Abstract
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.
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References
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
Artigas HFJ (1984) Manual Fitosanitario síntomas y signos de daño. Forestal Mininco SA, Superintendencia Técnica, Concepción
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
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
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
Craw RC, Gehan JR, Heads MJ (1999) Panbiogeography: tracking the history of life. Oxford University Press, New York
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 Aires
Fox RTV (2000) Biology and life cycle. In: Fox RTV (ed) Armillaria root rot: biology and control of honey fungus. Intercept, Andover, England, pp 3–44
Garrido N (1988) Agaricales s.l. und ihre Mykorrhizen in den Nothofagus-Wäldern Mittelchiles. Bibl Mycol 120:1–528
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 10–20
Harrington TC, Wingfield BD (1995) A PCR based identification method for species of Armillaria. Mycologia 87:280–288. doi:10.2307/3760915
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 81–85
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
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 122–149
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 Aires
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
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
Kauserud H, Schumacher T (2001) Outcrossing or inbreeding: DNA markers provide evidence for type of reproductive mode in Phellinus nigrolimitatus (Basidiomycota). Mycol Res 53:220–230
Kile GA, Watling R (1981) An expanded concept of Armillaria luteobubalina. Trans Br Mycol Soc 77:75–83
Kile GA, Watling R (1983) Armillaria species from South-Eastern Australia. Trans Br Mycol Soc 81:129–140
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 91:305–315
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 102–121
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 411–436
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
Korhonen K (1978) Interfertility and clonal size in the Armillaria mellea complex. Karstenia 18:31–42
Lima MLA, Asai T, Capelari M (2008) Armillaria paulensis: a new South American species. Mycol Res. doi:10.1016/j.mycres.2008.03.006
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
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
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
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
Posada D, Crandall KA (1998) Modeltest: the model of DNA substitution. Bioinformatics 14:817–818. doi:10.1093/bioinformatics/14.9.817
Ramírez GO (1990) Guía de reconocimiento de plagas y enfermedades en plantaciones forestales. Conaf, Santiago
Ramírez GO, Baldini UA, Friz CR (1992) Daños bióticos y abióticos en eucalipto: guía de reconocimiento. Monteáguila SA, Conaf, Corma X Región, Chile
Singer R (1953) Four years of mycological work in southern South America. Mycologia 45:865–891
Singer R (1956) The Armillariella mellea Group. Lloydia 19:176–187
Singer R (1969) Mycoflora Australis. Beih Nova Hedwigia 29:40–49
Singer R (1970) Flora Neotropica Monograph n° 3, Omphalinae. Hafner, New York
Smith AG, Briden JC (1977) Mesozoic and Cenozoic Paleocontinental Maps. Cambridge University Press, Cambridge
Swofford DL (2000) PAUP* 4.0: phylogenetic analysis using parsimony. Sinauer Associates, Sunderland, Mass.
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
van Steenis CGGJ (1971) Nothofagus, key genus to plant geography, in time and space, living and fossil, ecology and phylogeny. Blumea 19:65–98
Volk TJ, Burdsall HH (1995) A nomenclatural study of Armillaria and Armillariella species (Basidiomycotina, Tricholomataceae). Fungiflora, Førde, Norway
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 615–322
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 Austin
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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.
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Pildain, M.B., Coetzee, M.P.A., Rajchenberg, M. et al. Molecular phylogeny of Armillaria from the Patagonian Andes. Mycol Progress 8, 181–194 (2009). https://doi.org/10.1007/s11557-009-0590-8
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DOI: https://doi.org/10.1007/s11557-009-0590-8