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A molecular-genetic reassessment of the circumscription of the lichen genus Icmadophila

Published online by Cambridge University Press:  03 June 2020

Lars R. Ludwig
Affiliation:
Department of Botany, University of Otago, Dunedin, New Zealand
Gintaras Kantvilas
Affiliation:
Tasmanian Herbarium, Tasmanian Museum & Art Gallery, P.O. Box 5058, UTAS LPO, Sandy Bay, Tasmania7005, Australia
Andy R. Nilsen
Affiliation:
Department of Botany, University of Otago, Dunedin, New Zealand
David A. Orlovich
Affiliation:
Department of Botany, University of Otago, Dunedin, New Zealand
Yoshihito Ohmura
Affiliation:
Department of Botany, National Museum of Nature and Science, 4-1-1 Amakubo, Tsukuba, Ibaraki, 3050005, Japan
Tina C. Summerfield
Affiliation:
Department of Botany, University of Otago, Dunedin, New Zealand
Karina Wilk
Affiliation:
Department of Lichenology, W. Szafer Institute of Botany, Polish Academy of Sciences, Lubicz 46, PL-31-512, Kraków, Poland
Janice M. Lord*
Affiliation:
Department of Botany, University of Otago, Dunedin, New Zealand
*
Author for correspondence: Janice M. Lord. E-mail: janice.lord@otago.ac.nz

Abstract

The circumscription of the lichenized ascomycete genus Icmadophila Trevis. in the family Icmadophilaceae Triebel was investigated. Sequences of the internal transcribed spacer (ITS) region and large subunit of nuclear ribosomal DNA (nuLSU) were generated for the five Icmadophila species and additional members of Icmadophilaceae from the genera Dibaeis, Endocena, Knightiella, Siphula, Siphulella and Thamnolia. Phylogenetic analyses indicate that three Icmadophila species are closely related: the type, I. ericetorum (L.) Zahlbr., which is widespread in Eurasia and North America, I. aversa (Nyl.) Rambold & Hertel from Central and South America, and I. japonica (Zahlbr.) Rambold & Hertel, which is restricted to Far East Russia and Japan. The genus Knightiella Müll. Arg. is reinstated to accommodate I. splachnirima (Hook.f. & Taylor) D. J. Galloway emend. L. Ludw., which occurs in New Zealand and Australia. Two further species of Knightiella, K. eucalypti (Kantvilas) Kantvilas and K. queenslandica Kantvilas, are found to be unrelated to K. splachnirima, and are accommodated in two newly described genera, Knightiellastrum and Siphulopsis respectively. Knightiellastrum L. Ludw. & Kantvilas is characterized by a squamulose, erhizinate, whitish to pale grey thallus with a green, coccoid photobiont and by containing thamnolic acid. Siphulopsis Kantvilas & A. R. Nilsen is similarly characterized by an erhizinate, whitish to pale grey thallus, with a green, coccoid photobiont and containing thamnolic acid, but is instead fruticose. This study reveals considerable diversity within Australasian Icmadophilaceae; ongoing work in the Southern Hemisphere and tropical regions may reveal additional species in this family and clarify the relationships of these newly described genera.

Type
Standard Papers
Copyright
Copyright © British Lichen Society 2020

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References

Cao, S, Wei, X, Zhou, Q and Wei, J (2013) Phyllobaeis crustacea sp. nov. from China. Mycotaxon 126, 3136.10.5248/126.31CrossRefGoogle Scholar
Cubero, OF, Crespo, A, Fatehi, J and Bridge, PD (1999) DNA extraction and PCR amplification method suitable for fresh, herbarium-stored, lichenized, and other fungi. Plant Systematics and Evolution 216, 243249.10.1007/BF01084401CrossRefGoogle Scholar
Cubeta, MA, Echandi, E, Abernethy, T and Vilgalys, R (1991) Characterization of anastomosis groups of binucleate Rhizoctonia species using restriction analysis of an amplified ribosomal RNA gene. Phytopathology 81, 13951400.10.1094/Phyto-81-1395CrossRefGoogle Scholar
De Lange, PJ, Galloway, DJ, Blanchon, DJ, Knight, A, Rolfe, JR, Crowcroft, GM and Hitchmough, R (2012) Conservation status of New Zealand lichens. New Zealand Journal of Botany 50, 303363.10.1080/0028825X.2012.691426CrossRefGoogle Scholar
Doidge, EM (1950) The South African fungi and lichens to the end of 1945. Bothalia 5: 11094.Google Scholar
Drège, JF (1843) Zwei Pflanzengeographische Dokumente. III. Standörter-Verzeichnis der von J.F. Drège in Südafrika gesammelten Pflanzen. Flora (Regensburg) 26 (2, Besondere Beigabe), 44160.Google Scholar
Eriksson, OE (2005) Outline of Ascomycota – 2005. Myconet 11, 1113.Google Scholar
Eriksson, OE, Baral, H-O, Currah, RS, Hansen, K, Kurtzman, CP, Rambold, G and Laessøe, T (2003) Outline of Ascomycota – 2003. Myconet 9, 189.Google Scholar
Eriksson, OE, Baral, H-O, Currah, RS, Hansen, K, Kurtzman, CP, Rambold, G and Laessøe, T (2004) Outline of Ascomycota – 2004. Myconet 10, 199.Google Scholar
Fryday, AM, Schmitt, I and Pérez-Ortega, S (2017) The genus Endocena (Icmadophilaceae): DNA evidence suggests the same fungus forms different morphologies. Lichenologist 49, 347363.CrossRefGoogle Scholar
Galloway, DJ (1985) Flora of New Zealand Lichens. Wellington, New Zealand: P.D. Hasselberg.Google Scholar
Galloway, DJ (1992) Checklist of New Zealand Lichens. DSIR Land Resources Scientific Report, No. 26. Christchurch: DSIR Land Resources.Google Scholar
Galloway, DJ (2000) Knightiella belongs in Icmadophila (Helotiales: Icmadophilaceae). Lichenologist 32, 294297.10.1006/lich.1999.0260CrossRefGoogle Scholar
Galloway, DJ (2007) Flora of New Zealand Lichens. Revised Second Edition Including Lichen-Forming and Lichenicolous Fungi. Volumes 1 and 2. Lincoln, New Zealand: Manaaki Whenua Press.Google Scholar
Galloway, DJ (2008) Lichen biogeography. In Nash, TH III (ed.), Lichen Biology. Cambridge: Cambridge University Press, pp. 315335.10.1017/CBO9780511790478.017CrossRefGoogle Scholar
Gardes, M and Bruns, TD (1993) ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Molecular Ecology 2, 113118.10.1111/j.1365-294X.1993.tb00005.xCrossRefGoogle ScholarPubMed
Gierl, C and Kalb, K (1993) Die Flechtengattung Dibaeis. Eine Übersicht über die rosafrüchtigen Arten von Baeomyces sens. lat. nebst Anmerkungen zu Phyllobaeis gen. nov. Herzogia 9, 593645.Google Scholar
Grube, M and Kantvilas, G (2006) Siphula represents a remarkable case of morphological convergence in sterile lichens. Lichenologist 38, 241249.10.1017/S0024282906005500CrossRefGoogle Scholar
Guindon, S, Dufayard, JF, Lefort, V, Anisimova, M, Hordijk, W and Gascuel, O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307321.10.1093/sysbio/syq010CrossRefGoogle ScholarPubMed
Jaklitsch, W, Baral, H-O, Lücking, R and Lumbsch, HT (2016) Syllabus of Plant Families. Adolf Engler's Syllabus der Pflanzenfamilien. 13th edition by Wolfgang Frey. Part 1/2 Ascomycota. Stuttgart: Borntraeger Science Publishers.Google Scholar
James, TY, Kauff, F, Schoch, C, Matheny, PB, Hofstetter, V, Cox, CJ, Celio, G, Gueidan, C, Fraker, E, Miadlikowska, J, et al. (2006) Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443, 818822.CrossRefGoogle ScholarPubMed
Kantvilas, G (2018) A new species of Dibaeis from Australia (Tasmania), with notes on the family Icmadophilaceae. Herzogia 31, 562570.Google Scholar
Kantvilas, G and Elix, JA (2002) The taxonomy, chemistry and morphology of some South American species of Siphula [Die Taxonomie, Chemie und Morphologie von einigen südamerikanischen Arten der Gattung Siphula]. Herzogia 15, 112.Google Scholar
Kantvilas, G, Elix, JA and James, PW (1992) Siphulella, a new lichen genus from southwest Tasmania. Bryologist 95, 186191.CrossRefGoogle Scholar
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772780.10.1093/molbev/mst010CrossRefGoogle ScholarPubMed
Knight, A (2014) Lichens of New Zealand. An Introductory Illustrated Guide. Dunedin: Botanical Society of Otago.Google Scholar
Kroken, S and Taylor, JW (2001) A gene genealogical approach to recognize phylogenetic species boundaries in the lichenized fungus Letharia. Mycologia 93, 3853.CrossRefGoogle Scholar
Lanfear, R, Frandsen, PB, Wright, AM, Senfeld, T and Calcott, B (2017) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772773.Google ScholarPubMed
Lendemer, JC and Hodkinson, BP (2012) Chirleja buckii, a new genus and species of lichenized fungi from Tierra del Fuego, southern South America. New Zealand Journal of Botany 50, 449456.CrossRefGoogle Scholar
Lord, JM, Knight, A, Bannister, JM, Ludwig, LR, Malcolm, WM and Orlovich, DA (2013) Rediscovery of pycnidia in Thamnolia vermicularis: implications for chemotype occurrence and distribution. Lichenologist 45, 397411.CrossRefGoogle Scholar
Lücking, R, Dal-Forno, M, Sikaroodi, M, Gillevet, PM, Bungartz, F, Moncada, B, Yánez-Ayabaca, A, Chaves, JL, Coca, LF and Lawrey, JD (2014) A single macrolichen constitutes hundreds of unrecognized species. Proceedings of the National Academy of Sciences of the United States of America 111, 1109111096.10.1073/pnas.1403517111CrossRefGoogle ScholarPubMed
Lücking, R, Hodkinson, BP and Leavitt, SD (2017) The 2016 classification of lichenized fungi in the Ascomycota and Basidiomycota – approaching one thousand genera. Bryologist 119, 361416.CrossRefGoogle Scholar
Ludwig, LR (2011) Marginal soralia and conidiomata in Icmadophila splachnirima (Icmadophilaceae) from southern New Zealand. Australasian Lichenology 68, 411.Google Scholar
Ludwig, LR (2015) The reproductive ecology of Icmadophila splachnirima, including aspects of the reproduction in additional members of Icmadophilaceae. Ph.D. thesis, University of Otago.Google Scholar
Ludwig, LR (2016) The biogeography of Knightiella splachnirima. Australasian Lichenology 78, 4651.Google Scholar
Ludwig, LR, Knight, A and Kantvilas, G (2016) Discovery of ascomata in the Siphula decumbens group, and its placement in a separate genus. In Abstracts of the 8th International Association for Lichenology Symposium, 1–5 August 2016, Helsinki, Finland, p. 148.Google Scholar
Ludwig, LR, Summerfield, TC, Lord, JM and Singh, G (2017) Characterization of the mating-type locus (MAT) reveals a heterothallic mating system in Knightiella splachnirima. Lichenologist 49, 373385.CrossRefGoogle Scholar
Lumbsch, HT and Huhndorf, SM (2007) Outline of Ascomycota – 2007. Myconet 13, 158.Google Scholar
Lumbsch, HT and Huhndorf, SM (2010) Outline of Ascomycota – 2009. Myconet 14, 140.Google Scholar
Lumbsch, HT, Schmitt, I, Lücking, R, Wiklund, E and Wedin, M (2007) The phylogenetic placement of Ostropales within Lecanoromycetes (Ascomycota) revisited. Mycological Research 111, 257267.CrossRefGoogle ScholarPubMed
Lumbsch, HT, Ahti, T, Altermann, S, Amo de Paz, G, Aptroot, A, Arup, U, Bárcenas Peña, A, Bawingan, PA, Benatti, MN, Betancourt, L, et al. (2011) One hundred new species of lichenized fungi: a signature of undiscovered global diversity. Phytotaxa 18, 1127.CrossRefGoogle Scholar
McCarthy, PM (2016) Checklist of the Lichens of Australia and its Island Territories. Australian Biological Resources Study, Canberra. Version 22 January 2016. [WWW resource] URL http://www.anbg.gov.au/abrs/lichenlist/introduction.html.Google Scholar
Miadlikowska, J and Lutzoni, F (2004) Phylogenetic classification of Peltigeralean fungi (Peltigerales, Ascomycota) based on ribosomal RNA small and large subunits. American Journal of Botany 91, 449464.10.3732/ajb.91.3.449CrossRefGoogle ScholarPubMed
Miadlikowska, J, Kauff, F, Hofstetter, V, Fraker, E, Grube, M, Hafellner, J, Reeb, V, Hodkinson, BP, 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, 10881103.CrossRefGoogle ScholarPubMed
Moncalvo, JM, Rehner, SA and Vilgalys, R (1993) Systematics of Lyophyllum section Difformia based on evidence from culture studies and ribosomal DNA sequences. Mycologia 85, 788794.CrossRefGoogle Scholar
Nilsson, H, Tedersoo, L, Abarenkov, K, Ryberg, M, Kristiansson, E, Hartmann, M, Schoch, C, Nylander, J, Bergsten, J, Porter, T, et al. (2012) Five simple guidelines for establishing basic authenticity and reliability of newly generated fungal ITS sequences. MycoKeys 4, 3763.10.3897/mycokeys.4.3606CrossRefGoogle 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, 5561.Google Scholar
Pereira, I, Müller, F and Valderrama, A (2006) Diversity and distribution of bryophytes and lichens of El Colorado, Central Chile. Nova Hedwigia 83, 117127.CrossRefGoogle Scholar
Platt, JL and Spatafora, JW (2000) Evolutionary relationships of nonsexual lichenized fungi: molecular phylogenetic hypotheses for the genera Siphula and Thamnolia from SSU and LSU rDNA. Mycologia 92, 475487.10.1080/00275514.2000.12061183CrossRefGoogle Scholar
Rambaut, A (2014) FigTree: tree figure drawing tool. Version 1.4.2. [WWW resource] URL http://tree.bio.ed.ac.uk/software/figtree/Google Scholar
Rambold, G, Triebel, D and Hertel, H (1993) Icmadophilaceae, a new family in the Leotiales. Bibliotheca Lichenologica 53, 217240.Google Scholar
Resl, P, Schneider, K, Westberg, M, Printzen, C, Palice, Z, Thor, G, Fryday, A, Mayrhofer, H and 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, 239258.CrossRefGoogle Scholar
Ronquist, F and Huelsenbeck, JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.10.1093/bioinformatics/btg180CrossRefGoogle ScholarPubMed
Schmitt, I and Lumbsch, HT (2004) Molecular phylogeny of the Pertusariaceae supports secondary chemistry as an important systematic character set in lichen-forming ascomycetes. Molecular Phylogenetics and Evolution 33, 4355.CrossRefGoogle ScholarPubMed
Schmitt, I, Messuti, MI, Feige, GB and Lumbsch, HT (2001) Molecular data support rejection of the generic concept in the Coccotremataceae (Ascomycota). Lichenologist 33, 315321.CrossRefGoogle Scholar
Schmull, M, Miadlikowska, J, Pelzer, M, Stocker-Wörgötter, E, Hofstetter, V, Fraker, E, Hodkinson, BP, Reeb, V, Kukwa, M, Lumbsch, HT, et al. (2011) Phylogenetic affiliations of members of the heterogeneous lichen-forming fungi of the genus Lecidea sensu Zahlbruckner (Lecanoromycetes, Ascomycota). Mycologia 103, 9831003.10.3852/10-234CrossRefGoogle Scholar
Spribille, T, Resl, P, Ahti, T, Pérez-Ortega, S, Tønsberg, T, Mayrhofer, H and Lumbsch, HT (2014) Molecular systematics of the wood-inhabiting, lichen-forming genus Xylographa (Baeomycetales, Ostropomycetidae) with eight new species. Symbolae Botanicae Upsalienses 37, 187.Google ScholarPubMed
Stenroos, S, Myllys, L, Thell, A and Hyvönen, J (2002) Phylogenetic hypotheses: Cladoniaceae, Stereocaulaceae, Baeomycetaceae, and Icmadophilaceae revisited. Mycological Progress 1, 267282.CrossRefGoogle Scholar
Summerfield, TC (2003) Investigation of symbiont specificity in cyanolichens and differential gene expression in symbiotic Nostoc strain. Ph.D. thesis, University of Otago.Google Scholar
Swofford, DL (1991) PAUP: Phylogenetic Analysis Using Parsimony, Version 3.1. Computer program distributed by the Illinois Natural History Survey, Champaign, Illinois. [WWW resource] URL http://paup.csit.fsu.edu/Google Scholar
Tehler, A and Wedin, M (2008) Systematics of lichenized fungi. In Nash, TH III (ed.), Lichen Biology. Cambridge: Cambridge University Press, pp. 336352.10.1017/CBO9780511790478.018CrossRefGoogle Scholar
Vilgalys, R and Hester, M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172, 42384246.CrossRefGoogle ScholarPubMed
Wedin, M, Wiklund, E, Crewe, A, Döring, H, Ekman, S, Nyberg, Å, Schmitt, I and Lumbsch, HT (2005) Phylogenetic relationships of Lecanoromycetes (Ascomycota) as revealed by analyses of mtSSU and nLSU rDNA sequence data. Mycological Research 109, 159172.CrossRefGoogle ScholarPubMed
White, TJ, Bruns, T, Lee, S and Taylor, J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis, MA, Gelfand, DH, Sninsky, JJ and White, TJ (eds), PCR Protocols: A Guide to Methods and Applications. New York: Academic Press, pp. 315322.Google Scholar
Wilk, K (2010) Icmadophila aversa and Piccolia conspersa, two lichen species new to Bolivia. Polish Botanical Journal 55, 217221.Google Scholar
Ye, J, Ji, A, Parra, EJ, Zheng, X, Jiang, C, Zhao, X, Hu, L and Tu, Z (2004) A simple and efficient method for extracting DNA from old and burned bone. Journal of Forensic Sciences 49, 16.Google ScholarPubMed