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Species Diversity of Hypogeous Ascomycetes in Israel

We conducted a species diversity study of the hypogeous Ascomycetes of Israel. The hypogeous Ascomycetes in Israel include members of the families Pyronemataceae, Pezizaceae, and Tuberaceae, which are represented by seven species: Hydnocystis piligera, Terfezia arenaria, T. claveryi, T. oligosperma, Tirmania africana, Tuber asa, and T. nitidum; only T. asa is new to Israeli mycobiota. Synonymy, locations, collection data, general distribution, distribution in Israel, descriptions, a key to identification, illustrations, and taxonomic remarks are provided.

The hypogeous Ascomycetes represent one of the most interesting and complicated systematic groups of Ascomycetes. The species diversity of this group in Israel is poorly known compared to many other fungal groups, and only a few surveys on this subject have been published. The most notable ones include the elaborations by Rayss [1,2] and Binyamini [3][4][5]. However, none of these researchers provided a critical species diversity study or a taxonomic analysis of the hypogeous Ascomycetes in Israel.
Hypogeous fungi colonize a variety of forests and semi-arid ecosystems in the Mediterranean region. Most of these fungi frequently establish mutualistic associations with vascular plants via specialized nutrient-gathering organs called mycorrhizas [6]. Many hypogeous fungi occurring in semi-arid and arid desert ecosystems of the Mediterranean Basin belong to the genera Hydnocystis, Terfezia, Tirmania, and Tuber. Most are endemic not only to Israel but also to the Mediterranean region and establish mycorrhizal symbioses with members of the Cistaceae, mainly with Helianthemum species.
According to classical mycology, most species have been described based on their morphological features such as ascospore and peridium morphology, gleba color, odor and other organoleptic characteristics. However, these fungi are difficult to identify at the species level. The use of morphological features is problematic for the systematics of hypogeous Ascomycetes because of the reduced set of morphological characteristics and homoplasy. Ascocarp features are homoplastic as a result of the parallel evolution of independent lineages of epigeous/hypogeous fruit bodies during the evolutionary history of the Peziza-les [7]. This accounts for the early artificial classification of hypogeous fungi in the order Tuberales. Tuberales includes several hypogeous families with similar morphology that originated by parallel or convergent evolution [8]. Realizing that the Tuberales artificially grouped many Pezizales, Trappe [7] transferred some of families from Tuberales to Pezizales and amended some families in Pezizales to include related hypogeous fungi. He also amended the Pezizaceae Fries sensu Korf to accommodate several related hypogeous taxa lacking forcible spore discharge, such as Tirmania. In addition, Trappe [7] included Terfezia in the Terfeziaceae and Picoa in the Balsamiaceae, based on a comparative morphological study.
The increasing amount of molecular phylogenetic data now available has led to a continued revision of the hypogeous Ascomycetes [8][9][10][11][12]. O'Donnell et al. [8] provided support for the occurrence of independent lines of epigeous/hypogeous fruit body evolution in the Pezizales, which has affected classification of the desert truffles. Moreover, an 18S rDNA sequence analysis has revealed a close relationship between Terfezia and the Pezizaceae [13,14].
Subgeneric relationships within the Pezizales have been subjected to molecular analysis [14][15][16][17]. However, other than studies of the genus Tuber [16], no recent work has addressed subgeneric relationships within the hypogeous genera. Many hypogeous Ascomycetes have a rich synonymy, i.e., some species have, at times, been placed in different genera, families, or orders by different authors, and species names have been changed as well. New interpretations based on molecular phylogenetic analyses are leading to the assignment of species to different genera based on generic relationships rather than structural relationships. Therefore, the names accepted in this study have *Corresponding author <E-mail : gbarseghyan@gmail.com> been used currently by many mycologists but are subject to change with new interpretations.
After searching the literature, we found that six species of hypogeous Ascomycetes are known in Israel. During the investigation, one new species from the genus Tuber was added to Israel's mycobiota. At present, the hypogeous Ascomycetes in Israel are represented by seven species.

Materials and Methods
This investigation was based on the 2002 and 2007 growing seasons and on published literature devoted to Ascomycetes of Israel. The collected specimens were preserved at the Institute of Evolution, University of Haifa (HAI, Israel) herbarium. The microscopic characteristics were observed with a Carl Zeiss-amplival microscope (Carl Zeiss, Jena, Germany), and photomicrographs were taken with a Sony camera (Sony, Tokyo, Japan). Fungal material was mounted on a microscope slide and examined in water using a light/dark field microscope with or without phase contrast at a magnification of up to ×1,000. Micromorphological characteristics of our specimens were observed using Melzer's reagent. For statistical calculations, 30~40 ascospores, asci, exscipular hyphae, and paraphyses were measured for each preparation.

Habitat & Distribution in
Note. This is a rare species for Israeli mycobiota. This species was found for the first time and described in Israel by Rayss [2]. After Binyamini [3], a detailed discussion and a comparison with species described by Tulasne and Tulasne [23] and Bataille [24] as T. leonis was conducted. The name T. leonis, under which this species is commonly known, has to be rejected as an illegitimate name, according to Trappe and all other modern authors. Note. This is a very rare species for Israeli mycobiota. Terfezia claveryi was found in Israel for the first time by Rayss [1]; the location of the sample collection or the herbarium as well as other important information was not mentioned. This species has since been properly characterized by its ascosporal ornamentation and habitat. Habitat & Distribution in Israel. Fruiting from January to April, in wood of Pinus halepensis at a depth of 3~5 cm or at the surface of soil at maturity, in groups of 3~8. The outward sign of the presence of these fungi is the appearance of cracks in a slight elevation of the soil. SP: Tel Aviv, Ramat Gan Park, March 22, 1977, January 24, 1979, leg. B. Shemen, det. N. Binyamini (Fig. 3) [3].
Habitat & General distribution. Mycorrhizal species. Not a very common species, generally growing in deciduous woods, preferably with a Mediterranean climate, typical on sandy coast-lines, where it grows in autumn and also in spring in warmer locations. Asia: Israel. Europe: France.
Note. This fungi was described for the first time in Israel by Reichert [25] under the name Delastripsis oligosperma. Mycorrhizal fungi, mostly endemic to arid and semi-arid areas of the Mediterranean Region, are associated with Helianthemum species [26].  fig. 4, 20: fig. 10 a, b,  Note. This is a rare species for Israeli mycobiota. This species was found for the first time and briefly described in Israel by Rayss [2]. According to Montecchi and Sarasini [21], Tirmania africana is in synonymy with T. nivea and its current name is T. africana, according to the Index Fungorum online database. This species can be confused morphologicaly with T. pinoi but the smooth surface and ellipsoid spores of T. africana make it easy to distinguish from T. pinoi.
Habitat & General distribution. Mycorrhizal species. This species is associated with both coniferous and deciduous trees, widely spread in all environments. Asia: Israel. Europe: Austria, Italy, Poland, Spain, Switzerland.
Note. This is a very rare species for Israeli mycobiota. According to Hawker [27], this species is very close to Tuber rufum but differs in color. The hymenium does not have a red tinge, and the spore spines are more slender and more densely crowded [5]. According to Montecchi and Sarasini [21], the differential characteristics of this "form" are limited to the fairly regular fruit bodies' form and light colors on a smooth and bright surface, even during late maturity. Due to these characteristics, this entity could be mistaken for a species in the so-called T. puberulum group, but the aculeate and none reticulate-alveolate spores, or in the case of immature ascospores, the peridium structure of the interwoven hyphae eliminate any doubt.