. & Lumbsch, H. T. (2005) Phylogenetic relationships of Lecanoromycetes (Ascomycota) as revealed by analyses of mtSSU and nLSU rDNA sequence data. Mycological Research 109: 159–172.CrossRefGoogle ScholarPubMed
White, T. J., Bruns, T. D., Lee, S. B. & Taylor, J. W. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols: A Guide to Methods and Applications (M. A. Innis, D. H. Gelfand, J. J. Sninsky & T. J. White, eds): 315–322. New York: Academic Press.Google Scholar
Zahlbruckner, A. (1917) Botanische Ergebnisse der schwedischen Expedition nach Patagonien und dem Feuerlande 1907–1909. VI. Die Flechten. Kungliga Svenska Vetenskaps-Akademiens Handlingar, Stockholm 57: 1–62.Google Scholar
Zhou, S. & Stanosz, G. R. (2001) Primers for amplification of mtSSU rDNA, and a phylogenetic study of Botryosphaeria and associated anamorphic fungi. Mycological Research 105: 1033–1044.CrossRefGoogle Scholar
Zhurbenko, M. P. (2015) Sphaerellothecium siphulae (Dothideomycetes incertae sedis), a new lichenicolous fungus on Siphula ceratites from the Arctic. Nova Hedwigia 101: 419–425.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: 2049–2059.CrossRefGoogle ScholarPubMed