Advertisement

Fungal Diversity

, Volume 51, Issue 1, pp 155–162 | Cite as

New insights into relationships of lichen-forming Dothideomycetes

  • Matthew P. NelsenEmail author
  • Robert Lücking
  • Joelle S. Mbatchou
  • Carrie J. Andrew
  • Adriano A. Spielmann
  • H. Thorsten Lumbsch
Article

Abstract

Here we continue to investigate the phylogenetic relationships of taxa ascribed to the primarily lichen-forming families Trypetheliaceae, Monoblastiaceae and Arthopyreniaceae. We demonstrate that the genera Julella and Arthopyrenia do not form monophyletic groups with taxa from these genera instead being placed both in Pleosporales and Trypetheliales. Within Dothideomycetes, lichen-forming species with brown ascospores are generally placed in the genera Mycomicrothelia, Architrypethelium, and Aptrootia in the family Trypetheliaceae. We tested the taxonomic placement of Anisomeridium phaeospermum, in Monoblastiaceae. This species produces brown-spores with wall ornamentation and therefore appears morphologically similar to Mycomicrothelia. Despite these morphological similarities, molecular data confirmed its placement in Anisomeridium. Consequently, the distinction between these two genera is in need of clarification and ascus characters are identified as the principal discriminating feature. Finally, we identify the non-lichenized taxa Heleiosa barbatula and Funbolia dimorpha as being part of the otherwise lichen-forming family Monoblastiaceae. This is confirmed by the perithecial anatomy of the sexually reproducing Heleiosa barbatula.

Keywords

Lichens Trypetheliaceae Pleosporales Systematics 

Notes

Acknowledgements

We are grateful to a number of organizations for funding including: NSF-DEB 0715660 “Neotropical Epiphytic Microlichens—An Innovative Inventory of a Highly Diverse yet Little Known Group of Symbiotic Organisms” to The Field Museum (PI Robert Lücking), NSF-DEB 0717476 “Systematics of Dothideomycetes to The Field Museum (coPI Thorsten Lumbsch; PI: J. Spatafora), a Cirrus grant to DePaul University supported Joelle Mbatchou, a grant from the Committee on Evolutionary Biology, University of Chicago to Matthew Nelsen, and the Caterpillar® company provided funds to study lichens from Panama. E. Rivas Plata and Z. Palice are thanked for use of collections. K. Hyde and C. Schoch are thanked for the invitation to contribute this manuscript, and K. Hyde is thanked for comments that improved the manuscript. R. Harris and A. Aptroot are thanked for discussions providing insight into the taxonomy of Anisomeridium and Mycomicrothelia. Most DNA analyses were performed at the Pritzker Laboratory for Molecular Systematics and Evolution at the Field Museum.

Supplementary material

13225_2011_144_MOESM1_ESM.pdf (126 kb)
Online Resource 1 List of taxa including their Genbank accession numbers, culture or collection information, family and order. Familial and ordinal level taxonomy follows Aptroot et al. (2008), Crous et al. (2011), Ertz & Tehler (2011), Lumbsch and Huhndorf (2010) and Schoch et al. (2009b). (PDF 126 KB)

References

  1. Aguileta G, Marthey S, Chiapello H, Lebrun M-H, Rodolphe F, Fournier E, Gendrault-Jacquemard A, Giraud T (2008) Assessing the performance of single-copy genes for recovering robust phylogenies. Syst Biol 57:613–627PubMedCrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Schäffer ZJ, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  3. Aptroot A, Lücking R, Sipman HJM, Umaña L, Chaves JL (2008) Pyrenocarpous lichens with bitunicate asci: a first assessment of the lichen biodiversity inventory of Costa Rica. Bibl Lichenol 97:1–162Google Scholar
  4. Avis PG, McLaughlin DJ, Dentinger BC, Reich PB (2003) Long-term increase in nitrogen supply alters above- and below-ground ectomycorrhizal communities and increases the dominance of Russula spp. in a temperate oak savanna. New Phytol 160:239–253CrossRefGoogle Scholar
  5. Bayev A, Georgiev OI, Hadjiolov AA, Nikolaev N, Skryabin KG, Zakharyev VM (1981) The structure of the yeast ribosomal RNA genes. 3. Precise mapping of the 18S and 25S rRNA genes and structure of the adjacent regions. Nucleic Acids Res 9:789–799PubMedCrossRefGoogle Scholar
  6. Crous PW, Groenewald JZ, Shivas RG, Edwards J, Seifert KA, Alfenas AC, Alfenas RF, Burgess TI, Carnegie AJ, Hardy GE, St J, Hiscock N, Hüberli D, Jung T, Louis-Seize G, Okada G, Pereira OL, Stukely MJC, Wang W, White GP, Young AJ, McTaggart AR, Pascoe IG, Porter IJ, Quaedvlieg W (2011) Fungal Planet description sheets: 69–91. Persoonia 26:108–156PubMedCrossRefGoogle Scholar
  7. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797PubMedCrossRefGoogle Scholar
  8. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  9. Gargas A, DePriest PT (1996) A nomenclature for fungal PCR primers with examples from intron-containing SSU rDNA. Mycologia 88:745–748CrossRefGoogle Scholar
  10. Gargas A, Taylor JW (1992) Polymerase chain reaction (PCR) primers for amplifying and sequencing nuclear 18S rDNA from lichenized fungi. Mycologia 84:589–592CrossRefGoogle Scholar
  11. Gueidan C, Ruibal C, de Hoog GS, Schneider H (2011) Rock-inhabiting fungi originated during periods of dry climate in the late Devonian and middle Triassic. Fung Div 115:987–996Google Scholar
  12. Harris RC (1995) More Florida lichens. Published by the author, BronxGoogle Scholar
  13. 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 Res 30:3059–3066PubMedCrossRefGoogle Scholar
  14. Kirk PM, Cannon PF, Minter DW, Stalpers JA (eds) (2008) Dictionary of the Fungi, 10th edn. CAB International, WallingfordGoogle Scholar
  15. Kohlmeyer J, Volkmann-Kohlmeyer B, Eriksson OE (1996) Fungi on Juncus roemerianus. 8. New bitunicate ascomycetes. Can J Bot 74:1830–1840CrossRefGoogle Scholar
  16. Kroken S, Taylor JW (2001) A gene genealogical approach to recognize phylogenetic species boundaries in the lichenized fungus Letharia. Mycologia 93:38–53CrossRefGoogle Scholar
  17. 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. Fung Div 11:176–187Google Scholar
  18. Lücking R, Seavey F, Common RS, Beeching SQ, Breuss O, Buck WR, Crane L, Hodges M, Hodkinson BP, Lay E et al (2011) The lichens of the Fakahatchee Strand Preserve state park, Florida: proceedings from the 18th Tuckerman workshop. Bull Flor Mus Nat Hist 49:127–186Google Scholar
  19. Lumbsch HT, Schmitt I, Lindemuth R, Miller A, Mangold A, Fernandez F, Huhndorf S (2005) Performance of four ribosomal DNA regions to infer higher-level phylogenetic relationships of inoperculate euascomycetes (Leotiomyceta). Mol Phyl Evol 34:512–524CrossRefGoogle Scholar
  20. Maddison WP, Maddison DR (2010) Mesquite: a modular system for evolutionary analysis Version 2.73, Available at website: http://mesquiteproject.org
  21. 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 November 2010, New Orleans, Louisiana, pp 1–8Google Scholar
  22. Mugambi GK, Huhndorf SM (2009) Molecular phylogenetics of Pleosporales: Melanommataceae and Lophiostomataceae re-circumscribed (Pleosporomycetidae, Dothideomycetes, Ascomycota). Stud Mycol 64:103–121PubMedCrossRefGoogle Scholar
  23. 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 64:135–144PubMedCrossRefGoogle Scholar
  24. Raja HA, Schoch CL, Hustad VP, Shearer CA, Miller AN (2011) Testing the phylogenetic utility of MCM7 in the Ascomycota. MycoKeys 1:63–94CrossRefGoogle Scholar
  25. Rambaut A (1996) Se-Al: Sequence Alignment Editor Available at website: http://evolve.zoo.ox.ac.uk/
  26. Rehner SA, Buckley E (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97:84–98PubMedCrossRefGoogle Scholar
  27. Rubstov PM, Musakhanov MM, Zakharyev VM, Krayev AS, Skryabin KG, Bayev AA (1980) The structure of the yeast ribosomal RNA genes. I. The complete nucleotide sequence of the 18S ribosomal RNA gene from Saccharomyces cerevisiae. Nucleic Acids Res 8:5779–5794CrossRefGoogle Scholar
  28. Schmitt I, Crespo A, Divakar PK, Fankhauser JD, Herman-Sackett E, Kalb K, Nelsen MP, Nelson NA, Rivas-Plata E, Shimp AD, Widhelm T, Lumbsch HT (2009) New primers for promising single-copy genes in fungal phylogenetics and systematics. Persoonia 23:35–40PubMedCrossRefGoogle Scholar
  29. Schoch CL, Sung G-H, López-Giráldez F, Townsend JP, Miadlikowska J, Hofstetter V, Robbertse B, Matheny B, Kauff F, Wang Z, Gueidan C, Andrie RM, Trippe K, Ciufetti LM, Wynns A, Fraker E, Hodkinson BP, Bonito G, Groenewald JZ, Arzanlou M, de Hoog GS, Crous PW, Hewitt D, Pfister D, Peterson K, Gryzenhout M, Wingfield MJ, Aptroot A, Suh S-O, Blackwell M, Hillis DM, Griffith GW, Castlebury LA, Rossman A, Lumbsch HT, Lücking R, Büdel B, Rauhut A, Diederich P, Ertz D, Geiser DM, Hosaka K, Inderbitzin P, Kohlmeyer J, Volkmann-Kohlmeyer B, Mostert L, O’Donnell K, Sipman H, Rogers JD, Shoemaker R, Sugiyama J, Summerbell RC, Untereiner W, Johnston PR, Stenroos S, Zuccaro A, Dyer PS, Crittenden PD, Cole MS, Hansen K, Trappe JM, Yahr R, Lutzoni F, Spatafora JW (2009a) Ascomycota Tree of Life: A phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst Biol 58:224–239PubMedCrossRefGoogle Scholar
  30. Schoch CL, Crous PW, Groenewald JZ, Boehm EWA, Burgess TI, de Gruyter J, de Hoog GS, Dixon LJ, Grube M, Gueidan C, Harada Y, Hatakeyama S, Hirayama K, Hosoya T, Huhndorf SM, Hyde KD, Jones EBG, Kohlmeyer J, Kruys Å, Li YM, Lücking R, Lumbsch HT, Marvanová L, Mbatchou JS, McVay AH, Miller AN, Mugambi GK, Muggia L, Nelsen MP, Nelson P, Owensby CA, Phillips AJL, Phongpaichit S, Pointing SB, Pujade-Renaud V, Raja HA, Rivas Plata E, Robbertse B, Ruibal C, Sakayaroj J, Sano T, Selbmann L, Shearer CA, Shirouzu T, Slippers B, Suetrong S, Tanaka K, Volkmann-Kohlmeyer B, Wingfield MJ, Wood AR, Woudenberg JHC, Yonezawa H, Zhang Y, Spatafora JW (2009b) A class-wide phylogenetic assessment of Dothideomycetes. Stud Mycol 64:1–15PubMedCrossRefGoogle Scholar
  31. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690PubMedCrossRefGoogle Scholar
  32. Suetrong S, Schoch CL, Spatafora JW, Kohlmeyer J, Volkmann-Kohlmeyer B, Sakayaroj J, Phongpaichit S, Tanaka K, Hirayama K, Jones EBG (2009) Molecular systematics of the marine Dothideomycetes. Stud Mycol 64:155–173PubMedCrossRefGoogle Scholar
  33. Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246PubMedGoogle Scholar
  34. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, San Diego, pp 315–322Google Scholar
  35. 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 the Pleosporales: a taxonomic, ecological and evolutionary re-evaluation. Stud Mycol 64:85–102PubMedCrossRefGoogle Scholar
  36. Zhang Y, Crous PW, Schoch CL, Hyde KD (2011) Pleosporales. Fung. Div. in pressGoogle Scholar
  37. Zhou S, Stanosz GR (2001) Primers for amplification of mt SSU rDNA, and a phylogenetic study of Botryosphaeria and associated anamorphic fungi. Mycol Res 105:1033–1044CrossRefGoogle Scholar
  38. Zoller S, Scheidegger SC (1999) PCR primers for the amplification of mitochondrial small subunit ribosomal DNA of lichen-forming ascomycetes. Lichenologist 31:511–516Google Scholar

Copyright information

© Kevin D. Hyde 2011

Authors and Affiliations

  • Matthew P. Nelsen
    • 1
    • 2
    Email author
  • Robert Lücking
    • 2
  • Joelle S. Mbatchou
    • 2
    • 3
    • 4
  • Carrie J. Andrew
    • 2
    • 5
  • Adriano A. Spielmann
    • 6
  • H. Thorsten Lumbsch
    • 2
  1. 1.Committee on Evolutionary BiologyUniversity of ChicagoChicagoUSA
  2. 2.Department of BotanyThe Field MuseumChicagoUSA
  3. 3.Department of Biological SciencesDePaul UniversityChicagoUSA
  4. 4.Department of StatisticsUniversity of ChicagoChicagoUSA
  5. 5.Department of BiologyNortheastern Illinois UniversityChicagoUSA
  6. 6.Laboratório de Botânica, Departamento de Biologia, Centro de Ciências Biológicas e da SaúdeUniversidade Federal de Mato Grosso do SulCampo GrandeBrazil

Personalised recommendations