Mycological Progress

, 8:181 | Cite as

Molecular phylogeny of Armillaria from the Patagonian Andes

  • M. B. PildainEmail author
  • M. P. A. Coetzee
  • M. Rajchenberg
  • R. H. Petersen
  • M. J. Wingfield
  • B. D. Wingfield
Original Article


A number of species in the plant pathogen genus Armillaria are known from South America where they cause root rot disease on a wide variety of hosts. Knowledge pertaining to phylogenetic relationships of these species with those of other Armillaria species is almost non-existent. In addition, very few cultures representing these species are available, making DNA-based phylogenetic analyses impossible. The aim of this study was to characterise a collection of Armillaria isolates from the Patagonian Andes using DNA sequences and to determine their phylogenetic relationships with other Armillaria species. DNA sequences were obtained from the internal transcribed regions (ITS1, 5.8S and ITS4) and ribosomal large subunit (LSU) gene and used in phylogenetic analyses. Phylogenetic trees generated from the sequences separated the Armillaria isolates into four lineages. Lineages I and II represented A. novae-zelandiae and A. luteobubalina, respectively. Isolates belonging to A. novae-zelandiae from Malaysia, New Zealand, Australia and South America showed considerable intra-clade sub-structure. Lineages III and IV are probably distinct species and are most closely related to A. hinnulea and an unnamed species isolated from New Zealand and Kenya. This is the first comprehensive study of the phylogenetic relationships of Armillaria species from Patagonia and it provides a foundation for future research in this region.


Armillaria luteobubalina Armillaria novae-zelandiae Armillaria hinnulea Patagonia Nothofagus 



The authors thank the National Research Council of Argentina (CONICET), members of the Tree Protection Co-operative Programme (TPCP) and the NRF/DST Centre of Excellence in Tree Health Biotechnology (CTHB), South Africa, for financial support.


  1. 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. doi: 10.1093/nar/25.17.3389 PubMedCrossRefGoogle Scholar
  2. Artigas HFJ (1984) Manual Fitosanitario síntomas y signos de daño. Forestal Mininco SA, Superintendencia Técnica, ConcepciónGoogle Scholar
  3. Coetzee MPA, Wingfield BD, Harrington TC, Dalevi D, Coutinho TA, Wingfield MJ (2000) Geographical diversity of Armillaria mellea s.s. based on phylogenetic analysis. Mycologia 92:105–113. doi: 10.2307/3761454 CrossRefGoogle Scholar
  4. Coetzee MPA, Wingfield BD, Bloomer P, Ridley GS, Kile GA, Wingfield MJ (2001) Phylogenetic relationships of Australian and New Zealand Armillaria species. Mycologia 93:887–896. doi: 10.2307/3761754 CrossRefGoogle Scholar
  5. Coetzee MPA, Wingfield BD, Bloomer P, Ridley GS, Wingfield MJ (2003) Molecular identification and phylogeny of Armillaria isolates from South America and Indo-Malaysia. Mycologia 95:285–293. doi: 10.2307/3762039 CrossRefGoogle Scholar
  6. Craw RC, Gehan JR, Heads MJ (1999) Panbiogeography: tracking the history of life. Oxford University Press, New YorkGoogle Scholar
  7. Dimitri MJ, Leonardis RFJ, Biloni JS (1997) El nuevo libro del árbol. Tomo I: especies forestales de la Argentina occidental, 2da. Edición, El Ateneo Buenos AiresGoogle Scholar
  8. Fox RTV (2000) Biology and life cycle. In: Fox RTV (ed) Armillaria root rot: biology and control of honey fungus. Intercept, Andover, England, pp 3–44Google Scholar
  9. Garrido N (1988) Agaricales s.l. und ihre Mykorrhizen in den Nothofagus-Wäldern Mittelchiles. Bibl Mycol 120:1–528Google Scholar
  10. Guillaumin JJ, Anderson JB, Korhonen K (1991) Life cycle, infertility, and biological species. In: Shaw CG, Kile GA (eds) Armillaria root disease, Agricultural Handbook no. 691. USDA Forest Service, Washington DC, p 10–20Google Scholar
  11. Harrington TC, Wingfield BD (1995) A PCR based identification method for species of Armillaria. Mycologia 87:280–288. doi: 10.2307/3760915 CrossRefGoogle Scholar
  12. Harrington TC, Worrall JJ, Baker FA (1992) Armillaria. In: Singleton LL, Mihail JD, Rush CM (eds) Methods for research on soilborne phytopathogenic fungi. APS Press, St Paul, Minnesota, pp 81–85Google Scholar
  13. Hill RS (2001) Biogeography, evolution and palaeoecology of Nothofagus (Nothofagaceae): the contribution of the fossil record. Aust J Bot 49:321–332. doi: 10.1071/BT00026 CrossRefGoogle Scholar
  14. Hood IA, Redfern DB, Kile GA (1991) Armillaria in planted hosts. In: Shaw CG III, Kile GA (eds) Armillaria root disease, Agricultural Handbook no. 691, USDA Forest Service, Washington DC, p 122–149Google Scholar
  15. Horak E (1979) Flora criptogámica de Tierra del Fuego. Fungi: Basidiomycetes agaricales y Gasteromycetes secotioides. Tomo XI, fascículo. Fundación para la Educación, la Ciencia y la Cultura, Buenos AiresGoogle Scholar
  16. Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294:2310–2314. doi: 10.1126/science.1065889 PubMedCrossRefGoogle Scholar
  17. Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518. doi: 10.1093/nar/gki198 PubMedCrossRefGoogle Scholar
  18. Kauserud H, Schumacher T (2001) Outcrossing or inbreeding: DNA markers provide evidence for type of reproductive mode in Phellinus nigrolimitatus (Basidiomycota). Mycol Res 53:220–230Google Scholar
  19. Kile GA, Watling R (1981) An expanded concept of Armillaria luteobubalina. Trans Br Mycol Soc 77:75–83Google Scholar
  20. Kile GA, Watling R (1983) Armillaria species from South-Eastern Australia. Trans Br Mycol Soc 81:129–140Google Scholar
  21. Kile GA, Watling R (1988) Identification and occurrence of Australian Armillaria species, including A. pallidula sp. nov. and comparative studies between them and non-Australian tropical and Indian Armillaria. Trans Br Mycol Soc 91:305–315CrossRefGoogle Scholar
  22. Kile GA, McDonald GI, Byler JW (1991) Ecology and disease in natural forests. In: Shaw CG, Kile GA (eds) Armillaria root disease. Agricultural Handbook no. 691, USDA Forest Service, Washington DC, p 102–121Google Scholar
  23. Kile GA, Guillaumin JJ, Mohammed C, Watling R (1994) Biogeography and pathology of Armillaria. In: Johanson M, Stenlid J (eds).Proceedings of the Eigth International Conference on Root and Butt Rots. Uppsala, Sweden: Swedish University of Agricultural Sciences, S-750 07, p 411–436Google Scholar
  24. Kim MS, Klopfenstein NB, Hanna JW, McDonald GI (2006) Characterization of North American Armillaria species: genetic relationships determined by ribosomal DNA sequences and AFLP markers. For Pathol 36:145–164. doi: 10.1111/j.1439-0329.2006.00441.x Google Scholar
  25. Korhonen K (1978) Interfertility and clonal size in the Armillaria mellea complex. Karstenia 18:31–42Google Scholar
  26. Lima MLA, Asai T, Capelari M (2008) Armillaria paulensis: a new South American species. Mycol Res. doi: 10.1016/j.mycres.2008.03.006
  27. Maphosa L, Wingfield BD, Coetzee MPA, Mwenje E, Wingfield MJ (2006) Phylogenetic relationships among Armillaria species inferred from partial elongation factor 1-alpha DNA sequence data. Australas Plant Pathol 53:513–520. doi: 10.1071/AP06056 CrossRefGoogle Scholar
  28. Moncalvo JM, Lutzoni FM, Rehner SA, Johnson J, Vilgalys R (2000) Phylogenetic relationships of agaric fungi based on nuclear large subunit ribosomal DNA sequences. Syst Biol 49:278–305. doi: 10.1080/10635159950173852 PubMedCrossRefGoogle Scholar
  29. Mwenje E, Wingfield BD, Coetzee MPA, Nemato H, Wingfield MJ (2006) Armillaria species on tea in Kenya identified using isozyme and DNA sequence comparisons. Plant Pathol 55:343–350. doi: 10.1111/j.1365-3059.2006.01347.x CrossRefGoogle Scholar
  30. Pérez-Sierra A, Guillaumin JJ, Spooner BM, Bridge PD (2004) Characterization of Armillaria heimii from Africa. Plant Pathol 53:220–230. doi: 10.1111/j.0032-0862.2004.00999.x CrossRefGoogle Scholar
  31. Posada D, Crandall KA (1998) Modeltest: the model of DNA substitution. Bioinformatics 14:817–818. doi: 10.1093/bioinformatics/14.9.817 PubMedCrossRefGoogle Scholar
  32. Ramírez GO (1990) Guía de reconocimiento de plagas y enfermedades en plantaciones forestales. Conaf, SantiagoGoogle Scholar
  33. Ramírez GO, Baldini UA, Friz CR (1992) Daños bióticos y abióticos en eucalipto: guía de reconocimiento. Monteáguila SA, Conaf, Corma X Región, ChileGoogle Scholar
  34. Singer R (1953) Four years of mycological work in southern South America. Mycologia 45:865–891Google Scholar
  35. Singer R (1956) The Armillariella mellea Group. Lloydia 19:176–187Google Scholar
  36. Singer R (1969) Mycoflora Australis. Beih Nova Hedwigia 29:40–49Google Scholar
  37. Singer R (1970) Flora Neotropica Monograph n° 3, Omphalinae. Hafner, New YorkGoogle Scholar
  38. Smith AG, Briden JC (1977) Mesozoic and Cenozoic Paleocontinental Maps. Cambridge University Press, CambridgeGoogle Scholar
  39. Swofford DL (2000) PAUP* 4.0: phylogenetic analysis using parsimony. Sinauer Associates, Sunderland, Mass.Google Scholar
  40. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. doi: 10.1093/molbev/msm092 PubMedCrossRefGoogle Scholar
  41. van Steenis CGGJ (1971) Nothofagus, key genus to plant geography, in time and space, living and fossil, ecology and phylogeny. Blumea 19:65–98Google Scholar
  42. Volk TJ, Burdsall HH (1995) A nomenclatural study of Armillaria and Armillariella species (Basidiomycotina, Tricholomataceae). Fungiflora, Førde, NorwayGoogle Scholar
  43. White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MS, Gelfand DH (eds) PCR protocols: a guide to methods and applications, City Publisher, pp 615–322Google Scholar
  44. Zwickl D (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD thesis, University of Texas at AustinGoogle Scholar

Copyright information

© German Mycological Society and Springer 2009

Authors and Affiliations

  • M. B. Pildain
    • 1
    Email author
  • M. P. A. Coetzee
    • 2
  • M. Rajchenberg
    • 1
  • R. H. Petersen
    • 3
  • M. J. Wingfield
    • 2
  • B. D. Wingfield
    • 2
  1. 1.Forest Protection AreaCentro de Investigación y Extensión Forestal Andino Patagónico (CIEFAP), Esquel, ArgentinaChubutArgentina
  2. 2.Department of Genetics, Forestry and Agricultural Biotechnology Institute (FABI)University of PretoriaPretoriaSouth Africa
  3. 3.Ecology and Evolutionary BiologyUniversity of TennesseeKnoxvilleUSA

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