Skip to main content
Log in

DNA barcoding and phylogenetic analyses of the genus Coleosporium (Pucciniales) reveal that the North American goldenrod rust C. solidaginis is a neomycete on introduced and native Solidago species in Europe

  • Original Article
  • Published:
Mycological Progress Aims and scope Submit manuscript

Abstract

Recently, an unknown rust fungus of the genus Coleosporium appeared in Germany and Switzerland on giant goldenrod, Solidago gigantea, an invasive neophyte from North America, and on the indigenous European goldenrod, S. virgaurea. For identification, DNA barcodes were assembled in the course of the German Barcode of Life (GBOL) project and the investigation of neomycetes in Switzerland. Phylogenetic analyses were performed using ITS and LSU sequences of Coleosporium species representing various host plants and geographic regions. These analyses resulted in the first molecular evidence of the North American rust Coleosporium solidaginis in Europe. Coleosporium solidaginis is split into two subclades that are closely related to Coleosporium asterum, a species on Aster s.l., which was formerly synonymized with C. solidaginis. The genus is divided into an American and a Eurasian clade. This phylogenetic pattern indicates that the geographic distribution, rather than the relationship with host plants, played a major role in the evolution of Coleosporium species. This finding particularly applies to the European species, which are genetically uniform according to the ITS and LSU sequences. Taxonomical consequences are discussed. Coleosporium solidaginis is fragmentarily distributed in Europe. The place of its introduction and host shift to S. virgaurea remains uncertain. Life cycle and propagation are mainly restricted to asexual urediniospores. Telia were found only once and the aecial stage was not observed at all on pine trees. The ecological impact of this neomycete is still unknown, but C. solidaginis has the potential to harm wild and cultivated goldenrods in Europe.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Notes

  1. Neomycetes were originally defined as introduced alien fungi that had established in a new area after 1492 (Kreisel and Scholler 1994). Other authors (e.g., Beenken and Senn-Irlet 2016; Klenke and Scholler 2015) have used the term in a broader sense, including also non-established ephemeral fungi.

  2. The S. canadensis record from SW Germany by Klenke and Scholler (2015) was revised by one of the authors of the present study (M.S.) and was determined as S. gigantea.

  3. The record includes a photo of the infected plant and a photo of urediniospores viewed through a microscope. Therefore, we consider this a valid record and the first one from Europe, even though it was not published in a scientific journal.

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Arthur JC (1907) Uredinales, Coleosporiaceae, Uredinaceae, Aecidiaceae (pars). North Am Flora 7(2):83–95

    Google Scholar 

  • Arthur JC (1924) Uredinales, additions and corrections (concluded). North Am Flora 7(9):649–668

    Google Scholar 

  • Arthur JC (1927) Uredinales, additions and corrections. North Am Flora 7(12):797–848

    Google Scholar 

  • Arthur JC (1962) Manual of the rusts in United States and Canada. Hafner Publishing Company, New York, 438 pp

    Google Scholar 

  • Arthur JC, Bisby GR (1918) An annotated translation of the part of Schweinitz’s two papers giving the rusts of North America. Proc Am Phil Soc 57(3):173–292

    Google Scholar 

  • Back C-G, Nam G-Y, Lee S-Y, Jung H-Y (2014) Outbreak of rust caused by Coleosporium asterum on Solidago virgaurea var. gigantea in Ulleung-do. Mycobiology 42(1):79–81

    Article  PubMed  PubMed Central  Google Scholar 

  • Bahcecioglu Z, Kabaktepe S (2012) Checklist of rust fungi in Turkey. Mycotaxon 119:494. http://www.mycotaxon.com/resources/checklists/Bahcecioglu-v119-checklist.pdf

    Google Scholar 

  • Baranyay JA, Bourchier RJ, Stevenson GR (1962) Province of Alberta. Forest disease conditions. In: Annual report of the forest insect and disease survey 1962. Can Dep Forest, Ottawa, pp 99–105

  • Beenken L (2017) First records of the powdery mildews Erysiphe platani and E. alphitoides on Ailanthus altissima reveal host jumps independent of host phylogeny. Mycol Prog 16:135–143

    Article  Google Scholar 

  • Beenken L, Senn-Irlet B (2016) Neomyceten in der Schweiz, Stand des Wissens und Abschätzung des Schadpotentials der mit Pflanzen assoziierten gebietsfremden Pilze. WSL Berichte 50, pp 1–93. https://www.dora.lib4ri.ch/wsl/islandora/object/wsl:9106

  • Beenken L, Zoller S, Berndt R (2012) Rust fungi on Annonaceae II: the genus Dasyspora Berk. & M.A. Curtis. Mycologia 104:659–681

    Article  CAS  PubMed  Google Scholar 

  • Boerema GH, Verhoeven AA (1972) Check-list for scientific names of common parasitic fungi. Series 1a: Fungi on trees and shrubs. Neth J Plant Pathol 78(Suppl 1):1–55

    Article  Google Scholar 

  • Braun U (1982) Die Rostpilze (Uredinales) der Deutschen Demokratischen Republik. Feddes Repert 93:213–333

    Article  Google Scholar 

  • Braun U, Cook RTA (2012) Taxonomic manual of the Erysiphales (powdery mildews), CBS Biodiversity Series, vol 11. CBS, Utrecht

    Google Scholar 

  • Brodtbeck T (2017) Coleosporium asterum (Dietel) Syd. & P. Syd. (Pucciniales, Pucciniomycota), pp 135–138. In: Kruse J et al. Bemerkenswerte Funde phytoparasitischer Pilze (7). Z Mykol 83(1):127–156

  • Brown JKM, Hovmøller MS (2002) Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297:537–541

    Article  CAS  PubMed  Google Scholar 

  • Bufford JL, Hulme PE, Sikes BA, Cooper JA, Johnston PR, Duncan RP (2016) Taxonomic similarity, more than contact opportunity, explains novel plant–pathogen associations between native and alien taxa. New Phytol 212:657–667. https://doi.org/10.1111/nph.14077

    Article  CAS  PubMed  Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    Article  CAS  PubMed  Google Scholar 

  • Clinton GP (1908) Report of the botanist for 1907 III. Heteroecious rusts of Connecticut having a Peridermium for their aecial stage. Rep Connecticut Agric Exp Sta: 368–396, plates XXV–XXXII

  • Cummins GB (1962) Supplement to Arthur’s manual of the rusts in United States and Canada. In: Arthur JC (ed) Manual of the rusts in United States and Canada. Hafner Publishing Company, New York, pp 1A–24A

    Google Scholar 

  • Cummins GB (1978) Rust fungi on legumes and composites in North America. University of Arizona Press, Tucson

    Google Scholar 

  • Dietel P (1900) Uredineae japonicae I. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie. Bot Jahrb Syst 27:564–576, plate VIII

    Google Scholar 

  • Farr DF, Rossman AY (2017) Fungal databases, systematic mycology and microbiology laboratory, ARS, USDA. Retrieved 15 May 2017, from https://nt.ars-grin.gov/fungaldatabases/fungushost/fungushost.cfm

  • Frantzen J, Müller-Schärer H (2006) Modeling the impact of a biocontrol agent, Puccinia lagenophorae, on interactions between a crop, Daucus carota, and a weed, Senecio vulgaris. Biol Control 37:301–306

    Article  Google Scholar 

  • Gäumann E (1959) Die Rostpilze Mitteleuropas mit besonderer Berücksichtigung der Schweiz. Beitr Kryptogamenflora Schweiz 12:1–1407

    Google Scholar 

  • Geiger MF, Astrin JJ, Borsch T, Burkhardt U, Grobe P, Hand R, Hausmann A, Hohberg K, Krogmann L, Lutz M, Monje C, Misof B, Morinière J, Müller K, Pietsch S, Quandt D, Rulik B, Scholler M, Traunspurger W, Haszprunar G, Wägele W (2016) How to tackle the molecular species inventory for an industrialized nation—lessons from the first phase of the German Barcode of Life initiative GBOL (2012–2015). Genome 59(9):661–670

    Article  CAS  PubMed  Google Scholar 

  • Ginns JH (1986) Compendium of plant disease and decay fungi in Canada 1960–1980. Res Br Can Agric Publ 1813:1–416

    Google Scholar 

  • Gudžinskas Z, Žalneravičius E (2016) Solidago × snarskisii nothosp. nov. (Asteraceae) from Lithuania and its position in the infrageneric classification of the genus. Phytotaxa 253(2):147–155

    Article  Google Scholar 

  • Hantula J, Scholler M (2013) NOBANIS—invasive alien species fact sheet—Melampsoridium hiratsukanum. From: online database of the European Network on Invasive Alien Species—NOBANIS. https://www.nobanis.org/fact-sheets/. Accessed 15 May 2017

  • Heath MC (1992) Host species specificity of the goldenrod rust fungus and the existence of rust resistance within some goldenrod species. Can J Bot 70:2461–2466

    Article  Google Scholar 

  • Hedgcock GG, Hunt NR (1922) Notes on some species of Coleosporium: II. Mycologia 14(6):297–310

    Article  Google Scholar 

  • Heger T, Böhmer HJ (2005) The invasion of Central Europe by Senecio inaequidens DC. Erdkunde 59:34–49

    Article  Google Scholar 

  • Helfer S (2013) Coleosporium in Europe. Mycotaxon 124:87–99

    Article  Google Scholar 

  • Hennen JF, Figueiredo MB, de Carvalho AA Jr, Hennen PG (2005) Catalogue of the species of plant rust fungi (Uredinales) of Brazil. Jardim Botanico do Rio de Janeiro, Rio de Janeiro. https://aplicacoes.jbrj.gov.br/publica/livros_pdf/catalogue.pdf

  • Hunt WR (1926) The Uredinales or rusts of Connecticut and the other New England states. Connecticut State Geol Surv Bull 36:1–198

    Google Scholar 

  • Huson DH, Richter DC, Rausch C, Dezulian T, Franz M, Rupp R (2007) Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinformatics 8:460

    Article  PubMed  PubMed Central  Google Scholar 

  • Hylander N, Jørstad I, Nannfeldt JA (1953) Enumeratio uredinearum Scandinavicarum. Opera Bot 1:1–102

    Google Scholar 

  • Index Fungorum (2017) http://www.indexfungorum.org. Accessed January 2017

  • Kabaktepe S (2010) Kars ve Ardahan Yoresi vaskuler bitkiler uzerinde tespit edilen mikrofunguslar. Inonu Universitesi Fen Bilimleri Enstitusu. Phd thesis, Malatya

  • Kaneko S (1981) The species of Coleosporium, the causes of pine needle rusts, in the Japanese Archipelago. Rep Tollori Mycol lnst 19:1–159

    Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780. https://doi.org/10.1093/molbev/mst010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 30:3059–3066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Ainsworth & Bisby’s dictionary of the fungi, 10th edn. CAB International, Wallingford

    Book  Google Scholar 

  • Klebahn H (1914) Kulturversuche mit Rostpilzen XV. Z Pflanzenkrankh 24:1–32

    Google Scholar 

  • Klenke F, Scholler M (2015) Pflanzenparasitische Kleinpilze. Springer, Berlin

    Book  Google Scholar 

  • Kolmer JA (2005) Tracking wheat rust on a continental scale. Curr Opin Plant Biol 8:441–449

    Article  PubMed  Google Scholar 

  • Kołodziej B (2009) Optimalisation of mineral fertilization in goldenrod (Solidago virgaurea L. ssp. virgaurea) cultivated for pharmaceutical purposes. Acta Sci Pol Hortorum Cultus 8(1):27–36

    Google Scholar 

  • Kowarik I, Rabitsch W (2010) Biologische Invasionen: Neophyten und Neozoen in Mitteleuropa. Eugen Ulmer, Stuttgart

    Google Scholar 

  • Kreisel H, Scholler M (1994) Chronology of phytoparasitic fungi introduced to Germany and adjacent countries. Bot Acta 107:387–392

    Article  Google Scholar 

  • Large E (2003) The advance of the fungi. APS Press, St. Paul, MN

    Google Scholar 

  • Laundon GF (1978) A Coleosporium rust new to New Zealand. Plant Dis Rep 62(9):796–797

    Google Scholar 

  • Maier W, Begerow D, Weiß M, Oberwinkler F (2003) Phylogeny of the rust fungi: an approach using nuclear large subunit ribosomal DNA sequences. Can J Bot 81:12–23

    Article  CAS  Google Scholar 

  • Mains EB (1916) The wintering of Coleosporium solidaginis. Phytopathology 6:371–372

    Google Scholar 

  • Majewski T, Ruszkiewicz-Michalska M (2008) Uredinales. In: Mulenko W et al (eds) A preliminary checklist of micromycetes in Poland. W. Szafer Institute of Botany, Krakow, pp 263–297

    Google Scholar 

  • McKenzie EHC (1998) Rust fungi of New Zealand—an introduction, and list of recorded species. N Z J Bot 36(2):233–271

    Article  Google Scholar 

  • McNeill J, Barrie FR, Burdet HM, Demoulin V, Hawksworth DJ, Marhold K, Nicolson DH, Prado J, Silva PC, Skog JE, Wiersema JH, Turland NJ (2006) International Code of Botanical Nomenclature (Vienna Code). Regnum Vegetabile 146(i–xviii):1–568

    Google Scholar 

  • McNeill J, Barrie FR, Buck WR, Demoulin V, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Marhold K, Prado J, Prud’homme Van Reine WF, Smith GF, Wiersema JH, Turland NJ (2012) International Code of Nomenclature for algae, fungi and plants (Melbourne Code) adopted by the Eighteenth International Botanical Congress Melbourne, Australia, July 2011. Koeltz Scientific Books, Regnum Vegetabile 154: i–xxx, 1–208. http://www.iapt-taxon.org/nomen/main.php

  • McTaggart AR, Shivas RG, van der Nest MA, Roux J, Wingfield BD, Wingfield MJ (2016) Host jumps shaped the diversity of extant rust fungi (Pucciniales). New Phytol 209:1149–1158

    Article  PubMed  Google Scholar 

  • Menéndez JL, Rubio E (2012) https://www.asturnatura.com/fotografia/setas-hongos/coleosporium-asterum-dietel-syd-p-syd-1/13863.html. Accessed 7 Feb 2017

  • Mihail JD, Bruhn JN, Meyer TR, Bell FW (2002) Pine needle rust effect on Pinus banskiana in response to interspecific plant competition and telial host density. Can J For Res 32(8):1372–1380

    Article  Google Scholar 

  • Nehring S, Kowarik I, Rabitsch W, Essl F (eds) (2013) Naturschutzfachliche Invasivitätsbewertungen für in Deutschland wild lebende gebietsfremde Gefäßpflanzen. BfN-Skripten 352:1–202

  • Nicholls TH, Patton RF, Van Arsdel EP (1968) Life cycle and seasonal development of Coleosporium pine needle rust in Wisconsin. Phytopathology 58:822–829

    Google Scholar 

  • Palm ME, Rossman AY (2003) Invasion pathways of terrestrial plant-inhabiting fungi. In: Ruiz GM, Carleton JT (eds) Invasive species: vectors and management strategies. Island Press, Washington, DC, pp 31–43

    Google Scholar 

  • Pfunder M, Schürch S, Roy BA (2001) Sequence variation and geographic distribution of pseudoflower-forming rust fungi (Uromyces pisi s. lat.) on Euphorbia cyparissias. Mycol Res 105:57–66

    Article  CAS  Google Scholar 

  • Pliszko A, Zalewska-Gałosz J (2016) Molecular evidence for hybridization between invasive Solidago canadensis and native S. virgaurea. Biol Invasions 18:3103–3108

    Article  Google Scholar 

  • Santini A, Ghelardini L, De Pace C, Desprez-Loustau ML, Capretti P, Chandelier A, Cech T, Chira D, Diamandis S, Gaitniekis T, Hantula J, Holdenrieder O, Jankovsky L, Jung T, Jurc D, Kirisits T, Kunca A, Lygis V, Malecka M, Marcais B, Schmitz S, Schumacher J, Solheim H, Solla A, Szabò I, Tsopelas P, Vannini A, Vettraino AM, Webber J, Woodward S, Stenlid J (2013) Biogeographical patterns and determinants of invasion by forest pathogens in Europe. New Phytol 197:238–250

    Article  CAS  PubMed  Google Scholar 

  • Schenk R, Lück L (2012) Goldrute, Echte (Solidago virgaurea L.), pp. 488–500. In: Hoppe B (ed) Handbuch des Arznei- und Gewürzpflanzenbaus. Band 4. Verein für Arznei- und Gewürzpflanzen Saluplanta e.V., Bernburg, Germany

  • Schmitz G, Werner DJ (2001) The importance of the alien plant Senecio inaequidens DC. (Asteraceae) for phytophagous insects. Z Ökol Nat 9(3):153–160

    Google Scholar 

  • Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W; Fungal Barcoding Consortium (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc Nat Acad Sci U S A 109:6241–6246

    Article  CAS  Google Scholar 

  • Scholler M, Hemm V, Lutz M (2012) Erysiphe platani: monitoring of an epidemic spread in Germany and molecular characterization based on rDNA sequence data. Andrias 19:263–272

    Google Scholar 

  • Scholler M, Schmidt A, Siahaan SAS, Takamatsu S, Braun U (2016) A taxonomic and phylogenetic study of the Golovinomyces biocellatus complex (Erysiphales, Ascomycota) using asexual state morphology and rDNA sequence data. Mycol Prog 15:56. https://doi.org/10.1007/s11557-016-1197-5

    Article  Google Scholar 

  • Schweinitz LD (1822) Synopsis fungorum Carolinae superioris. Schr Naturf Ges Leipzig 1:20–131

    Google Scholar 

  • Senn-Irlet BJ, Gross A, Blaser S (2017) SwissFungi: national data- and information center for the fungi of Switzerland (database). Version 2. Birmensdorf, Swiss Federal Institute WSL. http://www.swissfungi.ch. Accessed 24 Jan 2017

  • Shivas R, Beasley D, McTaggart A (2017) Rust Fungi of Australia. http://collections.daff.qld.gov.au/web/key/rustfungi/Media/Html/index.html

  • Sieber TN (2014) Neomyzeten—eine anhaltende Bedrohung für den Schweizer Wald. Schweiz Z Forstwes 165(6):173–182

    Article  Google Scholar 

  • Spinelli C (2016) Favolaschia calocera, un fungo tropici in marcia verso nord, ora anche Ticino. SZP/BSM 3:13–15

    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  CAS  PubMed  Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57:758–771

    Article  PubMed  Google Scholar 

  • Sydow H, Sydow P (1914) Beitrag zur Kenntnis der parasitischen Pilze der Insel Formosa. Ann Mycol 12(2):105–112

    Google Scholar 

  • Tai FL (1979) Sylloge Fungorum Sinicorum. Science Press, Academia Sinica, Peking

    Google Scholar 

  • Tanner RA, Pollard KM, Varia S, Evans HC, Ellison CA (2015) First release of a fungal classical biocontrol agent against an invasive alien weed in Europe: biology of the rust, Puccinia komarovii var. glanduliferae. Plant Pathol 64:1130–1139

    Article  Google Scholar 

  • Thite SV, Hande PR, Kore BA (2016) Occurrence of rust on Solidago canadensis, a new host record for Coleosporium asterum from India. Plant Pathol Quarant 6(1):43–46

    Article  Google Scholar 

  • Thümen F (1878) New species of North American Uredinei. Bull Torrey Bot Club 6(39):215–216

    Article  Google Scholar 

  • Van Reenen M (1995) An annotated list of Urediniomycetes (rust fungi) from South Africa 1: Melampsoraceae and Pucciniaceae, excluding Puccinia and Uromyces. Bothalia 25(2):173–181

    Google Scholar 

  • Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172(8):4238–4246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Viljanen-Rollinson SLH, Cromey MG (2002) Pathways of entry and spread of rust pathogens: implications for New Zealand’s biosecurity. N Z Plant Prot 55:42–48

    Google Scholar 

  • Vogel A (2017) http://www.avogel.ch/de/pflanzenlexikon/solidago_virgaurea.php. Accessed 7 Feb 2017

  • Wagenitz G (1979) Solidago L. In: Hegi G (ed) Illustrierte Flora von Mitteleuropa, 6 (3). Carl Hanser, München, pp 16–29

    Google Scholar 

  • Walker J, Priest MJ (1984) Coleosporium senecionis in Australia. New South Wales Department of Agriculture, Plant Disease Survey 1982–83, pp 28–29

  • Wang Q, Li X-L, Zhang J-Z (2017) First report of goldenrod rust caused by Coleosporium asterum in China. Plant Dis 101(2):389–389

    Article  Google Scholar 

  • Weber E (2013) Invasive Pflanzen der Schweiz. Haupt, Bern

    Google Scholar 

  • Weber E, Jakobs G (2005) Biological flora of central Europe: Solidago gigantea Aiton. Flora 200:109–118

    Article  Google Scholar 

  • Wilson M, Henderson DM (1966) British rust fungi. Cambridge University Press, Cambridge

    Google Scholar 

  • Zhuang J-Y (1983) A provisional list of Uredinales of Fujian Province, China. Acta Mycol Sin 2(3):146–158

    Google Scholar 

  • Zhuang W-Y (2001) Higher fungi of tropical China. Mycotaxon Ltd., Ithaca, New York

    Google Scholar 

  • Ziller WG (1974) The tree rusts of western Canada. Pacific Forest Research Centre, Victoria, BC. Publication 1329, 272 pp

Download references

Acknowledgements

The authors thank Beatrice Senn-Irlet and Valentin Queloz (WSL Birmensdorf) for their substantial support during the Swiss part of the study. Thomas Brodtbeck (Riehen near Basel) kindly shared locations of rust fungi in Switzerland. Jasmin Joshi (University of Potsdam) gave valuable information about neophytes in general and in particular about invasive goldenrods. Maxi Tomowski (University of Potsdam) kindly informed us about her observations of C. solidaginis in Constance. The authors thank Patrick Dornes, who collected and provided the first specimen from Central Europe. Many thanks go to the Genetic Diversity Centre (GDC) of the ETH Zurich, where the sequences of Swiss specimens were generated and all molecular data were analyzed. Melissa Dawes provided linguistic suggestions on the manuscript. The Swiss Federal Office for the Environment financed the first author’s (L.B.) involvement in this study (FOEN project 05.0040.PZ/O282-2391). DNA barcodes were determined within the framework of the German Barcode of Life (GBOL) project, which is supported by the German Federal Ministry of Education and Research (BMBF FKZ 01LI1501l to M.S.) as research for sustainable development (FONA, http://www.fona.de).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ludwig Beenken.

Additional information

Section Editor: Franz Oberwinkler

Electronic supplementary material

Below are the links to the electronic supplementary material.

ESM 1

(PDF 162 kb)

ESM 2

(DOCX 20 kb)

ESM 3

(DOCX 19 kb)

ESM 4

(PDF 269 kb)

ESM 5

(PDF 218 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Beenken, L., Lutz, M. & Scholler, M. DNA barcoding and phylogenetic analyses of the genus Coleosporium (Pucciniales) reveal that the North American goldenrod rust C. solidaginis is a neomycete on introduced and native Solidago species in Europe. Mycol Progress 16, 1073–1085 (2017). https://doi.org/10.1007/s11557-017-1357-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11557-017-1357-2

Keywords

Navigation