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Towards a revised generic classification of lecanoroid lichens (Lecanoraceae, Ascomycota) based on molecular, morphological and chemical evidence

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Abstract

The phylogenetic relationship of lecanoroid lichens is studied using two data sets: 1) a 2-locus data set including 251 OTUs representing 150 species, and 2) a 6-locus data set with 82 OTUs representing 53 species. The genus Lecanora as currently circumscribed is shown to be highly polyphyletic and several genera, including Adelolecia, Arctopeltis, Bryonora, Carbonea, Frutidella, Lecidella, Miriquidica, Palicella, Protoparmeliopsis, Pyrrhospora, and Rhizoplaca are nested within Lecanora sensu lato. A core group of Lecanora is supported as monophyletic and includes species of the L. carpinea, L. rupicola, and L. subcarnea groups, and a core group of the L. subfusca group. Three monophyletic clades that are well supported in our analyses and well characterized by phenotypical characters are accepted here: 1) Myriolecis to accommodate the Lecanora dispersa group and Arctopeltis; 2) Protoparmeliopsis for the L. muralis group; and 3) Rhizoplaca is emended to include three placodioid taxa previously classified in Lecanora (L. novomexicana. L. opiniconensis, L. phaedrophthalma), whereas R. aspidophora and R. peltata are excluded from Rhizoplaca. The latter is transferred into Protoparmeliopsis. Lecidella is strongly supported as a monophyletic group. Our studies indicate the presence of additional clades of species currently placed in Lecanora sensu lato that warrant taxonomic recognition but additional data will be necessary before the circumscription of these entities is fully understood. 37 new combinations are proposed into the genera Myriolecis (30), Protoparmeliopsis (2), and Rhizoplaca (5).

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References

  • Arup U, Grube M (1998) Molecular systematics of Lecanora subgenus Placodium. Lichenologist 30:415–425

  • Arup U, Grube M (1999) Where does Lecanora demissa (Ascomycota, Lecanorales) belong? Lichenologist 31:419–430

  • Arup U, Grube M (2000) Is Rhizoplaca (Lecanorales, lichenized Ascomycota) a monophyletic genus? Can J Bot 78:318–327

  • Blanco O, Crespo A, Elix JA, Hawksworth DL, Lumbsch HT (2004) A molecular phylogeny and a new classification of parmelioid lichens containing Xanthoparmelia-type lichenan (Ascomycota: Lecanorales). Taxon 53:959–975

  • Brodo IM (1984) The north American species of the Lecanora subfusca group. Beiheft zur Nova Hedwigia 79:63–185

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    Article  CAS  PubMed  Google Scholar 

  • Choisy M (1929) Genres nouveaux pour la lichénologie dans le groupe des lecanoracées. Bulletin de la Societé Botanique de France 67:521–527

    Article  Google Scholar 

  • Choisy M (1949) Catalogue des lichens de la region lyonnaise. [fasc. 2]. Bulletin Mensuel de la Societe Linneenne de Lyon 18:137–152

    Google Scholar 

  • Clauzade G, Roux C (1984) Les genres Aspicilia massal. et Bellemerea hafellner et roux. Bulletin de la Societe botanique de centre-Ouest. Nouvelle Serie 15:127–141

  • Crespo A, Lumbsch HT, Mattsson JE, Blanco O, Divakar PK, Articus K, Wiklund E, Bawingan PA, Wedin M (2007) Testing morphology-based hypotheses of phylogenetic relationships in Parmeliaceae (Ascomycota) using three ribosomal markers and the nuclear RPB1 gene. Mol Phylogenet Evol 44:812–824

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) JModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dickhäuser A, Lumbsch HT, Feige GB (1995) A synopsis of the Lecanora subcarnea group. Mycotaxon 56:303–323

  • Döring H, Clerc P, Grube M, Wedin M (2000) Mycobiont-specific PCR primers for the amplification of nuclear ITS and LSU rDNA from lichenized ascomycetes. Lichenologist 32:200–204

  • Eigler G (1969) Studien zur Gliederung der Flechtengattung Lecanora. Dissertationes Botanicae 4:1–195

  • Ekman S (2001) Molecular phylogeny of the Bacidiaceae (Lecanorales, lichenized Ascomycota). Mycol Res 105:783–797

  • Ekman S, Wedin M (2000) The phylogeny of the families Lecanoraceae and Bacidiaceae (lichenized Ascomycota) inferred from nuclear SSU rDNA sequences. Plant Biol 2:350–360

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes--application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

  • Grube M, Blaha J (2003) On the phylogeny of some polyketide synthase genes in the lichenized genus Lecanora. Mycol Res 107:1419–1426

  • Grube M, Baloch E, Arup U (2004) A phylogenetic study of the Lecanora rupicola group (Lecanoraceae, Ascomycota). Mycol Res 108:506–514

  • Guderley R, Lumbsch HT, Elix JA (1998) Lecanora flavopallida, a species of Lecanora sensu stricto with almost biatorine apothecia (Lecanorales). Bryologist 101:103–108

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hafellner J (1984) Studien in Richtung einer natürlicheren Gliederung der Sammelfamilien Lecanoraceae und Lecideaceae. Beiheft zur Nova Hedwigia 79:241–371

  • Hafellner J, Türk R (2001) Die lichenisierten Pilze Österreichs - eine Checkliste der bisher nachgewiesenen Arten mit Verbreitungsangaben. Stapfia 76:1–167

  • Hafellner J, Obermayer S, Obermayer W (2005) Zur Diversität der Flechten und lichenicolen Pilze im Hochschwab-Massiv (Nordalpen, Steiermark). Mitt der NaturwissVer Steiermark 134:57–103

  • Hertel H (1969) Die Flechtengattung Trapelia Choisy. Herzogia 1:111–130

  • Hertel H (1970) Trapeliaceae–eine neue Flechtenfamilie. Vorträge aus dem Gesamtgebiet der Botanik. NF [Deutsch Bot Ges] 4:171–185

  • Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192

    Article  Google Scholar 

  • Högnabba F (2006) Molecular phylogeny of the genus Stereocaulon (Stereocaulaceae, lichenized Ascomycetes). Mycol Res 110:1080–1092

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

  • Imshaug IM, Brodo IM (1966) Biosystematic studies on Lecanora pallida and some related lichens in the Americas. Nova Hedwigia 12:1–59

  • Jaklitsch WM, Baral HO, Lücking R, Lumbsch HT (2015) Ascomycota. In: Frey W (ed) Syllabus of Plant families - Adolf Engler’s Syllabus der Pflanzenfamilien, vol 1/2, 13 edn. Gebr, Borntraeger Verlagsbuchhandlung, Stuttgart, p. 150

  • Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinformatics 9:286–298

    Article  CAS  PubMed  Google Scholar 

  • Katoh K, Asimenos G, Toh H (2009) Multiple alignment of DNA sequences with MAFFT. Methods Mol Biol 537:39–64

    Article  CAS  PubMed  Google Scholar 

  • Knoph J-G, Leuckert C (2000) Chemotaxonomische Studien in der Gattung Lecidella (Lecanorales, Lecanoraceae) III. Die gesteinsbewohnenden Arten mit farblosem Hypothecium unter besonderer Berücksichtigung von europäischem Material. Herzogia 14:1–26

  • Kondratyuk S, Lokös L, Tschabanenko S, Haji-Moniri M, Farkas E, Wang X, Oh SO, Hur JS (2013) New and noteworthy lichen-forming and lichenicolous fungi. Acta Bot Hung 55:275–349

    Article  Google Scholar 

  • Kondratyuk SY, Jeong MH, Galanina IA, Yakovchenko LS, Yatsyna AP, Hur JS (2014) Molecular phylogeny of placodioid lichen-forming fungi reveal a new genus, Sedelnikovaea. Mycotaxon 129:269–282. doi:10.5248/129.269

  • Larena I, Salazar O, González V, Julián MC, Rubio V (1999) Design of a primer for ribosomal DNA internal transcribed spacer with enhanced specificity for ascomycetes. J Biotechnol 75:187–194

  • Leavitt SD, Johnson LA, Goward T, St. Clair LL (2011) Species delimitation in taxonomically difficult lichen-forming fungi: an example from morphologically and chemically diverse Xanthoparmelia (Parmeliaceae) in North America. Mol Phylogenet Evol 60:317–332

  • Lendemer JC, Harris RC (2014) Studies in lichens and lichenicolous fungi – no. 19: further notes on species from the coastal plain of southeastern North America. Opuscula Philolichenum 13:155–176

    Google Scholar 

  • Lendemer JC, Hodkinson BP (2013) A radical shift in the taxonomy of Lepraria s.l.: molecular and morphological studies shed new light on the evolution of asexuality and lichen growth form diversification. Mycologia 105:994–1018. doi:10.3852/12-338

  • Leuckert C, Poelt J (1989) Studien über die Lecanora rupicola-Gruppe in Europa (Lecanoraceae). Nova Hedwigia 49:121–167

  • Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Mol Biol Evol 16:1799–1808

  • Lumbsch HT (1999) Biodiversität tropischer Gruppen der Flechtengattung Lecanora Ach. (Lecanorales, Ascomycota). Courier Forschungsinstitut Senckenberg 215:143–146

  • Lumbsch HT (2004) Lecanoraceae. In: McCarthy PM, Mallett Ke (eds) Flora of Australia. Volume 56A, Lichens 4. ABRS/CSIRO Australia, Melbourne, pp 11–12

  • Lumbsch HT, Elix JA (2004) Lecanora. Flora of Australia 56A:12–62

    Google Scholar 

  • Lumbsch HT, Huhndorf SM (2010) Myconet volume 14. Part one. Outline of Ascomycota - 2009. Fieldiana (Life and Earth Sciences) 1:1–42

  • Lumbsch HT, Feige GB, Elix JA (1995) A revision of the usnic acid containing taxa belonging to Lecanora sensu stricto (Lecanorales: lichenized Ascomycotina). Bryologist 98:561–577

  • Lumbsch HT, Guderley R, Elix JA (1996) A revision of some species in Lecanora sensu stricto with a dark hypothecium (Lecanorales, Ascomycotina). Bryologist 99:269–291

  • Lumbsch HT, Plümper M, Guderley R, Feige GB (1997) The corticolous species of Lecanora sensu stricto with pruinose apothecial discs. Symbolae Botanicae Upsalienses 32(1):131–161

  • Lumbsch HT, Schmitt I, Döring H, Wedin M (2001a) ITS sequence data suggest variability of ascus types and support ontogenetic characters as phylogenetic discriminators in the Agyriales (Ascomycota). Mycol Res 105:265–274

  • Lumbsch HT, Schmitt I, Döring H, Wedin M (2001b) Molecular systematics supports the recognition of an additional order of Ascomycota: the Agyriales. Mycol Res 105:16–23

  • Lumbsch HT, 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. Mol Phylogenet Evol 31:822–832

  • Lumbsch HT, Parnmen S, Rangsiruji A, Elix JA (2010) Phenotypic disparity and adaptive radiation in the genus Cladia (Lecanorales, Ascomycota). Aust Syst Bot 23:239–247. doi:10.1071/sb10010

  • Lumbsch HT, Parnmen S, Kraichak E, Papong K, Lücking R (2014) High frequency of character transformations is phylogenetically structured within the lichenized fungal family Graphidaceae (Ascomycota: Ostropales). Syst Biodivers 12:271–291

  • Mangold A, Martin MP, Lücking R, Lumbsch HT (2008) Molecular phylogeny suggests synonymy of Thelotremataceae within Graphidaceae (Ascomycota : Ostropales). Taxon 57:476–486

  • Matheny PB, Liu YJ, Ammirati JF, Hall BD (2002) Using RPB1 and RPB2 nucleotide sequences (Inocybe; Agaricales). American Journal of Botany 89:688–698

  • Miadlikowska J, Kauff F, Hofstetter V, Fraker E, Grube M, Hafellner J, Reeb V, Hodkinson BP, Kukwa M, Lücking R, Hestmark G, Otalora MG, Rauhut A, Budel B, Scheidegger C, Timdal E, Stenroos S, Brodo I, Perlmutter GB, Ertz D, Diederich P, Lendemer JC, May P, Schoch CL, Arnold AE, Gueidan C, Tripp E, Yahr R, Robertson C, Lutzoni F (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

  • Miadlikowska J, Kauff F, Högnabba F, Oliver JC, Molnár K, Fraker E, Gaya E, Hafellner J, Hofstetter V, Gueidan C, Kukwa M, Lücking R, Björk C, Sipman HJM, Burgaz AR, Thell A, Passo A, Myllys L, Goward T, Fernández-Brime S, Hestmark G, Lendemer J, Lumbsch HT, Schmull M, Schoch C, Sérusiaux E, Maddison D, Arnold AE, Lutzoni F, Stenroos S (2014) Multigene phylogenetic synthesis for 1307 fungi representing 1139 infrageneric taxa, 312 genera and 66 families of the class Lecanoromycetes (Ascomycota). Mol Phylogenet Evol 79:132–168

  • Nelsen MP, Lücking R, Aptroot A, Andrew CJ, Cáceres M, Rivas Plata E, Gueidan C, da Silva Canêz L, Knight A, Ludwig LR, Mercado Diaz J, Parnmen S, Lumbsch HT (2014) Elucidating phylogenetic relationships and genus-level classification within the fungal family Trypetheliaceae (Dothideomycetes: Ascomycota). Taxon 63:974–992

  • Nordin A, Savic S, Tibell L (2010) Phylogeny and taxonomy of Aspicilia and Megasporaceae. Mycologia 102:1339–1349. doi:10.3852/09-266

  • Nylander JAA, Wilgenbusch JC, Warren DL, Swofford DL (2008) AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24:581–583

  • Papong K, Boonpragob K, Parnmen S, Lumbsch HT (2013) Molecular phylogenetic studies on tropical species of Lecanora sensu stricto (Lecanoraceae, Ascomycota). Nova Hedwigia 96:1–13. doi:10.1127/0029-5035/2012/0072

  • Parnmen S, Lücking R, Lumbsch HT (2012) Phylogenetic classification at generic level in the absence of distinct phylogenetic patterns of phenotypical variation: a case study in Graphidaceae (Ascomycota). PLoS One 7(12):e51392. doi:10.1371/journal.pone.0051392

  • Pérez-Ortega S, Spribille T, Palice Z, Elix JA, Printzen C (2010) A molecular phylogeny of the Lecanora varia group, including a new species from western North America. Mycol Prog 9:523–535. doi:10.1007/s11557-010-0660-y

  • Printzen C (2001) Corticolous and lignicolous species of Lecanora (Lecanoraceae, Lecanorales) with usnic or isousnic acid in the sonoran desert region. Bryologist 104:382–409

  • Printzen C, May P (2002) Lecanora ramulicola (Lecanoraceae, Lecanorales), an overlooked lichen species from the Lecanora symmicta group. Bryologist 105:63–69

  • Rambaut A (2009) FigTree 1.2.2. http://tree.bio.ed.ac.uk/software/figtree/

  • 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 Divers 73:1–20. doi:10.1007/s13225-015-0332-y

  • Rodriguez Flakus P, Printzen C (2014) Palicella, a new genus of lichenized fungi and its phylogenetic position within Lecanoraceae. Lichenologist 46:535–552. doi:10.1017/s0024282914000127

  • Ryan BD, Nash III TH (1993a) Lecanora sect. Placodium (lichenized Ascomycotina) in North America. Cryptogam Bot 3:264–269

  • Ryan BD, Nash III TH (1993b) Lecanora section Placodium (lichenized Ascomycotina) in North America: new taxa in the L. garovaglii group. Bryologist 96:288–298

  • Ryan BD, Nash TH (1997a) Placodioid taxa of Lecanoraceae sensu Zahlbr. (lichenized ascomycotina) in North America: taxa excluded from Lecanora subg. Placodium. Nova Hedwigia 64:393–420

  • Ryan BD, Nash III TH (1997b) Systematics of Lecanora subgenus Placodium (lichenized ascomycotina) in North America: an overview, with keys. Nova Hedwigia 64:111–127

  • Santesson R, Moberg R, Nordin A, Tønsberg T, Vitikainen O (2004) Lichen-forming and lichenicolous fungi of Fennoscandia. Uppsala University, Uppsala, Sweden, Museum of Evolution

  • Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504

    Article  CAS  PubMed  Google Scholar 

  • Schmitt I, Crespo A, Divakar PK, Fankhauser J, Herman-Sackett E, Nelsen MP, Nelson NA, Rivas Plata E, Shimp AD, Widhelm T, Lumbsch HT (2009) New primers for single-copy protein-coding genes for fungal systematics. Persoonia - Molecular Phylogeny and Evolution of Fungi 23:35–40

  • Schmull M, Miadlikowska J, Pelzer M, Stocker-Woergoetter E, Hofstetter V, Fraker E, Hodkinson BP, Reeb V, Kukwa M, Lumbsch HT, Kauff F, Lutzoni F (2011) Phylogenetic affiliations of members of the heterogeneous lichen-forming fungi of the genus Lecidea sensu Zahlbruckner (Lecanoromycetes, Ascomycota). Mycologia 103:983–1003. doi:10.3852/10-234

  • Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116

    Article  CAS  Google Scholar 

  • Śliwa L (2007) A revision of the Lecanora dispersa complex in North America. Polish Botanical Journal 52:1–70

  • Śliwa L, Miadlikowska J, Redelings BD, Molnar K, Lutzoni F (2012) Are widespread morphospecies from the Lecanora dispersa group (lichen-forming Ascomycota) monophyletic? Bryologist 115:265–277. doi:10.1639/0007-2745-115.2.265

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Stenroos SK, DePriest PT (1998) SSU rDNA phylogeny of cladoniiform lichens. Am J Bot 85:1548–1559

    Article  CAS  PubMed  Google Scholar 

  • Stiller JW, Hall BD (1997) The origin of red algae: implications for plastid evolution. Proceedings of the National Academy of Sciences of the United States of America 94:4520–4525

  • Strimmer K, Rambaut A (2002) Inferring confidence sets of possibly misspecified gene trees. Proceedings of the Royal Society of London Series B, Biological Sciences 269:137–142. doi:10.1098/rspb.2001.1862

    Article  Google Scholar 

  • Tehler A, Irestedt M (2007) Parallel evolution of lichen growth forms in the family Roccellaceae (Arthoniales, Ascomycota). Cladistics 23:432–454

  • van den Boom PPG, Brand AM (2008) Some new Lecanora species from western and Central Europe, belonging to the L. saligna group, with notes on related species. Lichenologist 40:465–497. doi:10.1017/s0024282908007299

  • Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus  species. J Bacteriol 172:4238–4246

  • Wedin M, Döring H (1999) The phylogenetic relationship of the Sphaerophoraceae, Austropeltum and Neophyllis (lichenized Ascomycota) inferred by SSU rDNA sequences. Mycol Res 103:1131–1137

  • Zahlbruckner A (1907) Lichenes (Flechten). Spezieller Teil. In: Engler A, Prantl K (eds) Die natürlichen Pflanzenfamilien, vol 8. Wilhelm Engelmann, Leipzig, pp. 61–263

  • Zhou S, Stanosz GR (2001) Primers for amplification of mt SSU rDNA, and a phylogenetic study of Botryosphaeria and associated anamorphic fungi. Mycol Res 105:1033–1044

  • 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

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Acknowledgments

The project was financially supported by the National Natural Science Foundation of China (31170187, 31570017). We thank the China Scholarship Council for supporting the first author’s study at the Field Museum (Chicago). Jolanta Miadlikowska is thanked for kind assistance with transferring isolates (Duke University). SPO was supported by grant CTM2012-38222-C02-02 from the Spanish Ministry of Economy and Competitiveness.

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Zhao, X., Leavitt, S.D., Zhao, Z.T. et al. Towards a revised generic classification of lecanoroid lichens (Lecanoraceae, Ascomycota) based on molecular, morphological and chemical evidence. Fungal Diversity 78, 293–304 (2016). https://doi.org/10.1007/s13225-015-0354-5

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