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Home , Acanthobasidium, Acanthophysium, Aleurodiscus, Amylostereum, Amylostereum laevigatum, Laxitextum

Mycologia, 93(4), 2001, pp. 720-731. ? 2001 by The Mycological Society of America, Lawrence, KS 66044-8897

Phylogenetic analyses of s.l. and allied genera

Sheng-Hua Wu INTRODUCTION Department of Botany, National Museum of Natural AleurodiscusRabenh. exJ. Schrot. is a member of the Science, Taichung, Taiwan, ROC corticioid homobasidiomycetes. Seventy one David S. Hibbett1 world-wide have been accepted in Aleurodiscus (Nu- Manfred Binder fiez and Ryvarden 1997). The limits of Aleurodiscus have been controversial. Lemke (1964) excluded Department of Biology, Clark University, taxa with inamyloid from Aleurodiscus sensu 950 Main Street, Worcester,MA 01610-1477 stricto. In contrast, Nunfiez and Ryvarden (1997) adopted a broad concept of Aleurodiscus. These two publications and the work of Boidin (1985) offer a Abstract: The limits and subdivision of possible comprehensive compilation of current and Aleurodiscus s.I. into , Acanthofun- species concepts of this group. In this paper, Aleuro- gus, Acanthophysellum, Aleurobotrys, Aleurocystidiel- discus sensu lato is essentially equivalent to Aleurod- lum, Aleurodiscus s.s., and Gloeosoma were evaluated. iscus sensu Nfuniezand Ryvarden (1997). An overview Molecular characters were obtained from an approx- of character combinations used to discriminate Aleu- imately 980 base pair fragment at the 5' end of the rodiscus s.s. and segregate genera of Aleurodiscus s.l. nuclear large subunit ribosomal DNA, in 33 strains is provided in TABLEI. representing 23 species of Aleurodiscus s.l., , Mycologists recognize Aleurodiscus using either a , and leucoxanthum. Pub- broad or a narrow generic concept (compare Boidin lished sequences of 20 additional species of the rus- et al 1985, and Nufiez and Ryvarden 1997). Several suloid clade were also included. Phylogenetic analy- narrowly defined genera have segregated from Aleu- ses suggest that Aleurodiscus s.l., Megalocystidium leu- rodiscus s.l., including Acanthobasidium Oberw., coxanthum, Stereum and Xylobolus form a monophy- Acanthofungus Sheng H. Wu et al, Acanthophysellum letic group, which may be classified as the family Parmasto, Aleurobotrys Boidin, Aleurocystidiellum P.A. . roseum, which is the type spe- Lemke, and Gloeosoma Bres. TABLE I summarizes cies of the , is not in this group, thus characters used to separate these groups. Most spe- Stereaceae is not synonymous with Corticiaceae. Aleu- cies of Aleurodiscus s.l. have acanthophyses, whereas rocystidiellumis supported as a monophyletic group. Aleurodiscus s.s. and Aleurocystidiellum lack them. Spe- Acanthobasidium, which is characterized by pleuro- cies of Aleurodiscus s.s. have hyphidia, which may be basidia, is also monophyletic. Aleurodiscus s.s. is sup- occasionally branched. Dendrohyphidia, present in a ported as monophyletic, but Gloeosoma is not, and few species, could be considered as an intermediate the two are not congeneric. The importance of am- form between acanthophyses and occasionally yloid acanthophyses for recognizing Aleurobotrysis branched hyphidia. Most species of Aleurodiscus s.l. suspect, and its generic status should be further stud- are associated with a uniform white rot in , ied. Most of the smooth-spored species form a mono- whereas Acanthofungus and Xylobolus are associated phyletic group. Phylogenetic analyses suggest that with a white-pocket rot in wood. In Aleurodiscus s.l., there has been homoplasy in most of the characters the mycelia of uniform white rot-causing species usu- that have been used to subdivide Aleurodiscus s.l., in- ally show a positive phenoloxidase reaction, while this cluding ornamentation, hymenial color, hyphal reaction is usually negative for the white pocket rot- (S.-H. Wu, septation, clamp connections, acanthophyses, and causing species unpubl). were phenoloxidase reactions. Macroscopically, cupulate gen- as the but this char- Key Words: , , mo- erally recognized typical form, lecular systematics, russuloid clade acter varies among Aleurodiscus s.l., and effuse, ef- fused-reflexed, or pulvinate forms are present. A pinkish- or orange-tinted hymenial surfaces was re- Accepted for publication February 12 2001. garded as typical for Aleurodiscus, but white, gray, or 1 Corresponding author, E-mail: [email protected] cream-colored hymenial surfaces occur in many spe-

720 WU ET AL: PHYLOGENY OF ALEURODISCUSS.L. 721

TABLEI. Main charactersused for separatingsegregate genera in Aleurodiscuss.l., as Stereumand Xylobolusa Clamp Ornamented connections Phenoloxidase spores Acanthophyses in basidiocarps reaction Acanthobasidium + + + + Acanthofungus -+ + Acanthophysellum - + + + Aleurobotrys + + - + Aleurodiscus s.s. + - + + Aleurocystidiellum + -+ + Gloeosoma + + + + Stereum +- b + xylobolus - + - - a Data from Boidin et al 1985, Nfifunezand Ryvarden1997, and Wu et al 2000. b Some species of Stereumlack acanthophysesbut have acutophyses,which might be a reduced form of acanthophyses. cies. Boidin et al (1985) suggested that the pink or smooth spores, acanthophyses, and simple-septate hy- orange spore print is an important feature of Aleu- phae; A. moniliferMalencon has smooth spores, lacks rodiscus s.s. (including Gloeosoma),which differs from acanthophyses, and has nodose-septate hyphae; and the white spore print of other genera in Aleurodiscus A. limonisporus D.A. Reid has smooth spores, lacks s.l. This character may be important, but is not acanthophyses, and has simple-septate hyphae. These known for many species. three species cannot be placed in any of the segre- Microscopically, gloeocystidia and amyloid basid- gated genera of Aleurodiscus s.l. as currently circum- iospores are uniformly present in all species. Basidia scribed In fact, the known species in Aleurodiscus s.l. and basidiospores of many species are large, relative have satisfied all possible combinations for the three to other species of corticioid fungi. Acanthophyses important characters of spore surface (ornamented characterize the majority of the species in Aleurodis- or smooth), acanthophyses (present or not), and hy- cus s.l. Lemke (1964) regarded Aleurodiscusas having phal septation (nodose or simple-septate). Thus, a catahymenium, but Eriksson and Ryvarden (1973) some mycologists (Hjortstam 1997, Nunfiezand Ryvar- considered this character to be questionable, espe- den 1997) consider the subdivision of this group im- cially for the members in Acanthophysellum.The ca- possible. tahymenium is more typically present in Aleurodiscus The purpose of this study is to assess the limits of s.s. The distinction between a euhymenium and a ca- Aleurodiscus s.l. and the monophyly of its generic seg- tahymenium is hard to define, however. For instance, regates. The taxa chosen represent various segregate Lemke (1964) described all species in his concept of genera of Aleurodiscus s.l., plus the allied genera Ster- Aleurodiscus s.s. as having a catahymenium, but this eum and Xylobolus. Mycologists have traditionally re- is not correct. As a result, this character is not con- garded Aleurodiscus s.l. as a member of the Cortici- sidered in this study. Some other important charac- aceae Heter in the broad sense (Donk 1964, Parmas- ters vary among species of Aleurodiscus s.l. For in- to 1986). Parmasto's (1995) analysis based on mor- stance, basidiospores can be ornamented or smooth phological characters suggested that this group is in and the hyphae can be nodose or simple-septate. In the Corticiaceae s.s. Stereum and Xylobolus are gen- addition, nuclear behavior and mating systems vary erally placed in the Stereaceae Pilat (e.g., Ginns and among species of Aleurodiscus s.l. (Boidin and Lan- Lefebvre 1993). Stereaceae has been customarily quetin 1984b). used to accommodate genera with stereoid basidi- Aleurodiscus s.l. includes species with highly varied ocarps and dimitic hyphal systems (Donk 1964, Par- characters, which is why many mycologists are not masto 1986). Wu (1996) stressed the importance of willing to accept Aleurodiscus as a single . More- amyloid basidiospores and gloeoplerous hyphae and over, the characters used for separating different limited the Stereceae (in his concept of the subfamily groups in Aleurodiscus s.l. are not congruent. For ex- Stereoideae Ulbr.) to Stereumand Xylobolus, exclud- ample, some groups with ornamented spores have ing all other genera that lack these two characteris- acanthophyses whereas other do not, and some have tics. Stereumand Xylobolus share an important char- nodose hyphae whereas other have simple-septate hy- acter, the acanthophyses, with Aleurodiscus s.l., which phae. Further, some species still do not fit any genus suggests that they are closely related (Lemke 1964, as listed in TABLEI. For example, A. farlowii has Boidin et al 1979). This view has been upheld by 722 MYCOLOGIA molecular phylogenies (Hibbett et al 1997, Hibbett fungi/mycolab/primers.htm). Sequencing reactions were and Donoghue in press), which suggest that Aleuro- purified using Pellet Paint (Calbiochem, San Diego, Cali- discus botryosus, A. cerrusatus, , S. fornia), and run on an Applied Biosystems 377XL auto- mated DNA with a 5% rugosum, , and Megalocystidium sequencer Long Ranger acrylamide BioProducts). were edited and assem- leucoxanthumform a monophyletic group that is nest- gel (FMC Sequences bled using (GeneCodes Corp., Ann Arbor, ed in the russuloid clade of the homobasidiomycetes Sequencher Michigan), and have been deposited in GenBank (accession and Thorn The rDNA internal tran- (Hibbett 2000). numbers AY039305-AY039336). scribed spacer (ITS) analysis of Boidin et al (1998) Sequences were manually aligned in the PAUP*4.0b4a also suggested that species of Aleurodicus s.l. are (Swofford 1999) data editor. The dataset has been depos- closely related to Gloeocystidiellum s.l., Stereum, Xylo- ited in TreeBASE (accession number S626). Three sets of bolus, and other members of the russuloid clade. In- analyses were performed. Analysis 1 included 42 complete terpretation of the phylogenetic tree of Boidin et al LROR-LR5sequences (31 new sequences, plus 11 published (1998, FIG. 6) is problematical, however, because sequences). Analysis 2 included the same sequences as anal- there are no bootstrap values or other measures of ysis 1, except the sequence from A. farlowii, which was to be robustness. Therefore, it is not possible to know what found highly divergent (see Results). Analysis 3 in- cluded all 42 complete LROR-LR5sequences, plus the 28 aspects of their tree are strongly supported by the of and Parmasto data. partial sequences Hallenberg (1998). Phylogenetic analyses were performed in PAUP* using equally weighted parsimony. In analyses 1 and 2, 1000 rep- MATERIALSAND METHODS licate heuristic searches were performed, each with a ran- dom taxon addition sequence, MAXTREES set to autoin- Molecular characters were obtained from an approximately crease, and TBR branch swapping. Bootstrapping in analy- 980 base pair (bp) fragment of the nuclear large subunit ses 1 and 2 used 1000 replicates, each with 100 heuristic ribosomal DNA (nuc-lsu rDNA), which was amplified using searches, random taxon addition sequences, MAXTREES primers LRORand LR5 (Moncalvo et al 2000). Sequences set to 100, and TBR branch swapping. The baseline parsi- were generated from 33 strains representing 19 species of mony search in analysis 3 used a two-step search protocol, Aleurodiscus s.l., plus two species of Stereumand Xylobolus with 1000 replicate searches in the first step, with random (TABLE II). Sequences of ten other species in the russuloid taxon addition sequences, TBR branch swapping, and keep- clade (Hibbett and Thorn 2000) that were published pre- ing up to ten trees per replicate. The second step used the viously, including A. cerrusatus and M. leucoxanthum (Hib- shortest trees found in the first step as starting trees for TBR bett et al 2000), were also included. A published sequence branch swapping with MAXTREES set to autoincrease. of Hyphodontia alutaria was included for rooting purposes Bootstrapping in analysis 3 used the same settings as anal- (Hibbett et al 2000). Based on previous studies, H. alutaria, yses 1 and 2, but only 100 replicates were performed. a member of the hymenochaetoid clade, is an appropriate Two constrained analyses were performed using the same outgroup for an analysis of the russuloid clade (Hibbett and taxa and settings as analysis 2. One constrained analysis Thorn 2000). Some analyses (see below) also included 28 forced the monophyly of Aleurodiscus s.l., including Acan- partial nuc-lsu rDNA sequences of wood-decaying species of thofungus (i.e., excluding Stereum, Xylobolus, M. leucoxan- the russuloid clade published by Hallenberg and Parmasto thum, and all other members of the russuloid clade). The (1998), including 7 species of Aleurodiscus s.l., 2 species of other constrained analysis forced the monophyly of Aleu- Stereum,13 species of , and others. The sequenc- rodiscus s.l., Stereum, Xylobolus, M. leucoxanthum, Peniopho- es of Hallenberg and Parmasto (1998) cover 477-606 bp ra nuda, and Amylostereumlaevigatum (FIG.1). This analysis (49-62%) of the LROR-LR5fragment. was done to evaluate the results of Hallenberg and Parmas- Cultures were grown on malt extract agar and liquid malt- to (1998), which suggested that Peniophora and Amyloster- yeast-glucose media. Isolates of A. abietis (T330), A. farlowii eum are nested in Aleurodiscus s.l. The constrained trees (HHB 14354), A. lapponicus (FP100753-R), and A. grantii were compared to unconstrained trees from analysis 2 using (T541) were tested for phenoloxidase activity, as described the Kishino-Hasegawa maximum likelihood ratio test by Wu (1996). (HKY85 model, transition/transversion bias = 2, empirical Freeze-dried or fresh liquid-cultured mycelium was base frequencies, 4 rate classes with "discrete gamma" dis- ground in a 1% SDS, 0.15 M NaCl, 50 mM EDTA extraction tribution) and the Templeton non-parametric test, both im- buffer, extracted twice with phenol-chloroform-isoamyl al- plemented in PAUP*. cohol (24:24:1), extracted once with chloroform, and pre- cipitated with ethanol and sodium acetate. DNA was diluted up to 1000-fold with deionized water for use as PCR tem- RESULTS plate. PCR products were generated using Promega (Mad- LROR-LR5 PCR were all 980 ison) reagents in an MJ Research thermal cycler, purified products approximately there no insertions or deletions. using GeneClean (BIO 101, La Jolla, California), and cycle bp long; were major sequenced using dye terminator sequencing reagents (Ap- Sequences generated for this analysis were 892-967 plied Biosystems, Foster City, California), with primers bp long. The aligned sequences included 997 posi- LROR,LR22, LR3, LR3R, and LR5 (www.botany.duke.edu/ tions, with 372 variable and 202 parsimony-informa- TABLEII. Strains used for obtaining new sequences Taxon Alternative genera Sourcea Acanthofungus rimosus Sheng H. Wu et al. Wu9601-1; Taiwan, Taichung, on Calocedrusformosana Aleurodiscus abietis H.S. Jacks. & P.A. Lemke T330; Canada, Nova Scotia; on Abies balsamea Aleurodiscus amorphous (Pers.:Fr.) J. Schrot. HHB15282; USA, Alaska; on Picea glauca Aleurodiscus aurantius (Pers.Fr.) J. Schr6t. T621 (= LY734, CBS), France, Rhone Aleurodiscus bisporus (Boidin & Lanq.) Nuniez & ?Stereum T627 (= LY7666, CBS; as bisporum); Guadeloupe, Cascade du Car- Ryvarden bet; on branch T614 (= LY7664, CBS; as A. bisporum); Guadeloupe, Cascade du Carbet; on dead twig Aleurodiscus botryosusBurt Aleurobotrys CBS195.91 (as Aleurodiscus botryosus); Canada, Ontario; on occidentalis Wu9302-61; Taiwan, Nantou; on angiosperm Aleurodiscus cerussatus (Bres.) Hohn. & Litsch. Acanthophysellum HHB11294 (as Acanthophysium cerussatum); USA, Minnesota, on Pinus banksiana FPL11572 (as Acanthophysium cerussatum) HHB11235 (as Aleurodiscus laurentianus); USA, Minnesota; on Abies balsameus Aleurodiscus disciformis (DC.:Fr.) Pat. Aleurocystidiellum T529; USA, California; on Quercus chrysolepsis It T629; USA, California; on Quercus ilex o Aleurodiscusfarlowii Burt Acanthobasidium HHB14354; USA, Wisconsin; on Tsuga Canadensis Aleurodiscus grantii Lloyd T541; Canada, British Columbia; on Abies lasiocarpa T569; USA, California; on Abies magnifica var. shastensis C-, Aleurodiscus lapponicus Litsch. Acanthophysellum FP100753; USA, Minnesota, on down branch of hardwood Aleurodiscus lividocoeruleus (P. Karst.) P.A. Lemke Acanthophysellum MB1825 (as Acanthophysium lividocaeruleum); USA, Colorado; on Abies lasiocarpa FP100292 (as Acanthophysium lividocaeruleum); USA, Colorado; on Pinus contorta Aleurodiscus mirabilis (Berk. & M.A. Curtis) H6hn. Gloeosoma Wu9304-105; Taiwan; Nantou; on angiosperm Aleurodiscus norvegicusJ. Erikss. & Ryvarden Acanthobasidium T623 (as Acanthobasidium norvegicum); France, near Calluna; on Rubus o% Aleurodiscus oakesii (Berk. & M.A. Curtis) Cooke HHB9243; USA, Michigan; on Ostrya virginiana FP101813; USA, Wisconsin, on Quercus rubra Aleurodiscus penicillatus Burt Gloeosoma 322; Canada, Nova Scotia; on Picea sp. Aleurodiscus phragmitis (Boidin et al.) Nufiez & Ryvar- Acanthobasidium CBS233.86 (as Acanthobasidium phragmitis); France, Landes; on Phragmites den australis Aleurodiscus weirii Burt Acanthobasidium FP134813 (as Acanthophysium weirii); USA, Idaho; on Thuja plicata HHB12678 (as Acanthophysium weirii); USA, Alaska; on Picea stichensis Megalocystidium leucoxanthum (Bres.) Julich CBS454.86 (as Gloeocystidiellumleucoxanthum) Stereum hirsutum (Willd.:Fr.) Gray TJV93-161; USA, Washington; on Alnus rubra Wu9711-20; Taiwan, Taichung; on angiosperm S. rugosum (Pers.:Fr.) Fr. HHB13390; USA, Alaska; on Alnus Xylobolusfrustulatus (Pers.:Fr.) Boidin FP106073-T; USA, Mississippi; on Quercus lyrata X. subpileatus (Berk. & M.A. Curtis) Boidin FP106735; USA, Mississippi; on Quercus stump a CBS = Centraalbureau voor Schimmelcutures, Baarn, Netherlands; HHB, FP, T, MB, TJV Center for Forest Research, USDA, Madison, WI, USA; W I = National Museum of Natural Science, Taichung, ROC. --I 724 MYCOLOGIA

Hyphodontia alutaria Analysis 1: all complete LROR-LR5 sequences. Bondarzewia berkeleyi Tree 1/45 Russula compacta Hyphodontia alutaria Heterobasidion annosum Bondarzewia berkeleyi '- Heterobasidion annosum Auriscalpium vulgare - Megalocystidium leucoxanthum ramosum Al. cerussatus HHB11294 FP100753 bicolor Al. lapponicus Al. cerussatus HHB11235 Megalocystidium leucoxanthum - Al. cerrusatus FPL11572 Al. cerussatus HHB112 Al. botryosus Wu9302-61 CBS195.91 FP100753 Al. botryosus Al. lapponicus r Xylobolus frustulatus FP106073-T Al. cerrusatus FPL1157 - FP106735 Al. botryosus Wu9302 61 Al. lividocoeruleus MB1825 IAl. lividocoeruleus FP100292 AI. botryosus CBS195 91 -Stereum rugosum HHB13390 Xylobolus frustulatus FP106073 -i- Stereum hirsutum TJV93-161 FP106735 Stereum hirsutum Wu9711-20 Xylobolus subpileatus I Al. bisporus T627 Al. lividocoeruleus MB1 - Al. bisporus T614 Al. lividocoeruleus FP100 Acanthofungus rimosus Wu9601-1 - Al. abietis T330 Stereum rugosum HHB13390 - Al. mirabilis Wu9304-105 Stereum hirsutum Wu9711 20 Al. phragmitis CBS233.86 Al. T623 hirsutum TJV93 161 norvegicus Stereum Al. weirii FP134813 Al. bisporus T627 Al. weirii HHB12678 Al. bisporus T614 Al. farlowii HHB14354 - L Al. penicillatus T322 Wu9601 1 Acanthofungus rimosus - Al. amorphus HHB15282 -Al. abietis T330 _ Al. grantii T541 Al. mirabilis Wu9304 10 Al. grantii T569 -Al. aurantius T621 Al. grantii T569 Al. oakesii FP101813 - -Al. aurantius T621 IAl. oakesii HHB9243 r Al. disciformis T529 Al. oakesi FP101813 Al. disciformis T629 'Al. oakesii HHB9243 - Russula compacta nuda ,Al. phragmitis CBS233 Peniophora laevigatumCBS623.84 ,Al. norvegicus T623 - Auriscalpium vulgare 'Al. weirii FP134813 Hericium ramosum - bicolor "Al.weirii HHB12678 Laxitextum ~Al.penicillatus T322 - = 20 steps ~Al.amorphus HHB15282 FIG.2. Analysis 1: phylogenetic relationships of Aleurod- Al. T541 grantii iscus s.l. inferred from of all LROR-LR5 nuda analysis complete \Peniophora one of 45 laevigatum sequences. Phylogram showing equally parsimo- \Amylostereum = = ?AI.disciformis T529 nious trees (841 steps, CI 0.577, RI 0.670). Note long \Al. disciformis T629 terminal branch leading to A. farlowii. FIG. 1. Constraint tree used to evaluate results of Hal- lenberg and Parmasto (1998). supported at 100%), but no nodes that received tive positions (calculated with all sequences includ- stronger bootstrap support in analysis 1 than analysis ed). 2 (FIG. 3). Analysis 1 (with all complete LROR-LR5 sequences) Strict consensus trees from both analyses 1 and 2 recovered 45 trees of 841 steps (CI = 0.577, RI = show a basal polytomy in the russuloid clade, with 0.670) in two islands (Maddison 1991; FIG. 2). Anal- eight unresolved lineages leading to Amylostereum, ysis 2 (with all complete LROR-LR5 sequences, except Auriscalpium, Bondarzewia/Heterobasidion, Hericium, A. farlowii) recovered 42 trees of 675 steps (CI = Laxitextum, Peniophora, Russula, and a large clade 0.538, RI = 0.697) in two islands (FIG. 3). In both consisting of Aleurodiscus s.l., Stereum, Xylobolus, and analyses 1 and 2, every replicate in the heuristic M. leucoxanthum, which we hereafter refer to as the searches found one of the two islands. There is no Stereaceae (FIG. 3). positive conflict among the strict consensus trees of The Stereaceae is supported by 87% of the boot- analyses 1 and 2; the only difference is that one strap replicates in analysis 1 and 91% of the bootstrap branch in the strict consensus tree of analysis 2 col- replicates in analysis 2. The first group branching off lapses in the strict consensus of analysis 1. Overall, in the Stereaceae is a strongly supported lineage levels of bootstrap support in analysis 1 are lower composed of two isolates of A. disciformis (bootstrap than those in analysis 2. Five nodes received equal = 100% in both analyses 1 and 2). The remaining support in analyses 1 and 2 (including four nodes taxa in the Stereaceae form a strongly supported WU ET AL: PHYLOGENY OF ALEURODISCUSS.L. 725

Hyphodontia alutaria Analysis 2: complete LROR-LR5 minus Al. farlowii. Bondarzewia berkeleyi sequences, Strict consensus/42 trees Heterobasidion annosum XX = bootstrap in analysis 2 Hericium ramosum (XX) = bootstrap in analysis 1 * = in 1 Auriscalpium vulgare collapses analysis Russula compacta alternative genera for Peniophora nuda Aleurodiscus s.l. spp. Megalocystidium leucoxanthui Al. cerussatus HHB11294 . Al. lapponicus FP100753 Acanthophysellum Al. cerussatus HHB11235 Al. cerrusatus FPL11572 ...... Al. botryosus Wu9302-61 Aleurobotrys Al. botryosus CBS1 95.91 Xylobolus frustulatus FP10607 Xylobolus subpileatus FP1067, Al. lividocoeruleus MB1825. C) Acanthophysellum Al. lividocoeruleus FP100292 .... -I Stereum rugosum HHB13390 Stereum hirsutum TJV93-161 m

Stereum hirsutum Wu9711-20 :: Al. bisporus T627 .- --."".. ?Stereum m Al. bisporus T614 ...... Acanthofungus rimosus Wu96 Al. abietis T330 0 Al. mirabilis Wu9304-105 . Gloeosoma m Al. phragmitis CBS233.86 ' Al. norvegicus T623 Acanthobasidium Al. weirii FP134813 m Al. weirii HHB12678 ...... : Al. penicillatus T322 ..... Gloeosoma Al. amorphus HHB15282 Al. grantii T541 Aleurodiscus s.s. Al. grantii T569 ....;...... Al. aurantius T621 Al. oakesii FP101813 Al. oakesii HHB9243 Al. disciformis T529 IAleurocystidiellum Al. disciformis T629 ...... FIG.3. Analysis 2: phylogenetic relationships of Aleurodiscus s.l. inferred from analysis of all complete LROR-LR5sequenc- es, except that of A. farlowii. Strict consensus of 42 trees (675 steps, CI = 0.538, RI = 0.697). Segregate genera of Aleurodiscus s.l. are indicated with brackets. Numbers by nodes indicate bootstrap support in a nalysis 1 (in parentheses). The placement of A. farlowii in analysis 1 is indicated with an arrow. The one branch that collapses in the strict consensus tree of analysis 1 is indicated with an asterisk. 726 MYCOLOGIA monophyletic group (bootstrap = 96% in analysis 1, ceae recovered nine trees of 684 steps (nine steps 98% in analysis 2; FIG. 3). longer than the unconstrained trees). The Kishino- Most pairs of putatively conspecific isolates were Hasegawa test rejected all of the constrained trees (P grouped together, including A. disciformis, A. botry- = 0.0073-0.0126), and the Templeton test rejected osus, A. oakesii, A. weirii, and A. bisporus (FIGS.2, 3). three of the trees (P = 0.0495-0.1282). However, the two isolates of A. lividocoeruleusform a Aleurodiscus abietis (T330), A. farlowii (HHB paraphyletic group, in which Xylobolusis nested, the 14354), A. lapponicus (FP100753-R), and A. grantii three isolates of A. cerrusatus form a paraphyletic (T541) gave positive phenoloxidase reactions. group in which A. lapponicus is nested, and the two isolates of S. hirsutum cannot be resolved from an DISCUSSION isolate of S. rugosum. Analysis 3 (with all sequences, including 28 partial The results of this study suggest that Aleurodiscuss.l., sequences of Hallenberg and Parmasto [1998]) re- Stereum, Xylobolus,and M. leucoxanthum are in a sin- covered 511 trees of 1034 steps (CI - 0.526, RI = gle clade (FIGS. 2-4), which we suggest should be 0.741), which were found in 54 replicate heuristic recognized as the Stereaceae. Bootstrap support for searches in the first step of the analysis. TBR branch the Stereaceae is strong in the analyses that include swapping on these trees in the second step of the only the full-length LROR-LR5sequences (87-91%) analysis recovered an additional 312 trees of the same but it is weak (40%) in the analysis that includes the length (FIG. 4). The Stereaceae is still supported as partial sequences of Hallenberg and Parmasto monophyletic in analysis 3, but the bootstrap support (1998). Thus, future analyses aimed at understanding is only 40%, vs 87-91% in analyses 1 and 2 (FIGS.3, relationships of Stereaceae with nuc-lsu rDNA should 4). As in analyses 1 and 2, a lineage including A. use full-length LROR-LR5sequences. Results of con- disciformis is the sister group of the rest of the Ster- strained analyses reject the view that Peniophora and eaceae. Two sequences of A. subcruentatum and A. Amylostereumare nested in the Stereaceae (Hallen- disciformisfrom Hallenberg and Parmasto (1998) are berg and Parmasto 1998). However, additional stud- also in this group in analysis 3. The bootstrap support ies are needed to estimate what other taxa are in the for the remaining taxa of the Stereaceae is only 68%, Stereaceae. In particular, more species of Gloeocysti- vs 96-98% in analyses 1 and 2 (FIGS.3, 4). diellum s.l. should be sampled. At present, Gloeocys- Several isolates from Hallenberg and Parmasto's tidiellum s.l. is represented in our dataset only by M. (1998) dataset are placed close to putatively conspe- leucoxanthum. As a result, we can not say whether all cific sequences generated in the present study, in- of Gloeocystidiellums.l. belongs to the Stereaceae. The cluding A. cerrusatus, S. hirsutum, and A. lividocoeru- analysis of Boidin et al (1998) suggests that species leus (FIG. 4). However, in each case, the species in of Gloeocystidiellums.l. are found in several lineages question is not supported as monophyletic (FIG. 4). in the russuloid clade. There are also two anomalous results. The sequences Gloeocystidiellums.l. appears to be allied to Aleuro- of A. aurantius and A. weirii published by Hallenberg discus s.l. (Ginns and Lefebvre 1993, Hibbett et al and Parmasto (1998) form a monophyletic group 1997, Boidin et al 1998). However, the subdivision of that is outside of the Stereaceae and far removed Gloeocystidiellums.l. has challenged mycologists for from the sequences generated for the present study. many years. Analysis of several characters for Gloeo- The sequence of A. aurantius and A. weirii published cystidiellums.l. allows separation of various genera in by Hallenberg and Parmasto (1998) differ at 56 and this group (Ginns and Freeman 1994, Wu 1996, Boi- 40 positions, respectively, from the sequences of din et al 1997). In the future, it will be necessary to these species generated in the present study. There- perform analyses including representatives of all the fore, we suspect that the sequences published for A. segregates of Gloeocystidiellums.l. and Aleurodiscus aurantius and A. weirii by Hallenberg and Parmasto s.l., as well as Stereumand Xylobolus. (1998) actually represent taxa that are outside of The type species of Corticium, C. roseum, is in a Aleurodiscus s.l. separate clade from the Stereaceae (FIG. 4). Thus, The constrained analysis that forced the monophy- the Stereacae is not a synonym of Corticiaceae. These ly of Aleurodiscus s.l. recovered 125 trees of 702 steps findings conflict with those of Parmasto (1995), who (27 steps longer than the unconstrained trees ob- suggested that Aleurodiscus is in the Corticiaceae s.s., tained in analysis 2), all of which were rejected by the based on an analysis of morphological characters. Kishino-Hasegawa test (P = 0.0015-0.0066) and the Aleurodiscus s.l. is paraphyletic (FIGS. 2-4), and Templeton test (P = 0.0056-0.0191). The con- therefore should not be recognized as a formal tax- strained analysis designed to test support for inclu- on. Two of the segregate genera, Aleurocystidiellum sion of Peniophora and Amylostereumin the Sterea- and Acanthobasidium, are supported as monophylet- .....

WU ET AL: PHYLOGENY OF ALEURODISCUSS.L. 727

Analysis 3: all complete LROR-LR5sequences (bold font), plus partial sequences (plain font). Majority-rule consensus/511 trees XX = bootstrap; *XX = branch collapses in strict consensus/frequency in MP trees

Hyphodontia alutaria alternative genera for Bondarzewia berkeleyi Aleurodiscus s.l. spp. Heterobasidion annosum Megalocystidium leucoxanthum Al. cerrusatus U80638 -''''-'"''^'"""" ''' Al. cerussatus HHB11294 Al. FP100753 2 lapponicus Acanthophysellum Al. cerussatus HHB11235 Al. cerrusatus FPL11572 ...... ;-:: Al. botryosus Wu9302-61 Aleurobotrys E Al. botryosus CBS195.91 ...... Stereum rugosum U80664 Stereum rugosum HHB13390 () Stereum hirsutumU80663 Stereum hirsutum TJV93-161 -I Al. wakefieldiae U80644 -:::-::;-: ::m ..... Gloeosoma Stereum hirsutum Wu9711-20 m A I. T627 ":':' "-' "''" ""'"'""''""""'""...."''""'..'"' bisporus ?Stereum Al. bisporus T614 .:.:.:^ss:.:...... Acanthofungus rimosus Wu9601-1 Xylobolus frustulatus FP106073-T Xylobolus subpileatus FP106735 m Al. lividocoeruleus MB1825 . Al. lividocoeruleus FP100292 . Acanthophysellum Al. lividocoeruleus U80639...... Al. abietis T330 0 Al. mirabilis Wu9304-10 Gloeosoma Al. phragmitis CBS233.86 m Al. norvegicus T623 Al. weirii FP134813 Acanthobasidium Al. weirii HHB12678 Al. farlowii HHB14354 ...... :... Al. penicillatus T322 ::i...... =Gloeosoma m Al. amorphus HHB15282 '.-' ' Al. grantii T541 ',.Aleurodiscus s.s. I A l. -:^::.::.;:..:...... grantii. T569 : Al. aurantius T621 Al. oakesii FP101 813 I Al. oakesii HHB9243 Al. subcruentatum U80642 ::::::::::::::.;:::::::::::::.:.. Al. disciformis U80641 Al. disciformis T629 Aleurocystidiellum Al. disciform is T529 ...... Russula compacta Amylostereum laevigatum i U80645 Hericium ramosum Laxitextum bicolor Auriscalpium vulgare Peniophora nuda Peniophora nuda U80656 U80652 Peniophora cinerea U80651 Peniophora versicolor U80662 Peniophora meridionalis U80655 Peniophora aurantiaca U80650 Peniophora rufa U80661 Peniophora polygonia U80659 i Peniophora decorticans U80653 Peniophora pini U80658 I Peniophora piceae U80657 Peniophora proxima U80660 Peniophora incarnata U80654 Vuilleminiacystidiata U80666 E Corticiumpolygonioides U80646 Vuilleminiacomedens U80665 Cytidiasalicina U80648 Duportellatristicula U80649 " Corticiumroseum U80647 Al. aurantius U80643--- 56 I Al. weirii U80640 --

FIG. 4. Analysis 3: phylogenetic relationships of Aleurodiscus s.l. inferred from analysis of all complete LROR-LR5 sequences (written in bold font) and partial sequences of Hallenberg and Parmasto (1998, written in plain font). Problematical se- quences of A. aurantius and A. weirii from Hallenberg and Parmasto (1998) are indicated with arrows. Other symbols as in FIG. 3. 728 MYCOLOGIA ic, but Acanthophysellumand Gloeosomaare polyphy- monophyletic (FIGS.3, 4). Pleurobasidia are clearly letic (FIGS.2-4). Aleurobotrysand Acanthofungus were present in A. phragmitis and A. norvegicus. Lemke represented in our analyses by only a single species (1964) suggested that the basidioles of A. weirii re- each. The taxonomic implications of our results, em- semble pleural basidia. Thus, molecular and anatom- phasizing the segregate genera, are discussed below. ical features suggest that A. weirii may be properly Aleurodiscus amorphus, which is the type species of classified as a member of Acanthobasidium. Aleurodiscus, and A. grantii are supported as a mono- Aleurodiscus farlowii has a close relationship with phyletic group in this study (FIGS.2-4). These two Acanthobasidium, according to analyses 2 and 3 (FIGS. species represent Aleurodiscus s.s., with occasionally 2-4). Aleurodiscusfarlowii differs from the three oth- branched hyphidia, but lacking acanthophyses and er species of Acanthobasidium in having smooth dendrohyphidia. Aleurodiscus aurantius resembles spores and simple-septate hyphae (FIG. 5). The po- Aleurodiscus s.s. morphologically, but it has dendro- sition of A. farlowii based on molecular characters is hyphidia and lacks the sparsely branched hyphidia. problematical because its rDNA sequence is highly The molecular results suggest that this species is basal divergent from other sequences of Aleurodiscus s.l. to the clade that includes Aleurodiscus s.s., A. penicil- (FIG. 2), which raises the possibility that its placement latus, and Acanthobasidium (FIGS.2-4). Further stud- is an artifact due to long branch attraction, and the ies are needed to verify whether Aleurodiscus s.s. only monophyly of A. farlowii, A. phragmitis, A. norvegi- includes species with occasionally branched hyphidia, cus, and A. weirii was supported by only 45% of the not dendrohyphidia. bootstrap replicates in analysis 1 (FIG. 3). Neverthe- Aleurocystidiellum,proposed by Lemke (1964) for less, the present molecular phylogeny suggests that a single species, Stereumsubcruentatum Berk. & M.A. this species is probably an Acanthobasidium. Curtis, was originally characterized by a dimitic hy- Species representing the genera Acanthophysellum, phal system and encrusted skeletal cystidia (pseudo- Aleurobotrys, Acanthofungus, Stereum, and Xylobolus, cystidia). Later, A. disciformis (DC.: Fr.) Boidin et al and the species A. bisporus, A. abietis, and Megalocys- (1968) was transferred to this genus. Unlike the type tidium leucoxanthum form a moderately supported species, A. disciformis is monomitic with gloeocysti- monophyletic group (bootstrap = 77%; FIG. 3). This dia. Nevertheless, both species occur on bark of living group is characterized by having smooth basidio- trees (Boidin et al 1985). In addition, Hallenberg spores (except A. botryosus; FIG. 5). The segregate and Parmasto (1998) observed similar wart-like or- genera of Aleurodiscus s.l. represented in this group namentations on the spore surfaces of both species, are discussed below. suggesting that they are closely related. The mono- Acanthophysellum is polyphyletic (FIGS. 2-4). The phyly of Aleurocystidiellum is strongly supported in type species, A. lividocoeruleum,appears to be closely this study (FIG. 4), as well as the analysis of Hallen- related to Xylobolus, but the remaining species, A. berg and Parmasto (1998). Thus, the skeletal cystidia cerussatus and A. lapponicus, appear to be the sister in A. subcruentatum and the gloeocystidia in A. dis- group of Aleurobotrys (A. botryosus; FIGS. 2-4). Aleu- ciformismay be homologous, both representing mod- rodiscus lapponicus appears to be nested in A. cerus- ifications of the gloeoplerous hyphae that character- satus, and it is possible that the two are conspecific ize other taxa in the russuloid clade (Donk 1964, (FIGS. 2-5). The close relationship of A. lividocoeru- Hibbett and Thorn 2000). A similar case is present leus and Xylobolus is surprising because A. lividocoeru- in Stereumwakullum (Burds et al) Sheng H. Wu. Most leus produces a white rot (positive phenoloxidase re- species of Stereum have distinct skeletal-like cystidia action) and has clamped hyphae in the basidiocarps, (pseudocystidia), but they are lacking in S. wakullurn, whereas Xylobolusproduces a white pocket rot (neg- which has gloeocystidia with basally thickened walls. ative phenoloxidase reaction) and has clampless hy- The skeletal-like cystidia of Stereum probably repre- phae in the basidiocarps (FIG.5). sent a modification of the gloeoplerous hyphae. Acanthofungus rimosus is closely related to A. bis- Acanthobasidium is also strongly supported as porus and Stereum s.s. (FIGS. 2-4). Acanthofungus dif- monophyletic in this study (FIGS.2-4). This genus is fers from Stereum in that it produces a white pocket characterized chiefly by the pleurobasidia (and or- rot and has clamped septa, whereas Stereumproduces namented spores and clamp connections). A feature a white rot and has unclamped septa in the basidi- of secondary importance is the lateral protuberances ocarp (FIG. 5). Taken together, the results for Acan- produced on the basidia (acanthobasidia). Acantho- thophysellum, Acanthofungus, Stereum, and Xylobolus basidia are not unique to Acanthobasidium, but are suggest that both decay type (uniform white rot vs also found in several other groups of Aleurodiscuss.l. white pocket rot) and hyphal septation (clamped vs and some species of Stereum.Aleurodiscus phragmitis, clampless) are evolutionarily labile (FIG.5). A. norvegicus and A. weirii are strongly supported as Aleurodiscus bisporus is closely related to Stereum WU ET AL: PHYLOGENY OF ALEURODISCUSS.L. 729

0 / leucoxanthumwhite/gray/cream so d leucoxanthum white/gray/cream smooth + + lapponicus gray/buff smooth + 4. cerrusatus white/gray/cream smooth + + botryosus white/buff ornamented + 4- rlobolusfrustulatus pale ochraceous/brownsmooth + . lividocoeruleus grayishblue smooth + + ereum rugosum ochraceous/buff smooth + + ereum hirsutum gray/orange smooth + . bisporus gray/buff smooth + - + white/cream smooth ++ . abietis cream/orange smooth + - + . mirabilis pink/orange ornamernted +S + + . phragmitis white/buff ornamernted + + + norvegicus white/cream ornamernted + + + white/cream ornamernted + + + .farlowii white/cream/buff smooth + - + . penicillatus white/cream ornamernted + + + pink/orange ornamernted - + pink/orange ornamerited - + + pink/orange smooth 4. pale cream ornamernted + +/- + white/gray ornamernted - + + FIG.5. Simplifiedtree showingtaxa sampledin this study,with characterstates for hymeniumcolor, spore ornamentation, acanthophyses,clamp connectionsin the ,and phenoloxidasereactions, from personalobservations and literature sources (Boidin 1950, 1958, Boidin et al 1968, Coates et al 1981, Raynerand Turton 1982, Boidin and Lanquetin 1984, Nakasone 1990, Wu 1996, Wu et al 2000).

and Acanthofungus (FIGS.2-4), but this clade is not A. parmuliformis G. Cunn., as suggested by Nunfiez strongly supported (bootstrap = 54-64%; FIGS.3, 4). and Ryvarden (1997). Nevertheless, this result is not so surprising because Acanthophysellum appears to be polyphyletic, and A. bisporus has morphological characters that resem- Stereum is paraphyletic or polyphyletic (FIGS.2-4), ble those of S. wakullum. Basidiocarps of S. wakullum suggesting that considerable taxonomic changes are and A. bisporus are effuse, not stereoid, as is typical necessary. However, insufficient sampling of Stereum, in Stereum.These two species also have gloeocystidia Acanthofungus, and Aleurodiscus s.l., and a lack of to- that are thick-walled except at the apex, which may pological robustness preclude making taxonomic be a modification of the skeletal-like cystidia that are changes. Therefore, for practical purposes, we will common in Stereum. Acanthofungus and A. bisporus continue to recognize Acanthophysellumand Acantho- are weakly supported as the sister group of Stereum . (FIGS.3, 4). If S. wakullum is in this clade, then Ster- Aleurobotrys is characterized by having acantho- eum, as presently circumscribed, is polyphyletic (cf. physes with coralloid and amyloid apical branches. So Boidin et al 1998). far, this genus includes only the type species A. botry- Analyses including sequences of Hallenberg and osus. Nunfiez and Ryvarden (1997) mentioned that Parmasto (1998) suggest that A. wakefieldaeis nested some other species of Aleurodiscus s.l. have acantho- in Stereum (FIG. 4). A few other species in Aleurodis- physes with amyloid reactions to varying extents. cus s.l. probably have a close relationship with Ster- Three species with amyloid acanthophyses, A. botry- eum, including A. antarcticus (Speg.) Ryvarden and osus, A. abietis, and A. farlowii, included in this study 730 MYCOLOGIA did not form a monophyletic group (FIGS. 2-4), LITERATURE CITED which suggests that amyloid acanthophyses have Boidin J. 1950. Sur la cytologie des StereumFr. en culture evolved more than once. Aleurodiscus botryosus is the pure. C R Acad S. Paris 230:1096-1098. with ornamented the only species spores among . 1958. Essai biotaxonomique sur les Hydnes resupi- monophyletic smooth-spored group. The distribu- nes et les Cortici6s. Rev Mycol Mem Hors-Ser 6:1-388. tion of character states on the tree (FIG. 5) suggests . 1985. Contribution a la connaissance des Aleurod- that the presence of ornamented spores in A. botry- iscoideae a spores amyloides (Basidiomycotina, Corti- osus is due to a reversal. ciaceae) I. Introduction. Bull Soc Mycol France 101: Aleurodiscus mirabilis, A. penicillatus, and A. wake- 334-340. , Lanquetin P. 1984a. 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Aleurodiscus oakesii resembles Gloeosoma but has both Contribution a la connaissance des Aleurodiscoideae a clamped and clampless septa. This species showed no spores amyloides (Basidiomycotina, Corticiaceae). Bull distinct close relationship with any other studied spe- Soc Mycol France 101:333-367. cies. Aleurodiscus s.s. probably represents a monophy- , MugnierJ, Canales R. 1998. Taxonomie moleculai- letic group, but Gloeosoma does not. re des Aphyllophorales. Mycotaxon 66:445-491. Parmasto P. 1979. Ster- Species with pinkish or orange-tinted hymenial sur- , E, Dhingra GS, Languetin eums with acanthophyses, their positions and affinities. faces occur in several different clades (FIG. 5). With Persoonia 10:311-324. our of taxa, it that the present sample appears ple- , Terra JP, Lanquetin P. 1968. Contribution a la con- siomorphic condition of the Stereaceae is to have naissance des caracteres myc6liens et sexuels des gray to white hymenial surfaces, but that there have genres Aleurodiscus, Dendrothele,Laeticorticium et Vuil- been multiple gains and (or) losses of pink to orange leminia (Basidiomycetes, Corticiaceae). Bull Soc Mycol hymenial surfaces (FIG. 5). Other characters that France 84:53-84. Coates NK. 1981. have undergone multiple transformations include D, Rayner ADM, Todd Mating behaviour, mycelial antagonism and the establishment of individ- spore ornamentation, presence/absence of clamp uals in Stereumhirsutum. Trans Br Mycol Soc 76:41-51. connections, decay type (phenoloxidase reactions), Donk MA. 1964. A conspectus of the families of Aphyllo- and of presence/absence acanthophyses (FIG. 5). phorales. Persoonia 3:199-324. Data regarding nuclear behavior and sexuality in Eriksson J, Ryvarden L. 1973. 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