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Amylostereum and Echinodontium

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Amylostereum and Echinodontium 585 Mycoscience 41: 585-593, 2000 Molecular phylogeny of species in the genera Amylostereum and Echinodontium Masanobu Tabata 1), Thomas C. Harrington 21, Wei Chen 21 and Yasuhisa Abe 3) 1) Shikoku Research Center, Forestry and Forest Products Research Institute, 2-91 5 Asakura-nishi, Kochi 780-8077, Japan 2) Department of Plant Pathology, Iowa State University, Ames, Iowa 50011, U.S.A. 3) Forestry and Forest Products Research Institute, P. O. Box 16, Tsukuba, Ibaraki 305-8687, Japan Accepted for publication 18 September 2000 Analyses of DNA sequences from the internal transcribed spacer (ITS) region of the nuclear rDNA and from a portion of a manganese-dependent peroxidase gene were used to assess the species in Amylostereum, including isolates from the mycangia of horntails, decay, and basidiomes. Four species are recognized: A. areolatum, A. chailletii, A. laevigatum, and A. ferreum. An unidentified Amylostereum isolate from the mycangium of Xoanon matsumurae had an ITS se- quence identical to that of A. areolatum. Another unidentified Amylostereum isolate from the mycangium of Sirex areolatus was near A. laevigatum, which appears to be the mycangial symbiont for those horntails attacking cedar-like trees. The other horntail isolates, primarily from Pinaceae, proved to be either A. areolatum or A. chailletii. The DNA sequences of Echinodontium tinctorium, E. tsugicola and E. japonicum were similar to those of the Amylostereum spe- cies, and Amylostereum species are now recognized as members of the family Echinodontiaceae rather than the family Stereaceae. Echinodontium taxodii was found to be distinct from the Echinodontiaceae and Stereum, and E. taxodii is recognized as a Laurilia species. Key Words Amy/ostereum; Echinodontium; Echinodontiaceae; internal transcribed spacer; manganese-dependent peroxidase. Excluding Dextrinocystidium sacratum (G. H. Cunnin- (1998) placed Amylostereum in the monotypic family gham) S. H. Wu (1995), there are four recognized spe- Amylostereaceae. Analyses of sequences of mitochon- cies of Amylostereum (Stereaceae): A. areolatum (Fr.: drial small subunit rDNA (Hsiau, 1996) suggested an Fr.) Boidin, A. chailletii (Pers.: Fr.) Boidin, A. ferreum affinity between A. chailletii and a group of Aphyl- (Berk. & Curt.) Boidin & Lanquetin, and A. laevigatum Iophorales informally recognized as "group 2" by Hibbett (Fr.: Fr.) Boidin (Boidin and Lanquetin, 1984). All of the and Donoghue (1995). In comparing the sequences of Amylostereum species occur on coniferous trees. the internal transcribed spacer (ITS) region of the nuclear Amylostereum areolatum, A. chailletii, and A. laevigatum rDNA, the sequence of A. chailletii was found to be very are associated with wood decay of Pinaceae and other similar to the sequence of Echinodontium tinctorium (Ell. conifers in the Northern Hemisphere (Breitenbach and & Ev.) Ell. & Ev. (Harrington, unpublished). Kranzlin, 1988; Chamuris, 1988; Eriksson and Ryvarden, Gross (1964) monographed the monotypic family 1973; Eriksson et al., 1978; Ginns and Lefebvre, 1 993), Echinodontiaceae and recognized six Echinodontium spe- and A. ferreum decays wood of Podocarpus spp. in Latin cies with smooth to spinose hymenophores. Echinodon- America (Boidin and Lanquetin, 1984). Some tium tinctorium and E. tsugicola (P. Henn. & Shirai) Imaz. Amylostereum species are also known as symbionts of cause white heartrot of living Pinaceae in USA and mycophagus horntails [Sirex and Urocerus species, Japan, respectively (Gilbertson and Ryvarden, 1986). (Hymenoptera: Siricinae)], which carry their fungal sym- Echinodontium ballouii (Banker) Gross was described biont in mycangia and inoculate the wood of the plant from Chamaecyparis thyoides (L.) B. S. P. in the eastern host with hyphal fragments or arthrospores as they USA (Gross, 1964). Echinodontium japonicum Imaz. is oviposit (Gaut, 1969, 1 970; Sano et al., 1995; Tabata known to occur on Quercus spp. in Japan (Imazeki, and Abe, 1997; Tabata and Abe, 1999; Terashita, 1935). Two Echinodontium species, E. taxodii (Lentz & 1970). Mckay) Gross and E. sulcatum (Burt) Gross, are often The genus Amylostereum has been traditionally placed in the genus Laurilia, which is in the Stereaceae placed in the Stereaceae (Donk, 1964), and species in (Parmasto, 1968; Pouzar, 1959) or in the Echinodontia- Amylostereum superficially resemble Stereum. How- ceae (J•lich, 1981). ever, molecular systematics has called for re-evaluation We used phylogenetic analyses to re-evaluate the of many of the families of Aphyllophorales. Boidin et al. genera Amylostereum and Echinodontium. We se- 586 M. Tabata et al. 1- F, CO 7~ 1.1_ < ~'~, ~" ~ LO 0"~ O0 r~ ~1 O~ ~4 0 0 0 0 0 0 T- v- g~ oo oo oo oo ~o oO ~0 o0o0 OO en . e- ffl N N N ~ N N N NN 7~ oO < < < < < < < << t- O e- ~o 0 (3 o e- ~ 0 ~ ~ ~ ~ ~ ~0 n ~ ~ ~ ~ ~ ~0 ~ 000 e-I-- en . 0 0 0 < <<< < < < ~ <<~ ~ ~ E <~ ~ < m~ m m m m ~<<~ oo ._ ~.~ ~ ~< ._ .s o 0 ..J E t~ EEE -~ E ~ .~.~.~ E E E ~E e~.~= ~===~,&~-N-N-N ...... c'~ = = o o m ~ ~ E ~ t~ ~~ ~,~,~,~ ~'Z~ ~ ~ O~ :~:~~ ~~ o Q~ ~'~ ~ ~ ~ ~ ~ ~ o ~ ~ ~ ~ ~ ~ r- .~.~ ~ .~ ~ ..... ~,~,~ ~ ~ .-~ ~, ~~.0.,~~~~-~ ....~~ ~,,~ ~E ~=~ .~ .s ~~ ~.~ .~,~~.~.~ .~ .~~~~ ~ ,_ 0 0 "1- Q~ ~ ~ ~ ~0~ o ~0 e- 0 0~ 0~ ~ ~ o~8oo~8~8~ ~o~ ~gooo~~ooo o~~o ~- 6~ ~ ~ Q~ ~8 OZ ooo ~~mmaaaaaaa ~ 0 ~0~0~~~~ ~ Q~ ~~~~0~~ 0 0 ~z J~ E r- Q~ o 0 ~0 Molecular phylogeny of Amylosterem and Echinodontium 587 quenced the ITS regions and a portion of a peroxidase as outlined for the ITS sequences, except that 1000 gene from isolates obtained from the Institute for Fer- bootstrap replications were made. mentation, the Centraalbureau voor Schimmelcultures, the Canadian Collection of Fungal Cultures, and from iso- Results lates we obtained from horntails and woody substrata in Japan. We also examined the morphology of ITS sequences The ITS sequences of each of the basidiomes of A. laevigatum collected from Japan and Amylostereum species aligned well with each other. In Sweden. order to find potential outgroup taxa and identify genera that may be closely related to Amylostereum, we com- Materials and Methods pared these ITS sequences with those generated in our studies (Harrington et al., 1998) of Heterobasidion. Het- Isolates The source and substrate of isolates are given erobasidion and other genera were placed in "group 2" in Table 1. Extracted DNA of Stereum annosum Berk. & based on mitochondrial rDNA sequences (Hibbett and Br., S. hirsutum (Willd.: Fr.) S. F. Gray, and Bondarzewia Donoghue, 1995; Hsiau, 1996). Extracted DNA from montana (Fr.) Sing. was kindly provided by David Hib- representatives of group 2 genera was provided by Dr. D. bert. Hibbett, and we generated ITS sequences for representa- ITS sequences Mycelia were grown at room tempera- tives of Bondarzewia, Lentinellus, Auriscalpium, Herici- ture (20-25~ for 10-12 days in 15-20 ml of MY liquid urn, Echinodontium, and Russula. Of these genera, the medium (2~ malt extract, l~ yeast extract). A fresh ITS sequence of E. tinctorium matched closely to ITS se- mycelial mat was collected by vacuum filtration, ground quences of Amylostereum. We subsequently generated to a fine powder in liquid nitrogen with a mortar and pes- ITS sequences for isolates of E. tinctorium, E. tsugicola, tle, and DNA was extracted following the protocol of and E. japonicum, and these sequences were easily DeScenzo and Harrington (1994). Template DNA of aligned with those of Amylostereum species. However, most of the isolates was extracted from liquid cultures, the ITS sequence of E. taxodii did not match closely to but mycelia of three Amylostereum isolate (B29, B1358, those of the other Echinodontium species. Because B1360) were scraped lightly with a pipette tip for tem- Amylostereum has been placed in the Stereaceae, we plate DNA (Harrington and Wingfield, 1995). also included ITS sequences of two Stereum species in A fragment of nuclear rDNA about 700 bp long from the analyses, and the ITS sequence of Perenniporia the 3' end of the 18S (small subunit gene) to the 5' end of subacida (Pk.) Donk was also compared as a potential the 28S (large subunit gene) was amplified and se- outgroup taxon. quenced using the primers ITS1-F (Gardes and Bruns, In the complete data set of ITS sequences of 1993) and ITS4 (White et al., 1990). The polymerase Amylostereum, Echinodontium, Stereum, and P. subaci- chain reaction (PCR) products were purified using QIA- da, there were 614 aligned characters with the insertions quick PCR Purification Kit (QIAGEN Inc., USA) and se- of gaps. However, 261 of these characters were ex- quenced with the ABI PRISM 377 DNA sequencer (Per- cluded from the initial analysis because of ambiguous kin-Elmer) in the DNA Sequencing Facility at Iowa State alignment. Of the included characters, 259 were con- University. Both the coding and template strands were stant, 39 were parsimony uninformative, and 55 charac- sequenced, with complete overlap of the complementary ters were informative. Ten most parsimonious trees of sequences. Sequences were visually aligned and ana- 150 steps were found, with a consistency index (CI) of lyzed using heuristic searches in PAUP 4.0, with step- 0.8200, a retention index (RI) of 0.8767, and a rescaled wise additions (simple) and tree-bisection-reconnection consistency index (RC) of 0.7189 (Fig. 1). Perenniporia (Swofford, 1998). Uninformative characters were ig- subacida, the only polypored species studied, was select- nored. Gaps were coded as a newstate (fifth character) ed as an outgroup taxon, rooting the tree at an internal because the gaps were consistently found within species node with basal polytomy. and, except for outgroup taxa, most gaps were only one The ITS sequence of E. taxodii was quite distinct or two bases in length. Bootstrapping (100 bootstrap from those of the other ingroup taxa. Strong bootstrap replicates) was used to determine confidence in the support was found for the inferred clade that included branches. two Stereum species, the Amylostereum species, and Manganese-dependent peroxidase In an earlier study the Echinodontium species, exclusive of E.
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