Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-27T09:32:57.308Z Has data issue: false hasContentIssue false
  • English
  • Français

Heterocyphelium leucampyx (Arthoniales, Ascomycota): another orphaned mazaediate lichen finds its way home

Published online by Cambridge University Press:  24 July 2017

Dries VAN DEN BROECK ,
Robert LÜCKING ,
Ester GAYA ,
José Luis CHAVES ,
Julius B. LEJJU  and
Damien ERTZ
Dries VAN DEN BROECK
Affiliation:
Botanic Garden Meise, Nieuwelaan 38, 1860 Meise, Belgium; and University of Antwerp, Groenenborgerlaan 171, 2020 Antwerp, Belgium. Email: dries.vandenbroeck@plantentuinmeise.be
Robert LÜCKING
Affiliation:
Botanischer Garten und Botanisches Museum Berlin-Dahlem, Freie Universität Berlin, Königin-Luise-Straße 6-8, 14195 Berlin, Germany
Ester GAYA
Affiliation:
Jodrell Laboratory, Royal Botanic Gardens, Kew, TW9 3DS, UK
José Luis CHAVES
Affiliation:
Laboratorio de Hongos, Instituto Nacional de Biodiversidad (INBio), Apdo. 22-3100, Santo Domingo de Heredia, Costa Rica
Julius B. LEJJU
Affiliation:
Faculty of Science, Mbarara University of Science & Technology, P.O. Box 1410, Mbarara, Uganda
Damien ERTZ
Affiliation:
Botanic Garden Meise, Nieuwelaan 38, 1860 Meise, Belgium; and Fédération Wallonie-Bruxelles, Direction Générale de l’Enseignement non obligatoire et de la Recherche Scientifique, Rue A. Lavallée 1, 1080 Bruxelles, Belgium
Get access Rights & Permissions [Opens in a new window]

Abstract

Heterocyphelium is a mazaediate genus containing a single species, H. leucampyx. The species was originally described from Cuba within the genus Trachylia (Arthoniales, Arthoniaceae) and later placed in various genera of the collective order Caliciales s. lat. For the past three decades, Heterocyphelium was considered an orphaned genus (incertae sedis) within the Ascomycota, since morphology alone could not resolve its systematic position. In this study, we added molecular data with the aim of resolving this uncertainty. Bayesian and maximum likelihood analyses of newly generated sequence data from the mitochondrial ribosomal RNA small subunit (mtSSU) and the RNA polymerase II second largest subunit gene (RPB2) provide clear evidence that Heterocyphelium leucampyx is nested within the order Arthoniales, in the family Lecanographaceae, sister to the genus Alyxoria. Heterocyphelium is a further example of parallel evolution of passive spore dispersal, prototunicate asci and the occurrence of a mazaedium in the Ascomycota, and another calicioid genus whose systematic placement could be eventually clarified by means of molecular data. Heterocyphelium is the fourth mazaediate genus in Arthoniales, in addition to Sporostigma, Tylophorella and Tylophoron.

Keywords

AlyxoriaCalicialesLecanographaceaemtSSUphylogenyRPB2
Type
Articles
Information
The Lichenologist , Volume 49 , Issue 4 , July 2017 , pp. 333 - 345
Copyright
© British Lichen Society, 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Acharius, E. (1808) Förteckning på de i Sverige växande arter af Lafvarnes familj. Kongliga Vetenskaps Academiens Nya Handlingar 29: 259–283.Google Scholar
Alfaro, M. E., Zoller, S. & Lutzoni, F. (2003) Bayes or bootstrap? A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Molecular Biology and Evolution 20: 255–266.Google Scholar
Aptroot, A. & Sparrius, L. B. (2013) Checklist of lichens of Thailand. http://www.tropicallichens.net/checklists/ Google Scholar
Balaji, P. & Hariharan, G. N. (2013) Checklist of microlichens in Bolampatti II Forest Range (Siruvani Hills), Western Ghats, Tamil Nadu, India. Czech Mycology 65: 219–232.Google Scholar
Binder, M. & Bresinsky, A. (2002) Derivation of a polymorphic lineage of Gasteromycetes from boletoid ancestors. Mycologia 94: 85–98.Google Scholar
Breinholt, J. W. & Kawahara, A. Y. (2013) Phylotranscriptomics: saturated third codon positions radically influence the estimation of trees based on next-gen data. Genome Biology and Evolution 5: 2082–2092.CrossRefGoogle ScholarPubMed
Bungartz, F., Yánez, A. & Nugra, F. (2013) Guía Rápida de Líquenes de las Islas Galápagos. Version 3. Puerto Ayora, Santa Cruz, Galápagos: Fundación Charles Darwin.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.Google Scholar
Dávalos, L. M. & Perkins, S. L. (2008) Saturation and base composition bias explain phylogenomic conflict in Plasmodium . Genomics 91: 433–442.Google Scholar
Elix, J. A. & McCarthy, P. M. (1998) Catalogue of the lichens of the smaller Pacific Islands. Bibliotheca Lichenologica 70: 1–361.Google Scholar
Eriksson, O. E. (1999) Outline of Ascomycota – 1999. Myconet 3: 1–88.Google Scholar
Ertz, D. & Tehler, A. (2011) The phylogeny of Arthoniales (Pezizomycotina) inferred from nucLSU and RPB2 sequences. Fungal Diversity 49: 47–71.Google Scholar
Ertz, D., Bungartz, F., Diederich, P. & Tibell, L. (2011) Molecular and morphological data place Blarneya in Tylophoron (Arthoniaceae). Lichenologist 43: 345–356.Google Scholar
Ertz, D., Tehler, A., Irestedt, M., Frisch, A., Thor, G. & van den Boom, P. (2015) A large-scale phylogenetic revision of Roccellaceae (Arthoniales) reveals eight new genera. Fungal Diversity 70: 31–53.CrossRefGoogle Scholar
Flakus, A., Sipman, H. J. M., Bach, K., Flakus, P. R., Knudsen, K., Ahti, T., Schiefelbein, U., Palice, Z., Jabłońska, A., Oset, M., et al. (2013) Contribution to the knowledge of the lichen biota of Bolivia. 5. Polish Botanical Journal 58: 697–733.Google Scholar
Fries, E. M. (1822) Lichenographia Europaea Reformata: Praemittuntur Lichenologiae Fundementa. Compendium in Theoreticum et Practicum Lichenum studium Conscripsit. Lundae: Mauritum.Google Scholar
Fries, E. M. & Sandberg, A. (1817) Lichenum Dianome Nova. Lund: Berlingiana.Google Scholar
Frisch, A., Thor, G., Ertz, D. & Grube, M. (2014) The Arthonialean challenge: restructuring Arthoniaceae . Taxon 63: 727–744.Google Scholar
Gaya, E., Högnabba, F., Holguin, Á., Molnar, K., Fernández-Brime, S., Stenroos, S., Arup, U., Søchting, U., van den Boom, P., Lücking, R., et al. (2012) Implementing a cumulative supermatrix approach for a comprehensive phylogenetic study of the Teloschistales (Pezizomycotina, Ascomycota). Molecular Phylogenetics and Evolution 63: 374–387.Google Scholar
Gray, S. F. (1821) A natural arrangement of British plants according to their relations to each other, as pointed out by Jussieu, De Candolle, Brown, & c. London: Baldwin, Cradock and Joy.Google Scholar
Grube, M. (2001) Sporostigma, a new calicioid genus in Arthoniales . Lichenologist 33: 387–391.CrossRefGoogle Scholar
Hansen, K., LoBuglio, K. F. & Pfister, D. H. (2005) Evolutionary relationships of the cup-fungus genus Peziza and Pezizaceae inferred from multiple nuclear genes: RPB2, beta-tubulin, and LSU rDNA. Molecular Phylogenetics and Evolution 36: 1–23.Google Scholar
Harris, R. C. (1990) Some Florida Lichens. Bronx, New York: Published by the author.Google Scholar
Henssen, A. & Jahns, H. M. (1973) Lichenes. Eine Einführung in die Flechtenkunde. Stuttgart: Georg Thieme.Google Scholar
Huelsenbeck, J. P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17: 754–755.Google Scholar
Jaklitsch, W., Baral, H. O., Lücking, R., Lumbsch, H. T. & Frey, W. (2016) Syllabus of Plant Families – A. Engler’s Syllabus der Pflanzenfamilien, Part 1/2: Ascomycota. 13th edition. Stuttgart: Bornträger.Google Scholar
Katoh, K., Misawa, K., Kuma, K. & Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30: 3059–3066.Google Scholar
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., et al. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649.Google Scholar
Krüger, D., Binder, M., Fischer, M. & Kreisel, H. (2001) The Lycoperdales. A molecular approach to the systematics of some gasteroid mushrooms. Mycologia 93: 947–957.Google Scholar
Liu, Y. J., Whelen, S. & Hall, B. D. (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Molecular Biology and Evolution 16: 1799–1808.Google Scholar
Lücking, R., Tehler, A., Bungartz, F., Rivas Plata, E. & Lumbsch, H. T. (2013) Journey from the West: did tropical Graphidaceae (lichenized Ascomycota: Ostropales) evolve from a saxicolous ancestor along the American Pacific coast? American Journal of Botany 100: 844–856.Google Scholar
Lumbsch, H. T. & Huhndorf, S. M. (2010) Myconet Volume 14. Part One. Outline of Ascomycota – 2009. Fieldiana Life and Earth Sciences 1: 1–42.Google Scholar
Lumbsch, H. T., Mangold, A., Lücking, R., Garciá, M. A. & Martín, M. P. (2004) Phylogenetic position of the genera Nadvornikia and Pyrgillus (Ascomycota) based on molecular data. Symbolae Botanicae Upsalienses 34: 9–17.Google Scholar
Lumbsch, H. T., Lücking, R. & Tibell, L. (2009) Molecular data place Tylophoron as an additional calicioid genus in the Arthoniales (Ascomycota). Bibliotheca Lichenologica 99: 287–298.Google Scholar
Lutzoni, F., Wagner, P., Reeb, V. & Zoller, S. (2000) Integrating ambiguously aligned regions of DNA sequences in phylogenetic analyses without violating positional homology. Systematic Biology 49: 628–651.Google Scholar
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.Google Scholar
Maddison, W. P. & Maddison, D. R. (2015) Mesquite: a modular system for evolutionary analysis. Version 3.04. Available from: http://mesquiteproject.org.Google Scholar
Mason-Gamer, R. J. & Kellogg, E. A. (1996) Testing for phylogenetic conflict among molecular data sets in the tribe Triticeae (Gramineae). Systematic Biology 45: 524–545.Google Scholar
Matheny, P. B., Curtis, J. M., Hofstetter, V., Aime, M. C., Moncalvo, J. M., Ge, Z. W., Yang, Z. L., Slot, J. C., Ammirati, J. F., Baroni, T. J., et al. (2006) Major clades of Agaricales: a multilocus phylogenetic overview. Mycologia 98: 982–995.Google Scholar
Medeiros, I. D., Kraichak, E., Lücking, R., Mangold, A. & Lumbsch, H. T. (2017) Assembling a taxonomic monograph of tribe Wirthiotremateae (lichenized Ascomycota: Ostropales: Graphidaceae). Fieldiana, Life and Earth Sciences 9: 1–31.Google Scholar
Miller, M. A., Pfeiffer, W. & 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. 1–8.Google Scholar
Müller, J. (1893) Lichenes exotici II. Hedwigia 32: 120–136.Google Scholar
Müller, J. (1894) Lichenes Eckfeldtiani. Bulletin de l’Herbier Boissier 2: 89–93.Google Scholar
Nannfeldt, J. A. (1932) Studien über die Morphologie und Systematik der nicht-lichenisierten inoperculaten Discomyceten. Nova Acta Regiae Societatis Scientiarum Upsaliensis 8: 1–368.Google Scholar
Nylander, W. (1862) Tylophoron et Parathelium genera lichenum nova. Botanische Zeitung (Berlin) 20: 278–279.Google Scholar
Poelt, J. (1973) Classification. In The Lichens (V. Ahmadjian & M. E. Hale, eds): 599–632. New York & London: Academic Press.Google Scholar
Prieto, M. & Wedin, M. (2016) Phylogeny, taxonomy and diversification events in the Caliciaceae. Fungal Diversity DOI 10.1007/s13225-016-0372-y.Google Scholar
Prieto, M., Baloch, E., Tehler, A. & Wedin, M. (2013) Mazaedium evolution in the Ascomycota (Fungi) and the classification of mazaediate groups of formerly unclear relationship. Cladistics 29: 296–308.Google Scholar
Rambaut, A. (2012) FigTree v1.3.1. Available from: http://tree.bio.ed.ac.uk/software/figtree/ Google Scholar
Rambaut, A., Suchard, M. A., Xie, W. & Drummond, A. J. (2013) Tracer v1.6.0. Available from: http://beast.bio.ed.ac.uk/ Google Scholar
Reeb, V., Lutzoni, F. & 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: 1036–1060.Google Scholar
Rivas Plata, E., Parnmen, S., Staiger, B., Mangold, A., Frisch, A., Weerakoon, G., Hernández, M. J. E., Cáceres, M. E. S., Kalb, K., Sipman, H. J. M., et al. (2013) A molecular phylogeny of Graphidaceae (Ascomycota: Lecanoromycetes: Ostropales) including 428 species. MycoKeys 6: 55–94.Google Scholar
Ronquist, F. & Huelsenbeck, J. P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.Google Scholar
Smith, A. L. (1911) A Monograph of the British Lichens. A Descriptive Catalogue of the Species in the Department of Botany, British Museum. London: Longmans & Co.Google Scholar
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.Google Scholar
Tehler, A., Baloch, E., Tibell, L. & Wedin, M. (2009) The systematic position of Schistophoron . Bibliotheca Lichenologica 99: 383–392.Google Scholar
Tibell, L. (1984) A reappraisal of the taxonomy of Caliciales . Beihefte zur Nova Hedwigia 79: 597–713.Google Scholar
Tibell, L. (1987) Australasian Caliciales . Symbolae Botanicae Upsaliensis 27: 1–279.Google Scholar
Tibell, L. (1996) Caliciales . Flora Neotropica 69: 1–78.Google Scholar
Tibell, L. (2001) A synopsis of crustose calicioid lichens and fungi from mainland Africa and Madagascar. Nordic Journal of Botany 20: 717–742.Google Scholar
Tuckerman, E. (1862) Observations on North American and other lichens. Proceedings of the American Academy of Arts and Sciences 5: 383–422.Google Scholar
Tuckerman, E. (1888) Synopsis of North American Lichens: Part II. Comprising the Lecideacei, and (in part) the Graphidacei. New Bedford, Massachusetts: E. Anthony & Sons.Google Scholar
Vainio, E. A. (1927) Lichenographia Fennica III. Coniocarpeae. Acta Societatis pro Fauna et Flora Fennica 57: 1–138.Google Scholar
Wedin, M., Döring, H., Nordin, A. & Tibell, L. (2000) Small subunit rDNA phylogeny shows the lichen families Caliciaceae and Physciaceae (Lecanorales, Ascomycotina) to form a monophyletic group. Canadian Journal of Botany 78: 246–254.Google Scholar
Wilson, A. W., Binder, M. & Hibbett, D. S. (2011) Effects of gasteroid fruiting body morphology on diversification rates in three independent clades of fungi estimated using binary state speciation and extinction analysis. Evolution 65: 1305–1322.Google Scholar
Zahlbruckner, A. (1903) Lichenes (Flechten). In: Die natürlichen Pflanzenfamilien. Teil 1, Abth. 1*:, B. Spezieller Teil. (A. Engler & K. Prantler, eds): 89–92. Leipzig: Wilhelm Engelmann.Google Scholar
Zahlbruckner, A. (1926) Lichenes. In Die Natürlichen Pflanzenfamilien 2nd ed., Vol.8: B. Spezieller Teil (A. Engler, ed.): 61–270. Leipzig: Borntraeger.Google Scholar
Zoller, S., Scheidegger, C. & Sperise, C. (1999) PCR primers for the amplification of mitochondrial small subunit ribosomal DNA of lichen-forming ascomycetes. Lichenologist 31: 511–516.Google Scholar