2006 AGERER Fungal relationships and struct of their ectomycorrhizae

Prévia do material em texto

Mycol Progress (2006) 5: 67–107
DOI 10.1007/s11557-006-0505-x
REVIEW ARTICLE
Reinhard Agerer
Fungal relationships and structural identity
of their ectomycorrhizae
Received: 3 January 2006 / Revised: 13 January 2006 / Accepted: 13 February 2006 / Published online: 1 June 2006
# German Mycological Society and Springer 2006
Abstract Aproximately 5,000–6,000 fungal species form
ectomyorrhizae (ECM), the symbiotic organs with roots of
predominantly trees. The contributing fungi are not evenly
distributed over the system of fungi. Within Basidiomycota
exclusively Hymenomycetes and within Ascomycota
exclusively Ascomycetes contribute to the symbiosis.
Hymenomycetes play a big part, Ascomycetes a minor
role; Zygomycetes only form exceptionally ECM. Re-
sponsible for ascomycetous ECM are mostly Pezizales
with their hypogeous derivatives, whereas Boletales,
Gomphales, Thelephorales, Amanitaceae, Cantharellaceae,
Cortinariaceae, Russulaceae, and Tricholomataceae are the
most important ectomycorrhizal relationships within
Hymenomycetes. ECM, as transmitting organs between
soil and roots, are transporting carbohydrates for growth of
mycelium and fruitbodies from roots and have to satisfy the
tree’s demand for water and nutrients. The latter task
particularly influences the structure of ECM as nutrients
are patchily distributed in the soil and saprotrophic as well
as ectomycorrhizal fungi can act as strong competitors for
nutrients. In focusing these requirements, ECM developed
variously structured hyphal sheaths around the roots, the
so-called mantles, and differently organized mycelium that
emanates from the mantle, the so-called extramatrical
mycelium. The mantles can be plectenchymatous consist-
ing of loosely woven, differently arranged hyphae or they
are densely packed, forming a pseudoparenchyma similar
to the epidermis of leaves. The extramatrical mycelium
grows either as simple scattered hyphae from the mantle
into the soil or it can be united to undifferentiated
rhizomorphs with a small reach or to highly organized
root-like organs with vessel-like hyphae for efficient water
and nutrient transport from distances of decimeters.
Cystidia, sterile and variously shaped hyphal ends,
possibly appropriate for preventing animal attack, in
addition, can cover mantles and rhizomorphs. Although
only a limited number of species could be considered, some
general conclusions are possible.
The genus Tuber forms needle-shaped cystidia and lacks
rhizomorphs and clamps. Gomphales ECM are identified
by rhizomorphs with ampullate inflations at septa of
some hyphae and by oleoacanthocystidia or/and
oleoacanthohyphae. Thelephoraceae reveal a great diver-
sity of mantle structures and of extramatrical mycelium,
with some additional optional characters, i.e., dark brown
color, cystidia, blue granules, amyloid hyphae, or amy-
loid septa. Bankeraceae are mostly characterized by
plectenchymatous mantles with star-like pattern and
chlamydospores. Russulaceae possess smooth and hydro-
philic ECM. Russula forms plectenchymatous mantles
with knob-bearing cystidia, so-called russuloid cystidia,
or pseudoparenchymatous mantles without cystidia.
Lactarius lacks cystidia and shows laticifers within
plectenchymatous or within pseudoparenchymatous man-
tles. The Boletales families Boletaceae, Gyroporaceae,
Melanogastraceae, Paxillaceae, Rhizopogonaceae, Sclero-
dermataceae, and Suillaceae have the most advanced
rhizomorph type, the so-called boletoid rhizomorphs, and
reveal generally plectenchymatous mantles, frequently
with ring-like patterns. Gomphidiaceae and Albatrella-
ceae provide cystidia, plectenchymatous mantles, and
amyloidy; Gomphidiaceae are generally growing in ECM
of Suillaceae and Rhizopogonaceae. Cortinariaceae reveal
plectenchymatous mantles and undifferentiated or differ-
entiated rhizomorphs or lack rhizomorphs at all.
Cortinarius and Dermocybe are distinct by irregularly
shaped, bent to tortuous ECM with many rhizomorphs,
some growing over the mycorrhizal tip into the soil.
Inocybe lacks rhizomorphs and its emanating hyphae are
furnished by many secondary septa and prominent
clamps with a hole. Rozites lacks rhizomorphs, too, and
reveals a distinctly amyloid gelatinous mantle matrix.
Descolea and Descomyces are covered by bolbitioid
cystidia. Lastly, the genus Tricholoma forms plectenchy-
matous mantles and a high diversity of rhizomorphs.
R. Agerer (*)
Department Biology,
Biodiversity Research and GeoBio-Center,
Ludwig-Maximilians-University München,
Menzinger Street 67,
80638 München, Germany
e-mail: reinhard.agerer@lrz.uni-muenchen.de
Some of the ectomycorrhizal features are used to
hypothesize relationships at different taxonomic levels.
These conclusions are compared with recently developed
molecular hypotheses. Correspondence between the two
types of hypotheses are evident, while some conflicts wait
for a settlement.
Introduction
Detailed drawings of ectomycorrhizae (ECM) published by
Gibelli (1883) and Frank (1885) already revealed a
structural diversity of ECM. Frank (1885) depicted three
different types: one with a plectenchymatous mantle and
emanating hyphae (EHY) growing out from the hyphal
sheath, a second with rhizomorphs (RH), and a third one
with a pseudoparenchymatous mantle possessing mantle
cells resembling those of a true parenchyma. Although all
three ECM have not been identified, i.e., the causing fungi
could not be proven, this was the staring point of a now
120-year period of anatomical studies on ECM. But it
lasted almost a century until the structure of ECM was
recognized as being important for function (e.g., Marx and
Davey 1969; Brownlee et al. 1983; Kammerbauer et al.
1989) and essential for studies on fungal relationships
(Giraud 1979; Godbout and Fortin 1985). The first detailed
ECM descriptions at species level using plan views of
mantle and rhizomorph organization originate from the late
1960s. Schramm (1966) characterized ECM of Astraeus
hygrometricus (Pers.) Morgan and Thelephora terrestris
Ehrh., while Chilvers (1968) those of Cenococcum
geophilum Fr. and Octaviania densa (Rodway) G. Cunn.
Since then, many short and several detailed descriptions of
ECM have been published (de Roman et al. 2005).
A first attempt to summarize ectomycorrhizal features
for definition and delimitation of fungal relationships
originates from Agerer (1995). In the last decade, some
more papers have been published that focus on ECM
anatomy of selected fungal groups and conclude that
rhizomorph and mantle features are an aid for delimitation
and recognition of fungi at different systematic levels
(Agerer 1999a; Agerer and Beenken 1998a; Agerer et al.
1996a, 1998b; Agerer and Iosifidou 2004; Agerer and
Rambold 1998; Beenken 2004a,b; Eberhardt 2000, 2002;
Eberhardt et al. 2000; Hahn et al. 2000). Some 5,000–6,000
fungal species are estimated to be ectomycorrhizally
symbiotic with plants (Molina et al. 1992), but only a
small proportion of these species is definitely known to
form ectomycorrhizae and from even less has their detailed
anatomy been investigated. de Roman et al. (2005) list 343
species, i.e., roughly 6–7% of the presumably ectomycor-
rhizal fungi. Most of them occur in Europe and North
America; extremely low is the number of ectomycorrhizal
species sufficiently studied from Asia, Africa, and
Australia (de Roman et al. 2005). In spite of this low
number, a few generalizations may now be attempted,
particularly for those relationships where a comparably
higher proportion of species has been studied. This regards
on the one hand a few genera, e.g., Tuber, Gomphidius, and
Russula, and on the other hand some families, e.g.,
Boletaceae, Gomphidiaceae, and Russulaceae, and lastly
orders, e.g., Gomphales. Even in underrepresented rela-
tionships with respect to the proportion of studied species,
conclusions can be drawn when extraordinaryfeatures
occur in all studied examples, e.g., Gomphales.
For the following classification of phyla, classes, and
subclasses, we follow Agerer (2003), Begerow et al.
(1997), and Weiss et al. (2004a).
Within Ascomycota, ECM are only known of the class
Ascomycetes and herein, almost exclusively within the
order Pezizales, Elaphomycetales (de Roman et al. 2005;
Molina et al. 1992). But there are a few brief, still
unconfirmed reports that some species of Leotiales should
be competent for ECM production (Maia et al. 1996). The
worldwide-distributed imperfect fungus C. geophilum
clusters in DNA studies close to the loculascomycete
orders Pleosporales and Dothideales (LoBuglio et al.
1996). Within the Basidiomycota, ECM are only known
within Hymenomycetes subclass Hymenomycetidae
(Agerer 1987–2006; de Roman et al. 2005; Molina et al.
1992). Several lineages of this subclass form ECM (Agerer
1987–2006, 1999a; Bruns et al. 1998; Hibbett et al. 2000).
Very restricted reports exist from ECM of Zygomycetes. A
few species of the Endogonales are known to form such
ectotrophic symbiotic organs (Bonfante-Fasolo and
Scannerini 1977; Chu-Chou and Grace 1979, 1983,
1984; Fassi 1965; Fassi and Palenzona 1969; Fassi et al.
1969; Powell 1976; Wu and Lin 1997). Enough detailed
descriptions of ECM are only available for Ascomycetes
and Hymenomycetidae to attempt a synthesis of structural
patterns and a comparison to fungal relationships, as they
are presently discussed or accepted. For the following
comparison between structural patterns of ECM and fungal
lineages, we use for Hymenomycetidae preferentially
Binder et al. (2005) and Moncalvo et al. (2002), and
for Ascomycetes Landvik et al. (1997) and O’Donnell
et al. (1997).
Informative ectomycorrhizal features
In general, all anatomical features that include hyphae can
be applied to characterize ECM (Agerer 1991a, 1987–2006;
Agerer and Rambold 2004–2005), but only four anatomical
complexes are informative for recognition of fungal
relationships: (a) structure of outer mantle layers as seen
in plan view, (b) structure of rhizomorphs, (c) shape of
cystidia (CY), and (d) features of emanating hyphae. Some
additional non-anatomical informative characters may
occur, for example, (e) chemical reactions (CR) and
(f) color of ECM (Agerer 1991a, 1987–2006; Agerer and
Rambold 2004–2005). The sequence from (a) to (f)
indicates decreasing taxonomic and systematic importance.
68
The mantle types
Since Frank’s (1885) publication of a plectenchymatous
and a pseudoparenchymatous mantle type (MTY), several
distinctive structures of outer mantle layers as seen in plan
view have been recognized and represented in several
publications by capital letters from A–Q (Agerer 1987–
2006, 1991a, 1995; Agerer and Rambold 2004–2005). A
plectenchymatous series (A–I), with a hyphal sheath still
showing individual hyphae, contrasts to a pseudoparenchy-
matous one with short-celled, inflated, and compactly
glued hyphae, resembling a true parenchyma (K–Q).
Pseudoparenchymatous mantles appear in a structural and
evolutionary sense more advanced than plectenchymatous
hyphal sheaths (Agerer 1995).
The most primitive mantle is composed of randomly
arranged hyphae (type B, Fig. 1a), whereas type A shows a
pattern of rings formed by a few hyphae growing together
for a short distance, ramifying at places where other hyphae
join, thus forming knots similar to those of a soccer net
(Fig. 1b). This pattern is called ring-like and not net-like, as
‘hyphal net’ is a general term for connected hyphae
irrespective of whether they form a structural pattern or not.
When the knots of the joining hyphae become very massive
and the connecting hyphae between these knots less
distinct, mantle type A is called star-like (Fig. 1c). In
Fig. 1 a–i Mantle types. a Mantle type B: plectenchymatous, with
irregularly arranged hyphae (from Tomentella brunneorufa, Agerer
and Bougher 2001, with permission). b Mantle type A: plecten-
chymatous, with a ring-like hyphal pattern (from Chamonixia
caespitosa, Raidl 1999, with permission). c Mantle type A:
plectenchymatous, with star-like pattern (from Bankera fuligineoal-
ba, Agerer and Otto 1997, with permission). d Mantle type C:
plectenchymatous, with gelatinous matrix (from Gomphus clavatus,
Agerer et al. 1998a, with permission). e Mantle type D:
plectenchymatous, with awl-shaped cystidia (from Thelephora
terrestris, Agerer and Weiss 1989, with permission). f Mantle type
D: plectenchymatous, with awl-shaped, and obclavate russuloid
cystidia (from Russula atroglauca, Beenken 2001c, with permis-
sion). g Mantle type E: plectenchymatous, with squarrosely
branched hyphae (from Elaphomyces muricatus, Brand 1991a,
with permission). h Mantle type F: plectenchymatous, with globular
cells (from Suillus grevillei, Treu 1990a, with permission). i Mantle
type G: plectenchymatous, with star-like tightly glued hyphae,
cenococcoid mantle (from Cenococcum geophilum, Gronbach 1988,
with permission)
69
some cases, a differently noticeable gelatinous matrix,
apparently as a water reservoir, can be present between the
hyphae (type C, Fig. 1d). This mantle type applies only
when there are no further distinctive features, such as rings
or cystidia. Cystidia are characteristic of mantle type D
(Fig. 1e,f). This type belongs to the plectenchymatous
series. Cystidia can also be present on the surface of
pseudoparenchymatous mantles (see below). Mantle type E
is very similar to type B, but the hyphae are squarrosely
branched, i.e., the hyphae are multi-ramified with short,
frequently y-shaped or almost rectangular branches
(Fig. 1g). Some inflated cells or globular terminal cells
on an otherwise undifferentiated mantle are characteristic
of mantle type F (Fig. 1h). Mantle type G forms star-like
patterns, but there is no space between the hyphae and, by
that, it is completely different from the star-like structures
of mantle type A. This structure is predominantly known
from Cenococcum geophilum Fr., and therefore, derived
from this genus name, this mantle can be called
cenococcoid (Fig. 1i). Mantle type H is very similar to
type E, but the hyphae appear rather inflated; however, they
still form interspaces (Fig. 2a). A more pronounced
inflation and the reduction of the interspaces would direct
to a pseudoparenchymatous mantle with epidermoid cells
(Fig. 2h). Rather short, often slightly tortuous or irregularly
bent perpendicular cells form a velvet-like structure on the
Fig. 2 a–j Mantle types. a Mantle type H: plectenchymatous,
transitional type to pseudoparenchymatous with inflated cells and
interspaces (from Russula xerampelina, Agerer 1986b, with
permission). b Mantle type I: plectenchymatous, with rather short,
often slightly tortuous or irregularly bent perpendicular cells
forming a velvet-like cover (from Lactarius acris, Brand 1991a,
with permission). c Mantle type L: pseudoparenchymatous, cells
angular to roundish (from Leucangium carthusianum, Palfner &
Agerer 1998b, with permission). d Mantle type K: pseudoparenchy-
matous, cells angular and with roundish cells on the mantle surface
(from Fagirhiza spinulosa, Brand 1991a, with permission). eMantle
type K: pseudoparenchymatous, cells angular, forming rosette-like
structures (roundish cells on the mantle surface not shown) (from
Quercirhiza tomentellocystidiata, after Azul and Freitas 2006c, with
permission). f Mantle type O: pseudoparenchymatous, cells angular,
heaps of flattened or easily collapsing cowl-shaped cells (from
Russula ochroleuca, Pillukat and Agerer 1992, with permission).
g Mantle type P: pseudoparenchymatous, cells angular to roundish,
with a hyphal net (from Lactarius lepidotus, Wiedmer and Senn-Irlet
2004, with permission). h Mantle type Q, pseudoparenchymatous,
cells epidermoid (left) with a hyphal net (right) (from Russula
lepida, Beenken 2004a, with permission).i Pseudoparenchymatous,
with solitary cells stainable in sulpho-vanillin (from Russula mairei,
Brand 1991a, with permission). j Laticifers in middle mantle layers
(from Lactarius salmonicolor, Pillukat 1996, with permission)
70
surface in mantle type I (Fig. 2b). As these cells are all
stainable with the dye sulpho-vanillin (Agerer 1986a),
these hyphal ends could also be regarded as cystidia.
The pseudoparenchymatous series can generally be
divided into mantles that show angular to roundish cells
(types K, L, O, and P) and those that form epidermoid,
puzzle-like structures (M and Q). Most of the pseudopar-
enchymatous sheaths bear either a hyphal net on the surface
or globular or flattened cells either singly or mostly in
groups. Naked pseudoparenchymatous mantles (type L and
M) are rare (Fig. 2c). Mantle type K with angular to
roundish cells (Fig. 2d), sometimes arranged in rosettes
(Fig. 2e), is furnished with globular cells either solitary or
in small groups, whereas heaps of flattened or easily
Fig. 3 a–f Rhizomorph types. aUniform-loose, hyphae uniform and
loosely arranged (from Cortinarius atropusillus, Wiedmer and Senn-
Irlet (1999b), with permission). b Uniform-compact, hyphae uniform
and densely packed and glued together (from Bankera fuligineoalba,
Agerer and Otto 1997, with permission). c Thelephoroid, peripheral
hyphae thinner than central ones (from Pinirhiza discolor, Golldack
et al. 1998b, with permission). d Thelephoroid, forming nodes (from
Quercirhiza nodulosomorpha, Azul et al. 1999, with permission).
e Ramarioid, with some ampullate inflations at septa (from
Ramaricium alboochraceum, Hahn et al. 2000, with permission).
f Phlegmacioid, some thicker, randomly distributed hyphae (from
Cortinarius hercynicus, Agerer 1988b, with permission)
71
collapsing cowl-shaped cells are characteristic of mantle
type O (Fig. 2f). A pseudoparenchyma with angular cells
bearing a hyphal net is typical of mantle P (Fig. 2g); when
the pseudoparenchyma cells are epidermoid (Fig. 2h), type
Q is applied. The formerly distinguished mantle type N
with solitary cells stainable in sulpho-vanillin is now
obsolete as such cells are, in some cases, an additional
feature of mantle types O, P, and Q (Fig. 2i; Beenken
2004a). Laticifers, latex-containing, long, thick, scarcely
branched hyphae can occur in plectenchymatous and
pseudoparenchymatous mantles (Fig. 2j).
The rhizomorph types
Although the term rhizomorph has been originally applied
to a root-like, continuously growing sclerotium (Agerer
and Iosifidou 2004) of the tree parasite Armillaria (comp.
Donk 1962), it is now generally accepted in a broader sense
for ‘multi-hyphal linear aggregates’ (Cairney et al. 1991;
Agerer 1999a) irrespective of their internal organization
and their ontogeny (Agerer and Iosifidou 2004). The
knowledge of the diversity of the internal organization has
a long tradition and dates back to Falck (1912), who
studied in detail the highly differentiated rhizomorphs of
the saprotrophic fungus Serpula lacrymans (Wulfen) J.
Schröt. In the 1960s, a structural diversity of the
rhizomorphs of ectomycorrhizal fungi has been shown
(e.g., Chilvers 1968; Luppi and Gautero 1967; Schramm
1966; Fassi and de Vecchi 1962). But a comprehensive
typology of rhizomorph structures was first published in
1991 (Agerer 1991a) and has been extended in 1999 under
inclusion of ontogenetical aspects (Agerer 1999a).
Seven rhizomorph types could be distinguished (Agerer
1999a; Agerer and Iosifidou 2004). Uniform-loose rhizo-
morphs (Fig. 3a) are composed of normal vegetative
hyphae, i.e., the hyphae are undifferentiated throughout the
rhizomorph. They are loosely bundled. Uniform-compact
rhizomorphs (Fig. 3b) possess uniformly shaped hyphae,
too; but these are densely agglutinated. Thelephoroid
rhizomorphs (Fig. 3c,d) are slightly differentiated with
only the peripheral hyphae differing somewhat in diameter
and structure. Ramarioid rhizomorphs (Fig. 3e) are
internally differentiated and distinctive due to ampullate
inflations at the hyphal septum of the lower cell. Russuloid
rhizomorphs (Fig. 4a) have some irregularly distributed
thickened hyphae with often incomplete septa, accompa-
nied by ladder-like thick-walled hyphae with several septa
in short distance. Phlegmacioid rhizomorphs (Fig. 3f)
possess a few randomly distributed slightly thicker hyphae,
often embedded in a matrix. They can enlarge their septal
pore, but a distinct septal dissolution is mostly lacking.
Agaricoid rhizomorphs are highly differentiated and
possess vessel-like hyphae, i.e., predominantly centrally
arranged, strongly inflated hyphae reveal partially or even
completely dissolved septa. These hyphae originate from
early ontogenetical stages and include forward and simple
backward growing hyphae (Agerer and Iosifidou 2004,
Fig. 8b). This type is yet unknown in ectomycorrhizal
fungi. The final structure of boletoid rhizomorphs (Fig. 4b)
is similar to that of agaricoid ones, but there are important
differences regarding the ontogeny of both types. The
vessel-like hyphae of boletoid rhizomorphs originate from
early ontogenetical stages, too; but the formation of the
hyphae differs. Backward-growing hyphae fork close to
their origin. One of the resulting branches grows backward,
i.e., towards the base of the rhizomorph, the other forward,
i.e., towards the tip of the rhizomorph (compare Agerer and
Iosifidou 2004, Fig. 8c). This type of hyphal ramification
will be subsequently called as split type. The internal
structure of the rhizomorphs with vessel-like hyphae has
very likely important impacts on their function (Brownlee
et al. 1983; Kammerbauer et al. 1989) but can also be
applied for recognition and delimitation of fungal relation-
ships (Agerer 1999a; Agerer and Iosifidou 2004). Several
ectomycorrhizal species do not form rhizomorphs at all.
In general, rhizomorphs connected to the stipe base of
fruitbodies and those growing out of the ectomycorrhizal
mantle are identical in structure. But there are a few
exceptions. So-called dimorphic rhizomorphs have been
shown for Thelephora terrestris Ehrh. (Schramm 1966),
Dermocybe crocea (Schaeff.) M.M. Moser, D. palustris
(M.M. Moser) M.M. Moser, D. semisanguinea (Fr.) M.M.
Moser (Agerer 1995; Uhl 1988a), and Russula ochroleuca
(Pers.) Fr. (Agerer 1986b; Gronbach 1988; Pillukat and
Agerer 1992). With the exception of R. ochroleuca, the
rhizomorphs of all other species remain though they are
dimorphic within their general type. R. ochroleuca reveals
uniform-loose rhizomorphs when they grow into the soil,
but russuloid ones when they grow along roots or connect
ECM with fruitbodies.
Fig. 4 a,b Rhizomorph types. a Russuloid, with thick and with
ladder-like hyphae with septa in short distances (from Russula
medullata, Beenken 2004a, with permission). b Boletoid, with
vessel-like hyphae (septa partially or completely dissolved) (from
Quercirhiza sclerotiigera, Azul et al. 2001, with permission)
72
In some relationships, short and wide mycorrhiza-like
outgrowths often with blunt tips can occur (Agerer 1998a).
ECM can form different amounts of rhizomorphs and
emanating hyphae, what can be used to distinguish so-
called exploration types (ET) (Agerer 2001). They can be
representative for some fungal relationships, too. The
‘contact ET’ forms smooth mantles with only a very
limited amount of emanating hyphae, which are in most
cases lost during isolation of the ECM from the soil. This
type is predominantly hydrophilic (HI), i.e., water can
easily contact and moisten the ECM. Many emanating
hyphae and hydrophily are characteristic of the ‘short-
distance ET’. The emanating hyphae are frequently very
dense and grow a considerable distance into the surround-
Fig. 5 a–j Cystidia types. a Awl-shaped, bent, unramified (from
Pinirhiza gomphidioidea, Mleczko 1998a, withpermission). b Awl-
shaped, proximally ramified (from Russula vesca, Beenken 2001m,
with permission). c Fibulocystidia-type, with an intercalar clamp
(from Tomentella galzinii, Jakucs et al. 1997, with permission).
d Capitate, with an abrupt inflation (from Pinirhiza globulifera,
Mleczko 1998c, with permission). e Bottle-shaped, with a strongly
inflated base and a long torn out neck (from Piceirhiza nigra, after
Berg 1989, with permission). f Bolbitioid, with lateral outgrowth
and an apical globule (from Descolea antarctica, Palfner 1997, with
permission). g Awl-shaped, with dichotomous and tritomous
ramifications (from Piceirhiza sp., Agerer, unpublished). h Capitate,
with a clavate distal end (from Populirhiza pustulosa, Mleczko
1987b, with permission). i Russuloid, flask-shaped with apical
knobs (from Russula nigricans, Mleczko 2004d, with permission). j
Oleoacanthocystidia, yellowish-filled hyphae with short lateral
outgrowths, roundish cells with the same contents (from Gomphus
clavatus, Agerer et al. 1998a, with permission)
73
ing soil (Agerer and Raidl 2004). The ‘medium-distance
ET’ forms rhizomorphs that are uniform-loose, uniform-
compact, thelephoroid, or phlegmacioid. They grow a
considerable distance into the soil, often up to more than
30–50 mm. The most frequent subgroup of this type is the
‘fringe subtype’ with many rhizomorphs that are often
interconnected by thinner filaments and by variably dense
emanating hyphae; the fringe subtype is hydrophobic (HO)
(Agerer and Raidl 2004). Hydrophobic ECM have a silvery
appearance when they are mounted in water because air
remains included between the hyphae, preventing a contact
with water. The ‘smooth subtype’, mostly hydrophilic,
forms smooth rhizomorphs. The ‘mat subtype’ occupies
rather large areas in the soil, where ECM with their
emanating hyphae and rhizomorphs are so densely
aggregated that there is apparently no space for other
ECM species; rhizomorphs are of the uniform-loose, of the
phlegmacioid, or of the ramarioid type. In addition, these
generally hydrophilic ECM may dry out the soil to such an
extent that engulfed soil particles are very difficult to get
remoistened. The ‘long-distance ET’ is characterized by
very long highly differentiated rhizomorphs with vessel-
like hyphae. These rhizomorphs obtain a length of several
decimeters. These ECM are including their rhizomorphs
generally hydrophobic.
The cystidia
Although cystidia occur on the cap skin, gills, and stipe of
fruitbodies of different hymenomycetous relationships,
their occurrence on ECM and rhizomorphs is not generally
known. They have already been depicted on ECM by
Dominik (1956, 1969). A compilation of different types
was published by Agerer (1991a, 1995, 1987–2006), and
some of the more distinctive cystidia useful for the
following considerations are briefly characterized here.
Cystidia that are called awl-shaped are provided with
thick walls including their distal end; they can be clamped
or only simple septate (Fig. 5a–c). Some are unramified
(Figs. 1f and 5a,c), others are ramified exclusively at their
proximal part (Fig. 5b), a third group is defined by a
monopodial ramification, and a last entity reveals dichot-
omous or tritomous or quadritomous ramifications
(Fig. 5g). The unramified cystidia can be straight, bent,
or hook-like. Russuloid cystidia (Figs. 1f and 5i) are flask-
shaped with oily contents, in most cases distinctly stainable
in sulpho-vanillin, and possess one or more small apical or
subapical knobs that can break off easily. Bolbitioid
cystidia (Fig. 5f) show a lateral, acuminate outgrowth
with a small globule. Capitate cystidia may have a clavate
distal end (Fig. 5h) or can terminate with an abrupt inflation
(Fig. 5d). Globular, cowl-shaped, or obclavate cells
(Fig. 2d,f) are often not regarded as cystidia. But they are
distinctive structures, particularly for delimitation of mantle
types, and are sometimes noticeable cells of the rhizomorph
surface. Bottle-shaped cells form a strongly inflated base
and a long torn-out neck. Both parts are thick-walled
(Fig. 5e). The necks can be straight, bent, or very
infrequently sinuous. Oleoacanthocystidia (Fig. 5j) have
short side-branches and are filled by yellow contents. These
cystidia are often accompanied by identically filled, thin-
walled globular cells (Fig. 5j).
Emanating hyphae
Many species-specific features can be found on emanating
hyphae: color, cell wall thickness, type of ramification,
surface, presence of crystals, or drops of pigments. But
these characters can only exceptionally be used for
delimitation of fungal relationships. Exceptions are the
formation and the shape of clamps, sometimes the presence
and distribution of secondary septa, and in particular the
kind of anastomoses. Open anastomoses are widely
distributed, but anastomoses closed by a simple septum
or a clamp are very informative (Agerer 1995).
Chemical reactions
Chemical reactions are only exceptionally important. Most
informative for discussion of fungal relationships is an
amyloid or dextrinoid reaction with Melzer’s reagent
(Agerer 1986a, 1995, 1999a) of portions of cell walls or
of a mantle matrix, but it can restrictedly occur in hyphal
septa. KOH sometimes changes brownish colors to greenish
and does this also with blue granules.
Color of ectomycorrhizae
A high diversity of colors can occur (Agerer 1987–2006).
This feature is especially important for identification of
species, as ECM color often mirrors the color of the
fruitbody’s cap. For some relationships, however, the color
might be a good marker. This applies for brown ECM and
of any color that changes to black, what is often followed
by a successive destruction of the ECM beginning from
their proximal end. This can be seen, for example, in ECM
of Phellodon niger (Fr.) P. Karst. (Agerer 1993a).
Abbreviations used MTY, mantle type (compare Figs. 1, 2,
3, 4 and 5); RH, rhizomorph (compare Figs. 3a–f and 4a,b);
CY, cystidia (compare Fig. 5a–j); EHY, emanating hyphae;
CR, chemical reactions; ET, exploration type (for explana-
tion, see above; Agerer 2001); HI/HO, hydrophilic/hydro-
phobic (for explanation, see above; Agerer and Rambold
2004–2005); and ECM, ectomycorrhizae.
Fungal relationships and their ectomycorrhizal features
The following compilation focuses at first on genera,
secondly – where appropriate – at subgeneric entities,
followed by considerations regarding family-specific
characteristics, if more than one genus of a family is
known regarding ECM, and lastly, in a few cases, also
74
orders or even higher systematic categories are briefly
discussed. For indication how weak or strong the provided
generalizations are, the number of investigated species, the
number of expected ectomycorrhizal species, and the
number of known species within a genus are provided, e.g.,
[3/20(30)]: the conclusions are based on 3 out of 20
supposed or known ectomycorrhizal species of a genus
with 30 species in total. Suppositions regarding ectomy-
corrhiza status are based on personal experience or/and on
assumptions made in various publications or/and with
reference to associations of fruitbodies with a limited set of
host tree genera; these data will not be accompanied by
citation of references. When families, orders, or higher
categories are discussed, these numbers refer to genera
[investigated genera/genera assumed as forming ECM
(total number of genera)]. These relations generally
indicate for most of the genera an urgent need for further
analyses of ECM anatomy. Although in many cases only a
few species have been sufficiently studied, general
conclusions might be possible when extraordinary features
occur that are not found elsewhere and therefore can be
accepted as synapomorphies of a group. Families with their
ectomycorrhizal genera are listed (Table 1), accompanied
by the totalnumber of known genera, and number and
names of proven or supposed ectomycorrhizal genera. This
should give the reader an impression what relationships
contribute to the estimated thousands of ectomycorrhizal
species.
The conclusions based upon ECM anatomy will
occasionally be compared to concepts that are predomi-
nantly based on fruitbody anatomy and to those of
molecular phylogenetics. Only sufficiently studied ECM
and unequivocally determined species are taken into
account and only those references that provide at least
important mantle and rhizomorph characteristics as seen in
plan views are added. Descriptions of ECM that are
exclusively based on synthesized material are usually
omitted, as artificial growth conditions often do not provide
features occurring in nature. When mantles are described
below as plectenchymatous or pseudoparenchymatous,
these terms generally refer to the structure in plan views
and not in sections. Family affiliations of genera and
number of species within the genera follow generally
Hawksworth et al. (2001), where indicated exceptionally
Hawksworth et al. (1995) or Agerer (1999a). Species
names and their authorities are taken from Index Fungorum
(2005).
Ascomycetous ectomycorrhizae
Cenococcum [1/1(1)]: MTY G; RH lacking; CY lacking;
EHY frequent, clamps lacking; CR lacking; ET short
distance; HI; ECM black.
C. geophilum Fr.: e.g., Chilvers (1968), Danielson (1984a), Gronbach (1988),
Harniman and Durall (1996a), Hatch (1934), Haug and Pritsch (1992),
Ingleby et al. (1990), Lihnell (1942), Palfner (2001), Rose et al. (1981),
Trappe (1964).
Remarks: The worldwide-occurring ECM C. geophilum is
possibly the most-known ECM, at least regarding its
distribution and its striking morphology (Trappe 1964), but
perhaps not the best known anatomically. Unpublished
studies (Berg 1986) showed that the anatomy of the mantle,
though generally cenococcoid, can vary in the dimensions
of the cells within the radiating mantle hyphae. The
occurrence of two different anatomotypes correlated with
the mantle cell dimensions. The small-celled type [(12)15–
19(19)×4–5 μm] occurred in sandy soil above a tertiary
limy gravel and formed many ECM and a small number of
sclerotia, whereas the large-celled type [15–20(25)×7–
10 μm] grew in loamy soil and produced only rather few
ECM and a high number of sclerotia. Differences in pH
between the two areas were not evident. Features of pure
culture differed, too; but at the beginning of the 1980s,
DNA comparison for confirming the identity of the
cultures was not available. It can be expected that the
genus Cenococcum does not only differ in DNA (Farmer
and Sylvia 1998; Jany et al. 2002) but is very likely
composed of several species.
Elaphomyces [3/20(20)], Elaphomycetaceae: MTY A, C,
or E; RH lacking; CY lacking; EHY abundant, clamps
lacking, frequently densely covered with soil particles,
sometimes with spindle-shaped wall swellings (Agerer and
Rambold 2004–2005); CR lacking; ET short distance; HI;
ECM reddish to brown.
Elaphomyces aculeatus Tul.: Agerer (1999b, 2002a); Elaphomyces granu-
latus Fr.: Gronbach (1988, 1989a, sub nomine Piceirhiza glutinosa);
Elaphomyces muricatus Fr.: Brand (1991a,b).
Elaphomycetaceae [1/1(1)]
Hymenoscyphus [1/1(100)], Helotiaceae: MTY E; RH
lacking; CY lacking; EHY infrequent, clamps lacking,
surface warty; CR lacking; ET contact; HI; ECM blackish.
Hymenoscyphs ericae (D.J. Read) Korf & Kernan: Gronbach (1988, sub
nomine Piceirhiza bicolorata), Brand et al. (1992, sub nomine P. bicolorata),
Vralstad et al. (2000).
Helotiaceae [1/2(100)]
Genea [2/24(24)], Pyronemataceae: MTY K, only with
solitary roundish cells on the surface; RH lacking; CY
lacking; EHY clampless, warty, with 5–7 μm rather thick;
ET short distance; CR lacking; HI; ECM brown.
Genea hispidula Berk.: Brand (1991a,c); Genea verrucosa Vittad: Jakucs and
Bratek (1998a); Jakucs et al. (1998b).
Humaria [1/15?(15)], Pyronemataceae: MTY B; RH
lacking; CY lacking; EHY infrequent, clampless, rough;
CR lacking; ET smooth; hydrophilic; ECM brown due to
root color.
Humaria hemisphaerica (F.H. Wigg.) Fuckel: Ingleby et al. (1990).
Sphaerosporella [1/2?(2)], Pyronemataceae: MYT B,
densely packed; RH lacking; CY lacking; EHY infrequent,
clampless, punctuate; CR lacking; ET smooth or short
distance; HI ?; ECM brown.
Sphaerosporella brunnea (Alb. & Schwein.) Svrček & Kubička: Danielson
(1984b), Meotto and Carraturo (1988).
75
Table 1 Genera of ectomycorrhizal fungi
Zygomycetes (Zygomycota)
Endogonaceae [0/1(1)]: Endogone
Ascomycetes (Ascomycota)
Discinaceae [0/2(3)]: Gymnohydnotria, Gyromitra
Elaphomycetaceae [1/1(1)]: ELAPHOMYCES
Geoglossaceae [0/2(6)] Geoglossum, Spathularia
Helotiaceae [1/2(100)]: HYMENOSCYPHUS, Neocudoniella
Helvellaceae [2/9(9)]: BALSAMIA, Barssia, Fischerula, Helvella, Hydnotria, LEUCANGIUM, Underwoodia, Picoa, Wynnella
Morchellaceae [1/2(3)]: Morchella, Verpa
Pezizaceae [1/10(19)]: Amylascus, Boudiera, Hydnobolites, Hydnotryopsis, Pachyphloeus, Peziza, Plicaria, Ruhlandiella,
SPHAEROZONE, Tirmania,
Pyronemataceae [4/11(68)]: GENEA, Geopora, HUMARIA, Hydnocystis, Nothojafnea, Phaeangium, Pulvinula, Sphaero -
soma, SPHAEROSPORELLA, TRICHARINA, Wilcoxina
Terfeziaceae [0/4(4)]: Cazia, Delastria, Loculotuber, Terfezia
Tuberaceae [1/6(6)]: Choiromyces, Dingleya, Labyrinthomyces, Paradoxa, Reddellomyces, TUBER
Hymenomycetes (Basidiomycota)
Albatrellaceae [2/3(5)]: ALBATRELLUS, POLYPOROLETUS, Scutiger
Amanitaceae [1/1(5)]: AMANITA
Atheliaceae [5/5(26)]: AMPHINEMA, BYSSOCORTICIUM, BYSSOPORIA, PILODERMA, TYLOSPORA
Bankeraceae [5/5(5)]: BANKERA, BOLETOPSIS, HYDNELLUM, PHELLODON, SARCODON
Bolbitiaceae [2/2(11)] DESCOMYCES, DESCOLEA
Boletaceae [6/22(26)]: Afroboletus, Aureoboletus, Austroboletus, Boletellus, BOLETUS, Chalciporus, CHAMONIXIA,
Gastroboletus, Gastroleccinum, Gastrotylopilus, LECCINUM, Paxillogaster, Phylloboletellus, Phylloporus, PORPHYRELLUS, Pulveroboletus,
Royoungia, Strobilomyces, Tubosaeta, TYLOPILUS, Veloporphyrellus, XEROCOMUS
Cantharellaceae [2/2(5)]: CANTHARELLUS, CRATERELLUS
Chondrogastraceae [0/1(1)]: Chondrogaster
Clavulinaceae [0/1(3)]: Clavulina
Cortinariaceae [8/14(31)]: Annamika, CORTINARIUS, Cuphocybe, DERMOCYBE, Destuntzia, HEBELOMA, INOCYBE, Mackintoshia,
Mycoamaranthus, NAUCORIA, ROZITES, Setchelliogaster, STEPHANOPUS, THAXTEROGASTER
Cribbeaceae [0/1(2)]: Cribbea, Mycolevis
Entolomataceae [1/2(8)]: Clitopilus, ENTOLOMA
Geastraceae [(1/2(7)]: GEASTRUM, Radiigera
Gomphaceae [2/2(11)]: CLAVARIADELPHUS, GOMPHUS
Gomphidiaceae [2/5(5)]: Brauniellula, CHROOGOMPHUS, Cystogomphus, GOMPHIDIUS, Gomphogaster
Gyroporaceae [1/2(2)]: GYROPORUS, Rubinoboletus
Hydnaceae [1/1(8)]: HYDNUM
Hydnangiaceae [1/4(4)]: Hydnangium, LACCARIA, Maccangia, Podohydnangium
Hygrophoraceae [1/2(10)]: Camarophyllus, HYGROPHORUS
Hymenochaetaceae [0/1(14)]: Coltricia
Hymenogastraceae [0/2(8)]: Hymenogaster, Quadrispora
Hysterangiaceae [1/2(11)]: HYSTERANGIUM, Trappea
Leucogastraceae [0/2(2)]: Leucogaster, Leucophlebs
Marasmiaceae [1/1(46)]: RHODOCOLLYBIA
Melanogastraceae [2/4(4)]: ALPOVA, Corditubera, Hoehnelogaster, MELANAOGASTER
Mesophelliaceae [0/4(6)]: Andebbia, Castoreum, Gummiglobus, Mesophellia
Octavianiaceae [1/2(2)]: OCTAVIANIA, Sclerogaster
Paxillaceae [3/5(9)]: Austrogaster, AUSTROPAXILLUS, Gymnopaxillus, GYRODON, PAXILLUS
Ramariaceae [2/3(8)]: Austrogautieria, GAUTIERIA, RAMARIA
Rhizopogonaceae [1/1(2)]: RHIZOPOGON
76
Tricharina [1/12?(12)], Pyronemataceae: MTY B; RH
lacking; CY lacking; EHY infrequent, clampless, rough;
CR lacking; ET smooth; HI; ECM brown due to root color.
Tricharina gilva (Boud. ex Cooke) Eckblad: Ingleby et al. (1990).
Pyronemataceae [4/11(68)]: In general, the ECM are of the
contact or short-distance exploration type with very few
rough and clampless emanating hyphae. The ECM appear
hydrophilic. The hypogeous genus Genea is theonly
member that forms pseudoparenchymatous mantles. Glob-
ular cells on the surface represent a further differentiation.
The hypogeous habit can be regarded as an apomorphic
feature as can be the pseudoparenchymatous mantle
(Agerer 1995). The mantle structure and the hypogeous
fruitbody type apparently evolved in parallel from epigeous
predecessors with plectenchymatous ECM mantles.
Balsamia [1/6?(6)], Helvellaceae: MTY B; RH lacking;
CY lacking; EHY clampless, smooth; CR lacking; ET
contact; HI; ECM brownish due to root color.
Balsamia alba Harkn.: Palfner (1998a), Palfner and Agerer (1998a).
Leucangium [1/1(1)], Helvellaceae: MTY L; RH lacking;
EHY clampless, smooth; CR lacking; ETcontact; HI; ECM
brownish.
Leucangium carthusianum (Tul.) Paol.: Palfner (1998b); Palfner and Agerer
(1998b).
Helvellaceae [2/9(9)]: Rhizomorphs do not occur; mantle
types are very diverse.
Sphaerozone [1/4?(4)], Pezizaceae: MTY B; RH lacking;
CY lacking; EHY clampless, smooth, with 7–10 μm very
wide, gradually becoming thick-walled and brown, envel-
oping the ECM with a dark brown tubular hyphal net; CR
lacking; ET short distance; HO; ECM brownish.
Sphaerozone ostiolatum (Tul.) Setch.: Brand (1988a, sub nomine Fagirhiza
tubulosa), Brand (1991a), Brand and Agerer (1988, sub nomine F. tubulosa)
Pezizaceae [1/10(19)]
Tuber [16/63(63)], Tuberaceae: MTY L, M, P, and Q; RH
lacking; CY awl-shaped, ramified in some species, at least
distal portions slightly rough (where cystidial surface
studied); EHY clampless, smooth; CR lacking; ET short
distance; HI; ECM brownish.
Tuber albidum Pico: Giraud (1990); Tuber aestivum Vittad: Granetti (1995),
Müller et al. (1996), Rauscher et al. (1996a), Zambonelli and Branzanti
(1984), Zambonelli et al. (1993, 1995); Tuber borchii Vittad.: Dunabeitia et
al. (1996), Granetti (1995), Rauscher et al. (1996b,c), Zambonelli and
Branzanti (1984), Zambonelli et al. (1993, 1995); Tuber brumale Vittad.:
Fischer et al. (2004), Fontana and Bonfante-Fasolo (1971), Granetti (1995),
Zambonelli et al. 1993; Tuber excavatum Vittad.: Giraud (1990); Tuber
himalayense B.C. Zhang & Minter: Comandini and Pacioni (1997); Tuber
indicum Cooke & Massee: Comandini and Pacioni (1997), Zambonelli et al.
(1997); Tuber maculatum Vittad.: Zambonelli et al. (1999); Tuber macro-
sporum Vittad: Giovannetti and Fontana (1981), Granetti (1995); Tuber
magnatum Pico: Granetti (1995), Zambonelli et al. (1993); Tuber melanos-
porum Vittad.: Granetti (1995), Rauscher and Chevalier (1995a), Rauscher et
al. (1995), Zambonelli et al. (1993, 1995); Tuber mesentericum Vittad.:
Granetti (1995), Rauscher and Chevalier (1995b), Rauscher et al. (1995),
Zambonelli et al. (1993, 1995); Tuber puberulum Berk. & Broome: Blaschke
(1987, 1988); Tuber rapaeodorum Tul. & C. Tul: Kovacs (2002); Tuber
rufum Pico: Palenzona et al. (1972), Rauscher et al. (1995), Rauscher and
Chevalier (1995c); Tuber uncinatum Chatin: Giraud (1990), Granetti (1995).
Remarks: The genus Tuber can be divided into two entities
with respect to ectomycorrhizal structures. One group is
characterized by pseudoparenchymatous mantles with
angular cells (MTY L, P: T. aestivum, T. excavatum,
T. mesentericum, T. uncinatum), the other group forms
pseudoparenchymatous mantles composed of epidermoid
cells (MTY M, Q: T. albidum, T. borchii, T. brumale,
T. macrosporum, T. maculatum, T. magnatum, T. mela-
nosporum, T. puberulum, T. rapaeodorum, and T. rufum).
Giomaro et al. (2000), however, reported that different
strains of T. borchii formed in synthesis experiments
pseudoparenchymatous mantles with angular, epidermoid,
and a transitional type of cells. Mantle cells of T. indicum
and T. himalayense ECM are irregularly polygonal and
represent a transitional type between typical angular and
epidermoid (Comandini and Pacioni 1997; Zambonelli
et al. 1997). The cystidia often originate on a hyphal net
on the mantle surface, but this is not reported in all studies,
possibly due to an inavailability of a differential interfer-
ence contrast microscope. Although cystidia are generally
present, they might be very infrequent, particularly when
isolation of ECM from soil was not cautious enough.
According to Rauscher et al. (1995), T. rufum lacks
cystidia, whereas in other studies they occurred infre-
quently (Chevalier, personal communication). Cystidia of
T. macrosporum and T. melanosporum are distinctly
branched, while those of T. himalyense and T. indicum
are less branched. Interpretations are sometimes difficult
due to the lack of exact drawings. Inasmuch the
Russulaceae [3/9(9)]: ARCANGELIELLA, Cystangium, Elasmomyces, Gymnomyces, LACTARIUS, Macowanites, Martellia, RUSSULA, Zelleromyces
Sebacinaceae [1/1(5)]: SEBACINA
Sclerodermataceae [3/4(7)]: ASTRAEUS, Calostoma, PISOLITHUS, SCLERODERMA
Suillaceae [2/4(4)]: BOLETINUS, Gastrosuillus, Psiloboletinus, SUILLUS
Thelephoraceae [4/6(12)]: Amaurodon, Lenzitopsis, PSEUDOTOMENTELLA, THELEPHORA, TOMENTELLA, TOMENTELLOPSIS
Tricholomataceae [2/4(107)]: Catathelasma, Leucopaxillus, LYOPHYLLUM, TRICHOLOMA
Truncocolumellaceae [1/1(1)]: TRUNCOCOLUMELLA
Numbers refer to genera [investigated regarding ECM / assumed as ECM forming (total number within the family)]. Italicized letters
indicate ECM species are proven within this genus. Normal letters indicate ECM species are supposed to occur. Capital letters indicate that
at least one species is sufficiently characterized regarding ECM (compare text). Genera affiliation follows Hawksworth et al. (2001),
complemented with Hawksworth et al. (1995) and Agerer (1999a). Compiled from different sources
Table 1 (continued)
77
holoblastic–sympodulosporous formation of conidia in
T. borchii and T. oligospermum (Tul. & C. Tul.) Trappe
(Urban et al. 2004) can be used as additional characters of
Tuber ECM has to be further studied.
Whether mantle and cystidia types fit to results obtained by
DNA sequencing is still an open question, as DNA
phylogenetic studies include on the one hand only species
with M/Q mantles and only a portion of species with such
mantles (Urban et al. 2004; Halász et al. 2005) and, on the
other hand, some of the considered species are not studied
regarding their ECM. In the study of Halász et al. (2005),
however, T. excavatum with L/P mantles is a branch of a
trichotomy with two sister groups showing type M/Q
mantles. But one sister group contains with T. foetidum
Vittad., a species with still unknown ECM structure.
Tuberaceae [1/6(6)]
Ascomycetes Ascomycetes ECM are apparently unable to
form rhizomorphs, therefore they generally belong to
exploration types that do not produce extensive and far-
reaching extramatrical mycelia. The exploitation of the
surrounding soil is restricted to the close vicinity of the
ECM. This capacity is supported by their hydrophily,
Sphaerozone ostiolatum with a hydrophobic mantle sur-
face being an exception. It is not unexpected that the ECM
do not form clamps. Cystidia are typical for the genus
Tuber and possibly complement or even substitute the
exploiting capacity of the emanating hyphae (Le Disquet
and Pargney 1996), as their emanating hyphae are
generally very scanty. The order Pezizales (Pyronemata-
ceae, Helvellaceae, Pezizaceae, and Tuberaceae) and
Elaphomycetales comprise most of the ECM-forming
species. Pleosporales (or Dothideales) and Leotiales are
only exceptionally represented.
Basidiomycetous ectomycorrhizae
The arrangement of basidiomycetous ECM follows the
sequence of clades as shown by Binder et al. (2005), where
necessary complemented by Bruns et al. (1998), Nebel
et al. (2004), and Larsson et al. (2004). The paper of
Moncalvo et al. (2002) is used for discussion of the
euagarics clade.
a. Sebacinales clade (Weiss et al. 2004a,b)
Sebacina [1/6?(6)], Sebacinaceae (ss. Weiß and
Oberwinkler 2001): MTY D/E; RH lacking; CY awl-
shaped, dichotomously,tritomously or quadritomously
ramified; EHY clampless, smooth; CR cystidia and mantle
hyphae dextrinoid; ET short distance; HI; ECM brownish.
Sebacina incrustans (Pers.) Tul. & C. Tul.: Urban et al. (2003), Azul et al.
(2006), Agerer, unpublished.
Sebacinaceae [1/1(5)]
b. Cantharelloid clade (Binder et al. 2005; Hibbett and
Thorn 2001; Larsson et al. 2004)
Cantharellus [2/65(65)], Cantharellaceae: MTY B, often
with oily droplets; RH uniform-compact; CY lacking; EHY
with clamps, anastomoses open (Cantharellus cibarius) or
closed by a clamp (Cantharellus formosus); CR lacking;
ET medium distance, smooth subtype; HI; ECM yellowish.
C. cibarius Fr.: Pillukat, unpublished; C. formosus Corner: Countess and
Goodman (2000).
Remarks: The number of known species possibly includes
also some Craterellus species, as some chanterelles have
recently been transferred to the genus Craterellus
(Dahlman et al. 2000; Feibelman et al. 1997).
Craterellus [3/20(20)], Cantharellaceae: MTY B, often with
oily droplets; RH lacking; CY lacking; EHY clamps lacking,
anastomoses not closed by a clamp; CR lacking; ET short
distance; HI; ECM yellowish to greyish.
Craterellus cornucopioides (L.) Pers.: Urban et al.(2003); Craterellus lutescens
(Pers.) Fr.: Harrington and Mitchell (2002), Pillukat, unpublished; Craterellus
tubaeformis (Bull.) Quél.: Fransson (2004a), Mleczko (2004a), Trappe et al.
(2000), Pillukat, unpublished.
Cantharellaceae [2/2(5)]: ECM are characterized by plec-
tenchymatous mantles without any pattern. Middle mantle
layers often organize the hyphae more compact and inflate
the hyphal cells. The hyphae are filled with oily droplets,
though varying considerably in density, often causing an
opaque habit. Hydrophily and lacking (Craterellus) or
uniform-compact rhizomorphs (Cantharellus) indicate soil
exploitation in the proximity of the ECM.
Although only a few species have been studied with respect
to their mycorrhizal anatomy, the lack of rhizomorphs
parallels the results obtained recently by DNA studies,
inasmuch as Cantharellus tubaeformis clusters with species
that have been regarded since a long time as typical Craterelli
(Dahlman et al. 2000; Feibelman et al. 1997; Pine et al.
1999). As a consequence, this clamp-forming species was
transferred back into the genus Craterellus (Dahlman et al.
2000), although the genus Craterellus was originally
delimited from Cantharellus by the lack of clamps (Corner
1966). Ectomycorrhizal features can apparently contribute to
genus delimitation as shape and texture of fruitbodies can,
whereas the presence of clamps, secondary septa in fruitbody
tissue, and hymenial configuration are of minor importance
(Feibelman et al. 1997).
Hydnum [2/120(120)], Hydnaceae: MTYA, with yellow oily
droplets; RH ramarioid without further differentiation; CY
lacking; EHY with clamps, anastomoses closed by a clamp;
CR lacking; ET medium distance; HO; ECM yellowish to
orange.
Hydnum repandum L.: Harrington andMitchell (2002);Hydnum rufescens Pers.:
Agerer et al. (1996b), Raidl and Agerer (1992).
Remarks: Harrington and Mitchell (2002) did not observe
rhizomorphs.
Hydnaceae [1/1(8)]
78
c. Gomphoid/phalloid clade (Binder et al. 2005; Hibbett
and Thorn 2001; Larsson et al. 2004)
Clavariadelphus [1/18?(18)], Gomphaceae: MTY B; RH
ramarioid with oleoacanthocystidia, oleoacanthohyphae and
thin-walled irregularly globular cells with yellowish contents;
in addition with short, mycorrhiza-like outgrowths often with
blunt tips; CY oleoacanthocystidia; EHY with clamps,
anastomoses open; CR lacking; ET medium distance, mat
subtype; HO; ECM whitish.
Calvariadelpus pistillaris (L.) Donk: Iosifidou and Raidl (2006).
Gomphus [1/10?(10)], Gomphaceae: MTY B/A; RH ramar-
ioid with no further differentiation, mycorrhiza- like out-
growths with often blunt tips lacking; CYonly on the hyphal
mantle: oleoacanthocystidia, oleoacanthohyphae, and thin-
walled irregularly globular cells with yellowish contents;
EHY with clamps, anastomoses open; CR lacking; ET
medium distance, mat subtype; HO; ECM whitish.
Gomphus clavatus (Pers.) Gray: Agerer (2002b), Agerer et al. (1998a).
Gomphaceae [2/2(11)]: Typical are hydrophobic ECM of the
medium-distance mat subtype, producing lots of ramarioid
rhizomorphs and abundant hyphae growing out of the
mantle. Soil particles are very densely enveloped and almost
completely dried out resulting in water-repellent crumbs
(Agerer, unpublished). The occurrence of oleoacanthohy-
phae and oleoacanthycystidia is evident.
Gautieria [1/26(26)], Ramariaceae: MTY B; RH ramarioid
with oleoacanthocystidia, oleoacanthohyphae, and thin-
walled irregularly globular cells with yellowish contents; in
addition short, mycorrhiza-like outgrowths often with blunt
tips; CY oleoacanthocystidia; EHY clamps lacking, anasto-
moses open; CR lacking; ET medium-distance, mat subtype;
HO; ECM whitish, greyish to blackish when older.
Gautieria inapire Palfner & E. Horak: Agerer 1999a, Agerer and Iosifidou
(2004), Palfner (2001).
Ramaria [11/60(221)], Ramariaceae: MTY A, B, C; RH
ramarioid with oleoacanthocystidia, oleoacanthohyphae and
thin-walled, irregularly globular cells with yellowish contents;
in addition with short, mycorrhiza-like outgrowths often with
blunt tips; CY oleo-acanthocystidia; EHY clamps frequently
lacking, anastomoses open; CR lacking; ET medium-
distance mat subtype; HO; ECM whitish, greyish to
blackish when older.
Ramaria acrisiccescens Marr & D.E. Stuntz: Nouhra et al. (2005); Ramaria
aurea (Schaeff.) Quél.: Agerer (1996a); Ramaria celerivirescensMarr & D.E.
Stuntz: Nouhra et al. (2005); Ramaria cyaneigranosa Marr & D.E. Stuntz:
Nouhra et al. (2005); Ramaria flavigelatinosa Marr & D.E. Stuntz: Scattolin
and Raidl (2006); Ramaria flavobrunnescens (G.F. Atk.) Corner: Nouhra et
al. (2005); Ramaria formosa (Pers.) Quél.: Raidl and Scattolin (2006);
Ramaria largentii Marr & D.E. Stuntz: Agerer (1996b,c); Ramaria
sandaracina Marr & D.E. Stuntz: Nouhra et al. (2005); Ramaria spinulosa
(Pers.) Quél.: Agerer (1996d); Ramaria subbotrytis (Coker) Corner: Agerer
(1996e, 1998a).
Remarks: Nouhra et al. (2005) observed oleoacanthohyphae
(they do not mention oleoacanthocystidia but should be
very likely present) only in R. cyaneigranosa and in
R. flavobrunnescens. As these structures are sometimes
only found on rhizomorphs and are very infrequent in some
species, oleoacanthocystidia should be looked for in further
collections. Oleoacanthocystidia and oleoacanthohyphae are
typical for rhizomorphs of fruitbodies, irrespective of
subgeneric affiliation (Christan and Hahn 2005). Ramaria
is heterogeneous regarding its ecology. Only Ramaria subg.
Ramaria apparently forms ECM, whereas R. subg. Asteror-
amaria, R. subg. Lentoramaria, and R. subg. Echinor-
amaria grow saprotrophic (Christan and Hahn 2005).
Ramariaceae [2/3(8)]: ECM are hydrophobic, of the medi-
um-distance mat subtype, and producing lots of ramarioid
rhizomorphs and abundant hyphae. Soil particles are very
densely engulfed and almost completely dried out resulting in
water-repellent crumbs (Agerer, unpublished). The occur-
rence of oleoacanthohyphae and oleoacanthocystidia is a
general feature.
Hysterangium [2/50(50)], Hysterangiaceae: MTY B; RH
ramarioid with oleoacanthocystidia, oleoacanthohyphae, and
thin-walled irregularly globular cells with yellowish contents;
CY oleoacanthocystidia; EHY clamps present or lacking,
anastomoses mostly open, infrequently closed by a simple
septum; CR lacking; ET medium-distance mat subtype; HO;
ECM whitish.
Hysterangium crassirhachis Zeller & C.W. Dodge: Agerer and Iosifidou (2004),
Müller and Agerer (1996a,b); Hysterangium stoloniferum Tul. & C. Tul.: Raidl
and Agerer (1998a), Agerer and Iosifidou (2004).
Hysterangiaceae [1/2(11)]
Geastrum [(1/?(50)], Geastraceae: MTY B; RH ramarioid
with peripheral,thick-walled, thin hyphae; CY oleoacantho-
cystidia, and thin-walled irregularly globular cells with
yellowish contents; EHY clamps lacking; CR peripheral,
thick-walled, thin hyphae are dextrinoid; ET medium-
distance mat subtype; HO; ECM whitish.
Geastrum fimbriatum Fr.: Agerer (1998b), Agerer and Beenken (1998a).
Remarks: G. fimbriatum does not form typical ECM, insofar
as only a mantle is formed and no Hartig net. Some hyphae
penetrating epidermal cells are encapsulated by plant cell
wall material, preventing an intracellular colonization
(Agerer and Beenken 1998a). Therefore, one of the typical
features of ECM is lacking.
Geastraceae [(1/2(7)]
Gomphales: Based upon rhizomorph structures, Agerer and
Iosifidou (2004) defined the order Gomphales and included
the families Clavariadelphaceae Corner, Gautieriaceae Zeller,
Geastraceae Corda, Gomphaceae Donk, Hysterangiaceae E.
Fisch, Ramariaceae Corner, and Sphaerobolaceae J. Schroet.
The study considered ectomycorrhizal and saprotrophic
species as well. The above compiled ectomycorrhizal
features confirm the conclusion (Agerer and Iosifidou
2004) that the order Gomphales can be delimited by
ramarioid rhizomorphs, oleoacanthocystidia and/or oleoa-
canthohyphae, and thin-walled, irregular globular yellowish
cells. These structures are generally present, although in
variable density and either on ectomycorrhizal mantles and/
or rhizomorphs of all hitherto studied species (Agerer and
Iosifidou 2004; Christan and Hahn 2005). Although the order
Phallales, as defined by Agerer and Iosifidou (2004), under
79
inclusion of Clathraceae Cheval., Gelopellaceae Zeller,
Phallaceae Corda, and Protophallaceae L.S. Olive, shows
ampullate hyphae in their rhizomorphs, too, the characteristic
oleoacanthohyphae/oleoacanthocystidia are lacking. They
instead form spheres of radially aggregated crystals within
inflated hyphae or hyphal cells.
As ramarioid rhizomorphs are with few exceptions
(H. rufescens, Agerer et al. 1996b; Boletopsis leucomelaena,
Agerer 1992b; Hydnellum peckii, Agerer 1993c; Sarcodon
imbricatus, Agerer 1991b), restricted to a group that is called
superorder Gomphanae by Agerer and Iosifidou (2004),
rhizomorphs with ampullate hyphae can be regarded as a
synapomorphy of this group. Oleoacanthohyphae/oleoa-
canthocystidia are a synapomorphy of the order Gomphales,
spheres of radially aggregated crystals a synapomorphy of
the Phallales. Therefore, both orders are well defined. The
limited number of DNA studies, however, presently does not
show a distinct hiatus between the two groups (compare
Agerer and Iosifidou 2004) but rather indicates a mixture
between these two orders (Binder and Bresinsky 2002; Bruns
et al. 1998; Hibbett et al. 1997a; Hibbett and Thorn 2001;
Humpert et al. 2001; Moncalvo et al. 2002). Species of both
orders form together the so-called gomphoid–phalloid clade.
Hawksworth et al. (2001) did not accept Clavariadelphaceae
(included it in Gomphaceae), Gautieriaceae (included it in
Ramariaceae), and Sphaerobolaceae (included it in Geas-
traceae). They propose a non-monophyletic order Phallales
with the families Geastraceae, Gomphaceae, Hysterangia-
ceae, Phallaceae, and Ramariaceae.
The almost identical general structure of ECM and/or
rhizomorphs of Clavariadelphus, Gomphus, Gautieria,
Hysterangium, Kavinia, Phallogaster, Ramaria, Ramari-
cium (Hahn et al. 2000), and Sphaerobolus justifies an
inclusion of these genera within a single family Gompha-
ceae Donk that has priority against Ramariaceae Corner
(Hawksworth et al. 2001). Geastraceae are apparently
defined by an own synapomorphy, namely, the dextrinoid,
thick-walled, and thin peripheral rhizomorph hyphae. Some
Ramaria species have to be possibly included in this family,
too (Agerer and Iosifidou 2004).
The evolutionary success of ramarioid rhizomorphs is
possibly based on the function of the ampullate hyphal
inflations. As these trumpet-like structures are mostly below
a clamp or a septum of the hypha, they might play a role as a
temporary storage reservoir of nutrients and water. This
could make sense as the ECM form mats of hyphae and
rhizomorphs that densely envelop soil crumbs. They dry
them out almost completely. Water and nutrients could be
stored before they are needed for growth or/and transfer to
the host. The formation of crystal-like particles on the inner
surface of the inflated portions (Petersen 1989) suggests the
necessity of functional studies. The second relationship with
medium-distance mat exploration type ECM, the Bank-
eraceae, form occasionally ampullate inflations in their
rhizomorphs (see below). Although they are not so frequent
as in Gomphales, their presence in the same exploration type
supports a possible storage function of ampullate hyphae in
ECM that are extraordinarily efficient in water extraction.
The function of the oleoacanthocystidia/oleoacanthohyphae
and their associated globular cells is a matter of debate, too.
Both insect repellent function and storage function for
nitrogen should be considered. That such cells could contain
stored nitrogen has been shown for similar cells in a variety
of species not affiliated to Gomphales or Phallales (Agerer et
al. 1994; Franz and Acker 1995; Clémençon 2005).
Ultrastructural studies are necessary.
The genus Hydnum is another genus with ramarioid
rhizomorphs, but oleoacanthocystidia/ oleoacanthohyphae
and associated globular cells do not occur. There is therefore
no reason to conclude at a closer relationship to Gomphales.
As also spheres of radially aggregated crystals within
globular cells are lacking, a relationship to Phallales can be
excluded. The Hydnum clade, containing also the supposed
ectomycorrhizal genus Clavulina, is, according to Pine et al.
(1999), a sister clade to the gomphoid–phalloid clade. The
formation of ramarioid rhizomorphs could therefore be also
a synapomorphy of both groups.
d. Thelephoroid clade (Binder et al. 2005; Hibbett and
Thorn 2001; Larsson et al. 2004)
Pseudotomentella [1/9?(9)], Thelephoraceae: MTY B/C;
RH lacking; CY lacking; EHY clamps lacking, anasto-
moses open; CR septa of inner mantle layers and of
emanating hyphae and patches of walls partially amyloid;
ET short distance; HI; ECM brownish to bluish.
Pseudotomentella tristis (P. Karst.) M.J. Larsen: Agerer (1994a,b).
Thelephora [1/49(49)], Thelephoraceae: MTY D; RH
thelephoroid; hyphal ramification of the split type; CY
awl-shaped with a basal clamp, smooth; EHY with clamps,
anastomoses open; CR septa of inner mantle layers and of
emanating hyphae partially amyloid; ET medium distance,
smooth subtype; HI; ECM brownish.
T. terrestris Ehrh.: Agerer (1988a), Agerer and Weiss (1989, 1990), Ingleby
and Mason (1996), Ingleby et al. (1990), Mohan et al. (1993), Raidl (1997),
and Schramm (1966).
Remarks: Some non-identified ECM show similar struc-
tures as those of T. terrestris but differ slightly in some
minor features, like length of cystidia (Brand 1991a;
Fischer and Agerer 1996; Montecchio and Agerer 1997;
Wöllecke et al. 1999). They are possibly formed by
Thelephora species, but similar ECM can also be caused by
Tomentella (see below). Almost identical are ECM of
Gomphidius species (compare this genus below); minor
structural differences allow, however, a distinction of these
two genera.
Tomentella [8/75?(75)], Thelephoraceae: MTYA/B, K, L,
and P, with or without blue granules; RH lacking, uniform-
loose, or thelephoroid (with or without nodes); when
thelephoroid then hyphal ramification of the split type; CY
lacking, awl-shaped, or capitate; EHY clamps lacking or
present, anastomoses open; ET contact, short- or medium-
distance smooth subtype; CR blue granules in KOH
greenish; in some species, septa of inner mantle layers
and of emanating hyphae partially amyloid, and/or patches
of hyphal walls amyloid; HI; ECM brownish to dark
brown.
80Tomentella brunneorufaM.J. Larsen: Agerer and Bougher (2001a); Tomentella
ferruginea (Pers.) Pat.: Raidl (1997, 1998a), Raidl and Müller (1996);
Tomentella galzinii Bourdot: Jakucs et al. (1997, 1998a, sub nomine
Quercirhiza fibulocystidiata), Köljalg et al. (2001); Tomentella pilosa
(Burt) Bourdot & Galzin: Jakucs (2002a), Jakucs and Agerer (1999a),
Köljalg et al. (2001); Tomentella stuposa (Link) Stalpers: Jakucs et al. (2005);
Tomentella sublilacina (Ellis & Holw.) Wakef.: Agerer (1996f,g, sub nomine
Tomentella albomarginata (Bourdot & Galzin) M.P. Christ.); Tomentella
subtestacea Bourdot & Galzin: Jakucs (2002b), Jakucs and Agerer (2001),
Köljalg et al. (2001).
Remarks: Tomentella ECM can be defined by several
features that occur either together or replace one another.
Dark brown ECM with pseudoparenchymatous mantles
and clamps or with cystidia usually belong to Tomentella.
The same applies to dark brown ECM with pseudopar-
enchymatous mantles and blue granules, irrespective of the
presence of clamps or cystidia. Blue granules that turn
green in KOH or dark brown ECM without blue granules
that become slightly green in KOH contain thelephoric acid
(Agerer et al. 1995), the typical compound of the order
Thelephorales (Gill and Steglich 1987). Light brown ECM
that lack cystidia but feature amyloidy may also belong to
Tomentella. If, in addition, cystidia cover the mantle, the
ECM likely originate from the genera Thelephora (see
above) or Gomphidius (see below). Several dark brown
ECM have been characterized in detail that either fit the
features compiled above or are proven to represent a
Tomentella by DNA analysis, i.e., Azul et al. (1999), Azul
and Freitas (2006a–e), de Román et al. (2002), Golldack et
al. (1998a, 1999), Goodman (1996a), Ingleby et al. (1990),
Mleczko (2004b,c).
Tomentella ECM reveal a high diversity regarding mantle,
cystidia, and rhizomorph structures. Rhizomorphs that are
peripherally densely entwined by very thin, multi-branched
hyphae forming a kind of rind (Fig. 3d) are typical for T.
ferruginea, T. pilosa, and T. subtestacea. In addition, these
rhizomorphs form nodes at their ramifications. Such a
rhizomorph type is unknown from fruitbodies of T.
ferruginea, and fruitbody rhizomorphs could not be
found in T. subtestacea (Köljalg 1996). So-called fibulo-
cystidia (short cystidia with an intercalar clamp, Fig. 5c),
capitate in T. subtestacea and T. pilosa, characterize ECM
of T. subtestacea and T. pilosa (Jakucs 2002b; Jakucs and
Agerer 2001; Köljalg et al. 2001) a well as T. galzinii
(Jakucs et al. 1997, 1998a). Those of T. galzinii are below
the clamp considerably thick-walled. T. galzinii, T. pilosa,
and T. subtestacea belong to a group of light brown to
greenish ECM (Jakucs et al. 1998a; Jakucs 2002a,b),
whereas T. ferruginea forms dark brown ECM. In
consideration of these rhizomorph and cystidia types,
combined with mantle structures, it could be concluded that
T. pilosa and T. subtestacea form a natural group. Both
possess the same type of cystidia, rhizomorphs, and color.
T. galzinii differs in its uniform-loose rhizomorphs. All
three species form a pseudoparenchymatous mantle with
angular cells. T. ferruginea lacks cystidia and produces
rhizomorphs with a rind of densely entwined, multi-
branched hyphae, and a plectenchymatous mantle.
The DNA-based phylogenetic hypothesis by Köljalg et al.
(2001), however, places T. subtestacea and T. galzinii
in sister clades, whereas T. pilosa is placed aside.
T. subtestacea and T. galzinii clades plus T. viridula form
a well-supported (bootstrap 87%) monophylum, but the
position of T. pilosa receives no bootstrap support.
T. ferruginea stands – unsupported again – in the vicinity
of T. pilosa (Köljalg et al. 2001). Using a different set of
species, Köljalg et al. (2000) found evidence that T. galzinii
and T. pilosa belong to sister clades, which received no
bootstrap support, however. Although unsupported, T.
ferruginea seems to be the sister group of the T. pilosa
clade in the latter publication.
The evolution of two complexes of features, viz. mantle
and rhizomorph types, has not been marching lock-step.
The structure of mantles evolves from plectenchymatous to
pseudoparenchymatous and rhizomorphs from undifferen-
tiated to highly differentiated (Agerer 1995, 1999a).
Elaborate rhizomorphs are combined with a primitive
mantle type in T. ferruginea, a highly evolved mantle with
primitive uniform-loose rhizomorphs in T. galzinii. As the
presence of cystidia can also be regarded as an apomorphic
character, it is difficult to unravel natural relationships
within this group from a structural point of view. But DNA-
based phylogenetic hypotheses also cannot remove the
conflicts. If the formation of rhizomorphs with a rind of
densely entwined, multi-branched hyphae is regarded as
convergent, T. galzinii, T. pilosa, and T. subtestacea form a
natural group, which is the sister group of T. ferruginea.
This conclusion is supported by anatomy, i.e., the same
mantle type (pseudoparenchymatous with angular cells),
colors (greenish to brownish), and cystidia (fibulocystidia)
in the T. galzini group vs a plectenchymatous mantle, dark
brown color, and lacking cystidia in T. ferruginea. Further
studies using DNA sequences and ECM anatomy will
possibly result in a natural classification.
Three further groups can be discerned in Tomentella. One
entity is represented by T. stuposa and other species with
dark brown pseudoparenchymatous mantles furnished by
solitary or groups of cells on its surface (mantle type K)
and/or bottle-shaped cystidia (Agerer et al. 1995). A
second group is formed by species like T. sublilacina that
produce pseudoparenchymatous mantles with a surface net
(mantle type P), and a third one is consisting of species
with plectenchymatous mantles without cystidia, as
represented by T. brunneorufa. Considerably more species
have to be studied yet to confirm these groups and to define
synapomorphies.
Tomentellopsis [1/5(5)], Thelephoraceae: MTY A; RH
uniform-compact; CY lacking; EHY clamps lacking,
anastomoses open; CR violet with KOH; ET medium-
distance smooth subtype; HO; ECM reddish to brownish.
Tomentellopsis submollis (Svrček) Hjortstam: Agerer
(1998c), Brand (1991a, sub nomine Fagirhiza rosea),
Haug and Pritsch (1992, sub nomine Piceirhiza rosea),
Köljalg et al. (2002), Schweiger et al. (2002), Uhl (1988a,
sub nomine Pinirhiza rosea).
Thelephoraceae [4/6(12)]: This family is characterized by
a heterogeneous mantle type assemblage. There is an
81
apparent progression from plectenchymatous mantles, as
shown in Pseudotomentella, Thelephora, Tomentellopsis,
and in some species of the genus Tomentella, to
pseudoparenchymatous mantles as possibly developed in
the greater portion of Tomentella species. These mantles
can be easily connected structurally by a change of hyphal
shape from normal hyphae to hyphae with inflated and
shorter cells. Only Tomentellopsis stands aside with a
typical ring-like arrangement of the outer mantle hyphae, a
feature characteristic of Bankeraceae (see below).
Extraordinary and structurally similar to those of Bank-
eraceae (see below) are the rhizomorphs of T. submollis in
being uniform-compact and clampless. In their molecular
phylogeny of corticioid homobasidiomycetes, Larsson et
al. (2004) included Tomentellopsis echinospora (Ellis)
Hjortstam. Though this species forms the sister group,
unsupported at the 50% level, of a clade comprising all
studied Thelephoraceae (with exclusion of Amaurodon)
and Bankeraceae, which form sister subclades. Tomentel-
lopsis’ position does not contradict a possible relationship
with Bankeraceae. It rather supports the systematic value of
mantle and rhizomorph structure for the definition of
Bankeraceae under inclusion of Tomentellopsis.
Pseudotomentella forms a separate group in the studies of
Binderet al. (2005), and is the sister group of a Tomentella
clade in the publication of Larsson et al. (2004). The
available structural data of Pseudotomentella ECM are not
sufficient for a comparison with the DNA-based phyloge-
netic hypotheses. Thelephora terrestris and Tomentella
sublilacina form a well-supported clade (Köljalg et al.
2000), but the species sampling appears too small for
reliable conclusions. A relationship between these two
species is improbable from an ectomycorrhizal point of
view, as T. terrestris forms plectenchymatous mantles with
cystidia, whereas T. sublilacina has bluish black ECM and
a pseudoparenchymatous mantle and lacks cystidia.
Bankera [1/2(2)], Bankeraceae: MTY A, star-like; RH
uniform-compact; CY lacking; EHY clamps lacking,
anastomoses open; formation of chlamydospores; CR
lacking; ET medium-distance mat subtype; HO; ECM
whitish, greyish to black when old; ‘carbonizing’, i.e., old
portions of ECM become black and fragile and old mantle
portions and cortical cells with Hartig net break off like
charcoal pieces and uncover a thin thread of the root axis.
Bankera fuligineoalba (J.C. Schmidt) Coker & Beers ex Pouzar: Agerer and
Otto (1997, 1998).
Boletopsis [1/5(5)], Bankeraceae: MTY A(B)/C, indis-
tinctly ring-like; RH phlegmacioid, with some ampullate
hyphae; CY lacking; EHY with clamps, anastomoses
closed by a clamp; formation of chlamydospores; CR small
patches of emanating hyphae slightly amyloid; ET medi-
um-distance mat subtype; HO; ECM whitish, greyish to
black when old.
B. leucomelaena (Pers.) Fayod: Agerer (1992b, 1993d).
Hydnellum [2/38(38)], Bankeraceae: MTY A(B)/C, indis-
tinctly ring-like, with blue granules; RH uniform-compact,
with some ampullate hyphae; CY lacking; EHY clamps
lacking, anastomoses open; formation of chlamydospores;
CR lacking, or greenish in KOH (Hydnellum caeruleum);
ET medium-distance mat subtype; HO; ECM whitish,
greyish to black when old; ‘carbonizing’, i.e., old portions
of ECM become black and fragile and old mantle portions
and cortical cells with Hartig net break off like charcoal
pieces and uncover a thin thread of the root axis.
H. caeruleum (Hornem.) P. Karst.: Kernaghan (2001); H. peckii Banker:
Agerer (1993b,c).
Phellodon [1/16(16)], Bankeraceae: MTYA, star-like; RH
uniform-compact; CY lacking; EHY clamps lacking,
anastomoses open; formation of chlamydospores; CR
lacking; ET medium-distance mat subtype; HO; ECM
whitish, greyish to black when old; ‘carbonizing’, i.e., old
portions of ECM become black and fragile and old mantle
portions and cortical cells with Hartig net break off like
charcoal pieces and uncover a thin thread of the root axis.
P. niger (Fr.) P. Karst: Agerer (1992a, 1993a).
Sarcodon [1/36(36)], Bankeraceae: MTYA, ring-like; RH
phlegmacioid; CY lacking; EHY with clamps, anasto-
moses closed by a simple septum; formation of chlamy-
dospores; CR lacking; ET medium-distance mat subtype;
HO; ECM whitish, greyish to black when old.
S. imbricatus (L.) P. Karst.: Agerer (1991b,c), Raidl and Agerer (1992).
Bankeraceae [5/5(5)]: Bankeraceae ECM are characterized
by plectenchymatous mantles with ring-like, though
sometimes indistinctly, or star-like hyphal arrangement.
A common feature is the mat subtype of the medium-
distance exploration type and blackening ECM when
ageing, carbonizing in Bankera, Hydnellum, and Phello-
don. Rhizomorphs are uniform-compact and can enlarge
some hyphae resulting in a phlegmacioid type; ampullate
inflations occur occasionally. The existence of chlamydo-
spores is apparently a constant feature. But the ontogeny
and the final shape of the chlamydospores differ extremely.
Oidia-like chlamydospores are characteristic of B. leuco-
melaena, star-like chlamydospores with hollow warts
characterize Sarcodon (S. imbricatus and S. leucopus
(Pers.) Maas Geest. & Nannf., Agerer, unpublished), H.
peckii possesses chlamydospores with thick, radially
splitting walls or simple thick-walled ones (H. caerulescens),
and Phellodon forms chlamydospores with concentrically
and asymmetrically splitting walls (P. niger). Thick-walled,
brown, and large chlamydospores were also found in B.
leucomelaena, but the affiliation to this ECM was
questionable (Agerer 1992b). A few comprehensively
described, but still unidentified ECM, have also been
proven to produce chlamydospores (Golldack et al. 1998b;
Wöllecke et al. 1999).
The genera Phellodon, Bankera, Boletopsis, Sarcodon, and
Hydnellum form a separate subclade within the thelephor-
oid clade (Larsson et al. 2004). This corroborates on the
one hand the importance of the faintly tinted spores of
Bankeraceae (Maas Geesteranus 1975), in comparison to
those of Thelephoraceae, and on the other hand the
significance of ECM features for delimitation of the family
Bankeraceae, i.e., plectenchymatous mantles with ring- or
star-like pattern, the presence of chlamydospores, black-
ening ECM, and, last but not least, the same medium-
distance mat exploration type. All tested species engulf soil
particles very densely and dry out the soil almost
82
completely resulting in water-repellent crumbs, similar as
in Gomphales. A similarity to Gomphales regards also
occasionally ampullate hyphae of rhizomorphs (see
Gomphales). With respect to the ring-like pattern of the
mantle, uniform-compact rhizomorphs, lacking clamps,
and finally the only faintly tinted spores found in
Tomentellopsis submollis connect the genus Tomentellopsis
closely to the genera that are traditionally treated as
members of the family Bankeraceae (see above). The lack
of ECM darkening and its medium-distance smooth
exploration type indicate that Tomentellopsis might be the
most primitive member of Bankeraceae, which is also
expressed by its primitive, corticioid fruitbody type
compared to the pileate that are typical of the other
bankeraceous genera (Oberwinkler 1977).
Thelephorales: ECM of Thelephorales are very diverse. A
few but not consistently present features can be unfolded.
The mycorrhizae are frequently brown or brownish and
may possess blue granules that become greenish in KOH or
hyphae that can simply turn green in KOH, indicating the
presence of thelephoric acid, a Thelephorales-specific
pigment (Bresinsky and Rennschmid 1971; Gill and
Steglich 1987; Oberwinkler 1977). Amyloid hyphal walls
or septa occur in ECM of several species, a character only
reported from fruitbodies of Tomentella subamyloidea
Agerer (Agerer and Bougher 2001b).
The almost identical structure of Albatrellus and
Thelephora ECM inveigled the author into concluding
that there is a close relationship between Albatrellaceae and
Gomphidiaceae (see below). In particular, the occurrence
of hyphal amyloidy and the presence of thelephoric acid
justified this conclusion. Agerer et al. (1996a) therefore
transferred the family Albarellaceae (named as Scutiger-
aceae) to Thelephorales. Recent DNA studies, however,
indicated the affiliation of Albatrellaceae to the russuloid
clade. But the widely lacking or insufficient bootstrap
support (lower than 70%) in the backbone of the russuloid
clade (Binder et al. 2005; Larsson et al. 2004; Larsson and
Larsson 2003) makes this hypothesis not yet superfluous.
e. Russuloid clade (Binder et al. 2005; Hibbett and
Binder 2002; Hibbett and Thorn 2001; Larsson et al.
2004)
Polyporoletus [1/1(1)], Albatrellaceae: MTY D (B, at
places); RH phlegmacioid; CY awl-shaped, sharply acu-
minate; EHY with clamps, anastomoses open; CR all thick-
walled hyphae, cystidia included, distinctly amyloid; ET
medium-distance smooth subtype; HI; ECM yellowish
brown.
Polyporoletus sublividus Snell: Agerer and Ammirati (1998), Agerer et al.
(1998b).
Albatrellus [2/12(12)], Albatrellaceae: MTY D; RH
phlegmacioid; CY awl-shaped, distally forked; EHY
clamps lacking, anastomoses open or occasionally closed
by a simple septum; some hyphae with blue granules;