Phylogenetic relationships of russuloid basidiomycetes with emphasis on aphyllophoralean taxa

1037

Mycologia, 95(6), 2003, pp. 1037–1065.q 2003 by The Mycological Society of America, Lawrence, KS 66044-8897

Phylogenetic relationships of russuloid basidiomycetes with emphasis onaphyllophoralean taxa

Ellen Larsson1

Karl-Henrik LarssonBotanical Institute, Goteborg University, P.O. Box 461,SE 405 30 Goteborg, Sweden

Abstract: Many homobasidiomycetes are character-ized by a combination of gloeocystidia and amyloidbasidiospores. They display a great variation in basi-dioma morphology, including erect and effusedforms and gilled and nongilled forms. Earlier studieshave shown these taxa to be related, and the grouphas been named the russuloid clade. Phylogenetic re-lationships among russuloid basidiomycetes were in-vestigated using sequence data from the nuclear 5.8S,ITS2 and large-subunit rDNA genes. A dataset in-cluding 127 ingroup sequences representing 43 gen-era and ca 120 species were analyzed by maximum-parsimony and neighbor-joining methods. The sam-pling of taxa had an emphasis on nongilled taxa andtwo-thirds of the species possessed corticioid basi-diomata. Thirteen major well-supported clades wereidentified within the russuloid clade. All clades ex-cept one include corticioid species. Ten charactersfrom basidioma morphology and cultured myceliumwere observed and evaluated. Results suggest thatgloeocystidia are a synapomorphy for taxa within therussuloid clade while the amyloidity of spores is in-consistent. The ornamentation of spores and type ofnuclear behavior seems to be informative charactersat genus level. The agaricoid genera Lactarius andRussula are nested in a clade with corticioid speciesat the basal position. The new combinations Boidiniaaculeata, Gloeodontia subasperispora, Gloeocystidiopsiscryptacantha and Megalocystidium wakullum are pro-posed.

Key words: amyloid spores, corticioid basidiom-ata, gloeocystidia, Homobasidiomycetes, nuclearrDNA, phylogeny, russuloid clade, sulfobenzaldehydereaction

INTRODUCTION

The classification of macrofungi traditionally has re-lied almost entirely on macro- and microanatomical

Accepted for publication April 2, 2003.1 Corresponding author. E-mail: [email protected]

features of the basidiome (e.g., Fries 1874, Patouil-lard 1900, Julich 1981). However, anatomical simplic-ity, a scanty fossil record and high phenotypic plastic-ity make it difficult to separate the traces of ancestryfrom instances of parallel evolution. As a result, manyfungal genera and families that we are familiar withnow are shown to be highly artificial. A few examplesare Coprinus, the ink-cap genus, (Redhead et al2001), the coral fungi in Clavariaceae (Pine et al1999) and Corticiaceae, the family partly at focus inthis study (Hibbett and Thorn 2001).

Along with morphological traits, staining reactionsalso have been widely applied in fungal systematics.Perhaps the best-known example is Melzer’s solution,which is used to detect some of the variable polysac-charide components of fungal cell walls. The activesubstance in Melzer’s is iodine. Some polysaccharidesreact with iodine to produce a bluish-violet (amyloid)coloration, while others turn reddish-brown (dextri-noid). Another chemical test involves sulfuric benz-aldehyde, usually in the form of sulfovanilline. Whenapplied to fungal tissue, a dark violet coloration oc-curs in cells containing certain sesquiterpenes (Glu-choff-Fiasson and Kuhner 1982). The reliability ofthese tests is subject to some uncertainty because col-or development is influenced by tissue age and con-dition and also by age and composition of the re-agents. Despite these uncertainties, both tests havebeen used extensively in fungal taxonomy for delim-iting species, genera and families (Boidin 1958, Le-mke 1964, Eriksson and Ryvarden 1975).

A number of basidiomycetes combine an amyloidreaction of the basidiospore wall with a sulfo-positivereaction (SA1) of thin-walled, tubular or bladder-likecystidia, so-called gloeocystidia. These examples illus-trate the variety of fungal forms having such prop-erties: Russula Pers. and Lactarius Pers., known asimportant ectomycorrhizal partners in forest ecosys-tems (Gardes and Bruns 1996, Smith and Read 1997)and also widely recognized and collected for con-sumption; coral fungi in the genus Hericium Pers.growing on stumps and living hardwood trees andhighly treasured as medical mushrooms in Asia (Ka-wagishi et al 1993, 1996); the aggressive parasite Het-erobasidion annosum, a polypore causing great eco-nomic losses to the forest industry (Stenlid 1986) andEchinodontium tinctorium, the hydnoid Indian paint

1038 MYCOLOGIA

fungus, also associated with aggressive decay of co-niferous trees (Thomas 1958); several thin inconspic-uous corticoid species of the genera GloeocystidiellumDonk, Boidinia Stalpers & Hjortstam and GloiotheleBres., which mainly live as saprobionts on differentkinds of deadwood (Eriksson and Ryvarden 1975).

Donk (1971) was the first to discuss a possible re-lationship between taxa such as those mentionedabove and other groups possessing a system of gloeo-plerous hyphae (gloeocystidia) and amyloid basidio-spores. His hypothesis was further expanded and de-veloped by Oberwinkler (1977), who also named theentire group the Russulales. Further arguments forrecognizing a unique russuloid lineage among thehomobasidiomycetes have come from recent molec-ular phylogenetic studies (Hibbett and Donoghue1995, Hibbett et al 1997). According to Hibbett andThorn (2001), the clade includes taxa formerlyplaced in the families Auriscalpiaceae Maas Geest.,Bondarzewiaceae Kotl. & Pouzar, ClavicoronaceaeCorner, Corticiaceae Herter sensu lato, Echinodon-tiaceae Donk, Hericiaceae Donk, LachnocladiaceaeDA Reid, Peniophoraceae Lotsy, Polyporaceae Fr. exCorda sensu lato, Russulaceae Lotsy, and StereaceaePilat and is estimated to hold about 1000 describedspecies (Hibbett and Thorn 2001 extrapolating fromHawksworth et al 1995).

Taxa with effused, corticioid basidiomata, a smoothhymenophore, and russuloid staining reactions firstwere placed together in Gloeocystidiellum Donk. Thehistory and scope of the genus was discussed thor-oughly by Donk (1956, 1964). Eriksson and Ryvarden(1975) regarded Gloeocystidiellum as unnatural andsuggested that the taxa known in Northern Europecould be divided into seven groups. All these groupssince have been segregated as genera (Hagstrom1977, Julich 1978, Hallenberg 1980, Hjortstam andStalpers 1982, Hjortstam 1987b, Boidin et al 1997a),and additional genera based on species from otherparts of the world have been added ( Julich 1982, Wu1995, 1996).

To elucidate evolutionary relationships within therussuloid clade, a dataset based on nuclear rDNA se-quence data (5.8S, ITS2 and 26S) was constructed.Taxa were selected with a particular emphasis on cor-ticioid species, but the range covers all major groupsof russuloid taxa except gasteroid and secotioidforms (Hibbett and Thorn 2001). We used this da-taset to (i) identify major clades among the russuloidfungi, (ii) explore how these clades correlate withprevious morphology based classifications and (iii)redefine corticioid genera within the russuloid clade.

MATERIALS AND METHODS

Sampling of taxa. The sampling (TABLE I) was guided byearlier classifications of Gloeocystidiellum in a wide sense and

by the discussions in Donk (1964), Julich (1981), Stalpers(1996) and Hibbett and Thorn (2001). Nomenclature ofthe species included follows Nordic Macromycetes vol 3(Hansen and Knudsen 1997), Hjortstam and Larsson(1995) and Hjortstam (1998), except in those cases wherewe suggest new taxonomic arrangements. We have adoptedthe convention for clade names introduced by Moncalvo etal (2002). Clade names are preceded by a slash, are spelledin lower-case letters and never italicized. We aimed to in-clude representatives from all groups with a combinationof amyloid basidiospores and gloeocystidia but also specieswith only the latter characteristic, providing they stain withsulfovanillin. The amyloid reaction is much more wide-spread and can be found in a number of genera, e.g., inthe corticioid Amyloathelia Hjortstam & Ryvarden, Aphan-obasidium Julich, and Melzericium Julich, in the poroid An-omoporia Pouzar, and in the agaricoid Catathelasma Lovej.,Hydropus (Kuhn) Singer, Melanoleuca Pat., Mycena (Pers. :Fr.) Roussel, and Panellus P. Karst. No comprehensive sam-pling was done from groups where basidiospore amyloidityis not combined with typical gloeocystidia.

A few genera with a gloeoplerous system were not avail-able for sequencing, viz. Acanthofungus Sheng H. Wu et al(three species), Amylofungus Sheng H. Wu (two), Amylos-porus Ryvarden (seven), Amylonotus Ryvarden (four), Dex-trinocystidium Sheng H. Wu (two), Dichantharellus Corner(two), Stecchericium D.A. Reid (13). We also wanted to in-clude Phlebiella paludicola Hjortstam & P. Roberts since itis the only species in Phlebiella with sulfo-positive gloeocys-tidia. The only modern material available is the holotype.The species forms thin basidiomata on dead leaves of marshplants, making it difficult to extract pure DNA. Since suc-cessful sequencing seemed questionable we decided not toput valuable type material at a risk.

All sequences first were aligned with an extensive datasetholding more than 600 taxa sampled from all major groupsof homobasidiomycetes (data not shown). This dataset iscontinuously expanded and used as an in-house tool forsequence quality control, approximate phylogenetic place-ment of new sequences and as a sampling guide. Trees aregenerated with the neighbor-joining method and the Has-egawa-Kishino-Yano 85 (HKY85) substitution model. Puta-tive russuloid taxa that did not cluster with the russuloidclade or showed ambiguous placement were excluded fromthe final dataset.

For 21 species two collections were sequenced to verifyresults but only one sequence was included in the final da-taset. In a few cases, two sequences with the same speciesname are included but then the nucleotide sequences di-verge and they might represent different species or origi-nate from different geographical areas.

Basidioradulum radula and Trichaptum abietinum were se-lected for rooting of trees because several molecular studiessuggest the hymenochaetoid clade as sister group to therussuloid clade (Binder and Hibbett 2001, Hibbett et al1997, 2000, Larsson 2001), although consistently with nosupport or weak support. Seven additional, more distantlyrelated species from Sistotrema Fr. and the heterobasidi-omycete genera Exidia Fr. and Auricularia Bull. were addedto the outgroup.

1039LARSSON AND LARSSON: PHYLOGENY OF RUSSULOID BASIDIOMYCETES

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(Ber

k.&

M.A

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onk

gloe

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tidi

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1043

4/19

33D

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(AF3

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loeo

cyst

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Tai

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(AF4

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cyst

idie

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sp.

gloe

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1325

8/27

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F310

089)

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eocy

stid

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oeoc

ysti

diel

lum

IIN

H12

972/

2679

Rus

sia

GB

(AF3

1009

0)G

loeo

cyst

idie

llum

suba

sper

ispo

rum

(Lit

sch

.)J.

Eri

kss.

&R

yvar

den

gloe

odon

tia

KH

L86

95N

orw

ayG

BA

F506

404

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stid

iellu

mw

aku

llum

Bur

ds.,

Nak

ason

e&

Free

-m

anst

erea

les

Osl

o-93

0107

Tan

zan

iaO

AF5

0644

3

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eocy

stid

iops

isfl

amm

ea(B

oidi

n)

Julic

hst

erea

les

AH

0002

19L

aR

eun

ion

GB

AF5

0643

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loeo

cyst

idio

psis

flam

mea

ster

eale

sC

BS3

24.6

6C

.A

fric

anR

ep.

LYA

F506

437

Glo

eocy

stid

iops

ishe

imii

(Boi

din

)Ju

lich

ster

eale

sC

BS3

21.6

6C

.A

fric

anR

ep.

LYA

F506

381

Glo

eodo

nti

aco

lum

bien

sis

Bur

tex

Bur

ds.

&L

omb.

gloe

odon

tia

NH

1111

8/21

33Sp

ain

,Te

ner

ife

GB

AF5

0644

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loeo

don

tia

disc

olor

(Ber

k.&

M.A

.C

urti

s)B

oidi

ngl

oeod

onti

aK

HL

1009

9Pu

erto

Ric

oG

BA

F506

445

Glo

eodo

nti

apy

ram

idat

a(B

erk.

&M

.A.

Cur

tis)

Hjo

rts-

tam

gloe

odon

tia

LR

1550

2C

olom

bia

OA

F506

446

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eohy

poch

nic

ium

anal

ogu

m(B

ourd

ot&

Gal

zin

)H

jort

stam

NH

1214

0R

ussi

aG

BA

F506

447

Glo

eom

yces

gram

inic

ola

Shen

gH

.W

ust

erea

les

Wu9

210-

12/2

650

Tai

wan

GB

AF5

0644

8


TA

BL

EI.

Con

tin

ued

Spec

ies

Cla

deVo

uch

er/F

CU

Gn

rC

oun

try

Her

bari

uma

Gen

Ban

kac

cess

.n

o.b

Glo

eope

nio

phor

ella

con

volv

ens

(P.

Kar

st.)

Boi

din

,L

anq.

&G

illes

russ

ulal

esK

HL

1010

3Pu

erto

Ric

oG

BA

F506

435

Glo

eope

nio

phor

ella

laxa

(Sh

eng

H.

Wu)

Boi

din

,L

anq.

&G

illes

russ

ulal

esW

u911

010-

8/26

45T

aiw

anN

MN

SA

F506

440

Glo

eope

nio

phor

ella

sp.

russ

ulal

esK

HL

1039

0Pu

erto

Ric

oG

BA

F506

436

Glo

iodo

nn

igre

scen

s(P

etch

)M

aas

Gee

st.

auri

scal

piac

eae

Des

jard

in72

87B

ali

GB

AF5

0645

0G

loio

don

stri

gosu

s(S

w.:F

r.)P.

Kar

st.

auri

scal

piac

eae

JS26

147

Nor

way

OA

F506

449

Glo

ioth

ele

irpi

sces

cen

sB

oidi

npe

nio

phor

ales

LR

3553

3Ve

nez

uela

OA

F506

452

Glo

ioth

ele

lact

esce

ns

(Ber

k.)

Hjo

rtst

ampe

nio

phor

ales

EL

8-98

Swed

enG

BA

F506

453

Glo

ioth

ele

lam

ello

sa(P

.H

enn

.)B

res.

pen

ioph

oral

esK

HL

1103

1Ve

nez

uela

GB

AF5

0645

4G

loio

thel

esp

.pe

nio

phor

ales

LR

4240

7Ve

nez

uela

GB

AF5

0645

1G

loio

thel

eto

rren

dii

(Bre

s.)

Boi

din

&H

.M

ich

elpe

nio

phor

ales

LY16

815

Fran

ceLY

AF5

0645

5H

eric

ium

abie

tis

(Wei

rex

Hub

ert)

K.

Har

riso

nh

eric

iace

aeN

H69

90/6

63C

anad

aG

BA

F506

456

Her

iciu

mal

pest

rePe

rs.

her

icia

ceae

NH

1324

0/27

54R

ussi

aG

BA

F506

457

Her

iciu

mam

eric

anu

mG

inn

sh

eric

iace

aeD

AO

M21

467

Can

ada,

On

t.D

AO

MA

F506

458

Her

iciu

mci

rrha

tum

(Per

s.:F

r.)N

ikol

ajev

ah

eric

iace

aeT

ubin

gen

F794

Ger

man

yT

UB

AF5

0638

5H

eric

ium

cora

lloid

es(S

copo

li:F

r.)Pe

rs.

her

icia

ceae

NH

282/

1229

Swed

enG

BA

F506

459

Her

iciu

mer

inac

eus

(Bul

l.:F

r.)Pe

rs.

her

icia

ceae

NH

1216

3/24

68R

ussi

aG

BA

F506

460

Het

erob

asid

ion

ann

osu

m(F

r.:F

r.)B

ref.

bon

darz

ewia

ceae

NH

1206

7/24

50R

ussi

aG

B(A

F347

096)

Lac

hnoc

ladi

um

sp.

pen

ioph

oral

esK

HL

1055

6Ja

mai

caG

BA

F506

461

Lac

tari

us

leon

isK

ytov

uori

russ

ulal

esSJ

9101

6Sw

eden

GB

AF5

0641

1L

acta

riu

ssu

ben

bora

tus

Lin

dgre

nru

ssul

ales

EL

10-0

0Sw

eden

GB

AF5

0641

2L

acta

riu

svo

lem

us

Fr.

russ

ulal

esK

HL

08-0

0Sw

eden

GB

AF5

0641

3L

auri

liasu

lcat

a(B

urt)

Pouz

arbo

nda

rzew

iace

aeK

HL

8267

Rus

sia

GB

AF5

0641

4L

axit

extu

mbi

colo

r(P

ers.

:Fr.)

Len

tzh

eric

iace

aeN

H51

66/1

350

Swed

enG

B(A

F310

102)

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tin

ellu

sau

ricu

la(F

r.)A

.St

rid

auri

scal

piac

eae

KG

N28

0994

Swed

enG

BA

F506

415

Len

tin

ellu

sca

stor

eus

Fr.

auri

scal

piac

eae

SJ93

067

Swed

enG

BA

F506

416

Len

tin

ellu

sco

chle

atu

s(F

r:F

r)P.

Kar

st.

auri

scal

piac

eae

KG

N96

-09-

28Sw

eden

GB

AF5

0641

7L

enti

nel

lus

omph

alod

es(F

r.)P.

Kar

st.

auri

scal

piac

eae

JJ20

77Sw

eden

GB

AF5

0641

8L

enti

nel

lus

urs

inu

s(F

r.:F

r.)K

uhn

erau

risc

alpi

acea

eE

L73

-97

USA

,N

.C.

GB

AF5

0641

9L

enti

nel

lus

vulp

inu

s(F

r.:F

r.)K

uhn

er&

Mai

reau

risc

alpi

acea

eK

GN

98-0

8-25

Swed

enG

B(A

F347

097)

Meg

aloc

ysti

diu

mch

elid

oniu

m(P

at.)

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din

Lan

q.&

Gil-

les

ster

eale

sL

odge

SJ11

0.1

USA

,V

irgi

nIs

l.G

BA

F506

441

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aloc

ysti

diu

mle

uco

xan

thu

m(B

res.

)Ju

lich

ster

eale

sH

K82

/191

5D

enm

ark

GB

AF5

0642

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egal

ocys

tidi

um

luri

dum

(Bre

s.)

Julic

hst

erea

les

JE24

636/

22Sw

eden

GB

AF5

9642

1M

egal

ocys

tidi

um

luri

dum

ster

eale

sK

HL

8635

Nor

way

GB

AF5

0642

2M

etu

lodo

nti

an

ivea

(P.

Kar

st.)

Parm

asto

pen

ioph

oral

esN

H13

108/

2712

Rus

sia

GB

AF5

0642

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enio

phor

aci

ner

ea(F

r.)C

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ssp.

fagi

cola

Hal

len

b.&

E.

Lar

ss.

pen

ioph

oral

esN

H98

08/1

788

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nG

BA

F506

424

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ioph

ora

inca

rnat

a(P

ers.

:Fr.)

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arst

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nio

phor

ales

NH

1027

1/19

09D

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ark

GB

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0642

5

1042 MYCOLOGIA

TA

BL

EI.

Con

tin

ued

Spec

ies

Cla

deVo

uch

er/F

CU

Gn

rC

oun

try

Her

bari

uma

Gen

Ban

kac

cess

.n

o.b

Pse

udo

xen

asm

ave

rru

cisp

oru

mK

.H.L

arss

.&H

jort

stam

EL

34-9

5Sw

eden

GB

AF5

0642

6R

uss

ula

aura

nti

aca

(Sch

aeff

.)Sc

hae

ff.

russ

ulal

esSJ

9300

6Sw

eden

GB

AF5

0642

7R

uss

ula

nau

seos

aFr

.ru

ssul

ales

SJ97

015

Swed

enG

BA

F506

462

Ru

ssu

lape

rsic

ina

Kro

nbl

.ru

ssul

ales

SJ98

044

Swed

enG

BA

F506

463

Ru

ssu

lasp

hagn

ophi

laK

aufm

.ru

ssul

ales

LA

S81/

108

Swed

enG

BA

F506

464

Ru

ssu

lavi

olac

eaQ

uel.

ss.

Rom

agn

esi

russ

ulal

esSJ

9300

9Sw

eden

GB

AF5

0646

5Sc

ytin

ostr

oma

gala

ctin

um

(Fr.)

Don

kpe

nio

phor

ales

NH

4863

/123

2Sw

eden

GB

AF5

0646

6Sc

ytin

ostr

oma

jack

son

iiB

oidi

npe

nio

phor

ales

NH

6626

/635

Can

ada,

B.C

.G

BA

F506

467

Scyt

inos

trom

aoc

hrol

eucu

m(B

res.

&To

rren

d)D

onk

pen

ioph

oral

esT

AA

1598

69A

ustr

alia

TA

AA

F506

468

Scyt

inos

trom

aod

orat

um

(Fr.)

Don

kpe

nio

phor

ales

KH

L85

46Sw

eden

GB

AF5

0646

9Sc

ytin

ostr

oma

port

ento

sum

(Ber

k.&

M.A

.Cur

tis)

Don

kpe

nio

phor

ales

EL

11-9

9Sw

eden

GB

AF5

0647

0Sc

ytin

ostr

omel

lahe

tero

gen

ea(B

ourd

ot&

Gal

zin

)Pa

r-m

asto

scyt

inos

trom

ella

JS18

244

Nor

way

OA

F506

471

Scyt

inos

trom

ella

nan

nfe

ldti

i(J

.E

riks

s.)

G.W

.Fr

eem

an&

R.H

.Pe

ters

enN

H74

76/1

742

Nor

way

GB

AF5

0647

2

Sist

otre

ma

brin

kman

nii

(Bre

s.)

J.E

riks

s.N

H11

412/

2206

Tur

key

GB

AF5

0647

3Si

stot

rem

aco

ron

illa

(Hoh

n.

&L

itsc

h.)

Don

kN

H75

98/7

85C

anad

a,Q

ue.

GB

AF5

0647

5Si

stot

rem

am

usc

icol

a(P

ers.

)S.

Lun

dell

KH

L87

94Sw

eden

GB

AF5

0647

4Si

stot

rem

ase

rnan

deri

(Lit

sch

.)D

onk

KH

L85

76Sw

eden

GB

AF5

0647

6St

ereu

mhi

rsu

tum

(Will

d.:F

r.)S.

F.G

ray

ster

eale

sN

H79

60/1

022

Rom

ania

GB

AF5

0647

9St

ereu

mre

flex

ulu

mR

eid

ster

eale

sE

L48

-97

Spai

n,

Ten

erif

eG

BA

F506

490

Ster

eum

rugo

sum

(Per

s.:F

r.)Fr

.st

erea

les

NH

1195

2/23

53D

enm

ark

GB

AF5

0648

1St

ereu

msp

.st

erea

les

FCU

G26

71R

ussi

aG

BA

F506

483

Ster

eum

subt

omen

tosu

mPo

uzar

ster

eale

sE

L11

-97

Spai

n,

Ten

erif

eG

BA

F506

482

Tri

chap

tum

abie

tin

um

(Fr.)

Ryv

arde

nN

H12

842/

2581

Fin

lan

dG

B(A

F347

104)

Vara

ria

inve

stie

ns

(Sch

wei

n.)

P.K

arst

.pe

nio

phor

ales

TA

A16

4122

Nor

way

TA

AA

F506

484

Vara

ria

ochr

oleu

ca(B

ourd

ot&

Gal

zin

)D

onk.

pen

ioph

oral

esJS

2440

0N

orw

ayO

AF5

0648

5Ve

sicu

lom

yces

citr

inu

s(P

ers.

)H

agst

rom

pen

ioph

oral

esE

L53

-97

Swed

enG

BA

F506

486

Vesi

culo

myc

esep

ithe

loid

esB

oidi

n,

Lan

q.&

Gill

espe

nio

phor

ales

CB

S404

.83

Mad

agas

car

LYA

F506

487

Wri

ghto

pori

aav

ella

nea

(Bre

s.)

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arsc

ytin

ostr

omel

laL

R41

710

Jam

aica

OA

F506

488

Wri

ghto

pori

ale

nta

(Ove

rh.

&L

owe)

Pouz

arK

N15

0311

Jam

aica

OA

F506

489

Wri

ghto

pori

atr

opic

alis

(Coo

ke)

Ryv

arde

nL

R40

352

Ven

ezue

laO

AF5

0649

0X

ylob

olu

sfr

ust

ula

tus

(Per

s.:F

r.)B

oidi

nst

erea

les

KG

N98

0928

Swed

enG

BA

F506

491

aA

cron

yms

for

her

bari

afo

llow

Hol

mgr

enet

al(1

990)

.b

Sequ

ence

sal

read

ypu

blis

hed

hav

eac

cess

ion

num

bers

inpa

ren

thes

es.


As standard mounting media for microscopic examina-tions of specimens, 2% KOH, Melzer’s reagent and sulfov-anillin have been used (Moser 1978).

Molecular techniques. DNA was isolated from herbariumspecimens and from cultured mycelia. Mycelia were grownat room temperature for 2 wk in 50 mL MYG liquid media(1% malt extract, 0.4% yeast extract, 1% glucose). Myceliawere harvested and dried between sheets of filter paper andca 50 mg was placed in microcentrifuge tubes. From her-barium specimens ca 3 3 3 mm of hymenium was used toextract DNA. DNA extractions were carried out using amodified 2% CTAB method (Savolainen et al 1995). Prep-arations from some of the herbarium specimens were fur-ther purified with Gene Clean (Bio 101 Inc.) to excludePCR inhibitors. The internal transcribed spacer 1 and 2(ITS 1 and 2) including the 5.8S region of nuclear rDNA,was amplified with primers ITS1F, ITS4B (Gardes and Bruns1993), ITS1 and ITS4 (White et al 1990). Approximately1200 bp of the 59 end of the large subunit of the rDNA(nuclear LSU) was amplified with LR0R and LR7 (Vilgalysand Hester 1990).

PCR amplifications were performed in 25 mL reactionsusing either Taq polymerase (Advanced Biotechnologies)together with reaction buffer IV or Ready To Goy PCRbeads (Amersham Pharmacia Biotech Inc.). The thermalcycling program included 4 min at 95 C, followed by 30cycles of 30 s at 95 C, 30 s at 52 C, 60 s at 72 C, and thenended by 8 min at 72 C. Fragments were examined on a1% SeaKem (FMC) agarose gel, and amplified productswere purified with QIAquick spin columns (QIAGEN).

Primers used for sequencing of both strands were ITS3,ITS4 (White et al 1990), LR5, LR21, LR3r (http://WWW.biology.duke.edu/fungi.html), and CTB6 (http://mendel.berkeley.edu/boletus.html). Cycle sequencing wascarried out using Thermosequenase flourescent labeledprimer cycle sequencing kit with 7-deaza-dGTP (AmershamPharmacia Biotech Inc.). Twenty-five ng of template DNAand 5 pmol Cy5-labeled primer were used per reaction. Se-quences were obtained using an ALFExpress (PharmaciaBiotech Inc.) automated sequencer. Sequences were editedand assembled using computer software ALF manager(Pharmacia Biotech) and Sequencher 3.1 (Gene CodesCorp.). Complete sequences were aligned manually usingthe data editor PAUP* 4.0 (Swofford 1999). Sequences weresubmitted to GenBank, and accession numbers are given inTABLE I.

The LSU sequence of Bondarzewia berkeleyi in this studywas taken from GenBank (AF218563). The aligned data ma-trices are available from the corresponding author uponrequest.

Phylogenetic analyses. Heuristic searches were performedusing PAUP* 4.0b8 (Swofford 1999) on a Power Macintoshcomputer. All transformations were considered unorderedand equally weighted. Variable regions with ambiguousalignment were excluded, and gaps were treated as missingdata. Heuristic searches with 1000 random-addition se-quence replicates, TBR branch swapping and MAXTREESset to 25 000 with restrictions to save 100 trees in each rep-licate, were performed.

Neighbor-joining analysis (NJ) was performed on thesame dataset using the Hasegawa-Kishino-Yano 85 (HKY85)substitution model.

Ten selected trees, with the best-likelihood score, fromthe initial heuristic searches were used as starting trees inrecurrent heuristic searches, with TBR and NNI branchswapping, under the maximum-likelihood criteria (ML) tosearch for more optimal trees. ML parameter settings cor-responded to HKY851I model, with the nucleotide substi-tution rate parameters estimated via ML. Searches usingTBR swapping were aborted before completion (after 24 h),due to the large dataset and computationally intensive al-gorithms. Trees with the best-likelihood scores were savedfor comparison.

To compare tree topologies of alternative phylogenetichypotheses for the dataset, several constrained analyseswere conducted. Constrained trees forcing monophyly of/peniophorales and keeping it as a sister clade to the restof the russuloid clade were constructed using Mac Clade4.0 (Maddison and Maddison 2000). All nodes within theclades were collapsed. Heuristic searches with 100 random-addition sequence replicate, enforcing constraints and sav-ing only trees compatible with constraint topologies wereperformed using the same taxa and settings as above. Con-strained analyses to test the support for monophyly of theG. porosum-clavuligerum complex were performed in thesame way.

Topological differences between the constrained phylo-genetic tree hypothesis and unconstrained trees were eval-uated with Kishino-Hasegawa (KH) maximum-likelihood ra-tio test (normal approximation, two-tailed test) and the Shi-modaira-Hasegawa (SH) test (using RELL bootstrap) imple-mented in PAUP*.

To improve the resolution within Stereum and allied gen-era, 27 sequences from the large dataset were realigned toinclude more characters from the variable ITS2 region.One sequence of Gloeocystidiellum aspellum was added, andGloeodontia pyramidata was selected as outgroup. In the par-simony analysis, all transformations were considered unor-dered and equally weighted. Variable regions with ambig-uous alignment were excluded, and gaps were treated asmissing data. Heuristic searches with 1000 random-additionsequence replicates, TBR branch swapping and MAXTREESset to auto-increase, were performed.

Relative robustness of clades was estimated by bootstrap-ping, with the following settings. For the large dataset byusing 1000 bootstrap replicates, with five random-additionsequences per replicate, TBR branch swapping and MAX-TREES set to 25 000 with restrictions to save 100 trees ineach replicate. For the Stereum-restricted dataset by using1000 bootstrap replicates, with 100 random-addition se-quences per replicate, TBR branch swapping and MAX-TREES set to auto-increase.

Morphological characters. Morphological features of thebasidiome, hymenophore and spore surface, presence ofclamps and skeletal hyphae, type of life strategy, nuclearbehavior and polarity (if available) have been observed orgathered from literature and compiled in TABLE II. Data onnuclear behavior and polarity are mainly taken from Boidin

1044 MYCOLOGIAT

AB

LE

II.

Sum

mar

yof

som

em

orph

olog

ical

and

cyto

logi

cal

char

acte

rs.

Tax

onor

der

follo

ws

the

stri

ctco

nse

nsu

str

ee(F

ig.

2).

Cur

ren

tly

acce

pted

gen

eric

posi

tion

sar

ein

dica

ted.

Spec

ies

Cla

deG

enus

Lif

eB

asb

Hym

cSp

dA

me

SAf

Skeg

PhN

uci

Cj

Vesi

culo

myc

esci

trin

us

Glo

ioth

ele

lact

esce

ns

Vesi

culo

myc

esep

ithe

loid

esG

loio

thel

eir

pisc

esce

ns

Glo

ioth

ele

lam

ello

saG

loio

thel

eto

rren

dii

Glo

ioth

ele

sp.

Scyt

inos

trom

apo

rten

tosu

mA

ster

ostr

oma

cerv

icol

orA

ster

ostr

oma

mu

scic

ola

pen

ioph

oral

espe

nio

phor

ales

pen

ioph

oral

espe

nio

phor

ales

pen

ioph

oral

espe

nio

phor

ales

pen

ioph

oral

espe

nio

phor

ales

pen

ioph

oral

espe

nio

phor

ales

Vesi

culo

myc

esG

loio

thel

eG

loio

thel

eG

loio

thel

eG

loio

thel

eG

loio

thel

eG

loio

thel

eSc

ytin

ostr

oma

Ast

eros

trom

aA

ster

ostr

oma

S S S S S S S S S S

Eff

Eff

Eff

Eff

Eff

Eff

Eff

Eff

Eff

Eff

S S S S S S S S S S

S S S S S S S S L L

Y Y Y Y Y Y Y Y Y Y

N Y Y Y Y Y Y Y N/Y

N

N N N N N N N Y Y Y

h h h h h IV h

SN SN SN SN SN SN*

SN*

a a a a a a a a

Ast

eros

trom

ala

xum

Scyt

inos

trom

aoc

hrol

eucu

mVa

rari

aoc

hrol

euca

Lac

hnoc

ladi

um

sp.

Scyt

inos

trom

aod

orat

um

Vara

ria

inve

stie

ns

Pen

ioph

ora

cin

erea

ssp.

fagi

cola

Pen

ioph

ora

inca

rnat

aD

ich

oste

reum

palle

scen

sD

ich

oste

reum

sp.

pen

ioph

oral

espe

nio

phor

ales

pen

ioph

oral

espe

nio

phor

ales

pen

ioph

oral

espe

nio

phor

ales

pen

ioph

oral

espe

nio

phor

ales

pen

ioph

oral

espe

nio

phor

ales

Ast

eros

trom

a? ? ? ? Va

rari

aP

enio

phor

aP

enio

phor

aD

icho

ster

eum

Dic

host

ereu

m

S S S S S S S S S S

Eff

Eff

Eff

Cla

vE

ffE

ffE

ffE

ffE

ffE

ff

S S S S S S S S S S

S S S S S S S S O O

Y N N Y N N/Y

N N Y Y

N Y N N N Y N Y Y Y

Y Y Y Y Y Y N N Y Y

h H h IV IV IV

SN HD

*

N N SN He

a a a a c c c c

Dic

host

ereu

mdu

rum

Dic

host

ereu

mgr

anu

losu

mD

icho

ster

eum

effu

scat

um

Scyt

inos

trom

aja

ckso

nii

Scyt

inos

trom

aga

lact

inu

mM

etu

lodo

nti

an

ivea

Con

fert

obas

idiu

mol

ivac

eoal

bum

Con

fert

obas

idiu

msp

.W

righ

topo

ria

trop

ical

isSc

ytin

ostr

omel

lan

ann

feld

tii

pen

ioph

oral

espe

nio

phor

ales

pen

ioph

oral

espe

nio

phor

ales

pen

ioph

oral

espe

nio

phor

ales

pen

ioph

oral

espe

nio

phor

ales

Dic

host

ereu

mD

icho

ster

eum

Dic

host

ereu

m? ? M

etu

lodo

nti

aC

onfe

rtob

asid

ium

Con

fert

obas

idiu

m? ?

S S S S S S S S S S

Eff

-Ref

Eff

Eff

Eff

Eff

Eff

Eff

Eff

Eff

Eff

S S S S S S S S P S

O O O S S S S S O O

Y Y Y N SP N Y Y Y Y

Y Y Y N/Y

Y Y Y Y Y Y

Y Y Y Y Y N Y Y Y Y

IV IV IV h IV IV h

He*

SN*

He

N N N

c c c c c c c c cG

loeo

hypo

chn

iciu

man

alog

um

Ech

inod

onti

um

ryva

rden

iiG

loeo

cyst

idie

llum

clav

ulig

eru

mG

loeo

cyst

idie

llum

purp

ure

mG

loeo

cyst

idie

llum

bisp

oru

mG

loeo

pen

ioph

orel

lala

xaG

loeo

pen

ioph

orel

laco

nvo

lven

sG

loeo

pen

ioph

orel

lasp

.L

acta

riu

sle

onis

Lac

tari

us

sube

nbo

ratu

s

gloe

ocys

tidi

ellu

mgl

oeoc

ysti

diel

lum

gloe

ocys

tidi

ellu

mru

ssul

ales

russ

ulal

esru

ssul

ales

russ

ulal

esru

ssul

ales

Glo

eohy

poch

nic

ium

? Glo

eocy

stid

iellu

mG

loeo

cyst

idie

llum

Glo

eocy

stid

iellu

mG

loeo

pen

ioph

orel

laG

loeo

pen

ioph

orel

laG

loeo

pen

ioph

orel

laL

acta

riu

sL

acta

riu

s

S S S S S S S S M M

Eff

Pil

Eff

Eff

Eff

Eff

Eff

Eff

Stip

Stip

S H S S S S S S L L

O O O O O O O O O O

N Y Y Y Y Y Y Y Y Y

Y Y N N/Y

Y Y Y Y Y N

N Y N N N N N N N N

? IV IV P

? N N HM

c b c c a a a a a


TA

BL

EII

.C

onti

nue

d

Spec

ies

Cla

deG

enus

Lif

eB

asb

Hym

cSp

dA

me

SAf

Skeg

PhN

uci

Cj

Lac

tari

us

vole

mu

sR

uss

ula

viol

acea

Ru

ssu

laau

ran

tiac

aR

uss

ula

spha

gnop

hila

Ru

ssu

lan

ause

osa

Ru

ssu

lape

rsic

ina

Glo

eocy

stid

iellu

mac

ule

atu

mB

oidi

nia

pron

inqu

aB

oidi

nia

sp.

Boi

din

iafu

rfu

race

a

russ

ulal

esru

ssul

ales

russ

ulal

esru

ssul

ales

russ

ulal

esru

ssul

ales

russ

ulal

esru

ssul

ales

russ

ulal

esru

ssul

ales

Lac

tari

us

Ru

ssu

laR

uss

ula

Ru

ssu

laR

uss

ula

Ru

ssu

laB

oidi

nia

Boi

din

iaB

oidi

nia

Boi

din

ia

M M M M M M S S S S

Stip

Stip

Stip

Stip

Stip

Stip

Eff

Eff

Eff

Eff

L L L L L L S S S S

O O O O O O O O O O

Y Y Y Y Y Y Y Y Y Y

N Y Y N Y N Y Y Y Y

N N N N N N N N N Nh

N

a a a a a a a a cP

seu

doxe

nas

ma

verr

uci

spor

um

Glo

iodo

nst

rigo

sus

Glo

iodo

nn

igre

scen

sA

uri

scal

piu

mvu

lgar

eA

uri

scal

piu

mvi

llipe

sD

enti

prat

ulu

mbi

alov

iese

nse

Len

tin

ellu

som

phal

odes

Len

tin

ellu

sca

stor

eus

Len

tin

ellu

su

rsin

us

Len

tin

ellu

svu

lpin

us

auri

scal

piac

eae

auri

scal

piac

eae

auri

scal

piac

eae

auri

scal

piac

eae

auri

scal

piac

eae

auri

scal

piac

eae

auri

scal

piac

eae

auri

scal

piac

eae

auri

scal

piac

eae

Pse

udo

xen

asm

aG

loio

don

Glo

iodo

nA

uri

scal

piu

mA

uri

scal

piu

mD

enti

prat

ulu

mL

enti

nel

lus

Len

tin

ellu

sL

enti

nel

lus

Len

tin

ellu

s

S S S S S S S S S P

Eff

Eff

-Ref

Eff

-Ref

Stip

Pil

Cla

vPi

lPi

lPi

lPi

l

S H H H H H L L L L

O O O O O O O O O O

Y Y Y Y Y Y Y Y Y Y

Y Y Y Y Y Y Y Y Y Y

N Y Y Y Y N Y Y Y Y

IV IV IV IV IV IV IV

N N

c c b c c c c c c cL

enti

nel

lus

auri

cula

Len

tin

ellu

sco

chle

atu

sG

loeo

cyst

idie

llum

suba

sper

ispo

rum

Glo

eodo

nti

aco

lum

bien

sis

Glo

eodo

nti

adi

scol

orG

loeo

don

tia

pyra

mid

ata

Con

fert

iciu

moc

hrac

eum

Meg

aloc

ysti

diu

mlu

ridu

mM

egal

ocys

tidi

um

leu

coxa

nth

um

Glo

eocy

stid

iellu

mw

aku

llum

auri

scal

piac

eae

auri

scal

piac

eae

gloe

odon

tia

gloe

odon

tia

gloe

odon

tia

gloe

odon

tia

ster

eale

sst

erea

les

ster

eale

sst

erea

les

Len

tin

ellu

sL

enti

nel

lus

Glo

eodo

nti

aG

loeo

don

tia

Glo

eodo

nti

aG

loeo

don

tia

Con

fert

iciu

mM

egal

ocys

tidi

um

Meg

aloc

ysti

diu

mM

egal

ocys

tidi

um

S S S S S S S S S S

Pil

Pil

Eff

Eff

Eff

Eff

Eff

Eff

Eff

Eff

L L S H H H S S S S

O O O O O O S S S S

Y Y Y Y Y Y Y Y Y Y

Y Y Y Y Y Y N N N N

Y Y N N Y Y N N N N

h II II H H H H

N N HC

He

He

HC

c c c c c a c c ovA

leu

rodi

scu

sce

russ

atu

sA

leu

rodi

scu

sde

xtri

noi

deoc

eru

ssat

us

Glo

eom

yces

gram

inic

ola

Ale

uro

botr

ysbo

tryo

sus

Glo

eocy

stid

iellu

mfo

rmos

anu

mG

loeo

cyst

idie

llum

com

pact

um

Glo

eocy

stid

iellu

mas

pellu

mM

egal

ocys

tidi

um

chel

idon

ium

Boi

din

iam

acro

spor

aSt

ereu

mre

flex

ulu

m

ster

eale

sst

erea

les

ster

eale

sst

erea

les

ster

eale

sst

erea

les

ster

eale

sst

erea

les

ster

eale

sst

erea

les

? ? Glo

eom

yces

Ale

uro

botr

ys? ? ? ? ? St

ereu

m

S S S S S S S S S S

Eff

Eff

Eff

Eff

Eff

Eff

Eff

Eff

Eff

Eff

-Ref

S S S S S S S S S S

S S S O O O O S O S

Y Y N Y Y Y Y Y Y Y

Y Y Y Y Y Y Y Y Y 0

N N N N N N N N N N

II H II h hII

H

He

Hc

SN SN N HD

c c ov i c c c c

1046 MYCOLOGIAT

AB

LE

II.

Con

tin

ued

Spec

ies

Cla

deG

enus

Lif

eB

asb

Hym

cSp

dA

me

SAf

Skeg

PhN

uci

Cj

Ster

eum

subt

omen

tosu

mSt

ereu

mhi

rsu

tum

Ster

eum

sp.

Ster

eum

rugo

sum

Aca

nth

ophy

sellu

mliv

idoc

aeru

leu

mX

ylob

olu

sfr

ust

ula

tus

Con

fert

iciu

mra

vum

Glo

eocy

stid

iops

ishe

imii

Glo

eocy

stid

iellu

mcr

ypta

can

thu

mG

loeo

cyst

idio

psis

flam

mea

ster

eale

sst

erea

les

ster

eale

sst

erea

les

ster

eale

sst

erea

les

ster

eale

sst

erea

les

ster

eale

sst

erea

les

Ster

eum

Ster

eum

Ster

eum

Ster

eum

Xyl

obol

us

Xyl

obol

us

Glo

eocy

stid

iops

isG

loeo

cyst

idio

psis

Glo

eocy

stid

iops

isG

loeo

cyst

idio

psis

S S S S S S S S S S

Eff

-Ref

Eff

-Ref

Eff

-Ref

Eff

-Ref

Eff

Eff

Eff

Eff

Eff

Eff

S S S S S S S S S S

S S S S S S O O O O

Y Y Y Y Y Y Y Y Y Y

0 0 0 0 Y 0 Y Y Y Y

N N N N N N N N N N

H H H II H H H H

HC

HC

HC

As

HC

HC

HC

HC

v v v va r ov v vA

leu

rodi

scu

sam

orph

us

Art

omyc

espy

xida

tus

Am

ylos

tere

um

areo

latu

mA

myl

oste

reu

mla

evig

atu

mA

myl

oste

reu

mch

aille

tii

Glo

eocy

stid

iellu

msp

.G

loeo

cyst

idie

llum

poro

sum

Glo

eocy

stid

iellu

msp

.B

oidi

nia

gran

ula

taH

eric

ium

alpe

stre

ster

eale

sam

ylos

tere

acea

eam

ylos

tere

acea

eam

ylos

tere

acea

eam

ylos

tere

acea

egl

oeoc

ysti

diel

lum

gloe

ocys

tidi

ellu

mgl

oeoc

ysti

diel

lum

gloe

ocys

tidi

ellu

mh

eric

iace

ae

Ale

uro

disc

us

Art

omyc

esA

myl

oste

reu

mA

myl

oste

reu

mA

myl

oste

reu

mG

loeo

cyst

idie

llum

Glo

eocy

stid

iellu

mG

loeo

cyst

idie

llum

Glo

eocy

stid

iellu

mH

eric

ium

S S S S S S S S S P

Eff

Cla

vE

ff-R

efE

ffE

ffE

ffE

ffE

ffE

ffPi

l

S S S S S S S S S H

O S S S S O O O O O

Y Y Y Y Y Y Y Y Y Y

0 Y Y Y Y Y Y Y Y N

N N Y N Y N N N N N

IV IV IV IV II IV

N N N N N N

a c c c c c c cH

eric

ium

amer

ican

um

Her

iciu

mab

ieti

sH

eric

ium

erin

aceu

sH

eric

ium

cirr

hatu

mH

eric

ium

cora

lloid

esD

enti

pelli

sdi

ssit

aD

enti

pelli

sfr

agili

sD

enti

pelli

ssp

.L

axit

extu

mbi

colo

rA

lbat

rellu

sco

nfl

uen

s

her

icia

ceae

her

icia

ceae

her

icia

ceae

her

icia

ceae

her

icia

ceae

her

icia

ceae

her

icia

ceae

her

icia

ceae

her

icia

ceae

alba

trel

lus

Her

iciu

mH

eric

ium

Her

iciu

mH

eric

ium

Her

iciu

mD

enti

nel

lisD

enti

nel

lisD

enti

nel

lisL

axit

extu

mA

lbat

rellu

s

P S P P S S P S S M?

Pil

Pil

Pil

Pil

Pil

Eff

Eff

Eff

Eff

-Ref

Stip

H H H H H H H S S P

O O O S O O O O O S

Y Y Y Y Y Y Y Y Y Y

N N N N N N N N N N

N N N N N N N N N N

IV IV IV IV II IV IV

N N

b b c c c c c cA

lbat

rellu

spe

s-ca

prae

Alb

atre

llus

subr

ube

scen

sA

lbat

rellu

sov

inu

sA

leu

rocy

stid

iellu

mdi

scif

orm

eA

leu

rocy

stid

iellu

msu

bcru

enta

tum

Bon

darz

ewia

berk

elev

iH

eter

obas

idio

nan

nos

um

Lau

rilia

sulc

ata

Ech

inod

onti

um

tin

ctor

ium

Scyt

inos

trom

ella

hete

roge

nea

Wri

ghto

pori

aav

ella

nea

Wri

ghto

pori

ale

nta

alba

trel

lus

alba

trel

lus

alba

trel

lus

aleu

rocy

stid

iellu

mal

euro

cyst

idie

llum

bon

darz

ewia

ceae

bon

darz

ewia

ceae

bon

darz

ewia

ceae

bon

darz

ewia

ceae

scyt

inos

trom

ella

scyt

inos

trom

ella

Alb

atre

llus

Alb

atre

llus

Alb

atre

llus

Ale

uro

cyst

idie

llum

Ale

uro

cyst

idie

llum

Bon

darz

ewia

Het

ereb

asid

ion

Lau

rilia

Ech

inod

onti

um

Scyt

inos

trom

ella

? Wri

ghto

pori

a

M?

M M S S P P S P S S S

Stip

Stip

Stip

Eff

Eff

Pil

Eff

Eff

-Ref

Pil

Eff

Eff

Eff

P P P S S P P S H S P P

S S S O O O O O O O O O

N Y N Y Y Y N Y Y Y Y Y

N N N Y 0 Y Y N N Y 0 Y

N N N N Y Y Y Y Y Y Y Y

IV IV II II IV

He

He

N N

c a a c c c c c c c c


←a Life 5 life strategy S 5 saprophytic. M 5 mycorrhizal; P 5 potentially parasitic.b Bas 5 basidiome morphology; Clav 5 clavarioid; Eff 5 effused; Eff-Ref 5 effused-reflexed; Pil 5 pileate; Stip 5 stipitate.c Hym 5 hymenophore configuration; H 5 hydnoid; L 5 lamellate; P 5 poroid; S 5 smooth.d Sp 5 basidiospore surface; L 5 smooth but lobed; O 5 ornamented; S 5 smooth.e Am 5 basidiospore wall reaction to Melzer’s; N 5 negative; Y 5 positive.f SA 5 reaction of gloeocystidia to sulfovanilline; N 5 negative; Y 5 positive; 0 5 gloeocystidia lacking.g Ske 5 presence of skeletal hyphae; N 5 skeletal hyphae lacking; Y 5 skeletal hyphae present.h P 5 sexual system (polarity); H 5 homothallic; h 5 heterothallic but polarity unknown; II 5 heterothallic bipolar; IV 5

heterothallic tetrapolar; P 5 parthenogenetic.i Nuc 5 nuclear behavior; As 5 astatocoenocytic; HC 5 holocoenocytic; HD 5 holodikaryotic; He 5 heterocytic; HM 5

holomonokaryotic; N 5 normal; SN 5 subnormal. An asterisk indicates that irregularities occur. For a description of thedifferent types of nuclear behavior see Boidin and Lanquetin (1984b).

j C 5 occurence of clamps in cultured mycelium; a 5 totally absent; b 5 clamps present but distribution not known; c 5constant, i 5 inconstant, clamps lacking at some septa; ov 5 opposite clamps at some septa but most septa simple; r 5 clampsrare; v 5 verticillate clamps present at subicular hyphae; va 5 variable, different septation at aerial and submerged hyphae.The terminology follows Boidin and Lanquetin (1984b).

and Lanquetin (1984b, 1997) and Boidin (1990). To visu-alize the distribution of observed characters, TABLE II showsspecimens in the order they occur in the strict consensustree (FIG. 2).

RESULTS

Initial analyses included sequences of Wrightoporiabracei (Murrill) Ryvarden, Dendrothele spp. and Dicho-pleuropus sp., which in preliminary tests with ourhomobasidiomycete inclusive dataset showed affinityto the russuloid clade. These taxa consistently gen-erated long branches because of extensive sequencedeviations in regions otherwise easily aligned. What-ever the cause of these differences, single taxa onlong branches might have negative effects on thephylogenetic analyses through so-called long-branchattraction (Felsenstein 1978). The problem can beaddressed best through the addition of taxa that canbreak up the long branches. Since we could not findsuch taxa, we preferred to exclude the above-men-tioned taxa from the present study. However, theyshould be given renewed consideration in futureanalyses with an expanded sampling of the russuloidclade. The final dataset included 127 ingroup se-quences representing 43 genera and ca 120 species,two-thirds of which (80 species) have effused basi-diomata and either a smooth or a hydnoid hymen-ophore. They would be considered by most mycolo-gists as corticioid and earlier were classified in thefamily Corticiaceae (FIG. 1).

The aligned data matrix covered 1993 base pairs(bp), starting at position 60 in the 5.8S region andincluding ITS2 and the 59 end of the LSU. Gaps forinsertion-deletion events were introduced to aid inthe alignment. The partial 5.8S region was easilyaligned through all sequences. The ITS2 region was

impossible to align over the entire dataset and, ex-cept for a small region of 12 base pairs, these char-acters were excluded. The 59 end of the LSU waseasily aligned in the conservative parts but moreproblematic in the variable domains D1–D3 (Hoppleand Vilgalys 1999). Most characters from ambiguousregions were excluded from the analysis. The finaldataset included 1240 aligned positions, of which 170were variable but uninformative and 364 were parsi-mony informative.

The phylogenetic analysis recovered 24 772 equallyparsimonious trees of 2468 steps (CI 5 0.3002, RI 50.7297). The trees were recovered from 263 islands,where the islands found in different replicates in factmight belong to the same island. A set of 2630 most-parsimonious (MP) trees (10 from each island) wereselected and kept for comparisons and analyses. FIG-URE 1 illustrates one of the MP trees presented as aphylogram to show the number of character statechanges per branch. The tree selected was one of theMP trees with the best-likelihood score. Species thathave been combined within Gloeocystidiellum aremarked with filled dots. FIGURE 2 illustrates the strict-consensus tree of all 24 772 MP trees.

The bootstrap analysis recovered 13 major sup-ported clades and six species on single branches.Each clade and its corresponding bootstrap value areindicated in the phylogram (FIG. 1) and the strict-consensus tree (FIG. 2). We have chosen names thatroughly correspond to the current concepts of or-ders, families and genera in fungal taxonomy (Hawk-sworth et al 1995). When competing names are avail-able, we have selected the oldest one. The clades are:/peniophorales, /amylostereaceae, /gloeocystidiel-lum I, /gloeocystidiellum II, /auriscalpiaceae,/gloeodontia, /aleurocystidiellum, /hericiaceae,

1048 MYCOLOGIA

FIG. 1. Phylogeny of the russuloid lineage based on unweighted parsimony analysis of nuclear rDNA sequence data. Oneof 24 772 equally parsimonious trees depicted as a phylogram (tree length 2468, CI 5 0.3002, RI 5 0.7297). Filled dotsindicate species that have been combined in Gloeocystidiellum. Bootstrap support is noted only for major clades discussed inthe text.


FIG. 2. Strict-consensus tree of 24 772 equally parsimonious trees. Bootstrap values for discussed major clades are givenas numeric values. Asterisks indicate other bootstrap values above 80%. Names marked with a dot represent genus typespecies.

1050 MYCOLOGIA

/bondarzewiaceae, /albatrellus, /scytinostromella,/russulales and /stereales. Taxa on single branchesare Wrightoporia tropicalis, W. lenta, Scytinostromellanannfeldtii, Gloeohypochnicium analogum, Echinodon-tium ryvardenii and Pseudoxenasma verrucisporum.The bootstrap consensus-tree topology was almostidentical to the strict-consensus tree with one maindifference, a node uniting /stereales and /gloeodon-tia in the strict-consensus tree. The NJ analysis recov-ered the same 13 clades as the parsimony analysis butwith a major difference in the basal topology. The NJtree places /peniophorales as a sister clade to the restof the ingroup (see FIG. 3). None of the MP treesrecovered a similar topology. However, short incom-plete (nonconstrained) heuristic searches with thesame settings as in the parsimony analysis, occasion-ally recovered a similar topology as the NJ tree. Suchtrees were three steps longer (2471 steps) than themost-parsimonious trees. Constrained parsimonyanalyses simulating the basal topology of the NJ tree(/peniophorales forced as a sister clade to the restof the russuloid clade) recovered 4700 trees of 2473steps (five steps longer than the unconstrainedtrees). The constrained trees were found not to besignificantly worse than the unconstrained trees,based on the KH test (P 5 0.2982–0.6028) and theSH test (P 5 0.754–0.959).

Heuristic searches, forcing constraints for mono-phyly of the Gloeocystidiellum porosum-clavuligerumcomplex, recovered 3600 trees of 2474 steps (sixsteps longer than the unconstrained trees). Thesetrees were found not to be significantly worse thanthe unconstrained trees by the KH test (P 5 0.1020–0.3651) or the SH test (P 5 0.515–0.892).

Recurrent heuristic searches under maximum-like-lihood criteria with starting trees from the MP anal-ysis recovered several trees with a better-likelihoodscore than the starting tree. In general the TBRbranch swapping recovered better likelihood scoresthan the NNI branch swapping, despite the incom-plete analyses. The result might indicate the exis-tence of more optimal trees not recovered in theheuristic searches.

Phylogenetic analysis of the realigned dataset re-stricted to /stereales recovered 12 MP trees of 407steps, based on 118 parsimony-informative characters(CI 5 0.5971, RI 5 0.6840). FIGURE 4 presents thestrict-consensus tree with bootstrap values indicatedabove branches. Six clades with bootstrap supportabove 50% were identified: /gloeocystidiopsis, /ster-eum, /xylobolus, /chelidonium, /cerussatus and/megalocystidium. Conferticium ochraceum is placedon a single branch between /chelidonium and /cer-ussatus. Aleurobotrys botryosus and Aleurodiscus amor-

phus also were placed on single branches at the baseof the tree.

Morphological and cytological features for all taxaare summarized in TABLE II.

DISCUSSION

The phylogenetic analyses identify 13 major cladeswith strong or fair bootstrap support. These cladesare recovered always and appear resistant to changesin taxon sampling, character selection and methodchosen for analysis. Basal nodes are poorly resolvedand most basal branches collapse to a polytomy inthe strict consensus and bootstrap trees.

A basal division of our dataset in /peniophoralesand /eurussuloid was recovered in the NJ tree (FIG.3) while the parsimony analyses generally did notsupport such a topology. As discussed below there aresome morphological trends in /peniophorales thatsets this clade apart from the rest of the russuloidlineage and the constrained analysis does not rejectthe NJ topology. A denser sampling within /penio-phorales eventually might show if the NJ topologyreceives increased support.

All species with a gloeoplerous hyphal system thatwe tested with our large homobasidiomycete datasetturned out to cluster with the russuloid clade. Thisgives strong indications that possession of a gloeo-plerous hyphal system, often primarily observed astubular gloeocystidia, is a synapomorphy for the rus-suloid clade. This assumption, however, must be test-ed finally with a more inclusive dataset. In most taxathe gloeoplerous system gives a positive reaction withsulfobenzaldehyde, while in others it reacts positiveonly when fresh but loses this reaction after someperiod of storage (e.g., Asterostroma). A third groupis formed by those taxa that never give a positive re-action with sulfobenzaldehyde. However, sequenceanalysis and morphological features support the hy-pothesis that all gloeoplerous systems within the rus-suloid lineage, whether sulfo-positive or not, are ho-mologous (TABLE II).

In species having basidiomes with a dense texturedominated by thick-walled hyphae, the gloeopleroushyphae might be hard to detect, e.g., in Heterobasi-dion annosum and Bondarzewia montana, which hasled to conflicting views presented in the literature(Redhead and Norvell 1993). In both cases sulfo-pos-itive gloeocystidia develop in culture (Gluchoff-Fias-son et al 1983). In Stereum Pers., typical gloeopleroushyphae are lacking but it seems likely that the lactif-erous hyphae present in most Stereum species are ho-mologues.

The amyloid reaction of the spore wall is a secondcharacter often used to characterize russuloid spe-


FIG. 3. Neighbor-joining distance based phylogenetic analysis of the nuclear rDNA sequence dataset. The NJ tree places/peniophorales as a sister clade to the rest of the ingroup, /eurussuloid.

1052 MYCOLOGIA

FIG. 4. Strict-consensus tree of 12 equally parsimonious trees, resulting from parsimony analysis of the realigned datasetof /stereales. Basal nodes with bootstrap values above 50% are indicated. Stippled line indicates uncertain support.

cies. However, amyloidity is a common phenomenonamong homobasidiomycetes and not a synapomor-phy for the russuloid clade. For example, MucronellaFr., possesses amyloid spores and previously was as-sociated with Hericiales based on basidiome mor-phology but the genus lacks gloeocystidia. In agree-ment with this, phylogenetic analysis of rDNA se-quence data places Mucronella outside the russuloidclade (data not shown). The genus Peniophora Cookelacks an amyloid reaction entirely while other genera,e.g., Scytinostroma Donk and Albatrellus S.F. Gray,contain both amyloid and non-amyloid species.

Most species in the russuloid clade have basidio-spores with an ornamented surface. The nature ofthis ornamentation has been extensively studied(e.g., Capellano and Keller 1978, Keller 1986, 1997).An outer layer, tectum, forms the ornamentation,and the same layer is responsible for the amyloid re-action. The tectum can be covered by up to threeadditional layers. Species with smooth basidiosporeslack a tectum, and in TEM no difference in sporewall structure between amyloid and non-amyloidspores can be detected (Keller 1997). We invariablyhave found the presence or absence of an ornamen-tation to be a generic character within the russuloid

clade (but see /hericiaceae below). The fine struc-ture of the spore wall as observed in TEM has beenstudied in a limited number of species only and itsuse as a phylogenetically informative character can-not be evaluated.

Corner (1932a, b) introduced hyphal analysis andthe concept of hyphal systems in fungal anatomy andtaxonomy. He defined skeletal hyphae as thick-walledto subsolid, nonseptate cells that retain ability forgrowth at the thin-walled tip. They arise from gen-erative hyphae. He also coined the terms monomiticfor species with only generative hyphae, dimitic forspecies with generative and skeletal hyphae, and trim-itic for species with generative, skeletal, and bindinghyphae. Corner’s ideas gained wide acceptance andhave greatly influenced basidiomycete systematics ingeneral and generic concepts in polypores in partic-ular. For an overview of the subject, see Pegler (1996)and Hibbett and Thorn (2001).

In the russuloid clade, skeletal hyphae occur inmany species and several genera have been intro-duced for species with a dimitic hyphal system, viz.Scytinostromella Parmasto, Wrightoporia Pouzar andConfertobasidium Julich. However, among the clades,we identify only /scytinostromella as completely dim-


itic. Genera such as Scytinostromella and Wrightoporiaseem to wither when scrutinized by molecular meth-ods, and Confertobasidium has its closest relative inthe monomitic Metulodontia Parmasto. The clade/auriscalpiaceae includes clearly dimitic species suchas Gloiodon strigosum and Auriscalpium vulgare andthe monomitic Dentipratulum bialovicense. A similarpicture is found in /gloeodontia, where dimitic spe-cies such as Gloeodontia discolor cluster with the mon-omitic Gloeocystidiellum subasperisporum. We con-clude that skeletal hyphae as presently defined havebeen overestimated as a taxonomic character at thegeneric level. Our results indicate that dimitic hyphalsystems have evolved many times within the russuloidclade and support the views presented by Hibbettand Thorn (2001).

Recent studies have shown that the agaricoid gen-era Russula and Lactarius form a monophyletic cladetogether with their gasteroid and pleurotoid relatives(Miller et al 2001, Calonge and Martin 2000, Henkelet al 2000, Binder and Bresinsky 2002). We show thatthis clade is nested among corticioid taxa in what wecall /russulales. Bootstrap support for /russulales isgood (86%) but internal branching is mainly unre-solved. A notable exception is the basal node con-necting Boidinia furfuracea to the rest of the clade,where bootstrap support is 76%. Boidinia furfuraceais a wood-inhabiting fungus that forms thin, white,strictly resupinate basidiomes on decaying coniferwood. According to Nakasone (1990), it is capable ofproducing extracellular oxidases and hence causes awhite rot. There is no report of mycorrhizal activityconnected to Boidinia or Gloeopeniophorella, the sec-ond corticioid genus in /russulales. The result sug-gests that the ancestor to the agaricoid radiation inRussula and Lactarius had a corticioid basidiome andwas saprotrophic. This is in accordance with the con-clusions in Hibbett et al (2000) that evolution haswitnessed several independent shifts in nutritionalmode from saprotrophy to mycorrhizal associations.It also is consistent with an evolution from simple tocomplex fruiting bodies as put forward in Hibbettand Binder (2002).

CLADE CHARACTERISTICS AND TAXONOMY

/peniophorales (bootstrap support 95%). Our sam-pling in this clade was too restricted to allow a de-tailed phylogenetic analysis. Peniophora, Scytinostromaand Vararia P. Karst. together hold close to 150 de-scribed species but here are represented by onlyeight specimens. Within /peniophorales, only twosubclades are distinct enough to be recognized, viz./asterostromataceae and /metulodontia (FIG. 2).

There is no obvious morphological synapomorphy

for /peniophorales. The most striking differencefrom /eurussuloid is the predominance of smooth-walled basidiospores and the tendency toward non-amyloid spore-walls. In addition, species in this cladealmost invariably have basidiomes with a smooth hy-menophore, while hydnoid, poroid and lamellatebasidiomata occur frequently in most of the otherclades. Monophyly for the same group of taxa thatwe here call /peniophorales was detected already inseveral other studies (Hibbett et al 1997, 2000, Hib-bett and Donoghue 2001, Hibbett and Binder 2002).

The genera Asterostroma Massee, Dichostereum Pilat,Lachnocladium Lev., Scytinostroma and Vararia usuallyhave been referred to a separate family, Lachnocla-diaceae (Reid 1965). They are held together mor-phologically by the thick-walled, dextrinoid hyphaetermed astero-, dendro- or dichohyphidia. These hy-phidia are functionally equivalent to binding hyphaefound in many polypores. It is the dominating hyphaltype in many species, imparting them with a more orless tough consistency. Most species in Lachnocladi-aceae do not form a closed hymenium. Instead, ba-sidia are initiated deep among the hyphidia and pen-etrate to the surface just enough to freely shed theirspores. This kind of hymenium has been termed acatahymenium as opposed to the more familiar eu-hymenium with a closed palisade of basidia (Lemke1964). Basidiomes with a catahymenium are adaptedto resist periods of drought and to quickly resumesporulation when conditions become more favorable.

In our analyses Peniophora, Gloiothele and Vesiculo-myces Hagstrom are nested among the traditionalmembers of Lachnocladiaceae. No species in thesegenera have dichohyphidia or asterohyphidia, but afew species in Peniophora have dendrohyphidia. SincePeniophora is the oldest genus name, we prefer tohave that situation reflected in the clade name.

The four species of Scytinostroma in our dataset alloccur on separate branches that are distantly sepa-rated. They are morphologically quite different. Scy-tinostroma portentosum has simple-septate hyphae,amyloid subglobose spores and SA1 gloeocystidia, S.odoratum has simple-septate hyphae, non-amyloid el-lipsoid spores and SA2 gloeocystidia, S. galactinumhas nodose-septate hyphae, non-amyloid (except forthe suprahilar patch) ellipsoid spores and SA1 gloeo-cystidia, and S. jacksonii has nodose-septate hyphae,non-amyloid, ovoid spores and SA2 gloeocystidia. Inaddition, the two species representing Vararia do notcluster together and also are separated from the fourScytinostroma branches.

The taxonomic distinction between Scytinostromaand Vararia has been questioned (Boidin and Lan-quetin 1987, Boidin et al 1998, Hallenberg 1985, Stal-pers 1996). However, there has been general agree-

1054 MYCOLOGIA

ment that the two genera are closely related and thatthey together make up a natural group. Our resultsstrongly suggest that neither skeletal hyphae northeir branching patterns have any predictive powerin a phylogenetic context.

Scytinostroma was introduced for species with dex-trinoid, sparsely branched, skeletal hyphae, differingfrom the richly branched dichohyphidia characteris-tic of Vararia (Donk 1956). It is typified by Scytinos-troma portentosum, which in our analyses takes a po-sition close to Gloiothele. We estimate that less than10 species have characters corresponding to those ofthe type. However, a thorough molecular investiga-tion of Scytinostroma, Lachnocladium and Vararia isnecessary before the circumscription of these generacan be settled.

Five species of Dichostereum (40% of known speciesincluding the type D. durum) cluster together andappear to be a monophyletic group. However, in thebootstrap tree the clade collapses to a polytomy. LikeVararia, the genus has dichohyphidia but differs byglobose, coarsely ornamented and strongly amyloidspores.

The two Peniophora species sampled cluster togeth-er. This large genus with many closely related speciesis ecologically quite distinct. Species typically arefound in exposed situations on dead but still-attachedbranches. Most species in Peniophora have nodose-septate hyphae, SA1 gloeocystidia, and characteristicthick-walled incrusted cystidia (metuloids). Sporesare always smooth and non-amyloid. Basidiomata ap-pear well adapted to desiccation and have a dense,often strongly pigmented hyphal structure.

Hallenberg et al (1996) investigated the phyloge-netic relationships in Peniophora. Three speciesgroups were identified, and the genus was confirmedas uniform and well distinguished. In the MP tree,Peniophora is positioned together with Vararia inves-tiens as a sister group to Dichostereum. However, thisarrangement has no bootstrap support.

/asterostromataceae (99%). This clade includes As-terostroma, Scytinostroma portentosum (see above),Gloiothele and Vesiculomyces. The position of Gloiotheleand Vesiculomyces in /peniophorales was unexpected.Both genera are characterized by simple septate hy-phae, a monomitic hyphal system and globose tosubglobose, smooth, amyloid spores. Gloiothele lamel-losa, type species of the genus, has a variable hymen-ophore that can be odontioid, irpicoid or subporoid.Thus it is not surprising that the species appears un-der additional names as Gloeocystidiellum irpiscescensBoidin and Vesiculomyces epitheloides Boidin & Lanq.(Hjortstam 1987a). The three specimens included inour sampling represent some of the hymenophore

variation. Molecular data support the conclusion byHjortstam (1987a) that these names refer to one andthe same species.

Vesiculomyces citrinus was segregated from Gloeocys-tidiellum because gloeocystidia in basidiomata areSA2 (Hagstrom 1977). Boidin (1958) and Maekawaet al (1982) have reported that SA1 gloeocystidiacould be found in cultured mycelium of V. citrinus.However, we could not confirm this observation inour own cultures. The position of V. citrinus in thetree as a sister group to Gloiothele fits well with mor-phological characters such as simple septate hyphae,narrowly clavate basidia and smooth globose amyloidspores with a prominent apiculus. We suggest thatVesiculomyces be retained as a separate genus.

Asterostroma (type species Corticium apalum Berk& Broome 5 A. muscicola) appears monophyleticwith 71% bootstrap support. In addition, the genusis morphologically well characterized by unique as-terohyphidia. This type of hyphidium is short, has adense branching and develops from thin-walled hy-phae. Because long, skeletal-like hyphidia are lack-ing, Asterostroma has soft, fragile basidiomata andthey usually are found in moist, sheltered places. Ba-sidiospores are always globose and either smooth orornamented. However, the ornamentation does notseem to be homologous to the ornamentation seenin other russuloid species. In the latter case, orna-mentation is caused by material deposited in the out-er layer of the spore-wall, while in Asterostroma or-namentation seems to consist of lobes formed by sev-eral layers of the spore wall. Boidin et al (1997b)recognized 14 species in Asterostroma. Nine of themare very similar morphologically and separated main-ly by differences in spore size and ornamentation.Our sampling includes two of these morphotypes,and we found the sequences to be almost identical.Additional sequencing in this species complexshould be undertaken.

/metulodontia (100%). In all analyses there isstrong bootstrap support for /metulodontia as themost basal subclade in /peniophorales. Parmasto(1968) introduced Metulodontia to accommodatespecies with thick-walled incrusted cystidia, so-calledmetuloids. Eriksson and Ryvarden (1976) showedthat the type species, Metulodontia nivea, differs fromall other species originally assigned to Metulodontiaby having SA1 gloeocystidia, and they regarded Me-tulodontia as a monotypic genus of uncertain affinity.Here we show that Metulodontia, despite lacking anamyloid reaction of the spores, belong to the russu-loid clade.

Julich (1972) introduced Confertobasidium forathelioid species with brownish basal hyphae and


with C. olivaceoalbum as the type. Hjortstam (1987a)showed that the type species had been misunder-stood already by Bourdot and that two species—onewith SA1 gloeocystidia and skeletal hyphae and onelacking these characters—were mixed into the spe-cies concept. The type specimen selected by Julichhas the gloeocystidia and skeletal hyphae. For speci-mens lacking those elements, the epithet fuscostratusBurt is available, now referred to Leptosporomyces Ju-lich.

Confertobasidium olivaceoalbum and Metulodontiashare an athelioid basidiome construction, small el-lipsoid smooth basidiospores and short, narrow SA1gloeocystidia confined to the hymenium. It is a mat-ter of taste if one wishes to combine the two speciesin one genus or keep them separate. Metulodontiahas inamyloid spores, a monomitic context and twokinds of cystidia, while Confertobasidium has amyloidbasidiospores, a dimitic context and only one kind ofcystidium.

Ginns and Lefebvre (1993) recently transferredCorticium olivaceoalbum to Scytinostromella. Theystressed the presence of gloeocystidia, skeletal hy-phae and an athelioid basidiome as the main reasonsfor the transfer. In our tree, Confertobasidium oliva-ceoalbum is not placed close to Scytinostromella heter-ogenea, the generic type of Scytinostromella.

/amylostereaceae (73%). The clade includes Amylos-tereum and Artomyces pyxidatus (5 Clavicorona pyxi-data [Pers. : Fr.] Doty). No obvious morphologicalcharacteristics indicate a close relationship betweenthese taxa, and no one before has suggested such arelation. Amylostereum has leathery, more or less re-flexed basidiomata with a smooth hymenophore,while Artomyces Julich has erect, clavarioid basidiom-ata with a characteristic branching pattern. Connec-tions can be found in micromorphology. They sharea constantly clamped hyphal system, a SA1 gloeo-plerous system and smooth, amyloid spores. Amylos-tereum usually is described as lacking gloeocystidia,but Eriksson and Ryvarden (1973) noticed thin-walled gloeocystidia-like organs in A. chailletii. In cul-ture, SA1 gloeocystidia regularly occur (Boidin andLanquetin 1984a, Nakasone 1990).

In the analyses by Hibbett et al (1997) and Pine etal (1999), Clavicorona pyxidata is nested in a cladewith Auriscalpium vulgare and Lentinellus spp. Therelation to Lentinellus is supported as well in laterstudies (Hibbett et al 2000, Hibbett and Donoghue2001). Our contradictory results prompted us to re-sequence the culture used to generate our sequenceof Artomyces pyxidatus, but the outcome was identical.However, it is possible that the culture actually rep-

resents something else. The position of Amylostereumis discussed with /bondarzewiaceae below.

Clavicorona Doty is typified by C. taxophila (Thom)Doty, a small, nonbranched species, quite differentfrom the large, multibranched C. pyxidata. Julich(1981) questioned the homogeneity of the genus andreferred C. pyxidata to a separate genus, Artomyces.Recent systematic and monographic studies in Arto-myces and Clavicorona support this arrangement(Lickey 2002).

/gloeocystidiellum I (92%) and II (66%). Gloeocysti-diellum porosum is the generic type for Gloeocystidiel-lum. In our tree, it clusters with Boidinia granulataand two unidentified specimens. Gloeocystidiellum cla-vuligerum was first regarded as a synonym of G. po-rosum but reinstated as a distinct species after a closerinvestigation of morphology and culture characteris-tics (Nakasone 1982). Larsson and Hallenberg(2001) found that molecular data support G. porosumand G. clavuligerum as distinct species and that eachof them also encompasses other closely related taxa.Our analyses confirm the results of Larsson and Hal-lenberg (2001). Gloeocystidiellum clavuligerum and G.porosum do not cluster together in any of our analysesirrespective of method, sampling or characters se-lected. However, constrained trees forcing monophy-ly of G. porosum/clavuligerum were found not to besignificantly worse than the MP trees.

One mitochondrial small-subunit rDNA sequenceof Gloeocystidiellum porosum was included in the anal-yses by Hibbett and Donoghue (2001), where it oc-curred nested with Laxitextum bicolor and Dentipellisseparans (Peck) Donk. The apparent deviation fromour results might be explained by the restricted sam-pling used by Hibbett and Donoghue (2001). In theirdataset, G. porosum simply had no closer relative toassociate with. It should be noted that Dentipellis se-parans is a younger synonym of Dentipellis leptodon(Mont) Maas Geest (Ginns 1986). However, most col-lections in American herbaria named D. separans infact belong to Dentipellis dissita (Ginns 1986). This isalso the correct name for the specimen and the sub-sequent culture collected by N. Hallenberg and byhim determined as D. separans. The culture (FCUG581) was the sequence source for both D. separansused by Hibbett and Donoghue (2001) and for D.dissita used in this study!

All species in Gloeocystidiellum sensu stricto arestrictly resupinate and have a smooth hymenophore.They are monomitic, have nodose-septate hyphae,gloeocystidia that are either SA1 or SA2, ellipsoidornamented amyloid spores and a heterothallic tetra-polar mating system. Gloeocystidiellum bisporum is a

1056 MYCOLOGIA

haploid mitosporic derivative from G. clavuligerum,and its status as a distinct species can be questioned.

Our analyses imply that Gloeocystidiellum porosumand G. clavuligerum have a long history as separatetaxa, but the generally low resolution at basal nodesprevents definite conclusions about phylogenetic re-lationships and generic limits. Because morphologi-cal characteristics of the two clades overlap almostentirely, we think it would be impractical to introducea new genus for the taxa around G. clavuligerum.

/auriscalpiaceae (86%). This clade corresponds tothe family Auriscalpiaceae. At its creation, Maas Gees-teranus (1963) included the hydnoid genera Auris-calpium Gray and Gloiodon P. Karst. and the lamellateLentinellus P. Karst. Most of the species have a dimitichyphal system with clamps and gloeocystidia that givea SA1 reaction. Spores are subglobose to ellipsoid,ornamented, and with a strong amyloid reaction.

Analyses recovered two distinct subclades, with71% and 86% bootstrap support respectively. Thefirst subclade includes five species with a hydnoid hy-menophore, viz. Auriscalpium vulgare, A. villipes,Gloiodon strigosum, G. nigrescens and Dentipratulumbialoviesense. Auriscalpium vulgare is stipitate with areniform pileus. The abhymenial surface is hairy anddark brown. Auriscalpium villipes has a similar con-struction, but pilei have only a short stipe or are ses-sile and more or less broadly attached. Gloiodon spe-cies are resupinate or effused-reflexed, and Dentipra-tulum Domanski finally has a strongly reduced basi-diome, consisting of scarcely separate spinesconnected by a barely visible sterile mycelium. Theinclusion of Dentipratulum in /auriscalpiaceae sup-ports earlier results by Boidin et al (1998).

Gloiodon and Auriscalpium are very similar, as al-ready noted by several authors (e.g., Koski-Kotirantaand Niemela 1988). They are dimitic, and the gloeo-plerous hyphae are less obvious than in the othergenera in this clade. The only difference is the ef-fused-reflexed basidioma in Gloiodon as opposed tothe stipitate basidioma in Auriscalpium. It must bequestioned if Gloiodon should be maintained as anindependent genus.

The second subclade consists of the lamellate ge-nus Lentinellus and has a bootstrap support of 86%.The genus is characterized by sessile or stipitate, fla-belliform basidiomata with serrate lamellae. The pi-leus is convex to depressed and glabrous or tomen-tose-villose. Five or six species occurring in NorthernEurope, including the type species L. cochleatus, havebeen sequenced. Lentinellus ursinus and L. castoreusare almost identical and differ only by the distribu-tion of hair on the cap surface and preference forconifer versus deciduous wood. Some authors have

accepted them as separate species (Ryman and Hol-masen 1984, Watling and Gregory 1989), while oth-ers have treated them as synonyms (Miller and Stew-art 1971, Printz 1986, Stalpers 1996). In this study,the glabrous and tomentose variants were shown tohave identical nucleotide sequences. However, con-sidering their different ecology, it is still possible thatthey genetically behave as independent species.

/gloeodontia (78%). This clade includes GloeodontiaBoidin and Gloeocystidiellum subasperisporum. A rela-tionship between these taxa was shown by Boidin etal (1998) based on ITS sequence data. Nodose sep-tate hyphae, verrucose amyloid spores and SA1gloeocystidia unite the species. Gloeodontia specieshave hydnoid to irpicoid basidiomata, more or lessthick-walled to dimitic hyphae, encrusted hyphoidcystidia in the hymenium and ellipsoid to subglobosebasidiospores. Gloeocystidiellum subasperisporum has asmooth hymenophore, a monomitic hyphal system,no encrusted cystidia, and reniform basidiospores.Gloeodontia columbiensis and G. discolor are hetero-thallic unifactorial (Boidin and Lanquetin 1984b).Gloeocystidiellum subasperisporum is confirmed as het-erothallic, but factorial type is not identified. Allthree species have a normal nuclear behavior (Boidinand Lanquetin 1984b, Boidin et al 1997a).

Hjortstam and Ryvarden (1988) referred Gloeocys-tidiellum subasperisporum to Amylosporomyces S.S. Rat-tan, a genus described as lacking any kind of cystidia(Rattan 1977). We restudied type material of Amylos-poromyces echinosporus and found that it has numer-ous gloeocystidia and spores that are almost identicalto those in Gloeocystidiellum subasperisporum. Thetype collection is not in the best condition and thegloeocystidia do not react with sulfovanillin, whichmight explain why they have gone unnoticed. We re-gard Amylosporomyces echinosporus as a synonym ofGloeocystidiellum subasperisporum. In our tree, G. su-basperisporum occurs nested in Gloeodontia and wesuggest that G. subasperisporum be transferred toGloeodontia.

/aleurocystidiellum (99%). Aleurocystidiellum sub-cruentatum is a dimitic species with discoid basidiom-ata and large, minutely verrucose, amyloid spores.The skeletal hyphae terminate in the hymenium ascystidia-like, more or less encrusted elements. Gloeo-cystidia or gloeoplerous hyphae seem to be lacking.These features prompted Lemke (1964) to segregatesubcruentatum from Aleurodiscus Rabenh. ex J.Schrot., where the species had been placed by mostauthors because of the discoid basidiomata and theamyloid basidiospores. Boidin et al (1968) found thatAleurodiscus disciformis exhibited almost identical cul-ture characteristics, although basidiomata differed by


being monomitic and by possessing SA1 gloeocysti-dia. Consequently they intended to make the appro-priate combination in Aleurocystidiellum Lemke butfailed to include a reference to the basionym. Tellerıa(1990) later provided a correct combination. Hallen-berg and Parmasto (1998) found that molecular datasupported a close relationship of the two species.They also studied basidiospores in SEM and showedthat the ornamentation in Aleurocystidiellum speciesis identical and clearly different from Aleurodiscusamorphus, type of Aleurodiscus. Both Aleurocystidiel-lum species are heterothallic tetrapolar and have aheterocytic nuclear behavior (Boidin et al 1968).They also have a similar ecology; they grow on thebark of living trees. In the tree presented by Wu etal (2001) Aleurocystidiellum is interpreted as belong-ing to the ingroup but actually is a sister group tothe rest of the ingroup. This position is still compat-ible with our tree, where Aleurocystidiellum has noclear connection to other clades.

/hericiaceae (87%). This clade includes three gen-era: Hericium with large coralloid, pileate or substip-itate basidiomata supporting a strongly hydnoid hy-menophore, Dentipellis Donk with effused-reflexedbasidiomata and a hydnoid hymenophore, and Lax-itextum Lentz with effused-reflexed basidiomata anda smooth hymenophore. They are all parasitic or sap-rotrophic and associated with a white rot. Morpho-logical characters uniting the clade are the monom-itic hyphal system with clamp connections, SA2gloeocystidia and relatively small subglobose to ellip-soid, slightly thick-walled and amyloid spores. Speciesseem to have a bifactorial mating system and are ei-ther heterothallic or amphithallic, and they have anormal nuclear behavior (Boidin and Lanquetin1984b, Boidin 1990).

Hericium cirrhatum usually has been referred to aseparate genus Creolophus P. Karst. One reason is thatbasidiospores have been interpreted as smooth. How-ever, when observed in SEM the spore surface ap-pears slightly rugose (Keller 1997). We cannot judgewhether this is an artifact caused by the preparationmethod or a true ornamentation. Since Hericium cir-rhatum in our tree occurs nested among Hericiumspecies that all have ornamented spores, we find itmost logical to regard Creolophus as a superfluous ge-nus.

The specimen called Dentipellis sp. is resupinatewith a smooth hymenophore. It is another strikingexample that basidiome morphology and hymenop-hore configuration are mostly of limited value as in-dicator of relationships.

/bondarzewiaceae (78%). This clade includes spe-cies with resupinate, effused-reflexed or pileate basi-

diomata and with smooth, poroid or hydnoid hymen-ophore configuration. All species cause a severewhite rot and several species, e.g., Bondarzewia ber-keleyi, Echinodontium tinctorium and Heterobasidionannosum, can attack living trees. The hyphal systemis characterized as di- or trimitic but, according toStalpers (1979), the skeletal hyphae are merely scler-ified generative hyphae with more distant septa thanusual. Donk (1964) did not regard Bondarzewia, Echi-nodontium, Heterobasidium and Laurilia as related,and he referred them all to different families, viz.Bondarzewiaceae, Echinodontiaceae, Polyporaceaeand Stereaceae. Stalpers (1979) suggested Bondar-zewiaceae sensu Donk also should include Heterobas-idion Bref., Echinodontium and Laurilia Pouzar. Hisview was further strengthened by the discovery thatboth Bondarzewia and Heterobasidion have a system ofSA1 gloeoplerous hyphae (Gluchoff-Fiasson et al1983). A summary of opinions on family arrange-ments can be found in Redhead and Norvell (1993).In the tree presented by Hibbett et al (1997), Bon-darzewia, Echinodontium and Heterobasidion belong tothe same superclade but not close together. In sub-sequent studies (Hibbett et al 2000, Hibbett andDonoghue 2001, Binder and Hibbett 2002, Hibbettand Binder 2002), Bondarzewia and Heterobasidioncluster together but always distinctly removed fromEchinodontium. Monophyly for Heterobasidion andBondarzewia also was detected by Bruns et al (1998).

Gross (1964) found the pileate-hydnoid Echinodon-tium and the resupinate-smooth Laurilia to be con-generic. They share constant presence of clamps,thick-walled encrusted cystidia, and a brown-coloredcontext. Molecular data presented here and by oth-ers (Hibbett and Donoghue 2001, Hibbett and Bind-er 2002) support this view, and we suggest that Laur-ilia be relegated to synonymy.

Amylostereum and Echinodontium cluster togetherwith high bootstrap support in the analysis by Hibbettet al (2000), Hibbett and Donoghue (2001), andBinder and Hibbett (2002). In our analyses, Amylos-tereum always is removed from Echinodontium insteadforming a moderately supported clade with Artomycespyxidatus. We have no explanation for this discrep-ancy; the rigorous four-gene analyses performed byBinder and Hibbett (2002) presents strong argu-ments for a phylogenetic connection between Amy-lostereum and Echinodontium. Similar morphologicalarguments can be found in the numerous conical,apically encrusted cystidia present in both genera.

Echinodontium ryvardenii is a recently describedspecies only found on Juniper on Corsica (Bernicchiaand Piga 1998). Despite having a hydnoid hymen-ophore, a dimitic hyphal system, amyloid, ornament-ed spores and SA1 gloeocystidia, it is not related to

1058 MYCOLOGIA

the other Echinodontium species. Its true affinities areunclear.

/albatrellus (100%). The four species of Albatrellusform a monophyletic group that includes the type A.ovinus. All species in the genus have stipitate basi-diomata with a poroid hymenophore. They form ec-tomycorrhiza and are associated with coniferous trees(Agerer et al 1996, Ryvarden and Gilbertson 1993).

Bruns et al (1998) found that Albatrellus syringae(Parmasto) Pouzar and A. peckianus were placed out-side their Russula-containing clade. A paraphyleticorigin for Albatrellus later was confirmed by Binderand Hibbett (2002) and Hibbett and Binder (2002).

The position of /albatrellus in the russuloid line-age is unclear, but morphological similarities existwith Hericium and Lentinellus. Both Albatrellus andHericium are monomitic with nodose septate hyphaeand have SA2 gloeocystidia. Albatrellus have amyloidhyphae in the context of the basidiomata, a characterfound also in Hericium and Lentinellus. In Albatrellusthe presence of clamp connections and amyloidity ofspores seem to be inconsistent characters, as A. sub-rubescens and A. ovinus lack clamps and only A. con-fluens and A. subrubescens have amyloid spores.

/scytinostromella (71%). Scytinostromella heterogenea,type of the genus, and Wrightoporia avellanea makeup this small clade. They share a dimitic hyphal sys-tem with nodose septate generative hyphae and atleast partly dextrinoid skeletal hyphae. They alsoshare small, ellipsoid, finely ornamented basidio-spores and a gloeoplerous system. However, supportfor the clade is not impressive and with only two ter-minal taxa the result must be regarded with caution.

Scytinostromella was introduced as a genus for re-supinate species with Gloeocystidiellum-like featuresbut with a dimitic instead of monomitic hyphal sys-tem (Parmasto 1968). Only two species originallywere included, the second one being Scytinostromellanannfeldtii (erroneously named subasperisporum byParmasto). In our tree, S. nannfeldtii is placed on asingle branch with no connection to the type species;its generic position remains unclear. We have se-quenced Scytinostromella cerina, and this species alsooccurs on a separate single branch (data not shown).

/russulales (86%). This clade includes corticioidwood-decaying species, e.g., Gloeopeniophorella convol-vens, Gloeocystidiellum aculeatum and Boidinia propin-qua and the whole family Russulaceae, with the ec-tomycorrhizal genera Russula and Lactarius and re-lated gasteroid and pleurotoid forms. Species in thisclade have a monomitic hyphal system, spores areglobose to subglobose often with a distinct ornamen-tation and a strong amyloid reaction, and gloeocys-

tidia are sulfo-positive. All species except Boidinia fur-furacea have simple septate hyphae. Spores are uni-nucleate and the secondary mycelium dikaryoticwhich indicates a normal nuclear behavior. Presum-ably most species are heterothallic (Boidin et al1997a). Gloeopeniophorella Rick differs from the otherspecies in the clade by the presence of incrusted cys-tidia (metuloids).

Boidinia furfuracea is placed at the first node in/russulales as a sister group to remaining taxa andmonophyly of species with simple septate hyphae issupported by a bootstrap value of 76%. Boidinia wassegregated from Gloeocystidiellum as a monotypic ge-nus (Hjortstam and Stalpers 1982). The authorsstressed basidiome structure and spore morphologyas the main diagnostic features. Later authors havepointed to the suburniform shape of basidia as anadditional characteristic ( Julich 1982, Hjortstam andRyvarden 1988, Ginns and Freeman 1994). Severalspecies subsequently have been placed in Boidinia,and three of them are included in our tree. Boidiniagranulata belongs in /gloeocystidiellum II, and Boi-dinia macrospora clusters in /stereales. Only Boidiniapropinqua belongs to /russulales, but its relation toBoidinia furfuracea could not be resolved. As notedabove, Boidinia propinqua differs from B. furfuraceaby simple-septate hyphae. Two other species with sim-ple septate hyphae, viz. Gloeocystidiellum aculeatumand Boidinia sp., also have their place in /russulales.Our results indicate that Boidinia still should be treat-ed as a monotypic genus. However, before a moredetailed view of the clade can be worked out we willuse the concept adopted by Hjortstam and Ryvarden(1988) and further developed by Wu and Buchanan(1998) and accept also species with simple-septate hy-phae in Boidinia.

Gloeopeniophorella was introduced with one speciesG. rubroflava Rick (Rick 1934) but since its introduc-tion has been largely ignored. Recently Boidin et al(1997) restudied the type specimen and concludedthat it shares similarities with Gloeocystidiellum con-volvens and G. laxum. They also made the appropri-ate combinations. In our tree Gloeopeniophorella con-volvens, G. laxa and one specimen closely related toG. laxa form a subclade in /russulales with weakbootstrap support (66%). The reintroduction ofGloeopeniophorella is a necessary step in the rear-rangement of Gloeocystidiellum. However, its relationto the nonclamped species now placed in Boidinianeeds further study.

/stereales (97%). This clade is strongly supported bybootstrap, and the same result was reported by Wuet al (2001). Species in this clade are saprotrophscausing a white rot on various deciduous and conif-


erous trees. Many species, e.g., Stereum and Aleurod-iscus, decay dead but still attached branches and fruiton trunks or dead parts of living trees. Several specieshave adaptations for resisting periods of dry weather,e.g., a leathery consistency in Stereum or a catahy-menial organization of the basidioma in Aleurodiscus(Boidin et al 1985).

There are some striking similarities with /penio-phorales: Many species have smooth spores, manyspecies have simple septate hyphae, all species havea smooth hymenophore, and catahymenial organi-zation of the basidiomes is widespread. The restricteddataset of the clade supported six subclades, /gloeo-cystidiopsis, /xylobolus, /stereum, /chelidonium,/cerussatus and /megalocystidium (FIG. 4). It shouldbe noted that the NJ tree has a rather different to-pology within /stereales and both /gloeocystidiopsisand /chelidonium collapses.

/gloeocystidiopsis. A weakly supported clade (57%),consisting of two subclades, each with stronger sup-port. In one subclade, the generic type Gloeocystidiop-sis flammea groups with Gloeocystidiellum cryptacan-thum (99% bootstrap support). The other clade con-sists of Gloeocystidiopsis heimii and Conferticium ravum(81% bootstrap support). All species are monomiticwith simple septate hyphae. Gloeocystidia are long,tubular and always with a SA1 reaction, although itcan be weak in G. flammea (Boidin et al 1997a).Spores are ellipsoid, finely verrucose and stronglyamyloid. According to Boidin et al (1997a), all fourspecies are homothallic with binucleate spores andmultinucleate primary and secondary mycelium (hol-ocoenocytic). Clamps are absent from basidiomes,but in cultured mycelium opposite or verticillateclamps can be found.

Gloeocystidiopsis Julich was introduced as a genusfor Gloeocystidiellum-like species, with simple septatehyphae and a coenocytic nuclear behavior ( Julich1982). Two species, Gloeocystidiopsis flammea and G.heimii, originally were included. Wu (1996) movedheimii to Conferticium Hallenb. mainly because hethought that the dense hyphal structure in this spe-cies is typical for Conferticium but not present in thetype of Gloeocystidiopsis. Boidin et al (1997a) accept-ed that arrangement. Conferticium indeed is charac-terized by a dense, almost hard context and basidi-omes often are stratified. Species are monomitic withsimple septate hyphae and internal basidia repetition(Hallenberg 1980). Hallenberg included three spe-cies, viz. C. insidiosum (Bourdot & Galzin) Hallenb.(type), C. ochraceum and C. ravum (as C. karstenii).The type species and C. ochraceum are morphologi-cally indistinguishable but have different substratepreferences, growing on angiosperm and conifer

hosts respectively. In our tree, Conferticium ochraceumdoes not cluster with C. ravum but occurs on a singlebranch. We conclude that the similarities in basidi-oma structure and basidia regeneration seen amongspecies in Conferticium are of uncertain value for agenus characterization. Further arguments in sup-port of the results in the phylogenetic tree are thatConferticium insidiosum and C. ochraceum havesmooth spores, while C. ravum has ornamentedspores. Conferticium insidiosum and C. ochraceumhave similar nuclear behavior as species in /gloeo-cystidiopsis but differ by being totally devoid ofclamps in culture.

/xylobolus (73%). The type species of Xylobolus P.Karst., X. frustulatus, is externally quite characteristicwith its dark brown, strictly resupinate and stronglycracked, stratified basidiomata. In micromorphologyit has clear similarities to Stereum but differs by a neg-ative reaction in tests for phenoloxidase activity andby a white-pocket rot. Wu et al (2001) found thatXylobolus frustulatus and Acanthophysellum lividoca-eruleum cluster together with a relatively strong boot-strap support, and we can confirm their results.These two species share characters such as dark-col-ored basidiomata, densely interwoven and fused hy-phae, acanthohyphidia, narrowly clavate basidia, SA2gloeocystidia, and smooth amyloid spores. They dif-fer by the positive phenoloxidase reaction and nor-mal white rot in A. lividocaeruleum. It is interestingto note that a French specimen of A. lividocaeruleumstudied by Boidin and Des Pomeys (1961) first wasidentified as an undescribed species of Xylobolus. Lat-er Boidin et al (1968) added culture characteristicsand studied nuclear behavior, which confirmed thesimilarities with X. frustulatus.

The genus Acanthophysellum Parmasto was intro-duced for resupinate species with acanthohyphidiaand smooth non-amyloid basidiospores (Parmasto1967). Only two species originally were assigned tothe genus, viz. Corticium lividocoeruleum P. Karst.(type species) and Corticium cerussatum Bres. Thestatement about non-amyloid spores must be regard-ed as a typographical error. A year later Parmasto(1968) treated Acanthophysellum as a genus withintribe Aleurodisceae defined as having amyloid spores.

Cunningham (1963) restricted Aleurodiscus to spe-cies with more or less discoid basidiomata and adopt-ed Acanthophysium (Pilat) G. Cunn. for species witha strictly resupinate basidioma. With this circumscrip-tion the micromorphological variation within Acan-thophysium becomes almost identical to that seen inAleurodiscus sensu lato and includes a variety of sterileorgans, both smooth and ornamented spores, simple-septate and nodose-septate hyphal systems, and spe-

1060 MYCOLOGIA

cies with and without gloeocystidia. The type speciesAleurodiscus apricans Bourdot has, according to theprotologue, both smooth and finely asperulatespores. Boidin et al (1985) used SEM to study thespores in one of the original collections and foundonly smooth spores. This specimen was selected aslectotype (Galzin 4157). Nunez and Ryvarden (1997)studied another of the original collections and foundall spores to be ornamented. Boidin et al (1985) re-stricted Acanthophysium to species with smooth amy-loid spores and SA1 gloeocystidia. Wu et al (2001)regards Acanthophysium as a synonym of Xylobolusbased on similarities in nuclear behavior, the negativephenoloxidase reaction, and white-pocket rot (Boi-din et al 1968). As a consequence, some of the spe-cies placed in Acanthophysium were transferred toAcanthophysellum (see also Boidin and Gilles 2001).

The close phylogenetic and morphological con-nection between Xylobolus frustulatus and Acantho-physellum lividocaeruleum that have been demonstrat-ed implies that Acanthophysellum also should be re-garded as a synonym of Xylobolus. However, consid-ering that many species in Aleurodiscus, among themA. apricans, have yet to be studied by molecularmethods we do not want to initiate further taxonom-ical upheaval now.

/chelidonium (87%). This clade includes five mon-omitic species with nodose septate hyphae and longtubular gloeocystidia with an SA1 reaction. Thespores are ellipsoid to cylindrical, finely verrucoseand strongly amyloid. Three species, viz. Gloeocysti-diellum aspellum, G. formosanum and G. compactum,are very closely related and their sequences are al-most identical. Incompatibility between them hasbeen shown (Wu 1996), and they may be regardedas sibling species. Boidinia macrospora is closely relat-ed but can be distinguished by having longer spores.It should be noted that G. aspellum was describedfrom Africa while the culture we have used as a DNAsource originates from Taiwan. We have not com-pared the Taiwanese specimen with the type. Megal-ocystidium chelidonium is a species with similar char-acteristics, except that the spore wall is smooth, atleast as seen in a light microscope.

The relation of /chelidonium to other clades is notclear. Judging from our analyses, the group is fairlywell delimited and appears as a distinct taxon. Nogenus name is available for the group, but we thinkit is premature to introduce a new one at this stage.Similarly we find it unwise to make new combinationsjust to make all clade members belong to the samegenus.

/stereum (88%). This clade is strongly supported asmonophyletic. Species have leathery and often re-

flexed or pileate basidiomata. They have a monomi-tic hyphal system with clamps present only as whorlson certain subicular hyphae. The basidiome containsconducting hyphae that are responsible for the well-known bleeding reaction in certain species. These hy-phae, sometimes called pseudocystidia, are probablyhomologous to the gloeoplerous hyphae in the restof the russuloid lineage. The spores are cylindricalto narrowly ellipsoid, smooth and amyloid. All spe-cies tested have a holocoenocytic nuclear behavior(Boidin and Lanquetin 1984b and references there-in) and are presumably heterothallic bipolar (Boddyand Rayner 1982). Stereum is an old genus name thatearlier was used for all species with leathery, effused-reflexed basidiomata and a smooth hymenophore. Inits restricted sense it appears as a well-defined, natu-ral genus containing many closely related species.

/cerussatus (77%). Aleurodiscus cerussatus, A. dex-trinoideocerussatus and Gloeomyces graminicola clustertogether with good bootstrap support. However, thisis not surprising because the sequences are extremelysimilar, even within the hypervariable regions thatwere discarded before analyses. All three species havesmooth, thin-walled ellipsoid spores with an amyloidreaction and numerous SA1 gloeocystidia with amore or less moniliform outline. Aleurodiscus cerus-satus and A. dextrinoideocerussatus also are similarmorphologically and separated primarily by the dex-trinoid reaction of the acanthophyses in A. dextrino-ideocerussatus. Acanthophyses are sterile terminalcells with numerous protuberances. They appear inmany forms and can be found in most species inAleurodiscus but also in Stereum and Xylobolus. Gloeo-myces graminicola, type of Gloeomyces Sheng H. Wu,lacks acanthophyses and has simple septate hyphae,while the other two species have hyphae that are no-dose septate. Gloeomyces is characterized as dimitic be-cause species have terminal thick-walled andbranched cells embedded in the subhymenium. Theycould be compared to binding hyphae but are fewand do not lend any tough consistency to the basi-dioma. With these characteristics Gloeomyces looksquite different from the other two species in theclade. Our sequence of G. graminicola was generatedfrom cultured mycelium received from the culturecollection at NMNS (Taiwan). We also tried to se-quence DNA from the holotype basidioma but with-out success. Our results should be interpreted withcaution because it cannot be ruled out that the my-celium labeled as Gloeomyces graminicola representssomething else.

/megalocystidium (89%). This clade includes Megal-ocystidium leucoxanthum, M. luridum and a sequenceretrieved from a specimen determined as Gloeocysti-


diellum wakullum. A connection between M. luridumand G. wakullum also was reported in the molecularstudy by Boidin et al (1998). Megalocystidium was oneof the earliest segregates from Gloeocystidiellum ( Ju-lich 1978). It originally included the two species se-quenced here and Gloiothele lactescens. Julich selectedM. leucoxanthum as type, but he gave no explanationas to why the genus was erected and how it was sup-posed to be circumscribed. Megalocystidium leucox-anthum and M. luridum have a monomitic hyphalsystem with nodose septate hyphae, SA1 gloeocysti-dia, and smooth, amyloid basidiospores. They are ho-mothallic with a holodikaryotic nuclear behavior(Boidin et al 1997). Gloeocystidiellum wakullum wasdescribed from subtropical areas in the United States(Burdsall et al 1981) and later also reported fromGuadeloupe (Boidin et al 1997a). Our specimenoriginates from Tanzania (Hjortstam and Larsson1995). We have not compared the Tanzanian speci-men with type material, but microscopical details fitthe description. The gloeocystidia originally were re-ported as sulfo-negative. However, Boidin et al(1997a) found, after an examination of the type, thatgloeocystidia are weakly but distinctly sulfo-positiveand we have seen the same reaction in our material.Wu (1996) moved Gloeocystidiellum wakullum to Ster-eum. The evidence he cited were presence of simpleseptate hyphae, smooth amyloid spores, acanthohy-phidia and culture characteristics.

Although Gloeocystidiellum wakullum possessessome features of Megalocystidium (resupinate basi-diomata, large smooth amyloid spores, SA1 gloeo-cystidia), there are some notable differences (acan-thohyphidia, simple septate hyphae). Consideringthe results from the phylogenetic analyses, we stillsuggest that the species should be transferred to Me-galocystidium.

Species on single branches. Aleurodiscus is a large andheterogeneous group of corticioid fungi that areloosely held together by some micromorphologicalcharacters, viz. large amyloid spores, catahymenial or-ganization of basidiomata, and various kinds of sterileorgans in the hymenium. Several new genera havebeen introduced in attempts to separate out morenatural groups (e.g., Lemke 1964, Oberwinkler 1965,Boidin et al 1985). Recently Wu et al (2001) pre-sented a molecular phylogenetic study of Aleurodis-cus, but no taxonomic changes were proposed. Thetype species, A. amorphus, is placed in our tree on asingle branch as a sister taxon to the rest of /stere-ales. This is in agreement with the results presentedby Wu et al (2001). The necessary rearrangements ofspecies in Aleurodiscus sensu lato must await a moredetailed molecular study that also includes a wider

sampling of the genera that we here demonstrate areclosely related.

Aleurobotrys botryosus was segregated from Aleurod-iscus based on the amyloid reaction of the botry-ophyses in combination with SA1 gloeocystidia, or-namented spores and a white-spore print (Boidin etal 1985). The phylogenetic analysis, with the restrict-ed dataset, confirms A. botryosus as distinct fromAleurodiscus, but because both are placed on singlebranches no further conclusions about relationshipscan be drawn. Wu et al (2001) found that Aleurobotrysbotryosus belongs in the vicinity of Aleurodiscus cer-ussatus, and they concluded that the phylogeneticimportance of the amyloid reaction of the botry-ophyses was doubtful.

Species in Wrightoporia share a poroid hymenop-hore, a dimitic context and amyloidity of the sporewall. Two other genera, viz. Amylonotus Ryvarden andAmylosporus Ryvarden, have similar features. Thescopes and limits of these three genera have beendebated (David and Rajchenberg 1985, 1987, Ryvar-den 1991). Three species are included here. Wrigh-toporia lenta (type species) occurs on a single branchbasal to /albatrellus (FIG. 1). Wrightoporia avellaneais included in /scytinostromella, which might be asister clade of /albatrellus, and W. tropicalis occurson a single branch with a basal position in /penio-phorales. For this study, but not included in the finaldata matrix, we also sequenced W. bracei and W. neo-tropica. In our preliminary analyses the former alwaysoccurred on a long, single branch with unclear po-sition. The latter species consistently appeared out-side the russuloid lineage.

Gloeohypochnicium analogum earlier was placed inHypochnicium J. Erikss. because of the thick-walledspores (Eriksson and Ryvarden 1976). Gloeohypochn-icium analogum has weakly ornamented but inamy-loid spores and SA1 gloeocystidia. Basidiomes arestrictly resupinate, and the hyphal system monomiticand nodose-septate. Gloeohypochnicium analogumcauses a white rot in deciduous wood. In our parsi-mony analyses, G. analogum often appears at themost basal node of the ingroup. However, in NJ treesit occurs inside /eurussuloid close to /amylosterea-ceae.

Pseudoxenasma verrucisporum has clear affinities to/russulales and occurs as a sister taxon to that cladein all our phylogenetic trees. However, the connec-tion is not supported by bootstrap. PseudoxenasmaKH. Larss. & Hjortstam was established as a mono-typic genus because it has pleurobasidia (lateral ba-sidia), a feature not known from any other genuswith ornamented amyloid spores and sulfo-positivecystidia. In some species with a dense, more or lessgelatinized hyphal texture, generative hyphae tend to

1062 MYCOLOGIA

grow horizontally in the hymenium and produce ba-sidia laterally. Both gelatinization of the hyphae andlateral production of basidia seem to facilitate quickresponse to favorable conditions for sporulation.Pseudoxenasma grows on dead but still attachedbranches of Picea abies and often is found fertile inmild periods of winter; its globose, coarsely orna-mented, and strongly amyloid spores fit well with thegeneral spore morphology in /russulales.

Scytinostromella nannfeldtii differs in many respectsfrom the type of the genus, and the only characterconnecting S. nannfeldtii to Scytinostromella is skeletalhyphae. In other respects, viz. ornamented amyloidspores and SA1 gloeocystidia, S. nannfeldtii fits manyof the genera in the russuloid lineage.

NEW COMBINATIONS

Boidinia aculeata (Sheng H. Wu) E. Larss. & K.H. Larss.comb. nov. Basionym: Gloeocystidiellum aculeatum ShengH. Wu, Mycotaxon 58: 29, 1996.

Gloeodontia subasperispora (Litsch.) E. Larss. & K.H.Larss. comb. nov. Basionym: Corticium subasperisporumLitsch. (Ann. Mycol. 39: 125, 1941).

Gloeocystidiopsis cryptacanthus (Pat.) E. Larss. & K.H.Larss. comb. nov. Basionym: Corticium cryptacanthumPat., Bull. Soc. Mycol. France 15: 210, 1899.

Megalocystidium wakullum (Burds., Nakasone & G.W. Free-man) E. Larss. & K.H. Larss. comb. nov. Basionym: Gloeo-cystidiellum wakullum Burds., Nakasone & G.W. Freeman,Syst. Bot. 6: 431, 1981.

ACKNOWLEDGMENTS

We are grateful to Drs Jacques Boidin, Sheng-Hua Wu, LeifRyvarden and Jogeir Stokland for loan of collections; to Er-ast Parmasto, Ronald H. Petersen, Lennart Andersson, NilsHallenberg and Roger Eriksson for valuable comments onearlier versions of the manuscript; to Andy Taylor for lin-guistic improvements and to David Hibbett and one anon-ymous reviewer for constructive comments. Financial sup-port for this study was received from the Royal SwedishAcademy of Sciences, Stiftelsen Anna-Greta och Holger Cra-foords fond, Kapten Carl Stenholms donationsfond, Annaoch Gunnar Vidfelts fond for biologisk forskning andKungl. Vetenskaps- och Vitterhets-Samhallet i Goteborg.

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Phylogenetic relationships of russuloid basidiomycetes with emphasis on aphyllophoralean taxa

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