Hydnotrya tulasnei and Mattirolomyces terfezioides () two hypogeous fungi that rarely appear in Greece

George KONSTANTINIDIS Summary: Two hypogeous Ascomycetes recently observed in Greece are presented: tulasnei and Vasileios KAOUNAS Mattirolomyces terfezioides. Descriptions based on specimens found are given, accompanied by macrosco- pic and microscopic images. Keywords: hypogeous fungi, , Hydnotrya, Mattirolomyces, , Greece.

Ascomycete.org, 6 (1) : 1-4. Σύνοψη: Παρουσιάζονται δύο υπόγειοι Ασκομύκητες που παρατηρήθηκαν πρόσφατα στην Ελλάδα: Hyd- Mars 2014 notrya tulasnei και Mattirolomyces terfezioides. Δίνονται περιγραφές που βασίστηκαν σε ευρεθέντα δείγματα, Mise en ligne le 15/03/2014 συνοδευόμενες από απεικονίσεις μακροσκοπικών και μικροσκοπικών χαρακτηριστικών.

Introduction ORIGINAL DESCRIPTION hypogaeus aut penitus hypogaeus, arrhizus, varius, globosus vel glo- boso-mammosus, tegumento levi, continuo, tenui praeditus. Aetate colore va- An intensive investigation of hypogeous fungi has been in riat, initio amoene ochraceo-rubiginosus dein ochraceus cinerascens. progress in Greece since 2007, and there have been quite a few dis- Caro lardacea aquoso-carnosa, initio pallidula albido-rosea, dein pallidula coveries so far. Some of the items found seem to be fairly rare in our ochraceo-rubiginosa; venis aeriferis albidis numerosis se anastomosantibus va- country, as demonstrated by the results of six years of research. This riegata. has led to the publication of several papers (DIAMANDIS & PERLEROU, Exsiccatione summopere contrahitur. 2008; KONSTANTINIDIS, 2009; AGNELLO & KAOUNAS, 2010, 2011; KONSTANTI- Asci ovato-oblongi, non rare leviter incurvati, brevi pedunculo elongati, oc- NIDIS & KAOUNAS, 2012) and, in some cases, the Greek collections tospori. Long. 123, Lat. 55 microm. helped to clarify certain important taxonomical issues (ALVARADO et Sporae sphaericae, maturae leviter luteolae, poene areolatae areolis ple- rumque exagonatis. Diam. 18 microm. al., 2011; KAOUNAS et al., 2011; ALVARADO et al., 2012). It seems that the Fungi, Solani aut Helianthi Tubera plane referentes. species here presented are rare in our country because DIAMANDIS & Immaturi vix odorantes, maturi odore graveolente ingratissimo notati. PERLEROU (2008) have only reported one collection of Mattirolomyces Immaturi forsan a nonnullis esculenti judicari possunt; maturi tamen, ob terfezioides (Mattir.) E. Fisch. eorum nauseantem ingratissimum odorem comedi posse haud credam. Hab. In Arvis prope Testona (Moncalieri-Piemonte) hieme et ineunte vere non Materials and methods infrequens.

Macroscopic characters are described from fresh specimens. For DESCRIPTION microscopic study, a Nikon Eclipse E100 trinocular microscope with Ascomata hypogeous or semi-hypogeous, small, moderate to plan achromatic objectives (4×, 10×, 40× and 100× in immersion oil) large, bulbous, irregular, with protuberances and grooves, whitish, was used. Microscopic characters were observed clay-coloured, grayish, reddish to brown-blackish, smooth or rough, from sections mounted in water for pigments and measurements; Melzer’s reagent, cotton blue, cre- syl blue and KOH were used to highlight orna- mentation; Congo red was used to highlight the walls of elements. Spore dimensions are based on at least 30 randomly selected spores, excluding ornamentation. Incidentally, Mattirolomyces spec- imens were discovered without the aid of hounds, while Hydnotrya specimens were discovered with the aid of hounds. Taxonomy

Mattirolomyces terfezioides (Mattir.) E. Fisch., Nat. Pflanzenfam., ed. ,2 5b VIII: 39 (1938).

BASIONYM Choiromyces terfezioides Mattir., Mem. R. Accad. Sci. Torino, Ser. 2, 38: 384 (1888). SYNONYM ≡ Terfezia terfezioides (Mattir.) Trappe, Trans. Br. mycol. Soc., 57(1): 91 (1971). Fig. 1 — Mattirolomyces terfezioides. Collection 2013 from Attica, Greece. Photo: G. Konstantinidis. 1 vated or uncultivated soils, in sandy and alkaline soils under trees such as Fagus sp., Prunus sp., Citrus sp., Pistacia sp. and Robinia pseudoacacia.

STUDIED COLLECTION Attica, under Pistacia sp. in barren land field, 2.I.2013, leg. A. Pou- los, det. G. Konstantinidis, conserved in personal herbarium GK 6465.

COMMENTS The species was originally described as Choiromyces terfezioides by MATTIROLO (1888), then transferred into the genus Mattirolomyces Fig. 2 — Mattirolomyces terfezioides. Photos: G. Konstantinidis. (FISCHER, 1938) and finally to ERFEZIAT (Trappe, 1971). However, mo- A. Ascospores in cresyl blue. B. Ascospores in cresyl blue and KOH. lecular works of PERCUDANI et al. (1999) and DÍEZ et al. (2002) showed the relationship between M. terfezioides and the other species within frequently with cracks, diam. (1–) 3–10 (–20) cm, mostly without a the genus Mattirolomyces E. Fisch. DÍEZ et al. (2002) observed differ- sterile base. Peridium very thin, with thick-walled, diaphragmatic ent habitats for this species and demonstrated that species of the filamentous hyphae (5.6 to 7 μm diam.), fleshy, first whitish, then genus Terfezia show a preference for plants of the family Cistaceae, pale rusty to ochre-greenish. Gleba fleshy, soft, whitish at first then particularly Helianthemum, while M. terfezioides seems to be related ochre-brownish or rusty with whitish, wide, sterile veins; taste very to plants such as Robinia pseudoacacia and Ribes rubrum. Different sweet and smell pleasant. habitats — Ficus spp. and Prunus spp. — are reported by ASTIER Spores globose, yellowish, sometimes biseriate, with large, fairly (1998), MONTECCHI & SARASINI (2000). The soils where M. terfezioides regular, polygonal meshes, (13.8–) 14.2–17.3 (–19.9) μm. Asci appears can be described as slightly alkaline or neutral, with thick ovoid~clavate, 69–124 × 48–57 μm, with a small stem, 8-spored, humus1, and variable phosphorus and medium to high potassium non-amyloid. content. The species can also occur in artificial plantations of Robinia Habitat: Ascomata grow hypogeously or semi-hypogeously, from pseudoacacia (BRATEK et al., 2007). Due to its strong fragrance and its August to January, inland on the mainland of the country, in culti- deliciousness, M. terfezioides has great gastronomic value. It is culti-

Fig. 3 — Mattirolomyces terfezioides. Photos: G. Konstantinidis. A-B. Immature asci and ascospores. C-D. Mature ascospores.

1 FILIPPA (comm. pers.) reported to us that he collected this species in Italy, Piedmont (same region of the type-collection) under Robinia and Ficus, in both cases without humus on the ground. 2 vated in Hungary, but it only grows wild in the Carpathian basin (GOGAN et al., 2006).

Hydnotrya tulasnei (Berk.) Berk. & Broome, Ann. Mag. nat. Hist., 18: 78 (1846).

BASIONYM Hydnobolites tulasnei Berk., Ann. Mag. nat. Hist., 13: 357 (1844). SYNONYMS ≡ Rhizopogon tulasnei (Berk.) Corda, Icon. fung., 6: 61 (1854). = Hydnotrya carnea (Corda) Zobel, in Corda, Icon. fung., 6: 61 (1854); Rhizopogon carneus Corda, Icon. fung., 6: 61 (1854), non Octa- viania carnea (Wallr.) Corda, Icon. fung., 6: 36 (1854) [= Hydnangium carneum Wallr.] = Hydnotrya jurana Quél., Enchir. Fung.: 262 (1886). = Hydnotrya tulasnei f. intermedia Bucholtz, Bull. Soc. Imp. Nat. Moscou, 4: 337 (1905). Fig. 4 — Hydnotrya tulasnei. Collection 2009 from Drosopigi Florina, Greece. Photo: G. Konstantinidis. ORIGINAL DESCRIPTION Depresso-globosa, basi plicata cribroso-porosa, rufa ve- lutina; cellulis magnis, parietibus albis pubescentibus; trama rufa; ascis longis; sporidiis globosis, demum lateritiis reticulatis, non echinulatis.

DESCRIPTION Ascomata compact, irregularly spherical or lobed, sometimes with inward folds, ochre-reddish to brick red, 2–3 cm diam. Perid- ium generally continuous, but sometimes with slits through which the gleba can be seen, slightly pruinose. Gleba initially cream- brown, later yellow-brown, with labyrinthic chambers covered with a whitish hymenium. Spores globose, 20–30 (–33) μm diam., initially smooth and hya- line, in maturity ochre-reddish, irregular with almost hemispherical variable protrusions, 3.5–7 μm in height, mono- or biseriate or ran- domly arranged. Asci clavate or saccate, 140–250 × 30–85 μm, with a short stem, 8-spored, non-amyloid. Paraphyses slightly longer than the asci, hyaline, cylindrical and slightly widened at the top, septate. Habitat: hypogeous or semi-hypogeous, occurs from April to Oc- tober, at altitudes up to 1,600 m, in both broadleaved and conifer- ous forests.

STUDIED COLLECTIONS Drosopigi Florina, under Fagus sp., 27.IX.2009, leg. D. Kleisiari, det. G. Konstantinidis, conserved in personal herbarium GK 4128.

COMMENTS Fig. 5 — Hydnotrya tulasnei. Photos: G. Konstantinidis. The genus Hydnotrya has been reported with the orthographic Details of ascospores, × 1000. variant Hydnotria by many authors (TULASNE & TULASNE, 1851; CORDA, 1854; HESSE, 1894; SOEHNER, 1959). Recently a neglected species, H. bailii Soehner, has been revalu- here. Thanks to Aggelos Papadimitriou (Xanthi, Greece) for editing ated after a phylogenetic study (STIELOW et al., 2010). H. bailii looks and Nicolas Van Vooren (Lyon, France) for publishing this paper, and like H. tulasnei macroscopically and microscopically, differing mor- also to Carlo Agnello (Mesagne, Italy) and Boris Assyov (Sofia, Bul- phologically by smaller and more rounded ascomata with strictly gary) for their decisive instructions and advice. monoseriate ascospores, besides its shows a preference for conifer- ous trees and has a distribution in more northern countries, in con- trast with H. tulasnei, which is associated with Fagus sylvatica, Pinus References spp. and Corylus avellana. AGNELLO C. & KAOUNAS V. 2010. — Ruhlandiella berolinensis, Genabea Acknowledgements cerebriformis, Helvella astieri: tre rarissime specie raccolte in Grecia. Micologia e Vegetazione Mediterranea, 25: 129-140. The authors are indebted to Despoina Kleisiari (Grevena, Greece) AGNELLO C. & KAOUNAS V. 2011. — Tuber asa and T. gennadii. A close and Andreas Poulos (Athens, Greece) for the collections presented morphological study of two species often confused in the past 3 FISCHER E. 1897. — Ascomyceten: Tuberaceen und Hemiasceen. Kryptogamen-Flora von Deutschland, Oesterreich und der Schweiz. I. Pilze, V. Leipzig, Kummer. FISCHER E. 1938. — Klasse Ascomycetes, Reihe Euas- cales. Unterreihe VIII. Tuberineae. In: ENGLER A. et al. (eds.). Die natürlichen Pflanzenfamilien V. Leipzig, Wilhelm Engelmann. GÓGÁN A., BRATEK Z., DIMÉNY J. & BUJÁKI G. 2006. — Truffle in Hungary – past, present and future.In : Biodiversity of hypogeous fungi 1: 31-35. HAWKER L. 1954. — British hypogeous fungi. Philo- sophical Transactions of the Royal Society of London, 237: 429-546. HESSE R. 1894. — Die Hypogaeen Deutschlands. Vol. 2: Die Tuberaceen und Elaphomyceten. Halle, L. Hofstetter, 140 p. + pl. XII-XXII. KAOUNAS V., ASSYOV B. & ALVARADO P. 2011. — New data on hypogeous fungi from Greece with special reference to Wakefieldia macrospora (Hymenogas- Fig. 6 — Hydnotrya tulasnei. Photos: G. Konstantinidis. traceae, Agaricales) and Geopora clausa (Pyrone- A, C, D. Ascospores. B. Asci and ascospores. mataceae, Pezizales). Mycologia Balcanica, 8: 105-113. KONSTANTINIDIS G. 2009. — Mushrooms, a photo- with a brief historical bibliographic summary. Ascomycete.org, 3 graphic guide for collectors. Athens, by the author, 526 p. (in Greek). (4) : 65-74. KONSTANTINIDIS G. & KAOUNAS V. 2012. — Elaphomyces muricatus and ALVARADO P., MORENO G., MANJON J.L., GELPI C., KAOUNAS V., KONSTANTINIDIS Fischerula macrospora, two interesting hypogeous fungi from G., BARSEGHYAM G. & VENTURELLA G. 2011. — First molecular data on Greece. Ascomycete.org, 4 (5): 95-98. Delastria rosea, Fischerula macrospora and Hydnocystis piligera. Bo- MATTIROLO O. 1888. — Illustrazione di tre nuove specie di Tuberacee letin de la Sociedad Micologica de Madrid, 35: 31-37. Italiane. Memorie della reale Accademia delle scienze di Torino, ser. ALVARADO P., MORENO G. & MANJÓN J.L. 2012. — Comparison be- 2, 38 : 377-393. tween Tuber gennadii and T. oligospermum lineages reveals the MONTECCHI A. & SARASINI M. 2000. — Funghi ipogei d’Europa. Trento, existence of the new species T. cistophilum (Tuberaceae, Pezizales). AMB, Fondazione Centro Studi Micologici, 714 p. PERCUDANI R., TREVISI A., ZAMBONELLI A. & OTTONELLO S. 1999. — Molecu- Mycologia, 104 (4): 894-910. lar phylogeny of trufflesPezizales ( : Terfeziaceae, Tuberaceae) de- ASTIER J. 1998. — Truffes blanches et noires (Tuberaceae et Terfezi- rived from nuclear rDNA sequence analysis. Molecular aceae). Gap, Louis-Jean, 127 p. Phylogenetics and Evolution, 13: 169-180. BERKELEY M.J. 1844. — Notices of British Fungi [257-322]. The Annals SOEHNER E. 1959. — Tuberaceen–Studien V. Mitteilungen der Botanis- and Magazine of natural History, 13: 340-360. chen Staatssammlung München, III: 13-33. BRATEK Z., GÓGÁN A., HALÁSK K. & DIMÉNY J. 2007. — Habitat preferences STIELOW B., BUBNER B., HENSEL G., MÜNZENBERGER B., HOFFMANN P., KLENK H- of Terfezia terfezioides in Hungary. In: KABAR L. (ed.). Actes du Pre- P. & G ÖKER M. 2010. — The neglected hypogeous fungus Hyd- mier symposium sur les Champignons hypogés du Bassin méditer- notrya bailii Soehner (1959) is a widespread sister taxon of ranéen. Rabat, Maroc, 5-8 avril 2004: 256-264. Hydnotrya tulasnei (Berk.) Berk. & Broome (1846). Mycological Progress, 9 (2): 195-203. CORDA A.C.J. 1854. — Icones fungorum. Vol. 6. Prague, F. Ehrlich, xix p. TRAPPE J.M. 1971. — A synopsis of the Carbomycetaceae and Terfezi- + 91 p. + pl. I-XX. aceae (Tuberales). Transactions of the British Mycological Society, DIAMANDIS S. & PERLEROU C. 2008. — Recent records of hypogeous 57: 85-92. fungi in Greece. Acta Mycologica, 43: 139-142. 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George Konstantinidis Vasileios Kaounas Agiou Kosma 25, ΤΚ 51100, Sokratous 40, TK 19016, Grevena Artemis Attiki Greece Greece [email protected] [email protected]

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