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Importance of Picoa spp. as desert truffles fungi.

Picoa spp. called "Birds' truffles" are considered as desert truffles. It is valuable as food and used as medicine in Arabian Gulf countries including Saudi Arabia and several other countries of the world. Truffles, in general, have been considered for centuries as valuable food due to their high nutritional value (1). As it is well known, desert truffles are a natural source for several chemical components such as proteins, amino acids, vitamins, flavor compounds, sterols, terpenes, fatty acids; they are also rich in minerals and carbohydrates (2,3,4,5). Truffles were usually used to make typical food in several cultures, while desert truffles are highly valued by people principally in Middle East and north of Africa (6-7). In addition, desert truffles were widely used in traditional medicine due to their pharmaceutical properties and medicinal value. Picoa spp. cited in all of the countries of Mediterranean basin including Saudi Arabia and Iran. It can be found in a gypsiferous and calcareous gravelly deserts soil and the fruiting bodies appears from January to April in Kuwait (8), while in Saudi Arabia appears from November to March (9), these periods is directly related to climatic conditions. During the fruiting season, Ascomata of Picoa spp. can indirectly noticed by remarking the surface of the soil which appears cracked or convex, this modification of soil surface and the presence of Helianthemeum spp. confirm that the ascomata of Picoa spp. are in the remarked place. In addition, the mutual relationship between desert truffles and Helianthemum sp. had been proved, via Isotopes tracer 14CO2 aided research (10). In comparison with desert truffles, birds' truffles have not been sufficiently studied; few research works concerning Picoa spp. were highlight ecological importance, distribution as well as the taxonomy. In this present article, we compile recent data on the importance of Picoa spp. as desert truffles fungi.

Occurrence of desert truffles

The desert truffles grows principally in countries around the Mediterranean basin, they have been reported by many scientists in countries of Southern Europe including Spain and Portugal (11-12), France (13), Italy and France (14), Hungary (15), Turkey (16), they have been also reported in North Africa that extends from Mauritania to Egypt (17,18,19,20,21), Middle East (22,23,24,25) and Qatar (26). However, some species of desert truffles were also found in Botswana, South Africa (7,27,28) and in North America (29). Regarding the morphology of desert truffles, several types have been collected in Africa and in the Middle East region. They have been evaluated by numerous scientists. Some wild macro-fungi species were reported in Saudi Arabia, Bahrain, and Egypt such as Terfezia claveryi and Tirmania nivea (4,5,30,31,32). Others types of desert truffles, such as Choiromyces echinulatus, Terfezia pfeilii and Kalaharituber pfeilii have been also reported in South Africa (33). Furthermore, various types were found in Tunisia such as Picoa juniperi, Picoa lefebvrei and Terfezia sp. (34). Moreover, five types of desert truffles were found and identified in different parts of Iran such as T claveryi, T. nivea, Tirmaniapinoyi, P juniperi and P lefebvrei (35).

Hosts plants of desert truffles

Desert trufues have a mycorrhizal association with numerous annual and perennial xerophytic host plants that belongs to the Cistaceae family. They form mycorrhizae mainly on roots of different species of the genus Helianthemum sp. (10), or Cistus sp. and Helianthemum sp. (36). The type of this association between desert truffles and Helianthemum sp. is function to culture conditions (36), and function to phosphorus content culture medium in sterile conditions; an ectomycorrhiza in high phosphorus level and ectendomycorrhiza in culture lacking phosphorus or an endomycorrhiza present in deficient level of available phosphorus (37). Interestingly, scientists have successfully obtained an endomycorrhiza between Helianthemim spp with Terfezia and Tirmania spp. (38,39) which were called few years later as "helianthemoid" mycorrhizae specific to this type of mycorrhizal association which is firstly described by Alsheikh (40). The plasticity of desert truffles to form different mycorrhizal association types have been demonstrated recently by Zitouni-Haouar et al. (41) when they inoculated in in vivo conditions six Cistaceae species with three Terfezia species: Terfezia leptoderma, Terfezia boudieri, and T claveryi. In fact, typical endomycorrhizae was formed in Helianthemum ledifolium, Helianthemum lippii and Fumana procumbens whereas an ectomycorrhiza was synthesized in Cistus species (C. albidus, C. incanus, C. salvifolius) and Pinus halepensis (Aleppo pine) in green house conditions.

Ecological importance

This association plays an important role in the maintenance of Mediterranean shrub lands and grasslands, furthermore, they help prevent erosion and desertification (42), and have an ecological and economical interest not only because they can be an alternative agriculture yield in arid and semi-arid lands but also because of their high price on the market (43), also can have positive effect on sustainability and biodiversity (44) and may play a considerable role in eco-tourism in arid and semi-arid regions.

Cultivation and conservation of desert truffles

Cultivation of truffles in arid and semiarid lands was studied by different authors, but certain were focused their work on cultivation and fruiting of T. boudieri Chatin in semi controlled conditions (green house) and in situ, by inoculating of Helianthemum sessiliflorum Desf. Pers. using two type of soil; gypsy and sandy soil (45), the results of this research are encouraging to turn toward "cultivation" of desert truffles. Cultivation of desert truffles may represent ex situ conservation (46), despite a specific cares should be followed in this activities. Evaluation of soil and environmental characteristics of the plantation site are crucial, especially in semi-arid areas where climate conditions are critical (47,48). Ex situ conservation of desert truffles can constitute a new branch of ecotourism for local population in Middle East and north of Africa. In this scope Saudi Wildlife Authority which manages several natural reserves in Saudi Arabia takes, every year, an action to organize desert truffles collecting inside the natural reserve of Harrat Al Harrah in the northern region of Saudi Arabia, in a way to preserve fungal, flora and fauna of this reserve (49).

Few studies have been conducted to characterize the mycorrhizae of desert truffles cultivated with their host plants under semicontrolled conditions in green house. In fact, the first attempt to cultivate desert truffles in the western desert in vivo was performed in Iraq (10). Actually, they simulated desert condition to cultivate desert truffles and investigate their relationship with Helianthemum herbs. Interestingly, Alrawi and co-workers have demonstrated that some critical factors are essential to improve desert truffles production such as soil composition and texture, moisture contents, temperature, as well as the type of water and vegetal flora. Moreover, they have also tested the effect of irrigation on the growth of desert truffles, surprisingly, irrigation test was succeeded and all irrigated areas have produced desert truffles. On the other hand, the research of at Arar city constitute an installation of a system of drip irrigation in a specific locality; these localities produce, naturally, desert truffles. Irrigation of these selected plots in autumn has a positive effect, qualitatively an quantitatively, on the production of desert truffles ascomata (50). Additionally, the importance of irrigation factor for successful cultivation has been reported, also, by Morte et al., (51). Others, demonstrated that irrigation should be applied twice during the season, one time at the end of the summer especially when rainfall is less than 150 mm and the second time during the fruiting season in dry period of the year (52). Several Helianthemum species such as H. salicifolium and H. ledifolium have been inoculated by different species of desert truffles in the conditions of green house (10).

Picoa spp.

Desert truffles include several valuable hypogeous macrofungus species; few scientists have been interested in discovering and studying new desert truffles species, especially the genus Picoa spp. which belong to Ascomycota (Pyronemataceae, Pezizales). Several Picoa species have been reported in arid and semi-arid ecosystem especially in Tunisia, Saudi Arabia, and Iran. Table1 present few examples of Picoa species reported in Africa and Middle East.

Actually, P juniperi and P lefebvrei are not, traditionally, the most highly appreciated desert truffles in Middle East and north of Africa. Because fruit-bodies of Picoa are very small and are not collected for this reason, in spite of their edibility. A recent field study (58), showed that drip irrigation of naturally producing plot of Picoa spp. in Muayala Natural Reserve near Arar city at the north-east of Saudi Arabia, has permit to obtain for the first time of relatively big ascomata of Picoa spp. with a diameter reach to 7.5 cm. The presence of Phaeangium lefebvrei in the northern area of Saudi Arabia has been confirmed by (57). Also, others studies revealed for the first time the presence of P lefebvrei in the eastern area of northern borders province in Saudi Arabia (9).

Classification

Classification of desert truffles including birds' truffles was based on morphological characters such as morphology of ascomata, spore, peridium, sporocarp odor, as well as color of the gleba. Classification of Phaeangium was the subject of different opinion. In taxonomical point of view, Picoa lefebvrei was firstly descried and grouped in the genus Phaeangium; P lefebvrei Pat. (59). Current name: Picoa lefebvrei (Pat.) Maire (60). Also, the same name was adopted by (61,62), other synonym: Terfezia schweinfurthii Henn. after Gucin et al. (55). While Phaeangium was placed temporarily in Peronymataceae (63). Classification based on morphological features is common and used till these days. Spores in Phaeangium are ornamented at maturity and a have tomentose peridium, whereas Picoa juniperi has smooth spores and no tomentum. Phaeangium and its single species, P. lefebvrei, are re-described and placed in the family Pyronemataceae, tribe Mycolachneae (22). Actually, classification basing on morphological characters is a complementary approach but, at the same time, it is difficult and not sufficient to differentiate two close species. This may be attributed to the effect environmental factors and various ecological habitat conditions on morphological characters (64).

Recent studies have been carried out to revise the classification of Picoa using molecular methods; the obtained results showed that most morphological character used in classifications of Picoa were not sufficient to study phylogenetic relationship and don't provide phylogenetic Information, whereas molecular markers especially Internal transcribed spacer (ITS), were principally phylogenetically informative and useful to separate the different lineages in Picoa, also in addition, geographical and ecological, rather than morphological data, are most useful character for separation of these lineages (65). Other phylogenetic analyses demonstrate that Picoa lefebvrei belongs to the Geopora-Tricharina clade of Pyronemataceae family. In fact Phaeangium lefebvrei was placed in Picoa Vittad. due to its close genetic relationship with P. juniperi Vittad. (65,66).

Chemical composition of Picoa

Chemical composition and nutritional value of several desert truffles and Picoa spp. were studied and evaluated by numerous reviewers and researchers (67,68,69,70). Precisely, other authors (68) have studied the composition of desert truffles "birds' truffle" Phaeangium lefebvrei Pat.; they reported that fruit-bodies are rich in minerals and contain 23% total protein (% dry weight), 18% total carbohydrates, 1% crude fat and 3% total crude fibers, and a total of 26 amino and 11 fatty acids, this can give us an indication to take care of these neglected desert truffle fungi which can participate in high quality of human nutrition.

Importance of Picoa spp.

Species belonging to Picoa spp. are not extremely appreciated by local people in Middle East and Africa, in spite of their nutritional value (2), antioxidant activity (71) and medicinal properties (72) but also for their important role in prevention of erosion and desertification. It has good chemical composition suitable for human health like other types of desert truffles. In comparison to desert truffles, the Picoa spp. does not have tremendous values and economic importance. The interesting study is, which confirm the importance of birds' truffles; P lefebvrei and Pjuniperi as antibacterial agent against the development or the inhibition of several bacteria; Escherichia coli, Bacillus subtilis, Pseudomonas aeruginosa, Staphylococcus aureus, Streptococcus mutans, Preteus vulgaris, Salmonella typhi, and same effects were observed against the yeast; Candida tropicalis and also against the dermatophyte Trichophyton sp. (72). The Picoa can play a significant role in biological control agents, which may reduce the harmful organisms in the soils. Also, can provide food for birds, the fruiting bodies which appear partially on the surface of the soil are eaten by birds (8,73). They were sought out by migratory birds and have been used by Bedouin as bait in bird traps (74). Interestingly, P. lefebvrei were generally used in folk medicine to treat people infectious eye diseases (71). By decomposition of the Picoa in the soils, it may improve physical, chemical and biological conditions of the soils that directly or indirectly improve the ecological conditions of the soils and environment.

CONCLUSION

Further studies are needed to develop molecular probes for desert truffles including birds ' truffles identification, and more researches are also required to study their biodiversity and to understand in a better way the physiology of these appreciated fungi in Middle East and north of Africa. In additions, international legislations need to be developed to regulate trading of desert truffles. These multiple actions may advance our scientific knowledge on desert truffles in arid and semi-arid ecosystems, and can play as a crucial element to improve natural production including preservation in their habitat. Also, these actions will indirectly help local population to realize the concept of eco-tourism. A special attention need to be focused on developing natural production, and why not to move to the "production of desert truffles" via controlled mycorrhization of annual or perennial associative desert plant, to meet the increasing demand of these highly valued hypogeous fungi.

ACKNOWLEDGMENTS

The authors wish to acknowledge the approval and the support of this research study by the grant No. 032-434 from the Deanship of the Scientific Research in Northern Border University (N.B.U.), Arar, KSA.

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A. Bawadekji [1] *, M. Abdelrazek [2], M.A.U. Mridha [3] and M. Al Ali [4]

[1] Northern Border University, Deanship of Scientific Research, Arar, P.O. Box 1321, Saudi Arabia.

[2] Taibah Universities, College of Applied Medical Sciences, Almadina Almonawara, Saudi Arabia.

[3] Plant Production Departments, King Saud University, Riyadh-11451, Saudi Arabia.

[4] Universite d'Angers, Institut Superieur de la Sante et des Bioproduits d'Angers, France.

(Received: 08 December 2015; accepted: 24 February 2016)

* To whom all correspondence should be addressed. E-mail: hakimbawadekji@gmail.com
Table 1. Examples of Picoa species reported in
Africa and Middle East

Truffles                     Countries     References

Picoa juniperi                Tunisia         [34]
Picoa lefebvrei
Picoa lefebvrei                Turkey         [53]
Picoa juniperi
Picoa Vittad.                                 [55]
Picoa lefebvrei             Saudi Arabia      [9]
"Phaeangium lefebvrei"                        [57]
Picoa lefebvrei                 Iran          [54]
Picoa spp.                                    [56]
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Author:Bawadekji, A.; Abdelrazek, M.; Mridha, M.A.U.; Ali, M. Al
Publication:Journal of Pure and Applied Microbiology
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Date:Mar 1, 2016
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