Phylogeny and Systematics of the Fungi with Special Reference to the Ascomycota and Basidiomycota

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Breitenbach M, Crameri R, Lehrer SB (eds): Fungal Allergy and Pathogenicity.
Chem Immunol. Basel, Karger, 2002, vol 81, pp 207–295
Phylogeny and Systematics of the
Fungi with Special Reference to the
Ascomycota and Basidiomycota
Hansjörg Prillingera,Ksenija Lopandica,Wolfgang Schweigkoflera,
Robert Deakb,Henk J. M. Aartsc,Robert Bauerd,Katja Sterflingera,
Günther F. Krausa,Anna Marazb
aUniversität für Bodenkultur, Arbeitsgruppe Mykologie und Bodenmikrobiologie,
Wien, Austria; bSzent Istvan University, Department of Microbiology and
Biotechnology, Budapest, Hungary; cState Institute for Quality Control of
Agricultural Products, RIKILT, Wageningen-UR, The Netherlands, and dUniversität
Tübingen, Lehrstuhl spezielle Botanik und Mykologie, Tübingen, Germany
In 1965, Zuckerkandl and Pauling [1] argued that sequence comparison of
informational macromolecules permits the evaluation of evolutionary related-
ness, thereby fomenting a phylogenetic revolution, especially in prokaryotic
organisms and protists [2, 3]. Protista were once considered as a distinct third
kingdom besides animals and plants by Haeckel [4]. Kimura’s neutral theory
of molecular evolution also had an impact on studies of the phylogeny and evo-
lution, especially of microorganisms with an inadequate fossil record [5–7].
Meanwhile, molecular systematics has revolutionized our understanding of the
microbial world. Currently, phylogenies of the Eukarya depend principally on
small [3, 8, 9–17] or large [18–24] ribosomal RNA (rRNA) subunits, although
5S rRNA [25, 26] and a number of protein sequences [27, 28] also influence
phylogenetic interpretations. Based on 18S rDNA sequencing, the Ascomycota
and Basidiomycota form monophyletic clades within the kingdom Mycobionta
or chitinous Fungi (fig. 1) [14, 29–31]. Defined by a membrane-bounded
nucleus, the kingdom Mycobionta is one of several kingdoms within the crown
groups of the Eukarya or eukaryotes (fig. 1).
Dedicated to Dr. C.P. Kurtzman on the occasion of his 60th birthday and for his valu-
able help in establishing the VIAM culture collection.

Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 208
1

The Eukarya constitute one of the three principal domains of life [32].
According to Knoll [33], the Eukarya are an ancient group, as old as the prokary-
otic Bacteria and Archea, or nearly so [2, 8]. Paleontological and biogeochemical
data suggest that Eukarya were significant organisms of ecosystems at least as
early as 1,700–1,900 million years ago [33]. Sequence analyses of protein-
encoding genes that duplicated before the divergence of the domains now suggest
that the general tree of life should be rooted between the Bacteria and Archea, with
the Eukarya bearing a specific phylogenetic relationship to the Archea [34, 35].
Within the Eukarya, the earliest diverging organisms (not shown in fig. 1)
are aerotolerant anaerobes, most of which live parasitically or symbiontically
within animal hosts (microsporidia, diplomonads, oxymonads, hypermastigids,
parabasalia and some others) [3, 8, 36]. Microsporidia contain many promis-
ing species for biological control of harmful insects. It is remarkable that
microsporidia cluster within the kingdom Fungi or Mycobionta (fig. 1) if
gene sequences encoding the largest subunit of the RNA polymerase II or the
elongation factors EF-1and EF-2 are used [37]. Doolittle [28] stresses the
importance of lateral gene transfers in prokaryotic and eukaryotic evolution.
This, however, may complicate phylogenetic interpretations. The diplomonad
Giardia infects the human intestine and can cause diarrhea, a disease known as
giardiasis, or ‘hiker’s diarrhea’. These organisms have a well-defined nucleus
and flagellum apparatus, but no mitochondria or chloroplasts and are included
in the kingdom Archezoa [38]. Representatives of the Archezoa have relatively
simple cytoskeletons and exhibit a number of ultrastructural (e.g. extranuclear
pleuromitosis) [39–41] and biochemical characters more similar to those of
prokaryotes than to other eukaryotes [38].
Protists occupying the middle branches of the phylogenetic tree [33] of the
Eukarya commonly contain mitochondria, but no chloroplasts. Euglenids are the
exception; about one third of them are photosynthetic. Euglenid chloroplasts
may be derived from symbiotic green algae [13], implying a relative late acqui-
sition of photosynthesis within this group. The amoebaflagellate Naegleria
(fig. 1) is considered to be one of the earliest diverging protists with mitochon-
dria. Nuclear rRNA phylogenies support this view. Heterolobosea emerge at
Systematics of the Ascomycota and Basidiomycota 209
Fig. 1. Phylogenetic tree of eukaryotic organisms based on the primary structure of the
18S rRNA gene. Complete sequences of the 18S rRNA gene were aligned by means of the
CLUSTALX program [44]. Software package PHYLIP [45] was used for phylogenetic infer-
ences. Distance matrix was constructed in the DNADIST program (Kimura 2 parameter
model) and the FITCH program was used for calculating phylogeny. The phylogenetic tree
was displayed in TREEVIEW [46]. Branch lengths are proportional to nucleotide differences
and the numbers given on branches represent the percentage of frequencies with which a
given branch appeared in 100 bootstrap replications. The sequences were retrieved from the
nucleotide sequence libraries (EMBL, GenBank and DDBJ).

the base of mitochondria-bearing eukaryotes, together with trypanosomids and
euglenoids. All three taxa feature extraordinarily long branch lengths [3] (fig. 1).
Although predominantly aerobic, organisms in this part of the phylogenetic tree
commonly thrive under relatively oxygen-poor conditions [42].
Most eukaryotic diversity is nested within the densely branched crown of the
phylogenetic tree (fig. 1) [3, 13, 33, 43]. Major clades that branch near a common
point include the kingdoms (fig. 1) Zoobionta or Animalia (Metazoa unicellu-
lar relatives), Chlorobionta (green algae and terrestrial plants), Mycobionta (chiti-
nous or true fungi), Heterokontobionta (Stramenopila or chromophyta: golden
brown algae, diatoms, brown algae, oomycetes, slimenets), Rhodobionta (red
algae) and Alveolobionta (Alveolates: ciliates, dinoflagellates, apicomplexans; not
shown in fig. 1) [3]. Because of rapid diversification, branching order within the
crown group of Eukarya remains uncertain.
Mitochondria and chloroplast genomes have molecular sequences that ally
them to the Bacteria (proteobacteria and cyanobacteria) [47, 48]. The sequence
data are congruent with ultrastructural and biochemical evidence supporting the
endocytobiotic theory for the origins of these organelles [49, 50]. Molecular data
are in agreement with a multiple origin of plastids, with some plastids originat-
ing from prokaryotic (simple plastids: chloroplasts, cyanelles, rhodoplasts) and
others from eukaryotic (complex plastids: cryptophytes, haptophytes, heterokon-
tophytes, euglenophytes, chlorarachniophytes, dinoflagellates) algae [13, 43].
The Kingdom Mycobionta (Eumycota) or True Fungi
Among earlier phylogenetic speculations extensively discussed in Jahrmann
and Prillinger [51] and Barr [52], the concept of Cavalier-Smith [53, 54] and
Prillinger [41, 51, 55] is noteworthy. Based on a framework of data on cell wall
chemistry, biosynthetic pathway of lysine, storage carbohydrates, ultrastructure of
mitochondrial cristae, type of motile cells and ploidy of vegetative hyphae,
Cavalier-Smith and Prillinger only considered the chytridiomycetes,
zygomycetes, ascomycetes and basidiomycetes as true or chitinous fungi and
included them in the kingdom fungi or Eumycota. These four fungal groups are
characterized by chitinous cell walls [56, 57], the -aminoadipic acid lysine
biosynthetic pathway [58, 59], glycogen as storage carbohydrate [54], nondiscoid
plate-like mitochondrial cristae [54], the absence of heterocont flagella, and the
absence of diploid vegetative hyphal compartments in the higher Ascomycota and
Basidiomycota (exceptions: forced heterokaryons: e.g. Aspergillus, Penicillium;
solopathogenicity in the smuts: Ustilago; Hymenomycetes: Armillaria [41, 60];
see Oomycota [61]). The primarily heterotrophic origin of this group is exten-
sively discussed by Jahrmann and Prillinger [51]. Within the Eumycota the
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 210

chytridiomycetes are considered basal, the Entomophthorales (zygomycetes)
evolved from a chytridiomycete by loss of the flagella [54]. Based on a single pos-
terior flagellum (opisthokont), flattened, nondiscoid mitochondrial cristae, a chiti-
nous exoskeleton, storage of glycogen instead of starch, lack of chloroplasts, and
the code UGA for tryptophan, not chain termination, in their mitochondria,
Cavalier-Smith [54] suggests a common origin of the true fungi with animalia and
choanoflagellate protozoa (fig. 1).
The oomycetes, hyphochytrids, labyrinthuloids, and thraustochytrids are
included in the kingdom Heterokontobionta or pseudofungi [54] based on the
presence of cellulose in their cell walls, a tubular mitochondrial crista, hetero-
kont flagella, one decorated with tripartite hairs, and the , -diaminopimelic
acid lysine biosynthetic pathway. The slime molds were classified into the king-
dom Protozoa [38].
Evidence from complete 18S rDNA sequence divergence (fig. 1) [29, 62] put
an end to the discussion on the kingdom Eumycota or true fungi and
corroborated the existence of four naturally related phyla or divisions: the
Chytridiomycota, the Zygomycota, the Ascomycota and the Basidiomycota within
the kingdom Fungi or Mycobionta (fig. 1) [63, 64] or Eumycota [41, 52]. Specific
acyclic polyols [65], an exclusively absorptive or lysotroph nutrition [66] and a dis-
tinct ultrastructure of the flagellar apparatus of the Chytridiomycota [52] are addi-
tional characteristics which support the kingdom Mycobionta.
Based on the complete sequence of the 18S rRNA gene and the amino
acid sequence of the elongation factor, the Animalia or Zoobionta appeared as
a sister group of the Mycobionta or true fungi (fig. 1) [3, 67–72]. Nikoh et al.
[73] come to a similar conclusion from a phylogenetic analysis of 23 different
proteins. A closer phylogenetic relationship of Zoobionta and Chlorobionta,
however, becomes apparent from homologous comparisons of ribosomal pro-
teins [74]. The protozoal Choanoflagellida are phylogenetically closely related
to the Zoobionta and Mycobionta (fig. 1) [52].
Prototheca is a ubiquitous achlorophyllous green alga (fig. 1) that lives on
decaying organic matter and exhibits a yeast-like growth pattern. Human infec-
tion usually involves the skin and underlying tissues. P. wickerhamii (fig. 1) is
recovered most often from human specimens, while P. zopfii usually is associ-
ated with infections in animals [75].
In the phylogenetic trees of Bruns et al. [29] and Sugiyama [14], the
phagotrophic plasmodial slime molds (Myxomycota) and cellular slime molds
(Dictyosteliomycota) diverged prior to the terminal radiation of eukaryotes
(fig. 1). Presently no data are available on the cellular Acrasiomycota. In con-
trast, parsimony analysis of amino acid sequences of EF-1, a protein involved
in the translation of messenger RNA, strongly supports a monophyletic origin
of the Dictyosteliomycota and Myxomycota and the amoeboflagellate protostelid
Systematics of the Ascomycota and Basidiomycota 211

Planoprotostelium (kingdom Mycetozoa). Among the multicellular eukary-
otes, the Mycetozoa appear closer to Animalia and true fungi than to green
plants [27]. The use of EF-1emphasizes the importance of developing multi-
ple sequence data sets. As a conclusion, the phylogeny of the Acrasiomycota,
Dictyosteliomycota and Myxomycota remains uncertain at the moment, and
additional sequence data are urgently needed. Based on 18S ribosomal DNA
sequencing, the plant parasitic slime mold Plasmodiophora brassicae
(Plasmodiophoromycota), a severe pathogen of crucifers, may be more closely
related to the Alveolobionta than to any of the fungi [76].
The Oomycota (fig. 1, Achlya, Lagenidium, Leptolegnia, Phytophthora,
Pythium, Saprolegnia), Hyphochytridiomycota (fig. 1, Hyphochytrium) and net
slime molds or Labyrinthulomycota (fig. 1, Labyrinthula, Thraustochytrium,
Ulkenia) form a clade with brown algae (Phaeophyceae), diatoms (Bacillario-
phyceae), Chrysophyceae, Xanthophyceae, and Chloromonadophyceae. These
organisms have heterokont flagella, one decorated with tripartite hairs;
autotrophic species contain chlorophylls a and c, and are classified within the
kingdom Chromista [38], Heterokontobionta [64] or Stramenopila [63]. The
Oomycota lack acylic polyols [65] and differ in sterol biosynthesis from the
true fungi [77]. Based on the biosynthesis of sterols, Berg and Patterson [77]
suggest a heterotrophic origin of the Oomycota. The labyrinthuloids appear to
be basal to other heterokont algae, Oomycota and Hyphochytridiomycota
within the Heterokontobionta (fig. 1) [78, 79].
The division Oomycota mainly consists of two orders. The order
Saprolegniales comprises aquatic species, some of which are pathogenic to fish.
Representatives of the order Peronosporales mostly occur in soil or as parasites of
plants [63]. The latter order comprises one species of clinical significance,
Pythium insidiosum [80]. Two members of the order Peronosporales, Phytophthora
infestans and Plasmopara viticola, have been implicated as allergenic fungi [81].
Morphological Differentiation within the Kingdom Mycobionta
Figure 2 shows a phylogenetic and ontogenetic scheme accounting for the
range of morphological organization in the kingdom Mycobionta. Figure 2 is
based on a scheme proposed by Pascher [82] for algae, but, unlike the latter,
envisages evolution from polykaryotic, via oligokaryotic to mono- and dikary-
otic systems [41]. Different types of morphological organization are extensively
discussed in Jahrmann and Prillinger [51] and Prillinger [41, 83]. The basal
position of the flagellate and rhizopodial types was further corroborated by a
compilation of ultrastructural data [41] and sequencing of the ribosomal RNA
genes [3, 84]. In figure 2 we used the term flagellate instead of monadal
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 212

because the first Eucarya was most probably already a chimera of two prokary-
otic organisms [49]. Presently, it is not clear whether the Amoebidiales with
free-living rhizopodial or amoeboid stages belong to the Zygomycota. The
yeast form, denoted by the term ‘coccal’ (i.e. a unicellular organism having a
rigid cell wall outside its plasma membrane), occupies a basal position among
the Zygomycota, Ascomycota, and Basidiomycota [Oberwinkler, pers. obs.],
but seems to be derived in the Chytridiomycota (e.g. Basidiobolus) [83, 85, 86].
Systematics of the Ascomycota and Basidiomycota 213
Pseudoparenchyma
Plectenchyma
Evolution of vegetative anastomosis
Trichal
Forcibly discharged
secondary spore
Siphonal
Colonies
Colonies
Polyphyletic evolution
Colonies
Ontogeny
Rhizopodial
Phylogeny
Flagellate
Aquatic
habitat
Coccal
Pseudotrichal
Terrestrial
habitat
Hyphal aggregates
Hyphal aggregates
Fig. 2. Evolutionary scheme for morphological differentiation within the kingdom
Mycobionta. Modified from Prillinger [83].

Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 214
3

A yeast/hypha dimorphism is common in all classes of the Ascomycota (fig. 3:
Hemiascomycetes, Protomycetes, and Euascomycetes) and Basidiomycota (fig.
4: Urediniomycetes, Ustilaginomycetes, Hymenomycetes), especially in primi-
tive representatives. It seems to be fundamental for a rapid evolution of the
fungi. Similarly, the pseudotrichal pattern is common in many dimorphic
Zygomycota, Ascomycota, and Basidiomycota and often reverts to the unicel-
lular condition [51, 83]. The polykaryotic siphonal (coenocytic) type is charac-
teristic for many eukarpic Chytridiomycota and the aflagellate Zygomycota.
The forcibly discharged secondary spore (ballistospore in the Basidiomycota)
is a specific adaptation of unicellular morphological differentiation to terres-
trial life [87]. Its polyphyletic origin in the Entomophthorales and its early exis-
tance in the Basidiomycota is discussed by Tucker [88] and Prillinger [83].
Forcibly discharged secondary spores stimulate a faster spreading on new solid
habitats and may help to escape or establish parasitic interactions. Septate
hyphae, or the trichal type of morphological organization, are well known in
advanced groups of the Zygomycota (Dimargaritales, Kickxellales) and fila-
mentous Ascomycota and Basidiomycota, the hyphal compartments may be
poly-, oligo- and monokaryotic in the Ascomycota or commonly dikaryotic in
the Basidiomycota [41]. The plectenchyma with vegetative anastomoses are
characteristic for the fruiting bodies of the higher Ascomycota (except dikary-
otic ascogenous hyphae) and Basidiomycota. Pseudoparenchyma, with approx-
imately isodiametric cells and synchronous cell and nuclear divisions, differ
from true parenchyma of plants by the absence of a phragmoplast and a meris-
tematic tissue. They are common in the Laboulbeniales and some other meris-
tematic Euascomycetes [89], aecidia of rust fungi, and fruiting structures of
diverse Ascomycota and Basidiomycota.
Sexual Differentiation within the Kingdom Mycobionta
Two markedly different concepts of sexuality in Mycobionta have arisen,
depending on the primary event(s) or mechanism believed to be involved.
According to the view favored here, the primary event is ‘sexual differentiation’
[41, 55, 83]; this being the process which leads to karyogamy and meiosis either
within the same strain (homothallism) or after the crossing of two different mating
Systematics of the Ascomycota and Basidiomycota 215
Fig. 3. Phylogenetic tree of Ascomycota based on the primary structure of the 18S rRNA
gene. Alignment, distance matrix and calculation of phylogenetic distances were made by means
of different programs as described in the legend of figure 1. Carbohydrate cell wall composition
[129] is assigned as follows: 䊉Glucose-mannose; 䉱glucose-mannose-galactose; 䊏glu-
cose, mannose, galactose, rhamnose. Human pathogenic genera are indicated by arrows.
TTeleomorphic species; A anamorphic species; Y yeasts or yeast stages.

Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 216
4

types (heterothallism). According to the other view, the primary mechanism is the
polarity resulting from sexual incompatibility [90], a phenomenon which sup-
presses karyogamy and meiosis in monoecious organisms. Fundamental differ-
ences between both concepts are extensively discussed in Prillinger [83].
To explain the evolution of sexuality via sexual differentiation in the
Mycobionta, two distinct steps seem to be worth discussing.
A. A polyphyletic evolution from mitotic to meiotic life cycles within
a polykaryotic and coenocytic homothallic organism (primary or primitive
homothallism [41, 83] (fig. 5).
B. A polyphyletic origin of heterothallism in different groups of fungi
[55, 83]. Mycoparasitic interactions which evolve to sexual symbiosis and a lat-
eral gene transfer are considered to be of fundamental importance for the evo-
lution of heterothallism [28, 83]. Burgeff [91, 92] was the first to detect a close
relationship between fungal sexuality and parasitism. In contrast to Prillinger
[83], however, he considered parasitism as a degenerated form of sexuality. A
polyphyletic evolution from heterothallism back to homothallism (secondary or
derived homothallism) appears to be very common in fungi [41, 55, 83, 93, 94]
(fig. 5). Yun et al. [95] analyzed mating type gene organization, together with a
phylogeny from ITS/glyceraldehyde-3-phosphate dehydrogenase gene sequences
to show that homothallism in Cochliobolus (C. luttrellii, C. cymbopogonis,
C. kusanoi, C. homomorphus; fig. 5) arose independently from heterothallic
ancestors. In the Basidiomycota there is in addition some evidence that unifac-
torial (bipolar) heterothallism as a mating system evolved polyphyletically [90]:
(1) primarily via mycoparasitic interactions, as suggested for the Ascomycota
(fig. 5) [55, 83]; (2) secondarily from bifactorial (tetrapolar) heterothallism
by close linkage of A and B loci, as demonstrated in Ustilago hordei [96]; (3)
secondarily from bifactorial mating systems by ‘self-compatible’ mutations in
either the A or B factors (or homothallism if both the A and B factors are
affected), as has been demonstrated in Coprinus [97].
During recent years, a lot of new information has accumulated in favor of
the concept of sexual differentiation:
(1) Hijri et al. [98], Hosny et al. [99] and Sanders [100] demonstrated that
polykaryotic, coenocytic and highly heterokaryotic homothallic strains without
recombination, a prerequiste for the evolution of sexuality according to the
Systematics of the Ascomycota and Basidiomycota 217
Fig. 4. Phylogenetic tree of Basidiomycota based on the primary structure of the
18S rRNA gene. Alignment, distance matrix and calculation of phylogenetic distances were
made by means of different programs as described in the legend of figure 1. Human patho-
genic genera are indicated by arrows. T Teleomorphic species; A anamorphic species;
Yyeasts or yeast stages.

concept of sexual differentiation, indeed exist in the Mycobionta within the
arbuscular mycorrhiza forming order Glomales of the Zygomycota. The authors
detected nuclei in the polykaryotic spores (Scutellospora castanea: approxi-
mately 800 nuclei/spore) which were genetically different at the genus level.
Since vegetative anastomoses occur in the Glomales [101], it is not clear
whether the homothallism of S. castanea is primitive (primary homothallism;
fig. 5) or derived (secondary homothallism) [41, 55, 83, 94]. The Glomales are
truly ancient, having remained largely morphologically unchanged since plants
first colonized the land around 400 million years ago [102]. No sexual stage has
been observed in the Glomales life cycle.
(2) Four yeast strains were isolated from different species of higher
Basidiomycota (Polyporus, Marasmiellus, Ganoderma). In Polyporus, the yeast
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 218
Heterothallism
Complex hetero-bifactorial (according to Kües, pers.com.)
A : IC, two subunits, multiple highly divergent alleles
B : IC? two subunits, multiple highly divergent alleles
Schizophyllum commun, Coprinus cinereus
Simple hetero-bifactorial
A : EC, two idiomorphs (SP)
B : IC, multiple alleles (RP)
Ustilago maydis
Unifactorial
IC, Two idiomorphs (RP)
Neurospora crassa, Podospora pauciseta
Saccharomyces cerevisiae
EC, Two idiomorphs?
Sexual symbionts
Asterophora  yeasts (Asterotremella)
Nonhaustorial parasites
Carcinomyces
Parasitella, Chaetocladium
Haustorial parasites
Tremella, Christiansenia
Syncephalis, Piptocephalis
Primary homothallism
Benjaminiella multispora
Secondary homothallism
Schizosaccharomyces pombe
Saccharomyces cerevisiae
Gelasinospora reticulospora
Anixiella sublineata
Neurospora terricola
Neurospora dodgei
Neurospora tetraspora
Podospora pauciseta
Cochliobolus luttrellii
Agaricus bisporus
Coprinus bilanatus
Haasiella venustissima
Mycena galericulata
Polyphyletic evolution
Polyphyletic evolution
Fig. 5. Hypothetical scheme for the evolution of heterothallism and secondary
homothallism in Mycobionta. For synchronous nuclear division in Benjaminiella multispora,
Cokeromyces and Mucor species with respect to primary homothallism, compare Forst and
Prillinger [159]. For molecular details, see Hiscock and Kües [90 and the literature cited
therein]. For secondary homothallsim, see Glass et al. [160] and Yun et al. [95].
IC Intracellular function; EC extracellular function; SP structural proteins which are
involved in pheromone binding; RP regulatory proteins which are involved in n-DNA
binding and regulation of transcription.

appeared on a cross of isogenized ramarioid inbreeding strains, which had lost
their ability to produce fertile hymenia (fig. 6 a, b) [83, 103, 104]. The yeast
isolate from Marasmiellus originates from aseptically grown cultures of young
fruiting body trama [104]. In Ganoderma two yeast strains were isolated dur-
ing germination experiments from basidiospores harvested in nature. A sper-
matia–trichogyne-like recognition reaction (fig. 6 c, d) and a specific homing
reaction (fig. 6 e) [104–106] as well as undistinguishable diglobular interphase
spindle pole bodies of nuclei (fig. 6 f, g) and closely similar mol% GC values
suggested conspecificity between the yeasts and the corresponding mycelial
fungi. Using genotypic identification methods, we were able to identify all the
yeast isolates. All yeast strains belong to Ustilago maydis [106]. Our results
were corroborated by breeding experiments with plant pathogenic haploid
mating type strains [106]. From our data we conclude that the spermatia-
trichogyne fertilization reaction can be traced back to mycoparasitic interac-
tions and has evolved polyphyletically in the Ascomycota and rust fungi (fig. 7
[107]). This is in agreement with a phylogenetic tree of complete sequences of
the 18S rRNA gene, where the Uredinales appear as a derived clade which can
be traced back to a dimorphic Mixia-like phylogenetic ancestor without mor-
phologically developed sexual organs within the Urediniomycetes (fig. 4).
(3) In auxotrophic mutants of Absidia glauca, a specific gene transfer
from the parasite Parasitella parasitica to the host A. glauca was detected by
Kellner et al. [108] and Wöstemeyer et al. [109].
(4) Prillinger [55] considered at least four different gene types to be
involved in sexual differentiation (mating-type genes, homothallism genes,
incompatibility genes and sterility genes). A more recent molecular character-
ization of mating-type genes based on DNA sequence comparisons [90 and liter-
ature cited therein] corroborates the interpretation of Prillinger [55] that
mating-type genes biochemically differ in function from the incompatibility
genes [110–120]. In addition, a similarity of the MAT-1 gene of Cochliobolus het-
erostrophus with Neurospora crassa mt A-1 protein, the Podospora pauciseta
(anserina) mat  protein and the known DNA-binding region of Saccharomyces
cerevisiae MAT 1 protein was detected. On the other hand, the MAT-2 gene
of C. heterostrophus exhibits similarities to the N. crassa mt a-1 protein, the
P. pauciseta mat protein and the known DNA-binding protein of
Schizosaccharomyces pombe mat-Mc [121–123]. In Saccharomyces cerevisiae
the cell-type-specific gene regulation in a and -cells clearly corroborates our
concept of sexual differentiation [90 and literature cited therein]. There is no
evidence for an incompatibility function of the mating type loci in S. cerevisiae.
An evolution from extracellular to intracellular functions of mating type genes
as was postulated by Prillinger [55] was detected by Bölker et al. [124] and
Kämper et al. [125] in Ustilago maydis. Molecular data on mating type genes of
Systematics of the Ascomycota and Basidiomycota 219

Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 220
a
c
f g
de
b
0.1m 0.1m
Fig. 6. Ustilago maydis isolated from Polyporus ciliatus (a–e) and Ganoderma adsper-
sum (f, g). aIsogenised ramarioid inbreeding strains with nonsporulating fruiting bodies;
bottom: haploid parents, top: dikaryotic cross. See Prillinger and Six [103]. bA yeast colony

Saccharomyces cerevisiae, Candida albicans, Schizosaccharomyces pombe,
Neurospora crassa, Ustilago maydis, Coprinus cinereus and Schizophyllum com-
mune [90, 125–128] point to a polyphyletic evolution of heterothallism in differ-
ent groups of fungi, as suggested by Prillinger [55, 83, 94]. The complexity of
mating type genes and their respective number of base pairs nicely correlate with
an evolution from the Hemiascomycetes to the Protomycetes and from the
Protomycetes on the one hand to the Euascomycetes (fig. 3) and the other hand
to the Urediniomycetes, Ustilaginomycetes and Hymenomycetes (fig. 4).
(5) Similarly to a polyphyletic evolution of heterothallism, a polyphyletic
loss of meiosis becomes obvious in several genera of the Eurotiales, Hypocreales
and Onygenales. Using rDNA sequencing, meiotic and strictly mitotic taxa were
often recovered clustered together, indicating that multiple independent losses
of teleomorphs had occurred: Aspergillus and related teleomorphs [130–132],
Penicillium, Geosmithia and their related Talaromyces and Eupenicillium
teleomorphs [133, 134], Blastomyces, Histoplasma, Coccidioides, Emmonsia,
Trichophyton, Oidiodendron species pathogenic in humans and related
Ajellomyces and Myxotrichum teleomorphs [135–137], Fusarium and related
Gibberella and Nectria teleomorphs [138–140], Gliocladium, Trichoderma and
their Nectria and Hypocrea teleomorphs [141, 142], Acremonium and the phylo-
genetically different teleomorphs [143], Uredinales [144], and asco- [23] and
basidiomycetous yeasts [24].
The molecular phylogenies do not support the existence of the
Deuteromycetes or Deuteromycota as a distinct higher taxon within the Myco-
bionta. Molecular characters offer the potential for combining the dual classifi-
cation into one natural classification [145]. Anamorphic genus and species
names of the Deuteromycetes, however, may also be necessary in the future for
purposes of identification. As shown in figures 3 and 4, mitotic genera could
be placed into meiotic orders and families [145].
Systematics of the Ascomycota and Basidiomycota 221
(arrow) which appeared in the mycelium of the sterile dikaryotic cross. c, d Trichogyne-like
approach of a hypha (large arrow) from the Polyporus mycelial culture towards the yeast
cells (small arrow) produced on the pseudomycelium by the Ustilago maydis strain. Open
star site of inoculum of Polyporus ciliatus; closed star site of the Ustilago maydis inocu-
lum; triangle empty hyphae of the pseudomycelium. eRecognition reaction between
pseudohyphae from U. maydis (coming from the left) and true hyphae from P. ciliatus (com-
ing from the right), hyphal annealing (small arrow), possible vegetative anastomosis? (large
arrow). For hyphal enveloping and lethal reaction, see Prillinger [104]. f, g Spindle pole body
of the nucleus in the hypha of G. adspersum and yeast of U. maydis; the nuclear envelope is
arrowed. From Prillinger, H.: Yeasts and anastomoses: Their occurrence and implications for
the phylogeny of Eumycota, figure 24.5; in Rayner et al. (eds): Evolutionary Biology of the
Fungi. London, Cambridge University Press, 1987. With permission from Cambridge
University Press.

Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 222
f
e
d
c
b
a
t
ascog
ab
Sexual symbionts
c
1
ssp
sp
t
t
a
a




1
3
3
2
Trichal ap
h
Siphonal
Haustorial parasites
Non-haustorial parasites
E v o l u t i o n
2
Piptocephalis Dispira Parasitella Phycomyces Chaetocladium Penicillium Podospora
AscomycotaZygomycota
7

A problem concerning DNA as the type specimen has been considered by
Reynolds and Taylor [146] and Haines and Cooper [147]. Prillinger et al. [148]
found that phenotypically identified strains of Sporothrix schenckii may be
heterogeneous and stressed the importance of culture collections in modern
genotypic identification.
(6) Different yeasts were isolated when culturing the pileitrama of young
fruit bodies of the two agarics Asterophora lycoperdoides and A. parasitica.
Both agarics occur as mycoparasites on Russula nigricans in nature. In A.
lycoperdoides, yeasts also appeared endophytically during the germination of
chlamydospores [51, 54, 104]. In subcultures of the original yeast isolates
from both Asterophora species, agaricoid fruit bodies developed after 4–6
weeks in artificial culture [51, 94, and Prillinger unpubl. obs.]. All attempts to
repeat these experiments from single yeast cells or different crossing experi-
ments, however, failed to produce fruit bodies, although some structures which
resemble holobasidia were observed [104]. These data suggest that the yeast
isolates from pileitrama were contaminated with Asterophora chlamydospores
and exclude parasitic interactions. Physiological patterns and the qualitative
and quantitative yeast cell wall carbohydrate spectrum of the yeast isolates
from the two Asterophora species closely resemble some mycoparasitic
Tremella species (e.g. T. encephala) [104, 149]. Using a positive selection vec-
tor to clone fungal nuclear DNA in Escherichia coli together with random
fragment hybridization analysis, the conspecificity of the Asterophora yeasts
and hyphae was excluded [150]. Based on mt-DNA RLFP [83] and
nDNA/nDNA hybridization as well as ribosomal DNA restriction fragment
analysis [455] the yeast isolates from A. lycoperdoides and A. parasitica can
be considered as distinct species. Based on complete sequences of the 18S
rDNA (fig. 4) and partial sequences of the 26S rDNA [24], the genus
Cryptococcus appeared heterogeneous with respect to the type species C. neo-
formans (fig. 4). We therefore have included C. humicola and the two
genotypically distinct yeast isolates from the agarics A. lycoperdoides and
Systematics of the Ascomycota and Basidiomycota 223
Fig. 7. Evolution of heterothallism in the kingdom Mycobionta. aHaustorial parasites
(after Jeffries and Young [153]); ap appressorium; h haustorium; arrow shows cell wall
of fungal host. b, c Nonhaustorial parasites (after Burgeff [91, 92]); hatched nuclei and
cytoplasm of the host; stippled nuclei and cytoplasm of the parasite; hatched and stippled
heterokaryosis; the arrow indicates septum formation in the parasite. dEarly successive
stages in the gametangiogamy of Phycomyces nitens (Orban [154], Burgeff [92]). eSuccessive
stages of gametangiogamy (arrows) in Talaromyces (Penicillium) stipitatus (after Emmons
[155]); note the budding asci (a). fSpermatia-trichogyne fertilization in Podospora fimbriata
(after Zickler [156, 157]: P. fimbriata (Bombardia lunata) after Mirza and Cain [158]); s 
spermatia; insert shows a spermatogonium (sp) fusing with a trichogyne (t).

A. parasitica in the new genus Asterotremella as As. humicola, As. lycoper-
doides and As. parasitica [Prillinger et al., in preparation]. We interpret As.
lycoperdoides and As. parasitica together with the agarics from which they
were isolated as sexual symbionts and missing links in the polyphyletic evolu-
tion from mycoparasitism to heterothallism (fig. 5, 7). Haustorial mycopara-
sites are common in the closely related genus Tremella.
As a conclusion, the trinity system Russula, Asterophora, and Asterotremella
is remarkable, and may be fundamental in the evolution of sexuality, especially
primary homothallism and subsequently heterothallism in fungi.
(7) Based on 18S ribosomal DNA sequencing, we have traced back the uni-
nucleate ascomycetous yeasts (Kluyveromyces, Saccharomyces) to a polykaryotic
(Eremothecium) ancestor [152].
Our arguments in favor of a sexual differentiation corroborate the idea that
genetic engineering was not discovered by molecular biologists of the 20th cen-
tury: it is common in nature and fundamental in the evolution of heterothallism
in the Mycobionta.
Phylogenetic Relationships among the Chytridiomycota and
Zygomycota
In the view of many mycologists, it is believed that the Chytridiomycota
are the most primitive fungi within the Mycobionta, because they are zoosporic
(fig. 2), and sexual reproduction has been reported to be accomplished by a
variety of different methods (isogamy, anisogamy, oogamy, gametangiogamy,
and somatogamy [63]. This view has been corroborated recently by the detec-
tion of the new order Neocallimasticales [161] which consists of species of
obligately anaerobic chytrids that inhabit the rumen of herbivorous animals.
While some species have typical uniflagellate zoospores, others are exceptional
within the chytrids because they are polyflagellate with more than 10 flagella
observed. In contrast to the other orders of the Chytridiomycota, the zoospores
of the Neocallimasticales lack the microbody-lipid globule complex and mito-
chondria [63, 162]. The order appears to be monophyletic based on preliminary
results from cladistic analysis of structural and molecular characters [161, 163,
164] and is, furthermore, ecologically distinct.
Our phylogenetic analysis of the Chytridiomycota and Zygomy cota
(fig. 1) corroborates the view of Nagahama et al. [86], Sugiyama [14], Tanabe
et al. [165] that both phyla are not monophyletic and instead suggest that
losses of flagella occurred in several lineages during the course of fungal
evolution. The Blastocladiales (Allomyces, Blastocladiella) form a clade dis-
tinct from the Monoblepharidales (Monoblepharis, Monoblepharella),
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 224

Spizellomycetales (Spizellomyces), Neocallimasticales (Neocallimastix) and
Chytridiales (Chytridium) [165]. Basidiobolus ranarum an aflagellate ento-
mophthoralean fungus, which has a yeast stage [85] must be included in the
Chytridiomycota (fig. 1) [86]. As McKerracher and Heath [166] already men-
tioned based on ultrastructural data, the morphology of the nucleus-associated
organelle of Basidiobolus is unusual since no other nonflagellated organism
contains microtubules as structural components of their nucleus-associated
organelle.
Within the Zygomycota three different clades appear. Mucor racemosus
(Mucorales: M. mucedo,Mycotypha microspora,Rhizopus oligosporus,
Syncephalstrum racemosum) [165] forms a distinct clade with three represen-
tatives of the Entomophthorales (Entomophthora muscae, Conidiobolus
coronatus and Zoophthora radicans; fig. 1) [86]. The insect-pathogenic
Entomophthorales (Conidiobolus,Entomophaga,Entomophthora,Eryniopsis,
Pandora,Strongwellsea,Zoophthora) form a monophyletic group except
Basidiobolus [165]. Based on Micromucor and Mortierella, the Mucorales
appear polyphyletic [165]. The arbuscular mycorrhizal fungi (Acaulospora,
Gigaspora,Glomus: Glomales) form a clade together with the ectomycorrhizal
fungus Endogone (Endogonales) and Geosiphon pyriforme, a fungus form-
ing endocytobiosis with Nostoc (Cyanobacteria; fig. 1) [165, 167]. As already
indicated by similarities in septal pore ultrastructure, cell wall structure,
asexual reproductive apparatus, and serological affinity [168], the Harpellales
(Smittium,Furculomyces), an order of the Trichomycetes, have a close
relationship to the Kickxellales (Coemansia,Martensiomyces,Linderina,
Kickxella; fig. 1) [169]. Spiromyces can be excluded from the Kickxellales; it
forms a distinct clade related to the Harpellales and Kickxellales (fig. 1) [169].
The monophyly of the mycoparasitic Dimargaritales received strong bootstrap
support [165]. Also the mycoparasitic and zooparasitic Zoopagales in which
Syncephalis,Thamnocephalis, and Rhopalomyces form a sister group to
Piptocephalis and Kuzuhaea appear monophyletic [165].
Basidiobolus ranarum (fig. 1) as a representative of the Chytridiomycota
rarely causes subcutaneous infections in humans [170]. B. haptosporus and
B. meristosporus are additional species of clinical importance [75]. Conidio-
bolus coronatus (fig. 1; Entomophthorales, Zygomycota), also known as
Delacroixia coronata, is a pathogen causing nasal granuloma in man [80, 171,
172] and other higher mammals [173]. C. incongruus is an extremely rare agent
of systemic mycosis with a pulmonary portal of entry [80]. No molecular infor-
mation is presently available for some other medically important genera of the
Zygomycota (e.g. Apophysomyces,Absidia,Cunninghamella,Rhizomucor and
Saksenaea; also see De Hoog and Guarro [80]. Allergen characterization has
been reported only for Rhizopus nigricans [81].
Systematics of the Ascomycota and Basidiomycota 225

Although Tanabe et al. [165] present a good overview of the phylogeny
of Chytridio- and Zygomycota, further studies of molecular systematics,
chemotaxonomy and ultrastructure will be necessary to establish a phylogenetic
system of the Chytridiomycota and Zygomycota.
Phylogenetic Relationships among the Ascomycota and
Their Anamorphs
About 70,500 species of true fungi or Mycobionta have been described;
however, some estimates of total numbers suggest that 1.5 million species
may exist [174, 175]. Most of them so far belong to the Ascomycota (32,300)
and the mitosporic fungi (14,100) which can generally be included in the
Ascomycota using sequencing of ribosomal DNA. There are numerous
hypotheses on the phylogeny and evolution of higher fungi [for references, see
51, 107, 176–178]. Among these, Savile’s [179] phylogenetic considerations of
higher fungi [107, 179] have attracted many mycologists. Savile suggested that
Taphrina was the closest survivor of a common ancestor of the Euascomycetes
and the Basidiomycota. He suggested that two major lineages evolved from
‘Prototaphrina’, a common ancestor. One major lineage led to the present-
day Taphrina and the higher Ascomycota – today’s Euascomycetes – whereas
another major route led to the Basidiomycota (the Uredinales line and the
parasitic Auriculariaceae line) through a ‘Protobasidiomycete’.
Phylogenetic trees inferred from 18S rDNA sequence divergence indicate
the existence of two distinct phyla or divisions among the higher fungi (fig. 1),
the Ascomycota and the Basidiomycota, e.g. [12, 14, 16, 29, 30, 180–182].
Using Mucor racemosus as an outgroup, our FITCH tree inferred from approx-
imately 1,600 alignable sites of the 18S rRNA gene sequence from about 200
selected species (fig. 3, 4) supports that both phyla appear to be monophyletic.
As already mentioned above, the use of the Deuteromycota or Deuteromycotina
as a formal taxon decreases [14, 16, 145, 175, 183, 184]. Molecular sequence
data clearly demonstrate that ascoma characters traditionally used to delimit
ascomycete orders or classes converge. Eriksson [185] focused attention on the
orders of ascomycetes and discouraged the use of supraordinal taxa.
Plectomycetes, Pyrenomycetes, Loculoascomycetes, Discomycetes and other
traditional class level categories are no longer used formally in the fungal
classification system [14, 175]. Similarly, the classical dipartite systems of the
Ascomycota (Hemiascomycetes, Euascomycetes) [177] and Basidiomycota
(Heterobasidiomycetes, Homobasidiomycetes) [186] are not corroborated by
molecular and biochemical data, instead tripartite systems appear in molecular
phylogenies. Based on complete or nearly complete 18S rDNA sequencing,
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 226

the qualitative and quantitative monosaccharide pattern of purified cell walls
(fig. 3) [129], the ultrastructure of septal pores and urease activity [Prillinger
unpubl. obs., and [187], three classes seem promising among the Ascomycota
(fig. 3): the Hemiascomycetes, the Protomycetes and the Euascomycetes
[16, 188–190]. We cannot confirm the concept of the basal Ascomycetes or
Archiascomycetes suggested by Berbee and Taylor [30], Nishida and Sugiyama
[181], and Sugiyama [14]. Based on our polyphasic biochemical and molecular
approach, the Euascomycetes and Protomycetes appear as a sister group (fig. 3),
whereas the Hemiascomycetes occupy a basal position.
The following data of the literature are in favor of our interpretation [also
see Cai et al., 191]:
(1) the nuclear genome size of the Hemiascomycetes appears to be about
one-third the size of Aspergillus, Schizosaccharomyces and the basidiomyce-
tous yeasts [192, 193]. More recent data from the whole genome sequencing
project, however, suggest that the genome of Saccharomyces cerevisiae and
Schizosaccharomyces pombe are similar in size (S. cerevisiae 13.4Mb [194];
Sch. pombe about 14 Mb [195]). The 14Mb are organized in 3 compact chro-
mosomes in Sch. pombe, which resemble higher eukaryotes. In S. cerevisiae 16
rather primitive chromosomes (see 2 and 5) were found.
(2) S. cerevisiae shows a rather unique cell cycle with the doubling of
the spindle pole body and the formation of a short mitotic spindle already in the
S-phase.The G2phase is missing. On the other hand, the cell cycle of Sch.
pombe resembles the higher eukaryotes with a characteristic G1, S, G2and
mitose phase [196].
(3) S. cerevisiae has a very compact nuclear genome with very few introns
(223 introns) [197, 198]. The higher frequency of introns in the genes of Sch.
pombe resembles the situation in the higher eukaryotes.
(4) S. cerevisiae is one of the few eukaryotes that can live without func-
tional mitochondria. On the other hand, Sch. pombe requires functional mito-
chondria for survival as do the higher eukaryotes.
(5) The centromers of S. cerevisiae are smaller and lack the repeated
sequences which are typical for higher eukaryotes. Sch. pombe has centromers
which resemble those in ‘higher’ascomycetes and have a similar function [199].
(6) The length of the mating type loci: S. cerevisiae has the shortest known
idiomorphs for the mating type loci (a: 640 bp, : 750bp). The respective lengths
for Sch. pombe are P: 1.1 kb, M: 1.1 kb; for Podospora pauciseta mat: 3.8 kb,
mat–: 4.7 kb, for Neurospora crassa A: 5.3 kb, a: 3.2kb; for Ustilago maydis a1:
4.5 kb, a2: 8 kb; and for the hymenomycetous yeast Cryptococcus neoformans
mat 35–45 kb (the mat-a locus of C. neoformans is not yet determined) [200].
(7) The lack of fruit bodies among the Hemiascomycetes could be
interpreted as a primitive rather than as a reduced character. Among the
Systematics of the Ascomycota and Basidiomycota 227

Protomyces/Schizosaccharomyces group the Neolectales produce club-shaped
fruit bodies, which are up to 7 cm tall and differ from other ascomycetous fruit
bodies mainly by the absence of sterile hyphae (paraphyses) between the asci,
the lack of ascogenous hooks (crosiers) prior to ascus development, and the
unusual combination of inoperculate asci having amyloid ascus walls [201].
(8) The coenzyme Q of the Hemiascomycetes contain a variable number
of isoprene units ranging from Q-5 to Q-9 (Q-10 was found in Lipomyces
lipofer). On the other hand, most strains of the Protomyces/Schizosaccharomyces
clade analyzed so far contain coenzyme Q-10 (with the exception of Schizo-
saccharomyces octosporus, which has Q-9), resembling the Euascomycetes,
which, in most cases contain coenzyme Q-10 and Q-10 (H2). Coenzyme Q-9
was found only rarely in some euascomycetous strains (e.g. Capronia parasitica,
Symbiotaphrina spp.). No strain with less isoprene units was found within the
Euascomycetes so far. Basidiomycetous yeasts possess coenzyme Q systems
with Q-7, Q-8, Q-9, Q-10 and Q-10 (H2) [202 and references therein].
(9) The Hemiascomycetes include morphologically primitive fungi (within
the genus Eremothecium) with coenocytic ‘siphonal’ [41, 83, 152] ontogenetic
stages which resemble the Zygomycota and Chytridiomycota.
(10) The haplo-diplontic life cycle of S. cerevisiae also shows some
similarities with the Chytridiomycota, where in contrast to the Euascomycetes,
this type of life cycle and diploid stages, are common [63].
Hemiascomycetes
Within the Hemiascomycetes, Kurtzman and Fell [202] presently accept a
single order, Saccharomycetales (Endomycetales), only. Based on the qualita-
tive and quantitative monosaccharide pattern of purified yeast cell walls and
complete 18S rDNA sequences (fig. 3) [203], we accept four different orders:
Saccharomycetales, Dipodascales, Lipomycetales and Stephanoascales.
Whereas the Saccharomycetales and Lipomycetales can be delimited by the cell
wall monosaccharide pattern and the presence or absence of extracellular amy-
loid compounds (Saccharomycetales: glucose, mannose, extracellular amyloid
compound ; Lipomycetales: glucose, mannose, galactose, extracellular amy-
loid compound ) it is not possible to separate the Dipodascales and
Stephanoascales based on the cell wall monosaccharide pattern. Within both
orders, glucose, mannose and galactose dominate; however, species with the
glucose mannose pattern appear intermingled [203]. Sequences of the complete
18S rRNA gene are important to decide, whether a species belongs to the
Dipodascales or the Stephanoascales. Extracellular amyloid compounds (starch
formation) are absent in the Dipodascales and Stephanoascales. Kurtzman and
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 228

Fell [202] extensively discuss the problem of using Saccharomycetales instead
of the older order Endomycetales. The order Dipodascales was already intro-
duced by Batra [204]. However, based on molecular characteristics, many gen-
era suggested by Batra cannot be included into this order. Additional complete
18S rDNA sequences are necessary to corroborate the orders Dipodascales,
Lipomycetales and Stephanoascales [203].
Within the Dipodascales, four yeast species are of medical importance:
Dipodascus capitatus and its anamorph Geotrichum capitatum, Yarrowia
lipolytica (anamorph: Candida lipolytica), G. candidum and G. clavatum.
Komagatella (Pichia) pastoris is a biotechnologically interesting yeast which
exhibits the glucose mannose cell wall monosaccharide pattern and comes close
to the Dipodascales [203] and [Prillinger unpubl. obs.). K. pastoris became an
important host for the expression of recombinant DNA in recent years [202].
Its gene expression system has been developed to produce large amounts of
medically and industrially important proteins [205]. D. capitatus is associated
with human lung disorders. It is increasingly being found in blood of immuno-
compromised hosts, particularly in cases of leukemia [80, 202]. C. lipolytica
has been isolated from patients with fungemia [75]. The main human disorders
caused by G. candidum are bronchial or pulmonary infections, in humans as
well as in nonhuman mammals [206]. Smith et al. [207] and Prillinger et al.
[208] have shown that Galactomyces geotrichum and its anamorph G. candidum
are genotypically heterogeneous. G. candidum should be conserved for a bene-
ficial species common in cheese and other dairy products. G. clavatum is
involved in human mycoses, particularly in connection with pulmonary disorders.
Within the Saccharomycetales, the following species are of clinical impor-
tance: Candida albicans, C. parapsilosis, C. tropicalis, C. viswanathii,
Debaryomyces fabryii (anamorph: C. famata var. flareri), Pichia guilliermondii
(anamorph: C. guilliermondii) are phylogenetically closely related and may be
included within the family Debaryomycetaceae (fig. 3) [23]. Pichia norvegensis
(anamorph: C. norvegensis) and Issatchenkia orientalis (anamorph: C. krusei),
Kluyveromyces marxianus (C. kefyr), S. cerevisiae, and C. glabrata, Clavispora
lusitaniae (C. lusitaniae) and C. haemulonii are additional groups of phylo-
genetically related species which can be included in the Saccharomycetales
(fig. 3) [23]. Last but not least Pichia anomala and its anamorph C. pelliculosa
are representatives of the Saccharomycetales.
As can be seen from figure 3, Kurtzman and Robnett [23] and Suzuki et al.
[203], within the Hemiascomycetes, the genera Candida and Pichia are still
heterogeneous. It was not possible to separate the genus Issatchenkia genotyp-
ically from the genus Pichia represented by its type species P. membranifaciens
(fig. 3) [23]. Genotypically, the genera Kluyveromyces, Saccharomyces,
Torulaspora and Zygosaccharomyces appear intermingled (fig. 3) [23, 191].
Systematics of the Ascomycota and Basidiomycota 229

K. delphensis is the teleomorphic species closest to Candida glabrata (fig. 3)
[23, 191]. C. dubliniensis was recently described as a new species [209] isolated
from 60 HIV-infected and 3 HIV-negative persons. Although C. dubliniensis
closely resembles C. albicans phenotypically, it could be distinguished geno-
typically [23, 209]. Rapid identification of C. dubliniensis with commercial
yeast identification systems was described recently [210]. However, Sullivan
et al. [209] did not compare their isolates with strains representing the many
synonyms of C. albicans, so it is possible that the species may be synonymous
with an earlier described species.
C. albicans commonly occurs in the digestive tract. Candidiasis is by
far the most important mycosis. Vaginal candidiasis is extremely frequent.
Mucocutaneous candidiasis occasionally leads to osteomyelitis [211]. Further
information on the pathogenicity of C. albicans can be found in De Hoog and
Guarro [80] and Murray et al. [75]. C. albicans and Saccharomyces cerevisiae
were also considered as allergenic yeasts [81]. S. cerevisiae has been isolated
from deep infections in debilitated patients and in patients with impaired immu-
nity, both natural and acquired [212, 213]. De Hoog [213] presents an excellent
overview of risk assessment of fungi reported from humans and animals.
An interesting process of ‘budding meiosis’ was reported by van der Walt
and Johannsen [214] in Candida albicans and C. tropicalis. Diploidization of
the sexually active haplophase appeared to involve somatogamous autogamy or
autodiploidization. The site of reduction divisions was identified when it was
shown that the diplophase formed multinucleate cells on which the haplophase
was delimited externally as buds. ‘Budding meiosis’ in ascomycetous yeast
may be a phylogenetic precursor of the concept of ‘yeast basidia’ which was
introduced by Prillinger et al. [215–217] and seemed to be fundamental in the
evolution of basidia in the Basidiomycota. Although the presence of sexuality
in C. albicans was corroborated recently by the presence of a mating-type-like
locus [128], the existence of ‘budding meiosis’ in hemiascomycetous yeasts
needs further confirmation by cytological and ultrastructural data.
C. glabrata is often involved in urogenital infections [218]. It can also be
involved in deep infections (heart [219]; lungs, occasionally with sepsis [220];
osteomyelitis [221]. There is evidence that C. glabrata may emerge after anti-
C. albicans therapy [222].
Debaryomyces hansenii var. fabryii and its anamorph C. famata var. flareri
were reported to be pathogenic by Vazquez et al. [223] and Nicand
et al. [224]. Using random amplified polymorphic DNA analysis (RAPD-PCR),
Prillinger et al. [208] considered D. hansenii var. fabryii as a distinct species, i.e.
D. fabryii.
A compilation of the pathogenicity of C. haemulonii,C. parapsilosis,
C. tropicalis,C. viswanathii,Clavispora lusitaniae,Issatchenkia orientalis,
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 230

Kluyveromyces marxianus,Pichia anomala,P. guilliermondii, and P. norvegensis
can be found in De Hoog and Guarro [80] and Murray et al. [75]. Blaschke-
Hellmessen [225] gives an overview of the habitats of pathogenic Candida species.
Based on ribosmal DNA sequencing, Messner et al. [21] and Prillinger et al.
[152] included the two filamentous and plant parasitic species Eremothecium ash-
byi and E. gossypii as well as the two dimorphic plant parasites E. coryli and
E. sinecaudum in the family Saccharomycetaceae (fig. 3). These data clearly indi-
cate that yeasts cannot be separated taxonomically from filamentous fungi.
Within the Stephanoascales Stephanoascus ciferrii and its anamorph
C. ciferrii are the only pathogenic species so far. The species is often associated
with animals and occasionally isolated from clinical specimens [226] as an agent
of human onychomycosis [227]. Some strains are strongly hyphal and produce
conidia from characteristically inflated, denticulate heads. This anamorph has
been described as Sporothrix catenata.
No species of the order Lipomycetales is known to be pathogenic in humans
so far. The order comprises typical soil yeasts (Babjevia, Lipomyces) and mycelial
species (Dipodascopsis).
Protomycetes
Figure 3 shows there is good bootstrap support for the new class of the
Protomycetes in our FITCH tree. A similar tree topology was obtained when the
programs neighbor-joining and maximum likelihood of the PHYLIP packages
were used for tree construction [16, 151]. Presently, four orders are accepted
within the Protomycetes. These are the Neolectales, the Pneumocystidales, the
Schizosaccharomycetales and the Taphrinales [228]. A fifth order, the
Protomycetales, suggested by Eriksson and Winka [228] and Kurtzman and Fell
[202], is not supported by biochemical and molecular data [182, 229, 230].
Prillinger et al. [229, 230] consider the Protomycetaceae as a family of the
Taphrinales.
Whereas the order Taphrinales was already introduced in 1928 by Gäumann
and Dodge [see Eriksson and Winka, [228], the Schizosaccharomycetales,
Neolectales, and Pneumocystidales were suggested only recently based on mol-
ecular characters. The order Schizosaccharomycetales was introduced by
Prillinger et al. [229]. It was accepted by Kurtzman [193], Eriksson et al. [231],
and Kurtzman and Fell [202]. The orders Neolectales and Pneumocystidales (fig.
3) were suggested by Landvik et al. [232] and Eriksson [233]. Based on the qual-
itative and quantitative monosaccharide pattern of purified cell walls, Prillinger
et al. [215, 216, 229, 234] consider the Protomycetes (Protomyces-Typ,
Schizosaccharomycetales) ancestral to the Euascomycetes and Basidiomycota,
Systematics of the Ascomycota and Basidiomycota 231

especially the Urediniomycetes sensu Swann and Taylor [10]. Morphological and
ultrastructural data of Mixia osmundae [235 and Bauer unpubl. obs.] and 5S
rRNA sequences from Protomyces inundatus [25] and Taphrina deformans [236]
are additional characteristics which give support to the concept that the
Protomycetes are ancestors of the Basidiomycota, as was originally suggested by
Savile [107]. Based on the presence of fucose in cell walls of T. vestergrenii [217,
229], we consider T. vestegrenii a missing link on the route from the
Protomycetes to the Urediniomycetes. Based on complete sequences of the
18S rDNA T. vestergrenii occupies an intermediate position between the genera
Protomyces and Taphrina. We have suggested the new genus Fucotaphrina for
this species.
Based on the qualitative and quantitative monosaccharide pattern of puri-
fied cell walls (glucose: 70, mannose: 23, galactose: 7) and rDNA sequencing
(fig. 3) [237], the anamorphic pigmented yeast Saitoella complicata unequivo-
cally belongs to the Protomycetes and can be excluded from the Uredin-
iomycetes where it was included originally. A two-layered cell wall, a negative
diazonium blue B test and positive urease activity are additional characteris-
tics of yeasts and yeast stages which belong to the Protomycetes [238].
Enteroblastic budding of S. complicata [14], however, suggests affinities to the
Basidiomycota.
The Neolectales are so far the only group of the Protomycetes where mor-
phologically distinct fruting bodies, apothecia similar to clavarioid basidiocarps,
are produced. Landvik et al. [232] and Landvik [239] excluded the apothecial
ascomycetes Neolecta vitellina and N. irregularis from the Euascomycetes
(fig. 3). Asci of N. vitellina are occasionally filled with numerous conidia and
the ascospores become conidiogenous by producing a single apical collarette
from which the phialoconidia emerge [201]. These features are similar to bud-
ding of ascospores within the ascus of Taphrina, and therefore do not conflict
with the proposed molecular phylogeny.
The Pneumocystidales is the only order of the Protomycetes which harbors
species pathogenic in humans. Pneumocystis carinii is a unicellular eukaryotic
organism with a tropism for growth on respiratory surfaces of mammals [75].
Epidemic pneumonia may occur in institutional housing, such as orphanages,
under conditions of overcrowding and malnutrition. P. carinii has emerged as
one of the most common pulmonary infections in AIDS patients in recent years;
the presence of Pneumocystis has become one of the first indications for the
disease [80]. The molecular phylogeny and systematics of P. carinii have been
controversial for a long time (fig. 3 [75, 240, 241]). P. carinii has a number of
features that are atypical for fungi (e.g. cholesterol instead of ergosterol) [75].
There is emerging molecular evidence that there are different varieties, and pos-
sibly different species of Pneumocystis.
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 232

The Schizosaccharomycetales comprise three distinct fermentative species
which reproduce by fission; none of them are of medical importance [202].
Schizosaccharomyces pombe is known from tropical millet beer.
The Taphrinales (fig. 3) comprise the Protomycetaceae and the
Taphrinaceae [230]. All species are dimorphic fungi with the mycelial phase
parasitic on ferns and especially woody dicotyledons, and the yeast phase sapro-
phytic [176]. The mycelia and meiosporangia of the Protomycetaceae are
polykaryotic, within the Taphrinaceae mycelia are commonly dikaryotic and
the young meiosporangia contain one nucleus only. Prillinger et al. [229] regard
the ascus of Taphrina as a ‘siphonal’ germination state of a chlamydospore. This
siphonal germ tube acts as a meiosporangium, where an evolution from an unde-
termined number of meiotic nuclei in the case of Protomyces to a single meiotic
nucleus represented by the Taphrina species becomes obvious.
Euascomycetes
The Euascomycetes with comparatively well-developed fruiting bodies or
ascomata comprise the plectomycetes, pyrenomycetes, loculoascomycetes,
laboulbeniomycetes, and discomycetes based on traditional morphological
classifications. In the monophyletic euascomycete lineage (100% bootstrap
support in our FITCH tree fig. 3) [14], two major lineages, the Plectomycetidae
with closed ascomata (cleistothecia) and the Pyrenomycetidae with flask-
shaped ascomata (perithecia), appeared monophyletic, each receiving 100%
bootstrap support (fig. 3). The tree topology in figure 3 supports the monophyly
of the Plectomycetidae and Pyrenomycetidae as already detected by Berbee and
Taylor [242] and Nishida and Sugiyama [181]. Our phylogenetic tree (fig. 3)
does not support the concept of Gargas and Taylor [243] that the apothecial
Pezizales (Ascobolus, Peziza, Gyromitra, Inermis, Morchella, Plectania) are
ancestral to the cleistothecial and perithecial forms. Based on the apothecial
Neolectales, however, Nannfeldt’s [244] phylogenetic hypothesis of primitive
apothecial ascomata with subsequent evolution of cleistothecial and perithecial
forms cannot be excluded. The cleistothecial Erysiphales which come close
to the Leotiales, however, appear as an exception (fig. 3) [63]. Within the
Hypocreales there are in addition some cleistothecial taxa, such as
Heleococcum, Mycoarachis and Roumegueriella, which have to be excluded
from the Plectomycetidae [142]. Analyses of 18S rDNA support that neither the
loculoascomycetes (fissitunicate ascomycetes) nor the discomycetes (apothe-
cial ascomycetes) are monophyletic (fig. 3) [16, 89, 243, 245–248]. Within the
fissitunicate ascomycetes, the loculoascomycete order Pleosporales (fig. 3)
appears as a monophyletic group including the families Pleosporaceae and
Systematics of the Ascomycota and Basidiomycota 233

Lophiostomataceae; similarly, the loculoascomycete order Dothideales (fig. 3)
may also constitute a monophyletic group, however, with weaker statistical
support [89, 247]. On the other hand, the fissitunicate Chaetothyriales appear
as a sister group of the Plectomycetidae or the lichen-forming Lecanorales
and Peltigerales (fig. 3) [16, 89, 246–249]. Within the Laboulbeniales, the
Pyxidiophora-Rickia lineage (obligate parasites of arthropods) lies outside the
other perithecial ascomycetes among loculoascomycetes and discomycetes
where taxon sampling is still incomplete [250]. At the moment, therefore,
previous hypotheses including Pyxidiophora in the Hypocreales, the
Ophiostomatales or the Hemiascomycetes are not supported [250].
For allergenic and human-pathogenic Euascomycetes, the following three
orders are of special importance: Chaetothyriales, Eurotiales and Onygenales
(fig. 3). Additional species can be found within the Dothideales, Hypocreales,
Leotiales, Microascales, Ophiostomatales, Phyllachorales, Pleosporales and
Sordariales. Extensive explanations of terms and types of mycosis used in
clinical pathology can be found in De Hoog and Guarro [80].
Chaetothyriales
There is molecular evidence that at least the families Chaetothyriaceae
and Herpotrichiellaceae belong to the Chaetothyriales [249]. Unexpectedly,
the Chaetothyriales were found to be remote from the remaining Loculoas-
comycetes such as Dothideales and Pleosporales and relatively close to the
Onygenales and Eurotiales (fig. 3) [246] or the lichen-forming Lecanorales and
Peltigerales [249]. The diversity of anamorphs in Chaetothyriales is remarkable
and it is often difficult to distinguish them from anamorphs of the Dothideales
[246]. Many species are dimorphic and are able to grow in yeast form (black
yeasts). Similarly to the fissitunicate ascomycetes, the black yeasts are poly-
phyletic as well, and occur within the Chaetothyriales, Dothideales and
Pleosporales. Calcium regulates in vitro dimorphism in chromoblastomycotic
fungi [251]. Basic morphological differences are associated with differences in
thallus structure and maturation [252], which explains why anamorphs of
Chaetothyriales are smaller and more homogeneously pigmented than those
of Dothideales [246]. Whereas Capronia species, a teleomorphic genus of
the Herpotrichiellaceae, were described from plants such as Ericaceae [253],
most anamorphs, however, have been associated with a wide spectrum of
human diseases. Chromoblastomycosis is a disease which is not found outside
the Herpotrichiellaceae [246]. Untereiner and Malloch [187] discussed the
patterns of substrate utilization within the Herpotrichiellaceae. Cladophialophora
(C. arxii,C. bantiana,C. boppii,C. carrionii,C. devriesii), Exophiala (E. berg-
eri,E. castellani,E. dermatitidis,E. jeanselmei,E. lecanii-corni,E. moniliae,
E. pisciphila,E. salmonis,E. spinifera), Fonsecaea (F. compacta,F. pedrosoi),
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 234

Phaeoannellomyces (P. elegans), Phialophora (P. bubaki,P. macrospora,
P. repens,P. richardsiae,P. verrucosa), Ramichloridium (R. mackenziei,
R. schulzeri), Rhinocladiella (R. aquaspersa,R. atrovirens), and Sarcinomyces
(S. phaeomuriformis) are important human pathogenic genera and species
within the Herpotrichiellaceae [75, 80, 246]. It was not possible to differentiate
S. phaeomuriformis from E. dermatitidis using complete sequences of the 18S
rDNA. Within the Herpotrichiellaceae, however, none of these genera appeared
phylogenetically homogeneous based on complete 18S rDNA sequences [246].
The genus Sarcinomyces is polyphyletic, S. crustaceus and S. petricola have to be
excluded from the Herpotrichellaceae [89]. The genus Wangiella was not
accepted by Haase et al. [246]. It is considered as a synonym of Exophiala.
Cladophialophora modesta takes a somewhat external position with respect to the
Herpotrichiellaceae and comes close to the Chaetothyriaceae. This is remarkable,
since the species was isolated from mycosis in the brain of a human patient [254].
Eurotiales
Benny and Kimbrough [255] redefined the classical morphological class
of the Plectomycetes with emphasis on centrum development and mode of dis-
charge of the asci, and recognized six orders (Ascosphaerales, Elaphomycetales,
Eurotiales, Microascales, Onygenales and Ophiostomatales). Molecular data,
however, suggest that only the Ascosphaerales, Elaphomycetales, Eurotiales
and Onygenales can be accepted within the subclass Plectomycetidae (fig. 3).
Presently, it is not clear whether the Ascosphaerales which lack ascocarps and the
hypogeous Elaphomycetales can be accepted as distinct orders or families within
the Eurotiales (fig. 3) [63, 228, 256]. Eriksson and Winka [228] suggest five fam-
ilies within the Eurotiales (Ascosphaeraceae, Elaphomycetaceae, Eremascaceae,
Monascaceae and Trichocomaceae) based on molecular characterization. The
plectomycete family Trichocomaceae within the Eurotiales includes cleistothecial
teleomorphic genera which are associated with economically and medically
important anamorphs, such as Penicillium, Geosmithia, Merimblia, Aspergillus,
Peacilomyces and related genera [257, 258]. The teleomorphic genera associated
with a Penicillium anamorph are Talaromyces, Hamigera, Eupenicillium,
Trichocoma, Penicilliopsis and Chromocleista [14, and literature cited therein].
Berbee et al. [259] and Sugiyama [14] gave a good overview of molecular
phylogenetic studies in the Trichocomaceae. According to these studies, the genus
Penicillium is not monophyletic; one group diverged first within the Trichoco-
maceae cluster and contains different Talaromyces species with the Penicillium-
producing Talaromyces flavus and the Geosmithia-producing T. bacillisporus. The
second group consists of the Penicillium-producing Eupenicillium javanicum, the
Aspergillus-producing Eurotium rubrum and Neosartorya fischeri as well as the
Basipetospora-producing Monascus purpureus.
Systematics of the Ascomycota and Basidiomycota 235

Emericella (Aspergillus) nidulans is a remarkable fungus which lacks synap-
tic meiosis. Prillinger [41, 83] considers this fungus besides S. pombe important for
a polyphyletic evolution of meiosis within the Eumycota or Mycobionta [260, 261].
Within the genus Aspergillus especially three species are of clinical impor-
tance A. flavus,A. fumigatus and A. terreus (fig. 3 ) [262]. A. flavus is one of the
main agents of human allergic bronchial aspergillosis. The species also occurs in
the external ear and may be involved in otitis [263]. It is a common agent of
mycotic sinusitis [80]. Systemic infections occur in leukemic patients [264].
Together with A. parasiticus,A. flavus is well known for the production of the
mycotoxin aflatoxin [63]. A. fumigatus is the main agent of aspergillosis in
immunocompromised patients. It causes a typical inhalation mycosis, whereby
colonization and invasion are commonly accompanied by allergic reactions. De
Hoog and Guarro [80] gave a good overview of the clinical importance of A. fumi-
gatus. This species has a natural habitat in rotten plant material at higher temper-
atures. It is especially common in air during biological waste treatment and
compost formation [265]. A. terreus causes allergic or invasive bronchopulmonary
aspergillosis [80]. De Hoog and Guarro [80] discuss the clinical importance of 29
additional Aspergillus species (A. alliaceus, A. caesiellus, A. candidus, A. carneus,
A. clavato-nanicus, A. clavatus, A. conicus, A. deflectus, A. janus, A. japonicus, A.
niger, A. ochraceus, A. oryzae, A. restrictus, A. sclerotiorum, A. sydowii, A.
tamarii, A. ustus, A. versicolor). Some of them have teleomorphs in Eurotium (E.
amstelodami, E. chevalieri, E. herbariorum, E. repens), Emericella (E. nidulans,
E. quadrilineata, E. unguis), and Fennellia (F. flavipes, F. nivea). Neosartorya
spinosa is a rare opportunistic human pathogen with an Aspergillus anamorph.
Cases of pulmonary infection and endocarditis have been reported [80].
Within the genus Penicillium only P. marneffei, a member of the subgenus
Biverticillium, is a true and common pathogenic fungus. P. marneffei occurs
naturally in bamboo rats in Southeast Asia. It is the third most common cause
of disseminated opportunistic infection in patients with AIDS in parts of
Southeast Asia. The species is unique among the genus Penicillium in being
dimorphic and forming a unicellular yeast stage that reproduces by planate
division (fission) in tissues [75, 80]. The mycosis is acquired by inhalation and
is mostly fatal when untreated. Ten additional Penicillium (P. chrysogenum,
P. citrinum, P. commune, P. decumbens, P. expansum, P. griseofulvum, P. pur-
purogenum, P. rugulosum, P. spinulosum, P. verruculosum) species are known
as rare opportunistic pathogenic fungi [80].
Within the genus Paecilomyces seven species (P. crustaceus, P. fumosoroseus,
P. javanicus, P. lilacinus, P. marquandii, P. variotii, P. viridis) are rare opportunis-
tic fungi pathogenic in humans [80]. The genus Paecilomyces has teleomorphs in
Byssochlamys, Talaromyces, and Thermoascus. Paecilomyces variotii (fig. 3)
causes pneumonia [266], sphenoid sinusitis [267], soft tissue infection of the
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 236

heel [268] and cutaneous hyalohyphomycosis [269] in humans. Further human
infections are discussed by De Hoog and Guarro [80]. P. tenuipes, a parasitic fun-
gus of moth larvae and pupae can be excluded from the genus Paecilomyces based
on 18S rDNA sequencing [270]. The data suggest P. tenuipes may be the anamorph
of an entomogenous fungus of the genus Cordyceps (Hypocreales).
Eremomyces langeronii with its anamorph Arthrographis kalrae is a cleis-
tothecial species whose inclusion in the Eurotiales has to be confirmed by ribo-
somal DNA sequence information. The species causes an onychomycosis and
is mainly isolated from human skin and nails [80, 271].
Onygenales
Eriksson and Winka [228] suggest three families within the Onygenales
(fig. 8; Arthrodermataceae, Gymnoascaceae and Onygenaceae). The Arthroder-
mataceae and Onygenaceae harbor two important groups of human pathogenic
fungi: the dermatophytes and the dimorphic systemic fungi. Dermatophytes
which were traditionally classified within the Hyphomycetes produce thallic,
one-celled microconidia in addition to multicelled macroconidia. Teleomorphs of
dermatophytes belong to the genus Arthroderma (e.g. Arthroderma simii is the
teleomorph of Trichophyton simii; Arthrodermataceae) [75, 80]. They have spher-
ical evanescent asci containing 8 ascospores; the ascoma wall is often a loose
network of hyphae with complicated branching and ornamentation [80, 272].
Dermatophytes are keratinophilic fungi which are capable of invading the kerati-
nous tissues of living mammals. They are grouped into three categories on the
basis of host preference and natural habitat. Anthropophilic species almost exclu-
sively infect humans, rarely animals. Zoophilic species are essentially pathogens
of nonhuman mammals or birds, although animal to human transmission is not
uncommon. Geophilic species are soil-associated organisms, and soil per se or
soil-borne keratinous debris is a source of infection for humans as well as other
animals. Epidermophyton floccosum, Microsporum audouinii, M. ferrugineum,
Trichophyton concentricum, T. gourrilii, T. kanei, T. megninii, T. metagrophytes,
T. raubitschekii, T. rubrum, T. schoenleinii, T. soudanense, T. tonsurans, T. vio-
laceum and T. yaoundei are the most important anthropophilic species. M. canis,
M. equinum, M. gallinae, T. equinum, T. simii and T. verrucosum are zoophilic
species and M. nanum, M. persicolor, M. praecox, M. vanbreuseghemii and
T. terrestre are geophilic species. The pathogenicity of these species is extensively
discussed in De Hoog and Guarro [80].
The dimorphic systemic fungi are phylogenetically closely related to the
dermatophytes and can be included in the family Onygenaceae (fig. 3, 8) [135,
273, 274]. Five clearly different genera can be distinguished: Blastomyces,
Coccidioides, Emmonsia, Histoplasma and Paracoccidioides. Each comprises
only a very few species and all are pathogenic. Species of Blastomyces
Systematics of the Ascomycota and Basidiomycota 237

Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 238
8

and Histoplasma have a teleomorph in Ajellomyces; for the other genera no
teleomorph is known so far. The natural habitat of all species are warm-blooded
animals. Humans are infected by inhalation of dry propagules or by trauma. In
healthy persons, symptoms are mild and mostly heal spontaneously [80].
Blastomyces dermatitidis is the agent of a chronic, granulomatous blastomyco-
sis of the skin, mostly originating as a pulmonary infection or possibly also
from trauma. Coccidioides immitis causes a coccidioidomycosis. Emmonsia
parva is the agent of a adiaspiromycosis. Adiaspores are liberated conidia,
which, after inhalation, enlarge in the alveoli of the host [80, 275]. Histoplasma
capsulatum causes histoplasmosis. The species is the agent of an intracellular
mycosis of the monocyte-macrophage system. Budding yeast cells are pro-
duced within phagocytosing cells. Paracoccidioides brasiliensis causes a para-
coccidioidomycosis. The species is responsible for a systemic, chronic disease.
It may cause painful, erosive stomatitis with loss of teeth, frequently associated
with swollen lymph nodes. The fungus is abundantly present with yeast cells in
pus and tissues. All species show a temperature-dependent yeast-hypha dimor-
phism. In the environment, they all produce a filamentous mycelial form at
room temperature; at 37 °C they reproduce as yeasts in the tissues.
Chrysosporium zonatum was detected recently as the agent of a dissemi-
nated infection in a patient with chronic granulomatous disease. C. zonatum is
the anamorph of the heterothallic ascomycete Uncinocarpus orissi [276].
Although a dimorphism is absent, this species is phylogenetically closely
related to Coccidioides immitis [277]. It produces abundant arthroconidia and
degrades cellulose as well as keratin [277].
Aphanoascus fulvescens (Onygenaceae), Arachnomyces nodososetosus
(anamorph: Onychocola canadensis; Gymnoascaceae), Gymnoascus dankaliensis,
Gymnascella hyalinospora (Gymnoascaceae), Myxotrichum deflexum, and
Neoarachnotheca keratinophilum (anamorph: Myriodontium keratinophilum;
Onygenaceae) are five rare opportunistic clinical fungi which belong to the
Onygenales [80, 278].
Hypocreales
The Hypocreales are pyrenomycetous ascomycetes with unitunicate
asci produced within fleshy, lightly or brightly colored, typically ostiolate
perithecial ascocarps [142]. However, as already mentioned above, they include
Systematics of the Ascomycota and Basidiomycota 239
Fig. 8. Phylogenetic tree of pathogenic yeasts and fungi based on the partial sequences
of the 18S rRNA gene. Alignment, distance matrix and calculation of phylogenetic distances
were made by means of different programs as described in the legend of figure 1.
Approximately 400bp long DNA fragments were compared corresponding to the position
582–1,006 bp in Saccharomyces cerevisiae.

some cleistothecial species within the Bionectriaceae too [142]. Eriksson
and Winka [228] and Rossman et al. [279] accept five families within the
Hypocreales (Bionectriaceae, Clavicipitaceae, Hypocreaceae, Nectriaceae,
Niessliaceae).
Fusarium solani and its teleomorph Nectria haematococca is a common
clinical species causing keratitis, endophthalmitis and disseminated and cuta-
neous infections (fig. 3) [80]. It is also known as an allergenic fungus [81].
Besides Cladosporium cladosporioides, C. sphaerospermum and Alternaria
alternata, species of Fusarium are the most common allergenic fungi in Canada
[280]. F. aquaeductuum, F. chlamydosporum, F. dimerum, F. incarnatum,
F. oxysporum, F. proliferatum, F. sacchari, F. tabacinum, and F. verticillioides
are rare opportunistic Fusarium species [80]. Based on ribosomal DNA
sequencing, F. dimerum makes the genus Fusarium polyphyletic [139].
Genotypic identification methods are necessary to identify Fusarium species
unequivocally [281]. Cylindrocarpon is an additional anamorph of Nectria
species which is phylogenetically closely related to Fusarium [139]. C. destruc-
tans (teleomorph: Nectria radicicola) and C. lichenicola are two rare oppor-
tunistic clinical fungi within the Hypocreales. No sequence data are available
for C. cyanescens recovered from a human mycetoma [80].
Species of the genus Trichoderma (e.g. T. viride) are potentially patho-
genic, toxigenic, and implicated in allergy or hypersensitivity pneumonitis
[80, 282]. Teleomorphs are known in different Hypocrea species [80, 283].
Trichoderma viride, T. longibrachiatum, T. pseudokoningii, T. koningii and
T. harzianum were reported in recent years to occur in humans [262]. As in the
case of Fusarium genotypic identification methods are necessary to identify
these species unequivocally [284, 285, Kubicek, pers. commun.].
Based on ribosomal DNA sequencing, Acremonium was shown to be a
highly polyphyletic genus affiliated to at least three ascomycetous orders [143].
Teleomorphs of Acremonium are found in several genera of the Euascomycetes
(Emericellopsis, Hapsidospora, Nectria, Nectriella, Neocosmospora, Pronectria
and Thielavia). A larger number of species including the type species A. alter-
natum and the human pathogenic A. kiliense exhibit affinities to the
Hypocreales. A. kiliense has been described to cause ulcerative, nodulous hyalo-
hyphomycosis, mycetomes and keratitis [80]. In A. strictum, a rare opportunistic
human pathogen, phylogenetically closely related to A. kiliense, we have recently
detected a yeast stage. A. alabamense is the known anamorph of Thielavia ter-
restris. It is a rare opportunistic fungus pathogenic in humans and phylogeneti-
cally related to the Sordariales [80, 143]. No molecular data are available for
some additional more or less rare opportunistic Acremonium species (A. blochii,
A. curvulum, A. falciforme, A. hyalinulum, A. potronii, A. recifei, A. roseogri-
seum) pathogenic in humans [80].
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 240

Stachybotrys chartarum is an anamorphic soil and indoor air toxigenic
fungus which especially degrades cellulose. It has been associated with a number
of human and veterinary health problems. Most notable among these has been
a cluster of idiopathic pulmonary hemorrhage cases that were observed in the
Cleveland, Ohio (USA), area [286]. A teleomorph, Melanomma pomiformis, is
known only in S. albipes. It is included in the Niessliaceae of the Hypocreales
based on morphology.
Beauveria bassiana and Metarhizium anisopliae are anamorphic soil fungi
well known as insect pathogens. Both genera have attracted a great deal of
attention because of their biological control potential [63]. Beauveria and
Metarhizium both produce mycotoxins, and the destruxins, a group of sec-
ondary metabolites produced by M. anisopliae, are considered an important
new generation of insecticides [287]. Although the proteinaceous insect cuticle
is an effective barrier to many fungi, insect pathogens, including Beauveria and
Metarhizium, have a series of extracellular proteolytic enzymes that degrade
native insect cuticle [288]. Whereas B. bassiana and M. anisopliae are polyphage
and attack a wide host range, B. brongniartii acts specifically against the
cockchafer (Melolontha melolontha) and is used as a biological control agent
(fig. 9). After the fungus has penetrated the cuticle and reached the hemocoel,
yeast-like blastospores are produced, most probably to overcome the host
Systematics of the Ascomycota and Basidiomycota 241
Conidia germinates on host cuticle Hypha penetrates host
New infection
Saprophytic growth
in the soil?
New sporulation on
mummified larva
Red colouring due
to oosporein production
Blastospores proliferation
white grub dies
Fig. 9. Life cycle of the entomopathogenic fungus Beauveria brongniartii.

defense system. After the death of the host the filamentous form will be
expressed again. This dimorphism is similar to that of some human pathogens
(e.g. Histoplasma capsulatum, Sporothrix schenckii). In addition, B. bassiana
and M. anisopliae cause rare infections in humans and have been identified
as agents of keratitis. Evidence that B. bassiana is an invasive human pathogen
is doubtful because in the only reported case, the isolated mould was described
as having greenish colonies and had microscopic features inconsistent with
those of B. bassiana [75]. rDNA analyses place these anamorphic fungi among
the Hypocreales [142, 289].
Verticillium is a further heterogeneous anamorph genus of many species
which are pathogenic in insects and plants. Although Messner et al. [290]
suggested a relationship between the common plant pathogen V. dahliae and
the Hypocreales, partial sequences of the 28S rDNA [142] and a more compre-
hensive phylogenetic tree of complete 18S rDNA sequences (fig. 3) exclude
V. dahliae from the Hypocreales. In contrast, the entomopathogenous V. lecanii
clusters within the Hypocreales [142].
Ophiostomatales
This order is usually characterized by perithecial ascocarps, but with cleis-
tothecia in one genus (Europhium) [291, 292] and evanescent asci. A yeast
stage is known in many species [148, 293]. The qualitative and quantitative
monosaccharide patterns of purified yeast cell walls resemble those of Protomyces
and Taphrina species containing rhamnose [148]. Based on cell wall sugars,
sensitivity to cycloheximide, rDNA sequencing (fig. 3) and some additional
characteristics [63], species of Ophiostoma are phylogenetically distinct from
morphologically similar Ceratocystis (Microascales; fig. 3) species [294, 295].
Genotypic methods are important to distinguish species unequivocally [148,
293]. Many species are associated with scolytid and platypodid bark beetles in
woody tissues where they occur as saprophytic blue stain fungi. O. novo-ulmi is
a highly virulent plant pathogenic fungus causing Dutch elm disease [63].
Ophiostoma stenoceras causes onychomycoses in humans [296].
Sporothrix schenckii (fig. 3) is an anamorphic species which is the agent of
human sporotrichosis; in addition it is known as an allergenic fungus [297].
Characteristic lesions at regional lymph nodes or localized cutaneous infection
are common [80]. Species with a Sporothrix anamorph are also known within
the Hemiascomycetes (Stephanoascales: Stephanoascus ciferrii) and
Basidiomycota (Cerinostereus cyanescens).
Phyllachorales
The characteristics of the perithecial order Phyllachorales are not clear-cut
and await further molecular characterization and investigation of additional
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 242

species. The order is accepted based on Alexopoulos et al. [63] and Eriksson
and Winka [228] for Glomerella, Phyllachora and Polystigma species.
Glomerella cingulata, more often encountered as the anamorph Colletotrichum
gloeosporioides, has been reported as a parasite of over 100 angiosperms.
Sutton [298] provided descriptions for almost 40 species of Colletotrichum;
however, morphological criteria are of little use when information on a plant
pathogenic isolate is needed. Colletotrichum coccodes, C. dematium and C.
gloeosporioides are known as rare opportunistic fungi causing keratitis in
humans [80].
Sordariales
The perithecial order Sordariales is less important from the economic
point of view; however, it harbors genera well known from experimental mycol-
ogy (Neurospora, Podospora, Sordaria; fig. 3). Neurospora sitophila
(Sordariaceae), the red bread mould, is known to infest bakeries and cause con-
siderable contamination. In culture, the fungus literally lifts the lid of petri
dishes, and contaminates by rapid growth and the production of enormous num-
bers of pinkish air-dispersed conidia. N. sitophila is also known as an allergenic
fungus [297].
Species of the Chaetomiaceae differ from Sordariaceae by their usually
globose or ovoid asci that lack an apical ring and deliquesce within the perithe-
cium or cleistothecium. In addition, the best-known species have conspicu-
ous hyphal appendages on the ascocarp surface. Chaetomium atrobrunneum,
C. funicola and C. globosum are known as rare opportunistic human pathogens
[80]. Members of the Chaetomiaceae are cellulolytic and occur naturally on
paper, tapestries, and cotton fabrics, sometimes causing considerable damage.
C. globosum is also known as an allergenic fungus [297].
Corynascus heterothallicus, with its anamorph Myceliophthora ther-
mophila, is another species of the Chaetomiaceae. This fungus was recovered
from a disseminated infection in a leukemic patient [80].
The genus Phaeoacremonium was introduced by Crous et al. [299] to
distinguish Acremonium species with pigmented vegetative hyphae and conid-
iophores. P. parasiticum, originally described as Phialophora parasitica, is
known as the agent of phaeohyphomycoses or mycetomes [80]. Partial
sequences of the 26S rDNA of P. parasiticum corroborate the exclusion of the
genus Phialophora [300]. De Hoog [pers. commun.] suggests a relationship
with Sordariales.
Lecythophthora hoffmannii, L. mutabilis, Phialemonium curvatum and
P. obovatum are rare opportunistic clinical fungi for which morphological and
molecular data suggest an affinity to Sordariales (Coniochaetaceae) [80,
Prillinger and Lopandic unpubl. obs.].
Systematics of the Ascomycota and Basidiomycota 243

Microascales
Members of this order are characterized by a lack of stromata, perithecia
in most species, but some possess cleistothecia. Previously, Microascaceae
were placed among plectomycetes by some mycologists because of the mature
condition of evanescent, scattered asci [255]. More recently, Barr [301] placed
the family among the pyrenomycetes. The work of Berbee and Taylor [242,
302] and Spatafora and Blackwell [295] using DNA analysis has clearly placed
the group within the perithecial ascomycetes (Pyrenomycetidae, fig. 3). The
conidia of Microascaceae are blastic, and conidiogenous cell proliferation
is percurrent or sympodial. Several anamorphs include Scopulariopsis,
Scedosporium and Wardomyces. Pseudallescheria boydii is a cleistothecial
species which is frequently encountered as a saprophyte in soil, manure and
polluted water. The species is reported worldwide as the agent of white grain
mycetomes. In addition, the fungus causes systemic infections in immuno-
compromised hosts or occurs in the respiratory tract where it triggers allergic
reactions, sinusitis, pneumonia or systemic pseudallescheriasis [80]. Species
causing onychomycosis include Scopulariopsis brevicaulis, by far the most
important as both a pathogen and a regular contaminant, S. candida, Microascus
cirrosus (fig. 3) and M. cinereus [75, 80]. S. brumptii is increasingly found as
a pulmonary invader in patients with impaired cellular immunity [80]. S. acre-
monium, S. asperula, S. flava, S. fusca and S. koningii are known as rare oppor-
tunistic pathogenic fungi in humans [80]. Microascus manginii has been
reported in several cases of onychomycosis [80].
Scedosporium prolificans has been frequently isolated from subcutaneous
lesions; in addition, it was recovered from a fatal case of endocarditis [80].
Ceratocystis fimbriata (fig. 3) is an aggressive primary pathogen with a
worldwide distribution that causes diseases in a wide range of plants (sweet
potato, rubber, coffee, quaking aspen, prune, apricot) [303]. Its long-necked
perithecia are morphologically closely similar to those of Ophiostoma species
[63]. In contrast to Ophiostoma, no yeast stage is known for Ceratocystis species.
Dothideales
Nannfeldt [244] first segregated the classical Loculoascomycetes (which he
called ascoloculares) from the other filamentous ascomycetes. While
the other filamentous ascomycetes usually have thin-walled asci with a single
functional wall layer, the Loculoascomycetes have thick-walled asci with two sep-
arable wall layers (fissitunicate) [63]. Luttrell [304] established the subclass
Loculoascomycetes to grant formal taxonomic status to Nannfeldt’s group.
He placed all other filamentous ascomycetes among the Euascomycetes.
Barr [253] accepted the Loculoascomycetes as a class and presented a highly
structured, hierachical view of its taxonomic subdivisions. Based on rDNA
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 244

sequencing, Berbee [247] and Sterflinger et al. [89] showed that the Loculoas-
comycetes are not monophyletic and can be separated into three distinct
orders: the Chaetothyriales, the Dothideales and the Pleosporales. Although the
jack-in-the-box-type ascus is a good marker for large, monophyletic loculoas-
comycete orders (fig. 3), it must have evolved at least twice or been lost at least
once [247].
Whereas species of the genus Cladosporium pathogenic in humans show a
phylogenetic relationship to the Chaetothyriales (Herpotrichellaceae) and were
therefore assigned to the genus Cladophialophora by Masclaux et al. [300], endo-
phytic, mycoparasitic, plant pathogenic, and saprophytic species of Cladosporium
can be included in the Dothideales (fig. 8). Cladosporium herbarum was proven
to represent the anamorph of Mycosphaerella tassiana [300]. C. cladosporioides
and C. sphaerospermum belong to the most common allergenic fungi in Canada
[282]. Mycosphaerella tassiana,C. herbarum,C. macrocarpum and C. cladospo-
rioides had the same partial 26S rRNA sequence. C. sphaerospermum was found
to have 14 base differences [300]. C. cladosporoides and C. herbarum were com-
monly found as endophytes of grapevine [305].
Hortaea werneckii is a dimorphic black yeast which exclusively causes
tinea nigra palmaris on one or both hands or on the sole. It is restricted to tropi-
cal, subtropical and mediterranean areas [80]. H. werneckii is halotolerant hav-
ing its natural habitat in salty environments [306]. Complete sequences of the
18S rDNA (fig. 3) [89] as well as partial sequences of the 26S rDNA suggest a
relationship of H. werneckii with the Dothideales.
Aureobasidium pullulans, a common dimorphic endophyte of grapevine
[305] and saprophyte on plant leaves, occurs in addition as an allergenic
fungus [297, 307] and as a rare opportunistic pathogen in humans, where it
caused keratitis, pulmonary infection, systemic infections, cutaneous infection,
peritonitis, and invasive mycosis in an AIDS patient [80]. Complete 18S as well
as partial 26S rDNA sequences corroborate a relationship of Aureobasidium
species with Dothideales (fig. 3) [16, 89, 300].
Hormonema dematioides is a very similar dimorphic fungus, but can be
differentiated from A. pullulans by the absence of synchronous conidiation, by
different physiological profiles and genotypic approaches like RAPD-PCR
[151]. It is also occasionally pathogenic in humans [262].
Madurella grisea and M. mycetomi are the main agents of human black
grain eumycetoma [80]. Presently no molecular data are available which
corroborate an affinity to Dothideales.
Nattrassia mangiferae (synanamorph: Scytalidium dimidiatum) is known as
a plant pathogen but is also commonly reported from human superficial infec-
tions in subtropical and tropical countries. In humans it causes extensive hyper-
keratosis with scaling of the skin of the extremities, as well as onychomycoses
Systematics of the Ascomycota and Basidiomycota 245

[308]. Scytalidium hyalinum probably comprises a hyaline mutant of S. dimidia-
tum causing similar clinical symptoms [80, 308].
Lasiodiplodia theobromae is a rare opportunistic human pathogen causing
keratitis, onycho- and phaeohyphomycosis [80]. Botryosphaeria rhodina is
known as a teleomorph of L. theobromae. B. rhodina clusters with B. ribis
(fig. 3.) in the Dothideales [247].
Neotestudina rosatii and Piedraia hortai are two human pathogenic
species where morphological data suggest a classification among the Dothide-
ales. N. rosatii occurs in soil of tropical countries and causes mycetoma in
humans [80]. P. hortai is the agent of black piedra on scalp hair [80].
Cenococcum geophilum is a cosmopolitan fungus and is the most wide-
spread ectomycorrhizal fungus. It has an extremely broad host range and
habitat. Parsimony and distance analyses positioned C. geophilum as a basal,
intermediate lineage between the two Loculoascomycete orders, the
Pleosporales and the Dothideales [309]. At least four independent lineages of
mycorrhizal fungi were identified among the Ascomycota examined (compare
Elaphomyces, Tuber; fig. 3).
Pleosporales
The Pleosporales form a monophyletic group with high bootstrap support
(fig. 3) [247]. In phylogenetic trees based on complete 18S rDNA sequences, they
commonly appear as a sister group of the Dothideales (fig. 3). This, however, may
change if partial sequences are used (fig. 8). Alternaria alternata is a saprophyte
on dead plant material and a common endophyte [305], but it may also cause skin
lesions in humans after a trauma. Rare cases of systemic infection, onychomyco-
sis and endophthalmitis following eye surgery were reported [80]. Besides
Cladosporium and Fusarium species A. alternata is the most common allergenic
fungus in Canada [282]. Breitenbach et al. [310] reported nucleotide sequences
of three cDNA clones coding for 53-, 22-, and 11-kD allergens. All of these aller-
gens are homologous to Cladosporium herbarum allergens and are abundant,
cytosolic housekeeping proteins. Teleomorphs of Alternaria species are known in
Pleospora and Lewia [311]; they can be included in the Pleosporales (fig. 3;
Pleosporaceae) [311] based on complete sequences of 18S rDNA (fig. 3).
Eriksson and Winka [228] accept four families within the Pleosporales
(Leptosphaeriaceae, Lophiostomataceae, Melanommataceae and Pleosporaceae).
A. chlamydospora, A. dianthicola, A. infectoria, and A. tenuissima are additional
Alternaria species of clinical importance [80]. Ulocladium morphologically
closely resembles Alternaria. Ulocladium chartarum was recovered from exten-
sive infection of subcutaneous human tissues and is considered to be allergenic
[80]. Further molecular data are necessary to clarify the phylogenetic relationship
between Alternaria and Ulocladium.
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 246

Species of Phoma are known to have teleomorphs in Leptosphaeria
(e.g. Phoma lingam) or chlamydospores with muriform septation, resembling
the conidia of Alternaria (e.g. Phoma glomerata). Partial sequences of the 18S
rDNA of Phoma species exhibit a relationship to the teleomorph Cucurbitaria
which can be included in the Pleosporales (Leptosphaeriaceae; fig. 3) [16].
Further sequence data are necessary to clarify whether the genus Phoma is
heterogeneous. Phoma cava, P. cruris-hominis, P. eupyrena, P. glomerata,
P. herbarum, P. minutella, P. minutispora, P. oculo-hominis and P. sorghina are
known as rare opportunistic pathogens in humans [80]. P. betae is considered to
be an allergenic fungus. Epicoccum nigrum is an allergenic fungus; molecular
data suggest that it is a synanamorph of Phoma epicoccina. It was isolated from
Vienna monument surfaces [Sterflinger and Prillinger, unpubl. obs.]. Lehrer
et al. [322] reported that E. nigrum is one of the most important sources of
spores isolated outdoors. It is a frequent sensitizing agent in the Scandinavian
population [307].
Leptosphaeria senegalensis and L. thompkinsii cause mycetoma in Africa
[80]. Coniothyrium fuckelii is the anamorph of L. coniothyrium. It is known as
a plant pathogen especially on Rosaceae and from human infections [80].
The genus Cochliobolus harbors many fungi pathogenic in plants and
humans [80, 311]. Based on ITS and glyceraldehyde-3-phosphate dehydrogenase
gene sequences, Berbee et al. [311] support a suggestion by Tsuda and Ueyama
[312] to separate the genus into two closely related genera: Cochliobolus and
Pseudocochliobolus. Additional molecular sequences, especially, of species path-
ogenic in humans, however, are necessary to corroborate this concept. Species of
Cochliobolus exhibit a Bipolaris anamorph. For species of Pseudocochliobolus,
two anamorphs (Bipolaris, Curvularia) are known [311]. Although De Hoog and
Guarro [80] used the anamorph genus Drechslera for different Cochliobolus
species (D. hawaiensis, D. spicifera and D. australiensis), Berbee et al. [311]
restricted Drechslera to Pyrenophora species, which again cluster within the
Pleosporales (fig. 3). There is some molecular evidence [311] that highly virulent
species pathogenic in plants are common within Cochliobolus (C. carbonum and
C. victoriae) and species pathogenic in humans cluster within Pseudocochliobolus
(P. australiensis, P. geniculatus, P. hawaiiensis, P. lunatus and P. verruculosus).
Presently, no molecular data are available for C. spiciferus (anamorph: Bipolaris
spicifera) an agent of human and animal sinusitis and cutaneous phaeohyphomy-
coses [80]. Bipolaris hawaiiensis is a common saprophyte on plant material.
Sinusitis and pulmonary and cerebral mycosis have been reported [80].
B. australiensis and B. papendorfii are rare opportunistic fungi pathogenic in
humans [80]. Curvularia geniculata was found after traumatic implantation in the
eye and as the agent of allergic sinusitis [80]. Curvularia lunata is a ubiquitous
saprophyte on plant material. It is known from allergic bronchopulmonary disease
Systematics of the Ascomycota and Basidiomycota 247

[313], sinusitis, keratitis, phaeohyphomycosis, onychomycosis or mycetomas
[80]. C. brachyspora, C. clavata, C. pallescens, C. senegalensis and C. verrucu-
losa are considered as rare opportunistic human pathogenic fungi [80].
Exserohilum is an anamorphic genus with teleomorphs in Setosphaeria
[311]. The genus comprises plant pathogenic species, mainly occurring on
grasses. Human mycoses mostly concern cases of sinusitis, partially with
cerebral involvement. E. mcginnisii, E. longirostratum and E. rostratum are
known from human infections [80]. Helminthosporium halodes is the
anamorph of Setosphaeria rostrata. It causes allergic bronchopulmonary myco-
sis [314].
Stemphylium is the anamorph which belongs to the teleomorphic
Pleospora species (fig. 3) [311]. S. macrosporoideum is recovered from a
mixed infection in antromycosis [315]. Together with Alternaria species,
Stemphylium botryosum is considered as one of the most important mold aller-
gens in the United States [307]. There is some molecular evidence that the
genus Pleospora (P. herbarum, P. rudis) [89] is heterogeneous.
Botryomyces caespitosus is a rare opportunistic fungus which causes a
chromoblastomycosis-like subcutaneous infection after trauma in humans [316].
Leotiales
The Leotiales are the largest of the orders of inoperculate discomycetes.
They are characterized by either cup- or disk-shaped apothecia and asci that have
more or less thickened apices. Although the apothecial discomycetes are not a
monophyletic group based on molecular characters [243], there is support that
the Leotiales, Lecanorales and Pezizales are monophyletic orders within the
apothecial Euascomycetes. Many members of the Leotiales live saprobically on
the soil, some are parasitic on plants and belong to the worst fungal pathogens.
Among these are Monilinia fructicola, the cause of brown rot of stone fruits and
Sclerotinia sclerotiorum, the cause of lettuce drop and other vegetable diseases
(fig. 3). Moserella radicicola produces hypogeous apothecia [317]. Botrytis
cinerea and its teleomorph Botryotinia fuckeliana is known as gray mould of let-
tuce and strawberries. The fungus is also known from dessert wines, grapes are
left in vineyards purposely to become infected with B. cinerea, the ‘noble rot’,
which enhances the sweetness of the grapes. In addition, B. cinerea is a common
allergenic fungus [297]. Based on partial sequences of the 18S rDNA, B. cinerea
can be assigned to the Sclerotiniaceae [318].
Ochroconis gallopava is a common agent of encephalitis in poultry. In addi-
tion, it is known to cause subcutaneous phaeohyphomycosis and endocarditis in
humans [80]. O. constricta, O. humicola and O. tshawytschae are known as rare
opportunistic pathogenic fungi [80]. Presently, no molecular data are available
which corroborate the inclusion of the genus Ochroconis in the Leotiales.
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 248

Interestingly, the cleistothecial powdery mildew Blumeria graminis (fig. 3;
Erysiphales) clusters with Sclerotinia sclerotiorum [319]. Additional complete
18S rDNA sequences of powdery mildew fungi are necessary to clarify the
phylogenetic relationship between Erisyphales and Leotiales. It is, however,
remarkable that many representatives of the Leotiales have asci with thick-
walled apices [Oberwinkler, pers. commun.].
Pezizales
Pezizales are a large monophyletic order that contains the species com-
monly called operculate discomycetes as well as derived hypogeous forms that
have evanescent asci with ascospores spread by mycophagy. O’Donnell et al.
[320] have recently investigated phylogenetic relationships among ascomyce-
tous truffels and the true and false morels. The results indicate that the hypo-
geous ascomycetous truffle and truffel-like taxa studied represent at least five
independent lineages within the Pezizales. The data also suggest that several
epigeous and most hypogeous taxa have been misplaced taxonomically. There
is strong support for a Tuberaceae-Helvellaceae clade which is a monophyletic
sister group of a Morchellaceae-Discinaceae clade (fig. 3). Members of the
Morchellaceae, the common morel (Morchella esculenta) and Tuberaceae
(Tuber melanosporum) are well known as food. There are only few poisonous
species (e.g. Gyromitra esculenta) of clinical importance.
Recently, a very rare and interesting fungus, Calyptrozyma arxii, was
isolated from a case of esophagitis. This fungus is typically dimorphic, initially
developing as a yeast and then producing hyphae. Both sexual and vegetative
reproductive structures are produced in the same thallus. Sexual reproduction is
represented by naked asci, and both blastic and thallic conidia are produced
[321]. Recent 5.8S rRNA sequence analysis suggests a close relationship with
Pezizales [262].
Phylogenetic Relationships of the Basidiomycota and
Their Anamorphs
Within the Basidiomycota neither the dipartite classical system of
Patouillard [323], which was recently improved by Oberwinkler [186, 324, 325],
nor the tripatite systems, which are based on the morphology of the basidium
according to Lowy [326], Talbot [327] and Donk [328, 329], could be corrob-
orated by biochemical and molecular data. In contrast to Lowy, Talbot and
Donk, Patouillard and Oberwinkler considered the mode of basidiospore
germination important for the definition of different classes of the Basidiomycota.
Systematics of the Ascomycota and Basidiomycota 249

Dörfler [330] and Prillinger et al. [215–217, 234] detected three phylogeneti-
cally distinct cell wall sugar patterns which correlate perfectly with the com-
plete 18S rDNA sequences of Swann and Taylor [10, 331], Schweigkofler and
Prillinger [16] or the partial 26S rDNA sequences of Begerow et al. [22], lead-
ing to three distinct classes: Urediniomycetes, Ustilaginomycetes and
Hymenomycetes. Yeasts or yeast stages are known in all three classes of the
Basidiomycota (fig. 4). In addition, a yeast stage could be genotypically
demonstrated in three species of the agaric Collybia (fig. 10) [150]. Meanwhile
yeast stages are also known from symbiontic agarics (Agaricales) of leaf-cut-
ting ants (e.g. different Cyphomyrmex species) [332]. A yeast/hypha dimor-
phism is considered of major importance in the evolution of Zygomycota,
Ascomycota and Basidiomycota.
With respect to basidia, Prillinger et al. [216] introduced two different
types of holobasidia. Whereas simple holobasidia are known in all three classes
of the Basidiomycota, complex holobasidia are reported from the Hymeno-
mycetes only [215, 216, 234]. Complex holobasidia can be traced back by
partially septate basidia to tremelloid basidia (e.g. Syzygospora) [216, 333].
Yeast cells were considered to be the most primitive basidia within the
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 250
ba
Fig. 10. A yeast stage in the agarics Collybia cirrata and C. tuberosa. aC. tuberosa on
decaying agaric; arrow indicates purple sclerotium. bC. cirrata: yeasts develop from
basidiospores on an acidic (pH 4.5) malt extract medium. From Prillinger et al.: Expel Mycol
1993;17:26. With permission from Academic Press.

Basidiomycota [215–217]. Similarly, the forcibly discharged basidiospore was
already established in yeast cells of the ‘Sporobolomyces’ type. Ballistospores
stimulate a faster spreading of yeast colonies on solid habitats and may help
to escape or establish parasitic interactions. In Melanotaenium endogenum, all
stages of transition from a mitotic ballistospore to the meiosporangium of
smuts can be observed [334]. Similarly, in the Zygomycota the structures of the
mitosporangium were used to disperse meiospores [63].
The new concept of the Urediniomycetes, Ustilaginomycetes and
Hymenomycetes can also be corroborated by ultrastructural data on septa and
spindle pole body morphology [325, 335, 336 and references cited therein; also
see Hibbett and Thorn, 337].
In tables 1–3 we have compiled some recent data of our cell wall sugar
analyses [129]. The Urediniomycetes are characterized by dominant amounts of
mannose and commonly the presence of fucose (table 1). Rhamnose, which is
characteristic of the Protomyces type [239], may occur sporadically together
with fucose (table 1). The absence of fucose in the Nahoidea/Sakaguchia clade
(table 1, fig. 4) needs further corroboration. Rhodotorula yarrowii is so far the
only species among the 64 investigated strains where xylose was detected as
well (table 1) [338]. In Mixia osmundae we cannot corroborate the data of
Sjamsuridzal et al. [182], who detected rhamnose instead of fucose. Based
on dominant amounts of mannose and the presence of fucose (table 1),
M. osmundae unequivocally belongs to the Microbotryum-type [217, 234], but
its position is uncertain. Morphological as well as ultrastructural data [235]
suggest that M. osmundae is a rather primitive representative of the Uredinio-
mycetes. Sadebeck [339] already observed a Mixia-like exogenization of spore
formation in Taphrina carpini.
The qualitative and quantitative monosaccharide patterns of purified yeast
cell walls of Sterigmatomyces halophilus closely resemble those of some
Saccharomyces species (table 1). They can be distinguished from those of
the Saccharomyces type by the absence of glucose fermentation and a positive
diazonium blue B and urease test (Microbotryum type) [217, 234]. The glucose
mannose cell wall sugar pattern also appears in extremely derived
Hymenomycetes (table 3), but is different from that of the Urediniomycetes, as
it exhibits very high amounts of glucose (e.g. symbiotic yeast isolates from the
leaf-cutting ants Cyphomyrmex). It seems that the glucose mannose pattern is
the alpha and omega in the evolution of the Basidiomycota. Glucose is low at
the beginning and high at the end of evolution. Among different representatives
of the Ustilagionomycetes, the qualitative and quantitative cell wall sugar
patterns are commonly very homogeneous (table 2) [215, 217, 340]. Glucose
dominates over mannose, and galactose is commonly present. Among the
Hymenomycetes we have included 10 filamentous species representing
Systematics of the Ascomycota and Basidiomycota 251

the Agaricales (Asterophora, Clitocybe, Mycena, Pholiota), Hymenochaetales
(Phellinus), Polyporales (Fomes, Laetiporus, Phanerochaete, Polyporus) and
Schizophyllales (Schizophyllum; fig. 4, table 3). Additional species can be
found in O’Brien and Ralph [341], Prillinger et al. [216, 217] and Messner
et al. [340]. Dominant amounts of glucose and the presence of xylose are well-
established characters of the Hymenomycetes. Presently, only Coniophora
puteana (Boletales) [341] deviates from this pattern, showing glucose, mannose
and galactose as cell wall monosaccharides.
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 252
Table 1. Cell wall sugars of yeasts or dimorphic Basidiomycota which belong to the Urediniomycetes
Species Strain Cell wall sugars
GLC MAN GAL XYL FUC RHA
Urediniomycetes
Nahoidea/Sakaguchia clade
Erythrobasidium hasegawianumY HB 62T28 70 2 – – –
Occultifur externus Y HB 262T23 74 3 – – –
Rhodotorula minuta Y HB 477T25 71 4 – – –
Agaricostilbales
Bensingtonia yuccicola Y HB 419T27 70 1 – 1 –
Kurtzmanomyces nectairei Y HB 106T12 87 0.4 – – –
K. tardus Y HB 268T17 81 2 – – –
Sporobolomyces ruber Y HB 317T14 75 6 – 5 –
S. xanthus Y HB 316T12 83 2 – 3 –
Sterigmatomyces elviae Y HB 104T19 80 1 – – –
St. halophilus Y HB 100T39 61 – – – –
Microbotryomycetidae
Bensingtonia intermedia Y HB 417T15 80 3 – 2 –
Microbotryum salviae Y HB 315 10 59 7 – 24 –
M. succisae Y HB 313 10 45 12 – 33 –
Rhodotorula auriculariae Y HB 413T16 79 1 – 1 3
R. glutinis var. glutinis Y HB 476T14 86 – – tr –
R. glutinis var. glutinis Y HB 462 20 78 1 – 1 –
Uncertain position
Rhodotorula yarrowii Y HB 705T20 58 2 5 2 13
Kriegeria eriophori Y HB 263 22 49 16 – 9 4
Mixia osmundae Y HB 748 33 55 10 – 2 –
M. osmundae Y HB 749 35 55 7 – 2 –
Platygloea disciformis Y HB 267 23 73 1 – 1 –
Y=Yeast stage.

Urediniomycetes
The Urediniomycetes presently comprise four distinct clades: the
Agaricostilbales, the Microbotryales, the Uredinales and the Cystobasidiales.
The Septobasidiales appear as a distinct order within the Uredinales clade. All
four clades are well supported by bootstrap factors close to 100% (fig. 4).
Swann et al. [11] recently introduced the subclass of the Microbotryomycetidae
which includes Heterogastridium pycnidiodeum (fig. 4) and Kriegeria
eriophori (table 1). In contrast to Swann and Taylor [10] and in agreement with
Sjamsuridzal et al. [342], the Cystobasidiales (Nahoidea/Sakaguchia clade)
occupy a basal position in our phylogenetic tree (fig. 4).
Other characters that generally corroborate the Urediniomycetes are the 5S
rRNA secondary structure of type A [236], plate-like spindle pole bodies, the
cell wall monosaccharide pattern (table 1) and simple septa tapering towards
the pore or poreless septa [22, 217, 234, 335, 336, 340, 343–348]. The mem-
bers of this class are predominantly dimorphic except the Uredinales
Systematics of the Ascomycota and Basidiomycota 253
Table 2. Cell wall sugars of dimorphic Basidiomycota which belong to the Ustilaginomycetes
Species Strain Cell wall sugars
GLC MAN GAL XYL FUC RHA
Ustilaginomycetes
Doassansiales
Nannfeldtiomyces sparganii Y HB 304 87 2 11 – – –
Rhamphospora nymphaeae Y HB 405 85 0.7 14 – – –
R. nymphaeae Y HB 406 86 0.4 14 – – –
Exobasidiales
Kordyana cubensisY HB 16 69 19 12 – – –
Ustilaginales
Schizonella sp. nov.Y HB 3 88 5 7 – – –
S. cocconii Y HB 112 93 2 5 – – –
S. melanogramma Y HB 195 87 4 9 – – –
Sporisorium ophiuri Y HB 19 96 2 2 – – –
Sp. reilianum Y HB 303 96 1 3 – – –
Ustilago avenae Y HB 302 71 27 2 – – –
U. bullata Y HB 296 72 25 3 – – –
U. hordei Y HB 297 84 13 3 – – –
YYeast stage.

[5,000–8,000 species; Oberwinkler, pers. commun.] and produce rhodotorulic
acid as siderochrome [349]. The formation of secondary spores (fig. 2) is
common in rust fungi [324]. Teliospores, thick-walled resting spores of the rust
and smut fungi in which karyogamy occurs, are present or absent. Based on
M. osmundae, the Urediniomycetes can be traced back to the Upper
Carboniferous by coevolution and a fossil records of the Osmundaceae
(Discopteris, Todeopteris and Kidstonia) [229].
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 254
Table 3. Cell wall sugars of dimorphic and filamentous Basidiomycota which belong to the
Hymenomycetes
Species Strain Cell wall sugars
GLC MAN GAL XYL FUC RHA
Hymenomycetes
Hymenomycetidae
Polyporus ciliatus M MB 15 83 12 – 5 1 –
Phanerochaete chrysosporium M MB 57 73 13 4 8 2 –
Fomes fomentarius M MB 79 77 13 2 8 – –
Laetiporus sulfureus M MB 80 89 6 – 3 0.7 0.5
Phellinus torulosus M MB 125 87 8 1 3 0.5 0.5
Schizophyllum commune M MB 148 91 9 – – – –
Asterophora parasitica M MB 29 95 4 – 1 –
Clitocybe phyllophila M MB 95 88 6 2 2 1 1
Collybia tuberosa Y Pr 1986/93 97 2 – 1 – –
C. cookei Y Pr 1987/146 94 3 – 2 1 –
Mycena gallopus M MB 140 91 4 – 3 2 –
Pholliota squarrosa M MB 111 88 6 2 4 – –
Lepiotaceae
Y.i. Cyphomyrmex minutus HB 667 98 2 – – – –
Y.i. C. salvini HB 666 97 3 – – – –
Tremellomycetidae
Asterotremella lycoperdoides Y HB 81T83 10 – 6 – –
A. parasitica Y HB 82T85 10 1 4 – –
A. humicola Y CBS 571T84 10 – 3 – –
Atractogloea stillata Y HB 260 91 7 – 3 – –
Captotrema sp.Y HB 259 57 13 4 25 – 1
Christiansenia pallida Y HB 91 62 22 – 12 4 –
Filobasidiella neoformans Y HB 420T82 14 0.5 3 – –
Y.i. Yeast isolate; M mycelium; Y yeast.

Cystobasidiales
Oberwinkler [pers. commun.] suggested to include basidiomycetes which
cluster within the Nahoidea/Sakaguchia or Erythrobasidium clade in the order
Cystobasidiales (fig. 4) [Bauer et al., in preparation, table 1]. Sampaio et al.
[350] call the teleomorphic nature of Erythrobasidium hasegawianum [351]
into question and consider Erythrobasidium as an anamorphic genus. They
interpret the proposed holobasidium as a conidiogenic structure. E. hasegaw-
ianum and Sporobolomyces elongatus are phylogenetically closely related and
so far the only basidiomycetous yeasts that possess a hydrogenated ubiquinone
Q-10 (H2) [24, 351]. This ubiquinone system is common to many filamentous
Euascomycetes [352]. Sexual cycles within the Cystobasidiales differ.
Sakaguchia (Rhodosporidium) dacryoideum produces teliospores that germinate
to a 2- to 4-celled phragmobasidium with repetitively budding basidiospores.
Occultifur externus is a non-teliospore-forming fungus with a yeast stage
that produces auricularioid basidia with ballistospores and physiologically
resembles the anamorphic yeast Rhodotrula minuta [350]. O. internus is an
interesting mycoparasite within fruiting bodies of the Dacrymycetales [353].
R. minuta is a species of clinical importance within the Cystobasidiales.
R. minuta was isolated from bronchoscopy specimens and from postoperative
endophthalmitis [80]. The genus Rhodotorula, however, is heterogeneous and
has representative species at least in three different clades of the Urediniomycetes
(Microbotryum, Sporidiobolus and Erythrobasidium clades) [24]. Genotypic
methods are necessary to identify a Rhodotorula species unequivocally [208].
Microbotryales
The order Microbotryales was proposed by Bauer et al. [335] as ‘phyto-
parasitic members of the Basidiomycota having transversely septate basidia
with multiple production of sessile basidiospores and only intercellular
hyphae’. The order especially comprises phragmobasidial smut fungi from
dicotyledonous host plants (Liroa, Microbotryum, Sphacelotheca and
Zundeliomyces) and phragmobasidial species from monocotyledonous
host plants (Aurantiosporium, Bauerago, Fulvisporium and Ustilentyloma)
[24, 217, 234, 335]. In contrast to the phragmobasidiate members of the
Ustilaginomycetes, they do not produce intracellular hyphae or haustoria [335].
Parasitic species occurring on dicots have poreless septa, whereas parasitic
species on monocots have simple septal pores [335]. Yeast stages from phyto-
parasitic smut fungi of the Microbotryales commonly have a narrower oxydative
degradation spectrum of carbon and nitrogen compounds than yeasts of smuts
from the Ustilaginales [149, 234]. Celerin et al. [354] noted a specific glycosy-
lation pattern that is unique to fimbriae from the Microbotryales. Based on
partial sequences of the 26S rDNA, Colacogloea peniophorae and Kriegeria
Systematics of the Ascomycota and Basidiomycota 255

eriophori as well as Heterogastridium pycnidioideum, which were traditionally
placed among the Platygloeales and Heterogastridiales [355], respectively, and
the basidiomycetous yeasts Leucosporidium, Mastigobasidium, Rhodotorula,
Bensingtonia, Sporobolomyces and Reniforma are closely related to the Micro-
botryales [24]. Presently, it is not clear whether the red pigmented teliosporic
yeasts Rhodosporidium and Sporidiobolus and their related anamorphs in the
genera Rhodotorula and Sporobolomyces form a distinct clade as suggested by
partial sequences of the 26S rDNA (Sporidiobolus clade) [24] or whether they
have to be included in the Microbotryales, which is supported by complete
sequences of the 18S rRNA gene (fig. 4).
Reniforma strues is unique among the basidiomycetous yeasts due to
the presence of kidney-shaped vegetative cells and the presence of ubiquinone
Q-7 [24].
Rhodotorula glutinis is a common saprophyte on various substrates;
disseminated cases in patients with compromised innate immunity do occur.
Sepsis due to the use of indwelling catheters has repeatedly been reported.
The species is also implicated in cases of keratitis and dacryoadenitis [80].
R. mucilaginosa is an additional species of clinical importance [262]. Genotypic
methods are necessary to identify these species unequivocally [208].
Sporidiobolus johnsonii and its anamorph Sporobolomyces holsaticus are
implicated in dermatitis [356]. The species is homothallic and forms simple
holobasidia with diploid basidiospores. Reduction division occurs with the
formation of dikaryotic hyphae with clamp connections [202].
Uredinales
Fungi belonging to the order Uredinales (fig. 4) commonly are referred to
as rust fungi. Approximately 5,000 species belonging to about 140–150 differ-
ent genera which occur on spikemosses (lycophytes), ferns, gymnosperms
and angiosperms are known. They are especially important from the economic
point of view. All are parasitic on plants, often causing great losses to many
cultivated crops [63]. Based on traditional morphological systematics, the
Uredinales were considered for a long time as primitive Basidiomycota [357
and also see ref. 51, 83 and the literature cited therein]. New molecular data,
however, suggest that the Uredinales include many modern and advanced
taxa without yeast/hypha dimorphism, probably arising from simple-septate
primitive auricularioid parasites on mosses and ferns (fig. 4) [342] within the
Urediniomycetes.
Deml et al. [358, 359] and Prillinger et al. [216] isolated many different
tremelloid yeasts specifically from spermogonia of different rust fungi.
To the best of our knowledge, there are no fungi of clinical importance
within the Uredinales.
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 256

Ustilaginomycetes
Although this clade comprises the least species of the three major lineages
of the Basidiomycota based on complete sequences of the 18S rRNA gene
(fig. 4), sufficient data from 5S rRNA [236], cell wall sugars [215, 217, 340]
(table 2), ultrastructure [335, 336], 18S rRNA gene (fig. 4) and partial
sequences of the large subunit rDNA (D1/D2 domain; [22, 24, 360] corroborate
the class of the Ustilaginomycetes. The species are usually dimorphic. Besides
some species pathogenic in humans (Malasseziales), almost all members of the
Ustilaginomycetes are known as phytoparasites. They share type B of 5S rRNA
secondary structure with the Hymenomycetes [236]. In addition, there are
some similarities in spindle pole body morphology with the Hymenomycetes
(fig. 6e, f) [336]. Figure 6e shows a characteristic hemispherical spindle pole
body of U. maydis. The spindle pole bodies of the Ustilaginomycetes roughly
resemble in their form those of the Hymenomycetes, but they have in common
with those of the Urediniomycetes an internal layering. Based on ultrastructural
data and partial sequences of the 26S rDNA there are three major lineages
which can be considered as subclasses: Entorrhizomycetidae, Exobasidio-
mycetidae and Ustilaginomycetidae [22, 335]. Teliospores are present or
absent. Presently, the Entorrhizomycetidae comprise one order: Entorrhizales,
the Ustilaginomycetidae two orders: Urocystales and Ustilaginales, and
the Exobasidiomycetidae seven orders: Malasseziales, Georgefischerales,
Tilletiales, Entylomatales, Microstromatales, Doassansiales, and Exobasidiales
[22, 335, 361]. Complete 18S rDNA sequences are urgently needed to corrob-
orate these orders further.
Except for five species, the host range of the Ustilaginomycetes is restricted
to angiosperms. The lycophytes with species of Selaginella represent the most
primitive host group of the Ustilaginomycetes. A new genus Melaniella with two
species M. oreophila and M. selaginellae was recently described [362]. The
origin of lycophytes can be dated back to the Lower Devonian, about 400 million
years ago [363]. According to Bauer et al. [362], there are two possibilities to
explain the occurrence of Ustilaginomycetes on lycophytes: either it is the result
of a jump, or the Ustilaginomycetes arose as parasites of at least early vascular
plants and the parasitic smut fungi of Selaginella species represent extant
representatives of this ancestral ustilaginomycetous group. Because the
systematically different hosts of the Doassansiales are all paludal or aquatic
plants, Bauer et al. [362] believe the Doassansiales represent a good example for
evolution bound to an ecosystem, but not to a specific host relationship and favor
the jump hypothesis. Exoteliospora (Ustilago) osmundae is another representa-
tive of the Ustilaginomycetes which occur on primitive leptosporangiate ferns
[364]. As already mentioned for Mixia osmundae (Urediniomycetes), the
Systematics of the Ascomycota and Basidiomycota 257

Osmundaceae can be traced back to the Upper Carboniferous. Earlier known
reports of leptosporangiate ferns are in the Lower Carboniferous. Subsequent
major filicalean radiations during the early Mesozoic resulted in several families
with extant representatives, but it was obviously not until the Upper Cretaceous
that much of the extant diversity has appeared [365]. Based on coevolution, the
Urediniomycetes and Ustilagionmycetes appeared as distinct lineages at least
since the Carboniferous.
Species allergenic and pathogenic in humans are known among four orders
within the Ustilaginomycetes; representatives of the Malasseziales are of
special importance.
Malasseziales
The order was introduced by Moore [366]. A separate position of the
different Malassezia species is in agreement with morphological, physiological,
ultrastructural, and molecular characteristics [24, 361]. The cell wall of the
Malassezia yeasts is thick, multilamellate and reveals a unique substructure
with a helicoidal band that corresponds to a helicoidal evagination of the
plasma membrane [367–369]. The lipophilic, dimorphic yeast genus Malassezia
is presently divided into seven different species (M. furfur, M. pachydermatis,
M. sympodialis, M. globosa, M. obtusa, M. restricta, M. slooffiae) [369–371].
Of these, six are strictly lipid dependent with a requirement for long-chain fatty
acid supplementation in the medium to ensure their growth, and one (M. pachy-
dermatis) for which the lipids present in rich media such as Sabouraud glucose
agar are sufficient. Whereas M. pachydermatis is isolated only rarely from
humans, the six lipid-dependent species are commonly found on human skin.
The yeasts are members of the normal human cutaneous flora and can be
cultured from almost all body areas. Under the influence of predisposing fac-
tors they become pathogenic and are associated with several diseases such as
pityriasis versicolor, Malassezia folliculits, seborrheic dermatitis, some forms
of atopic dermatitis, some forms of confluent and reticulate papillomatosis, and
even systemic infection [80, 371]. M. pachydermatis has occasionally been
implicated in cases of systemic infection.
A rapid and inexpensive identification method has been established to
separate the seven species routinely on the basis of morphological and physio-
logical differences [371]. The new taxonomy must be applied to epidemiological
surveys before one can conclude whether all seven Malassezia species have
clinical importance.
Georgefischerales
Species of Tilletiopsis are frequently found as epiphytes on leaves,
especially those infected with powdery mildew or rust fungi [372, 373].
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 258

T. pallescens is a potential biological control agent of Spaerotheca fulginea,
a powdery mildew which is common on cucumber leaves [373]. Among
the Ustilaginomycetes only the Melanotaeniaceae of the Ustilaginomycetidae,
the Georgfischeriaceae and Tilletiariaceae of the Georgefischerales and the
Entylomatales form Tilletiopsis-like pseudohyphal anamorphs that produce
ballistoconidia. This indicates that the genus Tilletiopsis is highly polyphyletic
[24, 361, 374]. T. albescens and T. pallescens are members of the Exobasidio-
mycetidae, but they cannot be assigned to any known order.
T. minor is a member of the Georgefischerales which caused subcutaneous
infection in an immunosuppressed patient [361, 375]. Based on the qualitative
and quantitative monosaccharide pattern of purified cell walls, T. minor fits
well in the Ustilaginomycetes [215].
Microstromatales
The genus Cerinosterus was erected by Moore [376] for basidiomycetous
hyphomycetes previously classified in Sporothrix. This transfer was necessary
because the type species of Sporothrix, S. schenckii, had been shown to be a
member of the euascomycetes order Ophiostomatales [377]. Two species were
accepted in Cerinostereus, with C. luteoalba as the type of the genus [376].
This species is the anamorph of Ditiola pezizaeformis (Femsjonia luteoalba),
which belongs to the Dacrymycetales. The second species, C. cyanescens was
excluded from the Dacrymycetales; 25S rRNA sequencing suggests an affinity
to Microstromatales [378]. Cells which produce conidia sympodially on
denticles, singly or in short chains, therefore can be found at least in four unre-
lated orders of the Ascomycota and Basidiomycota: Stephanoascales
(Hemiascomycetes), Ophiostomatales (Euascomycetes), Microstromatales
(Ustilaginomycetes) and Dacrymycetales (Hymenomycetes). C. cyanescens
has occasionally been isolated from human skin and blood and was involved in
nosocomial infections in patients with pneumonia [80]. Experimental inocula-
tion showed low virulence [379].
Based on partial ribosomal DNA sequencing, Rhodotorula bacarum,
R. hinnulea and R. phylloplana can be excluded from the genus Rhodotorula.
Together with Sympodiomycopsis paphiopedili (fig. 4), they can be included
in the Microstromatales [24]. Presently there are no morphological and ultra-
structural data to circumscribe this order [Oberwinkler, pers. commun.].
Ustilaginales
The genus Ustilago is representative of this order. Ustilago species
are commonly dimorphic phragmobasidial smut fungi parasitic on seeds and
flowers of many cereals and grasses [380]. Smut spores may be inhaled and
therefore may be isolated from sputum specimens. Based on partial sequences
Systematics of the Ascomycota and Basidiomycota 259

of the LSU rDNA, the genus Ustilago is heterogeneous. U. maydis appears to
be distinct from U. hordei, the type species of the genus [22, 24]. Rhodotorula
acheniorum is a candidate for reclassification. It clusters with the Ustilaginales
based on partial sequences of the LSU rDNA [24]. The species of Pseudozyma
are anamorphs of the Ustilaginales [360, 361].
Ustilago tritici is an allergenic species of the Ustilaginales [297].
Hymenomycetes
Representatives of the Hymenomycetes have dolipore septa with various
types of pore caps (without, cupulate, continuous or perforate) [325, 336], their
spindle pole bodies have a true globular morphology lacking obvious internal
differentiation [336]. In addition, they have a type B secondary structure of the
5S rRNA (cluster 5) [236]. A cell wall sugar analysis commonly exhibits dom-
inant amounts of glucose and the presence of xylose (table 3) [216, 217, 340].
Based on sequence analysis of the small subunit rDNA, Swann and Taylor [10]
recommended two subclasses among the Hymenomycetes: (1) the Tremel-
lomycetidae, which are commonly dimorphic and often yeast-like, and (2) the
Hymenomycetidae, containing the non-yeast-like macrofungi including the
mushrooms and puffballs. Nuclear (nuc) rDNA studies all support or are con-
sistent with the view that the classical Homobasidiomycetes plus Auriculariales
s. str., Tualsnellales, and Ceratobasidiales form a monophyletic group (fig. 4)
[337], and that the Tremellomycetidae and Dacrymycetales are at the base of
the hymenomycete lineage. Based on complete sequences of the 18S rDNA
[381], the Tremellomycetidae comprise two distinct orders: the Tremellales and
the Cystofilobasidiales (fig. 4). This is in contrast to partial sequences of the
26S rDNA where Fell et al. [24] accept the Tremellales, the Trichosporonales,
the Filobasidiales and the Cystofilobasidiales (fig. 4). Presently, however, no
ultrastructural data give support to the Filobasidiales and Trichosporonales
[Bauer, unpubl. results]. Takashima and Nakase [381] subdivide the Tremellales
into six different lineages: the Filobasidium lineage, the Trichosporon lineage,
the Cryptococcus luteolus lineage, the Fillobasidiella lineage, the Bulleromyces
lineage and the Sterigmatosporidium lineage. Additional complete 18S rDNA
sequences especially of Tremella species are necessary to clarify systematic
relationships within the Tremellales unequivocally.
The Hymenomycetidae include the Auriculariales as well as all groups
of the classical Homobasidiomycetes. Cantharellus tubaeformis, however,
causes some problems (fig. 4). In a phylogram which is based on combined
nuc-ssu and mt-ssu rDNA sequences, C. tubaeformis clusters together with
Hydnum repandum and Clavulina cristata (Cantharelloid clade) inside the
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 260

Hymenomycetidae [337, 382, 383]. In a phylogenetic tree based on nuc-ssu
rDNA, only C. tubaeformis remains distinct (fig. 4). As discussed by Pine et al.
[383], the rate of sequence evolution of nuc-ssu rDNA appears to be greater in
the cantharelloid clade than in most other Homobasidiomycetes, which makes
it very likely that long branch attraction is responsible for the placement
of C. tubaeformis near the base of the tree. We have observed a similar phe-
nomenon with complete 18S rDNA sequences from Tulasnella pruinosa and
T. violea. We therefore have excluded these sequences from our phylogram
presented in figure 4 Pine et al. [383] present cytological (stichic nuclear
division in basidia) [384] and molecular (combined data for mit-ssu rDNA and
nuc-ssu rDNA) evidence that the Cantharellales (Cantharellus, Craterellus,
Clavulina, Hydnum, Stichoclavaria) are a well-established clade within the
Hymenomycetidae.
Presently, it is not clear whether the Dacrymycetales should be included in
the Hymenomycetidae as suggested by Swann and Taylor [10] or not (fig. 4).
The classical Homobasidiomycetes were tentatively separated into eight major
clades by Hibbett et al. [382] and Hibbett and Thorn [337] based on molecular
data. In accordance with Oberwinkler [186], these clades commonly comprise
resupinate, bracket-like, club-shaped or coralloid, pileate and gasteroid
(secotioid gasteroid and hypogeous gasteroid) fruiting bodies with various
types of hymenia (e.g. corticoid, toothed, poroid, agaricoid, gleba chambers).
Similarly to Oberwinkler [186], we used distinct orders to circumscribe these
clades: Agaricales, Boletales, Cantharellales, Gomphales, Hymenochaetales,
Polyporales, Russulales, Thelephorales. Some of these orders have already been
accepted by Gäumann [385] (Agaricales, Cantharellales, Dacrymycetales,
Polyporales) and Kreisel [386] within his subclass Hymenomycetidae
(Agaricales, Boletales, Cantharellales, Dacrymycetales, Polyporales, Russulales)
but the genera included generally differ remarkably if molecular characters are
used in addition. In contrast to Hibbett et al. [382], the Schizophyllales appear
as an additional distinct group in our phylogram (fig. 4).
The oldest unambiguous homobasidiomycete fossils are from the mid-
Cretaceous, but indirect evidence, including molecular clock dating, suggests
that the higher Hymenomycetes may have existed by the late Triassic (ca. 200
million years) [30, 387].
Tremellales
Cryptococcus neoformans is a zoopathogenic basidiomycetous yeast
which has a teleomorph in Filobasidiella (F. neoformans) but is usually encoun-
tered in the imperfect state [388, 389]. Fell et al. [390] proposed to conserve
Cryptococcus with C. neoformans (Sanfelice) Vuillemin as the neotype species.
Cryptococcosis is an inhalation mycosis, occurring nearly exclusively in
Systematics of the Ascomycota and Basidiomycota 261

immunocompromised patients. Pleural effusion is a first indicator of AIDS.
Dissemination leads to chronic meningitis which is usually fatal when
untreated [80]. Based on genetic recombination in the F1 generation C. neofor-
mans consists of the following two varieties according to the current classifi-
cation: C. neoformans var. neoformans, with serotypes A, D and C. neoformans
var. gattii, with serotypes B, C. According to Boekhout et al. [389], the two vari-
eties differ in karyotype, RAPD-PCR patterns, in a number of physiological
characteristics, morphology of basidiospores, and in sensitivity to killer toxins
of Cryptococcus laurentii. The two varieties also differ in geographic distribu-
tion and habitat. C. neoformans var. neoformans occurs worldwide and is fre-
quently isolated from bird droppings. C. neoformans var. gattii is restricted
to the tropics and the southern hemisphere; it is usually associated with
Eucalyptus species [389]. Differentiation between the two varieties is usually
performed on L-canavanine-glycine-bromthymol blue medium [391, 392] or by
testing D-proline assimilation [393]. Boekhout et al. [389] considered the two
varieties as distinct species, Filobasidiella neoformans and F. bacillispora.
All species of Cryptococcus are nonfermentative aerobes exhibiting a
positive urease test, a positive diazonium blue B test, and the presence of extra-
cellular amyloid compounds. Cryptococcus differs from Trichosporon by the
presence of capsules and the absence of arthroconidia. Genotypic methods are
necessary to identify the species unequivocally [208].
C. laurentii is an additional species of clinical importance (pulmonary
abscess) which belongs to the Tremellales [24, 80, 262, 381]. Based on partial
26S rDNA and complete 18S rDNA sequences, the genus Cryptococcus is
polyphyletic and occurs in at least five different clades of the Tremellales, and
within the Cystofilobasidiales [24, 381] (fig. 4).
Filobasidium (Cryptococcus) uniguttulatum, Cryptococcus albidus, and
C. ater are three species of clinical importance which belong to the Filobasidium
lineage of the Tremellales [24, 262, 381] (fig. 4). The Filobasidium lineage may
be considered as a distinct family (Filobasidiaceae) within the Tremellales.
Although F. uniguttulatum has been isolated from human diseased nails or other
clinical specimens; it has not been documented to cause invasive disease [394].
Cases of meningitis and pulmonary infections have been reported to be caused
by C. albidus [80]. The type strain of C. ater was isolated from multiple ulcers
on the leg of a young man [202].
Species of Trichosporon are characterized by the presence of arthroconi-
dia, positive urease and diazonium blue B tests and the absence of extracellular
amyloid compounds. The septa have dolipores, which may or may not have
tubular/vesicular parenthesomes. Except for T. pullulans, which is a member of
the Cystofilobasidiales (fig. 4), all species form a coherent clade within the
Tremellales, which suggests a distinct family (Trichosporonaceae) [15, 24, 381,
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 262

395, 396]. Genotypic methods are essential to identify a Trichosporon species
unequivocally [208]. There are six Trichosporon species of clinical importance
(T. asahii, T. asteroides, T. cutaneum, T. inkin, T. mucoides, T. ovoides).
T. beigelii is a synonym of T. ovoides [202]. Two strains of Fissuricella
filamenta isolated from human skin showed DNA homology values around
85% with T. asteroides strains [395]. The groups of strains are thus genetically
close, despite the fact that F. filamenta strains were entirely composed of
meristematic cells, while such cells were absent from the strains of T. asteroides
[202]. T. asahii, T. inkin and T. mucoides are regularly isolated from clinical
specimens (white piedra), whereas the remaining species cause only occasional
infections [80, 262].
Cryptococcus humicola was isolated from human skin [262]. It is related to
the genus Trichosporon [24, 381, 397]. Based on 26S rDNA sequencing of the
D1/D2 region, C. humicola differs only by 2 bp from two yeast isolates of the
agarics Asterophora lycoperdoides and A. parasitica [151]. Prillinger et al. [190]
considered these yeast isolates, together with the agarics from which they were
isolated, as sexual symbionts and missing links in the evolution from mycopar-
asitism to sexuality (primary homothallism and heterothallism; fig. 5, 7). Based
on nucleotide divergence of the complete 18S rDNA from C. neoformans, the
type species of the genus Cryptococcus, we have placed the two yeast isolates
from the agarics and C. humicola in the new genus Asterotremella (fig. 4)
[Prillinger et al., in preparation].
Cantharellales
The Cantharellales (fig. 4) include cantharelloid to agaricoid (Cantharellus,
Craterellus), hydnoid (Hydnum), clavarioid to coralloid (Clavulina), clavarioid
(Multiclavula), and corticioid (Botryobasidium) fungi [337]. A distinctive
feature of the Cantharellales is the possession of ‘stichic’ basidia [383, 384].
Analyses of mt-rDNA sequences suggest that the classical heterobasidiomycete
order Tulasnellales belongs in the cantharelloid clade [398]. Based on morpho-
logical and ultrastructural data, Oberwinkler [pers. commun.] has some doubts
on this suggestion. Our alignments of complete 18S rDNA sequences suggests
a higher evolution rate in two Tulasnella species (see above). Except for
Botryobasidium, the species of this group have dolipores with perforate paren-
thosomes [325, 399, 400]. These data suggest that Botryobasidium occupies a
systematic position at the base of this group. Most members of the Cantharel-
lales are known or presumed to be mycorrhizal, but Multiclavula is a basidi-
olichen. Cantharellus cibarius and Craterellus cornucopioides are delicious
edible mushrooms.
Based on molecular data [383], there is no evidence for the ‘Clavaria
theory’ of Corner [401]. Corner [401] treats the cantharelloid and clavarioid
Systematics of the Ascomycota and Basidiomycota 263

fungi as a basal paraphyletic group from which all other Homobasidiomycetes
derived.
Presently, the Cantharellales comprise about 170 described species of
Hymenomycetes.
Gomphales
This order originally was introduced by Jülich [402] based on comparative
morphology and a dark green reaction of the fruiting body plectenchyma when
treated with an aqueous solution of ferric sulfate; however, Jülich does not
include gasteroid genera and families as suggested by Pine et al. [383]. The
Gomphales (fig. 4) [337, 383, 398] include club-shaped fungi (Clavariadelphus),
cantharelloid forms (Gomphus), coralloid fungi (Lentaria, Ramaria), hydnoid
resupinate fungi (Kavinia), gilled mushrooms (Gloeocantharellus), and some
Gasteromycetes (false truffels: Gauteria; earthstars: Geastrum; cannon-ball
fungus: Sphaerobolus; stinkhorns: Clathraceae, Phallaceae). The corticioid
fungus Ramaricium probably also belongs in this group [337].
The gomphoid-phalloid clade includes presently about 350 described
species.
Thelephorales
The thelephoroid clade (fig. 4) [337, 398] is a morphologically diverse
group that includes corticioid fungi (Tomentella), clavarioid forms (Thelephora),
and pileate fruiting bodies with poroid (Boletopsis), toothed (Hydnellum,
Sarcodon), smooth to wrinkled or tuberculate (Thelephora), or lamellate
hymenophores (Lenzitopsis). Oberwinkler [186] suggested that the agaricoid
fungus Verrucospora is related to the Thelephorales based on spore morphology.
Characters used by Donk [403] to support the Thelephoraceae include dark,
ornamented spores with an angular outline, pigmentation of the fruiting body,
and the presence of thelephoric acid [404]. Thelephoric acid, which is a
terphenylquinone product of the shikimate-chorismate pathway is found in
Bankera, Boletopsis, Hydnellum, Phellodon, Polyozellus, Pseudotomentella,
Sarcodon and Thelephora. This is consistent with molecular characters, which
strongly support monophyly of the Thelephorales. Nevertheless, thelephoric
acid also occurs in Suillus and Rhizopogon (Boletales), Omphalotus and
Lampteromyces (Agaricales) and Trametes (Polyporales) [337].
All members of this group are thought to be ectomycorrhizal or orchid
symbionts [398]. The phylogenetic relationship to the Bankeraceae (Phellodon)
awaits further molecular studies. So far only dolipores with perforate parenthe-
somes are known in the Thelephorales [399, 400].
The Thelephorales presently include about 240 described species of
Hymenomycetes.
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 264

Polyporales
The polyporoid clade (fig. 4) [337, 382] is primarily composed of corticioid
fungi and polypores, but also includes the gilled mushrooms Lentinus, Panus
and Faerberia as well as the ‘cauliflower fungus’ Sparassis. The brown rot root
parasite Sparassis spathulata appears to be phylogenetically related to the brown
rot polypores Laetiporus sulphureus, Phaeolus schweinitzii and Antrodia car-
bonica [337]. The phylogenetic relationship of the brown rot genera
Gloeophyllum and Neolentinus (Lentinus lepideus) to this clade (fig. 4) [337], is
presently not clear, however. Although the polyporoid clade as a whole is weakly
supported, there are four groups within the polyporoid clade that are strongly
supported and have corroborating anatomical and physiological characters.
They may be candidates for a new family delimitation (Fomitopsis-Daedalea
Piptoporus: brown rot, unifactorial mating system; Fomes Polyporus-Lentinus-
Ganoderma: white rot, bifactorial mating system; Bjerkandera-Phanerochaete-
Ceriporia-Phlebia: white rot; Antrodia-Phaeolus-Laetiporus-Sparassis: brown
rot) [405]. Dolipores with perforate parenthosomes are common in the
Polyporales [406, 407]; Phanerochaete so far is the only genus having imperfo-
rate parenthesomes [400]. A perforate parenthesome, however, was found in
Phanerochaete cremea [Bauer, unpubl. obs.]. Dimitic or trimitic hyphal systems
and hyphal pegs, fascicles of sterile hyphae that emerge from the hymenium are
common anatomical characters in the Polyporales [186].
Haploid apomixis was considered to be an extreme type of homothallic
breeding systems [41, 55, 83, 94], and its occurrence in the Basidiomycota in
nature was reviewed by Prillinger [93]. Using Polyporus ciliatus, we were able,
after eight inbreeding generations, to obtain isogenic strains which develop
fertile apomictic pileate fruiting bodies which could be distinguished from the
dikaryotic fruiting bodies only by microscopical investigations [103]. After 2
years of apomictic propagation, a Phlebia-like resupinate mutant (corticioid
morphology) appeared on a petri dish inoculated with one of these haploid-
apomictic pileate strains (fig. 11a). The Phlebia-like mutant exhibited a fertile
and predominantly bisporic apomictic hymenium, but it had still not lost its
mating capacity. It was therefore easy to obtain the three additional mating types
of the resupinate mutant by crossing with a compatible pileate strain
(fig. 11a). P. ciliatus is a complex hetero-bifactorial white rot fungus (fig. 5).
Compatible crosses of two resupinate strains yielded a morphologically similar
Phlebia-like dikaryotic strain, which, in contrast to the haploid-apomictic
strains, microscopically exhibited a clamped mycelium and predominantly
four-spored basidia (fig. 11b) [94]. This result clearly confirmed the polygenic
control of fruit body formation suggested by Prillinger and Six [103] and
excluded the existence of a ‘fruiting initiation gene’ which was postulated by
Esser et al. [408]. A genetic analysis of 200 haploid single-spore cultures of a
Systematics of the Ascomycota and Basidiomycota 265

cross of resupinate with pileate strains yielded a clear-cut 1:1 (95:92) segrega-
tion pattern (table 4), indicating a typically monogenic character. In view of this
monogenic difference between resupinate and pileate strains with a corticoid and
poroid hymenium, respectively, these resupinate fruiting bodies can be inter-
preted as atavistic only [94]. Our data are in favor of a concept of Oberwinkler
[186] which suggests that the different fruiting bodies of the classical
Homobasidiomycetes have evolved repeatedly from morphologically simple
resupinate ancestors. Different types of haploid fruiting bodies (resupinate,
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 266
a b
Fig. 11. A Phlebia-like resupinate monogenic mutant of Polyporus ciliatus. The
resupinate mutant appeared in a culture of a haploid pileate fruiter strain after 2 years of
apomictic propagation. aDifferent mating types of the resupinate mutant were obtained from
a cross between the resupinate haploid mutant and a pileate haploid fruiter strain (bottom);
from the dikaryon (top) it is obvious that the resupinate mutant behaves as a recessive gene.
bA dikaryotic resupinate strain was obtained (top) in a cross of two compatible haploid
resupinate strains. For additional information, see Prillinger [94] and text.
Table 4. A monogenic fertile resupinate mutant of Polyporus ciliatus
Dikaryotic cross Spores Haploid progeny
Resupinate haploid number germinated resupinate haploid
fruiting bodies fruiting bodies
A1B1A2B250 49 21 28
A1B2A2B150 45 22 21
A2B1A1B250 48 28 20
A2B2A1B150 47 24 23
Total 200 189 95 92

clavarioid, coralloid, pileate) detected in single-spore cultures of P. ciliatus are a
valuable tool to trace the phylogeny of the Polyporales (fig. 6a) [103].
Within Lentinus tigrinus (fig. 4) Rosinski and Robinson [409] detected
complete intercompatibility between monokaryotic isolates of the pileate
L. tigrinus and the gasteromycete Lentodium squamulosum. They accept
Le. squamulosum as a recessive mutant of L. tigrinus and recognized it as a
variety.
The polyporoid clade contains roughly 1,350 described species of the
Hymenomycetes, including about 90% of the morphologically described
Polyporaceae and 25% of the Corticiaceae, as well as all Ganodermataceae and
Sparassidaceae [337].
Ganoderma applanatum, G. lucidum and G. meredithae are known to
cause allergy in humans [81]. Anamorphs of polypores and corticoid fungi are
encountered with increasing frequency in clinical mycology. Identification to
species has been problematic, especially in the case of haploid monokaryons
[410]. Molecular techniques like ribosomal DNA sequencing may faciliate the
identification of filamentous haploid Hymenomycetes in the future.
Bjerkandera adusta is one of the most common Hymenomycetes isolated in
North America from sputum, skin, urine and air [410]. Other Polyporales
(Phlebia rufa, Phanerochaete chrysosporium, anamorph: Sporotrichum
pruinosum) are rarely isolated from human sputum [410].
Hymenochaetales
The order Hymenochaetales (fig. 4) was introduced by Oberwinkler
[186] and corroborated by Hibbett and Thorn [337] by molecular data. The
Hymenochaetales comprise the classical Hymenochaetaceae and some addi-
tional genera morphologically placed in the Corticiaceae (Basidioradulum,
Hyphodontia) and Polyporaceae (Trichaptum, Oxyporus, Schizopora). Thus, the
Hymenochaetales include resupinate and bracket-like poroid, toothed, and
corticoid forms. In addition, the clavarioid Clavariachaete belongs to the
Hymenochaetales, based on anatomical features [186]. Based on the following
characters the Hymenochaetaceae have been considered monophyletic:
clampless generative hyphae, fruiting bodies darkening in KOH, production of
white rot, presence of thick-walled tapering cystidia (setae). In addition, most
members of the Hymenochaetales have been shown to have imperforate paren-
thosomes (Basidioradulum, Hyphodontia, Inonotus, Phellinus, Schizopora,
Trichaptum) [325, 411–413]. Coltricia is a remarkable exception having
perforate parenthesomes and being the only ectomycorrhizal member of the
Hymenochaetales [406]. In our phylogram (fig. 4), Schizopora paradoxa
clusters outside the Hymenochaetales. In a phylogram of combined data for
mit-ssu rDNA and nuc-ssu rDNA, S. paradoxa is within the Hymenochaetales
Systematics of the Ascomycota and Basidiomycota 267

[337, 382]. Presently, there are no morphological-anatomical data to include
Basidioradulum, Hyphodontia, Oxyporus, Schizopora and Trichaptum in the
Hymenochaetales [Oberwinkler, pers. commun.].
The Hymenochaetales presently include about 630 described species of
Hymenomycetes.
Russulales
Based on comparative anatomy and morphology, Oberwinkler [186] rede-
fined the Russulales and discussed older concepts of this order. The russuloid
clade has a remarkable diversity of fruiting body morphologies (fig. 4)
[337, 382]. There are resupinate (Stereum), coralloid (Clavicorona), and pileate
(Russula) forms with smooth (Stereum), toothed (Hericium), lamellate
(Lentinellus, Russula), or poroid hymenophores (Bondarzewia). Gasteroid forms
are also common (e.g. Martellia, Macowanites, Zelleromyces). The russuloid
clade is also ecologically variable, having ectomycorrhizal (Lactarius,
Russula), parasitic (Heterobasidion), saprophytic (Auriscalpium, Stereum) and
possibly lichenized (Pleurogala igapoensis) [414] species. Heterobasidion
annosum (fig. 4) is one of the most important root pathogens in European
spruce forests [415]. Species of Hericeum occur as parasites (H. erinaceus) and
saprophytes (H. clathroides) and cause a white rot. As discussed by Donk [403]
and Oberwinkler [186], many members of the Russulales have spores with amy-
loid ornamentations and gloeoplerous cystidia or hyphae, but these characters are
variable within the group. Hibbett and Thorn [337] estimate that the russuloid
clade contains approximately 1,000 described species of Hymenomycetes,
including roughly 20% of the morphologically described Corticiaceae.
Lactarius deliciosus and Russula cyanoxantha are well known delicious,
edible mushrooms.
Boletales
The history and concept of the Boletales is extensively discussed in Bresinsky
[64]. The delimitation of the order is based on morphological (spindle-shaped
basidiospores), chemical (pigments: shikimate-chorismate pathway derivatives),
wood decay (brown rot), specific mycoparasites (Sepedonium) and more recently
and better reliable on molecular data [382, 398, 416–421]. Based on a sequence
database of the mitochondrial large subunit rRNA gene, Bruns et al. [398] divided
the Boletales into six groups. Complete 18S nuclear ribosomal DNA sequences
and additional species may be useful to corroborate this groups at the family
level: group 1 (Boletaceae): Boletus, Chamonixia, Gastroboletus, Leccinum,
Strobilomyces, Tylopilus, Xerocomus; within group 1 the genera Boletus and
Xerocomus appeared to be heterogeneous; group 2 (Paxillaceae): Chalciporus,
Paxillus s. str., Paragyrodon; group 3 (Tapinellaceae): Hygrophoropsis, Serpula,
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 268

Tapinella; group 4 (Coniophoraceae): Coniophora; group 5 (Gyrodonaceae):
Gyrodon, Gyroporus, Phaeogyroporus, Pisolithus; group 6 (Suillaceae): Alpova,
Brauniellula, Chroogomphus, Gomphidius, Hymenogaster, Melanogaster,
Rhizopogon.
The bolete clade contains resupinate fungi (Coniophora, Serpula), can-
tharelloid forms (Hygrophoropsis), gilled mushrooms (Gomphidius, Paxillus,
Tapinella), false truffels (Alpova, Hymenogaster, Melanogaster, Rhizopogon),
secotioid fungi (Brauniellula, Chamonixia, Gastroboletus, Gastrosuillus), and
puffballs (Pisolithus, Scleroderma), including the unusual stalked, gelatinous
puffball Calostoma [337].
The shikimate-chorismate pathway produces a number of compounds that
are characteristic of the Boletales (atrotomentin, pulvinic acid derivatives,
cyclopentanoids, polyprenylquinones). These compounds have been found in
diverse corticoid, resupinate, cantharelloid, lamellate, boletoid, and gasteroid taxa
including Boletus, Chamonixia, Chroogomphus, Coniophora, Gomphidius,
Gyrodon, Hygrophoropsis, Leucogyrophana, Paxillus, Phylloporus, Pisolithus,
Rhizopogon, Scleroderma, Serpula, Suillus, and some others [422]. Atrotomentin,
pulvinic acid derivatives, and cyclopentanoids have also been found in the ligni-
colous white rot agarics Omphalotus and Lampteromyces [423]. However, analy-
ses of rDNA sequences suggest that Omphalotus and Lampteromyces belong to a
distinct family Omphalotaceae within the Agaricales [421]. In addition, atroto-
mentin and cyclopentanoids are found outside the Boletales in Albatrellus,
a heterogeneous genus within the Polyporales and Russulales [337, 398] and
Hydnellum (Thelephorales). These observations imply that the production of atro-
tomentin, pulvinic acid derivatives, and cyclopentanoids has evolved repeatedly.
The Boletales presently include about 840 described species of
Hymenomycetes. Many species of the Boletales are known as tasty (Boletus
edulis, Xerocomus badius) and a few as poisonous (B. satanas, Paxillus involutus).
P. involutus caused immunohemolytic anemia after repeated consumption of its
carpophores. Bresinsky and Besl [424] present an extensive documentation of
poisonous mushrooms and fungal intoxications. Jarosch and Bresinsky [425]
investigated the problem of speciation and cryptic species in P. involutus. Boletus
species and Serpula lacrymans are known as allergenic fungi [297, 426, this vol-
ume]. The brown-rot fungus S. lacrymans is primarily important in Europe, where
the dreaded dry rot causes tremendous damage to wooden structural elements and
floors in houses and other buildings.
Schizophyllales
Different from the combined analysis of nuc-ssu and mt-ssu rDNA of
Hibbett et al. [382] and Hibbett and Thorn [337] Fistulina hepatica and
Schizophyllum commune form a distinct clade with high bootstrap support,
Systematics of the Ascomycota and Basidiomycota 269

closely related to the Agaricales in our phylograms of complete 18S nuc-DNA
and partial sequences of the 26S rDNA (fig. 4) [Schweigkofler unpubl.].
We tentatively use the order Schizophyllales originally suggested by Nuss [427]
based on comparative morphology for this clade. Additional sequences,
especially from cyphelloid fungi may be useful to corroborate or reject this order.
S. commune is probably the best-known basidiomycetous agent of infec-
tion. Reports involving the lung include fungus ball of the lung [428], a case of
allergic bronchopulmonary mycosis in an otherwise healthy female [429] and
repeated isolation of S. commune from the sputum of a patient with chronic
lung disease [430]. Other reports of S. commune infections include cases of
meningitis [431], sinusitis [432–434], ulcerative lesions of the hard palate
[435], and possible onychomycosis [436] in both immunocompetent and
immunosuppressed hosts. The presence of clamp connections on dikaryotic
hyphae and the development of fruiting bodies in culture are primary charac-
ters which allow the identification of S. commune in human infections. The
diagnostic problems presented by a monokaryotic nonclamped, nonfruiting iso-
late from a dense mass in the right upper lobe of the lung in a female with a past
history of pulmonary tuberculosis and diabetes are described and discussed by
Sigler et al. [428]. Genotypic identification methods like partial sequencing of
ribosomal DNAs [16] are a promising tool to solve these problems in the future.
Agaricales
The Agaricales sensu Fries have long been recognized as an artificial
taxon, but the number of independent evolutionary lines of gilled mushrooms,
and their order relationships, have remained controversial [186, 402, 437, 438].
In a molecular analysis Hibbett et al. [382] suggest that agaricoid forms evolved
at least six times independently within the Hymenomycetes. Our present under-
standing of the phylogeny of the Hymenomycetes is only partially consistent
with Corner’s [401] ‘Clavaria theory’; agarics are polyphyletic, but there is
no indication that they have all derived from paraphyletic grades of club and
coral fungi. The molecular data of Hibbett et al. [382] and Hibbett and Thorn
[337] agree well with a phylogenetic concept of Oberwinkler [186] and genetic
experiments (table 4, fig. 11) of Prillinger [94] which suggest that the agarics
have evolved polyphyletically from morphologically simple corticioid or
resupinate ancestors.
The Agaricales contain the majority of the gilled mushrooms in the
Agaricales sensu Singer [438]. The largest groups of gilled mushrooms outside
the Agaricales are Lentinus (Polyporales), Lactarius, Russula (Russulales),
Gomphidius, Paxillus, Tapinella (Boletales). Although the pigments of
Lampteromyces, Omphalotus and Ripartites point to a Boletales affinity, these
species were included in the Agaricales by Binder et al. [421] based on ribosomal
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 270

DNA sequencing. Pegler [439] restricted Lentinus to dimitic species, and there-
fore, transferred the monomitic shiitake fungus, traditionally known as Lentinus
edodes, into Lentinula which is close to Collybia within the Agaricales [440,
441]. In addition, ribosomal DNA sequence information suggests that species
of the clavarioid genera Clavaria, Clavulinopsis and Typhula belong to the
Agaricales too [382, 383]. Whereas Hibbett and Thorn [337] present evidence
to include at least some representatives of the Ceratobasidiales in the Agaricales,
data from Lee and Jung [442] and our investigations (Rhizoctonia solani;
fig. 4), however, are not in agreement with this suggestion and warrant further
investigations.
Classical Gasteromycetes that have been sampled in the Agaricales include
bird’s nest fungi, puffballs and many secotioid fungi. Lycoperdon, Calvatia, and
Tulostoma form a weakly supported monophyletic group within the Agaricales
which is phylogenetically closely related to Lepiota procera [382]. The exact
placement of the bird’s nest fungi (Nidulariaceae) is not resolved with
confidence [382]. Further gasteroid species or genera which have been studied
include Hydnangium (H. carneum, H. sublamellatum, H. microsporium),
Podohydnangium sp. which is closely related to Laccaria (L. bicolor, L. oblon-
gospora, L. laccata, L. trullisata, L. gomezii, L. vinaceobrunnea, L. glabripes,
L. proximella), Montagnea arenaria and Podaxis pistillaris, which are closely
related to Coprinus comatus (Coprinus appeared to be heterogeneous) and
Leratia and Weraroa, which show affinities to Stropharia [422, 443, 444].
According to Hibbett and Thorn [337], the Agaricales contain approxi-
mately 7,400 species of gilled fungi and 1,025 species of the classical Aphyl-
lophorales and Gasteromycetes. These species represent more than half of
all known classical Homobasidiomycetes, including approximately 87% of
all known gilled mushrooms [175]. Although symbionts of plants (mycor-
rhizae: Amanita, Cortinarius, Hebeloma, Inocybe) dominate, symbionts of ani-
mals (Amylostereum, Termitomyces), saprotrophs (Agaricus bisporus,
Pleurotus ostreatus, Lentinula edodes), pathogens (Armillaria mellea,
Crinipellis perniciosa, Mycena citricolor, Oudemansiella mucida, Pholiota
aurivella), and mycoparasites (Asterophora lycoperdoides) can be found as
well [337].
Agaricus bisporus, Calvatia cyathiformis, Coprinus comatus, C. quadri-
fidus, Lentinula edodes, Pleurotus ostreatus, Psilocybe cubensis are known
allergenic fungi [81, 426, this volume]. Psilocybe mexicana and other related
species have been referred to collectively as the ‘sacred or divine mushrooms’
or ‘teonanácatl’ used for centuries in certain religious rites of endemic peoples
of Mexico. The halucinogenic compounds present in these fungi were first isolated
and identified by Hofmann et al. [445] and named psilocin and psilocybin. The
hallucinogenic properties of both compounds are similar to d-lysergic acid
Systematics of the Ascomycota and Basidiomycota 271

diethylamide (LSD). They are extensively discussed in Bresinsky and Besl
[425] and Alexopoulos et al. [63].
Phylogenetic analyses of partial sequences from nuclear 26S rDNA
indicate monophyletic Pleurotaceae, consisting of the monophyletic genera
Pleurotus and Hohenbuehelia. The attack and consumption of nematodes
(nematophagy) support the monophyly of this family [441].
Agaricus campestris, Amanita caesarea, Coprinus comatus, Macrolepiota
procera, Marasmius scorodonius, Pholiota mutabilis and Rozites caperata are
well-known edible mushrooms. Bresinsky and Besl [424] present an overview
of many poisonous species (e.g. Amanita muscaria, A. phalloides, Cortinarius
orellanus, Inocybe patouillardi, Lampteromyces japonicus, Omphalotus
olearius) and different fungal intoxications.
Genotypic Identification
A number of fingerprinting methods based on the analysis of genomic
DNA polymorphism have been developed in the last decades for genotypic
species identification and delimitation. In our laboratory, we use two tech-
niques successfully. RAPD-PCR is a simple and highly specific method. It was
introduced independently by Welsh and McClelland [446] and Williams et al.
[447]. We used RAPD-PCR to separate different species of yeasts like Mrakia
and Sterigmatomyces [340], Kluyveromyces [448], Metschnikowia [449],
Saccharomyces [450, 451], to identify known and new species of yeasts from
nature [148, 452], and to identify or describe new species of filamentous micro-
fungi (Fusarium [281]; Ophiostoma [293]; Verticillium [290]; endophytic fungi
from grapevine [16, 305]). Rapid DNA extraction without digestion or removal
of RNA yields the template for RAPD analysis, which is routinely used to
determine the concentration of chromosomal DNA and the DNA to RNA ratio
on the basis of the intensities of ethidium-bromide-stained bands. Since the
amplification reaction for RAPD analysis cannot be completely standardized,
the absolute numbers and sizes of the fragments formed are by themselves not
significant markers for strain differentiation. Therefore, all of the strains that
are to be compared must be processed with one stock solution of premixed
reagents in one run of the thermocycler used and loaded onto one gel for max-
imum information output [340].
Amplified fragment length polymorphism (AFLP), developed by Vos et al.
[453], is also a new technique for DNA fingerprinting. This technique is based
on the selective amplification of restriction fragments (SARE) by PCR from a
digest of total genomic DNA.
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 272

AFLP involves four steps: (a) restriction enzymes digestion; (b) ligation of
adapters to the restriction fragments; (c) PCR amplification of the restriction/
ligation fragments, and (d) detection and analysis of the amplified fragments.
The restriction fragments are generated by two restriction enzymes, one of
them is a rarely cutting one and the other is a frequently cutting one. Specific
adapters are ligated to the restriction fragments at the temperature at which
restriction enzymes are still active to avoid concatamer formation of the restric-
tion fragments. Two different adapters are used, one specific for the rare cutting
enzyme and one specific for the frequent cutting enzyme. After ligation of the
adapters, the fragments have appropriate attachment sites for the selective PCR
primers. One of the two primers used is labeled (by isotopes or fluorescently).
Amplified fragments are detected according to the labeling technique.
Automatic laser fluorescence analysis (ALFA) [454] provides an automated
detection and analysis of fluorescently labeled samples.
The AFLP has the power of PCR and the solidity of RFLP analysis.
As the AFLP is highly reproducible and has a deep enough resolution due to
the number of estimable detected fragments; this technique allows us to analyze
the strains at the intraspecies level. With this technique we can carry out
epidemiological studies or can generate a database for routine identification.
We proved that its application is very useful in the determination of the route of
an infection or in the correct identification of pathogenic yeasts.
Figure 12 shows a digital electrophoresis image of ALFA-AFLP fragments
of Candida guilliermondii and C. glabrata strains, run on an automatic DNA
sequencer. A high degree of similarity can be clearly recognized among the
strains belonging to the same species. They share several (supposedly species-
specific) bands in the same position, while differentiation of some of the isolates
can be performed according to the noncommon fragments. Completely identical
patterns can be seen, e.g. lanes 12 and 13, indicating that these isolates are prob-
ably in epidemiological relation. Proof of the identity, however, requires the
performance of AFLP by an additional adapter and primer set. Separation of the
isolates belonging to the two different species is clear by a simple visual evalu-
ation of the patterns.
Recently we have shown that it is not possible to identify ascomycetous
and basidiomycetous yeasts unequivocally using the classical phenotypic
approach [208]. The score of correct identification using the phenotypic
approach is rather low especially in basidiomycetous yeasts. Partial sequences
of the 18S and 26S rDNA have become a reliable tool to identify yeast species
correctly [148, 452]. Meanwhile, partial sequences of the D1/D2 region of the
large subunit rDNA are available for all known ascomycetous [23] and basid-
iomycetous [24] yeasts in GenBank. This offers the possibility of a reliable
genotypic identification using the D1/D2 region. According to our experience
Systematics of the Ascomycota and Basidiomycota 273

Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 274
1 2 3 4 5 6 7 12 13 16 25 34
Fig. 12. Digital electrophoresis image of AFLP fragments of Candida strains run on
an automatic DNA sequencer. Markers: lanes 1, 16, 25, 34; Candida guilliermondii: clinical
isolates, lanes 2–6; Candida glabrata: type strain CBS 138 lane 7, clinical isolates: others.
it seems worthwhile to corroborate the identification data obtained with a
RAPD-PCR analysis with the respective type strain.
For the identification of new yeast species from nature we use a new
polyphasic approach [452]: (1) Species delimitation using RAPD-PCR or

AFLP; (2) Species identification using partial sequences of the 18S or 26S
rDNA and corroboration of the identification data using RAPD-PCR and the
respective type strain; (3) Ubiquinone system according to Messner et al. [340],
and (4) Qualitative and quantitative monosaccharide pattern of purified and
hydrolyzed cell walls [449].
Just as for the identification of yeasts, partial sequences of the 18S and 26S
rDNA are also useful for identifying filamentous microfungi. In contrast to
yeasts, however, reliable identification [16] is not always possible due to a lack
of sequences in Genbank.
Acknowledgments
We would like to thank Dr. D. Begerow, Dr. T. Boekhout, Prof. M. Breitenbach,
Dr. T.D. Bruns, Emeritus Prof. F. Ehrendorfer, Prof. O.E. Eriksson, Emeritus Prof. K. Esser,
Prof. J.W. Fell, Dr. M. Fischer, Emeritus Prof. W. Gams, Mag. G. Hagedorn, Dr. M.
Hamamoto, Dr. D.S. Hibbett, Dr. G. Himmler, Prof. G.S. de Hoog, Dr. P. Hoffmann, Dr. J.
Kämper, Prof. C. Kubicek, Dr. U. Kües, Dr. C.P. Kurtzman, Dr. S. Landvik, Dr. J. Loidl,
Prof. M. Melkonian, DI. Dr. R. Messner, Prof. U.G. Mueller, Dr. T. Nakase, Prof. L. Sigler,
Emeritus Prof. J. Sugiyama, Dr. M. Suzuki, Dr. E. Swann, Emeritus Prof. Y. Yamada for
sending interesting strains, valuable literature, critical comments or unpublished sequences.
My wife J. Prillinger and Ms. I. Mondl improved figures 2, 6 and 7. Ing. S. Huss prepared
a CD version of all figures. Prof. G.S. de Hoog informed the first author that his excellent
Atlas of Clinical Fungi is scheduled in a new, fully revised and greatly expanded edition for
early 2000.
Finally the first author is grateful to Prof. F. Oberwinkler of the University Tübingen
for his excellent introduction into mycology, sending interesting strains and many valuable
comments on the manuscript.
References
1 Zuckerkandl E, Pauling L: Molecules as documents of evolutionary history. J Theor Biol 1965;8:
357–366.
2 Woese CR: Bacterial evolution. Microbiol Rev 1987;51:221–271.
3 Sogin ML, Morrison HG, Hinkle G, Silberman JD: Ancestral relationships of the major eukaryotic
lineages. Microbiologia 1996;12:17–28.
4 Haeckel E: Systematische Phylogenie der Protisten und Pflanzen. Berlin, Reimer, 1894.
5 Kimura M: Evolutionary rate at the molecular level. Nature 1968;217:624–626.
6 Kimura M: A simple method for estimating evolutionary rates of base substitutions through
comparative studies of nucleotide sequences. J Mol Evol 1980;16:111–120.
7 Kimura M: The Neutral Theory of Molecular Evolution. Cambridge, Cambridge University Press,
1983.
8 Sogin ML, Gunderson JH, Elwood HJ, Alonso RA, Peattie DA: Phylogenetic significance of the
Kingdom concept: An unusual eukaryotic 16S-like ribosomal RNA from Giardia lamblia. Science
1989;243:75–77.
Systematics of the Ascomycota and Basidiomycota 275

9 Bhattacharya D, Elwood HJ, Goff LJ, Sogin ML: Phylogeny of Gracilaria lemaneiformis
(Rhodophyta) based on sequence analysis of its small subunit ribosomal RNA coding region.
J Phycol 1990;26:181–186.
10 Swann EC, Taylor JW: Phylogenetic diversity of yeast-producing basidiomycetes. Mycol Res
1995;99:1205–1210.
11 Swann EC, Frieders EM, McLaughlin DJ: Microbotryum, Kriegeria and the changing paradigm
in basidiomycete classification. Mycologia 1999;91:51–66.
12 Suh S-O, Nakase T: Phylogenetic analysis of the ballistosporous anamorphic genera Udenomyces
and Bullera, and related basidiomycetous yeasts, based on 18S rDNA sequence. Microbiology
1995;141:901–906.
13 Melkonian M: Phylogeny of photosynthetic protists and their plastids. Verh Dtsch Zool Ges
1996;89:71–96.
14 Sugiyama J: Relatedness, phylogeny, and evolution of the fungi. Mycoscience 1998;39:487–511.
15 Sugita T, Nakase T: Trichosporon japonicum sp. nov. isolated from the air. Int J Syst Bacteriol
1998;48:1425–1429.
16 Schweigkofler W, Prillinger H: Molekulare Identif izierung und phylogenetische Analyse von
endophytischen und latent pathogenen Pilzen der Weinrebe. Mitt Klosterneuburg 1999;49:65–78.
17 Yamada Y, Kawasaki H, Nagatsuka Y, Mikata K: The phylogeny of the cactophilic yeasts based on
the 18S ribosomal RNA gene sequences: The proposals of Phaffomyces antillensis and Starmera
caribaea, new combinations. Biosci Biotechnol Biochem 1999;63:827–832.
18 Perasso R, Baroin A, Qu LH, Bachellerie JP, Adoutte A: Origin of the algae. Nature 1989;339:
142–144.
19 Yamada Y, Nagahama T, Kawasaki H, Banno I: The phylogenetic relationships of the genera
Phaffia Miller, Yoneyama et Soneda and Cryptococcus Kützing emend. Phaff et Spencer
(Cryptococcaceae) based on the partial sequences of 18S and 26S ribosomal ribonucleic acids.
J Gen Appl Microbiol 1990;36:403–414.
20 Yamada Y, Higashi T, Mikata K: The phylogeny of species of the ascogenous telemorphic yeast
genera Ambrosiozyma, Hormoascus, Hyphopichia, Arthroascus, and Botryoascus based on the
partial sequences of 18S and 26S ribosomal RNAs. Bull Fac Agric Shizuoka Univ 1998;48:1–13.
21 Messner R, Prillinger H, Ibl M, Himmler G: Sequences of ribosomal genes and internal tran-
scribed spacers move three plant parasitic fungi, Eremothecium ashbyi, Ashbya gossypii, and
Nematospora coryli, towards Saccharomyces cerevisiae. J Gen Appl Microbiol 1995;41:31–42.
22 Begerow D, Bauer R, Oberwinkler F: Phylogenetic studies on nuclear large subunit ribosomal
DNA sequences of smut fungi and related taxa. Can J Bot 1997;75:2045–2056.
23 Kurtzman CP, Robnett CJ: Identification and phylogeny of ascomycetous yeasts from analysis of
nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie Van Leeuwenhoek 1998;
73:331–371.
24 Fell JW, Boekhout T, Fonseca A, Scorzetti G, Statzell-Tallman A: Biodiversity and systematics of
basidiomycetous yeasts as determined by large-subunit rDNA D1/D2 domain sequence analysis.
Int J Syst Evol Microbiol 2000;50:1351–1371.
25 Walker WF: 5S ribosomal RNA sequences from Ascomycetes and evolutionary implications.
Syst Appl Microbiol 1985;6:48–53.
26 Blanz PA, Unseld M: Ribosomal RNA as a taxonomic tool in mycology. Stud Mycol
1987;30:247–258.
27 Baldauf SL, Doolittle WF: Origin and evolution of the slime molds (Mycetozoa). Proc Natl Acad
Sci USA 1997;94:12007–12012.
28 Doolittle WF: Phylogenetic classification and the universal tree. Science 1999;284:2124–2128.
29 Bruns TD, Vilgalys R, Barns SM, Gonzalez D, Hibbett DS, Lane DJ, Simon L, Stickel S, Szaro
TM, Weisburg WG, Sogin ML: Evolutionary relationships within the fungi: Analyses of nuclear
small subunit rRNA sequences. Mol Phylogenet Evol 1992;1:231–241.
30 Berbee ML, Taylor JW: Dating the evolutionary radiations of the true fungi. Can J Bot 1993;71:
1114–1127.
31 Bresinsky A, Kadereit JW: Systematik-Poster Botanik. Stuttgart, Fischer, 1998.
32 Woese CR, Kandler O, Wheelis M: Towards a natural system of organisms: Proposal for the
domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 1990;87:4576–4579.
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 276

33 Knoll AH: The early evolution of eukaryotes: A geological perspective. Science 1992;256:
622–627.
34 Gogarten JP, Kibak H, Dittrich P, Taiz L, Bowman EJ, Bowman BJ, Manolson MF, Poole RJ, Date
T, Oshima T, Konishi J, Denda K, Yoshida M: Evolution of the vacuolar H-ATPase: Implications
for the origin of eukaryotes. Proc Natl Acad Sci USA 1989;86:6661–6665.
35 Iwabe N, Kuma K-I, Hasegawa M, Osawa S, Miyata T: Evolutionary relationship of archaebacte-
ria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc Natl
Acad Sci USA 1989;86:9355–9359.
36 Vossbrinck CR, Maddox JV, Friedman S, Debrunner-Vossbrinck BA, Woese CR: Ribosomal RNA
sequence suggests microsporidia are extremely ancient eukaryotes. Nature 1987;326:411–414.
37 Hirt RP, Logsdon JM, Healy B, Dorey MW, Doolittle WF, Embley TM: Microsporidia are related
to fungi: Evidence from the largest subunit of RNA polymerase II and other proteins. Proc Natl
Acad Sci USA 1999;96:580–585.
38 Cavalier-Smith T: Kingdom Protozoa and its 18 phyla. Microbiol Rev 1993;57:953–994.
39 Heath B: Variant mitoses in lower eukaryotes: Indicators of the evolution of mitosis? Int Rev Cytol
1980;64:1–80.
40 Raikov IB: The Protozoan Nucleus Morphology and Evolution. Cell Biol Monogr. Vienna,
Springer, 1982, vol 9.
41 Prillinger H: Zur Evolution von Mitose, Meiose und Kernphasenwechsel bei Chitinpilzen.
Z Mykol 1984;50:267–352.
42 Margulis L, Corliss JO, Melkonian M, Chapman DI: Handbook of Protoctista. Boston, Jones &
Barlett, 1989.
43 Melkonian M: II. Systematics and evolution of the algae: Endocytobiosis and evolution of the
major algal lineages. Prog Bot 1996;57:281–311.
44 Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The ClustalX windows
interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools.
Nucl Acids Res 1997;24:4876–4882.
45 Felsenstein J: Phylip-Phylogeny inference package (version 3.5c). Distributed by the author,
Department of Genetics, University of Washington, Seattle, 1993.
46 Page RDM: Treeview: An application to display phylogenetic trees on personal computers.
Comput Appl Biosci 1996;12:357–358.
47 Giovannoni SJ, Turner S, Olsen GJ, Barns S, Lane DJ, Pace NR: Evolutionary relationships among
the cyanobacteria and green chloroplasts. J Bacteriol 1988;170:3584–3592.
48 Yang D, Oyaizu Y, Oyaizu H, Olsen GJ, Woese CR: Mitochondrial origins. Proc Natl Acad Sci
USA 1985;82:4443–4447.
49 Margulis L: Symbiosis in Cell Evolution. San Francisco, Freeman, 1981.
50 Sitte P: Symbiogenetic evolution of complex cells and complex plastids. Eur J Protistol
1993;29:131–143.
51 Jahrmann HJ, Prillinger H: Das Vorkommen eines ‘Hefe’-Stadiums bei dem Homobasidiomyceten
Asterophora (Nyctalis) lycoperdoides (Bull.) Ditm. ex S.F. Gray und seine Bedeutung für die
Phylogenese der Basidiomyceten. Z Mykol 1983;49:195–235.
52 Barr DJS: Evolution and kingdoms of organisms from the perspective of a mycologist. Mycologia
1992;84:1–11.
53 Cavalier-Smith T: Eukaryote kingdoms: Seven or nine? Biosystems 1981;14:461–481.
54 Cavalier-Smith T: The origin of fungi and pseudofungi; in Rayner ADM, Brasier CM, Moore D (eds):
Evolutionary Biology of the Fungi. Cambridge, Cambridge University Press, 1987, pp 339–353.
55 Prillinger H: Zur genetischen Kontrolle und Evolution der sexuellen Fortpflanzung und
Heterothallie bei Chitinpilzen. Z Mykol 1982;48:297–324.
56 Bartnicki-Garcia S: Cell wall composition and other biochemical markers in fungal phylogeny; in
Harborne JB (ed): Phytochemical Phylogeny. London, Academic Press, 1970, pp 81–103.
57 Bartnicki-Garcia S: The cell wall: A crucial structure in fungal evolution; in Rayner ADM, Brasier
CM, Moore D (eds): Evolutionary Biology of the Fungi. Cambridge, Cambridge University Press,
1987, pp 389–403.
58 Vogel HJ: Distribution of lysine pathways among fungi: Evolutionary implication. Am Nat 1964;
98:435–446.
Systematics of the Ascomycota and Basidiomycota 277

59 Vogel HJ: Lysine biosynthesis and evolution: Fungi, gymnosperms and angiosperms; in
Bryson V, Vogel HJ (eds): Evolving Genes and Proteins. New York, Academic Press, 1965,pp 25–40.
60 Korhonen K: Breeding units in the forest pathogens Armillaria and Heterobasidion; in Rayner
ADM, Brasier CM, Moore D (eds): Evolutionary Biology of the Fungi. Cambridge, Cambridge
University Press, 1987, pp 301–310.
61 Sansome ER: Fungal chromosomes as observed with the light microscope; in Rayner ADM,
Brasier CM, Moore D (eds): Evolutionary Biology of the Fungi. Cambridge, Cambridge University
Press, 1987, pp 97–113.
62 Bruns TD, White TJ, Taylor JW: Fungal molecular systematics. Annu Rev Ecol Syst 1991;22:
525–564.
63 Alexopoulos CJ, Mims CW, Blackwell M: Introductory Mycology, ed 4, rev. New York, Wiley &
Sons, 1996.
64 Bresinsky A: Abstammung, Phylogenie und Verwandtschaft im Pilzreich. Z Mykol 1996;62:
147–168.
65 Rast DM, Pfyffer GE: Acyclic polyols and higher taxa of fungi. Bot J Linnean Soc 1989;99:39–57.
66 Zuck RK: Alternation of generations and the manner of nutrition. Drew Univ Stud 1953;6:1–19.
67 Baldauf SL, Palmer JD: Animals and fungi are each other’s closest relatives: Congruent evidence
from multiple proteins. Proc Natl Acad Sci USA 1993;90:11558–11562.
68 Hasegawa M, Iida Y, Yano T, Takaiwa F, Miyata T: Phylogenetic relationships among eukaryotic
kingdoms inferred from ribosomal RNA sequences. J Mol Evol 1985;22:32–38.
69 Hasegawa M, Hashimoto T, Adachi J, Iwabe N, Miyata T: Early branching in the evolution of
eukaryotes: Ancient divergence of Entamoeba that lacks mitochondria revealed by protein
sequence data. J Mol Evol 1993;36:380–388.
70 Hendriks L, de Baere R, van de Peer Y, Neefs J, Goris A, de Wachter R: The evolutionary position
of the rhodophyte Porphyra umbilicalis and the basidiomycete Leucosporidium scottii among
other eukaryotes as deduced from complete sequences of small ribosomal subunit RNA. J Mol
Evol 1991;32:167–177.
71 Kumar S, Rzhetsky A: Evolutionary relationships of eukaryotic kingdoms. J Mol Evol 1996;
42:183–193.
72 Wainright PO, Hinkle G, Sogin ML, Stickel SK: Monophyletic origins of the Metazoa: An evolu-
tionary link with fungi. Science 1993;260:340–342.
73 Nikoh N, Hayase N, Iwabe N, Kuma K, Miyata T: Phylogenetic relationships of the kingdoms
Animalia, Plantae, and Fungi inferred from 23 different protein species. Mol Biol Evol 1994;
11:762–768.
74 Veuthey AL, Bittar G: Phylogenetic relationships of Fungi, Plantae, and Animalia inferred from
homologous comparison of ribosomal proteins. J Mol Evol 1998;47:81–92.
75 Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH: Manual of Clinical Microbiology,
ed 7. Washington, ASM Press, 1999.
76 Castlebury LA, Domier LL: Small subunit ribosomal RNA gene phylogeny of Plasmodiophora
brassicae. Mycologia 1998;90:102–107.
77 Berg LR, Patterson GW: Phylogenetic implications of sterol biosynthesis in Oomycetes.
Exp Mycol 1986;10:175–183.
78 Leipe DD, Wainright PO, Gunderson JH, Porter D, Patterson DJ, Valois F, Himmerich S, Sogin
ML: The stramenopiles from a molecular perspective: 16S-like rRNA sequences from
Labyrinthuloides minuta and Cafeteria roenbergensis. Phycologia 1994;33:369–377.
79 van der Auwere G, de Baere R, van der Peer Y, de Rijk P, van den Broeck I, de Wachter R: The
phylogeny of the Hyphochytridiomycota as deduced from ribosomal RNA sequences of
Hyphochytrium catenoides. Mol Biol Evol 1995;12:671–678.
80 De Hoog GS, Guarro J: Atlas of Clinical Fungi. Baarn, Centraalbureau voor Schimmelcultures,
Universitat Rovira i Virgili, 1995.
81 Horner WE, Helbling A, Salvaggio JE, Lehrer SB: Fungal allergens. Clin Microbiol Rev 1995;
8:161–179.
82 Pascher A: Systematische Übersicht über die mit Flagellaten in Zusammenhang stehenden
Algenreihen und Versuch einer Einreihung dieser Algenstämme in die Stämme des
Pflanzenreiches. Beih Bot Centralbl II 1931;48:317–332.
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 278

83 Prillinger H: Yeasts and anastomoses: Their occurrence and implications for the phylogeny of
Eumycota; in Rayner ADM, Brasier CM, Moore D (eds): Evolutionary Biology of the Fungi.
Cambridge, Cambridge University Press, 1987, pp 355–377.
84 Sogin ML: Early evolution and the origin of eukaryotes. Curr Opin Gen Dev 1991;1:457–463.
85 Benjamin RK: Zygomycetes and their spores; in Kendrick WB (ed): The Whole Fungus. Ottawa,
National Museums of Canada, 1979, pp 573–616.
86 Nagahama T, Sato H, Shimazu M, Sugiyama J: Phylogenetic divergence of the entomophthoralean
fungi: Evidence from nuclear 18S ribosomal RNA sequence. Mycologia 1995;87:203–209.
87 McLauglin DJ, Beckett A, Yoon KS: Ultrastructure and evolution of ballistosporic basidiospores.
Bot J Linnean Soc 1985;91:253–271.
88 Tucker BE: A review of the nonentomogenous Entomophthorales. Mycotaxon 1981;13:481–505.
89 Sterflinger K, de Hoog GS, Haase G: Phylogeny and ecology of meristematic ascomycetes. Stud
Mycol 1999;43:5–22.
90 Hiscock SJ, Kües U: Cellular and molecular mechanisms of sexual incompatibility in plants and
fungi. Int Rev Cytol 1999;193:165–295.
91 Burgeff H: Sexualität und Parasitismus bei den Mucorineen. Ber Dtsch Bot Ges 1920;38:
318–327.
92 Burgeff H: Untersuchungen über Sexualität und Parasitismus bei Mucorineen; in Goebel K (ed):
Botanische Abhandlungen. Jena, Fischer, 1924, pp 1–135.
93 Prillinger H: Untersuchungen zur Fruchtkörper- und Artbildung bei Basidiomyceten: Das
Vorkommen von haploider Apomixis und Amphithallie in der Natur. Z Mykol 1982;48:275–296.
94 Prillinger H: Morphologische Atavismen bei Homobasidiomyceten durch natürliche und
künstliche Inzucht und ihre Bedeutung für die Systematik. Ber Dtsch Bot Ges 1986;99:31–42.
95 Yun S-H, Berbee ML, Yoder OC, Turgeon BG: Evolution of the fungal self-fertile reproduction
life style from self-sterile ancestors. Proc Natl Acad Sci USA 1999;96:5592–5597.
96 Bakkeren G, Kronstad JW: Linkage of mating-type loci distinguishes bipolar from tetrapolar
mating in basidiomycetous smut fungi. Proc Natl Acad Sci USA 1994;91:7085–7089.
97 Casselton LA, Kües U: Mating-type genes in homobasidiomycetes; in Esser K, Lemke PA (eds):
The Mycota. I. Growth, differentiation and sexuality. Berlin, Springer, 1994, pp 307–321.
98 Hijri M, Hosny M, van Tuinen, Dulieu H: Intraspecific ITS polymorphism in Scutellospora
castanea (Glomales, Zygomycota) is structured within multinucleate spores. Fungal Genet Biol
1999;26:141–151.
99 Hosny M, Hijri M, Passerieux E, Dulieu H: rDNA units are highly polymorphic in Scutellospora
castanea (Glomales, Zygomycetes). Gene 1999;226:61–71.
100 Sanders IR: No sex please, we’re fungi. Nature 1999;399:737–739.
101 Mosse B: Some studies relating to ‘independent’ growth of vesicular arbuscular endophytes. Can
J Bot 1988;66:2533–2540.
102 Remy W, Taylor TN, Hass H, Kerp H: Four hundred-million-year-old vesicular arbuscular
mycorrhizae. Proc Natl Acad Sci USA 1994;91:11841–11843.
103 Prillinger H, Six W: Genetische Untersuchungen zur Fruchtkörper- und Artbildung bei
Basidiomyceten: Genetische Kontrolle der Fruchtkörperbildung bei Polyporus ciliatus. Pl Syst
Evol 1983;141:341–371.
104 Prillinger H: Are there yeasts in Homobasidiomycetes? in de Hoog GS, Smith MT, Weijman ACM
(eds): The Expanding Realm of Yeast-Like Fungi. Amsterdam, Elsevier, 1987, pp 33–59.
105 Kemp RFO: Breeding biology of Coprinus spp. in the section Lanatuli. Trans Br Mycol Soc
1975;65:375–388.
106 Prillinger H, Altenbuchner J, Schulz B, Dörfler C, Forst T, Laaser G, Stahl U: Ustilago maydis
isolated from Homobasidiomycetes; in Galling G (ed): Proceedings Applied Plant Molecular Biology
(Braunschweig Symposium, Nov 1988). Braunschweig, Technische Universität, 1989, pp 408–425.
107 Savile DBO: A phylogeny of the Basidiomycetes. Can J Bot 1955;33:60–104.
108 Kellner M, Burmester A, Wöstemeyer A, Wöstemeyer J: Transfer of genetic information from the
mycoparasite Parasitella parasitica to its host Absidia glauca. Curr Genet 1993;23:334–337.
109 Wöstemeyer J, Wöstemeyer A, Burmester A, Czempinski K: Relationship between sexual
processes and parasitic interactions in the host-pathogen system Absidia glauca-Parasitella
parasitica. Can J Bot 1995;73 (suppl 1):S243–S250.
Systematics of the Ascomycota and Basidiomycota 279

110 Philley ML, Staben C: Functional analyses of the Neurospora crassa MT a-1 mating type polypep-
tide. Genetics 1994;137:715–722.
111 Saupe SJ, Descamps C, Turcq B, Begueret J: Inactivation of the Podospora anserina vegetative
incompatibility locus het-c, whose product resembles a glycolipid transfer protein, drastically
impairs ascospore production. Proc Natl Acad Sci USA 1994;91:5927–5931.
112 Saupe SJ, Stenberg L, Shiu KT, Griffiths AJ, Glass NL: The molecular nature of mutations in the
mt-A-1 gene of the Neurospora crassa A idiomorph and their relation to mating-type function.
Mol Gen Genet 1996;250:115–122.
113 Saupe SJ, Kuldau GA, Smith ML, Glass NL: The product of the het-C heterokaryon incompati-
bility gene of Neurospora crassa has characteristics of a glycine-rich cell wall protein. Genetics
1996;143:1589–1600.
114 Saupe SJ, Glass NL: Allelic specificity at the het-c heterokaryon incompatibility locus of
Neurospora crassa is determined by a highly variable domain. Genetics 1997;146:1299–1309.
115 Coustou V, Deleu C, Saupe S, Bequeret J: The protein product of the het-s heterokaryon incom-
patibility gene of the fungus Podospora anserina behaves as a prion analog. Proc Natl Acad Sci
USA 1997;94:9773–9778.
116 Espagne E, Balhadere P, Begueret J, Turcq B: Reactivity in vegetative incompatibility of the HET-
E protein of the fungus Podospora anserina is dependent on GTP-binding activity and a WD40
repeated domain. Mol Gen Genet 1997;256:620–627.
117 Ferreira AV, An Z, Metzenberg RL, Glass NL: Characterization of mat A-2, mat A-3 and
deltamatA mating-type mutants of Neurospora crassa. Genetics 1998;148:1069–1079.
118 Wu J, Saupe SJ, Glass NL: Evidence for balancing selection operating at the het-c heterokaryon
incompatibility locus in a group of filamentous fungi. Proc Natl Acad Sci USA 1998;95:
12398–12403.
119 Shiu PK, Glass NL: Molecular characterization of tol, a mediator of mating-type-associated
vegetative incompatibility in Neurospora crassa. Genetics 1999;151:545–555.
120 Wickner RB, Taylor KL, Edskes HK, Maddelein ML, Moriyama H, Roberts BT: Prions in
Saccharomyces and Podospora spp.: Protein-based inheritance. Microbiol Mol Biol Rev 1999;63:
844–861.
121 Glass NL, Grotelueschen J, Metzenber RL: Neurospora crassa A mating-type region. Proc Natl
Acad Sci USA 1990;87:4912–4916.
122 Staben C, Yanofsky C: Neurospora crassa A mating-type region. Proc Natl Acad Sci USA 1990;
87:4917–4921.
123 Turgeon BG, Christiansen SK, Yoder OC: Mating type genes in Ascomycetes and their
imperfect relatives; in Reynolds DR, Taylor JW (eds): The Fungal Holomorph: Mitotic, Meiotic
and Pleomorphic Speciation in Fungal Systematics. Wallingford, CAB International, 1993, pp
199–215.
124 Bölker M, Urban M, Kahmann R: The a mating type locus of Ustilago maydis specifies cell
signalling components. Cell 1992;68:441–450.
125 Kämper J, Bölker M, Kahmann R: Mating-type genes in Heterobasidiomycetes; in Esser K,
Lemke PA (eds): The Mycota, Growth, Differentiation and Sexuality. Heidelberg, Springer, 1994,
vol I, pp 323–332.
126 Hicks JB, Klar JS: Transposable mating type genes in Saccharomyces cerevisiae. Nature
1979;282:478–483.
127 Schulz B, Banuett F, Dahl M, Schlesinger R, Schäfer W, Martin T, Herskowitz I, Kahmann R: The
b alleles of Ustilago maydis, whose combinations program pathogenic development, code for
polypeptides containing a homeodomain-related motif. Cell 1990;60:295–306.
128 Hull CM, Johnson AD: Identification of a mating type-like locus in the asexual pathogenic yeast
Candida albicans. Science 1999;285:1271–1275.
129 Lopandic K: Genotypic Identification and Comparative Analysis of Cell Wall Sugars from
Asco- and Basidiomycetous Yeasts; PhD thesis, University of Zagreb, 1998.
130 Geiser DM, Timberlake WE, Arnold ML: Loss of meiosis in Aspergillus. Mol Biol Evol 1996;
13:809–817.
131 Peterson SW: Phylogenetic analysis of Penicillium species based on ITS and lsu-rDNA nucleotide
sequences. Proc 3rd Int Workshop Penicillium Aspergillus, Baarn, May 1997.
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 280

132 Tamura M, Kawahara K, Sugiyama J: Molecular phylogeny of Aspergillus and associated
teleomorphs in the Trichocomaceae (Eurotiales). Proc 3rd Int Workshop Penicillium Aspergillus,
Baarn, May 1997.
133 LoBuglio KF, Pitt JI, Taylor JW: Phylogenetic analysis of two ribosomal DNA regions indicates
multiple independent losses of a sexual Talaromyces state among asexual Penicillium species in
subgenus Biverticillium. Mycologia 1993;85:592–604.
134 Ogawa H, Yoshimura A, Sugiyama J: Polyphyletic origins of species of the anamorphic genus
Geosmithia and the relationships of the cleistothecial genera: Evidence from 18S, 5S and 28S
rDNA sequence analyses. Mycologia 1997;89:756–771.
135 Bowman BH, Taylor JW: Molecular phylogeny of pathogenic and non-pathogenic Onygenales; in
Reynolds DR, Taylor JW (eds): The Fungal Holomorph: Mitotic, Meiotic and Pleomorphic
Speciation in Fungal Systematics. Wallingford, CAB International, 1993, pp 169–178.
136 Bowman BH, White TJ, Taylor JW: Human pathogenic fungi and their close nonpathogenic
relatives. Mol Phylogenet Evol 1996;6:89–96.
137 Hambleton S, Egger KN, Currah RS: The genus Oidiodendron: Species delimitation and phyloge-
netic relationships based on nuclear ribosomal DNA analysis. Mycologia 1998;90:854–869.
138 Guadet J, Julian J, Lafay JF, Brygoo Y: Phylogeny of some Fusarium species, as determined by
large subunit rRNA sequence comparison. Mol Biol Evol 1989;6:227–242.
139 O’Donnell K: Fusarium and its near relatives; in Reynolds DR, Taylor JW (eds): The Fungal
Holomorph: Mitotic, Meiotic and Pleomorphic Speciation in Fungal Systematics. Wallingford,
CAB International, 1993, pp 225–233.
140 O’Donnell K, Cigelnik E, Nirenberg HI: Molecular systematics and phytogeography of the
Gibberella fujikuroi species complex. Mycologia 1998;90:465–493.
141 Rehner SA, Samuels GJ: Taxonomy and phylogeny of Gliocladium analysed from nuclear large
subunit DNA sequences. Mycol Res 1994;98:625–634.
142 Rehner SA, Samuels GJ: Molecular systematics of the Hypocreales: A teleomorph gene
phylogeny and the status of their anamorphs. Can J Bot 1995;73(suppl 1):S816–S823.
143 Glenn AE, Bacon CW, Price R, Hanlin RT: Molecular phylogeny of Acremonium and its
taxonomic implications. Mycologia 1996;88:369–383.
144 Vogler DR, Bruns TD: Use of molecular characters to identify holomorphs: An example from the rust
genus Cronartium; in Reynolds DR, Taylor JW (eds): The Fungal Holomorph: Mitotic, Meiotic and
Pleomorphic Speciation in Fungal Systematics. Wallingford, CAB International, 1993, pp 237–245.
145 Reynolds DR, Taylor JW: The Fungal Holomorph: Mitotic, Meiotic and Pleomorphic Speciation
in Fungal Systematics. Wallingford, CAB International, 1993.
146 Reynolds DR, Taylor JW: DNA specimens and the ‘international code of botanical nomenclature’.
Taxon 1991;40:311–315.
147 Haines JH, Cooper CR: DNA and mycological herbaria; in Reynolds DR, Taylor JW (eds): The
Fungal Holomorph: Mitotic, Meiotic and Pleomorphic Speciation in Fungal Systematics.
Wallingford, CAB International, 1993, pp 305–315.
148 Prillinger H, Messner R, König H, Bauer R, Lopandic K, Molnár O, Dangel P, Weigang F, Kirisits
T, Nakase T, Sigler L: Yeasts associated with termites: A phenotypic and genotypic characterization
and use of coevolution for dating evolutionary radiations in Asco- and Basidiomycetes. Syst Appl
Microbiol 1996;19:265–283.
149 Laaser G: Vergleichende systematische Studien an Basidiomycetenhefen unter besonderer
Berücksichtigung der Hefestadien. Bibl Mycol 1989;130:2–335.
150 Prillinger H, Altenbuchner J, Laaser G, Dörfler C: Yeasts isolated from Homobasidiomycetes
(Asterophora, Collybia): New aspects for sexuality, taxonomy, and speciation. Exp Mycol 1993;
17:24–45.
151 Schweigkofler W: Molekulare Identifizierung und Charakterisierung von endophytischen und
latent pathogenen Pilzen aus Weinreben (Vitis vinifera L.) in Österreich und Südtirol; Dissertation,
Universität für Bodenkultur, Wien, 1998, pp 1–179.
152 Prillinger H, Schweigkofler W, Breitenbach M, Briza P, Staudacher E, Lopandic K, Molnár O,
Weigang F, Ibl M, Ellinger A: Phytopathogenic filamentous (Ashbya, Eremothecium) and
dimorphic fungi (Holleya, Nematospora) with needle-shaped ascospores as new members within
the Saccharomycetaceae. Yeast 1997;13:945–960.
Systematics of the Ascomycota and Basidiomycota 281

153 Jeffries P, Young TWK: Ultrastructure of infection of Cokeromyces recurvatus by Piptocephalis
unispora (Mucorales). Arch Microbiol 1976;109:277–288.
154 Orban G: Untersuchungen über die Sexualität von Phycomyces nitens. Beih Bot Centralbl I
1919;36:1–59.
155 Emmons CW: The ascocarps in species of Penicillium. Mycologia 1935;27:128–150.
156 Zickler H: Die Spermatienbefruchtung bei Bombardia lunata. Ber Dtsch Bot Ges 1937;55:
114–119.
157 Zickler H: Zur Entwicklungsgeschichte des Askomyceten Bombardia lunata Zckl. Arch Protistenk
1952;98:1–70.
158 Mirza JH, Cain RF: Revision of the genus Podospora. Can J Bot 1969;47:1999–2048.
159 Forst TG, Prillinger H: Vergleichende karyologische Untersuchungen an dimorphen
Zygomyceten. Z Mykol 1988;54:139–154.
160 Glass NL, Metzenberg RL, Raju NB: Homothallic Sordariaceae from nature: The absence of
strains containing only the a mating type sequence. Exp Mycol 1990;14:274–289.
161 Li J, Heath IB: The phylogenetic relationships of the anaerobic chytridiomycetous gut fungi
(Neocallimasticaceae) and the Chytridiomycota. II. Cladistic analysis of structural data and
description of the Neocallimasticales ord. nov. Can J Bot 1993;71:393–407.
162 Barr DJS, Kudo H, Jakober KD, Cheng K-J: Morphology and development of rumen fungi:
Neocallimastix sp., Piromyces communis, and Orpinomyces bovis gen. nov., sp. nov. Can J Bot
1989;67:2815–2824.
163 Li J, Heath IB: The phylogenetic relationships of the anaerobic chytridiomycetous gut fungi
(Neocallimasticaceae) and the Chytridiomycota. I. Cladistic analysis of rRNA sequences. Can J
Bot 1992;70:1738–1746.
164 Bowman BH, Taylor JW, White TJ: Molecular evolution of the fungi: Human pathogens. Mol Biol
Evol 1992;9:893–904.
165 Tanabe Y, O’Donnell K, Saikawa M, Sugiyama J: Molecular phylogeny of parasitic Zygomycota
(Dimargaritales, Zoopagales) based on nuclear small subunit ribosomal DNA sequences. Mol
Phylogenet Evol 2000;16:253–262.
166 McKerracher LJ, Heath IB: The structure and cycle of the nucleus-associated organelle in two
species of Basidiobolus. Mycologia 1985;77:412–417.
167 Gehrig H, Schüssler A, Kluge M: Geosiphon pyriforme, a fungus forming endocytobiosis
with Nostoc (Cyanobacteria), is an ancestral member of the Glomales: Evidence by SSU rRNA
analysis. J Mol Evol 1996;43:71–81.
168 Moss ST, Young TWK: Phyletic considerations of the Harpellales and Asellariales
(Trichomycetes, Zygomycotina) and the Kickxellales (Zygomycetes, Zygomycotina). Mycologia
1978;70:944–963.
169 O’Donnell K, Cigelnik E, Benny GL: Phylogenetic relationships among the Harpellales and
Kickxellales. Mycologia 1998;90:624–639.
170 Davis SR, Ellis DH, Goldwater P, Dimitriou S, Byard R: First human culture-proven Australian
case of entomophthoromycosis caused by Basidiobolus ranarum. J Med Vet Mycol 1994;32:
225–230.
171 Ng KH, Chin CS, Jalleh RD, Siar CH, Ngui CH, Singaram SP: Nasofacial zygomycosis. Oral Surg
Oral Med Oral Pathol 1991;72:685–688.
172 Gugnani HC: Entomophthoromycosis due to Conidiobolus. Eur J Epidemiol 1992;8:391–396.
173 Moll HD, Schumacher J, Hoover TR: Entomophthoromycosis conidiobolae in a lama. J Am Vet
Med Assoc 1992;200:969–970.
174 Hawksworth DL: The fungal dimension of biodiversity: Magnitude, significance, and conserva-
tion. Mycol Res 1991;95:641–655.
175 Hawksworth DL, Kirk PM, Sutton BC, Pegler DN: Dictionary of the Fungi, ed 8, rev. Wallingford,
CAB International, 1995.
176 Kramer CL: The Taphrinales; in de Hoog GS, Smith MT, Weijman ACM (eds): The Expanding
Realm of Yeast-Like Fungi. Amsterdam, Elsevier, 1987, pp 151–166.
177 Müller E: Systemfragen bei Ascomyceten; in Frey W, Hurka H, Oberwinkler F (eds): Beiträge zur
Biologie der niederen Pflanzen. Stuttgart, Fischer, 1977, pp 43–57.
178 Tehler A: A cladistic outline of the Eumycota. Cladistics 1988;4:227–277.
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 282

179 Savile DBO: Possible interrelationships between fungal groups; in Ainsworth GC, Susmann AS
(eds): The Fungi, an Advanced Treatise. New York, Academic Press, 1968, pp 649–675.
180 Gargas A, DePriest PT, Grube M, Tehler A: Multiple origins of lichen symbioses in fungi
suggested by ssu rDNA phylogeny. Science 1995;268:1492–1495.
181 Nishida H, Sugiyama J: Archiascomycetes: Detection of a major new lineage within the
Ascomycota. Mycoscience 1994;35:361–366.
182 Sjamsuridzal W, Tajiri Y, Nishida H, Thuan TB, Kawasaki H, Hirata A, Yokota A, Sugiyama J:
Evolutionary relationships of members of the genera Taphrina, Protomyces, Schizosaccharomyces,
and related taxa within the archiascomycetes: Integrated analysis of genotypic and phenotypic
characters. Mycoscience 1997;38:267–280.
183 Taylor JW: A contemporary view of the holomorph: Nucleic acid sequence and computer
databases are changing fungal classification; in Reynolds DR, Taylor JW (eds): The Fungal
Holomorph: Mitotic, Meiotic and Pleomorphic Speciation in Fungal Systematics. Wallingford,
CAB International, 1993, pp 3–13.
184 Taylor JW: Making the Deutereomycota redundant: A practical integration of mitosporic and
meiosporic fungi. Can J Bot 1995;73(suppl 1):S754–S759.
185 Eriksson OE: Origin and evolution of the Ascomycetes. Opera Bot 1981;60:175–209.
186 Oberwinkler F: Das neue System der Basidiomyceten; in Frey W, Hurka H, Oberwinkler F (eds):
Beiträge zur Biologie der niederen Pflanzen. Stuttgart, Fischer, 1977, pp 59–105.
187 Untereiner WA, Malloch D: Patterns of substrate utilization in species of Capronia and allied
black yeasts: Ecological and taxonomic implications. Mycologia 1999;92:417–427.
188 Prillinger H, Lopandic K, Schweigkofler W: Zellwandzucker als Hilfsmittel zur Klärung
phylogenetischer Beziehungen bei Hefen. Abstr Tagung Ges Mykol Lichenol, Regensburg, Okt
1997, p 35.
189 Prillinger H, Lopandic K, Schweigkofler W: Phylogeny of ascomycetous yeasts and yeast stages
from the Ascomycota based on cell wall sugars, 18S ribosomal DNA sequences, and coevolution.
Abstr 6th Int Mycol Congr, Jerusalem, Aug 1998, p 93.
190 Prillinger H, Schweigkofler W, Lopandic K, Bauer R, Mueller UG: Evolution of Asco- and
Basidiomycota based on cell wall sugars, 18S ribosomal DNA sequences and coevolution with
animals and plants. Yeast Newslett 1999;48:12.
191 Cai J, Roberts IN, Collins MD: Phylogenetic relationships among members of the ascomycetous
yeast genera Brettanomyces, Debaryomyces, Dekkera, and Kluyveromyces deduced by small-
subunit rRNA gene sequences. Int J Syst Bacteriol 1996;46:542–549.
192 Kurtzman CP: Molecular taxonomy of the fungi; in Benett JW, Lasure LL (eds): Gene
Manipulations in Fungi. Orlando, Academic Press, 1985, pp 35–63.
193 Kurtzman CP: Systematics of the ascomycetous yeasts assessed from ribosomal RNA sequence
divergence. Antonie Van Leeuwenhoek 1993;63:165–174.
194 Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq
C, Johnston M, Louis EJ, Mewes HW, Murakami Y, Philippsen P, Tettelin H, Oliver SG: Life with
6,000 genes. Science 1996;274:546–567.
195 Hoheisel JD, Maier E, Mott R, McCarthy L, Gregoriev AV, Schalkwyk LC, Nizetic D, Francis F,
Lehrach H: High resolution cosmid and P1 maps spanning the 14 Mb genome of the fission yeast
S. pombe. Cell 1993;73:109–120.
196 Byers B, Goetsch L: Electronic microscopic observations on the meiotic karyotype of diploid and
tetraploid Saccharomyces cerevisiae. Proc Natl Acad Sci USA 1975;72:5056–5069.
197 Mewes HW, Albermann K, Bähr M, Frishman D, Gleissner A, Hani J, Heuman K, Kleine K,
Maierl A, Oliver SG, Pfeifer F, Zollner A: Overview of the yeast genome. Nature 1997;387:7–65.
198 Mewes HW, Albermann K, Heumann K, Liebl S, Pfeifer F: MIPS: A database for protein
sequences, homology data and yeast genome information. Nucleic Acid Res 1997;35:28–30.
199 Clarke L, Baum MP: Functional analysis of a centromere from fission yeast: A role for
centromere-specific repeated DNA sequences. Mol Cell Biol 1990;10:1863–1872.
200 Moore TDE, Edman JC: The a-mating type locus of Cryptococcus neoformans contains a peptide
pheromone gene. Mol Cell Biol 1993;13:1962–1970.
201 Redhead SA: The genus Neolecta (Neolectaceae fam. nov., Lecanorales, Ascomycetes) in Canada.
Can J Bot 1977;55:301–306.
Systematics of the Ascomycota and Basidiomycota 283

202 Kurtzman CP, Fell JW: The Yeasts, a Taxonomic Study, ed 4, rev. Amsterdam, Elsevier, 1998.
203 Suzuki M, Suh S-O, Sugita T, Nakase T: A phylogenetic study on galactose-containing Candida
species based on 18S ribosomal DNA sequences. J Gen Appl Microbiol 1999;45:229–238.
204 Batra LR: Taxonomy and systematics of the Hemiascomycetes (Hemiascomycetidae);
in Subramanian CV (ed): Taxonomy of Fungi. Madras, University of Madras, 1973, pp 187–214.
205 Cregg JM, Vedvick TS, Raschke WC: Recent advances in the expression of foreign genes in
Pichia pastoris. Biotechnology 1993;11:905–910.
206 Rhyan JC, Stackhouse LL, Davis EG: Disseminated geotrichosis in two dogs. J Am Vet Med
Assoc 1990;197:358–360.
207 Smith MT, de Cock AWAM, Poot GA, Steensma HY: Genome comparisons in the yeastlike
fungal genus Galactomyces Redhead et Malloch. Int J Syst Bacteriol 1995;45:826–831.
208 Prillinger H, Molnár O, Eliskases-Lechner F, Lopandic K: Phenotypic and genotypic identifica-
tion of yeasts from cheese. Antonie Van Leeuwenhoek 1999;75:267–283.
209 Sullivan DJ, Westerneng TJ, Haynes KA, Bennett DE, Coleman DC: Candida dubliniensis sp. nov.:
Phenotypic and molecular characterization of a novel species associated with oral candidosis in
HIV-infected individuals. Microbiology 1995;141:1507–1521.
210 Pincus DH: Rapid identification of Candida dubliniensis with commercial yeast identification
systems. J Clin Microbiol 1999;37:3533–3539.
211 Mateev G, Kantjardjiev T, Vassileva S, Tsankov N: Chronic mucocutaneous candidosis with
osteomyelitis of the frontal bone. Int J Dermatol 1993;32:888–889.
212 Clemons KV, McCusker JH, Davis RW, Stevens DA: Comparative pathogenesis of clinical and
nonclinical isolates of Saccharomyces cerevisiae. J Infect Dis 1994;169:859–867.
213 De Hoog GS: Risk assessment of fungi reported from humans and animals. Mycoses 1996;39:
407–417.
214 van der Walt JP, Johannsen E: The dangeardian and its significance in the taxonomy of ascomyce-
tous yeasts. Antonie Van Leeuwenhoek 1974;40:185–192.
215 Prillinger H, Dörfler C, Laaser G, Hauska G: Ein Beitrag zur Systematik und Entwicklungsbiologie
höherer Pilze: Hefe-Typen der Basidiomyceten. III. Ustilago-Typ. Z Mykol 1990;56:
251–278.
216 Prillinger H, Laaser G, Dörfler C, Ziegler K: Ein Beitrag zur Systematik und Entwicklungsbiologie
höherer Pilze: Hefe-Typen der Basidiomyceten. IV. Dacrymyces-Typ, Tremella-Typ. Sydowia
1991;53:170–218.
217 Prillinger H, Oberwinkler F, Umile C, Tlachac K, Bauer R, Dörfler C, Taufratzhofer E: Analysis
of cell wall carbohydrates (neutral sugars) from ascomycetous and basidiomycetous yeasts with
and without derivatization. J Gen Appl Microbiol 1993;39:1–34.
218 Redondo-Lopez V, Lynch M, Schmitt C, Cook R, Sobel JD: Torulopsis glabrata vaginitis: Clinical
aspects and susceptibility to antifungal agents. Obstet Gynecol 1990;76:651–654.
219 Nishida T, Mayumi H, Kawachi Y, Tokunaga S, Murayama A, Yasui H, Tokunaga K: The efficacy
of fluconazole in treating prosthetic valve endocarditis caused by Candida glabrata: Report of a
case. Surg Today Tokyo 1994;24:651–654.
220 Hickley WF, Sommerville LH, Schoen FJ: Disseminated Candida glabrata: Report of a unique
severe infection and a literature review. Am J Clin Pathol 1983;80:724–727.
221 Owen PG, Willis BK, Benzel EC: Torulopsis glabrata vertebral osteomyelitis. J Spinal Disord
1992;5:370–373.
222 Hoppe JE, Klingebiel T, Niethammer D: Selection of Candida glabrata in pediatric bone marrow
transplant recipients receiving fluconazole. Pediatr Hematol Oncol 1994;11:207–210.
223 Vazquez J, Lundstrom T, Dembry L, Perry MB, Zervos M: Disseminated Torulopsis candida
(Candida famata) infection: An unusual human pathogen. Abstr Gen Meet Am Soc Microbiol
1993;93:534.
224 Nicand E, Buisson Y, Auzanneau G, Improvisi L, Dupont B: Septicémie à Debaryomyces hansenii
(Candida famata), levure pathogène opportuniste. J Mycol Méd 1993;4:242–244.
225 Blaschke-Hellmessen R: Standorte für Candida aus medizinisch-hygienischer Sicht. Mycoses
1999;42(suppl 1):22–29.
226 Furman RM, Ahearn DG: Candida ciferrii and Candida chiropterorum isolated from clinical
specimens. J Clin Microbiol 1983;18:1252–1255.
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 284

227 De Gentile L, Bouchara JP, Cimon B, Chabasse D: Candida ciferrii: Clinical and microbiological
features of an emerging pathogen. Mycoses 1991;34:125–128.
228 Eriksson OE, Winka K: Families and higher taxa of Ascomycota. Myconet 1998;1:17–24.
229 Prillinger H, Dörfler C, Laaser G, Eckerlein B, Lehle L: Ein Beitrag zur Systematik und
Entwicklungsbiologie höherer Pilze: Hefe-Typen der Basidiomyceten. I. Schizosaccharomycetales,
Protomyces-Typ. Z Mykol 1990;56:219–250.
230 Prillinger H, Bacigálová K, Lopandic K, Binder M: Taphrina padi (Jacz.) Mix in Bayern und der
Slowakei. Hoppea, 2000;61:275–294.
231 Eriksson OE, Svedskog A, Landvik S: Molecular evidence for the evolutionary hiatus between
Saccharomyces cerevisiae and Schizosaccharomyces pombe. Systema Ascomycetum 1993;11:
119–162.
232 Landvik S, Eriksson OE, Gargas A, Gustafsson P: Relationships of the genus Neolecta (Neolectales
ordo nov.) inferred from 18S rDNA sequences. Systema Ascomycetum 1993;11:107–118.
233 Eriksson OE: Pneumocystis carinii, a parasite in lungs of mammals, referred to a new family and
order (Pneumocystidaceae, Pneumocystidales, Ascomycota). Systema Ascomycetum 1995;13:
165–180.
234 Prillinger H, Deml G, Dörfler C, Laaser G, Lockau W: Ein Beitrag zur Systematik und
Entwicklungsbiologie höherer Pilze: Hefe-Typen der Basidiomyceten. II. Microbotryum-Typ. Bot
Acta 1991;104:5–17.
235 Nishida H, Ando K, Ando Y, Hirata A, Sugiyama J: Mixia osmundae: Transfer from the
Ascomycota to the Basidiomycota based on evidence from molecules and morphology. Can J Bot
1995;73(suppl 1):S660–S666.
236 Gottschalk M, Blanz PA: Untersuchungen an 5S ribosomalen Ribonukleinsäuren als Beitrag zur
Klärung von Systematik und Phylogenie der Basidiomyceten. Z Mykol 1985;51:205–243.
237 Sugiyama J, Nishida H, Suh S-O: The paradigm of fungal diagnoses and descriptions in the era of
molecular systematics: Saitoella complicata as an example; in Reynolds DR, Taylor JW (eds):
The Fungal Holomorph: Mitotic, Meiotic and Pleomorphic Speciation in Fungal Systematics.
Wallingford, CAB International, 1993, pp 261–269.
238 Ahearn DG, Sugiyama J, Simmons RB: Saitoella S. Goto, Sugiyama, Hamamoto & Komagata;
in Kurtzman CP, Fell JW (eds): The Yeasts, a Taxonomic Study. ed 4. Amsterdam, Elsevier, 1998,
pp 600–601.
239 Landvik S: Neolecta, a fruit-body-producing genus of the basal ascomycetes, as shown by SSU
and LSU rDNA sequences. Mycol Res 1996;100:199–202.
240 Taylor JW, Bowman BH: Pneumocystis carinii and the ustomycetous red yeast fungi. Mol
Microbiol 1993;8:425–426.
241 Taylor JW, Swann EC, Berbee ML: Molecular evolution of ascomycete fungi: Phylogeny and
conflict; in Hawksworth DL (ed): Ascomycete Systematics: Problems and Perspective in the
Nineties. New York, Plenum Press, 1994, pp 201–212.
242 Berbee ML, Taylor JW: Two Ascomycetes classes based on fruiting-body characters and
ribosomal DNA sequence. Mol Biol Evol 1992;9:278–284.
243 Gargas A, Taylor JW: Phylogeny of discomycetes and early radiations of the apothecial
Ascomycotina inferred from SSU rDNA sequence data. Exp Mycol 1995;19:7–15.
244 Nannfeldt JA: Studien über die Morphologie und Systematik der nicht-lichenisierten inopercu-
laten Discomyceten. Nova Acta Reg Soc Sci Upsaliensis 1932;8:1–368.
245 Haase G, Sonntag L, van der Peer Y, Uijthof JMJ, Podbielski A, Melzer Krick B: Phylogenetic
analysis of ten black yeast species using nuclear small subunit rRNA gene sequences. Antonie Van
Leeuwenhoek 1995;68:19–33.
246 Haase G, Sonntag L, Melzer-Krick B, de Hoog GS: Phylogenetic inference by SSU gene analysis
of members of Herpotrichiellaceae with special reference to human pathogenic species. Stud
Mycol 1999;43:80–97.
247 Berbee ML: Loculoascomycete origins and evolution of filamentous ascomycete morphology
based on 18S rRNA gene sequence data. Mol Biol Evol 1996;13:462–470.
248 Sterflinger K, de Baer R, de Hoog GS, de Wachter R, Krumbein WE, Haase G: Coniosporium
perforans and C. appollinis, two new rock inhabiting fungi isolated from marble in the Sanctuary
of Delos (Cyclades, Greece). Antonie Van Leeuwenhoek 1997;72:349–363.
Systematics of the Ascomycota and Basidiomycota 285

249 Winka K, Eriksson OE, Bang A: Molecular evidence for recognizing the Chaetothyriales.
Mycologia 1998;90:822–830.
250 Blackwell M: Minute morphological mysteries: The influence of arthropods on the lives of fungi.
Mycologia 1994;86:1–17.
251 Mendoza L, Karuppayil SM, Szaniszlo PJ: Calcium regulates in vitro dimorphism in chromo-
blastomycotic fungi. Mycoses 1993;36:157–164.
252 Takeo K, de Hoog GS: Karyology and hyphal characters as taxonomic criteria in ascomycetous
black yeasts and related fungi. Antonie Van Leeuwenhoek 1991;60:35–42.
253 Barr ME: Prodromus to Class Loculoascomycetes. Amherst, published by the author 1987.
254 McGinnis MR, Lemon SM, Walker D, de Hoog GS, Haase G: Fatal cerebritis caused by a new
species Cladophialophora. Stud Mycol 1999;43:166–171.
255 Benny GL, Kimbrough JW: A synopsis of the orders and families of Plectomycetes with keys to
genera. Mycotaxon 1980;12:1–91.
256 Landvik S, Shailer NFJ, Eriksson OE: SSU rDNA sequence support for a close relationship
between the Elaphomycetales and the Eurotiales and Onygenales. Mycoscience 1996;37:237–241.
257 Pitt JI: Phylogeny in the genus Penicillium: A morphologist’s perspective. Can J Bot 1995;
73(suppl 1):S768–S777.
258 Pitt JI, Samson RA: Species names in current use in the Trichocomaceae (Fungi, Eurotiales); in
Greuter W (ed): Names in Current Use in the Families Trichocomaceae, Cladoniaceae, Pinaceae,
and Lemnaceae. Königstein, Koeltz, 1993, pp 13–57.
259 Berbee ML, Yoshimura A, Sugiyama J, Taylor JW: Is Penicillium monophyletic? An evolution in
the family Trichocomaceae from 18S, 5.8S and ITS DNA sequence data. Mycologia 1995;
87:210–222.
260 Egel-Mitani M, Olson LW, Egel R: Meiosis in Aspergillus nidulans: Another example for
lacking synaptonemal complexes in the absence of crossover interference. Hereditas 1982;97:
179–187.
261 Bähler J, Wyler T, Loidl J, Kohli J: Unusual nuclear structures in meiotic prophase of fission yeast:
A cytological analysis. J Cell Biol 1993;121:241–256.
262 Guarro J, Gené J, Stchigel AM: Developments in fungal taxonomy. Clin Microbiol Rev 1999;
12:454–500.
263 Jesenska Z, Durkovsky J, Rosinski I, Polak M, Zamboova E, Baca B: Filamentous micromycetes
in otitis. Cesk Epidemiol Mikrobiol Imunol 1992;41:337–341.
264 Shitara T, Yugami S-I, Sotomatu M, Oshima Y, Ijima H, Kuroume T, Matsumoto T: Invasive
aspergillosis in leukemic children. Pediatr Hematol Oncol 1993;10:169–174.
265 Göttlich E: Untersuchungen der Pilzbelastung der Luft an Arbeitsplätzen in Betrieben zur
Abfallbehandlung; thesis, University of Stuttgart, 1995.
266 Byrd RP, Roy TM, Fields CL, Lynch JA: Paecilomyces variotii pneumonia in a patient with
diabetes mellitus. J Diabetes Complications 1992;6:150–153.
267 Thompson RF, Bode RB, Rhodes JC, Gluckman JL: Paecilomyces variotii: An unusual cause of
isolated sphenoid sinusitis. Arch Otolaryngol Head Neck Surg 1988;114:567–569.
268 Williamson PR, Kwon-Chung KJ, Gallin JI: Successful treatment of Paecilomyces variotii
infection in a patient with chronic granulomatous disease and review of Paecilomyces species
infections. Clin Infect Dis 1992;14:1023–1026.
269 Jaisree N, Singh SM: Hyalohyphomycosis caused by Paecilomyces variotii: A case report, animal
pathogenicity and in vitro sensitivity. Antonie Van Leeuwenhoek 1992;62:225–230.
270 Fukatsu T, Sato H, Kuriyama H: Isolation, inoculation to insect host, and molecular phylogeny of
an entomogenous fungus Paecilomyces tenuipes. J Invert Pathol 1997;70:203–208.
271 Cochet G: Sur un nouveau champignon arthrosporé (Arthrographis langeroni n. g., n. sp.), agent
pathogène d’une onychomycose humaine. Ann Parasitol Hum Comp 1939;17:97–102.
272 Scott JA, Malloch DW, Gloer JB: Polytolypa, an undescribed genus in the Onygenales. Mycologia
1993;85:503–508.
273 Leclerc MC, Philippe H, Guého E: Phylogeny of dermatophytes and dimorphic fungi based on
large subunit ribosomal RNA sequence comparisons. J Med Vet Mycol 1994;32:331–341.
274 Pan S, Sigler L, Cole GT: Evidence for a phylogenetic connection between Coccidioides immitis
and Uncinocarpus reesii (Onygenaceae). Microbiology 1994;140:1481–1494.
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 286

275 Sigler L: Agents of adiaspiromycosis; in Ajello L, Hay R (eds): Topley and Wilson’s Microbiology
and Microbial Infections, 9 ed. London, Arnold, 1998, pp 571–583.
276 Roilides E, Sigler L, Bibashi E, Katsifa H, Flaris N, Panteliadis C: Disseminated infection due
to Chrysosporium zonatum in a patient with chronic granulomatous disease and review of
non-Aspergillus fungal infections in patients with this disease. J Clin Microbiol 1999;37:18–25.
277 Sigler L, Flis AL, Carmichael JW: The genus Uncinocarpus (Onygenaceae) and its synonym
Brunneospora: New concepts, combinations and connections to anamorphs in Chrysosporium,
and further evidence of relationship with Coccidioides immitis. Can J Bot 1998;76:1624–1636.
278 Iwen PC, Sigler L, Tarantolo S, Sutton DA, Rinaldi MG, Lackner RP, McCarthy DI, Hinrichs SH:
Pulmonary infection caused by Gymnascella hyalinospora in a patient with acute myelogenous
leukemia. J Clin Microbiol 2000;38:375–381.
279 Rossman AY, Samuels GJ, Rogerson CT, Lowen R: Genera of Bionectriaceae, Hypocreaceae and
Nectriaceae (Hypocreales, Ascomycetes). Studies Mycol 1999;42:1–248.
280 Tarlo SM, Fradkin A, Tobin RS: Skin testing with extracts of fungal species derived from the
homes of allergy clinic patients in Toronto, Canada. Clin Allergy 1988;18:45–52.
281 O’Donnell K, Gherbawy Y, Schweigkofler W, Adler A, Prillinger H: Phylogenetic analyses of
DNA sequence and RAPD data compared in Fusarium oxysporum and related species from maize.
J Phytopathol 1999;147:445–452.
282 Sigler L, Abbott SP, Gauvreau H: Assessment of worker exposure to airborne molds in honeybee
overwintering facilities. Am Indust Hyg Assoc J 1996;57:484–490.
283 Kuhls K, Lieckfeldt E, Samuels GJ, Kovacs W, Meyer W, Petrini O, Gams W, Börner T,
Kubicek CP: Molecular evidence that the asexual industrial fungus Trichoderma reesi is a clonal
derivative of the ascomycete Hypocrea jecorina. Proc Natl Acad Sci USA 1996;93:7755–7760.
284 Kuhls K, Lieckfeldt E, Samuels GJ, Meyer W, Kubicek CP, Börner T: Revision of Trichoderma
sect. Longibrachiatum including related teleomorphs based on analysis of ribosomal DNA
internal transcribed spacer sequences. Mycologia 1997;89:442–460.
285 Turner D, Kovacs W, Kuhls K, Lieckfeldt E, Peter B, Arisan-Atac I, Strauss J, Samuels GJ, Börner
T, Kubicek CP: Biogeography and phenotypic variation in Trichoderma sect. Longibrachiatum
and associated Hypocrea species. Mycol Res 1997;101:449–459.
286 Vesper SJ, Dearborn DG, Yike I, Sorenson WG, Haugland RA: Hemolysis, toxicity, and randomly
amplified polymorphic DNA analysis of Stachybotrys chartarum strains. Appl Environ Microbiol
1999;65:3175–3181.
287 Tanada Y, Kaya HK: Insect Pathology. New York, Academic Press, 1993.
288 Paterson IC, Charnley AK, Cooper RM, Clarkson JM: Partial characterization of specific
inducers of a cuticle-degrading protease from the insect pathogenic fungus Metarhizium anisopliae.
Microbiology 1994;140:3153–3159.
289 Ito Y, Hirano T: The determination of the partial 18S ribosomal DNA sequences of Cordyceps
species. Lett Appl Microbiol 1997;25:239–242.
290 Messner R, Schweigkofler W, Ibl M, Berg G, Prillinger H: Molecular characterization of the plant
pathogen Verticillium dahliae Kleb. using RAPD-PCR and sequencing of the 18S rRNA-gene.
J Phytopathol 1996;144:347–354.
291 Hausner G, Reid J, Klassen GR: Ceratocystiopsis: A reappraisal based on molecular criteria.
Mycol Res 1993;97:625–633.
292 Hausner G, Reid J, Klassen GR: On the subdivision of Ceratocystis s.l., based on partial ribo-
somal DNA sequences. Can J Bot 1993;71:52–63.
293 Halmschlager E, Messner R, Kowalski T, Prillinger H: Differentiation of Ophiostoma piceae and
Ophiostoma quercus by morphology and RAPD analysis. Syst Appl Microbiol 1994;17:554–562.
294 Spatafora JW, Blackwell M: Molecular systematics of unitunicate perithecial Ascomycetes:
The Clavicipitales-Hypocreales connection. Mycologia 1993;85:912–922.
295 Spatafora JW, Blackwell M: The polyphyletic origins of ophiostomatoid fungi. Mycol Res 1994;
98:1–9.
296 Summerbell RC, Kane J, Krajden S, Duke EE: Medically important species and related
ophiostomatoid fungi; in Wingfield MJ, Seifert KA, Webber JF (eds): Ceratocystis and
Ophiostoma: Taxonomy, Ecology, and Pathology. St Paul, American Phytopathological Society,
1993, pp 185–192.
Systematics of the Ascomycota and Basidiomycota 287

297 Rieth H: Pilz-Datei: Erläuterungen zu einigen allergologisch wichtigen Dermatophyten, Hefen
und Schimmelpilzen, ed 5. Reinbek b. Hamburg, Allergopharma Joachim Ganzer KG, 1983.
298 Sutton BC: The genus Glomerella and its anamorph Colletotrichum; in Bailey JA, Jeger MJ (eds):
Colletotrichum: Biology, Pathology and Control. Wallingford, CAB International, 1992, pp 1–26.
299 Crous PW, Gams W, Wingfield MJ, van Wyk PS: Phaeoacremonium gen. nov. associated with wilt
and decline diseases of woody hosts and human infections. Mycologia 1996;88:786–796.
300 Masclaux F, Guého E, de Hoog GS, Christen R: Phylogenetic relationships of human-pathogenic
Cladosporium (Xylohypha) species inferred from partial LS rRNA sequences. J Med Vet Mycol
1995;33:327–338.
301 Barr ME: Prodromus to nonlichenized, pyrenomycetous members of class Hymenoascomycetes.
Mycotaxon 1990;39:43–184.
302 Berbee ML, Taylor JW: Convergence in ascospore discharge mechanism among pyrenomycete
fungi based on 18S ribosomal RNA gene sequence. Mol Phylogenet Evol 1992;1:59–71.
303 Wingfield MJ, de Berr C, Visser C, Wingfield BD: A new Ceratocystis species defined using
morphological and ribosomal DNA sequence comparisons. Syst Appl Microbiol 1996;19:
191–202.
304 Luttrell ES: The ascostromatic Ascomycetes. Mycologia 1955;47:511–532.
305 Schweigkofler W, Prillinger H: Untersuchungen von endophytischen und latent pathogenen Pilzen
aus Rebholz in Österreich und Südtirol. Mitt Klosterneuburg 1997;47:149–158.
306 Zalar P, de Hoog GS, Gunde-Cimerman N: Ecology of halotolerant dothideaceous black yeasts.
Stud Mycol 1999;43:38–48.
307 Karlsson-Borga A, Jonsson P, Rolfsen W: Specific IgE antibodies to 16 widespread mold genera
in patients with suspected mold allergy. Ann Allergy 1989;63:521–526.
308 Roeijmans HJ, de Hoog GS, Tan CS, Figge MJ: Molecular taxonomy and GC/MS of metabolites
of Scytalidium hyalinum and Nattrassia mangiferae (Hendersonula toruloidea). J Med Vet Mycol
1997;35:181–188.
309 LoBuglio KF, Berbee ML, Taylor JW: Phylogenetic origins of the asexual mycorrhizal symbiont
Cenococcum geophilum Fr. and other mycorrhizal fungi among the Ascomycetes. Mol Phylogenet
Evol 1996;6:287–294.
310 Breitenbach M, Achatz G, Oberkofler H, Simon B, Unger A, Lechenauer E, Kandler D, Ebner C,
Kraft D: Molecular characterization of allergens of Cladosporium herbarum and Alternaria
alternata. Int Arch Allergy Immunol 1995;107:458–459.
311 Berbee ML, Pirseyedi M, Hubbard S: Cochliobolus phylogenetics and the origin of known, highly
virulent pathogens, inferred from ITS and glyceraldehyde-3-phosphate dehydrogenase gene
sequences. Mycologia 1999;91:954–977.
312 Tsuda M, Ueyama A: Pseudocochliobolus australiensis, the ascigerous state of Bipolaris
australiensis. Mycologia 1981;73:88–96.
313 McAleer R, Kroenert DB, Elder JL, Froudist JH: Allergic bronchopulmonary disease caused by
Curvularia lunata and Drechslera hawaiiensis. Thorax 1981;36:338–344.
314 Hendrick DJ, Ellithorpe DB, Lyon F, Hattier P, Salvaggio JE: Allergic bronchopulmonary
helminthosporiosis. Am Rev Respir Dis 1982;126:935–938.
315 Bassiouny A, Maher A, Bucci TJ, Moawad MK, Hendawy DS: Noninvasive antromycosis
(diagnosis and treatment). J Laryngol Otol 1982;96:215–228.
316 Benoldi D, Alinovi A, Polonelli L, Conti S, Gerloni M, Ajello L, Padhye AA, de Hoog GS:
Botryomyces caespitosus as an agent of cutaneous phaeohyphomycosis. J Med Vet Mycol 1991;
29:9–13.
317 Pöder R, Scheuer C: Moserella radicicola gen. et sp. nov., a new hypogeous species of Leotiales
on ectomycorrhizas of Picea abies. Mycol Res 1994;98:1334–1338.
318 Holst-Jensen A, Kohn LM, Schumacher T: Nuclear rDNA phylogeny of Sclerotiniaceae.
Mycologia 1997;89:885–899.
319 Saenz GS, Taylor JW, Gargas A: 18S rRNA gene sequences and supraordinal classification of the
Erysiphales. Mycologia 1994;86:212–216.
320 O’Donnell K, Cigelnik E, Weber NS, Trappe JM: Phylogenetic relationships among ascomycetous
truffles and the true and false morels inferred from 18S and 28S ribosomal DNA sequence
analysis. Mycologia 1997;89:48–65.
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 288

321 Boekhout T, Roeijmans H, Spaay F: A new pleomorphic ascomycete, Calyptrozyma arxii gen. et
sp. nov., isolated from the human lower oesophagus. Mycol Res 1995;99:1239–1246.
322 Lehrer SB, Aukrust L, Salvaggio JE: Respiratory allergy induced by fungi. Clin Chest Med 1983;
4:23–41.
323 Patouillard NT: Essai taxonomique sur les familles et les genres des Hyménomycètes. Paris,
Lonsle-Saunier, 1900, pp 1–184.
324 Oberwinkler F: Was ist ein Basidiomycet? Z Mykol 1978;44:13–29.
325 Oberwinkler F: Anmerkungen zur Evolution und Systematik der Basidiomyceten. Bot Jahrb Syst
1985;107:541–580.
326 Lowy B: Taxonomic problems in the Heterobasidiomycetes. Taxon 1968;17:118–127.
327 Talbot PHB: Fossilized pre-Patouillardian taxonomy? Taxon 1968;17:620–628.
328 Donk MA: The heterobasidiomycetes: A reconnaissance. I. A restricted emendation. Proc Kon
Ned Akad Wetensch Ser C 1972;75:365–375.
329 Donk MA: The heterobasidiomycetes: A reconnaissance. Part IV. Proc Kon Ned Akad Wetensch
Ser C 1972;76:109–125.
330 Dörfler C: Vergleichende Untersuchungen zum biochemischen Aufbau der Zellwand an
Hefestadien von niederen und höheren Basidiomyceten. Bibl Mycol 1990;129:1–164.
331 Swann EC, Taylor JW: Higher taxa of Basidiomycetes: An 18S rRNA gene perspective.
Mycologia 1993;85:923–936.
332 Mueller UG, Rehner SA, Schultz TR: The evolution of agriculture in ants. Science 1998;281:
2034–2038.
333 Oberwinkler F, Bandoni R: Carcinomycetaceae: A new family in the Heterobasidiomycetes. Nord
J Bot 1982;2:501–516.
334 Ingold CT: Ballistospores in Melanotaenium endogenum. Trans Br Mycol Soc 1988;91:712–714.
335 Bauer R, Oberwinkler F, Vánky K: Ultrastructural markers in smut fungi and allied taxa. Can
J Bot 1997;75:1273–1314.
336 McLaughlin DJ, Frieders EM, Lü H: A microscopist’s view of heterobasidiomycete phylogeny.
Stud Mycol 1995;38:91–109.
337 Hibbett DS, Thorn RG: Basidiomycota: Homobasidiomycetes; in McLaughlin DJ, McLaughlin
EJ, Lemke PA (eds): The Mycota: Systematics and Evolution. Heidelberg, Springer, 2000, vol VII,
part B, pp 121–168.
338 Boekhout T, Fell JW, Fonseca A, Prillinger H, Lopandic K, Roeijmans H: The basidiomycetous
yeast Rhodotorula yarrowii comb. nov. Antonie Van Leeuwenhoek 2000;77:355–358.
339 Sadebeck R: Untersuchungen über die Pilzgattung Exoascus und die durch dieselbe um Hamburg
hervorgerufenen Baumkrankheiten. Jahrb Hamburg Wissensch Anst 1884;1:93–124.
340 Messner R, Prillinger H, Altmann F, Lopandic K, Wimmer K, Molnár O, Weigang F: Molecular
characterization and application of random amplified polymorphic DNA analysis of Mrakia and
Sterigmatomyces species. Int J Syst Bacteriol 1994;44:694–703.
341 O’Brien RW, Ralph BJ: The cell wall composition and taxonomy of some Basidiomycetes and
Ascomycetes. Ann Bot NS 1966;30:831–843.
342 Sjamsuridzal W, Nishida H, Ogawa H, Kakishima M, Sugiyama J: Phylogenetic positions of rust fungi
parasitic on ferns: Evidence from 18S rDNA sequence analysis. Mycoscience 1999;40: 21–27.
343 Khan SR, Kimbrough JW: A reevaluation of the Basidiomycetes based upon septal and basidial
structures. Mycotaxon 1982;15:103–120.
344 Oberwinkler F, Bauer R: The systematics of gasteroid, auricularioid Heterobasidiomycetes.
Sydowia 1989;41:224–256.
345 Boekhout T, Yamada Y, Weijman ACM, Roeymans HJ, Batenburg-van der Vegte WH: The
significance of Coenzyme Q, carbohydrate composition and septal ultrastructure for the taxonomy
of ballistoconidia-forming yeasts and fungi. Syst Appl Microbiol 1992;15:1–10.
346 Bauer R, Oberwinkler F: Meiosis, septal pore architecture, and systematic position of the
heterobasidiomycetous fern parasite Herpobasidium filicinum. Can J Bot 1994;72:1229–1242.
347 Suh S-O, Hirata A, Sugiyama J, Komagata K: Septal ultrastructure of basidiomycetous yeasts and
their taxonomic implications with observations on the ultrastructure of Erythrobasidium hasegaw-
ianum and Sympodiomycopsis paphiopedili. Mycologia 1993;85:30–37.
348 Wells K: Jelly fungi, then and now! Mycologia 1994;86:18–48.
Systematics of the Ascomycota and Basidiomycota 289

349 Deml G: Taxonomy of phragmobasidial smut fungi. Stud Mycol 1987;30:127–135.
350 Sampaio JP, Bauer R, Begerow D, Oberwinkler F: Occultifur externus sp. nov., a new species of
simple-pored auricularioid heterobasidiomycete from plant litter in Portugal. Mycologia 1999;
91:1094–1101.
351 Hamamoto M, Sugiyama J, Komagata K: Transfer of Rhodotorula hasegawae to a new
basidiomycetous genus Erythrobasidium as Erythrobasidium hasegawae comb. nov. J Gen Appl
Microbiol 1988;34:279–287.
352 Kuraishi H, Katayama-Fujimura Y, Sugiyama J, Yokoyama T: Ubiquinone systems in fungi. I.
Distribution of ubiquinones in the major families of ascomycetes, basidiomycetes, and
deuteromycetes, and their taxonomic implications. Trans Mycol Soc Jpn 1985;26:383–395.
353 Oberwinkler F: New genera of auricularioid heterobasidiomycetes. Rept Tottori Mycol Inst 1990;
28:113–127.
354 Celerin M, Day AW, Castle AJ, Laudenbach DE: A glycosylation pattern that is unique to fimbriae
from the taxon Microbotryales. Can J Microbiol 1995;41:452–460.
355 Bandoni RJ: Dimorphic Heterobasidiomycetes: Taxonomy and parasitism. Stud Mycol 1995;
39:13–28.
356 Bergman AG, Kauffman CA: Dermatitis due to Sporobolomyces infection. Arch Dermatol 1984;
120:1059–1060.
357 De Bary A: Untersuchungen über die Peronosporeen und Saprolegnieen und die Grundlagen eines
natürlichen Systems der Pilze. Abh Senckenb Naturf Ges 1881;12:225–370, Tafel 1–6.
358 Deml G, Bauer R, Oberwinkler F: Studies in Heterobasidiomycetes. 9. Axenic cultures of
Coleosporium tussilaginis (Uredinales). I. Isolation, identification and characterization of the
cultures. Phytopathol Z 1982;104:39–45.
359 Deml G, Bauer R, Oberwinkler F: Untersuchungen an Heterobasidiomyceten. 16. Axenische
Kultur von Coleosporium tussilaginis (Pers.) Lév. (Uredinales). II. Kreuzungsversuche mit
monokaryotischen Stämmen. Phytopathol Z 1982;103:149–155.
360 Boekhout T, Fell JW, O’Donnell K: Molecular systematics of some yeast-like anamorphs
belonging to the Ustilaginales and Tilletiales. Stud Mycol 1995;38:175–183.
361 Begerow D, Bauer R, Boekhout T: Phylogenetic placements of ustilaginomycetous anamorphs as
deduced from nuclear LSU rDNA sequences. Mycol Res 2000;104:53–60.
362 Bauer R, Vánky K, Begerow D, Oberwinkler F: Ustilaginomycetes on Selaginella. Mycologia
1999;91:475–484.
363 Schweizer HJ: Introduction to the plant bearing beds and the flora of the Lower Devonian of the
Rhineland. Bonner Paläobot Mitt 1987;13:1–94.
364 Bauer R, Oberwinkler F, Vánky K: Ustilaginomycetes on Osmunda. Mycologia 1999;91:
669–675.
365 Pryer KM, Smith AR, Skog JE: Phylogenetic relationships of extant ferns based on evidence from
morphology and rbcL sequences. Am Fern J 1995;85:205–282.
366 Moore RT: Taxonomic proposals for the classification of marine yeasts and other yeast-like fungi
including the smuts. Bot Mar 1980;23:361–373.
367 Takeo K, Nakai E: Mode of cell growth of Malassezia (Pityrosporium) as revealed by using
plasma membrane configurations as natural markers. Can J Microbiol 1986;32:389–394.
368 Guillot J, Guého E, Prévost MC: Ultrastructural features of the dimorphic yeast Malassezia
furfur. J Méd 1995;5:86–91.
369 Guého E, Midgley G, Guillot J: The genus Malassezia with description of four new species.
Antonie Van Leeuwenhoek 1996;69:337–355.
370 Boekhout T, Kamp M, Guého E: Molecular typing of Malassezia species with PFGE and RAPD.
Med Mycol 1998;36:365–372.
371 Guého E, Boekhout T, Ashbee HR, Guillot J, van Belkum A, Faergemann J: The role of
Malassezia species in the ecology of human skin and as pathogens. Med Mycol 1998;36(suppl 1):
220–229.
372 Boekhout T: A revision of ballistoconidia-forming yeasts and fungi. Stud Mycol 1991;33:1–194.
373 Urquhart EJ, Punja ZK: Epiphytic growth and survival of Tilletiopsis pallescens, a potential
biological control agent of Sphaerotheca fulginea on cucumber leaves. Can J Bot 1997;75:
892–901.
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 290

374 Takashima M, Nakase T: A phylogenetic study of the genus Tilletiopsis, Tilletiaria anomala and
related taxa based on the small subunit ribosomal DNA sequences. J Gen Appl Microbiol 1996;
42:421–429.
375 Ramani R, Kahn RT, Chaturvedi V: Tilletiopsis minor: A new etiologic agent of human subcuta-
neous mycosis in an immunocompromised patient. J Clin Microbiol 1997;35:2992–2995.
376 Moore RT: Micromorphology of yeasts and yeast-like fungi and its taxonomic implications. Stud
Mycol 1987;30:203–226.
377 Weijman ACM, de Hoog GS: Carbohydrate patterns and taxonomy of Sporothrix and Blastobotrys.
Antonie Van Leeuwenhoek 1985;51:111–120.
378 Middelhoven WJ, Guého E, de Hoog GS: Phylogenetic position and physiology of Cerinosterus
cyanescens. Antonie van Leeuwenhoek 2000;77:313–320.
379 Sigler L, Harris JL, Dixon DM, Flis AL, Salkin IF, Kemna M, Duncan RA: Microbiology
and potential virulence of Sporothrix cyanescens, a fungus rarely isolated from blood and skin.
J Clin Microbiol 1990;28:1009–1015.
380 Vánky K: Illustrated genera of smut fungi; in Jülich W (ed): Cryptogamic Studies. Stuttgart,
Fischer, 1987, vol 1, pp 1–159.
381 Takashima M, Nakase T: Molecular phylogeny of the genus Cryptococcus and related species
based on the sequences of 18S rDNA and internal transcribed spacer regions. Microbiol Cult Coll
1999;15:35–47.
382 Hibbett DS, Pine EM, Langer E, Langer G, Donoghue MJ: Evolution of gilled mushrooms and
puffballs inferred from ribosomal DNA sequences. Proc Natl Acad Sci USA 1997;94:
12002–12006.
383 Pine EM, Hibbett DS, Donoghue MJ: Phylogenetic relationships of cantharelloid and clavariod
Homobasidiomycetes based on mitochondrial and nuclear rDNA sequences. Mycologia 1999;
91:944–963.
384 Maire R: Recherches cytologiques et taxonomiques sur les Basidiomycètes. Bull Soc Mycol Fr
1902;18:1–212.
385 Gäumann E: Vergleichende Morphologie der Pilze. Jena, Fischer, 1926.
386 Kreisel H: Grundzüge eines natürlichen Systems der Pilze. Lehre, Cramer, 1969.
387 Hibbett DS, Grimaldi D, Donoghue MJ: Fossil mushrooms from Miocene and Cretaceous ambers
and the evolution of homobasidiomycetes. Am J Bot 1997;84:981–991.
388 Kwon-Chung KJ: Filobasidiaceae – A taxonomic survey. Stud Mycol 1987;30:75–85.
389 Boekhout T, van Belkum A, Leenders ACAP, Verbrugh HA, Mukamurangwa P, Swinne D,
Scheffers WA: Molecular typing of Cryptococcus neoformans: Taxonomic and epidemiological
aspects. Int J Syst Bacteriol 1997;47:432–442.
390 Fell JW, Kurtzman CP, Kwon-Chung KJ: Proposal to conserve Cryptococcus (Fungi). Taxon 1989;
38:151–152.
391 Kwon-Chung KJ, Polacheck I, Bennett JE: Improved diagnostic medium for separation of
Cryptococcus neoformans var. neoformans (serotypes A and D) and Cryptococcus neoformans
var. gattii (serotypes B and C). J Clin Microbiol 1982;15:535–537.
392 Swinne D: Study of Cryptococcus neoformans varieties. Mykosen 1984;27:137–141.
393 Dufait R, Velho R, de Vroey C: Rapid identification of the two varieties of Cryptococcus
neoformans by D-proline assimilation. Mykosen 1987;30:483.
394 Kwon-Chung KJ: Filobasidium; in Kurtzman CP, Fell JW (eds): The Yeasts, a Taxonomic Study,
ed 4, rev. Amsterdam, Elsevier, 1998, pp 663–669.
395 Guého E, Smith MT, de Hoog GS, Billon-Grand G, Christen R, Batenburg-van der Vegte WH:
Contributions to a revision of the genus Trichosporon. Antonie Van Leeuwenhoek 1992;61:289–316.
396 Fell JW, Roeijmans H, Boekhout T: Cystofilobasidiales, a new order of basidiomycetous yeasts.
Int J Syst Bacteriol 1999;49:907–913.
397 Guého E, Improvisi L, Christen R, de Hoog GS: Phylogenetic relationships of Cryptococcus
neoformans and some related basidiomycetous yeasts determined from partial large subunit
rRNA. Antonie Van Leeuwenhoek 1993;63:175–189.
398 Bruns TD, Szaro TM, Gardes M, Cullings KW, Pan JJ, Taylor DL, Horton TR, Kretzer A,
Garbelotto M, Li Y: A sequence database for the identification of ectomycorrhizal basidiomycetes
by phylogenetic analysis. Mol Ecol 1998;7:257–272.
Systematics of the Ascomycota and Basidiomycota 291

399 Langer G: Die Gattung Botryobasidium Donk (Corticiaceae, Basidiomycetes). Bibl Mycol
1994;158:1–459.
400 Keller J: Atlas der Basidiomycetes. Neuchâtel, Union des Sociétés Suisses de Mycologie, 1997.
401 Corner EJH: A monograph of Clavaria and allied genera. Ann Bot Mém 1950;2:1–740.
402 Jülich W: Higher Taxa of Basidiomycetes. Vaduz, Cramer, 1981.
403 Donk MA: A conspectus of the families of the Aphyllophorales. Persoonia 1964;3:199–324.
404 Bresinsky A, Rennschmid A: Pigmentmerkmale, Organisationsstufen und systematische Gruppen
bei höheren Pilzen. Ber Dtsch Bot Ges 1971;84:313–329.
405 Hibbett DS, Donoghue MJ: Progress toward a phylogenetic classification of the Polyporaceae through
parsimony analyses of mitochondrial ribosomal DNA sequences. Can J Bot 1995; 73(suppl 1):
s853–s861.
406 Moore RT: Taxonomic significance of septal ultrastructure in the genus Onnia Karsten
(Polyporineae/Hymenochaetaceae). Bot Notiser 1980;133:169–175.
407 Mims CW, Seabury F: Ultrastructure of tube formation and basidiospore development in
Ganoderma lucidum. Mycologia 1989;81:754–764.
408 Esser K, Stahl U, Meinhardt F: Genetic aspects of differentiation in fungi; in Meyrath J,
Bullock JD (eds): Biotechnology and Fungal Differentiation. New York, Academic Press, 1977,
pp 67–75.
409 Rosinski MA, Robinson AD: Hybridization of Panus tigrinus and Lentodium squamulosum.
Am J Bot 1968;55:242–246.
410 Sigler L, Abbott SP: Characterizing and conserving diversity of filamentous Basidiomycetes from
human sources. Microbiol Cult Coll 1997;13:21–27.
411 Moore RT: The challenge of the dolipore septum; in Moore D, Casselton LA, Wood DA,
Frankland JC (eds): Developmental Biology of Higher Fungi. Cambridge, Cambridge University
Press, 1985, pp 175–212.
412 Langer E, Oberwinkler F: Corticoid basidiomycetes. I. Morphology and ultrastructure. Windahlia
1993;20:1–28.
413 Langer E: Die Gattung Hyphodontia John Eriksson. Bibl Mycol 1994;154:1–298.
414 Redhead SA, Norvell L: Notes on Bondarzewia,Heterobasidion and Pleurogala. Mycotaxon
1993;48:371–380.
415 Jahn H: Pilze, die an Holz wachsen. Herford, Bussesche Verlagshandlung, 1979.
416 Bresinsky A, Bachmann R: Bildung von Pulvinsäurederivaten durch Hygrophoropsis aurantiaca
(Paxillaceae-Boletales) in vitro. Z Naturforsch 1971;26b:1086–1087.
417 Nilsson T, Ginns J: Cellulolytic activity and the taxonomic position of selected brown-rot fungi.
Mycologia 1979;71:170–177.
418 Besl H, Bresinsky A, Kämmerer A: Chemosystematik der Coniophoraceae. Z Mykol 1986;52:
277–286.
419 Besl H, Dorsch R, Fischer M: Zur verwandtschaftlichen Stellung der Gattung Melanogaster
(Melanogastraceae, Basidiomycetes). Z Mykol 1996;62:195–199.
420 Bresinsky A, Jarosch M, Fischer M, Schönberger I, Wittmann-Bresinsky B: Phylogenetic
relationships within Paxillus s. l. (Basidiomycetes, Boletales): Separation of a Southern hemi-
sphere genus. Plant Biol 1999;1:327–333.
421 Binder M, Besl H, Bresinsky A: Agaricales oder Boletales? Molekularbiologische Befunde
zur Zuordnung einiger umstrittener Taxa. Z Mykol 1997;63:189–196.
422 Gill M, Steglich W: Pigments of fungi (Macromycetes). Prog Chem Org Nat Prod 1987;51:1–317.
423 Kämmerer A, Besl H, Bresinsky A: Omphalotaceae fam. nov. und Paxillaceae, ein
chemotaxonomischer Vergleich zweier Pilzfamilien der Boletales. Plant Syst Evol 1985;150:
101–117.
424 Bresinsky A, Besl H: A Colour Atlas of Poisonous Fungi. London, Wolfe, 1990.
425 Jarosch M, Bresinsky A: Speciation and phylogenetic distances within Paxillus s. str.
(Basidiomycetes, Boletales). Plant Biol 1999;1:701–706.
426 Helbling A, Brander KA, Horner WE, Lehrer SB: Allergy to basidiomycetes. Chem Immunol.
Basel, Karger, 2002, vol 81, pp 28–47.
427 Nuss I: Untersuchungen zur systematischen Stellung der Gattung Polyporus. Hoppea 1980;
39:127–198.
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 292

428 Sigler L, de la Maza LM, Tan G, Egger KN, Sherburne RK: Diagnostic difficulties caused by a
nonclamped Schizophyllum commune isolate in a case of fungus ball of the lung. J Clin Microbiol
1995;33:1979–1983.
429 Kamei K, Unno H, Nagao K, Kuriyama T, Nishimura K, Miyaji M: Allergic bronchopulmonary
mycosis caused by the basidiomycetous fungus Schizophyllum commune. Clin Infect Dis 1994;
18:305–309.
430 Ciferri R, Chavez Batista A, Campos S: Isolation of Schizophyllum commune from sputum.
Atti Inst Bot Lab Crittogam Univ Pavia 1956;14:118–120.
431 Chavez-Batista A, Maia JA, Singer R: Basidioneuromycosis of man. Anais Soc Biol Pernambuco
1955;13:52–60.
432 Catalano P, Lawson W, Bottone E, Lebenger J: Basidiomycetous (mushroom) infection of the
maxillary sinus. Otolaryngol Head Neck Surg 1990;102:183–185.
433 Rosenthal J, Katz R, DuBois DB, Morrissey A, Machicao A: Chronic maxillary sinusitis associ-
ated with the mushroom Schizophyllum commune in a patient with AIDS. Clin Infect Dis 1992;
14:46–48.
434 Sigler L, Bartley JR, Parr DH, Morris AJ: Maxillary sinusitis caused by medusoid form of
Schizophyllum commune. J Clin Microbiol 1999;37:3395–3398.
435 Restrepo A, Greer DL, Robledo M, Osorio O, Mondragon H: Ulceration of the palate caused by
a basidiomycete Schizophyllum commune. Sabouraudia 1973;9:201–204.
436 Kligman AM: A basidiomycete probably causing onychomycosis. J Invest Dermatol 1950;14:
67–70.
437 Kühner R: Les Hyménomycètes agaricoides (Agaricales, Tricholomatales, Pluteales, Russulales).
Numéro spécial du Bulletin de la Sociéte Linnéenne de Lyon, 1980.
438 Singer R: The Agaricales in Modern Taxonomy, ed 4, rev. Koenigstein, Koeltz Scientific
Books, 1986.
439 Pegler DN: The genus Lentinus, a world monograph. Kew Bull Add Ser 1983;10:1–281.
440 Hibbett DS, Vilgalys R: Phylogenetic relationships of Lentinus (Basidiomycotina) inferred from
molecular and morphological characters. Syst Bot 1993;18:409–433.
441 Thorn RG, Moncalvo J-M, Reddy CA, Vilgalys R: Phylogenetic analyses and the distribution of
nematophagy support a monophyletic Pleurotaceae within the polyphyletic pleurotoid-lentinoid
fungi. Mycologia 2000;92:241–252.
442 Lee S-S, Jung HS: Phylogenetic analysis of the Corticiaceae based on gene sequences of nuclear
18S ribosomal DNAs. J Microbiol 1997;35:253–258.
443 Mueller GM, Pine EM: DNA data provide evidence on the evolutionary relationships between
mushrooms and false truffles. McIlvainea 1994;11:61–74.
444 Hopple JS, Vilgalys R: Phylogenetic relationships among coprinoid taxa and allies based on data
from restriction site mapping of nuclear rDNA. Mycologia 1994;86:96–107.
445 Hofmann A, Heim R, Brack A, Kobel H, Frey A, Ott H, Petrzilka T, Troxler F: Psilocybin and
Psilocin. Helv Chim Acta 1959;42:1557–1572.
446 Welsh J, McClelland M: Fingerprint genomes using PCR with arbitrary primers. Nucleic Acids
Res 1990;18:7213–7218.
447 Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV: DNA-polymorphisms amplified
by arbitrary primers are useful as genetic markers. Nucleic Acids Res 1990;18:6531–6535.
448 Molnár O, Prillinger H, Lopandic K, Weigang F, Staudacher E: Analysis of coenzyme Q systems,
monosaccharide patterns of purified cell walls, and RAPD-PCR patterns in the genus
Kluyveromyces. Antonie Van Leeuwenhoek 1996;70:67–78.
449 Lopandic K, Prillinger H, Molnár O, Giménez-Jurado G: Molecular characterization and
genotypic identification of Metschnikowia species. Syst Appl Microbiol 1996;19:393–402.
450 Molnár O, Messner R, Prillinger H, Stahl U, Slavikova E: Genotypic identification of
Saccharomyces species using random amplified polymorphic DNA analysis. Syst Appl Microbiol
1995;18:136–145.
451 Molnár O, Messner R, Prillinger H, Scheide K, Stahl U, Silberhumer H, Wunderer W:
Genotypische Identifizierung von Saccharomyces-Arten aus der Getränkeindustrie mit Hilfe der
Zufallsprimer-abhängigen Polymerase-Kettenreaktion (RAPD-PCR). Mitt Klosterneuburg
1995;45:113–122.
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452 Prillinger H, Kraepelin G, Lopandic K, Schweigkofler W, Molnár O, Weigang F, Dreyfuss MM:
New species of Fellomyces isolated from epiphytic lichen species. Syst Appl Microbiol 1997;
20:572–584.
453 Vos P, Hogers R, Bleeker M, Reijaus M, van de Lee T, Hornes M, Frijtens A, Pot J, Peleman J,
Kuiper M, Zabeau M: AFLP: A new technique for DNA fingerprinting. Nucleic Acids Res
1995;23:4407–4414.
454 Aarts H, Keijer J: Genomic Fingerprinting of Micro-Organisms by Automatic Laser Fluorescence
Analysis (ALFA) of Amplified Fragment Length Polymorphism (AFLP™); in Akkermans ADL,
van Elsas JD, de Bruijn FJ (eds): Molecular Microbial Ecology Manual 3.4.9. Dordrecht, Kluwer
Academic, 1999.
455 Laaser G, Möller E, Jahnke KD, Bahnweg G, Prillinger H, Prell HH: Ribosomal DNA restriction
fragment analysis as a taxonomic tool in separating physiologically similar Basidiomycetous
yeasts. Syst Appl Microbiol 1989;11:170–175.
Notes added in proof
The 2nd edition of the Atlas of Clinical Fungi [De Hoog et al., 2000] includes 65 addi-
tional clinical fungi. It often presents small subunit, large subunit or ITS restriction maps
for genotypic identification. According to the data of Binder and Hibbett [2002], the
Schizophyllales can be included among the euagarics. A publication by Sterflinger and
Prillinger [2001] presents molecular evidence that the genera Phoma and Epicoccum can
be included among the Pleosporales. According to Sugita et al. [2000], C. laurentii is a
genetically heterogeneous species; this must be taken into consideration when identifying
C. laurentii clinical isolates. Data by Sugita et al. [in press] suggest that the IGS region has a
powerful capacity of distinguishing between phylogenetically closely related strains and that
there may be a geographic substructure among T. ashai clinical isolates. O’Donnell et al.
[2001] and Voigt and Wöstemeyer [2001] present overviews on the phylogenetic relationship
among the Zygomycota. Sterflinger et al. [1999] describe the RFLP technique used in the
new edition of the Atlas of Clinical Fungi [Hoog et al., 2000]. Dr. C. Kurtzman kindly
showed us, with strongly deleted files, that the alignment in the Ascomycota becomes much
better. With these files the Archiascomycetes sensu Nishida and Sugiyama move into a basal
position. Sipiczki [2001] presents molecular data on the Archiascomycetes; however, he did
not find many similarities between the Archiascomycetes and the Basidiomycota (e.g. 5S rDNA
of Taphrina, enteroblastic budding, carotin pigments in Saitoella).
New notes on Ascomycota can be obtained from Myconet, vol. 6, 2001, edited by
O.E. Eriksson.
References
Binder M, Hibbett DS: Higher-level phylogenetic relationships of the Homobasidiomycetes (mushroom-
forming fungi) inferred from four rDNA regions. Mol Phylogenet Evol 2002;22:76–90.
De Hoog GS, Guarro J, Gené J, Figueras MJ (eds): Atlas of Clinical Fungi, ed 2. Centraalbureau voor
Schimmelcultures, Utrecht/Universitat Rovira i Virgili, Reus, 2000.
O’Donnell K, Lutzoni F, Ward TJ, Benny GL: Evolutionary relationships among mucoralean fungi
(Zygomycota): Evidence for family polyphyly on a large scale. Mycologia 2001;93:286–296.
Sipiczki M: Identification of Schizosaccharomyces pombe genes that encode putative homologues of
Saccharomyces cerevisiae mediator complex subunits. Acta Microbiol Immunol Hung
2001;48:519–531.
Prillinger/Lopandic/Schweigkofler/Deak/Aarts/Bauer/Sterflinger/Kraus/Maraz 294

Sterflinger K, de Hoog GS, Haase G: Phylogeny and ecology of meristematic ascomycetes. Stud Mycol
1999;43:5–22.
Sterflinger K, Prillinger H: Molecular taxonomy and biodiversity of rock fungal communities in an
urban environment (Vienna, Austria). Antonie van Leeuwenhoek 2001;80:275–286.
Sugita T, Nakajima M, Ikeda R, Matsushima T, Shinoda T: Molecular analysis of intergenic spacer 1
region of the rRNA gene of Trichosporon species. J Clin Microbiol, in press.
Sugita T, Takashima M, Ideka R, Nakase T, Shinoda T: Intraspecies diversity of Cryptococcus laurentii
as revealed by sequences of internal transcribed spacer regions and 28S rDNA gene and taxo-
nomic positions of C. laurentii clinical isolates. J Clin Microbiol 2000;38:1468–1471.
Voigt K, Wöstemeyer J: Phylogeny and origin of 82 zygomycetes from all 54 genera of the Mucorales
and Mortierellales based on combined analysis of actin and translation elongation factor EF-1
genes. Gene 2001;270:113–120
Prof. DI. Dr. Hansjörg Prillinger, Universität für Bodenkultur,
Institut für Angewandte Mikrobiologie, Arbeitsgruppe Mykologie und Bodenmikrobiologie,
Muthgasse 18, A–1190 Wien (Austria)
Tel. 43 1 36006 6207, Fax 43 1 3697615, E-Mail H.Prillinger@iam.boku.ac.at
Systematics of the Ascomycota and Basidiomycota 295