ArticlePDF Available

Dr. Robert Bauer (1950-2014) in memoriam: botanist, mycologist, and electron microscopist

Authors:

Abstract

Unexpectedly and tragically, Robert Bauer died September 7, 2014. He was born March 20, 1950 in Großbettlingen, Baden- Württemberg. After qualification as a metal craftsman, he decided to study biology at the University of Tübingen, where he obtained a diploma for his study BSporenbildung bei Coleosporium tussilaginis (Pers.) Lév.^ in 1980. He continued an experimental approach to elucidate ontogenetic and karyological features in rust fungi and finished his dissertation BExperimentell-ontogenetische und karyologische Untersuchungen an Uredinales^ in 1983. Expanding such studies in related groups, Bauer became more andmore interested in smuts, developed special skills for transmission electron microscopy, and successfully combined culture work on fungi with newly available techniques and organisms. This reappraisal of Bauer’s contributions to mycology is arranged systematically and partly chronologically and includes exclusively his publications as author or coauthor. A list of these scientific publications concludes this tribute to him with the intention to unroll a scientist’s life dedicated to fungi and their hosts.
OBITUARY
Dr. Robert Bauer (1950-2014) in memoriam: botanist, mycologist,
and electron microscopist
Franz Oberwinkler
1
Received: 17 August 2015 /Accepted: 21 September 2015
#German Mycological Society and Springer-Verlag Berlin Heidelberg 2015
Unexpectedly and tragically, Robert Bauer died September 7,
2014. He was born March 20, 1950 inGroßbettlingen, Baden-
Württemberg. After qualification as a metal craftsman, he de-
cided to study biology at the University of Tübingen, where he
obtained a diploma for his study BSporenbildung bei
Coleosporium tussilaginis (Pers.) Lév.^in 1980. He continued
an experimental approach to elucidate ontogenetic and kary-
ological features in rust fungi and finished his dissertation
BExperimentell-ontogenetische und karyologische
Untersuchungen an Uredinales^in 1983. Expanding such stud-
ies in related groups, Bauer became more and more interested in
smuts, developed special skills for transmission electron
microscopy, and successfully combined culture work on fungi
with newly available techniques and organisms.
This reappraisal of Bauers contributions to mycology is
arranged systematically and partly chronologically and in-
cludes exclusively his publications as author or coauthor. A
list of these scientific publications concludes this tribute to
him with the intention to unroll a scientistslifededicatedto
fungi and their hosts.
Pucciniomycotina, rust fungi, and related taxa
The nomenclature for the subdivision Pucciniomycotina of
Basidiomycota was introduced by Bauer et al. (2006). It in-
cluded a systematic and phylogenetic rearrangement of taxa
down to ordinal level (Fig. 1). It is a comprehensive overview
that since then is called Bsimple-septate basidiomycetes^and
was adopted by later studies of Aime et al. (2006) and Hibbett
et al. (2007), of which Bauer was coauthor.
Cryptomycocolax abnormis was described by Oberwinkler
and Bauer (1990) from material collected on the volcano
Irazú, Costa Rica, in which the species parasitizes an ascomy-
cete through two types of colacosomes. One of these
colacosomes was described by Oberwinkler et al. (1990a)
and Bauer and Oberwinkler (1991) from Platygloea
peniophorae. The simple-pored septa of C. abnormis are as-
sociated with Woronin body-like structures, a characteristic,
found in basidiomycetes only in one additional species,
Colacosiphon filiformis (Kirschner et al. 2001). The interphase
of nuclear division shows spindle pole bodies (SPBs) whose
position, structure, and duplication are similar to those of asco-
mycetes. In late interphase, SPB middle pieces as in basidiomy-
cetes are developed. These subcellular organelles support the
interpretation that Cryptomycocolacomycetes range in a basal
position of basidiomycetous phylogeny, a view supported by
molecularly based hypotheses (Bauer et al. 2006). The apparent-
ly convergent occurrence of the colacosomes, unique
mycoparasitic cell organelles in Cryptomycocolacomycetes
and Microbotryomycetes was discussed by Bauer et al. (2006).
Several collections of Mixia osmundae from Japan were
kindly provided by Junta Sugiyama for electronmicroscopic
studies. Unfortunately, unambiguous stages of nuclear divi-
sions in the Mixia sporangium could not be detected. Thus,
it remained unsolved whether Mixia propagules are
meiospores or conidia. However, subcellular characteristics
of cell walls and SPBs indicate a basal position of
M. osmundae in Basidiomycota, an interpetation supported
by molecular data (Weiß et al. 2004a, Aime et al. 2006,
Bauer et al. 2006). The order Mixiales and the class
Mixiomycetes were introduced by Bauer et al. (2006).
Section Editor: Dominik Begerow
*Franz Oberwinkler
franz.oberwinkler@uni-tuebingen.de
1
Universität Tübingen, Tübingen, Germany
Mycol Progress (2015) 14:98
DOI 10.1007/s11557-015-1120-5
Ontogenetic studies in phragmobasidia of Agaricostilbum
pulcherrimum, Gymnosporangium clavariiforme,
Helicogloea lagerheimii, Phleogena faginea, Platygloea
peniophorae,andSphacelotheca polygoni-persicariae
(Bauer and Oberwinkler 1986a) under different experimental
conditions led to the conclusion that external factors, such as
air, water, and water agar, strongly influence germination pat-
terns. They can induce the formation of ballistospores,
microconidia, or yeast cells. Also, hyphae with terminal ap-
pressoria can be formed. The authors concluded that with the
formation of basidial cells, the meiosporangial ontogeny is
terminated. Meiosis and its SPB cycle of A. pulcherrimum
were studied with a transmission electron microscope
(Bauer et al. 1992). Together with Spiculogloeales, the
Agaricostilbales were placed in the Agaricostilbomycetes
(Bauer et al. 2006). A new anamorphic yeast,
Kurtzmanomyces insolitus, was described by Sampaio et al.
(1999b). Molecular studies (Weiß et al. 2004, Aime et al.
2006, Bauer et al. 2006, Bauer et al. 2009) confirmed a basal
position of Agaricostilbomycetes within the Pucciniomycotina.
Members of Spiculogloeales (Bauer et al. 2006) are
mycoparasites with tremelloid haustoria.
In a revision of the gasteroid, auricularioid
heterobasidiomycetes, Oberwinkler and Bauer (1989) studied
basidiocarps, hyphae, cell organelles, basidia, basidiospores,
yeasts, and conidia. They also considered the available data of
5S RNAs and recognized complex subcellular structures such
as symplechosomes, apparently synapomorphic for members
of the Atractiellales. As a taxonomical consequence for
stilboid, gasteroid taxa they proposed Agaricostilbales,
Agaricostilbaceae, Pachnocybaceae, and Atractogloeaceae.
Later, two pycnidial atractielloid basidiomycetes, the
teleomorph Basidiopycnis hyalina and the anamorph
Proceropycnis pinicola, were described (Oberwinkler et al.
2006). Still enigmatic is the report of atractielloid fungi as
mycosymbionts in epiphytic neotropical orchids (Kottke
et al. 2010).
The teleomorphic genus Classicula and the anamorphic
Jaculispora were included in the Classiculales (Bauer et al.
2003), later raised to Classiculomycetes (Bauer et al. 2006).
Classicula fluitans is the basidial stage of Naiadella fluitans.
They are mycoparasites with tremelloid haustoria. In
Naohidea sebacea, Bauer (2004) detected nanometer pores
in the intracellular haustoria of this mycoparasite, and Weiß
et al. (2004) supported the phylogenetic position of the
Naohideales in the Cystobasidiomycetes by molecular data.
Occultifur internus, a mycoparasite growing in the
basidiocarps of Dacrymycetes species, has tremelloid
haustoria with nanometer pores and septal pores with
cystosomes (Bauer 2004). Sampaio et al. (1999a) found
Occultifur externus, developing basidial stages under labora-
tory conditions, and the affiliation to Cystobasidiales could
be proven.
Meiosis, spindle pole cycle, and septal pores of
Herpobasidium filicinum,Platygloeales were studied trans-
mission electron microscopically by Bauer and Oberwinkler
(1994).
Spectacular results were derived from intensive studies in
Tuberculina spp., Helicobasidiales, turning out to be
anamorphs of Helicobasidium (Lutz et al. 2004a), and
mycoparasites of the comparatively closely related rust fungi.
The identity of Tube rcu lina spp. and Helicobasidium spp. was
Fig. 1 Simplified phylogeny of
Pucciniomycotina. The ordinal
phylogeny and the listed genera
are intended to serve as a
guideline for the accompanying
text. The genus Bauerago,
dedicated to Robert Bauer, is a
member of the Microbotryales
98 Page 2 of 11 Mycol Progress (2015) 14:98
proven experimentally (Lutz et al. 2004b). Bauer et al. (2004)
studied Tube rculina p er sicina parasitizing Puccinia silvatica
and Tranzschelia pruni-spinosae. They found micrometer fu-
sion channels between parasite and host cells, apparently
allowing transfer of cell organelles. Experiments to elucidate
host specificities revealed a high diversity of the
mycoparasites (Lutz et al. 2004c). Two reports about BThe
double life of a fungus^were published by the German
Research Council, DFG (Lutz et al. 2006, 2007).
The ontogeny of basidia and nuclear changes in Pucciniales
were studied by Bauer (1983, 1986, 1987) in experimental
approaches. Axenic cultures of Coleosporium (Deml et al.
1982a, b) later turned out to be yeast contaminations. Bauer
found that secondary spore formation depends on the
monokaryotic stage. Nuclear degeneration during ballistospore
production was investigated in Cronartium asclepiadeum
(Bauer and Oberwinkler 1988). The unusual case of gasteroid
basidia in Ochropsora ariae was studied in vivo and in vitro
(Bauer and Oberwinkler 1986b), and the ultrastructure of the
host-parasite interface in the fern rusts Milesia, Uredinopsis,
and Hyalopsora was analysed (Berndt et al. 1994). The
morphology and phylogenetics of Stomatisora, including
Stomatisora psychotriicola sp. nov., were investigated by
Wood et al. (2014).
Comprehensive transmission electron microscopic studies
resulted in data that allowed reconstructing meiosis and SPB
cycle in Pachnocybe ferruginea (Bauer and Oberwinkler
1990c), a species that was raised in taxonomic ranks to
Pachnocybaceae (Oberwinkler and Bauer 1989) and
Pachnocybales (Bauer et al. 2006).
The detection of auricularioid basidia with sessile,
tetraradiate basidiospores in the pycnidioid Hyalopycnis
blepharistoma led to the introduction of Heterogastridium
pycnidioideum (Oberwinkler et al. 1990b). All members of
the Heterogastridiales are mycoparasites and possess
colacosomes (Bauer 2004), as described by Oberwinkler
et al. (1990a) and Bauer and Oberwinkler (1991) from
Platygloea peniophorae,thennamedColacogloea
peniophorae. A second species, C. bispora, parasitizing
Tubulicrinis sp., with collections from Denmark and Taiwan,
was described by Oberwinkler et al. (1999). A new species,
vectored by bark beetles on conifers was isolated, cultivated,
and described in a new genus, Atractocolax pulvinatus
(Kirschner et al. 1999).
On the basis of nutritional, ultrastructural, and molecular
data, Sampaio et al. (2003) proposed the new orders
Leucosporidiales and Sporidiobolales, the new genus
Leucosporidiella and the new species Leucosporidium
golubevii.
A smut collected in Madeira on Polygonum persicaria was
described as the new species Sphacelotheca polygoni-
persicariae (Deml et al. 1985) and considered to be related
to those of the genus Microbotryum because of their obvious
similarities.Inacomparativeultrastructuralstudyof
Sphacelotheca polygoni-serrulati and Ustilago spp., Bauer
et al. (1989) realised that hyphal septa of these false and true
smuts differ markedly. In Ustilago, the septal ingrowth stops,
leaving a central pore, while in S. polygoni-serrulati,septal
pores could not be found. Meiosis and SPB cycle of this spe-
cies were studied by Bauer et al. (1991), and that of
Microbotryum violaceum by Berbee et al. (1990), and com-
pared with the corresponding features of Ustilago maydis and
Sphacelotheca polygoni-serrulati. Analysing cell wall carbo-
hydrates, Prillinger et al. (1993) succeeded in separating
Ustilago s. str., Sporisorium, Entyloma,andMelanotaenium
from Microbotryum and Sphacelotheca, later transferred to
their own order, Microbotryales (Bauer et al. 1997). The
genus Bauerago, introduced for Ustilago species parasitizing
Cyperus, Juncus,andLuzula hosts, could be verified subsequent-
ly by molecular analyses (Bauer et al. 2006). Also, Fulvisporium
is a genus in the Microbotryales (Vánky et al.1997). A well
illustrated life cycle of Microbotryum lychnidis-dioicae on
Silene latifolia was published by Schäfer et al. (2010).
The unique basidiomycetous parasite Kriegeria eriophori,
only found in scattered regions and occurring in aerenchymas
of Scirpus, was studied intensively light and electron micro-
scopically as well as molecularly (Bauer et al. 2006). Multi-
pored hyphal septa were detected, unique at that time for
Basidiomycota, but later also found in Bartheletia paradoxa
(see below).
Ustilaginomycotina, true smut fungi
In the context of our research preferences, smut fungi became
the main objects of Robert Bauer, to be studied with a trans-
mission electron microscope intensively and comprehensively
since the end of the 1980s. In addition, it is important to
mention here that many controversial discussions were going
on in our teaching and lab programmes about host dependen-
cies of specialised parasitic fungi in general, but with a main
focus on rusts and smuts. It was already well understood that
Pucciniales passed through a close coevolutionary history
with their host plants. In contrast, Ustilaginales were generally
assumedtolacksuchtraits,and species-rich genera with
broadly spreading host ranges, like Urocystis and Ustilago,
was considered convincing evidence. However, when it be-
came clear that, for example, Exobasidium and Graphiola
belong to the smut relationship, and the heterogeneity of
Ustilago was elucidated step by step in our group, the attitude
switched completely. Very quickly, smuts underwent a re-
markable series of taxonomic reappraisals.
For the convenience of the reader, the phylogeny within the
class (Fig. 2), as published by Bauer et al. (1997), is used here
as guideline for the following text. The morphological and
ultrastructural characters studied before, and interpreted
Mycol Progress (2015) 14:98 Page 3 of 11 98
comparatively, were applied in a cladistic approach to propose
a new systematic arrangement with the intention of a phylo-
genetic concept. After step by step approval of this phylogeny
through newly coming up molecular hypotheses (Begerow
et al. 1997, Bauer et al. 1998, Begerow et al. 2006), the class
was taxonomically raised to subdivisional level (Bauer et al.
2006). Because there were no justifying data to exclude smuts,
such as BUstomycota^, from Basidiomycota, Bauer and
Oberwinkler (1997) rejected this proposal rigorously. The
new data on smuts accumulated since then were summarised
by Bauer et al. (2001a) and accepted in following generalizing
treatments (Hibbett et al. 2007). Teliospore development, ul-
trastructure, liberation, and dispersal in Ustilaginales and
Tilletiales as well as in Microbotryum, were studied in 120
species of 37 genera by Piepenbring et al. (1998a-c). The
cellular and subcellular ustilaginomycete-host interactions
were outlined by Bauer and Oberwinkler (2004). Based on
sequence data, yeasts of smuts could be integrated in the
new phylogenetic system of Begerow et al. (2000). Bauer
contributed also to assembling the fungal tree of life (Celio
et al. 2006).
Traditionally, Entorrhiza species, parasitizing root cells of
Cyperaceae and Juncaceae, were classified as smuts (Fig. 2).
They were studied in our institute intensively. When maturing,
the intracellulary grown smut spores are internally divided
into four cells, each of them producing a germination hypha
(Bauer et al. 2001a). Using ultrastructural and molecular data,
Bauer et al. (1997) and Begerow et al. (1997) classified the
Entorrhizales as sister to the remaining smuts. Entorrhizaceae
and Entorrhizales were described by Bauer and Oberwinkler
(in Bauer et al. 1997). Vánky et al. (2007) transferred the
South African Entorrhiza calospora, growing in roots of
diverse species of Aizoaceae, Molluginaceae, and
Portulacaceae, and also producing galls in the newly proposed
Fig. 2 Systematic arrangement and phylogeny of the Ustilaginomycetes
as proposed by Bauer et al. (1997). (1) Interaction with primary
interactive vesicles without such vesicles. (2) Membranous pore caps
or bands without these structures. (3) Dolipores simple pores. (4)
Haustoria intercellular hyphae. (5) Enlarged interaction zones local
interaction zones. (6) Haustoria intercellular hyphae. (7) Loss of septal
pores simple pores. (8) Septal pores with membranous bands without
membranous bands. (9) Basidia reduced to teliospores teliospores are
probasidia. (10) Intracellular hyphae intercellular hyphae. (11)
Ballistosporic basidiospores repeated loss of ballisto-basidiospores.
(12) Loss of septal pores simple pores. (13) Dolipores simple pores.
(14) Loss of teliospores teliospores. (15) Interaction apparatus
primary interactive vesicles. (16) Complex interaction apparatus
simple interaction ring. (17) Interaction apparatus with cytoplasmic
compartments without cytoplasmic compartments. (18) Haustoria
intercellular hyphae. (19) Interaction ring without interaction ring.
(20) Basidia in chains not in chains. (21) Clamped haustoria
intercellular hyphae. (22) Unclamped haustoria intercellular hyphae.
The text follows the scheme from left to right
98 Page 4 of 11 Mycol Progress (2015) 14:98
genus Talbotiomyces. Because of lacking ontognetic, ultra-
structural, and molecular data, a proper systematic treatment
was impossible, but recently available sequences indicate the
relationship with Entorrhiza (Riess et al. 2015).
Simultaneously, the results of a five-gene phylogeny were
taken for granted to propose the Entorrhizomycota,andto
suggest that the teliospore tetrads of Entorrhiza represent the
prototype of the dikaryan meiosporangium (Bauer et al.
2015).
In the new phylogenetic system of smut fungi (Bauer et al.
1997), Bauer and Oberwinkler proposed the Urocystales and
the Mycosyringaceae. Bauer et al. (1995a) studied the cellular
interaction of Ustacystis waldsteiniae and also investigated its
septal pores (Bauer et al. 1995b). For Mycosyrinx nonveilleri,
Vánky and Bauer (in Vánky 1996, not cited) introduced the
new genus Geminago. Unusual basidial ontogenies in the
Costa Rican smuts Doassansiopsis limnocharidis,
Mycosyrinx cissi,andThecaphora haumani were found by
Piepenbring and Bauer (1995). Melanotaenium indicum, par-
asitizing Ischaemum indicum was transferred into the new
genus Phragmotaenium by Bauer et al. (2001b). The marine
Ruppia maritima can be infected by a smut, originally de-
scribed as Melanotaenium ruppiae, but recognized as a sepa-
rate genus, Flamingomyces, by Bauer et al. (2007). Another
new genus, Antherospora, was proposed for the anther smut in
Muscari and Scilla species, Ustilago vaillantii (Bauer et al.
2008b). The new family, Floromycetaceae, was introduced to
accomodate this genus and Floromyces anemarrhenae
(Thecaphora a.), growing in Anemarrhena asphodeloides,
Agavaceae, (Vánky et al. 2008b). A revision of Thecaphora
(Glomosporiaceae) showed that Glomosporium, Kochmania
and Tothiella had to be synonymized with Thecaphora
(Vánky et al. 2008a). For Melanotaenium oxalidis, known
from the North American Oxalis oregana,anewgenus,
Melanoxa, was erected (Lutz et al. 2011).
Ustilaginales Ustilago esculenta causes hypertrophy in its
host Zizania latifolia and produces edible tissues, highly
esteemed in East Asia. Smut spore germination, SPBs, septal
pores, and ultrastructural features of host interaction were
studied by Nagler et al. (1990). They recognized the natural
relationship with Ustilago s. str. and concluded that its own
genus, Yen ia, is justified. Bauer et al. (1999a) analysed mor-
phological and ultrastructural characters of Ustilago
osmundae on Osmunda regalis and O. cinnamomea. They
recognized high structural conformity with the
Melanotaeniaceae. Consequently, the smut on the royal fern
was transferred into its own genus, Exoteliospora,and
Ustilago marina, growing on the marine Eleocharis parvula,
also deserved to be excluded from Ustilago, and was, there-
fore, generically renamed as Parvulago by Bauer et al. (2007).
The female flowers of Carex and of other cyperaceous plants
infected by Anthracoidea species, were long lasting objects of
intensive collecting and studies in our group (Hendrichs et al.
2005), which required also partial re-investigations of the
main host itself (Hendrichs et al. 2004). Prillinger et al.
(2009) reported the new Schizonella caricis-atratae,growing
on Carex atrata in Austria. In a predominantly molecularly
based phylogenetic approach of the Ustilaginomycotina,
Begerow et al. (2006) confirmed the Anthracoideaceae,
Ustilaginaceae, and Websdaneaceae, but rejected the
Cintractiaceae, Dermatosoraceae, Melanopsichiaceae, and
Farysiaceae.
Georgefischeriales Ultrastructural features of species in this
order are local interaction zones between parasite and hostand
the lack of septal pores (Bauer et al. 1997). Additionally,
newly available sequence data confirmed the taxon
(Begerow et al. 1997). An enlarged sampling enabled Bauer
et al. (2001b) to discriminate three families, Eballistraceae,
Georgefischeriaceae, and Tilletiariaceae. Eballistra and
Phragmotaenium were proposed as new genera. A restudy
of Entyloma ossifragi on Narthecium ossifragum (Bauer
et al. 2005) provided evidence to include this smut in the
Georgefischeriales. The new genus Gjaerumia and the new
family Gjaerumiaceae were based on this species.
Tilletiales, bunts Vánky and Bauer (1992) introduced the
new genus Conidiosporomyces, characterized by Y-shaped
conidia in the smut spore layers. A smut occurring on the grass
Ortachne (Muhlenbergia) erectifolia in the Cordillera de
Mérida, Venezuela, was described by Vánky and Bauer
(1995) as Oberwinkleria anulata. In this species, smut spores
are the meiosporangia themselves, and consequently germi-
nate with basidiospores. For Tilletia hyalospora,growingon
Nassella and Stipa species, Vánky and Bauer (1996) proposed
the genus Ingoldiomyces, which produces ballisto-conidia and
ballisto-basidiospores. Black spots on Phaseolus leaves are
caused by fungi known previously as Entyloma vignae or
Protomycopsis patelii. Piepenbring and Bauer (1997) realised
that both names cover the same parasite, which was found to
be a member of the Tilletiales, and which was renamed as
Erratomyces.
Microstromatales Members of this order have gasteroid
holobasidia without probasidia, i.e. without smutspores.
Local interaction zones between parasites and hosts were rec-
ognized as synapomorphies by Bauer et al. (1997) who also
introduced the ordinal name. A revision of Muribasidiospora
(Begerow et al. 2001, 2002b) resulted in the separation of
M. triumfetticola from M. indica and the introduction of the
new genus Volvocisporium. The latter belongs to the
Microstromatales, but M. indica remains with the
Exobasidiales. De Beer et al. (2006) described the
Quambalariaceae for anamorphic fungal parasites of
Mycol Progress (2015) 14:98 Page 5 of 11 98
Eucalyptus and Corymbia and included them in the
Microstromatales according to sequence data.
Entylomatales Bauer and Oberwinkler (in Bauer et al. 1997)
proposed the Entylomataceae and Entylomatales, character-
ized as smuts with teliospores, simple hyphal septa, and inter-
action apparatus with homogeneous contents.
Doassansiales The order was described by Bauer and
Oberwinkler (in Bauer et al. 1997), and besides
Doassansiaceae, an additional family, Rhamphosporaceae,
was introduced. Host parasite interactions were found to de-
pend on subcellular complex structures. Sequence data sup-
ported the new classification (Begerow et al. 1997).
Doassinga callitrichis is specialised on Callitriche hosts
(Vánky et al. 1998). Two smut species were known from
Selaginella hosts, Melanotaenium oreophilum and
M. selaginellae. A restudy (Bauer et al. 1999b) delivered facts
of Doassansiales relationship, and consequently, the new ge-
nus Melaniella and the family Melaniellaceae were proposed.
Graphiolales, the palm smuts Until 1982 the taxonomic po-
sition of Graphiola was unsettled. However, our own data
unambiguously showed basidiomycetous relationship. This
was strongly supported by subsequently available interaction
structures (Bauer et al. 1997), and sequencing results
(Begerow et al. 1997, Bauer et al. 2006). The latter favoured
the insertion of Graphiolales in Exobasidiales.
Exobasidiales In addition to the very distinctive
meiosporangial characters of incurved basidiospore develop-
ment, parasite host interaction is an important synapomorphy
of the order (Bauer et al. 1997). It was mentioned already with
the Microstromatales that only Muribasidiospora indica be-
longs to the Exobasidiales, but not M. triumfetticola (Begerow
et al. 2001). Begerow et al. (2002a, 2014) preferred a broad
concept of Exobasidiales, including the Exobasidiaceae, pre-
dominantly infecting Ericanae, and the Cryptobasidiaceae
preferring Lauraceae, Brachybasidiaceae on Poaceae and
Graphiolaceae on palms. The Cryptobasidiaceae of tropical
Central and South America with the genera Botryoconis,
Clinoconidium,andDrepanoconis were treated by
Hendrichs et al. (2003) morphologically and ultrastructurally.
Ceraceosorales Begerow et al. (2006) described the order
with species having intracellular hyphae in hosts and local
interaction zones. Two sterigmate basidia emerge through sto-
mata. Based on sequence data, Ceraceosorus is closely related
to Entyloma.
Agaricomycotina
To match taxonomy with phylogeny, Bauer et al. (2006)
erected the subdivision Agaricomycotina whose members
are said to share type B of the 5S RNA secondary structure,
and to contain predominantly glucose and xylose in the cell
walls.
Bartheletiaceae A most remarkable rediscovery in recent
years was Bartheletia paradoxa, inhabiting leaves of Ginkgo
biloba (Scheuer et al 2008). As mentioned above, the species
has multipored hyphal septa, thus reminiscent of Kriegeria
eriophori. However, even the very careful integrative study
could not solve its definite phylogenetic position.
The basal class of Agaricomycotina, Tremellomycetes,
comprising Tremellales, Filobasidiales, and
Cystofilobasidiales (Fig. 3), was recently reviewed by Weiß
et al. (2014). A yeast, isolated from Asterophora
lycoperdoides, developed a hyphal phase in culture. The septal
pores of these hyphae were of the Tremella type (Laaser et al.
1988). The mycoparasitic interaction of Tetragoniomyces
uliginosus with Rhizoctonia sp. was studied transmission elec-
tron microscopically by Bauer and Oberwinkler (1990a). A
direct cytoplasm-cytoplasm connection through a single nano-
meter pore at the haustorial hyphal tip could be detected. The
pore membrane appeared continuous with the plasma mem-
brane of both cells. An intrahymenial mycoparasite,
Phragmoxenidium mycophilum,wasfoundin
Uthatobasidium fusisporum (Oberwinkler et al. 1990c).
Because tremelloid parenthesomes were lacking at the
dolipores, the species and the family Phragmoxenidiaceae
were assigned to Tremellales only tentatively. The
mycoparasitic interactions of Tremella mesenterica, T.
encephala, and T. mycophaga were analysed by Zugmaier
et al. (1994) light and transmission electron microscopically.
They found ultrastructural features similar to those in
Tetr ago n io m yce s. Also, subcellular characteristics were used
by Kwon-Chung et al. (1995) to discriminate between
Filobasidiella depauperata and F. neoformans.Withaninte-
grative approach, Sampaio et al.(2002) characterized two new
genera, Bulleribasidium and Papiliotrema, and three new spe-
cies, Bulleribasidium oberjochense, Papiliotrema bandonii,
and Fibulobasidium murrhardtense.
Filobasidiales With the help of culture experiments,
Oberwinkler et al. (1984) were successful to elucidate the life
history of Christiansenia pallida, a mycoparasite on
Phanerochaete cremea. The tremelloid nanometer pore inter-
action was found again (Bauer and Oberwinkler 1990b).
Cystofilobasidiales Crossing compatible yeast strains of
Cryptococcus ferigula resulted in a teleomorph that was de-
scribed as Cystofilobasidium ferigula by Sampaio et al.
98 Page 6 of 11 Mycol Progress (2015) 14:98
(2001). The genome of the basal agaricomycete
Xanthophyllomyces dendrorhous provided insights into the
organization of its acetyl-CoA derived pathways (Sharma
et al. 2015).
Dacrymycetales The uniform Dacrymyces dolipore with con-
tinuous parenthesomes was used for detailed ultrastructural
comparison with similar pore types of the Sebacinales,
Auriculariales, and Tulasnellales (unpublished).
Sebacinales Sebacina spp., sampled from European Picea
abies, Fagus sylvatica, Quercus robur, Carpinus betulus,
Tilia sp., and others, were identified molecularly and addition-
ally characterised by dolipores with continuous
parenthesomes (Selosse et al. 2002, Urban et al. 2003). Weiß
et al. (2011) considered the previously overlooked
sebacinalean endophytes of ubiquitous distribution. The phy-
logenetic diversity and structure of sebacinoid fungi, associ-
ated with plant communities along an altitudinal gradient, was
analysed by Garnica et al. (2012). The state of knowledge on
Sebacinales was summarized by Oberwinkler et al. (2013a).
The authors concluded that Bit appears to be extremely diffi-
cult with the techniques available today to gain a better under-
standing of this enigmatic diversity^. This topic was specifi-
cally well investigated at the regional scale in Sebacina
epigaea and S. incrustans (Riess et al. 2013). Extensive col-
lections of these species and of additional ones from genera,
belonging to former BSebacinales group A^,thennamed
Sebacinaceae s. str., were used to find out whether the high
molecular diversity can be verified by micromorphological
characteristics (Oberwinkler et al. 2014). Herbaceous plants
in agricultural and grassland ecosystems were found to be
dominated by Serendipita herbamans sp. nov. (Riess et al.
2014).
Tulasnellales The Aneuraceae with their tulasnelloid
mycobionts were considered a model for early steps in fungal
symbiosis with terrestrial plants (Krause et al. 2011).
Cantharellales A taxonomic re-evaluation of the
Ceratobasidium-Rhizoctonia complex was carried out by
Oberwinkler et al. (2013b). A new species, Rhizoctonia
butinii, attacking spruce, was described.
Occasionally, and for comparative purposes, Robert Bauer
studied septal pores of mushrooms, e.g. in Sphaerobolus of
the Geastrales, and Schizophyllum of the Agaricales (Hibbett
et al. 2014).
Ascomycota
In the course of intensive investigations in smuts, Nagler et al.
(1989) studied Schroeteria delastrina and S. poeltii and found
that their septal pores have Woronin bodies, that SPBs are
ascomycetes-like, and that karyogamy and meiosis are lacking
in sporulating germination hyphae. These results identified
Schroeteria as an ascomycete. Cymadothea trifolii is a para-
site in the leaves of Trifolium repens. In a transmission elec-
tron microscopic study of freeze substituted material, Simon
et al. (2004) found interaction apparatus with long cisternae in
the hyphae. The adjacent host cells are forced to let their
plasma membranes invaginate into the parasite cells as bub-
bles that finally are connected with fungal interaction appara-
tus via tubular structures. Immunochemical tests provided
Fig. 3 Systematic arrangement
and part of the phylogeny of
Agaricomycotina with a selection
of genera discussed from below
upwards in the following text.
Tree compiled after Scheuer et al.
(2008) and Hibbett et al. (2014),
and strongly modified
Mycol Progress (2015) 14:98 Page 7 of 11 98
evidence that Cymadothea degrades pectins, but not cellulose
and xyloglucan (Simon et al. 2005a). Also, the vegetative life-
cycle of the clover pathogen was clarified by Simon et al.
(2005b). Mycosphaerella podagrariae, a necrotrophic phyto-
pathogen, produces another special cellular interaction system
of electron dense appositions with its host Aegopodium
podagraria (Simon et al. 2009). The interaction apparatus of
Asteridiella callista, Meliolaceae, growing on Stachytarpheta
mutabilis, was electron microscopically analysed by
Rodríguez Justavino et al. (2014). They found a cisternal in-
teraction apparatus, surrounded by a membrane in a continu-
um with the fungal plasma membrane, deposition of material
at the host cytoplasmic membrane, an encasement of the in-
fection area, and a final degeneration.
Bauer contributed also to broader studies dealing with the
phylogeny and systematics of fungi, with special reference
to Ascomycota and Basidiomycota, and their yeasts
(Prillinger 1996, 2002).
Concluding remarks
Robert Bauers 120 publications were concisely reviewed
here to provide an insight in his scientific work. He focused
decidedly on ultrastructural features of plant parasites, espe-
cially basidiomycetes, and their cellular and subcellular inter-
actions with the hosts. The huge amount of data, accumulated
over the years, were a challenge to use them for comparative
analyses, with the aime to deduce phylogenetic trends for the
fungi involved. The upcoming flood of molecular data did not
overshadow his work. In contrast, there was a welcome
chance to verify hypotheses that were exclusively based on
structural characters.
During the few last years, Robert worked on several man-
uscripts at the same time. He concentrated on his most impor-
tant, not yet published results. This task was recognized by the
German Research Council, DFG, who supported this attempt
that, unfortunately, could not be finished by him.
I met Robert first when he was a student of biology at our
university, supervised his diploma and doctoral theses, and ac-
companied his academic and scientific career over 30 years. He
was a vital, reliable, friendly, and at times humorous member of
our former mycology group, qualities that had a very positive
influence on our many students in biology for a long time.
His colleagues, worldwide, will respectfully perpetuate his
memory.
Chronological list of Robert Bauers publications
The development of research preferences, availability of new
methods, and cooperative constellations can be perceived
from this arrangement in a time sequence.
1980
Bauer R (1980) Sporenbildung bei Coleosporium tussilaginis (Pers.) Lév.
Diplomarbeit, Universität Tübingen
1982
Deml G, Bauer R, Oberwinkler F (1982a) Axenische Kultur von Coleosporium
tussilaginis (Pers.) Lév. (Uredinales). II. Kreuzungsversuche mit
monokaryotischen Stämmen. Phytopath Z 103:149-155
Deml G, Bauer R, Oberwinkler F (1982b) Axenic cultures of
Coleosporium tussilaginis (Uredinales). I. Isolation, identification
and characterization of the cultures. Phytopath. Z. 104:39-45
1983
Bauer R (1983) Experimentell-ontogenetische und karyologische
Untersuchungen an Uredinales. Dissertation Universität Tübingen
1984
Oberwinkler F, Bandoni RJ, Bauer R, Deml G, Kisimova-Horovitz L
(1984) The life history of Christiansenia pallida, a dimorphic,
mycoparasitic heterobasidiomycete. Mycologia 76:9-22
1985
Deml G, Oberwinkler F, Bauer R (1985) Sphacelotheca polygoni-
persicariae G. Deml & Oberw. spec. nov. Phytopath Z 113:231-242
1986
Bauer R (1986) Basidiosporenentwicklung und -keimung bei
Heterobasidiomyceten. Teil A: Experimentell-ontogenetische
und karyologische Untersuchungen an keimenden
Rostpilzbasidiosporen. Ber Deutsch Bot Ges 99:67-81
Bauer R, Oberwinkler F (1986a) Experimentell-ontogenetische
Untersuchungen an Phragmobasidien. Z Mykol 52:259-264
Bauer R, Oberwinkler F (1986b) Experimentell-ontogenetische und
karyologische Untersuchungen an Ochropsora ariae (Fuck.)
Ramsb. Z Mykol 52:271-275
1987
Bauer R (1987) Uredinales Germination of basidiospores and
pycnospores. Stud Mycol 30:111-125
1988
Bauer R, Oberwinkler F (1988) Nuclear degeneration during
ballistospore formation of Cronartium asclepiadeum (Uredinales).
Bot Acta 101:272-282
Laaser G, Jahnke KD, Prillinger HJ, Bauer R, Hoffmann P, Deml G,
Oberwinkler F (1988) A new-tremelloid yeast isolated from
Asterophora lycoperdoides. Antonie van Leeuwenhoek 54:57-74
1989
Bauer R, Oberwinkler F, Deml G (1989) Ultrastruktur der
Basidiensepten phragmobasidialer Brandpilze. Z Mykol 55:
163-168
Nagler A, Bauer R, Berbee ML, Vánky K, Oberwinkler F (1989) Light
and electron microscopic studies of Schroeteria delastrina and
S. poeltii. Mycologia 81:884-895
Oberwinkler F, Bauer R (1989) The systematics of gasteroid,
auricularioid heterobasidiomycetes. Sydowia 41:224-256
1990
Bauer R, Oberwinkler F (1990a) Direct cytoplasm-cytoplasm con-
nection: an unusual host-parasite interaction of the tremelloid
mycoparasite Tetragoniomyces uliginosus. Protoplasma 154:
157-160
Bauer R, Oberwinkler F (1990b) Haustoria of the mycoparasitic
heterobasidiomycete Christiansenia pallida. Cytologia 55:
419-424
Bauer R, Oberwinkler F (1990c) Meiosis, spindle pole body cycle and
taxonomy of the heterobasidiomycete Pachnocybe ferruginea. Plant
Syst Evol 172:241-261
Berbee M, Bauer R, Oberwinkler F (1990) The spindle pole body cycle,
meiosis, and basidial cytology of the smut fungus Microbotryum
violaceum. Canad J Bot 69:1795-1803
98 Page 8 of 11 Mycol Progress (2015) 14:98
Nagler A, Bauer R, Oberwinkler F, Tschen J (1990) Basidial develop-
ment, spindle pole body, septal pore, and host-parasite interaction in
Ustilago esculenta. Nord J Bot 10:457-464
Oberwinkler F, Bauer R (1990) Cryptomycocolax: a new mycoparasitic
heterobasidiomycete. Mycologia 82:671-692
Oberwinkler F, Bauer R, Bandoni RJ (1990a) Colacogloea: a new genus
in the auricularioid heterobasidiomycetes. Canad J Bot 68:2531-
2536
Oberwinkler F, Bauer R, Bandoni RJ (1990b) Heterogastridiales: a new
order of Basidiomycetes. Mycologia 82:48-58
Oberwinkler F, Bauer R, Schneller J (1990c) Phragmoxenidium
mycophilum sp. nov, an unusual mycoparasitic
heterobasidiomycete. System Appl Microbiol 13:186-191
1991
Bauer R, Oberwinkler F (1991) The colacosomes: new structures at the
host-parasite interface of a mycoparasitic basidiomycete. Bot Acta
104:53-57
Bauer R, Berbee ML, Oberwinkler F (1991) An electron-microscopic
study of meiosis and the spindle pole body cycle in the smut fungus
Sphacelotheca polygoni-serrulati. Canad J Bot 69:245-255
1992
Bauer R, Oberwinkler F, McLaughlin DJ (1992) Meiosis, spindle pole
body cycle and basidium ontogeny in the heterobasidiomycete
Agaricostilbum pulcherrimum. System Appl Microbiol 15:259-274
Vánky K, Bauer R (1992) Conidiosporomyces, a new genus of
Ustilaginales. Mycotaxon 43:426-435
1993
Prillinger H, Oberwinkler F, Umile C, Tlachac K, Bauer R, Dörfler C,
Taufratzhofer E (1993) Analysis of cell wall carbohydrates (neutral
sugars) from ascomycetous and basidiomycetous yeasts with and
without derivatization. J Gen Appl Microbiol 39:1-34
1994
Bauer R, Oberwinkler F (1994) Meiosis, septal pore architecture, and
systematic position of the heterobasidiomycetous fern parasite
Herpobasidium filicinum. Canad J Bot 72:1229-1242
Berndt R, Bauer R, Oberwinkler F (1994) Ultrastructure of the host-
parasite interface in the fern rusts Milesia, Uredinopsis,and
Hyalopsora (Uredinales, Pucciniastraceae). Canad J Bot 72:1084-
1094
Zugmaier W, Bauer R, Oberwinkler F (1994) Mycoparasitism of some
Trem ell a species. Mycologia 86:49-56
1995
Bauer R, Mendgen K, Oberwinkler F (1995a) Cellular interaction of the
smut fungus Ustacystis waldsteiniae.CanadJBot73:867-883
Bauer R, Mendgen K, Oberwinkler F (1995b) Septal pore apparatus of
the smut Ustacystis waldsteiniae. Mycologia 87:18-24
Kwon-Chung KJ, Chang YC, Bauer R, Swann EC, Taylor JW, Goel R
(1995) The characters that differentiate Filobasidiella depauperata
from Filobasidiella neoformans.StudMycol38:67-79
Piepenbring M, Bauer R (1995) Noteworthy germinations of some Costa
Rican Ustilaginales. Mycol Res 99:853-858
Vánky K, Bauer R (1995) Oberwinkleria, a new genus of Ustilaginales.
Mycotaxon 53:361-368
1996
Prillinger H, Messner R, König H, Bauer R, Lopandic K, Molnar O,
DangelP,WeigangF,KirisitsT,NakaseT,SiglerL(1996)Yeasts
associated with termites: a phenotypic and genotypic characteriza-
tion and use of coevolution for dating evolutionary radiations in
asco- and basidiomycetes. System Appl Microbiol 19:265-283
Vánky K, Bauer R (1996) Ingoldiomyces, a new genus of Ustilaginales.
Mycotaxon 59:277-287
1997
Bauer R, Oberwinkler F (1997) The Ustomycota: an inventory.
Mycotaxon 64:303-319
Bauer R, Oberwinkler F, Vánky K, (1997) Ultrastructural markers and
systematics in smut fungi and allied taxa. Canad J Bot 75:1273-1314
Begerow D, Bauer R, Oberwinkler F (1997) Phylogenetic studies on
nuclear large subunit ribosomal DNA sequences of smut fungi and
related taxa. Can J Bot 75:2045-2056
Piepenbring M, Bauer R (1997) Erratomyces, a new genus with species
on Leguminosae. Mycologia 89:924-936
Vánky K, Bauer R, Begerow D (1997) Fulvisporium, a new genus of
Ustilaginales. Mycotaxon 64:57-66
1998
Bauer R, Begerow D, Oberwinkler F, (1998) Progress in the systematics
of smut fungi. Z Pflanzenkrankheiten 105:224-238
Piepenbring M, Bauer R, Oberwinkler F (1998a) Teliospores of smut
fungi general aspects of teliospore walls and sporogenesis.
Protoplasma 204:155-169
Piepenbring M, Bauer R, Oberwinkler F (1998b) Teliospores of smut
fungi teliospore walls and the development of ornamentation stud-
ied by electron microscopy. Protoplasma 204:170-201
Piepenbring M, Bauer R, Oberwinkler F (1998c) Teliospores of smut
fungi teliospore connections, appendages, and germ pores studied
by electron microscopy; phylogenetic discussion of characteristics
of teliospores. Protoplasma 204:202-218
Vánky K, Bauer R, Begerow D (1998) Doassinga, a new genus of
Doassansiales. Mycologia 90:964-970
1999
Bauer R, Oberwinkler F, Vánky K (1999a) Ustilaginomycetes on
Osmunda. Mycologia 91:669-675
Bauer R, Vánky K, Begerow D, Oberwinkler F (1999b)
Ustilaginomycetes on Selaginella. Mycologia 91:475-484
Kirschner R, Bauer R, Oberwinkler F (1999) Atractocolax, anew
heterobasidiomycetous genus based on a species vectored by
conifericolous bark beetles. Mycologia 91:538-543
Oberwinkler F, Bauer R, Tschen J (1999) The mycoparasitism of
Platygloea bispora. Kew Bull 51:763-769
Sampaio JP, Bauer R, Begerow D, Oberwinkler F (1999a) Occultifur
externus sp. nov, a new species of simple-septate auricularioid
heterobasidiomycete from plant litter in Portugal. Mycologia 91:
10941101
Sampaio JP, Fell JW, Gadanho M, Bauer R (1999b) Kurtzmanomyces
insolitus sp. nov, a new anamorphic heterobasidiomycetous yeast
species. System Appl Microbiol 22:619-625
2000
Begerow D, Bauer R, Boekhout T (2000) Phylogenetic placements of
ustilaginomycetous anamorphs as deduced from nuclear LSU
rDNA sequences. Mycol Res 104:53-60
2001
Bauer R, Begerow D, Oberwinkler F, Piepenbring M, Berbee ML (2001a)
Ustilaginomycetes. In Mycota VII Part B. Systematics and evolu-
tion. Edited by McLaughlin DJ, McLaughlin EG, Lemke PA,
Springer Verlag, Heidelberg, New York, pp. 57-83
Bauer R, Begerow D, Nagler A, Oberwinkler F (2001b) The
Georgefischeriales: a phylogenetic hypothesis. Mycol Res 105:
416-424
Begerow D, Bauer R, Oberwinkler F (2001) Muribasidiospora:
Microstromatales or Exobasidiales? Mycol Res 105:798-810
Kirschner R, Bauer R, Oberwinkler F (2001) Colacosiphon:anewgenus
described for a mycoparasitic fungus. Mycologia 93:634-644
Sampaio JP, Gadanho M, Bauer R (2001) Taxonomic studies on the
genus Cystofilobasidium: description of Cystofilobasidium ferigula
sp. nov. and clarification of the status of Cystofilobasidium lari-
marini. Int J System Evol Microbio 51:221-229
2002
Begerow D, Bauer R, Oberwinkler F (2002a) The Exobasidiales: an
evolutionary hypothesis. Mycol Progr 1:187-199
Mycol Progress (2015) 14:98 Page 9 of 11 98
Begerow D, Bauer R, Oberwinkler F (2002b) The sterigmata of
Volvocisporium: a clarification. Mycol Res 106:131
Sampaio JP, Weiß M, Gadanho M, Bauer R (2002) New taxa in the
Tremellales: Bulleribasidium oberjochense gen. et sp. nov,
Papiliotrema bandonii gen. et sp. nov. and Fibulobasidium
murrhardtense sp. nov. Mycologia 94:873-887
Selosse MA, Bauer R, Moyersoen B (2002) Basal hymenomycetes be-
longing to the Sebacinaceae are ectomycorrhizal on temperate de-
ciduous trees. New Phyt 155:183-195
2003
Bauer R, Begerow D, Oberwinkler F, Marvanova L (2003) Classicula:
the teleomorph of Naiadella fluitans. Mycologia 95:756-764.
Hendrichs M, Bauer R, Oberwinkler F (2003) The Cryptobasidiaceae of
tropical Central and South America. Sydowia 55:33-64
Prillinger H, Lopandic K, Schweigkofler W, Deak R, Aarts HJ, Bauer R,
Sterflinger K, Kraus GF, Maraz A (2002) Phylogeny and systemat-
ics of the fungi with special reference to the Ascomycota and
Basidiomycota. In: Breitenbach M, Crameri R, Lehrer SB (eds.).
Fungal Allergy and Pathogenicity. Chem Immunol 81:207-295
Sampaio JP, Gadanho M, Bauer R, Weiß M (2003) Taxonomic studies in
the Microbotryomycetidae: Leucosporidium golubevii sp. nov.,
Leucosporidiella gen. nov. and the new orders Leucosporidiales
and Sporidiobolales. Mycol Progr 2:53-68
Urban A, Weiß M, Bauer R (2003) Ectomycorrhizae in the Sebacinaceae.
Mycol Res 107:3-14
2004
Bauer R (2004) Basidiomycetous interfungal cellular interactions a
synopsis. In: Agerer R, Piepenbring M, Blanz P, (eds) Frontiers in
basidiomycote mycology. IHW-Verlag, Eching, pp. 325337
Bauer R, Oberwinkler F (2004) Cellular ustilaginomycete-host interac-
tions. In: Varma A, Abbott L, Werner D, Hampp R (eds). Plant
Surface Microbiology. Springer, Heidelberg, pp 227-236
Bauer R, Lutz M, Oberwinkler F (2004) Tuberculina-rusts: a unique
basidiomycetous interfungal cellular interaction with horizontal nu-
clear transfer. Mycologia 96:960-967
Hendrichs M, Oberwinkler F, Begerow D, Bauer R (2004) Carex,sub-
genus Carex (Cyperaceae) A phylogenetic approach using ITS
sequences. Plant Syst Evol 246:89-107
Lutz M, Bauer R, Begerow D, Oberwinkler F, Triebel D (2004a)
Tuberculina: rust relatives attack rusts. Mycologia 96:614-626
Lutz M, Bauer R, Begerow D, Oberwinkler F (2004b) Tuberculina
Thanatophytum / Rhizoctonia crocorum Helicobasidium: a unique
mycoparasiticphytoparasitic life strategy. Mycol Res 108: 227-238
Lutz M, Bauer R, Begerow D, Oberwinkler F (2004c) Tuberculina
Helicobasidium: host specificity of the Tuberculina-stage reveals
unexpected diversity within the group. Mycologia 96:1316-1329
Simon UK, Bauer R, Oberwinkler F (2004) The unique cellular interac-
tion between the leaf pathogen Cymadothea trifolii and Trifolium
repens. Mycologia 96:1209-1217
Weiß M, Bauer R, Begerow D (2004) Spotlights on heterobasidiomycetes.
In Agerer R, Piepenbring M, Blanz P (eds) Frontiers in
Basidiomycote Mycology, pp. 7-48. IHW-Verlag, Eching
2005
Bauer R, Lutz M, Oberwinkler F (2005) Gjaerumia, a new genus in the
Georgefischeriales (Ustilaginomycetes). Mycol Res 109:1250-1258
Hendrichs M, Begerow D, Bauer R, Oberwinkler F (2005) The genus
Anthracoidea (Basidiomycota, Ustilaginales) a molecular phyloge-
netic approach using LSU rDNA sequences. Mycol Res 109:31-40
Simon UK, Bauer R, Rioux D, Simard M, Oberwinkler F (2005a) The
intercellular biotrophic leaf pathogen Cymadothea trifolii locally
degrades pectins, but not cellulose or xyloglucan in cell walls of
Trifolium repens. New Phyt 165:243-260
Simon UK, Bauer R, Rioux D, Simard M, Oberwinkler F (2005b) The
vegetative life-cycle of the clover pathogen Cymadothea trifolii as re-
vealed by transmission electron microscopy. Mycol Res 109:764-778
2006
Aime MC, Matheny PB, Henk DA, Frieders EM, Nilsson RH,
Piepenbring M, Mclaughlin DJ, Szabo LJ, Begerow D, Sampaio
JP, Bauer R, Weiß M, Oberwinkler F, Hibbett D (2006) An overview
of the higher level classification ofPucciniomycotina based on com-
bined analyses of nuclear large and small subunit rDNA sequences.
Mycologia 98:896-905
Bauer R, Begerow D, Sampaio JP, Weiß M, Oberwinkler F (2006) The
simple-septate basidiomycetes: a synopsis. Mycol Progr 5:41-66
Begerow D, Stoll M, Bauer R (2006) A phylogenetic hypothesis of
Ustilaginomycotina based on multiple gene analyses and morpho-
logical data. Mycologia 98:906-916
Celio GJ, Padamsee M, Dentinger BTM, Bauer R, McLaughlin DJ
(2006) Assembling the Fungal Tree of Life: constructing the struc-
tural and biochemical database. Mycologia 98:850-859
De Beer W, Begerow D, Bauer R, Pegg GS, Crous PW, Wingfield MJ
(2006) Phylogeny of the Quambalariaceae fam. nov, including im-
portant Eucalyptus pathogens in South Africa and Australia. Stud
Mycol 55:293-302
Lutz M, Bauer R, Oberwinkler F (2006) Das Doppelleben des
Birnengitterrostes. Forschung 4/2006:13-15
Oberwinkler F, Kirschner R, Arenal F, Villareal M, Rubio V, Begerow D,
Bauer R (2006) Two new pycnidial members of the Atractiellales:
Basidiopycnis hyalina and Proceropycnis pinicola. Mycologia 98:
637-649
2007
Bauer R, Lutz M, Piatek M, Vánky K, Oberwinkler, F (2007)
Flamingomyces and Parvulago, new genera of marine smut fungi
(Ustilaginomycotina). Mycol Res 111:1199-1206
Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson
OE, Huhndorff S, James T, Kirk PM, Lücking R, Lumbsch HL,
Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S,
Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC,
AptrootA,BauerR,BegerowD,BennyGL,CastleburyLA,
Crous PW, Dai Y-C, Gams W, Geiser DM, Griffith GW, Gueidan
C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde
KD, Ironside JE, Kõljalg U, Kurtzman CP, Larsson K-H, Lichtwardt
R, Longcore J, Miadlikowska J, Miller A, Moncalvo J-M, Mozley-
Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux
C, Ryvarden L, Sampaio JP, Schüßler A, Sugiyama J, Thorn RG,
Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiß M,
White MM, Winka K, Yao Y-J, Zhang N (2007) A higher-level
phylogenetic classification of the Fungi. Mycol Res 111:509547
Lutz M, Bauer R, Oberwinkler F (2007) The double life of a fungus.
German Research 1/2007:21-23
Vánky K, Bauer R, Begerow D (2007) Talbotiomyces, a new genus for
Entorrhiza calospora (Basidiomycota). Mycol Balcan:4:11-14
2008
Bauer R, Lutz M, Begerow D, Piatek M, Vánky K, Bácigalová K,
Oberwinkler F (2008) Anther smut fungi on monocots. Mycol Res
112:1297-1306
Scheuer C, Bauer R, Lutz M, Stabentheiner E, Melnik VA, Grube M
(2008) Bartheletia paradoxa is a living fossil on Ginkgo leaf litter
with a unique septal structure inthe Basidiomycota. MycolRes 112:
1265-1279
Vánky K, Lutz M, Bauer R (2008a) About the genus Thecaphora
(Glomosporiaceae) and its new synonyms. Mycol Progr 7:31-39
Vánky K, Lutz M, Bauer R (2008b) Floromyces, a new genus of
Ustilaginomycotina. Mycotaxon 104:171184
2009
Bauer R, Metzler B, Begerow D, Oberwinkler F (2009) Cystobasidiopsis
nirenbergiae, a new agaricostilbomycete (Pucciniomycotina).
Mycol Res 113:960-966
Prillinger H, Wuczkowski M, Lopandic K, Bauer R, Molmár O,
Sterflinger K (2009) Schizonella caricis-atratae
98 Page 10 of 11 Mycol Progress (2015) 14:98
(Ustilaginomycetes) a new cryptic species on Carex atrata from
Austria. Mycol Progr 8:157-164
Simon UK, Groenewald JZ, Stierhof Y-D, Crous PW, Bauer R (2009)
Mycosphaerella podagrariae a necrotrophic phytopathogen
forming a special cellular interaction with its host Aegopodium
podagraria. Mycol Progr 9:49-56
2010
Kottke I, Suárez JP, Herrera P, Cruz D, Bauer R, Haug I, Garnica S (2010)
Atractiellomycetes belonging to the 'rust' lineage (Pucciniomycota)
form mycorrhizae with terrestrial and epiphytic neotropical orchids.
Proc Royal Soc B 277:1289-1298
Schäfer AM, Kemler M, Bauer R, Begerow D (2010) The illustrated life
cycle of Microbotryum on the host plant Silene latifolia.CanadJBot
88:875885
2011
Lutz M, Vánky K, Bauer R (2011) Melanoxa,anewgenusinthe
Urocystidales. Mycol Progr 11:149-158
Krause C, Garnica S, Bauer R, Nebel M (2011) Aneuraceae
(Metzgeriales) and tulasnelloid fungi (Basidiomycota) - a model
for early steps in fungal symbiosis. Fungal Biology115:839-851
Weiß M, Sykorová Z, Garnica S, Riess K, Martos F, Krause C,
Oberwinkler F, Bauer R, Redecker D (2011) Sebacinales every-
where: previously overlooked ubiquitous fungal endophytes. PloS
ONE 6(2) e16793
2012
Garnica S, Riess K, Bauer R, Oberwinkler F, Weiß M (2012)
Phylogenetic diversity and structure of sebacinoid fungi associated
with plant communities along an altitudinal gradient. FEMS
Microbiol Ecol, DOI: 10.1111/j.1574-6941.2012.01473.x
2013
Oberwinkler F, Riess K, Bauer R, Selosse M-A, Weiß M, Garnica S,
Zuccaro A (2013a) Enigmatic Sebacinales. Mycol Progr, DOI
10.1007/s11557-012-0880-4
Oberwinkler F, Riess K, Bauer R, Kirschner R, Garnica S (2013b)
Taxonomic re-evaluation of the Ceratobasidium-Rhizoctonia
complex and Rhizoctonia butinii, a new species attacking spruce.
Mycol Progr, DOI 10.1007/s11557-013-0936-0
Riess K, Oberwinkler F, Bauer R, Garnica S (2013) High genetic diver-
sity at the regional scale andpossible speciation in Sebacina epigaea
and S. incrustans. BMC Evol Biol 13:102, http://
www.biomedcentral.com/1471-2148/13/102
2014
Begerow D, Schäfer AM, Keller R, Yurkov A, Kemler M, Oberwinkler F,
Bauer R (2014) Ustilaginomycetes. In: Mycota VII Part A.
Systematics and evolution. Edited by McLaughlin DJ, Spatafora
JW. Springer, pp. 295-329
Hibbett DS, Bauer R, Binder M, Giachini AJ, Hosaka K, Justo A, Larsson
E, Larsson KH, Lawrey JD, Miettinen O, Nagy LG, Nilsson RH,
Weiss M, Thorn RG (2014) Agaricomycetes. In: Mycota VII Part A.
Systematics and evolution. Edited by McLaughlin DJ, Spatafora
JW. Springer, pp. 372-429
Oberwinkler F, Riess K, Bauer R, Garnica S (2014) Morphology and
molecules: the Sebacinales, a case study. Mycol Progr, DOI
10.1007/s11557-014-0983-1
Riess K, Oberwinkler F, Bauer R, Garnica S (2014) Communities of
endophytic Sebacinales associated with roots of herbaceous plants
in agricultural and grassland ecosystems are dominated by
Serendipita herbamans sp. nov. PloS ONE 9(4): e94676. doi:
10.1371/journal.pone.0094676
Rodríguez Justavino D, Carranza Velásquez J, Morales Sánchez CO,
Rincón R, Oberwinkler F, Bauer R (2014) The interaction apparatus
of Asteridiella callista (Meliolaceae, Ascomycota) Mycologia 106:
216-223
Weiß M, Bauer R, Sampaio JP, Oberwinkler F (2014) Tremellomycetes
and related groups. In: Mycota VII Part A. Systematics and evolution.
Edited by McLaughlin DJ, Spatafora JW. Springer, pp. 331-355
Wood AR, Lutz M, Bauer R, Oberwinkler F (2014) Morphology and
phylogenetics of Stomatisora, including Stomatisora psychotriicola
sp. nov. Mycol Progr, DOI 10.1007/s11557-014-0997-8
2015
Bauer R, Garnica S, Oberwinkler F, Riess K, Weiß M, Begerow D (2015)
Entorrhizomycota: a new fungal phylum reveals new perspectives
on the evolutionof fungi. PLoS ONE 10(7): e0128183.doi:10.1371/
journal.pone.0128183
Riess K, Bauer R, Kellner R, Kemler M, Piątek M, Vánky M, Begerow D
(2015) Identification of a new order of root-colonising fungi in the
Entorrhizomycota: Talbotiomycetales ord. nov. on eudicotyledons.
IMA Fungus 6:129-133
Sharma R, Gassel S, Steiger S, Xia X, Bauer R, Sandmann G, Thines M
(2015) The genome of the basal agaricomycete Xanthophyllomyces
dendrorhous provides insights into the organization of its acetyl-
CoA derived pathways and the evolution of Agaricomycotina.
BMC Genomics 16:233, DOI 10.1186/s12864-015-1380-0
Mycol Progress (2015) 14:98 Page 11 of 11 98
ResearchGate has not been able to resolve any citations for this publication.
Article
Sporulation, septal pore apparatus and host-parasite interaction between Ustilago osmundae and its host, the royal fern, were analyzed by light and electron microscopy using herbarium material and compared with findings in other species of Basidiomycota. The fungus produced thick-walled and thin-walled hyphae on leaf surfaces and sporulated externally. Coralloid haustoria with numerous lobes were present only in epidermal cells. Hyphae in intercellular spaces were lacking. The septal pore apparatus was composed of a simple pore with two caps. Ustilago osmundae shares the type of septal pore apparatus and host-parasite interaction with the Melanotaeniaceae of Ustilaginomycetes. It differs from the other species of this family primarily in the external sporulation and in the lack of intercellular hyphae. To accomodate this unusual fungus in Melanotaeniaceae a new genus, Exoteliospora, is proposed. Description and illustrations are given for Exoteliospora osmundae.
Article
Christiansenia pallida Hauerslev, a heterobasidiomycetous parasite of Phanerochaete cremea (Corticiaceae), was cultivated and studied with light and electron microscopes. Monokaryotic basidiospores bud as yeasts. Compatible cells conjugate and dikaryotic mycelia develop when yeast cells are grown together with the host on artificial media. Thread-like, monokaryotic hyphal outgrowths originate from clamps and function as haustoria, penetrating host cells. In its parasitic stage, Christiansenia pallida propagates chiefly by conidia. These are formed on short, terminal, monokaryotic, conidiogenous cells; conidia originate side by side, then fuse to form one dikaryotic zygoconidium. Dikaryotic conidia germinate to produce short-celled, dikaryotic hyphae which bear haustorial branches. Dikaryotic conidia are capable of dedikaryotization, thereby producing monokaryotic yeast cells. Usually, in a later stage of ontogeny, basidia develop on dikaryotic hyphae. Basidial morphology is rather variable, but suburniform basidia are typical. More than four sterigmata often are formed.
Article
The septal pore apparatus in intercellular hyphae of Ustacystis waldsteiniae was analyzed by serial-section electron microscopy using chemically fixed and high pressure frozen/freeze substituted samples. Septa have a central “simple” pore with rounded, nonswollen margins. However, the pore apparatus is a highly complex structure, differing significantly from that found in “simple”- and complex-septate basidiomycetes. Three features are typical: 1) the pore canal is traversed by two symmetrically arranged bands, 2) a dome shaped membranous cap, intimately attached to the plasma membrane, encloses the pore on both sides, and 3) a thin electron transparent layer and a layer of medium electron density cover the cytoplasmic side of the membranous cap. From our observations of septal pore morphology we suggest a general absence of transport of organelles including ribosomes through the pore.
Article
Descriptions are provided of new basidiomycetous taxa, i.e., Cryptomycocolacales, Cryptomycocolacaceae, Cryptomycocolax, and Cryptomycocolax abnorme. The type species is parasitic on an ascomycete and is characterized by scattered, clamped hyphae without basidiocarps. In cell contact zones, the host cell forms globose to botryose outgrowths. These are completely surrounded by a closely attached cell of the parasite. Specialized cell organelles of the parasite, designated here as colacosomes, interact with host cells. Basidia are subulate. After the first meiotic division, an apical, spore-like body develops from the upper part of the basidium. Meiosis II takes place there and in the remaining basal part of the basidium. The latter elongates and produces terminal, sessile basidiospores. The simple septal pores are associated with Woronin bodies. Interphase and prophase spindle pole bodies have large lateral discs that are connected by small middle pieces. Meiosis is described in detail. The heterobasidiomycete Cryptomycocolax abnorme appears to be closely related to the ascomycetes.
Article
Schroeteria delastrina and 5. poeltii were studied by light and transmission electron microscopy. Schroeteria has traditionally been classified in the Ustilaginales, but karyogamy and meiosis do not occur in spores or in germination hyphae. Spores and Hyphae are multinucleate and the conidia (“sporidia”) arise endogenously. Based on these facts, on the morphology of the spindle pole bodies, on the presence of pores with a pore plug and Woronin bodies at the septa and, on the absence of layering in the cell wall, we conclude that S. delastrina and S. poeltii are anamorphs of Ascomycetes. Consequently, the genus Schroeteria should be exchided from the Ustilaginales.
Article
The parasitic interaction of Tremella mesenterica, T. encephala and T. mycophaga was studied by light and electron microscopy. The host range of T. mesenterica was tested with Peniophora laeta, Peniophora incarnata, Phlebia radiata, Schizopora paradoxa, Stereum hirsutum and Diatrype stigma. It was demonstrated that T. mesenterica is, at least in vivo, a mycoparasite of the corticiaceous homobasidiomycete Peniophora laeta. Specialized interactive cells of T. mesenterica, T. encephala and T. mycophaga, designated as tremelloid haustorial cells with haustorial filaments, penetrated the cell walls of their respective hosts. A single micropore connected the cytoplasm of the haustorial filament with that of the host cell. The pore membrane appears to be continuous with the plasmalemma of both cells. In older interaction structures, the micropore was often overgrown on the host side by secondary wall formation. In vitro such micropores were present in the interaction of T. mesenterica with Peniophora laeta, P. incarnata and Phlebia radiata but could not be found in the interaction of T. mesenterica with Schizopora paradoxa, Stereum hirsutum and Diatrype stigma. However, only in Peniophora laeta and P. incarnata was the pore domain delimited by a more or less circular arrangement of ER cisternae. Wall thickening may be responsible for the nonmicropore interaction.
Article
In India and in the American tropics angular black spot disease on leaves of Vigna spp. and Phaseolus vulgaris (Fabaceae) is caused by Protomycopsis patelii and Entyloma vignae, respectively. According to a study of recently collected material from Nicaragua and of Indian herbarium specimens the two names are synonyms. The fungus is related to smut fungi of the genus Tilletia because it produces relatively large, opaque teliospores which have a partition layer in their wall and which germinate with holobasidia carrying needle-shaped basidiospores. It also has dolipores in the hyphal septa and ballistoconidia in culture. In contrast to species of Tilletia and related genera, the teliospores are scattered in intercellular spaces in the mesophyll without rupturing it and develop mostly intercalaryly. Additionally taking into account the distinct host family, the agent of angular black spot disease of beans cannot be classified in any known genus. The new genus Erratomyces is proposed. Further species of Protomycopsis described from India, namely P. ajmeriensis, P. crotalariae, P. smithiae, and P. thirumalacharii, belong to this new genus because they are also characterized by the production of leaf spots on Leguminosae, and have partition layers and dolipores. They are presented as new combinations in the new genus.
Article
We document here for the first time ultrastructural details of the cellular interaction of Asteridiella callista and its host Stachytarpheta mutabilis var. violacea from Costa Rica. A. callista attaches to the host with appressoria, invades the epidermal cell wall and forms an apoplastic complex cisternal net, presumably for nutrient uptake from its host. This unique structure, called an interaction apparatus (Ia), consists of cisternae surrounded by a membrane continuous with the fungal cytoplasmic membrane. Subsequently the apoplastic trunk of the Ia extends into the host epidermal cell wall and contacts the host cytoplasmic membrane. Electron-opaque material, probably of fungal origin appears at the host cytoplasmic membrane. Finally these electron-opaque deposits are encased by host material. Functional and systematical aspects of this interaction scenario are discussed.
Article
In this study we provide a phylogenetically based introduction to the classes and orders of Pucciniomycotina (= Urediniomycetes), one of three subphyla of Basidiomycota. More than 8000 species of Pucciniomycotina have been described including putative saprotrophs and parasites of plants, animals and fungi. The overwhelming majority of these (~90%) belong to a single order of obligate plant pathogens, the Pucciniales (= Uredinales), or rust fungi. We have assembled a dataset of previously published and newly generated sequence data from two nuclear rDNA genes (large subunit and small subunit) including exemplars from all known major groups in order to test hypotheses about evolutionary relationships among the Pucciniomycotina. The utility of combining nuc-lsu sequences spanning the entire D1–D3 region with complete nuc-ssu sequences for resolution and support of nodes is discussed. Our study confirms Pucciniomycotina as a monophyletic group of Basidiomycota. In total our results support eight major clades ranked as classes (Agaricostilbomycetes, Atractiellomycetes, Classiculomycetes, Cryptomycocolacomycetes, Cystobasidiomycetes, Microbotryomycetes, Mixiomycetes and Pucciniomycetes) and 18 orders.