Improving ITS sequence data for identification of plant pathogenic fungi

R. Henrik Nilsson1, Kevin D. Hyde2, Julia Pawłowska3, Martin Ryberg4, Leho Tedersoo5, Anders Bjørnsgard6, Siti Aisyah Alias7, Artur Alves8, Cajsa Lisa Anderson1, Alexandre Antonelli1, A. Elizabeth Arnold9, Barbara Doreen Bahnmann10, Mohammad Bahram5, Johan Bengtsson‐Palme11, Anna Berlin12, Sara Branco13, Putarak Chomnunti14, Asha J. Dissanayake14, Rein Drenkhan15, Hanna Friberg12, Tobias Guldberg Frøslev16, Bettina Halwachs17, Martin Hartmann18, B. Henricot19, Ruvishika S. Jayawardena14, Ari Jumpponen20, Håvard Kauserud6, Sonja Koskela21, Tomasz Kulik22, Kare Liimatainen23, Björn D. Lindahl12, Daniel L. Lindner24, Jian‐Kui Liu14, Sajeewa S. N. Maharachchikumbura14, Dimuthu S. Manamgoda14, Svante Martinsson1, Maria Alice Neves25, Tuula Niskanen23, Stephan Nylinder26, Olinto Liparini Pereira27, Danilo Batista Pinho27, Teresita M. Porter28, Valentin Queloz29, Taavi Riit5, Marisol Sánchez-García30, Filipe Sousa1, Emil Stefańczyk31, Mariusz Tadych32, Susumu Takamatsu33, Qing Tian14, Dhanushka Udayanga14, Martin Unterseher34, Zheng Wang35, Saowanee Wikee14, Jiye Yan36, Ellen Larsson1, Karl ­Henrik Larsson37, Urmas Kõljalg38, Kessy Abarenkov38
1Department of Biological and Environmental Sciences, University of Gothenburg, Box 461, 405 30, Gothenburg, Sweden
2Institute of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai, 57100, Thailand
3Department of Plant Systematics and Geography, Faculty of Biology, University of Warsaw, Al. Ujazdowskie 4, 00-478, Warsaw, Poland
4Department of Organismal Biology, Uppsala University, Norbyvägen 18D, 75236, Uppsala, Sweden
5Institute of Ecology and Earth Sciences, University of Tartu, Lai 40, Tartu 51005, Estonia
6Microbial Evolution Research Group, University of Oslo, Blindernveien 31, 0371, Oslo, Norway
7Institute of Biological Sciences, University of Malaya, 50603 Kuala Lumpur, Malaysia
8Department of Biology, CESAM, University of Aveiro, 3810-193 Aveiro, Portugal
9School of Plant Sciences, The University of Arizona, 1140 E South Campus Drive, Forbes 303, Tucson, AZ, 85721, USA
10Laboratory of Environmental Microbiology, Institute of Microbiology ASCR, Vídeňská 1083, 14220, Prague 4, Czech Republic
11Department of Infectious Diseases, Institute of Biomedicine, Sahlgrenska Academy, University of Gothenburg, Guldhedsgatan 10, 413 46, Göteborg, Sweden
12Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences, Box 7026, 750 07, Uppsala, Sweden
13University of California at Berkeley, 321 Koshland Hall University of California, Berkeley, CA, 94720-3102, USA
14School of Science, Mae Fah Luang University, Chiang Rai 57100, Thailand
15Institute of Forestry and Rural Engineering, Estonian University of Life Sciences, Kreutzwaldi 5, 51014 Tartu, Estonia
16Natural History Museum of Denmark, Øster Voldgade 5-7, 1350 København K, Denmark
17Institute for Genomics and Bioinformatics, Graz University of Technology, 8010, Graz, Austria
18Forest Soils and Biogeochemistry, Swiss Federal Research Institute WSL, Zuercherstrasse 111, 8903, Birmensdorf, Switzerland
19Plant Pathology, The Royal Horticultural Society, Wisley, Woking, Surrey, GU23 6QB, UK
20Division of Biology, Kansas State University, Manhattan, KS 66506, USA
21Metapopulation Research Group, Department of Biosciences, University of Helsinki, PO Box 65, 00014, Helsinki, Finland
22Department of Diagnostics and Plant Pathophysiology, University of Warmia and Mazury in Olsztyn, Plac Lodzki 5, Olsztyn 10-957, Poland
23Plant Biology, Department of Biosciences, University of Helsinki, P.O. Box 65, 00014, Helsinki, Finland
24US Forest Service, Northern Research Station, Center for Forest Mycology Research, One Gifford Pinchot Drive, Madison, WI, USA
25Departamento Botânica, PPG Biologia de Fungos, Algas e Plantas, Universidade Federal de Santa Catarina, Florianópolis, SC, Brazil
26Department of Botany, Swedish Natural History Museum, Svante Arrhenius väg 7, 10405, Stockholm, Sweden
27Departamento de Fitopatologia, Universidade Federal de Viçosa, Viçosa, Minas Gerais, 36570-900, Brazil
28Department of Biology, McMaster University, Hamilton, ON L8S 4K1, Canada
29ETH Zürich, Institute for Integrative Biology, CHN G 68.3, Universitätsstrasse 16, 8092, Zürich, Switzerland
30Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37996-1610, USA
31Plant Breeding and Acclimatization Institute-National Research Institute, Młochów Research Centre, Platanowa 19, 05831, Młochów, Poland
32Department of Plant Biology and Pathology, School of Environmental and Biological Sciences, Rutgers, The State University of New Jersey, 59 Dudley Rd., New Brunswick, NJ, 08901, USA
33Laboratory of Plant Pathology, Faculty of Bioresources, Mie University, 1577 Kurima-Machiya, Tsu-city, 514-8507, Japan
34Institute of Botany and Landscape Ecology, Ernst-Moritz-Arndt University, Soldmannstr. 15, 17487, Greifswald, Germany
35Biostatistics Department, Yale School of Public Health, New Haven, CT, 06520, USA
36Institute of Plant and Environment Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, China
37Natural History Museum, P.O. Box 1172, Blindern, 0318, Oslo, Norway
38Natural History Museum, University of Tartu, Vanemuise 46, Tartu, 51014, Estonia

Tóm tắt

Từ khóa


Tài liệu tham khảo

Abarenkov K, Nilsson RH, Larsson K-H, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Ursing BM, Vrålstad T, Liimatainen K, Peintner U, Kõljalg U (2010a) The UNITE database for molecular identification of fungi - recent updates and future perspectives. New Phytol 186:281–285

Abarenkov K, Tedersoo L, Nilsson RH, Vellak K, Saar I, Veldre V, Parmasto E, Prous M, Aan A, Ots M, Kurina O, Ostonen I, Jõgeva J, Halapuu S, Põldmaa K, Toots M, Truu J, Larsson K-H, Kõljalg U (2010b) PlutoF - a web-based workbench for ecological and taxonomic research, with an online implementation for fungal ITS sequences. Evol Bioinform 6:189–196

Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

Barnes I, Crous PW, Wingfield BD, Wingfield MJ (2004) Multigene phylogenies reveal that red band needle blight is caused by two distinct species of Dothistroma, D. septosporum and D. pini. Stud Mycol 50:551–565

Bates ST, Ahrendt S, Bik HM, Bruns TD, Caporaso JG, Cole J, Dwan M, Fierer N, Gu D, Houston S, Knight R, Leff J, Lewis C, Maestre JP, McDonald D, Nilsson RH, Porras-Alfaro A, Robert V, Schoch C, Scott J, Taylor DL, Wegener Parfrey L, Stajich JE (2013) Meeting report: fungal ITS workshop (October 2012). Stand Genomic Sci 8:118–123

Bengtsson-Palme J, Ryberg M, Hartmann M, Branco S, Wang Z, Godhe A, De Wit P, Sánchez-García M, Ebersberger M, de Sousa F, Amend A, Jumpponen A, Unterseher M, Kristiansson E, Abarenkov K, Bertrand YJK, Sanli K, Eriksson MK, Vik U, Veldre V, Nilsson RH (2013) Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol Evol 4:914–919

Bidartondo M, Bruns TD, Blackwell M et al (2008) Preserving accuracy in GenBank. Science 319:5870

Britton KO, Liebhold AM (2013) One world, many pathogens! New Phytol 197:9–10

Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

Cunha KCD, Sutton DA, Fothergill AW, Gené GJ, Cano J, Madrid H, Hoog SD, Crous PW, Guarro J (2013) In vitro antifungal susceptibility and molecular identity of 99 clinical isolates of the opportunistic fungal genus Curvularia. Diagn Microbiol Infect Dis 76:168–174

Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430

Delaye L, García-Guzmán G, Heil M (2013) Endophytes versus biotrophic and necrotrophic pathogens – are fungal lifestyles evolutionarily stable traits? Fungal Divers 60:125–135

Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186–194

Gauthier G, Keller N (2013) Crossover fungal pathogens: the biology and pathogenesis of fungi capable of crossing kingdoms to infect plants and humans. Fungal Genet Biol 61:146–57

Ghannoum MA, Jurevic RJ, Mukherjee PK, Cui F, Sikaroodi M, Naqvi A, Gillevet PM (2010) Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog 6:e1000713

Heath TA, Hedtke SM, Hillis DM (2008) Taxon sampling and the accuracy of phylogenetic analyses. J Syst Evol 46:239–257

Hibbett DS, Ohman A, Glotzer D, Nuhn M, Kirk P, Nilsson RH (2011) Progress in molecular and morphological taxon discovery in fungi and options for formal classification of environmental sequences. Fungal Biol Rev 25:38–47

Hyde KD, Udayanga D, Manamgoda DS, Tedersoo L, Larsson E, Abarenkov K, Bertrand YJK, Oxelman B, Hartmann M, Kauserud H, Ryberg M, Kristiansson E, Nilsson RH (2013) Incorporating molecular data in fungal systematics: a guide for aspiring researchers. Curr Res Environ Appl Mycol 3:1–32

Kang S, Mansfield MAM, Park B, Geiser DM, Ivors KL, Coffey MD, Grünwald NJ, Martin FN, Lévesque CA, Blair JE (2010) The promise and pitfalls of sequence-based identification of plant pathogenic fungi and oomycetes. Phytopathology 100:732–737

Ko Ko TWK, Stephenson SL, Bahkali AH, Hyde KD (2011) From morphology to molecular biology: can we use sequence data to identify fungal endophytes? Fungal Divers 50:113–120

Kõljalg U, Nilsson RH, Abarenkov K et al (2013) Towards a unified paradigm for sequence-based identification of Fungi. Mol Ecol 22:5271–5277

Kowalski T, Holdenrieder O (2009) The teleomorph of Chalara fraxinea, the causal agent of ash dieback. For Pathol 39:304–308

La Duc MT, Vaishampayan P, Nilsson RH, Torok T, Venkateswaran K (2012) Pyrosequencing-derived bacterial, archaeal, and fungal diversity of spacecraft hardware destined for Mars. Appl Environ Microbiol 78:5912–5922

Lanzén A, Jørgensen SL, Huson DH, Gorfer M, Grindhaug SH, Jonassen I, Øvreås L, Urich T (2012) CREST – classification resources for environmental sequence tags. PLoS One 7:e49334

Maharachchikumbura SSN, Guo LD, Cai L, Chukeatirote E, Wu WP, Sun X, Crous PW, Bhat DJ, McKenzie EHC, Bahkali AH, Hyde KD (2012) A multi-locus backbone tree for Pestalotiopsis, with a polyphasic characterization of 14 new species. Fungal Divers 56:95–129

Manamgoda DS, Cai L, McKenzie EHC, Crous PW, Madrid H, Chukeatirote E, Shivas RG, Tan YP, Hyde KD (2012) A phylogenetic and taxonomic re-evaluation of the Bipolaris, Cochliobolus, Curvularia complex. Fungal Divers 56:131–144

Nakamura Y, Cochrane G, Karsch-Mizrachi I (2013) The international nucleotide sequence database collaboration. Nucleic Acids Res 41:D21–D24

Nilsson RH, Ryberg M, Sjökvist E, Abarenkov K (2011) Rethinking taxon sampling in the light of environmental sequencing. Cladistics 27:197–203

Nilsson RH, Tedersoo L, Abarenkov K, Ryberg M, Kristiansson E, Hartmann M, Schoch CL, Nylander JAA, Bergsten J, Porter TM, Jumpponen A, Vaishampayan P, Ovaskainen O, Hallenberg N, Bengtsson-Palme J, Eriksson KM, Larsson K-H, Larsson E (2012) Five simple guidelines for establishing basic authenticity and reliability of newly generated fungal ITS sequences. MycoKeys 4:37–63

Pautasso M (2013) Fungal under-representation is (slowly) diminishing in the life sciences. Fungal Ecol 6:129–135

Pennisi E (2008) “Proposal to ‘wikify’ GenBank meets stiff resistance”. Science 319:1598–1599

Queloz V, Grunig CR, Berndt R, Kowalski T, Sieber TN, Holdenrieder O (2011) Cryptic speciation in Hymenoscyphus albidus. For Pathol 41:133–142

Robbertse B, Schoch CL, Robert V et al. (2014) Finding needles in haystacks: linking scientific names, reference specimens and molecular data for Fungi. Database, in press

Rossman AY, Palm-Hernández ME (2008) Systematics of plant pathogenic fungi: why it matters. Plant Dis 10:1376–1386

Ryberg M, Kristiansson E, Sjökvist E, Nilsson RH (2009) An outlook on the fungal internal transcribed spacer sequences in GenBank and the introduction of a web-based tool for the exploration of fungal diversity. New Phytol 181:471–477

Samerpitak K, Van der Linde E, Choi HJ, Gerrits van den Ende AHG, Machouart M, Gueidan C, de Hoog GS (2014) Taxonomy of Ochroconis, a genus including opportunistic pathogens on humans and animals. Fungal Divers 65:89–126. doi: 10.1007/s13225-013-0253-6

Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

Schoch CL, Seifert KA, Huhndorf S et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc Natl Acad Sci U S A 109:6241–6246

Seifert K, Rossman AY (2010) How to describe a new fungal species. IMA Fungus 1:109–116

Sharma G, Kumar N, Weir BS, Hyde KD, Shenoy BD (2013) Apmat gene can resolve Colletotrichum species: a case study with Mangifera indica. Fungal Divers 61:117–138

Shenoy BD, Rajesh J, Hyde KD (2007) Impact of DNA sequence-data on the taxonomy of anamorphic fungi. Fungal Divers 26:1–54

Stajich JE, Berbee ML, Blackwell M, Hibbett DS, James TY, Spatafora JW, Taylor JW (2009) The fungi. Curr Biol 19:R840–R845

Tedersoo L, Abarenkov K, Nilsson RH, Schussler A, Grelet G-A, Kohout P, Oja J, Bonito GM, Veldre V, Jairus T, Ryberg M, Larsson K-H, Kõljalg U (2011) Tidying up international nucleotide sequence databases: ecological, geographical, and sequence quality annotation of ITS sequences of mycorrhizal fungi. PLoS One 6:e24940

Udayanga D, Liu XX, Crous PW, McKenzie EHC, Chukeatirote E, Hyde KD (2012) A multi-locus phylogenetic evaluation of Diaporthe (Phomopsis). Fungal Divers 56:157–171

Unterseher M, Peršoh D, Schnittler M (2013) Leaf-inhabiting endophytic fungi of European Beech (Fagus sylvatica L.) co-occur in leaf litter but are rare on decaying wood of the same host. Fungal Divers 60:43–54

U’Ren JM, Dalling JW, Gallery RE, Maddison DR, Davis EC, Gibson CM, Arnold EA (2009) Diversity and evolutionary origins of fungi associated with seeds of a neotropical pioneer tree: a case study for analyzing fungal environmental samples. Mycol Res 113:432–449

Woudenberg JHC, Groenewald JZ, Binder M, Crous PW (2013) Alternaria redefined. Stud Mycol 75:171–212