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Thelopsis challenges the generic circumscription in the Gyalectaceae and brings new insights to the taxonomy of Ramonia

Published online by Cambridge University Press:  12 March 2021

Damien Ertz*
Affiliation:
Meise Botanic Garden, Department Research, Nieuwelaan 38, 1860Meise, Belgium Fédération Wallonie-Bruxelles, Service général de l'Enseignement supérieur et de la Recherche scientifique, Rue A. Lavallée 1, 1080Bruxelles, Belgium
Neil Sanderson
Affiliation:
3 Green Close, Woodlands, Southampton, SO40 7HU, UK
Marc Lebouvier
Affiliation:
Université de Rennes, CNRS, EcoBio (Ecosystèmes, biodiversité, évolution) - UMR 6553, F-35000Rennes, France
*
Author for correspondence: Damien Ertz. E-mail: [email protected]

Abstract

The genus Thelopsis was classified in the family Stictidaceae but its systematic position has never been investigated by molecular methods. In order to determine its family placement and to test its monophyly, fungal DNA of recent collections of Thelopsis specimens was sequenced. Phylogenetic analyses using nuLSU, RPB2 and mtSSU sequences reveal that members of Thelopsis form a monophyletic group within the genus Gyalecta as currently accepted. The placement of Thelopsis, including the generic type T. rubella, within the genus Gyalecta challenges the generic circumscription of this group because Thelopsis is well recognized by the combination of morphological characters: perithecioid ascomata, well-developed periphysoids, polysporous asci and small, few-septate ellipsoid-oblong ascospores. The sterile sorediate Opegrapha corticola is also placed in the Gyalectaceae as sister species to Thelopsis byssoidea + T. rubella. Ascomata of O. corticola are illustrated for the first time and support its placement in the genus Thelopsis. The hypothesis that O. corticola might represent the sorediate fertile morph of T. rubella is not confirmed because the species is phylogenetically and morphologically distinct. Thelopsis is recovered as polyphyletic, with T. melathelia being placed as sister species to Ramonia. The new combinations Thelopsis corticola (Coppins & P. James) Sanderson & Ertz comb. nov. and Ramonia melathelia (Nyl.) Ertz comb. nov. are introduced and a new species of Gyalecta, G. amsterdamensis Ertz, is described from Amsterdam and Saint-Paul Islands, characterized by a sterile thallus with discrete soralia. Petractis luetkemuelleri and P. nodispora are accommodated in the new genus Neopetractis, differing from the generic type (P. clausa) by having a different phylogenetic position and a different photobiont. Francisrosea bicolor Ertz & Sanderson gen. & sp. nov. is described for a sterile sorediate lichen somewhat similar to Opegrapha corticola but having an isolated phylogenetic position as sister to a clade including Gyalidea praetermissa and the genera Neopetractis and Ramonia. Gyalecta farlowii, G. nidarosiensis and G. carneola are placed in a molecular phylogeny for the first time. The taxonomic significance of morphological characters in Gyalectaceae is discussed.

Type
Standard Papers
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of the British Lichen Society

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References

Aptroot, A and Schumm, F (2012) The genus Melanophloea, an example of convergent evolution towards polyspory. Lichenologist 44, 501509.CrossRefGoogle Scholar
Aptroot, A, Diederich, P, Sérusiaux, E and Sipman, HJM (1997) Lichens and lichenicolous fungi from New Guinea. Bibliotheca Lichenologica 64, 1220.Google Scholar
Aptroot, A, Van de Vijver, B, Lebouvier, M and Ertz, D (2011) Lichens of Ile Amsterdam and Ile Saint-Paul (TAAF, southern Indian Ocean). Nova Hedwigia 92, 343367.CrossRefGoogle Scholar
Aptroot, A, Mendonça, CO, Ferraro, LI and Cáceres, MES (2014 a) A world key to species of the genera Topelia and Thelopsis (Stictidaceae), with the description of three new species from Brazil and Argentina. Lichenologist 46, 801807.CrossRefGoogle Scholar
Aptroot, A, Parnmen, S, Lücking, R, Baloch, E, Jungbluth, P, Cáceres, MES and Lumbsch, HT (2014 b) Molecular phylogeny resolves a taxonomic misunderstanding and places Geisleria close to Absconditella s. str. (Ostropales: Stictidaceae). Lichenologist 46, 115128.Google Scholar
Baloch, E, Lücking, R, Lumbsch, HT and Wedin, M (2010) Major clades and phylogenetic relationships between lichenized and non-lichenized lineages in Ostropales (Ascomycota: Lecanoromycetes). Taxon 59, 14831494.CrossRefGoogle Scholar
Baloch, E, Gilenstam, G and Wedin, M (2013 a) The relationships of Odontotrema (Odontotremataceae) and the resurrected Sphaeropezia (Stictidaceae) – new combinations and three new Sphaeropezia species. Mycologia 105, 384397.CrossRefGoogle ScholarPubMed
Baloch, E, Lumbsch, HT, Lücking, R and Wedin, M (2013 b) New combinations and names in Gyalecta for former Belonia and Pachyphiale (Ascomycota, Ostropales) species. Lichenologist 45, 723727.CrossRefGoogle Scholar
Breuss, O and Schultz, M (2007) Thelopsis paucispora, a new lichen species from Socotra (Yemen). Lichenologist 39, 3540.CrossRefGoogle Scholar
Coppins, BJ and James, PW (1979) New or interesting British lichens IV. Lichenologist 11, 139179.CrossRefGoogle Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
Dou, M-Z, Wu, X-H, Li, M, Zhao, X and Jia, Z-F (2018) Gyalecta caudiospora sp. nov. from China. Mycotaxon 133, 721727.CrossRefGoogle Scholar
Egea, JM and Torrente, P (1996) Tres nuevas especies de hongos liquenizados de la Provincia del Cabo (Sudáfrica). Cryptogamie, Bryologie-Lichénologie 17, 305312.Google Scholar
Eriksson, OE (ed.) (1999) Outline of Ascomycota – 1999. Myconet 3, 188.Google Scholar
Eriksson, OE and Hawksworth, DL (1986) An alphabetical list of the generic names of Ascomycetes. Systema Ascomycetum 5, 3111.Google Scholar
Ertz, D, Tehler, A, Irestedt, M, Frisch, A, Thor, G and van den Boom, P (2015) A large-scale phylogenetic revision of Roccellaceae (Arthoniales) reveals eight new genera. Fungal Diversity 70, 3153.CrossRefGoogle Scholar
Ertz, D, Coppins, BJ and Sanderson, NA (2018 a) The British endemic Enterographa sorediata is the widespread Syncesia myrticola (Roccellaceae, Arthoniales). Lichenologist 50, 153160.CrossRefGoogle Scholar
Ertz, D, Sanderson, N, Łubek, A and Kukwa, M (2018 b) Two new species of Arthoniaceae from old-growth European forests, Arthonia thoriana and Inoderma sorediatum, and a new genus for Schismatomma niveum. Lichenologist 50, 161172.CrossRefGoogle Scholar
Ertz, D, Sanderson, N, Coppins, BJ, Klepsland, JT and Frisch, A (2019) Opegrapha multipuncta and Schismatomma quercicola (Arthoniomycetes) belong to the Lecanoromycetes. Lichenologist 51, 395405.CrossRefGoogle Scholar
Fernández-Brime, S, Llimona, X, Molnar, K, Stenroos, S, Högnabba, F, Björk, C, Lutzoni, F and Gaya, E (2011) Expansion of the Stictidaceae by the addition of the saxicolous lichen-forming genus Ingvariella. Mycologia 103, 755763.CrossRefGoogle ScholarPubMed
Fernández-Brime, S, Olariaga, I, Baral, H-O, Friebes, G, Jaklitsch, W, Senn-Irlet, B and Wedin, M (2018) Cryptodiscus muriformis and Schizoxylon gilenstamii, two new species of Stictidaceae (Ascomycota). Mycological Progress 17, 295305.CrossRefGoogle Scholar
Frisch, A, Kalb, K and Grube, M (2006) Contributions towards a new systematics of the lichen family Thelotremataceae. Bibliotheca Lichenologica 92, 1539.Google Scholar
Henssen, A (1976) Studies in the developmental morphology of lichenized Ascomycetes. In Brown, DH, Hawksworth, DL and Beiley, RH (eds), Lichenology: Progress and Problems. London: Academic Press, pp. 107138.Google Scholar
Huelsenbeck, JP and Ronquist, F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755.CrossRefGoogle ScholarPubMed
Jørgensen, PM and Vězda, A (1984) Topelia, a new Mediterranean lichen genus. Beiheft zur Nova Hedwigia 79, 501511.Google Scholar
Jørgensen, PM, Vězda, A and Botnen, A (1983) Clathroporina calcarea, a misunderstood lichen species, and a note on the genus Clathroporina in Europe. Lichenologist 15, 4555.CrossRefGoogle Scholar
Kauff, F and Büdel, B (2005) Ascoma ontogeny and apothecial anatomy in the Gyalectaceae (Ostropales, Ascomycota) support the re-establishment of the Coenogoniaceae. Bryologist 108, 272281.CrossRefGoogle Scholar
Kauff, F and 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, 138156.CrossRefGoogle ScholarPubMed
Katoh, K, Misawa, K, Kuma, K and Miyata, T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 30593066.CrossRefGoogle ScholarPubMed
Kistenich, S, Timdal, E, Bendiksby, M and Ekman, S (2018) Molecular systematics and character evolution in the lichen family Ramalinaceae (Ascomata: Lecanorales). Taxon 67, 871904.CrossRefGoogle Scholar
Kondratyuk, SY, Lökös, L, Halda, JP, Haji Moniri, M, Farkas, E, Park, JS, Lee, BG, Oh, S-O and Hur, J-S (2016 a) New and noteworthy lichen-forming and lichenicolous fungi 4. Acta Botanica Hungarica 58, 75136.CrossRefGoogle Scholar
Kondratyuk, SY, Lökös, L, Halda, JP, Upreti, DK, Mishra, GK, Haji Moniri, M, Farkas, E, Park, JS, Lee, BG, Liu, D, et al. (2016 b) New and noteworthy lichen-forming and lichenicolous fungi 5. Acta Botanica Hungarica 58, 319396.CrossRefGoogle Scholar
Kondratyuk, SY, Lökös, L, Halda, JP, Farkas, E, Upreti, DK, Thell, A, Woo, J-J, Oh, S-O and Hur, J-S (2018) New and noteworthy lichen-forming and lichenicolous fungi 7. Acta Botanica Hungarica 60, 115184.CrossRefGoogle Scholar
Kraichak, E, Huang, J-P, Nelsen, M, Leavitt, SD and Lumbsch, HT (2018) A revised classification of orders and families in the two major subclasses of Lecanoromycetes (Ascomycota) based on a temporal approach. Botanical Journal of the Linnean Society 188, 233249.Google Scholar
Liu, YJ, Whelen, S and Hall, BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Molecular Biology and Evolution 16, 17991808.CrossRefGoogle Scholar
Lücking, R (2019) Stop the abuse of time! Strict temporal banding is not the future of rank-based classifications in fungi (including lichens) and other organisms. Critical Reviews in Plant Sciences 38, 199253.CrossRefGoogle Scholar
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
Lücking, R, Moncada, B and Hawksworth, DL (2019) Gone with the wind: sequencing its type species supports inclusion of Cryptolechia in Gyalecta (Ostropales: Gyalectaceae). Lichenologist 51, 287299.CrossRefGoogle Scholar
Lumbsch, HT and Papong, K (2009) Ocellularia gyrostomoides belongs to the genus Schizoxylon (Stictidaceae, Ascomycota). Mycotaxon 109, 319322.CrossRefGoogle Scholar
Lumbsch, HT, Schmitt, I, Palice, Z, Wiklund, E, Ekman, S and Wedin, M (2004) Supraordinal phylogenetic relationships of Lecanoromycetes based on a Bayesian analysis of combined nuclear and mitochondrial sequences. Molecular Phylogenetics and Evolution 31, 822832.CrossRefGoogle ScholarPubMed
Lutzoni, F, Wagner, P, Reeb, V and Zoller, S (2000) Integrating ambiguously aligned regions of DNA sequences in phylogenetic analyses without violating positional homology. Systematic Biology 49, 628651.CrossRefGoogle ScholarPubMed
Lutzoni, F, Pagel, M and Reeb, V (2001) Major fungal lineages are derived from lichen symbiotic ancestors. Nature 411, 937940.CrossRefGoogle ScholarPubMed
Maddison, WP and Maddison, DR (2015) Mesquite: a modular system for evolutionary analysis, version 3.04. [WWW resource] URL http://mesquiteproject.org.Google Scholar
Mason-Gamer, RJ and Kellogg, EA (1996) Testing for phylogenetic conflict among molecular data sets in the tribe Triticeae (Gramineae). Systematic Biology 45, 524545.CrossRefGoogle Scholar
Miadlikowska, J, McCune, B and Lutzoni, F (2002) Pseudocyphellaria perpetua, a new lichen from western North America. Bryologist 105, 110.CrossRefGoogle Scholar
Miadlikowska, J, Kauff, F, Högnabba, F, Oliver, JC, 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, 132168.CrossRefGoogle ScholarPubMed
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, Louisiana, pp. 18.CrossRefGoogle Scholar
Moon, KH and Aptroot, A (2009) Pyrenocarpous lichens in Korea. Bibliotheca Lichenologica 99, 297314.Google Scholar
Navarro-Rosinés, P and Llimona, X (1997) Belonia mediterranea, a new calcicolous lichen species from Catalonia (NE Spain). Lichenologist 29, 1527.CrossRefGoogle Scholar
Orange (2009) A new species of Petractis (Ostropales s. lat., lichenized Ascomycota) from Wales. Lichenologist 41, 213221.CrossRefGoogle Scholar
Orange, A, James, PW and White, FJ (2010) Microchemical Methods for the Identification of Lichens. London: British Lichen Society.Google Scholar
Parnmen, S, Cáceres, MES, Lücking, R and Lumbsch, HT (2013) Myriochapsa and Nitidochapsa, two new genera in Graphidaceae (Ascomycota: Ostropales) for chroodiscoid species in the Ocellularia clade. Bryologist 116, 127133.CrossRefGoogle Scholar
Pentecost, A and James, PW (2009) Opegrapha Ach. (1809). In Smith, CW, Aptroot, A, Coppins, BJ, Fletcher, A, Gilbert, OL, James, PW and Wolseley, PA (eds), The Lichens of Great Britain and Ireland. London: British Lichen Society, pp. 631647.Google Scholar
Phukhamsakda, C, McKenzie, EHC, Phillips, AJL, Jones, EBG, Bhat, DJ, Marc, S, Bhunjun, CS, Wanasinghe, DN, Thongbai, B, Camporesi, E, et al. (2020) Microfungi associated with Clematis (Ranunculaceae) with an integrated approach to delimiting species boundaries. Fungal Diversity 102, 1203.CrossRefGoogle Scholar
Pino-Bodas, R, Zhurbenko, MP and Stenroos, S (2017) Phylogenetic placement within Lecanoromycetes of lichenicolous fungi associated with Cladonia and some other genera. Persoonia 39, 91117.CrossRefGoogle ScholarPubMed
Rambaut, A (2012) FigTree v.1.4.2. [WWW resource] URL http://tree.bio.ed.ac.uk/software/figtree/Google Scholar
Rambaut, A, Drummond, AJ, Xie, D, Baele, G and Suchard, MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901904.CrossRefGoogle ScholarPubMed
Reeb, V, Lutzoni, F and Roux, C (2004) Contribution of RPB2 to multilocus phylogenetic studies of the euascomycetes (Pezizomycotina, Fungi) with special emphasis on the lichen-forming Acarosporaceae and evolution of polyspory. Molecular Phylogenetics and Evolution 32, 10361060.CrossRefGoogle ScholarPubMed
Renobales, G, Barreno, E and Atienza, V (1996) Thelopsis foveolata, a new lichen from northern Spain. Lichenologist 28, 105111.CrossRefGoogle Scholar
Rivas, Plata E, Parnmen, S, Staiger, B, Mangold, A, Frisch, A, Weerakoon, G, Hernández, JE, Cáceres, MES, Kalb, K, Sipman, HJM, et al. (2013) A molecular phylogeny of Graphidaceae (Ascomycota, Lecanoromycetes, Ostropales) including 428 species. Mycokeys 6, 5594.Google Scholar
Ronquist, F and Huelsenbeck, JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.CrossRefGoogle ScholarPubMed
Rose, F, James, PW and Orange, A (2009) Thelopsis Nyl. (1855). In Smith, CW, Aptroot, A, Coppins, BJ, Fletcher, A, Gilbert, OL, James, PW and Wolseley, PA (eds), The Lichens of Great Britain and Ireland. London: British Lichen Society, pp. 889891.Google Scholar
Roux, C, Bauvet, C, Bricaud, O and Coste, C (2008) Gyalecta crozalsii (Gyalectaceae, Ostropales, Ascomycota), malbone konata specio. Sauteria 15, 421432.Google Scholar
Sherwood, MA (1977) The Ostropalean fungi. Mycotaxon 5, 1277.Google Scholar
Spribille, T, Fryday, AM, Pérez-Ortega, S, Svensson, M, Tønsberg, T, Ekman, S, Holien, H, Resl, P, Schneider, K, Stabentheiner, E, et al. (2020) Lichens and associated fungi from Glacier Bay National Park, Alaska. Lichenologist 52, 61181.CrossRefGoogle ScholarPubMed
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 13121313.CrossRefGoogle ScholarPubMed
van den Boom, PPG (2012) Additions and notes to the checklist of lichens and lichenicolous fungi of Cape Verde. Österreichische Zeitschrift für Pilzkunde 21, 516.Google Scholar
Vězda, A (1965) Flechtensystematische Studien I. Die Gattung Petractis Fr. Preslia (Praha) 37, 127143.Google Scholar
Vězda, A (1966) Flechtensystematische Studien III. Die Gattungen Ramonia Stiz. and Gloeolecta Lett. Folia Geobotanica et Phytotaxonomica 1, 154175.CrossRefGoogle Scholar
Vězda, A (1967) Flechtensystematische Studien V. Die Gattung Ramonia Stiz. Zusätze. Folia Geobotanica et Phytotaxonomica 2, 311317.CrossRefGoogle Scholar
Vězda, A (1968) Taxonomische Revision der Gattung Thelopsis Nyl. (Lichenisierte Fungi). Folia Geobotanica et Phytotaxonomica 3, 363406.CrossRefGoogle Scholar
Vězda, A, Øvstedal, DO and Smith, RIL (1992) Eine neue Gyalecta-Art aus der Antarctis: G. pezizoides sp. n. (lichenisierte Fungi, Gyalectaceae). Nova Hedwigia 55, 227229.Google 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, Döring, H, Könberg, K and Gilenstam, G (2005) Generic delimitations in the family Stictidaceae (Ostropales, Ascomycota): the Stictis–Conotrema problem. Lichenologist 37, 6775.CrossRefGoogle Scholar
Wedin, M, Döring, H and Gilenstam, G (2006) Stictis s. lat. (Ostropales, Ascomycota) in northern Scandinavia, with a key and notes on morphological variation in relation to lifestyle. Mycological Research 110, 773789.CrossRefGoogle ScholarPubMed
Yang, C, Baral, H-O, Xu, X and Liu, Y (2019) Parakarstenia phyllostachydis, a new genus and species of non-lichenized Odontotremataceae (Ostropales, Ascomycota). Mycological Progress 18, 833845.CrossRefGoogle Scholar
Zoller, S, Scheidegger, C and Sperisen, C (1999) PCR primers for the amplification of mitochondrial small subunit ribosomal DNA of lichen-forming ascomycetes. Lichenologist 31, 511516.CrossRefGoogle Scholar