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Molecular phylogeny of the tropical lichen family Pyrenulaceae: contribution from dried herbarium specimens and FTA card samples

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An Erratum to this article was published on 21 January 2016

Abstract

The Pyrenulaceae is one of the most common lichen families in tropical rainforests. These mostly lichenised ascomycete fungi are relatively well known, as identification tools are available for many members of the family, including the most species-rich genus Pyrenula. However, despite the past boom in DNA sequence generation for most living organisms, molecular data are still mainly lacking for these crustose corticolous lichens, mainly because genomic DNA does not seem to preserve well after specimen desiccation. Because of lengthy customs procedures, newly collected specimens are therefore often too old for molecular work when they reach the laboratory. Here, a new method of DNA extraction and storage using FTA card samples was investigated. New DNA sequences were generated using both DNA extractions from freshly collected material (116 sequences) and FTA card samples (115 sequences) for 100 taxa within Pyrenulaceae. Inferences using three ribosomal genes (nuLSU, mtSSU and ITS) highlighted delimitation problems in few taxa, including the pantropical species P. mamillana and P. quassiicola. Issues related to generic delimitations were also confirmed, with Anthracothecium, Pyrgillus and Lithothelium nested within Pyrenula. Although further taxon and gene sampling will be required to fully revise species and generic concepts within this family, our data allowed us to describe two new species from Brazil (Lithothelium immersum and Pyrenula minutispora) and one from North America (Pyrenula reebiae).

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References

  • Aptroot A (1991) A monograph of the Pyrenulaceae (excluding Anthracothecium and Pyrenula) and the Requienellaceae, with notes on the Pleomassariaceae, the Trypetheliaceae and Mycomicrothelia (lichenized and non-lichenized ascomycetes). Bibl Lichenol 44:1–178

    Google Scholar 

  • Aptroot A (2009) Diversity and endemism in the pyrenocarpous lichen families Pyrenulaceae and Trypetheliaceae in the Malesian flora region. Blumea 54:145–147

    Article  Google Scholar 

  • Aptroot A (2012) A world key to the species of Anthracothecium and Pyrenula. Lichenologist 44:5–53

    Article  Google Scholar 

  • Aptroot A, Andrade DS, Mendonça C, Lima ELD, Cáceres MES (2015) Ten new species of corticolous pyrenocarpous lichens from NE Brazil. Phytotaxa 197:197–206

    Article  Google Scholar 

  • Aptroot A, Lücking R, Sipman HJM, Umaña L, Chaves JL (2008) Pyrenocarpous lichens with bitunicate asci. A first assessment of the lichen biodiversity inventory in Costa Rica. Bibl Lichenol 97:1–162

    Google Scholar 

  • Aptroot A, Sipman HJM, Cáceres MES (2013) Twenty-one new species of Pyrenula from South America, with a note on over-mature ascospores. Lichenologist 45:169–198

    Article  Google Scholar 

  • Becker S, Franco JR, Simarro PP, Stich A, Abel PM, Steverding D (2004) Real-time PCR for detecting Trypanosoma brucei in human blood samples. Diagn Microbiol Infect Dis 50:193–199

    Article  CAS  PubMed  Google Scholar 

  • Borman AM, Fraser M, Linton CJ, Palmer MD, Johnson EM (2010) An improved protocol for the preparation of total genomic DNA from isolates of yeast and mould using Whatman FTA filter papers. Mycopathologia 169:445–449

    Article  CAS  PubMed  Google Scholar 

  • Cáceres MES, Aptroot A, Nelsen MP, Lücking R (2013) Pyrenula sanguinea (lichenized Ascomycota: Pyrenulaceae), a new species with unique, trypethelioid ascomata and complex pigment chemistry. Bryologist 116:350–357

    Article  Google Scholar 

  • Cáceres MES, Lima ELD, Aptroot A, Lücking R (2014) Liquens brasileiros: novas descobertas evidenciam a riqueza no Norte e Nordeste do país. Bol Mus Biol Mello Leitão 35:101–119

    Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. doi:10.1038/nmeth.2109

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Del Prado R, Schmitt I, Kautz S, Palice Z, Lücking R, Lumbsch HT (2006) Molecular data place Trypetheliaceae in Dothideomycetes. Mycol Res 110:511–520

    Article  PubMed  Google Scholar 

  • Dentinger BTM, Margaritescu S, Moncalvo JM (2010) Rapid and reliable high-throughput methods of DNA extraction for use in barcoding and molecular systematics of mushrooms. Mol Ecol Resour 10:628–633

    Article  CAS  PubMed  Google Scholar 

  • Drescher A, Graner A (2002) PCR-genotyping of barley seedlings using DNA samples from tissue prints. Plant Breed 121:228–231

    Article  CAS  Google Scholar 

  • Geiser DM, Gueidan C, Miadlikowska J, Lutzoni F, Kauff F, Hofstetter V, Fraker E, Schoch C, Tibell L, Untereiner WA, Aptroot A (2006) Eurotiomycetes: Eurotiomycetidae and Chaetothyriomycetidae. Mycologia 98:1054–1065

    Article  Google Scholar 

  • Gueidan C, Roux C, Lutzoni F (2007) Using a multigene analysis to assess generic delineation and character evolution in the Verrucariaceae (Eurotiomycetes, Ascomycota). Mycol Res 111:1147–1170

    Article  Google Scholar 

  • Gueidan C, Villaseñor CR, de Hoog GS, Gorbushina A, Untereiner WA, Lutzoni F (2008) A rock-inhabiting ancestor for mutualistic and pathogen-rich fungal lineages. Stud Mycol 61:111–119

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gueidan C, Aptroot A, Cáceres MES, Badali H, Stenroos S (2014) A reappraisal of orders and families within the subclass Chaetothyriomycetidae (Eurotiomycetes, Ascomycota). Mycol Prog 13:1027–1039

    Article  Google Scholar 

  • 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 

  • Harris RC (1989) A sketch of the family Pyrenulaceae (Melanommatales) in eastern North America. Mem N Y Bot Gard 49:74–107

    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 the fungi using a six-gene phylogeny. Nature 443:818–822

    Article  CAS  PubMed  Google Scholar 

  • Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the fungi, 10th edn. CAB International, Wallingford

    Google Scholar 

  • Komposch H, Hafellner J (2002) Life form diversity of lichenized fungi in an Amazon lowland rainforest. Bibl Lichenol 82:311–326

    Google Scholar 

  • Lampel A, Orlandi PA, Kornegay L (2000) Improved template preparation for PCR based assays for detection of food bourne bacterial pathogens. Appl Environ Microbiol 66:4539–4542

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lampel KA, Dyer D, Kornegay L, Orlandi PA (2004) Detection of Bacillus spores using PCR and FTA Filters. J Food Prot 67:1036–1038

    CAS  PubMed  Google Scholar 

  • Lange DA, Penuela S, Denny RL, Mudge J, Concidido VC, Orf JH, Young ND (1998) A plant isolation protocol suitable for polymerase chain reaction based marker-assisted breeding. Crop Sci 138:217–220

    Article  Google Scholar 

  • Li CC, Beck IA, Seidel KD, Frenkel LM (2004) Persistence of human immunodeficiency virus type 1 subtype B DNA in dried blood on FTA filter paper. J Clin Microbiol 42:3847–3849

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lin JJ, Fleming R, Kuo J, Matthews BF, Saunders JA (2000) Detection of plant genes using a rapid, nonorganic DNA Purification method. Biotechniques 28:346–350

    CAS  PubMed  Google Scholar 

  • Lumbsch HT, Huhndorf SM (2007a) Whatever happened to the pyrenomycetes and loculoascomycetes? Mycol Res 111:1064–1074

    Article  PubMed  Google Scholar 

  • Lumbsch HT, Huhndorf SM (2007b) Outline of Ascomycota – 2007. Myconet 13:1–58

    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. Syst Biol 49:628–651

    Article  CAS  PubMed  Google Scholar 

  • Lutzoni F, Kauff F, Cox C, McLaughlin D, Celio G, Dentinger B, Padamsee M, Hibbett D, James T, Baloch E et al (2004) Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. Am J Bot 91:1446–1480

    Article  PubMed  Google Scholar 

  • Maddison WP, Maddison DR (2003) MacClade: analysis of phylogeny and character evolution. Version 4.6. Sinauer, Sunderland

    Google Scholar 

  • Mason-Gamer R, Kellogg E (1996) Testing for phylogenetic conflict among molecular datasets in the tribe Triticeae (Graminae). Syst Biol 45:524–545

    Article  Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans

  • Nelsen MP, Lücking R, Mbatchou JS, Andrew CJ, Spielmann AA, Lumbsch HT (2011) New insights into relationships of lichen-forming Dothideomycetes. Fungal Divers 51:155–162

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Parguey-Leduc A (1973) Recherches préliminaires sur l’ontogénie et l’anatomie comparée des ascocarpes des pyrénomycètes ascohyméniaux. VI. Conclusions générales. Rev Mycol 37:60–82

    Google Scholar 

  • Parguey-Leduc A, Janex-Favre MC (1981) The ascocarps of ascohymenial pyrenomycetes. In: Reynolds DR (ed) Ascomycete systematics. The Luttrellian concept. Springer, New York, pp 102–123

    Chapter  Google Scholar 

  • Rajendram D, Ayenza R, Holder FM, Moran B, Long T, Shah HN (2006) Long-term storage and safe retrieval of DNA from microorganisms for molecular analysis using FTA matrix cards. J Microbiol Methods 67:582–592

    Article  CAS  PubMed  Google Scholar 

  • Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. Available from http://beast.bio.ed.ac.uk/Tracer

  • Redchenko O, Vondrák J, Košnar J (2012) The oldest sequenced fungal herbarium sample. Lichenologist 44:715–718

    Article  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. Mol Phylogenet Evol 32:1036–1060

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres D, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2011) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  Google Scholar 

  • Schoch CL, Sung G-H, López-Giráldez F, Townsend JP, Miadlikowska J, Hofstetter V, Robbertse B, Matheny PB, Kauff F, Wang Z et al (2009) The ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst Biol 58:224–239

    Article  CAS  PubMed  Google Scholar 

  • Sipman HJM, Harris RC (1989) Lichens. In: Lieth H, Werger MJA (eds) Tropical rain forest ecosystems. Elsevier, Amsterdam, pp 303–309

    Chapter  Google Scholar 

  • Smith LM, Burgoyne LA (2004) Collecting, archiving and processing DNA from wildlife samples using FTA databasing paper. BMC Ecol 4:4. doi:10.1186/1472-6785-4-4

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sohrabi M, Myllys L, Stenroos S (2010) Successful DNA sequencing of a 75 year-old herbarium specimen of Aspicilia aschabadensis (J. Steiner) Mereschk. Lichenologist 42:626–628

    Article  Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 75:758–771

    Article  Google Scholar 

  • Stamatakis A, Ludwig T, Meier H (2005) A fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21:456–463

    Article  CAS  PubMed  Google Scholar 

  • Staiger B, Kalb K, Grube M (2006) Phylogeny and phenotypic variation in the lichen family Graphidaceae (Ostropomycetidae, Ascomycota). Mycol Res 110:765–772

    Article  CAS  PubMed  Google Scholar 

  • Swofford DL, Swofford DL (1999) PAUP*: phylogenetic analysis using parsimony (* and other methods) Version 4.0b10. Sinauer, Sunderland

    Google Scholar 

  • Thiers B (2015) Index herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available from http://sweetgum.nybg.org/ih/

  • Weerakoon G, Aptroot A, Lumbsch HT, Wolseley PA, Wijeyaratne SC, Gueidan C (2012) New molecular data on Pyrenulaceae from Sri Lanka reveal two well­supported groups within this family. Lichenologist 44:639–647

    Article  Google Scholar 

  • Zolan ME, Pukkila PJ (1986) Inheritance of DNA methylation in Coprinus cinereus. Mol Cell Biol 6:195–200

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The fieldwork in Vietnam was funded by a grant from the Natural History Museum (NHM) in London and organised in collaboration with the Vietnam National Museum of Nature (VNMN) in Hanoi. The MESC expedition to Brazil was financed by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-Rede Integrada de Plantas e Fungos, do Sisbiota Brasil). The CNPq is also thanked for a research grant to MESC (Processo 501633/2009-0). The molecular work was funded by the NHM. AA thanks the Stichting Hugo de Vries-Fonds for a travel grant. The authors would also like to thank the curatorial staff of ABL, BM, DUKE, ISE and VNMN for providing specimens and Thorsten Lumbsch for recommending the use of FTA cards at the Graphidaceae workshop in Thailand.

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  1. Cécile Gueidan

    Present address: National Facilities and Collections, National Research Collections Australia, Australian National Herbarium, CSIRO, P.O. Box 1600, Canberra, ACT, 2601, Australia

Authors and Affiliations

  1. Department of Life Sciences, Natural History Museum, Cromwell Road, SW7 5BD, London, UK

    Cécile Gueidan

  2. ABL Herbarium, Gerrit van der Veenstraat 107, NL-3762 XK, Soest, The Netherlands

    André Aptroot

  3. Departamento de Biociências, Universidade Federal de Sergipe, CEP: 49500-000, Itabaiana, Sergipe, Brazil

    Marcela Eugenia da Silva Cáceres

  4. Department of Biology, Vietnam Academy of Science and Technology, Vietnam National Museum of Nature, 18 Hoang Quoc Viet Street, Cau Giay, Hanoi, Vietnam

    Nguyen Quoc Binh

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  1. Cécile Gueidan
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  2. André Aptroot
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  3. Marcela Eugenia da Silva Cáceres
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  4. Nguyen Quoc Binh
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Correspondence to Cécile Gueidan.

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Gueidan, C., Aptroot, A., Cáceres, M.E.d.S. et al. Molecular phylogeny of the tropical lichen family Pyrenulaceae: contribution from dried herbarium specimens and FTA card samples. Mycol Progress 15, 7 (2016). https://doi.org/10.1007/s11557-015-1154-8

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