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3 Sampling localities for Tulasnella spp., extracted from literature. Tulasnelloid associates with liverworts are marked with green dots. Orchid mycorrhizae (red dots) summarize isolates of Tulasnella from orchid roots and molecularly identified samples. Tulasnelloid ectomycorrhizae are marked with yellow dots. Lignicolous (blue dots) means that basidiomata were collected on wood
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Species of Tulasnellaceae share the unique feature of tulasnelloid basidia, characterised by swollen sterigmata. All species have a resupinate inconspicuous or lacking basidiomata. Only three genera are assigned to the family, two of them being monospecific. Here, we treat the species of the genus Tulasnella phylogenetically, ecologically, and biog...
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... This clade contains isolates related to Tulasnella helicospora, representing an early diverging lineage in some other phylogenies of Tulasnellaceae in basal position of the trees [23,72]. So far, T. helicospora was found dominant in the roots of several members of the genus Orchis [57,73], and its distribution in soil has been reported in western and central Europe and South America [73,74]. Recently, Calevo et al. (2020) [73] cultivated a T. helicospora strain from the rare species Orchis patens (GenBank accession No. MT489316, showing 97.9% similarity with our TUL4 strain No. MZ503004) and used it for the successful germination of O. patens and O. provincialis seeds. ...
Many orchid species are endangered due to anthropogenic pressures such as habitat destruction and overharvesting, meanwhile, all orchids rely on orchid mycorrhizal fungi (OMF) for seed germination and seedling growth. Therefore, a better understanding of this intimate association is crucial for orchid conservation. Isolation and identification of OMF remain challenging as many fungi are unculturable. In our study, we tested the efficiency of both culture-dependent and culture-independent methods to describe OMF diversity in multiple temperate orchids and assessed any phylogenetic patterns in cultivability. The culture-dependent method involved the cultivation and identification of single pelotons (intracellular hyphal coils), while the culture-independent method used next-generation sequencing (NGS) to identify root-associated fungal communities. We found that most orchid species were associated with multiple fungi, and the orchid host had a greater impact than locality on the variability in fungal communities. The culture-independent method revealed greater fungal diversity than the culture-dependent one, but despite the lower detection, the isolated fungal strains were the most abundant OMF in adult roots. Additionally, the abundance of NGS reads of cultured OTUs was correlated with the extent of mycorrhizal root colonization in orchid plants. Finally, this limited-scale study tentatively suggests that the cultivability character of OMF may be randomly distributed along the phylogenetic trees of the rhizoctonian families.
... In addition, orchids are known to associate with other fungi (Rasmussen 2002; see articles reviewed in Li et al. 2021), though their mycorrhizal status have not always been confirmed. The Tulasnellaceae have a globally widespread distribution (Dearnaley et al. 2012) and have been found to associate with or form mycorrhizal associations with over 41 genera of orchids (Yukawa et al. 2009;Oberwinkler et al. 2017;Rasmussen et al. 2015;Arifin et al. 2021Arifin et al. , 2022. Some 24 new species of Tulasnella were described in recent years as either associating with or forming mycorrhizal relationships with orchids (Arifin et al. 2022). ...
Orchids (Orchidaceae) are dependent on mycorrhizal fungi for germination and to a varying extent as adult plants. We isolated fungi from wild plants of the critically endangered terrestrial orchid Thelymitra adorata and identified them using a multi-region barcoding approach as two undescribed Tulasnella species, one in each of phylogenetic group II and III (OTU1) of the Tulasnellaceae. Using symbiotic propagation methods, we investigated the role of Tulasnella identity (species and isolate) and age post isolation, on the fungus’s ability and efficacy in germinating T. adorata. The group II isolate did not support germination. Seed germination experiments were conducted using either (i) three different isolates of OTU1, (ii) 4- and 12-week-old fungal cultures (post isolation) of a single isolate of OTU1, and (iii) T. subasymmetrica which is widespread and known to associate with other species of Thelymitra. Culture age and fungal species significantly (P < 0.05) affected the time to germination and percentage of seed germination, with greater and faster germination with 4-week-old cultures. Tulasnella subasymmetrica was able to germinate T. adorata to leaf stage, although at slightly lower germination percentages than OTU1. The ability of T. adorata to germinate with T. subasymmetrica may allow for translocation sites to be considered outside of its native range. Our findings on the age of Tulasnella culture affecting germination may have applications for improving the symbiotic germination success of other orchids. Furthermore, storage of Tulasnella may need to take account of the culture age post-isolation, with storage at − 80 °C as soon as possible recommended, post isolation.
... Tulasnella spp. are among the most common OMF found in the roots of orchids [38]. The main results in this study indicated that long-term greenhouse cultivation might not lead to a complete change of the dominant group of Tulasnella associated with Paphiopedilum spp. ...
Ex situ conservation, an important way to increase the survival and sustainability of endangered species, is widely used in the conservation of endangered orchids. However, long-term ex situ conservation might affect the dominant group of orchid symbiotic fungi, which are crucial for orchid growth and reintroduction. This study investigated the culturable Tulasnella spp. associated with Paphiopedilum orchids after long-term greenhouse cultivation, and identified germination-enhancing isolates. A total of 44 Tulasnella isolates were obtained from the roots of 14 Paphiopedilum spp., and 29 of them were selected for phylogenetic analysis. They clustered mainly with Tulasnella deliquescens, Tulasnella calospora, Tulasnella bifrons, and Tulasnella irregularis, but included two potential new groups. Compared with published uncultured data, most of the isolates were grouped together with the reported types, and the dominant Tulasnella associated with P. armeniacum and P. micranthum could still be isolated after ten years of cultivation, most of which were the first isolation. In vitro symbiotic germination showed that certain root isolates could promote seed germination (e.g., parm152 isolated from P. armeniacum, Php12 from P. hirsutissimum, and prhi68 from P. rhizomatosum). These data indicated that the dominant Tulasnella types colonizing the roots of cultivated Paphiopedilum are stable over time, and germination-enhancing fungi colonizing the roots would benefit for seed reproduction after population reintroduction into the wild.
... In orchids, mycorrhizal fungi form coiled-intracellular complexes, known as pelotons, in the root cortical cells (Peterson and Massicotte, 2004;Smith and Read, 2008;Sisti et al., 2019;Li et al., 2021). Photosynthetic terrestrial orchids most commonly associate with three main groups of orchid mycorrhizal fungi (OMF; Smith and Read 2008); Serendipitaceae (formerly Sebacinales Group B) (Weib et al., 2016), Tulasnellaceae (Warcup, 1971(Warcup, , 1973Oberwinkler et al., 2017), and Ceratobasidiaceae (Warcup, 1981;Dearnaley, 2007). Members of these fungal families are typically saprotrophic (Roberts, 1999), or less frequently ectomycorrhizal with non-orchids (Bidartondo et al., 2004;Solís et al., 2017), and are not dependent on the orchid for survival. ...
While many Australian terrestrial orchids have highly specialized mycorrhizal associations, we tested the hypothesis that the geographically widespread orchid genus Cryptostylis associates with a diversity of fungal species. We investigated the mycorrhizal associations of five Australian Cryptostylis species (27 sites sampled) and included limited sampling from three Asiatic Cryptostylis species (two sites), using fungal isolation and molecular approaches. Like related orchid genera, Tulasnellaceae formed the main fungal associations of the Cryptostylis species we sampled, although some ectomycorrhizal, ericoid and saprotrophic fungi were detected infrequently. Each species of Australian Cryptostylis associated with three to seven Tulasnella Operational Taxonomic Units (OTUs), except for C. hunteriana where only one Tulasnella OTU was detected. In total, eleven Tulasnella OTUs associated with Australian Cryptostylis. The Asiatic Cryptostylis associated with four different Tulasnella OTUs belonging to the same lineage as the Australian species. While five Tulasnella OTUs (T. australiensis, T. prima, T. warcupii, T. densa, and T. punctata) were used by multiple species of Australian Cryptostylis, the most commonly used OTU differed between orchid species. The association with different Tulasnella fungi by Cryptostylis species co-occurring at the same site suggests that in any given environmental condition, Cryptostylis species may intrinsically favour different fungal OTUs.
... Previously, asexual forms of Tulasnella were placed in Epulorhiza R.T. Moore (Moore 1987); however, based on the concept "one fungus, one name" (Hawksworth 2011), Epulorhiza is now treated as a synonym of Tulasnella (Stalpers et al. 2021). Species of Tulasnella have been isolated from orchids around the world and have been found to form mycorrhizal associations with over 40 orchid genera (Oberwinkler et al. 2017;Rasmussen et al. 2015;Yukawa et al. 2009). Species of Tulasnella can: form associations with liverworts in the Aneuraceae (Kottke et al. 2008;Krause et al. 2011;Preußing et al. 2010); grow as saprotrophs in decayed wood (Cruz et al. 2014;Mack et al. 2021;Roberts 1992Roberts , 1993; and play an important role as ectomycorrhizal fungi of forest trees (Bidartondo et al. 2004;Solís et al. 2017;Tedersoo et al. 2010). ...
Tulasnella (Tulasnellaceae) is a genus of fungus that can form mycorrhizal associations with orchids (Orchidaceae). Here we used molecular phylogenetic analyses and morphological characteristics of pure cultures across four different media to support the description of five new Tulasnella species associated with commonly occurring and endangered Australian orchids. Tulasnella nerrigaensis associates with Calochilus; T. subasymmetrica and T. kiataensis with Thelymitra; and T. korungensis and T. multinucleata with Pyrorchis and Rimacola respectively. The newly described species were primarily delimited by analyses of five loci: nuc rDNA internal transcribed spacer region ITS1-5.8S-ITS2 (ITS), C14436 (adenosine triphosphate [ATP] synthase), C4102 (glutamate synthase), C3304 (ATP helicase), and mt large subunit 16S rDNA (mtLSU). Tulasnella subasymmetrica is introduced for some isolates previously identified as T. asymmetrica, and this latter species is characterized from multilocus sequencing of a new isolate that matches ITS sequences from the ex-type culture. Morphological differences between the new species are slight. Tulasnella multinucleata has 6-12 nuclei per hyphal compartment which is the first instance of multinucleate rather than binucleate or trinucleate hyphal compartments in Tulasnella. The formal description of these species of Tulasnella will aid in future evolutionary and ecological studies of orchid-fungal interactions.
... Tulasnella species form mycorrhizae with several types of plants, especially several genera of orchids (Currah et al. 1997, Dearnaley et al. 2012, Almeida et al. 2014, Linde et al. 2017, Oberwinkler et al. 2017, Fujimori et al. 2019, Arifin et al. 2020, and liverworts (Preußing et al. 2009). Using mito 28S, Almeida et al. (2014) showed that the species formerly included in the asexual genus Epulorhiza, namely T. amonilioides, T. epiphytica, T. albertaensis and T. anaticula, do not form their own distinct clade, but are distributed across Tulasnella. ...
The taxonomy of the genus Hormomyces, typified by Hormomyces aurantiacus, which based on circumstantial evidence was long assumed to be the hyphomycetous asexual morph of Tremella mesenterica (Tremellales, Tremellomycetes) or occasionally Dacrymyces (Dacrymycetales, Dacrymycetes), is revised. Phylogenies based on the three nuc rDNA markers [internal transcribed spacers (ITS), 28S large ribosomal subunit nrDNA (28S) and 18S small ribosomal subunit nrDNA (18S)], based on cultures from Canada and the United States, suggest that the genus is synonymous with Tulasnella (Cantharellales, Agaricomycetes) rather than Tremella or Dacrymyces. Morphological studies of 38 fungarium specimens of Hormomyces, including the type specimens of H. callorioides, H. fragiformis, H. paridiphilus and H. peniophorae and examination of the protologues of H. abieticola, H. aurantiacus and H. pezizoideus suggest that H. callorioides and H. fragiformis are conspecific with H. aurantiacus while the remaining species are unlikely to be related to Tulasnella. The conidial chains produced by H. aurantiacus are similar to monilioid cells of asexual morphs of Tulasnella species formerly referred to the genus Epulorhiza. The new combination Tulasnella aurantiaca is proposed and the species is redescribed, illustrated and compared with similar fungi. The ecological niche of T. aurantiaca and its possible relationship to orchid root endophytes is discussed. A key to asexual genera with similar conidium ontogeny to T. aurantiaca is provided.
Citation: Mack J, Assabgui RA, Seifert KA (2021). Taxonomy and phylogeny of the basidiomycetous hyphomycete genus Hormomyces. Fungal Systematics and Evolution 7: 177–196. doi: 10.3114/fuse.2021.07.09
... Despite extensive research on the diversity of OMF colonizing orchid roots, their spatial distribution and abundance in soil has received more limited attention. Several reports suggest that OMF either exist in saprophytic form in the soil or form ECM or endophytic colonization on adjacent plants Dearnaley et al., 2012;van der Heijden et al., 2015;Oberwinkler et al., 2017); however, the distribution of OMF in soil remains unclear . Analyzing and understanding this is vital for restoring the populations of endangered orchids and for artificially-assisted colonization. ...
Orchids form mycorrhizal symbioses with fungi in natural habitats that affect their seed germination, protocorm growth, and adult nutrition. An increasing number of studies indicates how orchids gain mineral nutrients and sometime even organic compounds from interactions with orchid mycorrhizal fungi (OMF). Thus, OMF exhibit a high diversity and play a key role in the life cycle of orchids. In recent years, the high-throughput molecular identification of fungi has broadly extended our understanding of OMF diversity, revealing it to be a dynamic outcome co-regulated by environmental filtering, dispersal restrictions, spatiotemporal scales, biogeographic history, as well as the distribution, selection, and phylogenetic spectrum width of host orchids. Most of the results show congruent emerging patterns. Although it is still difficult to extend them to all orchid species or geographical areas, to a certain extent they follow the “everything is everywhere, but the environment selects” rule. This review provides an extensive understanding of the diversity and ecological dynamics of orchid-fungal association. Moreover, it promotes the conservation of resources and the regeneration of rare or endangered orchids. We provide a comprehensive overview, systematically describing six fields of research on orchid-fungal diversity: the research methods of orchid-fungal interactions, the primer selection in high-throughput sequencing, the fungal diversity and specificity in orchids, the difference and adaptability of OMF in different habitats, the comparison of OMF in orchid roots and soil, and the spatiotemporal variation patterns of OMF. Further, we highlight certain shortcomings of current research methodologies and propose perspectives for future studies. This review emphasizes the need for more information on the four main ecological processes: dispersal, selection, ecological drift, and diversification, as well as their interactions, in the study of orchid-fungal interactions and OMF community structure.
... Tulasnella species occur worldwide as free-living saprotrophs in decayed wood (Roberts 1994;Cruz et al. 2011), as mycobionts in orchids (Warcup 1981;Rasmussen and Rasmussen 2009) and liverworts (Kottke et al. 2008), and as ectomycorrhizal associates of the nonphotosynthetic liverwort Cryptothallus mirabilis (Bidartondo et al. 2003). The asexual (anamorph) form was previously named Epulorhiza R.T. Moore (Moore 1987;Oberwinkler et al. 2017). However, based on the concept "one fungus, one name," the separate anamorph nomenclature was discontinued (Hawksworth 2011). ...
Many orchids have an obligate relationship with Tulasnella mycorrhizal fungi for seed germination and support into adulthood. Despite the importance of Tulasnella as mycorrhizal partners, many species remain undescribed. Here, we use multiple sequence locus phylogenetic analyses to delimit and describe six new Tulasnella species associated with Australian terrestrial orchids from the subtribes Cryptostylidinae and Drakaeinae. Five of the new species, Tulasnella australiensis, T. occidentalis, T. punctata, T. densa, and T. concentrica, all associate with Cryptostylis (Cryptostylidinae), whereas T. rosea associates with Spiculaea ciliata (Drakaeinae). Isolates representing T. australiensis were previously also reported in association with Arthrochilus (Drakaeinae). All newly described Tulasnella species were delimited by phylogenetic analyses of four loci (nuc rDNA internal transcribed spacer region ITS1-5.8S-ITS2 [ITS], C14436 [ATP synthase], C4102 [glutamate synthase], and mt 16S rDNA [mtLSU]). The pairwise sequence divergence between species for the ITS region ranged from 5.6% to 25.2%, and the maximum sequence divergence within the newly described species ranged from 1.64% to 4.97%. There was a gap in the distribution of within- and between-species pairwise divergences in the region of 4–6%, with only one within-species value of 4.97% (for two T. australiensis isolates) and one between-species value of 5.6% (involving an isolate of T. occidentalis) falling within this region. Based on fluorescence staining, all six new Tulasnella species are binucleate and have septate, cylindrical hyphae. There was some subtle variation in culture morphology, but colony diameter as measured on 3MN+vitamin medium after 6 wk of growth did not differ among species. However, T. australiensis grew significantly (P < 0.02) slower than others on ½ FIM and ¼ potato dextrose agar (PDA) media. Formal description of these Tulasnella species contributes significantly to documentation of Tulasnella diversity and provides names and delimitations to underpin further research on the fungi and their relationships with orchids.
... In fact, soil fungal communities including, but not limited to, mycorrhizae are known to fluctuate in response to vegetation management such as prescribed fires and grazing (Lauber et al., 2008;V alyi et al., 2015;Egidi et al., 2016;Dove and Hart, 2017;Kyaschenko et al., 2017). And while the edaphic characteristics can also change in response to ecosystem management practices, it is not clear if, or how, they may affect biogeographical patterns in soil microbial or mycorrhizal communities (Lauber et al., 2008;Oberwinkler et al., 2017). Regardless, diversity patterns of OMF in most habitats, including the grasslands of North America, are not known despite the uniqueness, rarity, and high biodiversity of many such ecosystems. ...
The Orchidaceae are globally distributed and represent a diverse lineage of obligate mycotrophic plants. Given their dependence on symbiotic fungi for germination and/or plant development, fungal community structure in substrates is expected to influence the distribution and persistence of orchid species. Yet, simultaneous characterization of orchid mycorrhizal fungal (OMF) communities in roots and in soil is rarely reported. To explain the co-distributions of OMF in roots, orchid-occupied, and bulk soil, we characterized mycorrhizal fungi associated with Platanthera praeclara over multiple years across its entire natural distribution within the North American tallgrass prairie. Root derived OMF communities included 24 Ceratobasidiaceae and 7 Tulasnellaceae operational taxonomic units (OTUs) though the orchid exhibited high spatio-temporal specificity toward a single Ceratobasidiaceae OTU, which was strongly stable across population sizes and phenological stages of the sampled individuals. The preferred OMF OTUs were primarily restricted to orchid-occupied locations while infrequent or absent in bulk soil. Variation in soil OMF assemblies was explained most by soil moisture, magnesium, manganese, and clay. In this first study of coupled root and soil OMF communities across a threatened grassland ecosystem, we report a strong relationship, further nuanced by soil chemistry, between a rare fungus and a rare orchid.
... Tulasnellales seems to be the main order associated with terrestrial orchids (Ogura-Tsujita et al. 2012). They are often fungal associates of several orchids and live in the photosynthetic roots of some epiphytic orchids or in the underground organs of terrestrial orchids (Jacquemyn et al. 2017;Oberwinkler et al. 2017). ...
In order to confront the constant decline in global biological diversity, amelioration strategies are needed for threatened species to design reintroduction policies, particularly in plants with critical reproduction steps, such as orchids. Orchids are part of a highly diverse plant family, with several species under imminent extinction risk. This is the case of Chilean Orchidaceae, which has shown a constant decay in their populations due to an increase in the alteration processes of their natural distribution habitats. Successful orchid reintroductions require a full understanding of orchid mycorrhizal fungi and their dynamic according to different developmental stages and environmental conditions because orchid seeds need mycorrhizal fungi to obtain nutritional compounds at early developmental stages. This article performed a critical literature review of the ecological studies conducted on Chilean orchids and their relationships with mycorrhizal fungi in order to focus on the best scientific approach to achieve successful restoration programs involving orchid seeds and compatible mycorrhizal fungi.
