| Mycologia Iranica | ||
| Article 1, Volume 7, Issue 1 - Serial Number 1013, January 0, Pages 1-43 PDF (1.68 M) | ||
| DOI: 10.22092/mi.2021.123456 | ||
| Full Text | ||
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INTRODUCTION
Gilled fungi and boletes (often referred to as ‘mushrooms’) are among the most prevalent groups of macrofungi. Traditionally they are the best-studied fungi in many parts of the world probably on account of their potential value as a food source but also their conspicuous and often eye-catching fruitbodies. The number of described species worldwide now exceeds the ca. 14,500 species of Chang & Miles (2004) and Kirk et al. (2008). Gilled fungi, also commonly known as agarics, share a structural characteristic, i.e., vertical plates, denoted as lamellae or more colloq-uially as gills (with varying shapes, sizes, thicknesses, distances from each other) which serve as spore-producing tissue on the undersurface of the cap and are a highly efficient way of increasing the surface area of the fertile part of the fungus. Boletes have tubes which are, in effect, simply rolled up gills, with some members of the Boletales having true gills e.g., the genus Phylloporus. According to molecular evolutionary studies, the formation of gills has evolved several times and therefore, is considered to have been a characteristic worth preserving to assist in spore dispersal and species survival (Hibbett et al. 1997). Gilled fungi and boletes are very diverse, morphologically, chemically and ecologically. They range in size from a few millimeters in diameter (e.g., species of Mycena, Marasmius and Coprinellus), to more than a metre across the cap (Macrocybe titans, Phlebopus marginatus). Important variable characteristics include the presence or absence of a stipe, of veils, or veil remnants. The species exhibit numerous colors, odors and flavours. Chemically, some gilled taxa e.g., in the genera Amanita, Galerina, and Cortinarius contain a number of the most toxic natural compounds namely amatoxins, phallotoxins and orellanine; boletes do not have such lethal compounds although the genus Rubroboletus has a toxin (bolesatine) that causes severe gastrointestinal problems. In contrast, various species, e.g. Agaricus campestris, Amanita caesarea, and Boletus edulis are considered edible. There are other taxa of the genera Psilocybe, Copelandia, Gymnopilus, Inocybe, Panaeolus, Pholiotina and Pluteus, that produce hallucinogenic substances such as psilocybin and/or psilocin. Ecologically, as symbiotic partners involved in plant development (mycorrhizae), and as decomposers, with enzymes breaking down lignin and cellulose in woody and herbaceous debris, they are critical for carbon recycling and ecosystem functioning. Some species e.g. Armillarialuteobubalina and Moniliophthora perniciosa are pathogenic and/or parasitic and cause destruction of eucalypt forests and cacao crops respectively (Shearer & Tippett 1988, Meinhardt et al. 2008). The substrates also vary, as they grow on soil, wood, dung and litter. Many agarics and boletes also provide food and medicines for humans, and nutrition and habitat for other organisms. Biogeographically, they are widespread in temperate, equatorial, arctic and sub-antarctic ecosystems, possibly wherever a vegetation layer exists. From a systematic viewpoint, the first comprehensive phylogenetic studies on agarics were published by Moncalvo et al. (2002) and Matheny et al. (2006). They were, and still are, the basis for the next studies of individual clades and groups of agarics worldwide. Concerning boletoid genera, the study by Wu et al. (2014) opened a broad field for defining many new genera. A ten-year phylogenetic overview of the Basidiomycota and related phyla in relation to DNA-based phylogeny was published by Zhao et al. (2017). An extensive study dealing with global patterns of mushroom evolution was recently published by Varga et al. (2019). According to the most recent account of a systematic outline of the Basidiomycota (He et al. 2019), the class Agaricomycetes currently contains 22 orders, of which agarics and boletes are distributed across the six orders Agaricales, Boletales, Cantharellales, Hymenochaetales, Polyporales, and Russulales. Iran, with a wide elevational range, from 26 m b.s.l. along the southern coastline of the Caspian Sea, to 5,671 m a.s.l. at Damavand Mt. in Central Alborz, harbors diverse climates and habitats. Vast hot and dry deserts with a precipitation of less than 25 mm/yr in central Iran, coincide with narrow sub-tropical humid regions at the northern parts of the country with precipitation exceeding 1,800 mm/yr. In Iran three macrobioclimates have been recognized, namely, mediterranean, tropical and temperate, largely correlating with the three biogeographical regions Irano-Turanian, Saharo-Sindian and Euro-Siberian, respectively (Djamali et al. 2011). Large parts of the country are characterized by continentality, with hot and dry summers, cold and harsh winters, and low precipitation, while forests are mainly confined to the northern and western borders (Zohary 1973, Djamali et al. 2012). From a biodiversity viewpoint, Iran is at the crossroad of two global biodiversity hotspots, i.e. the Irano-Anatolian and the Caucasus (Mittermeier et al. 2005, Manafzadeh et al. 2017, Noroozi et al. 2019), covering the major mountain ranges of the country. Diverse topography and climate have resulted in the development of diverse flora and vegetation types. More than 8,000 vascular plant species are known from Iran with ca. 32% endemism (Noroozi et al. 2019). The number of woody plants in Iran is about 956 species (Mozaffarian 2005). Desert and semi-desert steppes, halophytes, montane grasslands, shrublands and woodlands, deciduous temperate forests, wetlands and alpine habitats are among the major vegetation types of the country (Noroozi 2020). Hyrcanian forests, on the northern slopes of the Alborz mountain range, are at the southeastern reaches of the Caucasus biodiversity hotspot. Despite its small area (ca. 5% of the total area of Iran), the majority of the Iranian macromycetes come from the Hyrcanian region (e.g. Ghobad-Nejhad 2011, Ghobad-Nejhad & Hallenberg 2012). Broad-leaved dense forests have developed due to the high precipitation (ca. 700 to 2000 mm/yr) and mild climate of the region. These forests are known to belong to the northern hemisphere Pleistocene glacial refugia, and contain several Arcto-Tertiary elements, such as Celtis australis, Parrotia persica, Pterocarya fraxinifolia and Zelkovacarpinifolia as well as evergreen plants (Zohary 1973, Frey et al. 1999, Akhani et al. 2010, Gholizadeh et al. 2020). The Zagros forests in western Iran are comprised of xerophytic open woodlands of deciduous trees and shrubs mainly dominated by Quercus species and constitute less than 40% of the forest cover in Iran (Sagheb Talebi et al. 2014). Among the few coniferous forests native to Iran, Juniperus excelsa woodlands are noteworthy, sparsely covering the subalpine zone of the Irano-Turanian parts of the Iranian mountains, mostly distributed at 2000 to 3000 m a.s.l. Macrofungi in Iran are far less studied compared to microfungi. Historically, mycology in Iran has been divided up into five distinct periods, with publications starting from 1860 (Ershad & Zare 2014). While the majority of studies are characterized by records on microascomycetes, the second period in Iranian mycology (1860–1941) also harbors publications containing some agarics and boletes. Interestingly, the oldest publication related to the fungi of Iran (Buhse 1860) contains eight species of agarics and boletes from the country, most of them later recorded in other publications (Table 1). The second oldest literature on Iranian fungi (Rabenhorst 1871) enumerates two species of this group. Later, publications by Petrak (1941, 1940, 1949) alone and jointly with the first Iranian mycologist E. Esfandiari (Petrak & Esfandiari 1941), appear, recording a few species of agarics and boletes from Iran (Table 1). Most of the fungi of Iran recorded until 2008 (excluding lichenized fungi, clinical fungi, and some other taxa) have been listed in a book by Ershad (2009). In this book, a list of 3229 fungal species has been sorted in alphabetical order, but with no attempt at taxonomic classification. Therefore, to figure out the number of any fungal groups from this book, a full systematic categorization of the records is needed. With regard to the number of macrobasidiomycetes in Iran, no clear figure is available, but up to now ca. 430 aphyllophoroid species are known from the country, covering polypores (poroids), corticioids, hydnoids, clavarioids and heterobasidiomycetes (Ghobad-Nejhad & Hallenberg 2012, Ghobad-Nejhad & Langer 2017); of these, 132 species are polypores (Ghobad-Nejhad & Bernicchia 2019). Statistics on agarics and boletes recorded from the country are largely lacking. Therefore, the aim of this study is to provide a first account on the diversity of gilled fungi and boletes in Iran, with annotations on their distribution, classification, and nrDNA.
MATERIALS AND METHODS
Species data The study group includes species commonly known as gilled fungi (agarics) and boletes. Basically, the taxa such as Schizophyllum commune and Daedalea/Daedaleopsis/Lenzites which have some sort of 'gills' (but studied among aphyllophoroid fungi), are not included. Data on agarics and boletes in this study were obtained from a thorough survey of scientific journal articles and books published up to the year 2020 and specimens collected by the first author. Moreover, sequences of Iranian material in GenBank and UNITE databases were incorporated after full identity check (see below). The basidiomata specimens were collected during 2000–2019 in different provinces of Iran. Samples were dehydrated using a mushroom drier or were air-dried. Macro- and micro-morphological characters of the specimens were studied under a binocular and a light microscope, using bright field or phase contrast optics. Microscopy routines generally followed Largent et al. (1977). Several identification keys (e.g., Knudsen & Vesterholt 2008, Justo et al. 2011, Antonín et al. 2013, Zervakis et al. 2014, Mahdizadeh et al. 2016, Voto et al. 2019, etc.), and some of the literature in He et al. (2019) for specific genera were used. A full list of examined specimens is available in Suppl. Table. Vouchers were deposited at Iranian Cryptgamic Herbarium (Index Herbariorum acronym ICH). Species current names and species authorities mostly follow MycoBank (www.mycobank.org), and Index Fungorum (www.indexfungorum.org). Recent or otherwise relevant taxonomic revisions and phylogenetic publications were also consulted. Records published in journals not approved by the Iranian Ministry of Science, Research and Technology (‘black-listed journals’) are not included here.
Molecular study A clean portion of the spore-producing part of the dried basidiomata was taken for molecular study. For DNA extraction, PCR and sequencing, we generally followed the protocol by Bußkamp et al. (2020): from each basidioma, 1–2 mg of tissue was suspended in 100 μl TE buffer in a 1.5 ml tube. Immediately, for cell lysis, a microwave (600 W) was used twice for 1 min each, with a pause of 30 s followed by cooling the tubes to −20 °C for 20 minutes. The tubes were centrifuged at 10,000 rpm for 5 minutes. For PCR, 100 times diluted portion of the supernatant was used. The PCR primers for amplification of ITS1, 5.8S and ITS2 regions were ITS1F/ITS4 or ITS1/ITS4 (White et al. 1990, Gardes & Bruns 1993). For PCR, a 45 μl master mix (QIAGEN, Hilden, Germany) was used, adding 5 μl of extracted DNA. PCR was performed with initial denaturation at 94°C for 3 min, followed by 29 cycles of denaturation at 94°C for 30 s, annealing at 55°C for 45 s, and extension at 72°C for 60 s. Final elongation was performed at 72°C for 7 min. The D1–D4 domain of nuclear ribosomal large subunit (LSU; 28S) was amplified using primers LR0R and LR5 (Vilgalys & Hester 1990). The PCR thermal cycling for LSU differed from the ITS only by an increased cycle extension time (90 s per cycle). PCR products were visualized on a 1% agarose gel stained with GelRed fluorescence dye (Biotium, Hayward, CA, USA). Bands were cut out and cleaned with QIAquick PCR Purification Kit (QIAGEN, Hilden, Germany). Purified products were sequenced using Sanger sequencing method (Sanger et al. 1977). The obtained DNA sequences were edited using MEGA6 (Tamura et al. 2013) and DNA Sequence Assembler v4 (Heracle BioSoft 2013, www.DnaBaser.com), checked with BLASTn (Altschul et al. 1990) and UNITE (Nilsson et al. 2019), and submitted to GenBank. We also searched through GenBank and UNITE databases extracting DNA sequences of agarics and boletes obtained from Iranian material, with a special focus on the ITS sequences. The sequences’ associated metadata were carefully checked, and BLASTn searches were performed against sufficiently identified and reliable sequences in those databases. In UNITE, the Species Hypothesis (SH) with 0–1.5% threshold was accepted. Accession numbers with incorrect, ambiguous, or otherwise unverifiable identity were excluded. Selected ITS accession numbers were inserted in Table 1.
RESULTS Species data The annotated list of species of agarics and boletes currently known from Iran is presented in Table 1. Nineteen species are newly recorded from the country, based on vouchered specimens all provided with nrDNA data from basidiomata (Table 3). In situ basidiomata photographs of selected species are shown in Fig. 1. Overall, 585 species of agarics and boletes are recorded from Iran, comprising 556 agarics and 29 bolete species (Fig. 2a). From a taxonomical viewpoint, the Iranian species belong to 147 genera and 34 families, distributed in the six Agaricomycetes orders Agaricales, Russulales, Boletales, Polyporales, Cantharellales, and Hymenochaetales (Fig. 2b). The largest order is Agaricales which encompasses 82% of the species (Fig. 2b). The three largest families are Agaricaceae (59 species), Russulaceae (57 species), and Psathyrellaceae (51 species) (Fig. 3). The family Polyporaceae is represented with seven agaric species in Iran, in the genera Lentinus, Neofavolus and Neolentinus (Fig. 3). Out of a total of 147 genera in Iran, 20 genera have ≥ ten species (Fig. 2g). The three most species-rich genera in Iran are Russula (43 species), Cortinarius (26 species), and Inocybe (25 species) (Fig. 2g); these genera are ectomycorrhizal. Excluded and doubtful taxa are presented in Table 2. Based on this, 28 species are excluded from the Iranian mycobiota (Table 2). Considering the geographic distribution of the species, we summarized data on species occurring in the Hyrcan (northern Iran), Zagros (western Iran), and other regions in Iran (Fig. 2c). Based on our analyses, the majority (79%) of agaric and bolete species recorded from Iran reside in the narrow, small area of Hyrcanian forests (Fig. 2c). Here, Mazandaran province is at the top, being the most species-rich province in the country (244 species), followed by Gilan (143 species) and Golestan provinces (134 species) (Fig. 4). The Zagros region harbors only 13% of the species (Fig. 2c). In total, 8% of the species have not been recorded in Hyrcan/Zagros forests, but were found mainly in central Iran. Tehran province is shown to have 65 species, while no species is yet known from Yazd province. For 89 species, distribution data is lacking (Fig. 4). Lists of species for each province of the country are provided in Table 4. Regarding the situation with the literature records, our analyses demonstrate that as much as 42% of records in Iran arise merely from single abstracts presented in conferences (Fig. 2f, species marked with ! in the Table 1). This means that such species have appeared in congress abstract only, with no subsequent evidence to support them; most of these records lack sufficient characterization, species name authority, or vouchers. For many of these, modern interpretation of the names was difficult, if not impossible. We were not able to trace the vouchers to re-examine them. Therefore, it is recommended that these records be considered tentatively for the time being, until more data become available about their identity. Molecular study In this study, a total number of 128 new nrDNA sequences was obtained, comprising 70 sequences from the ITS barcode region, and 58 sequences from the nrLSU (Table 3). The scrutiny through public databases GenBank and UNITE was also performed to extract the available DNA sequences of Iranian agarics and boletes and selected ITS accession numbers were inserted in Table 1 after careful checking. Our analyses show that in total, only 24% of Iranian agarics and bolete species have at least one publically available nrITS sequence, while 76% still lack any DNA sequences (Fig. 2d). We also show that 64 species of agarics and boletes in Iran are known from environmental sequences of ectomycorrhizal root tips (Fig. 2e). Moreover, nine species have been recovered as plant endophyte (Fig. 2e).
DISCUSSION
In this study, we presented a first annotated checklist of 585 species of agarics and boletes in Iran. To our current knowledge, perhaps except for Agaricus iranicus which is currently known only from Iran, there is no agaric nor bolete species endemic to the country. Also no lichenized agaric is yet known in Iran. The ITS region has been a favored and practically suitable DNA barcode marker for identification of mushrooms (Dentinger et al. 2011). Here, we obtained 70 new ITS sequences, and have also made a full scrutiny of the sequences of Iranian agarics and boletes available in GenBank and UNITE. We tried to contrast environmental sequences against well-identified fungi or the Species Hypothesis. Selected verified ITS sequences were reported in Table 1. Currently, only 24% of the Iranian agarics and boletes have at least one reliable ITS sequence in the public databases. Application of sequence-based records in checklists and taxonomy studies is not straightforward. The majority of the extracted GenBank/UNITE sequences in our study are from environmental samples (Bahram et al. 2012 and 2013). Many include insufficiently identified sequences or lack vouchered basidiomata. Considering fruitbody-based sequences in GenBank, we also noticed that a perceptible number of them suffer from a wrong interpretation of Basic Local Alignment Search Tool (BLAST), with medium to large ignorance of standards of molecular identification. In most cases, we carefully did a re-BLAST, to correct for the identifications. While sequences from environmental samples are highly important in ecological studies, using them in regional species checklists and taxonomy studies is still not routine. Interestingly, environmental samples (from ectomycorrhizal root tips) added 64 more species to our checklist. Noteworthily, 42% of agaric and bolete species in Iran (248 out of 585 species) arise merely from congress abstracts, with no other supporting data in other sources. Usually, abstracts presented in congresses are intended as informal announcements of scientific research and are not regarded citable by most peer journals. The same also applies to university theses, dissertations, and research reports. Data including biodiversity records in such informal publications are more reliable when they are subsequently supported by other types of evidence and published in peer reviewed journals or other formal publications. We noticed that many of these records lack sufficient characterization, species authority, or vouchers; so, they are considered here as tentative records. We preferred to keep these records in our checklist, to encourage more research on them, but recommend them to be used with caution. In the present work, we were able to confirm the presence of some of the previously recorded species by new specimens or by DNA sequences. Recent studies highlight that climate change will be a serious threat for biodiversity in Iran due to severe habitat fragmentation and destruction, and land-use alteration, specifically in the North West, West (Zagros), and central parts of Iran (Yousefi et al. 2019). Although no studies have been done to test the impact of climate change on fungi in Iran, the range reductions predicted for some plant species (reviewed by Yousefi et al. 2019) might also affect their associated fungi, more notably ectomycorrhizae and wood-inhabiting macromycetes. It is highly probable that many species will go extinct before they are recorded. In Iran, agaric specialists are rare, while forest decline is intensive, which makes it even more imperative to record the agarics and boletes of the country. Undoubtedly, standard DNA barcodes would promote identification and verification of agarics and boletes in Iran; this would close the gap in the empirical knowledge of these fungi. The above discussed problems of unverifiable literature records in congress abstracts, and the need to increase expertise in fungal molecular identification, are not limited to agarics and boletes but are also affecting other fungal groups in Iran. Tackling these problems would ultimately promote mycology and fungal conservation in Iran. Therefore, general recommendations are given to the mycological society in Iran, to prevent dissemination of low quality and ambiguous species records.
General recommendations:
Conclusions This study provides a preliminary account on 585 species of agarics and boletes in Iran, with about half of them being regarded as tentative records. It fills in some of the gaps in our knowledge of these important groups of macrofungi in Iran and provides a framework for biodiversity and phylogenetic studies. Up to now, no taxonomic monograph/revision studies have been done for Iranian agarics and boletes, and among large species-rich genera in Iran (Fig. 2g), only the genus Agaricus has been taxonomically and phylogenetically studied (Mahdizadeh et al. 2017a, 2017b, 2016). Therefore, for the time being it is difficult to figure out the actual number of species of agarics and boletes in Iran. The Hyrcanian region comprises only ca. 5% of the total area of Iran, yet a large proportion of the Iranian agarics and boletes (79%) come from this region. This pattern is similar for other macrobasidiomycetes of Iran such as aphyllophoroid fungi (Ghobad-Nejhad & Hallenberg 2012). Macrofungi are vital members of forest ecosystems warranting their persistence and conservation. This accentuates the importance of taking immediate habitat protection strategies in the narrow, fragile Hyrcanian forests of Iran.
ACKNOWLEDGEMENTS
The authors thank Else C. Vellinga (Berkeley, USA) for providing comments and input in the use of names of taxa. Jacob Heilmann-Clausen (Copenhagen, Denmark) is thanked for some taxonomic notes and suggestions. Mohammad Sohrabi (Tehran, Iran) is gratefully acknowledged for field surveys accompany. This work has been supported by the Center for International Scientific Studies & Collaboration (CISSC), Ministry of Science, Research and Technology. | ||
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