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First Bulgarian collections of Mattirolomyces terfezioides (Pezizaceae), a potentially valuable hypogeous fungus

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The paper discusses occurrence of Mattirolomyces terfezioides in Bulgaria, presenting the easternmost locality in Europe known so far. Description and illustrations of the first Bulgarian collections are included.
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303
PHYTOLOGIA BALCANICA 22 (3): 303 – 307, Sofia, 2016
First Bulgarian collections of Mattirolomyces terfezioides
(Pezizaceae), a potentially valuable hypogeous fungus
Boris Assyov1 & Monica Slavova2
1 Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences,
2 Gagarin Str., 1113 Sofia, Bulgaria, e-mail: contact@boletales.com (corresponding
author)
2 4 Krivolak Str., 1000 Sofia, Bulgaria, e-mail: el_modo@mail.bg
Received: August 10, 2016 ▷ Accepted: November 08, 2016
Abstract. The paper discusses occurrence of Mattirolomyces terfezioides in Bulgaria, presenting the easternmost locality
in Europe known so far. Description and illustrations of the first Bulgarian collections are included.
Key words: Bulgarian mycota, Pezizales, subterranean ascomycetes, Terfeziaceae, truffle-like fungi
Introduction
Truffles (i.e. the members of genus Tuber Micheli
ex F.H. Wigg.) are well-known and prized delica-
cy mushrooms which are extensively traded. Some
truffle-like species of other genera are also subject
of commercial interest, notably members of the gen-
era Terfezia (Tul. & C.Tul.) Tul. & C.Tul. and Tirma-
nia Chatin. Another related genus, Mattirolomyces
E. Fisch., and its only European species, M. terfez-
ioides (Mattir.) E. Fisch., have received little atten-
tion so far, irrespective of some peculiar properties,
not found in other hypogeous fungi (Gógán Csorb-
ainé 2009). In 2015, the authors received from cor-
respondents two specimens of hypogeous fungus,
which turned out to be the first Bulgarian collections
of M. terfezioides. Those findings are presented and
discussed herein.
Materials and methods
One of the specimens was received in fresh state
shortly after collecting. Ascomata were photographed
ex situ and important macroscopic and organoleptic
characters were noted down. The second collection
was presented to us in dried state, supplied with pho-
tographs taken in situ and ex situ. Microscopic exam-
ination was held on fresh and dried materials with the
aid of Amscope T360B light micro scope, equipped
with Amscope MU900 digital camera. Microscopic
slides were mostly prepared in tap water, but Congo
red in ammonia, aqueous Floxine and aqueous cot-
ton blue were also used arbitrarily to visualize better
some of the micro scopic structures. Amiloidity was
tested with Melzer’s reagent and IKI. Measurements
were taken on pre-calibrated digital photographs
with Piximetre ver. 5.9. Ascospore measurements re-
ported below refer to 50 spores, measured without
the ornamentation on slides in water. In the quota-
tion of ascospore size, the figures in parenthesis rep-
resent the average value and the respective standard
deviation, while the minimum and maximum values
are not included in parenthesis. For the remaining
microscopic structures only the minimum and maxi-
mum values are recorded; the figures are based on
20 measurements for asci and 15 for cells of peridi-
um and gleba.
304 Assyov, B. & Slavova, M. • Mattirolomyces terfezioides in Bulgaria
Description of species
Mattirolomyces terfezioides (Mattir.) E. Fisch., in
Engler & Harms, Nat. Pflanzenfam., Edn 2, 5bVIII:
39 (1938); Choiromyces terfezioides Mattir., Mém.
R. Accad. Sci. Torino, Ser. 2, 38: 384 (1888); Terfezia
terfezioides (Mattir.) Trappe, Trans. Brit. Mycol. Soc.
57(1): 91 (1971). (Fig. 1a-i)
Ascomata hypogeous, later semihypogeous, tu-
beriform, irregularly wrinkled to lobate, up to 11 cm
across. Peridium smooth or with pubescent appear-
ance, occasionally disappearing in places, initially
white, subsequently darkening to somewhat yellow-
ish- ochraceous or ochraceous, changing to yellow
when bruised. Gleba initially compact and brittle, with
age becoming softer, at first whitish, then cream to
pale-ochraceous, with numerous whitish sterile veins,
branching and anastomosing and separating differ-
ent in size fertile areas. Odour agreeable or somewhat
spermatic in young and mature specimens, unpleas-
ant in overmature ascomata. Taste characteristic, very
sweet, reminding of sweeteners. Asci ovoid to ovoid
elongate, pedicellate, 122.5–199.5 × 45.5–71.9 μm,
mostly with irregularly disposed ascospores, seldom
loosely biseriate, 8-spored, inamyloid. Ascospores
globose, 14.8–(16.6±1.0)–18.6 μm across, hyaline,
with up to 0.6 μm high, in places incomplete, areolate-
reticulate ornamentation; meshes regular, polygonal,
up to 6 across the spore diameter, at the corners with
projecting aculei up to 1.8 μm high. Peridium com-
posed of loosely connected inflated elements, 17–69.1
× 18.7–74.9 μm. Gleba composed of randomly dis-
posed asci and chains of variable in shape inflated cells
up to 146.5 × 40.9 μm, tissues of the veins more or less
similar to those of the fertile areas.
Specimens examined. Bulgaria: in the vicinity
of Karantsi village, close to Robinia pseudoacacia L.,
13.11.2015, D. Dimitrov (SOMF 28802); in the vicin-
ity of Svishtov town, 16.11.2015, C. Geneva (SOMF
28803); idem, 20.12.2015, C. Geneva (obs.).
Discussion
The studied specimens in their macromorphology
and microscopic features agree perfectly with the con-
temporary descriptions of M. terfezioides (Astier 1998;
Montecchi & Sarasini 2000; Gori 2005). Konstantinid-
is & Kaounas (2014) describing their collection of the
species have found a slightly different size range of the
ascospores. Nevertheless, the values from our materi-
al fall within this range. Gori (2005) also cited a wid-
er range, but his measurements apparently include the
spore ornamentation.
The species was originally described by Mattirolo
(1888) as Choiromyces terfezioides and provided with
ample description and detailed illustration. Fischer
(1938) erected a new genus, Mattirolomyces. Later on,
Trappe (1971) proposed placement in the genus Ter-
fezia, but retained Mattirolomyces at subgeneric lev-
el. Further molecular research did not confirm the ac-
commodation of the fungus in this genus, but rather
supported the resurrection of Mattirolomyces (Per-
cudani & al. 1999; Díez & al. 2002). The genus Mat-
tirolomyces includes four more species, all extra-Eu-
ropean. Mattirolomyces spinosus (Harkn.) Kovacs,
Trappe & Alsheikh and M. mexicanus Kovacs, Trappe
& Alsheikh are established as distinct by ITS and LSU
phylogenetic analysis. They are described and dis-
cussed in detail in Kovács & al. (2011b). Both spe-
cies share a lot of similarities and are difficult to dis-
tinguish from M. terfezioides, although M. spinosus is
said to have indistinctive flavour (Kovács & al. 2011b).
Mattirolomyces mulpu Kovacs, Trappe & Claridge is
described in Trappe & al. (2010a) and M. austroafri-
canus (Trappe & Marasas) Kovacs, Trappe & Claridge
is presented in Trappe & al. (2010a, b). Those two spe-
cies have larger spores (exceeding 19 μm) with high-
er ornamentation.
Mattirolomyces terfezioides is well-distinguished
from the related hypogeous fungi of the genera Ter-
fezia and Tirmania by a combination of characters,
including morphology of ascomata, peridium of in-
flate elements, inamyloid asci and ornamentation of
the ascospores. The species of Tirmania have amy-
loid asci and smooth ascospores and thus are sep-
arated easily from Mattirolomyces (Díez & al. 2002).
The genus Terfezia includes species with non-amy-
loid asci and variable ornamentation: spinose or re-
ticulate. The members of this genus, however, feature
variable in structure, but compact peridium, different
from the peridium of M. terfezioides, which is com-
posed of loosely connected elements and therefore is
often fleeting. Healy & Kovács (2010) provided ultra-
structural evidence for the distinction of Mattirolo-
myces from Terfezia, namely heterogeneously staining
spines of the spore wall and hexagonal Woronin bod-
ies. Several species of Terfezia possess reticulate or-
namentation. In Europe and adjacent areas, these are
305Phytol. Balcan. 22(3) • Sofia • 2016
T. alsheikhii Kovács, M.P. Martín & Calonge (reticu-
late ascospores), T. boudieri Chatin (warty-reticulate),
T. canariens Bordallo & Ant. Rodr. (reticulate), and T.
claveryi Chatin (reticulate). All four species have ei-
ther pseudoparenchymatic or hyphal peridium (Ko-
vács & al. 2011a, Bordallo & al. 2012). From ecologi-
cal point of view, the species of this genus are known
to form mycorrhizae with representatives of the plant
family Cistaceae Juss. On the other hand, Mattirolo-
myces terfezioides has been documented to enter in-
to relationship with a broader spectrum of vascular
plants (see comments below).
The distribution of M. terfezioides is apparently yet
to be clarified, judging from the Bulgarian findings,
which expand further its known geographic range and
appear to be its easternmost part so far known. So far
it seems that the fungus is most common in Hunga-
ry (Szemere 1970; Ławrynowicz 1990; Király & Bratek
1992), where it is collected for alimentary purposes.
Scattered records exist also from France (Ławrynowicz
1990; Ławrynowicz & al. 1997), Italy (Montecchi &
Sarasini 2000; Bizio 2002), Slovakia (Glejdura & Kun-
ca 2012), and Spain (Kovács & al. 2009). In the Balkan
countries, previous records are known only from Ser-
bia (Ławrynowicz & al. 1997) and Greece (Konstan-
tinidis & Kaounas 2014), in both countries rather lo-
calized. Data for the occurrence of the species outside
Europe is included in a single report from India (Khare
1975) and another one from China (Zhang 1992). In
relation to the collection of Khare (1975), the discov-
ery of the very similar M. spinosus in Pakistan should
be noted (Kovács & al. 2011b). Mention deserves the
fact that the ascospores of the Indian collection were
reported to be larger, 18.5–24 μm. Extra-European re-
cords of M. terfezioides are of special interest, as it is
yet unclear whether it is a native species in Europe,
Fig. 1. Macromorphological and microscopic features: a-c – ascomata ex situ; d – cross section of peridium; e – gleba (sterile veins);
f – randomly disposed asci with ascospores; g-i – asci with ascospores, with emphasis on spore ornamentation (a – aqueous oxine,
g – aqueous cotton blue, e,f,h,i – tap water). Scale bars = 50 μm (d-f) & 20 μm (g-i).
a
d
g
b
e
h
c
f
i
306 Assyov, B. & Slavova, M. • Mattirolomyces terfezioides in Bulgaria
a question raised by its common putative association
with some non-native trees. Various host plants were
reported in Europe, including representatives of the
genera Ficus L., Robinia L., Prunus L., and Asparagus
L. (Astier 1998; Montecchi & Sarasini 2000). Studies
by Kovács & al. (2003, 2007) have found evidence for
the relation of M. terfezioides with both woody and
herbaceous plants, namely Celtis occidentalis L., Cra-
taegus monogyna Jacq., Helianthemum ovatum (Viv.)
Dunal, Ligustrum vulgare L., Muscari racemosum (L.)
Mill., Robinia pseudoacacia, Salvia glutinosa L., and
Viola cyanea Čelak.
Mattirolomyces terfezioides presents certain inter-
est for practical purposes as it has peculiar flavour and
taste, being the only European hypogeous ascomycete
with strong sweet taste, very similar to that of sweet-
eners. Although not very popular, which is probably
due to the fact that it is not found in most European
countries, it has interesting potential applications. In
Hungary, where it seems more common, it is collect-
ed and used for preparation of various deserts (Gógán
Csorbainè 2009). Due to this, it has been considered as
a species with potential in truffle gastronomy (Bratek
& al. 2013). The authors are not aware if the fungus is
collected for practical purposes in Bulgaria.
Another important peculiarity of M. terfezioides
is that it associates with the roots of different plants,
but very often with R. pseudoacacia. The associa-
tion might be achieved also under laboratory condi-
tions (Bratek & al. 1996; Kovács & al. 2002, 2003), a
fact which could encourage further attempts for cul-
tivation. Robinia pseudoacacia is a non-native tree,
which is extensively planted in various parts of Bul-
garia and has become one of the most important in-
vasive species in this country (Petrova & al. 2012). A
recent account shows that plantations of this species
cover approxi mately 150 000 ha in Bulgaria (Dimitro-
va 2012). Although there is no published evidence so
far, our field experience has shown that Robinia stands
in this country are generally poor in terms of edible
fungi. The presence of species of potential commercial
importance could thus elevate the value of such arti-
ficial plantations. So far the authors have been aware
of the existence of two localities of M. terfezioides in
Bulgaria, although it could be much more widespread.
Further research should reveal the actual extent of its
occurrence and provide precise characterization of its
habitats.
Acknowledgements. The authors extend their thanks to Mrs
C. Geneva and Mr D. Dimitrov for presenting the specimens cit-
ed in this paper. Thanks are also due to the anonymous review-
er for his helpful comments. Mr Carlo Agnello is thanked for pro-
viding the missing literature. The work of the first author is within
the framework of the project “Taxonomy, conservation and sus-
tainable use of fungi”.
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... (Pezizales, Pezizaceae). This mushroom has a prevalently European distribution (Gógán Csorbainé et al. 2009;Kovács et al. 2009;Assyov and Slavova 2016), but has been reported also from India, South Korea, and China, where the conspecificity of specimens from the northern part of the country with European samples has been demonstrated (Wang et al. 2017). M. terfezioides is described to possess a peculiar sweet flavour and a distinctive taste, and is considered a truffle with significant potential as gastronomic delicacy (Gógán Csorbainé et al. 2009;Assyov and Slavova 2016). ...
... This mushroom has a prevalently European distribution (Gógán Csorbainé et al. 2009;Kovács et al. 2009;Assyov and Slavova 2016), but has been reported also from India, South Korea, and China, where the conspecificity of specimens from the northern part of the country with European samples has been demonstrated (Wang et al. 2017). M. terfezioides is described to possess a peculiar sweet flavour and a distinctive taste, and is considered a truffle with significant potential as gastronomic delicacy (Gógán Csorbainé et al. 2009;Assyov and Slavova 2016). The other species of interest is Choiromyces cerebriformis (Pezizales, Tuberaceae), a new taxon that was described from Yunnan Province, linked to Pinus yunnanensis (Yuan et al. 2021). ...
... .., or spirituous to aromatic that turns unpleasant after drying (Moreno et al. 2012). On the other hand, the flavour of Mattirolomyces is described as "agreeable or somewhat spermatic in young and mature specimens, unpleasant in overmature ascomata," (Assyov and Slavova 2016). No specific data on the spore dispersion of either Mattirolomyces or Choiromyces exist, but on the basis of what we knew about the ecology of other hypogeous Ascomycota, it can be speculated that also in the case of these desert truffles the spores are either released passively into the soil from disintegrated asci (or, if the sporocarp emerges, spores can be dispersed with the help of wind and water) or are dispersed through animal mycophagy, mainly by mammals but also birds and arthropods (Trappe and Claridge 2005;Bradai et al. 2014). ...
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The septal pore ultrastructure of non-ascogenous and reproductive hyphae, as well as development of the spore wall were examined in the truffle Mattirolomyces terfezioides (Mattir.) E.Fisch. (Ascomycota, Pezizales, Pezizaceae) and compared with other pezizalean taxa. The septal pore in ascogenous hyphae of M.terfezioides is a uni- or bi-convex band of the type found in the Pezizaceae. Septal pore ultrastructure in other hyphae included a uniconvex band with lamellate structure. Woronin bodies were globose to hexagonal, and infrequently ellipsoid in shape. Hexagonal Woronin bodies have not been previously reported in the Pezizaceae. Ascospore delimitation starts with two delimiting membranes and the spore-wall development is typical of the Pezizales. The heterogeneously staining spines of the secondary cell wall differ from the structures of Terfezia species. The ultrastructural characteristics of M.terfezioides show the general characteristics of the Pezizaceae, except that the hexagonal Woronin body form is new to this family. The spore delimitation, spine-cap structure, and Woronin body shape of M.terfezioides presented here are in agreement with molecular taxonomic results, which separate the genus from Terfezia and call into question the generic position of Mattirolomycestiffanyae Healy.
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