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Research Article

Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi

Conrad L. Schoch, Keith A. Seifert, Sabine Huhndorf, Vincent Robert, John L. Spouge, C. André Levesque, Wen Chen, and Fungal Barcoding Consortium
  1. aNational Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20892;
  2. bBiodiversity (Mycology and Microbiology), Agriculture and Agri-Food Canada, Ottawa, ON, Canada K1A 0C6;
  3. cDepartment of Botany, The Field Museum, Chicago, IL 60605; and
  4. dCentraalbureau voor Schimmelcultures Fungal Biodiversity Centre (CBS-KNAW), 3508 AD, Utrecht, The Netherlands
  1. 3Department of Botany, The Field Museum, 1400 S. Lake Shore Drive, Chicago, IL 60605
  2. 4Centraalbureau voor Schimmelcultures (CBS-KNAW) Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands
  3. 5Life Technologies, 850 Lincoln Centre Drive, Foster City, CA 9440
  4. 6Jena Microbial Resource Collection, Institute of Microbiology, University of Jena & Leibniz Institute for Natural Product Research and Infection Biology, Beutenbergstrasse 11 a, 07745 Jena, Germany
  5. 7University of Illinois, Illinois Natural History Survey, 1816 South Oak Street, Champaign, IL 61820
  6. 8Department of Microbiology and Plant Pathology, Forestry & Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, 0001, South Africa
  7. 9Louisiana State University Agricultural Center, Department of Plant Pathology and Crop Physiology, Baton Rouge, LA 70803
  8. 10Japan Collection of Microorganisms, RIKEN BioResource Center, Wako, Saitama 351-0198, Japan
  9. 11State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Bei-Chen-Xi Road, Chaoyang District, Beijing, 100101, China
  10. 12Departamento de Fitopatologia, Universidade Federal de Viçosa, 36570-000 Viçosa, Minas Gerais, Brazil
  11. 13Ruhr-Universität Bochum, Geobotanik ND03/174, Universitätstr. 150, 44801 Bochum, Germany
  12. 14Laurentian Forestry Centre, Canadian Forest Service, Natural Resources Canada, 1055 du PEPS, PO Box 10380, Stn. Sainte-Foy, Québec G1V 4C, Canada, 7
  13. 15Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803
  14. 16Department of Internal Medicine and Infectious Diseases, University Medical Center, Utrecht, The Netherlands
  15. 17Department of Biology, Brandon University, Brandon, Manitoba R7A 6A9, Canada
  16. 18National Center for Genetic Engineering and Biotechnology (BIOTEC),113 Paholyothin Road, Pathum Thani 12120, Thailand
  17. 19Departamento de Biología Vegetal I, Facultad de Biología, Universidad Complutense de Madrid, Madrid 28040, Spain
  18. 20Muséum National d’Histoire Naturelle, Dépt. Systématique et Evolution CP39, UMR7205, 12 Rue Buffon, F-75005 Paris, France
  19. 21Key Laboratory of Biodiversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, Yunnan, China
  20. 22Dipartimento Biologia Applicata- Microbiologia, Università degli Studi di Perugia, Perugia, Italy
  21. 23University of Maryland, Department of Plant Sciences and Landscape Architecture, 2112 Plant Sciences Building, College Park, MD 20742
  22. 24Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh, EH3 5LR, UK
  23. 25Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Madrid 28040, Spain
  24. 26Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, UK
  25. 27Real Jardín Botánico, RJB-CSIC, Plaza de Murillo 2, 28014 Madrid, Spain
  26. 28Institute of Biological, Environmental and Rural Sciences, Prifysgol Aberystwyth, Aberystwyth, Ceredigion Wales SY23 3DD, UK
  27. 29Department of Genetics, Forestry & Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, 0001, South Africa
  28. 30Department of Microbiology and Molecular Genetics, Oklahoma State University, Stillwater, OK 74074
  29. 31Institute of Animal Physiology and Genetics, Czech Academy of Sciences, v.v.i., Prague, Czech Republic
  30. 32Royal Botanic Gardens Melbourne, Birdwood Avenue, South Yarra, VIC 3141, Australia
  31. 33Institut für Pflanzenwissenschaften, Karl-Franzens-Universität Graz, Holteigasse 6, 8010 Graz, Austria
  32. 34Department of Plant Sciences, University of the Free State, P.O. Box 339, Bloemfontein 9300, South Africa
  33. 35Department of Cryptogamic Botany, Swedish Museum of Natural History, P.O. Box 50007, SE-104 05, Stockholm, Sweden
  34. 36Faculty of Agriculture and Life Science, Hirosaki University, 3 Bunkyo-cho, Hirosaki, Aomori 036-8561, Japan
  35. 37Department of Science Education, National Taipei University of Education, Taipei 10642, Taiwan
  36. 38Agroscope Changins-Wädenswil Research Station ACW, Département de recherche en Protection des végétaux grandes cultures et vigne/Viticulture et oenologie, CP 1012, CH-1260 Nyon, Switzerland
  37. 39Botanical Museum, Finnish Museum of Natural History, FI-00014 University of Helsinki, Finland
  38. 40Korean Agricultural Culture Collection, National Academy of Agricultural Science, RDA, Suwon, 441-707, Korea.
  39. 41National Museum of Nature and Science, Tsukuba, Japan
  40. 42Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37920
  41. 43Herbarium, University of Turku, FI-20014 University of Turku, Finland
  42. 44Mae Fah Luang University, 57100 Chiang Rai, Thailand
  43. 45Botany and Microbiology Department, College of Science, King Saud University, P.O. Box: 2455, Riyadh 1145, Saudi Arabia
  44. 46Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109
  45. 47Landcare Research, Private Bag 92170, Auckland 1142, New Zealand
  46. 48CABI-UK, Bakeham Lane, Egham, Surrey TW20 9TY, UK
  47. 49Eötvös Loránd University, Institute of Biology, Department of Plant Anatomy, Pázmány Péter sétány 1/c, 1117 Budapest, Hungary
  48. 50Institute of Ecology and Earth Sciences, University of Tartu, 40 Lai St, Tartu 51005, Estonia
  49. 51National Center for Agricultural Utilization Research, ARS, USDA, 1815 N. University St, Peoria, IL
  50. 52Fungal Screening, Novozymes A/S, Krogshoejvej 36, DK-2880 Bagsvaerd, Denmark
  51. 53University of Helsinki, Plant Biology, Department of Biosciences, P.O. Box 65, 00014, Finland
  52. 54Department of Biology, McMaster University, 1280 Main Street West, Hamilton, Ontario L8S 4K1, Canada
  53. 55Deppartment of Biology, Eastern Illinois University, Charleston, IL 61920
  54. 56Molecular Mycology Research Laboratory, Centre for Infectious Diseases and Microbiology, Westmead Millennium Institute, University of Sydney Western Clinical School at Westmead Hospital, Westmead, Australia
  55. 57Department of Natural History, Royal Ontario Museum, and Department of Ecology and Evolutionary Biology, University of Toronto, 100 Queen's Park, Toronto, Ontario, M5S 2C6, Canada
  56. 58University of Szeged, Faculty of Science and Informatics, Department of Microbiology, Közép fasor 52, Szeged, H-6726, Hungary
  57. 59Department of Plant and Environmental Sciences, University of Gothenburg, Box 461, Gothenburg, Sweden
  58. 60NITE Biological Resource Center (NBRC), National Institute of Technology and Evaluation, Kisarazu, Chiba 292-0818, Japan
  59. 61Biodiversity and Climate Research Center (BiK-F), Senckenberg Gesellschaft für Naturforschung, Senckenberganlage 25, D-60325 Frankfurt, (Main), Germany
  60. 62The University of North Carolina at Greensboro, Department of Chemistry and Biochemistry, 457 Sullivan Science Building, P.O. Box 26170, Greensboro, NC 27402-6170
  61. 63Université de Bourgogne/INRA, UMR1347 Agroécologie, BP 86510, F-21000 Dijon, France
  62. 64Goethe Universität Frankfurt, Department of Biological Sciences, Siesmayerstr. 70, 60323 Frankfurt, (Main), Germany
  63. 65Genetics, Department Biology, Biocenter of Ludwig-Maximilians-University Munich, Grosshaderner Strasse 2-4, 82152 Martinsried, Germany
  64. 66University of Illinois, Department of Plant Biology, 505 South Goodwin Avenue, Urbana, IL 61801
  65. 67Fungus/Mushroom Resource and Research Center, Faculty of Agriculture, Tottori University 4-101 Koyama-Minami, Tottori 680-8553, Japan
  66. 68Mycology and Botany Program, American Type Culture Collection (ATCC), 10801 University Blvd., Manassas, VA 20110
  67. 69Mushroom Research Division, National Institute of Horticultural and Herbal Science, Rural Department Administration, Suwon, 404-707, Korea
  68. 70Natural History Museum of Tartu University, 46 Vanemuise Street, 51014 Tartu, Estonia
  69. 71Boise State University, Department of Biological Sciences, 1910 University Dr., Boise, ID 83725
  70. 72Institute of Evolution and Ecology, University of Tübingen, Auf der Morgenstelle 1, D-72076 Tübingen, Germany
  71. 73Department of Plant Biology and Pathology, Rutgers University, New Brunswick, NJ 08901
  72. 74CBOL, National Museum of Natural History, Smithsonian Institution, P.O. Box 37012, MRC-105, Washington, DC 20013-7012

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PNAS first published March 27, 2012; https://doi.org/10.1073/pnas.1117018109
Conrad L. Schoch
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  • For correspondence: schoch2@ncbi.nlm.nih.gov Keith.Seifert@AGR.GC.CA
Keith A. Seifert
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  • For correspondence: schoch2@ncbi.nlm.nih.gov Keith.Seifert@AGR.GC.CA
Sabine Huhndorf
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Vincent Robert
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John L. Spouge
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C. André Levesque
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Wen Chen
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  1. Edited* by Daniel H. Janzen, University of Pennsylvania, Philadelphia, PA, and approved February 24, 2012 (received for review October 18, 2011)

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Abstract

Six DNA regions were evaluated as potential DNA barcodes for Fungi, the second largest kingdom of eukaryotic life, by a multinational, multilaboratory consortium. The region of the mitochondrial cytochrome c oxidase subunit 1 used as the animal barcode was excluded as a potential marker, because it is difficult to amplify in fungi, often includes large introns, and can be insufficiently variable. Three subunits from the nuclear ribosomal RNA cistron were compared together with regions of three representative protein-coding genes (largest subunit of RNA polymerase II, second largest subunit of RNA polymerase II, and minichromosome maintenance protein). Although the protein-coding gene regions often had a higher percent of correct identification compared with ribosomal markers, low PCR amplification and sequencing success eliminated them as candidates for a universal fungal barcode. Among the regions of the ribosomal cistron, the internal transcribed spacer (ITS) region has the highest probability of successful identification for the broadest range of fungi, with the most clearly defined barcode gap between inter- and intraspecific variation. The nuclear ribosomal large subunit, a popular phylogenetic marker in certain groups, had superior species resolution in some taxonomic groups, such as the early diverging lineages and the ascomycete yeasts, but was otherwise slightly inferior to the ITS. The nuclear ribosomal small subunit has poor species-level resolution in fungi. ITS will be formally proposed for adoption as the primary fungal barcode marker to the Consortium for the Barcode of Life, with the possibility that supplementary barcodes may be developed for particular narrowly circumscribed taxonomic groups.

  • DNA barcoding
  • fungal biodiversity

Footnotes

  • ↵1To whom correspondence may be addressed. E-mail: schoch2{at}ncbi.nlm.nih.gov or Keith.Seifert{at}AGR.GC.CA.
  • ↵2A complete list of the Fungal Barcoding Consortium can be found in the SI Appendix.

  • Author contributions: C.L.S. and K.A.S. designed research; K.A.S., V.R., E.B., K.V., P.W.C., A.N.M., M.J.W., M.C.A., K.-D.A., F.-Y.B., R.W.B., D.B., M.-J.B., M. Blackwell, T.B., M. Bogale, N.B., A.R.B., B.B., L.C., Q.C., G.C., P. Chaverri, B.J.C., A.C., P. Cubas, C.C., U.D., Z.W.d.B., G.S.d.H., R.D.-P., B. Dentinger, J.D-U., P.K.D., B. Douglas, M.D., T.A.D., U.E., J.E.E., M.S.E., K.F., M.F., M.A.G., Z.-W.G., G.W.G., K.G., J.Z.G., M. Groenewald, M. Grube, M. Gryzenhout, L.-D.G., F. Hagen, S. Hambleton, R.C.H., K. Hansen, P.H., G.H., C.H., K. Hirayama, Y.H., H.-M.H., K. Hoffmann, V. Hofstetter, F. Högnabba, P.M.H., S.-B.H., K. Hosaka, J.H., K. Hughes, Huhtinen, K.D.H., T.J., E.M.J., J.E.J., P.R.J., E.B.G.J., L.J.K., P.M.K., D.G.K., U.K., G.M.K., C.P.K., S.L., S.D.L., A.S.L., K.L., L.L., J.J.L., H.T.L., H.M., S.S.N.M., M.P.M., T.W.M., A.R.M., A.S.M., W.M., J.-M.M., S.M., L.G.N., R.H.N., T.N., I.N., G.O., I. Okane, I. Olariaga, J.O., T. Papp, D.P., T. Petkovits, R.P.-B., W.Q., H.A.R., D.R., T.L.R., C.R., J.M.S.-R., I.S., A.S., C.S., K.S., F.O.P.S., S. Stenroos, B.S., H.S., S. Suetrong, S.-O.S., G.-H.S., M.S., K.T., L.T., M.T.T., E.T., W.A.U., H.U., C.V., A.V., T.D.V., G.W., Q.M.W., Y.W., B.S.W., M.W., M.M.W., J.X., R.Y., Z.-L.Y., A.Y., J.-C.Z., N.Z., W.-Y.Z., and D.S performed research; V.R., J.L.S., C.A.L., and W.C. analyzed data; C.L.S., K.A.S., and S.H. wrote the paper.

  • The authors declare no conflict of interest.

  • ↵*This Direct Submission article had a prearranged editor.

  • Data deposition: The sequences reported in this paper have been deposited in GenBank. Sequences are listed in Dataset S1.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1117018109/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi
Conrad L. Schoch, Keith A. Seifert, Sabine Huhndorf, Vincent Robert, John L. Spouge, C. André Levesque, Wen Chen, Fungal Barcoding Consortium
Proceedings of the National Academy of Sciences Mar 2012, 201117018; DOI: 10.1073/pnas.1117018109

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Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi
Conrad L. Schoch, Keith A. Seifert, Sabine Huhndorf, Vincent Robert, John L. Spouge, C. André Levesque, Wen Chen, Fungal Barcoding Consortium
Proceedings of the National Academy of Sciences Mar 2012, 201117018; DOI: 10.1073/pnas.1117018109
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