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New Records and Data on Hypogeous Ectomycorrhizal Fungi in Bulgaria

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New Records and Data on Hypogeous Ectomycorrhizal Fungi in Bulgaria FORESTRY IDEAS, 2016, vol. 22, No 2 (52): 113-126 NEW RECORDS AND DATA ON HYPOGEOUS ECTOMYCORRHIZAL FUNGI IN BULGARIA Teodor Nedelin1*, Melania Gyosheva2, Kaloyan Kostov3, and Slavcho Savev1 1Department of Silviculture, Faculty of Forestry, University of Forestry, 10 St. Kliment Ohridski Blvd., 1797 Sofia, Bulgaria. *E-mail: [email protected] 2Department of Plant and Fungal Diversity and Resources, Institute of Biodiversity and Ecosystem Research, BAS, 23 Acad. G. Bonchev Str., 1113 Sofia, Bulgaria 3AgroBioInstitute, Agricultural Academy, 8 Dragan Tsankov Blvd., 1164 Sofia, Bulgaria Received: 05 June 2016 Accepted: 26 July 2016 Abstract In this article, new data on species diversity of hypogeous macrofungi in Bulgaria are re- ported. Three species: Tuber rufum, Gautieria graveolens and Lactarius stephensii were recorded for first time in the country. New localities of noteworthy fungi Tuber excavatum and Gautieria morchelliformis are also reported. A DNA sequencing for most studied hypogeous fungi and de- tailed phylogenetic analysis for T. excavatum were performed. Results confirmed that representa- tives of T. excavatum group have a very high intraspecific genetic variability. Key words: ascomycetes, basidiomycetes, Bulgaria, fungal conservation, hypogeous fungi, phylogenetic analysis. Introduction ten reported in present studies as one of the main components of ectomycorrhizal Almost all of hypogeous macrofungi (as- associations in various forest ecosystems comycetes and basidiomycetes) are ec- under particular ecological conditions (Be- tomycorrhizal species, living in symbiotic nucci et al. 2011). Truffles generally grow relationship with roots of trees. Because in calcareous soils, but some of them are of their cryptic, subterranean fruit bodies, well adapted to slightly acidic soils (Jail- they are often overlooked and neglected lard et al. 2014, Pacioni and Comandini in different studies until now, when a rap- 1999). Most of them have a relatively idly development of molecular tools takes wide plant partners range and also grow- main part of scientific research. The de- ing conditions and only a few number is sign and construction of specific prim- restricted to particular ones. ers can be used as an easier and more The Balkan Peninsula and the western sensitive tool for the identification of truf- parts is still insufficiently explored regard- fle species in any stage of their life cycle, ing hypogeous fungi, including ’true‘ truf- including the mycorrhizal phase (Bertini et fles of the genus Tuber (Gyosheva et al. al. 1999). 2012a, Marjanović et al. 2010, Dimitrova Many hypogeous fungi, for instance and Gyosheva 2008). truffles, are pioneer species. They are of- Geographic position of Bulgaria and 114 T. Nedelin, M. Gyosheva, K. Kostov, and S. Savev respectively the great diversity of ecologi- tum and Gautieria morchelliformis Vittad cal conditions let to assume that the large are also presented. Most of fungal speci- number of hypogeous ectomycorrhizal mens are DNA sequenced. Phylogenetic fungi could be found in the country. We analyses have been done for T. excava- can expect slightly genotype difference for tum and T. fulgens Quél. Recent molecu- some known species because of particu- lar studies have shed some light on com- lar conditions in a process of adaptation to plex diversity among closely related Tuber their plant partners. taxa. Molecular and phylogenetic stud- Eleven hypogeous ascomycetes (truf- ies on well-known species T. excavatum fles and truffles-like fungi) have been are insufficient until now (Alvarado et al. published until now from Bulgaria: Choi- 2012; Bonito et al. 2010a,b,c; Zampieri et romyces meandriformis Vittad., Elapho- al. 2009; Chen and Liu 2007; Wang et al. myces granulatus Fr., Hydnotrya cerebri- 2006, etc.). formis Harkn., H. tulasnei (Berk.) Berk. & Broome, Stephensia bombycina (Vittad.) Tul., Tuber aestivum Vittad., T. brumale Materials and Methods Vittad., T. borchii Vittad., T. excavatum Vittad., T. macrosporum Vittad., T. pu- The investigated specimens were har- berulum Berk. & Broome (Dimitrova and vested in several localities in Bulgaria in Gyosheva 2008, 2009; Gyosheva et al. 2014–2015. Some information concern- 2012a,b; Lacheva 2012; Peev et al. 2015). ing their habitats was recorded – habitat There is a great species diversity of type, nearby trees, soil structure and type larger basidiomycetes in Bulgaria and (where data are available). One perma- up-to-date more than 1500 species are nent plot (3×3 m) in the area near Gradets recorded (Denchev and Assyov 2010). village was chosen on a productive site Some of them from genera Gautieria Vit- for periodical observation and ecological tad., Hymenogaster Vittad., Macowanites studies (at least 1 time per month from Kalchbr., Melanogaster Corda, Octaviania September to April). Vittad. and Rhizopogon Fr. are hypogeous Morphological observation of main and ectomycorrhizal. character features of fungal specimens Hypogeous macrofungi are with high was studied on fresh specimens using conservation value. Ten species (5 asco- Carl Zeiss Jena Citoval stereo micro- mycetes and 5 basidiomycetes) were in- scope. Micromorphological characters cluded in the Red List of Fungi in Bulgaria were observed under Amplival, Leitz (Gyosheva et al. 2006) and also in the Laborlux Phase-contrast microscope and Red Data Book of the Republic of Bulgar- Zeiss light microscope. As mounting me- ia (Peev et al. 2015). All species are from dium deionized water was used. For bet- categories Critically Endangered (CR) – 1 ter observation and for important diagnos- and Endangered (EN) – 9. ing chemical reactions some colorizing This paper presents three species reagents were used – KOH, Congo Red of hypogeous fungi: Tuber rufum Picco, in ammonia solution, Cotton Blue in lac- Gautieria graveolens Vittad. and Lactarius tophenol, and Melzer’s reagent. The mi- stephensii (Berk.) Verbeken and Walleyn, crophotographs were taken by AmScope recorded for first time in Bulgaria. New MA1000, 10 MP× camera. Measurement data for the distribution of Tuber excava- of asci, spores and peridium were per- New Records and Data on Hypogeous Ectomycorrhizal Fungi in Bulgaria 115 formed by Piximetre 5.8 software (http:// lyzed for best fit model – lowest-scoring ach.log.free.fr/Piximetre/). maximum likelihood tree. To obtain this, Scanning electron microscopy (SEM) several tests were used: hierarchical like- was carried out at the Institute of Physi- lihood ratio test (hLRT), BIC test (Bayes- cal Chemistry, Bulgarian Academy of ian information criterion) – BIC = -2ln(L) + Sciences. Specimens were examined on Kln(n), where ln(L) = loglikelihood of the JSM-5510 scanning electron microscope best tree found, K = number of parameters at 10 kV. and AIC Model test – AIC = -2ln(L)+2K, All studied specimens are kept at the where ln(L) = loglikelihood of the best tree Mycological Collection of the Institute of found and K = number of parameters. Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, Sofia (SOMF). Results and Discussion The nomenclature of hypogeous fungi follows Kirk et al. (2001). The author’s abbreviations of fungi are according to New records of hypogeous Kirk and Ansell (2004). Hypogeous fungi macrofungi for Bulgaria were identified following Riousset et al. Ascomycota (2012), Dissing (2000), Montecchi and Pezizales Sarasini (2000), Montecchi and Lazzari Tuberaceae (1993), Pegler et al. (1993), Breitenbach Tuber rufum Picco, Meleth. Bot.: 80 and Kränzlin (1984), Trappe (1979), Den- (1788) nis (1978) and Moser (1963). The threat Ascomata hypogeous or semihypo- status follows the Red List of Fungi in Bul- geous, irregular, lobed and very rare garia (Gyosheva et al. 2006). subglobose (Fig. 1a), 1.5–4 cm in diam- For DNA analysis was used only prop- eter, yellow-brown to reddish-brown, fine erly dried material (5–6 h, 55–60 °C) stored warted and areolate, cartilaginous. Warts in freezer at – 20 °C. For DNA extraction, are fine and almost pyramidal. Peridium was followed and modified Dellaporta et al. is very thick (380–480 μm) and two lay- (1983) protocol for plant tissue isolation. ers can be distinguished – outer, which PCR amplification was performed with the is composed by 3–5 rows of thick-walled primers ITS1 and ITS4 (White et al. 1990, large hyphae and inner layer, which is Gardes and Bruns 1993) for the ITS re- paler and almost white, forming pseudo- gions. After gel-electrophoresis, success- parenchymatous tissue (Fig. 1b). Gleba ful DNA fragments were visualized and of interwoven to parallel hyphae is more cleaned using GeneMATRIX Basic DNA loosely structured than the inner layer of Purification Kit. Samples were sequenced peridium, hard and solid, initially whitish, at GATC biotech laboratory in Germany. than yellowish, ochre to olive-brown or The results were compared with their olive-gray at maturity, with a close net- closest relatives obtained with BLAST al- work of whitish meandering and translu- gorithm. Phylograms are constructed for cent veins. Odor: relatively strong, not T. excavatum and T. fulgens. Sequences specific and unpleasant. Taste is mild. were first aligned in CLC Genomics work- Asci 50–70 × 80–100 μm, clavate to al- bench 8.0 and then corrected manually. most globose (depending of spore posi- Dendrogram was constructed and ana- tion and view – Fig. 1d), short-stalked 116 T. Nedelin, M. Gyosheva, K. Kostov, and S. Savev Fig. 1. Tuber rufum (BG13AG10): a – general view; b – inner layer of pseudoparenchymatous tissue of peridium in Melzer’s reagent; c– SEM detail view of spore; d – SEM general view; e – asci with ascospores in Congo red; f – Tuber excavatum (BG13AG06) – ascospores. (10–25 μm) (Fig. 1e), usually 3–4-spored. N = 50; C = 95 % Me = 33.9 × 25.4 µm; Ascospores 27.1 [32.9; 34.8] 40.7 × 20.2 Qe = 1.3, broadly ellipsoid, ornamented [24.6; 26.1] 30.5 µm; Q = 1.0 [1.3; 1.4] 1.6; with conical spines (Fig. 1c), 2.5–3.5 μm New Records and Data on Hypogeous Ectomycorrhizal Fungi in Bulgaria 117 high, initially translucent, yellow – ochre p. 27, 1831. tobrownish at maturity (Fig. 1e). Basidiomata hypogeous or semi- Habitat.
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