Characterization of Desert Truffles in the Great Moroccan Sahara: A Review ^†

Abstract

Desert truffles are edible mushrooms compulsorily living in symbiosis with plants’ roots. They are rich in essential nutrients and secondary metabolites, conferring therapeutic properties. In Morocco, around ten species can be found in semiarid and arid climate regions with low annual rainfalls and high average temperatures. They can be associated with the Cistus and Pinus species and some other species, but they are detected more often under the Helianthemum species. In this study, we present a short review of the distribution of Moroccan desert truffles in the Great Sahara, along with the progress achieved in their morphological and molecular identification and the evaluation of their nutritional content.

1. Introduction

Desert truffles or Terfess are mycorrhizal fungi classified into the Pezizales order (previously known as Tuberales), belonging to the Pezizaceae family in the phylum of Ascomycota, including the Terfezia, Tirmania, Delastria, Picoa, Balsamia, and Melanogaster genera. They produce edible hypogeous fruiting bodies called ascocarps that grow around the roots of some known desert plants as a result of the symbiotic association known as mycorrhiza [1]. In Arab countries, they are commonly called” Kamé”, “Kholassi”, and “Zoubaïdi” but also “truffles of sand” given that they are found in deserts’ sandy soils; they are called “Criadilla de tierra” and “Criadilla vaquera” in Spain [2]. In Morocco, the discovered desert truffles are Terfezia boudieri Chatin, T. leptoderma (Tul. & C. Tul), T. arenaria (Moris) Trappe, and T. claveryi (Chatin) as well as Tirmani nivea (Desf.) Trappe and Ti.pinoyi (Maire) Malençon, particularly found in the southeast of the country [2]. In addition to Morocco, desert truffles can be found in all semi-arid and arid regions characterized by warm climates. They are distributed in North Africa, Middle Eastern countries, and the Mediterranean Basin [2]. The objective of this paper is to present a short review about the distribution of desert truffles in the Great Sahara and to explore the species discovered in Morocco along with their ecology, host plants, and the nutrient content of each species.

2. Ecology of Desert Truffles

2.1. In the Great Sahara of Morocco

According to [2], desert truffles are located in calcareous, aerated, sandy soil, characterized by a homogeneous texture and sometimes found in calcareous sandy loam soil but rarely in acidic soil. For host plants, most species that belong to the Helianthemum genus are able to grow in symbiosis with desert truffles, for example, Helianthemum lipii Pers., H. ledifolium (L.) Mill., H. hirtum Mill., H. asperum Lag. Ex Dunal, etc. The content of organic matter in the soils must be low, along with the fertility and exchange capacity. Regarding minerals, desert truffles require the presence of nitrogen, phosphate, potassium, calcium, and iron although it has been reported that a low content of phosphate and iron increases the mycorrhization potential. Similar environmental conditions have also been reported by [3] in Figuig regions. Concerning climatic conditions, the main limiting factor for desert truffles is rainfall, both the quantity and period of precipitation. For some species, precipitation must be in autumn, but generally, it is more needed during winter and spring. The bioclimatic stages where desert truffles may be found are diverse, from arid and semi-arid to sub-Saharan and Saharan. According to recent research [3], desert truffles are mostly found in the regions of Beni Guil and Abou Lakhal, characterized by moderate rainfall all year despite the desertic climate. The average temperatures are 17.9 and 18.6 °C, respectively. The annual rainfall in those regions is around 170 mm. These regions are also characterized by heavy rain in the evenings and early mornings, dewfalls, thunder, and lightning, which significantly contribute to truffles’ growth. Most of these parameters can be found in the south regions of Morocco, including the Great Sahara.

2.2. In Other Countries

A study of desert truffle ecology in Saudi Arabia [4] also mentioned rainfall parameter as the important factor for desert truffle growth. A lower rate of precipitation may affect the physiology of the host plant and, consequently, decrease spore and further ascocarp production. Other factors are physiochemical properties of soil, meteorology, and ambient temperature. In basic soils, dominant host plants are H. ledifolium and H. salicifolium (L.) Mill. The climate in the desert truffle regions in Saudi Arabia is also hyper-arid to Saharan, with rainfall in October and December and a harvest period starting from the beginning of December.

3. Distribution of Desert Truffles

3.1. In the Great Sahara of Morocco

As already mentioned, some species of desert truffles discovered in Morocco are found in the south of the country. The first one is T.claveryi (T. hafizi Chat.), also called the “Red Terfess of Tafilalet”. It is found in Aïn Beni Mather, Tendrara, Bouarfa, regions of Erfoud, and near Ksar es-Souk, Bou Bernous, Boudenib, and Figuig (Bni Guil and Abou Lakhal regions) [2,3]. It can be harvested after rainfall, from March to May, under the H. lipii as a host plant. Furthermore, T.boudieri is found in Had Hrara, the region of Oualidia, and a few kilometers to the east of Safi city in the Abda plains. It is also found in Aïn Beni Mather along with regions in Erfoud. Most importantly, it can be detected in desertic plains where it is harvested in March and April under the Helianthemum species H. lipii and H. ledifolium. Other species belonging to the Tirmania genus have been identified, namely Ti. nivea and Ti. pinoyi. They are distributed in the southeast, especially in regions of Aïn Beni Mather, Tendrara, Bouarfa, Erfoud, Figuig, and Rissani. The harvest period is from early December until March under the H. hirtum as a host plant.

3.2. In Other Countries

Desert truffles are distributed in Algeria, Tunisia, Libya, Egypt, Saudi Arabia, Iraq, Iran, Kuwait, Syria, and Palestine. They are also spread in the Mediterranean Basin, in the south of Italy, Spain, France, Portugal, and Greece [2]. T.claveryi is found in Algeria, Tunisia, Egypt [2], and Libia [3] as well as in the European countries France and Spain (especially in semi-desertic areas in the south) [2]. T.boudieri is also found in Algeria and Tunisia under the Helianthemum lipii and sometimes under the Rhatherium suaveolens Desf., particularly in Libya and Egypt.

4. Characterization of Desert Truffles

4.1. Morphological Traits

In Morocco, the collected ascocarps of T.claveryi (Figure 1a) had different shapes (cordiform, ovoid, and round) measuring 3 to 5 cm and fresh weights from 17 to 50 g. The color of the peridium was pinkish-white at the beginning and converted to brownish-black at maturity; there was a few millimeters of spotting to the gleba. The gleba was firm with a little spongy consistency, and its nodules were round, fertile, and pinkish then light brown, separated by pale veins. The asci were ovoid (64–68 × 72–84 µm) and contained hyaline, grey, spheric ascospores (18–21 µm) with an alveolus network. For Tirmania sp. ascocarps, the shapes and sizes changed (Figure 1b) from sub-globular and piriform to similar to that of a turbine, with lobes or irregular shapes along with a protruding basis that was easily detachable. The peridium was pale showing cracks and furrows, and the gleba was whitish-yellow, pulpy, and firm or a little spongy. Inside the ascocarp, fertile nodules were visible in labyrinth patterns, separated with sterile veins. The asci were round on the top and elongated at the basis, containing eight claviform, globular, or elliptic ascospores, with a double smooth membrane [2].

4.2. Molecular Traits and Genetic Diversity

Morphological observations of desert truffles are very informative in the identification of species although, sometimes, the morphology can vary. It depends on temperature, moisture, and the physicochemical properties of the soil but also on intraspecific variations. To face those challenges, the utilization of molecular approaches is useful in order to study intraspecific variability identification more closely [4]. To study the genetic diversity of Iraqi truffles, a team of researchers focused on a molecular study of the internal transcribed spacer (ITS) regions of ribosomal DNA by amplification with specific primers: ITS1-F and ITS4-R, followed by electrophoresis in BET-stained agarose gel, and, finally, observation with a special UV camera [6]. They proceeded with a purification of the PCR products, blasting on the NCBI GenBank database and comparing with other sequences of the same species. Then, the sequences obtained from the collected sample were deposited in the NCBI GenBank to obtain accession numbers. All accessions were studied for genetic diversity by generating a phylogenetic tree using MEGA 6.06. Indeed, all sequences from the collected samples were identified and belonged to two species, T.claveryi and Ti.pinoyi, as presumed. However, in the phylogenetic analysis, they were separated into two main groups, A and B, according to their rDNA ITS sequences of each species.

4.3. Chemical Composition

Although truffles are known to be rich in nutrients, the research in this field is scarce. Among the research, [7] conducted a study concerning the phytochemical composition and nutritional value of the Ti.pinoyi species in Morocco. After measuring different chemical compounds and nutrients from fresh material, dried material, and material macerated to powder, the following results were discovered: 81.5% of moisture and 64.7%, 26.2% and 3.0% of carbohydrates, crude proteins and lipids, respectively. For minerals, Cu measured about 65.3 mg/Kg, Zn about 38.1 mg/Kg, and Se about 35.3 mg/Kg; low quantities of Pb and Cd were detected. In Saudi Arabia [4], it was reported that desert truffles are rich in fibers and amino acids and have high quality proteins with a percentage between 16.3 and 18.5%. For other nutrients, lipid content is between 6.2 and 5.9%, and carbohydrates are between 67.2 and 65%. In addition, alkaline phosphatase (ALP) activity has been reported as a key indicator of metabolic activity of desert truffles as it is produced in drought conditions at a higher rate. Other compounds such as phenolic acids, carotenoids, flavonoids, antioxidants, and minerals can be found as well as different compounds conferring medical and therapeutic activities. Another study conducted on Iraqi T.claveryi [8] reported that the total proteins reached 17.6%, lipids arrived at 1.0%, twelve essential amino acids reached 1567.7 µg/g of dry weight, and carbohydrates arrived at 79.8%. The authors also obtained a moisture value of 82.0%, ash value of 1.5%, and a total phenolic compound value of about 6479.0 µg/g, which mainly included the rutin.

5. Conclusions

Desert truffles are a widely spread mushroom with a high nutritional, medical, and therapeutic value. In Morocco, their distribution is already known, but the characterization of their species and the evaluation of their chemical composition is barely studied. These aspects need to be explored further, given that the data available are not sufficient. Therefore, it is considered a promising area of study, especially in the regions of the Great Sahara, located in the south of the country, where optimal growth conditions of desert truffles can be found. As a perspective, we aim to continue the progress achieved in this field, focusing our work in south regions of Morocco. The study of growth conditions and the characterization of desert truffle species to achieve its domestication in the Great Sahara of Morocco represent a priority to preserve this desert diversity.