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Phylogenetic placement of lichenicolous Phoma species in the Phaeosphaeriaceae (Pleosporales, Dothideomycetes)

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Abstract

More than twenty species of lichenicolous fungi have been described in Phoma, a large anamorphic genus of primarily plant-associated pathogens with broad geographic distributions. We obtained nuclear and mitochondrial rDNA sequences from 19 fungal cultures isolated from specimens representing four described and two undescribed lichenicolous species in the genus. Our multilocus phylogeny indicates that lichenicolous Phoma species represent at least two phylogenetically distinct clades in the Phaeosphaeriaceae, one including a new species, Phoma puncteliae, isolated from a specimen of Punctelia rudecta collected in Maryland, USA, and another group of primarily lichenicolous species. This latter group includes four described lichenicolous Phoma species, an unidentified melanized rock fungus, and a new lichenicolous Phoma species isolated from Xanthomendoza species collected in Canada that we are naming P. xanthomendozae. Some specimens in this clade collected from different lichen genera and species were found to be very similar genetically, which calls into question the recent practice of recognizing lichenicolous Phoma species mainly by differences in host preference.

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References

  • Alstrup V, Kocourková J, Kukwa M, Motiejūnaitė J, Brackel W von, Suija A (2009) The lichens and lichenicolous fungi of South Greenland. Folia Cryptogamica Estonica 46:1–24

    Google Scholar 

  • Arnold AE, Miadlikowska J, Higgins KL, Sarvate SD, Gugger P, Way A, Hofstetter V, Kauff F, Lutzoni F (2009) A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic diversification? Systematic Biology 58:283–297

    Article  PubMed  Google Scholar 

  • Aveskamp MM, de Gruyter J, Crous PW (2008) Biology and recent developments in the systematics of Phoma, a complex genus of major quarantine significance. Fungal Diversity 31:1–18

    Google Scholar 

  • Aveskamp MM, de Gruyter J, Woudenberg JHC, Verkley GJM, Crous PW (2010) Highlights of the Didymellaceae: a polyphasic approach to characterise Phoma and related pleosporalean genera. Stud Mycol 65:1–60

    Article  PubMed  CAS  Google Scholar 

  • Berger F, Türk R (1993) Neue und seltene Flechten und lichenicole Pilze aus Oberösterreich, Österreich. Linzer Biologische Beitrage 25:167–204

    Google Scholar 

  • Boerema GH (1997) Contributions toward a monograph of Phoma (coelomycetes) V. Subdivision of the genus in sections. Mycotaxon 64:321–333

    Google Scholar 

  • Boerema GH, de Gruyter J, Noordeloos ME, Hamers MEC (2004) Phoma identification manual. Differentiation of specific and infra-specific taxa in culture. CABI Publishing, Wallingford, p 470

    Book  Google Scholar 

  • Brackel W von (2008a) Phoma ficuzzae sp. nov. and some other lichenicolous fungi from Sicily, Italy. Sauteria 15:103–120

    Google Scholar 

  • Brackel W von (2008b) Zwackhiomyces echinulatus sp. nov. and some other lichenicolous fungi from Sicily, Italy. Herzogia 21:181–198

    Google Scholar 

  • Brackel W von (2010) Weitere Funde von flechtenbewohnenden Pilzen in Bayern. Beiträge zu einer Checkliste V. Berichte der Bayerischen Botanischen Gesellschaft 80:5–32

    Google Scholar 

  • Câmara MPS, Palm ME, van Berkum P, O’Neill RN (2002) Molecular phylogeny of Leptosphaeria and Phaeosphaeria. Mycologia 94:630–640

    Article  PubMed  Google Scholar 

  • Crous PW, Wood AR, Okada G, Groenwald JZ (2008) Foliicolous microfungi occurring on Encephalartos. Persoonia 21:135–146

    Article  PubMed  CAS  Google Scholar 

  • Crous PW, Braun U, Wingfield MJ, Wood AR, Shin HD, Summerell BA, Alfenas AC, Cumagun CJR, Groenewald JZ (2009) Phylogeny and taxonomy of obscure genera of microfungi. Persoonia 22:139–161

    Article  PubMed  CAS  Google Scholar 

  • de Gruyter J, Aveskamp MM, Woudenberg JHC, Verkley GJM, Groenewald JZ, Crous PW (2009) Molecular phylogeny of Phoma and allied anamorph genera: toward a reclassification of the Phoma complex. Mycol Res 113:508–519

    Article  PubMed  Google Scholar 

  • de Gruyter J, Woudenberg JHC, Aveskamp MM, Verkley GJM, Groenewald JZ, Crous PW (2010) Systematic reappraisal of species in Phoma section Paraphoma, Pyrenochaeta and Pleurophoma. Mycologia 102:1066–1081

    Article  PubMed  Google Scholar 

  • Diederich P, Kocourková J, Etayo J, Zhurbenko M (2007) The lichenicolous Phoma species (coelomycetes) on Cladonia. Lichenologist 39:153–163

    Article  Google Scholar 

  • Diederich P, Lawrey JD, Sikaroodi M, van den Boom PG, Ertz D (2012) Briancoppinsia, a new coelomycetous genus of Arthoniaceae (Arthoniales) for the lichenicolous Phoma cytospora with a key to this and similar taxa. Fungal Diversity 52:1–12

    Article  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed  CAS  Google Scholar 

  • Etayo J, Diederich P (1995) Lichenicolous fungi from the western Pyrenees, France and Spain. I. New species of deuteromycetes. In: Daniëls FJA, Schulz M, Peine J (eds) Flechten Follmann. Contributions to lichenology in Honour of Gerhard Follmann. Geobotanical and Phytotaxonomical Study Group, Botanical Institute, University of Cologne, Cologne, pp. 205–221

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

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

    Article  PubMed  CAS  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 

  • Hafellner J (2000) Zur Biodiversität lichenisierter und lichenicoler Pilze in den Eisenerzer Alpen (Steiermark). Mitt. naturwiss. Ver. Steiermark 130:71–106

    Google Scholar 

  • Hafellner J, Kocourková J, Obermayer W (2004) Records of lichenicolous fungi from the northern Schladminger Tauern (Eastern Alps, Austria, Styria). Herzogia 17:59–66

    Google Scholar 

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

    Google Scholar 

  • Hafellner J, Herzog G, Mayrhofer H (2008) Zur Diversität von lichenisierten und lichenicolen Pilzen in den Ennstaler Alpen (Österreich: Steiermark, Oberösterreich). Mitt. naturwiss. Ver. Steiermark 137:131–204

    Google Scholar 

  • Harutyunyan S, Muggia L, Grube M (2008) Black fungi in lichens from seasonally arid habitats. Stud Mycol 61:83–90

    Article  PubMed  CAS  Google Scholar 

  • Hawksworth DL (1981) The lichenicolous coelomycetes. Bulletin of the British Museum (Natural History). Botany Series 9:1–98

    Google Scholar 

  • Hawksworth DL (2001) The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycol Res 105:1422–1432

    Article  Google Scholar 

  • Hawksworth DL, Cole MS (2004) Phoma fuliginosa sp. nov., from Caloplaca trachyphylla in Nebraska, with a key to the known lichenicolous species. Lichenologist 36:7–13

    Article  Google Scholar 

  • Hawksworth DL, Rossman AY (1997) Where are all the undescribed fungi? Phytopathology 87:888–891

    Article  PubMed  CAS  Google Scholar 

  • Higgins KL, Arnold AE, Miadlikowska J et al (2007) Phylogenetic relationships, host affinity, and geographic structure of boreal and arctic endophytes from three major plant lineages. Mol Phylogenet Evol 42:543–555

    Article  PubMed  CAS  Google Scholar 

  • Hofstetter V, Miadlikowska J, Kauff F, Lutzoni F (2007) Phylogenetic comparison of protein-coding versus ribosomal RNA-coding sequence data: a case study of the Lecanoromycetes (Ascomycota). Mol Phylogenet Evol 44:412–426

    Article  PubMed  CAS  Google Scholar 

  • Huang Y, Niu B, Gao Y, Fu L, Li W (2010) CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 26:680–682

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Katoh K, Misawa K, Kuma K-I, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066

    Article  PubMed  CAS  Google Scholar 

  • Katoh K, Toh H (2010) Parallelization of the MAAFT multiple sequence alignment program. Bioinformatics 26:1899–1900

    Article  PubMed  CAS  Google Scholar 

  • Kauff F, 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. Mol Phylogenet Evol 25:138–156

    Article  PubMed  CAS  Google Scholar 

  • Kauff F, Lutzoni F (2003) Compat.py—a program to detect topological conflict between supported clades in phylogenetic trees, available online at http://www.lutzonilab.net/pages/download.shtml

  • Khodosovtsev AY, Umanets OY (2009) Phoma cladoniicola Diederich, Kocourk. & Etayo, a new for Ukraine lichenicolous fungus from Oleshkivs’ky Sands. Chornomors’k. bot. z., 5:273–275

  • Kondratyuk S, Kärnefelt I, Goward T, Galloway D, Kudratov I, Lackovičova A, Lisická E, Guttová A (2010) Diagnoses of new taxa. In Oksner AM: Flora lišajnikiv Ukraini y dvoch tomach, Tom 2, Vypusk 3. Kiiv, Naukovo Dumka: 435–445

  • Larget B, Simon DL (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16:750–759

    Article  CAS  Google Scholar 

  • Lawrey JD (2002) Isolation and culture of lichenicolous fungi. In: Kranner I, Beckett R, Varma A (eds) Protocols in lichenology: culturing, biochemistry, physiology and use in biomonitoring. Springer, Berlin, pp 75–84

    Google Scholar 

  • Lawrey JD, Diederich P (2003) Lichenicolous fungi: interactions, evolution, and biodiversity. Bryologist 106:80–120

    Article  Google Scholar 

  • Lawrey JD, Diederich P, Nelsen MP, Sikaroodi M, Gillevet PM, Brand AM, van den Boom P (2011) The obligately lichenicolous genus Lichenoconium represents a novel lineage in the Dothideomycetes. Fungal Biology 115:176–187

    Article  PubMed  CAS  Google Scholar 

  • Maddison WP, Maddison DR (2010) Mesquite: a modular system for evolutionary analysis. Version 2.73 http://mesquiteproject.org

  • 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), 14 Nov. 2010, New Orleans, USA, pp. 1–8

  • Motiejūnaitė J, Brackel W von, Stončius D, Preikša Ž (2011) Contribution to the Lithuanian flora of lichens and allied fungi. III. Botanica Lithuanica 17:39–46

    Google Scholar 

  • Nelsen MP, Lücking R, Grube M, Mbatchou JS, Muggia L, Rivas Plata E, Lumbsch HT (2009) Unravelling the phylogenetic relationships of lichenised fungi in Dothideomyceta. Stud Mycol 64:135–144

    Article  PubMed  CAS  Google Scholar 

  • Nylander JA, 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

    Article  PubMed  CAS  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  PubMed  CAS  Google Scholar 

  • Ruibal C, Platas G, Bills GF (2008) High diversity and morphological convergence among melanised fungi from rock formations in the Central Mountain System of Spain. Persoonia 21:93–110

    Article  PubMed  CAS  Google Scholar 

  • Ruibal C, Gueidan C, Selbmann L, Gorbushina AA, Crous PW, Groenewald JZ, Muggia L, Grube M, Isola D, Schoch CL, Staley JT, Lutzoni F, de Hoog GS (2009) Phylogeny of rock-inhabiting fungi related to Dothideomycetes. Stud Mycol 64:123–133

    Article  PubMed  CAS  Google Scholar 

  • Smith SA, Dunn CW (2008) Phyutility: a phyloinformatics tool for trees, alignments and molecular data. Bioinformatics 24:715–716

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sutton BC (1980) The coelomycetes: Fungi imperfecti with pycnidia, acervuli and stromata. CMI, Kew, p 696

    Google Scholar 

  • Urbanavichus G, Urbanavichene I (2011) New records of lichens and lichenicolous fungi from the Ural Mountains, Russia. Folia Cryptogamica Estonica 48:119–124

    Google Scholar 

  • Wilgenbusch JC, Warren DL, Swofford DL (2004) AWTY: a system for graphical exploration of MCMC convergence in Bayesian phylogenetic inference. http://ceb.csit.fsu.edu/awty

  • Zhang Y, Schoch CL, Fournier J, Crous PW, de Gruyter J, Woudenberg JHC, Hirayama K, Tanaka K, Pointing SB, Spatafora JW, Hyde KD (2009) Multi-locus phylogeny of Pleosporales: a taxonomic, ecological and evolutionary re-evaluation. Stud Mycol 64:85–102

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Crous PW, Schoch CL, Hyde KD (2012) Pleosporales. Fungal Diversity 53:1–221

    Article  Google Scholar 

  • Zhurbenko MP (2009) Lichenicolous fungi and some lichens from the Holarctic. Opuscula Philolichenum 6:87–120

    Google Scholar 

  • 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

    Google Scholar 

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Acknowledgements

We thank Peter Scholz for providing us with a copy of the original description of Phoma pisutii, and Walter Obermayer for searching for an isotype of P. pisutii. Sequencing partially supported by grant DEB 0841405 from the National Science Foundation. MPN is supported by the Brown Family Graduate Fellowship through the Field Museum.

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Authors and Affiliations

  1. Department of Environmental Science and Policy, George Mason University, 4400 University Drive, Fairfax, VA, 22030-4444, USA

    James D. Lawrey & Masoumeh Sikaroodi

  2. Musée national d’histoire naturelle, 25 rue Munster, L-2160, Luxembourg, Luxembourg

    Paul Diederich

  3. Committee on Evolutionary Biology, University of Chicago, 1025 E. 57th Street, Chicago, IL, 60637, USA

    Matthew P. Nelsen

  4. Department of Botany, The Field Museum, 1400 S. Lake Shore Drive, Chicago, IL, 60605, USA

    Matthew P. Nelsen

  5. Canadian Museum of Nature, P.O. Box 3443, Station D, Ottawa, ON, K1P 6P4, Canada

    Colin Freebury

  6. Jardin Botanique National de Belgique, Domaine de Bouchout, B–1860, Meise, Belgium

    Dries Van den Broeck & Damien Ertz

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  1. James D. Lawrey
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Correspondence to James D. Lawrey.

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Table S1

Specimens and sequences used in two-locus (nuLSU + mtSSU) phylogenetic analysis of lichenicolous Phoma species and relatives in the Pleosporales (Fig. 1). (XLSX 16 kb)

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Lawrey, J.D., Diederich, P., Nelsen, M.P. et al. Phylogenetic placement of lichenicolous Phoma species in the Phaeosphaeriaceae (Pleosporales, Dothideomycetes). Fungal Diversity 55, 195–213 (2012). https://doi.org/10.1007/s13225-012-0166-9

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