Abstract
Hysterangium basidiomata were collected associated with Coccoloba alnifolia and C. laevis (Polygonaceae), in the Guaribas Biological Reserve in the Atlantic rainforest, of northeastern Brazil during the rainy seasons of 2012–2013. Based on its unique morphological and molecular traits, this new taxon is described as Hysterangium atlanticum sp. nov. The most prominent morphological characters that separate H. atlanticum from other close relatives are the large size of the basidiomata, the white peridium that rapidly turns greyish-orange to pale-red where bruised or exposed to air, and the ellipsoid to suboblong spores with a minutely verrucose surface. Molecular analyses of the LSU, SSU, atp6, and EF-1α markers were done. The analyses of the concatenated atp6–EF-1α matrix confirmed the placement of the new species in the /hysterangium lineage. Moreover, at the infra-generic level, Hysterangium atlanticum sp. nov. forms a sister clade with Hysterangium sp. from Dicymbe forests located in neighboring Guyana. Moreover, the ectomycorrhizae (EcM) formed by H. atlanticum and roots of Coccoloba species was confirmed, based on identical ITS nrDNA sequences obtained from basidiomata and EcM root tissues. The main conspicuous features of the EcM are: a well-developed plectenchimatous mantle, the ramarioid, abundant emanating hyphae with clamps and covered with crystals, the presence of oleoacanthocystidia, and the whitish rhizomorphs. This is the first report of a Hysterangium species forming EcM with native members of Coccoloba spp. in South America.
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1 Introduction
Ectomycorrhizal (EcM) fungal associations have been for long time considered unusual in the tropics (Alexander 1989; Béreau et al. 1997). Historically, they were though to be restricted to temperate and boreal regions of the world. In contrast, the more recent literature have shown that various tropical and subtropical tree species form ECM associations with a wide range of plant families, including Dipterocarpaceae, Fabaceae (Caesalpinioideae and Faboideae), Fagaceae, Gnetaceae, Nyctaginaceae, Polygonaceae and Sapotaceae (Moyersoen et al. 1998; Henkel et al. 2012; Smith et al. 2013; Moyersoen and Weiß 2014; Roy et al. 2017; Corrales et al. 2018).
The genus Hysterangium Vittad. belongs to the Hysterangiaceae E. Fisch., in the order Hysterangiales, subclass Phallomycetidae (Hosaka et al. 2006). The genus harbors over 50 species, all forming hypogeous sporocarps, diagnosed by the enclosed basidiomata, an irregularly developed columella, a cartilaginous gleba, and narrowly ellipsoid or fusoid, smooth to rugose basidiospores, covered by a membranous utricle or perisporium (Kirk et al. 2008). Hysterangium is a globally distributed genus known to form EcM with Fagaceae, Myrtaceae, Nothofagaceae and Pinaceae (Beaton et al. 1985; Castellano 1999; Hosaka et al. 2008).
EcM symbiosis also influence plant productivity and plant diversity, and connect plants below ground via a hyphal network, allowing the movement of resources among coexisting plants (van der Heijden et al. 2015). Species of Hysterangium are hyphal-mat-forming fungi (Agerer 2001) and have the capacity to modify soil chemistry and microbial biomass (Griffiths et al. 1994; Entry et al. 1992; Trappe et al. 2012), playing an important role in the cycling of nutrients, water uptake and also in soil stabilization of forest ecosystems (Entry et al. 1991, 1992; Trappe et al. 2012).
This genus is widely distributed in both the Northern and Southern Hemispheres, with characteristic discrete host ranges (Castellano 1999). The most comprehensive revision of the genus Hysterangium diversity in South America was conducted by Castellano and Muchovej (1996). In that study, four new species associated with Eucalyptus and Nothofagus were described; furthermore, Hallingea Castellano, a new genus related to Hysterangium and exclusively found in South America, was proposed. Currently, based on DNA analysis and intensive sampling of unexplored areas, new species of Hysterangium from various world regions have been described (Xu and Liu 2003; Hosaka et al. 2007; Guerrero et al. 2008; Elliott et al. 2015).
Despite its global distribution, the genus is poorly known in the neotropics and subtropics. In Brazil, only a few records of Hysterangium species are available, primarily from introduced eucalypt and pine plantations. Among them, H. australe Speg. (Rick 1961), H. gardneri E. Fisch. (Giachini et al. 2000), H. affine Massee & Rodway and H. inflatum Rodway (Cortez et al. 2011). Hysterangium thaxteri Zeller & Dodge, also reported for Brazil by Zeller and Dodge (1929) is currently considered a member of the genus Gelopellis Zeller.
This study reports morphological and molecular characteristics of a novel species of Hysterangium associated to Coccoloba (Polygonaceae) in northeast Brazil. In addition, the morpho-anatomical description of the EcM and the ITS nrDNA sequences analyses of DNA extracted from basidiomata, and from root mantle confirmed its mycorrhizal status and its associtation with Coccoloba.
2 Material and methods
Specimens were collected during the rainy season, from July to September 2012 and in June 2013, at the Guaribas Biological Reserve, 6°44′14”S, 35°8′55”W. This area is located in the State of Paraíba, Brazil, covering 4029 ha of the Atlantic rainforest. The vegetation ranges from lowland semi-deciduous forest to savannas. The forests contain primarily members of the families Fabaceae, Melastomataceae, Myrtaceae, Nyctaginaceae, Rubiaceae, Polygonaceae Cyperaceae and Poaceae (Barbosa et al. 2011). Soils are Tertiary sediments of the “Barreiras” formation (Barbosa et al. 2011) the topsoil is sandy, composed mainly of marine quartz sand (Quartzarenic Neosoil).
Fresh basidiomata were collected randomly by raking the litter and topsoil organic layer among the native vegetation, as described by Castellano et al. (2004). After analysis, basidiomata were dried in a forced air dryer at 40 °C for further preservation.
Firstly, coarse roots from Coccoloba were traced from the stem into the area of fruiting sporocarps and marked. Subsequently a soil core for EcM analyses was taken from a single plot in June of 2013 directly from under the basidiomata (Sulzbacher 455 – UFRN-fungos 1750). The soil sample including humus layer and mineral soil of 15 × 15 cm and 5 cm deep was collected, following Suz et al. (2008).
2.1 Morphological analyses
Collections were photographed in situ. Informative macro and micro characters were observed with the aid of a dissecting microscope (EZ4 Leica), and photographed using light microscopy at ×40–×100 (Eclipse Ni Nikon and digital camera DS-Ri1 Nikon). Spores were studied by scanning electron microscopy (XL30-ESEM Phillips). Line drawings of the microstructures were made with the aid of a drawing tube attached to the microscope (BX41 Olympus), with 100X magnifications. The basidiospore were measured as proposed by Tulloss et al. (1992) and based on 30 mature spores. Abbreviations include: L(W) = average basidiospore length (width), Q = the length to width ratio range as determined from all measured basidiospores, and Qm = the Q value averaged from all measured basidiospores. Basidiomata coloration was registered from fresh material; color codes followed Kornerup and Wanscher (1978). Vouchers were deposited at the Universidade Federal do Rio Grande do Norte Herbarium, Natal, Rio Grande do Norte, Brazil (UFRN), with duplicate material deposited in Father Camille Torrend Herbarium, Recife, Pernambuco, Brazil (URM).
EcM root tips were carefully washed and separated from the soil sample with tap water. Morphological analyses of fresh EcM tips followed Agerer (1991), under a dissecting microscope (EZ4 Leica) and light microscopy at magnifications of 40X–100X (Eclipse Ni Nikon) and photographed with a microscopy digital camera (DS-Ri1 Nikon). Line drawings of the microstructures were made using a drawing tube attached to the microscope (BX41 Olympus) at 100X magnification.
2.2 DNA extraction, amplification and sequencing
Total fungal DNA from gleba and EcM root tips tissue (5–15 tips per three samples) were extracted using DNeasy Plant Mini Kit (Qiagen, Hilden, Germany) following the manufacturer’s instructions. Extracted DNA was re-suspended in pre-warmed, sterile milli-Q water to the approximate final concentration of 100 ng μl−1and kept at −80 °C.
Four nuclear or mitochondrial markers were amplified for basidiomata: complete nuc-ITS-rDNA spacer (ITS), partial nuc-LSU-rDNA, partial atp6, and partial EF-1α, using primer pairs ITS1/ITS4 (White et al. 1990), NS1/NS4 (White et al. 1990), ATP6-2F/ATP6-3R (Kretzer and Bruns 1999) and rEF1-983F/rEF1-1953R (Rehner and Buckley 2005), respectively. For the fungal DNA isolated from EcM only the ITS marker was amplified. PCR reactions were performed as follows: 1.0 μl DNA; 2.5 μl PCR buffer 10×; 3.0 μl dNTPs (1.5 mM); 2.0 μl MgCl2 (20 mM); 3.0 μl of each primer (25 pmol); 0.5 U Taq polymerase (5 U μl−1); and 10.5 μl ultrapure water. PCR conditions followed previously published protocols for selected primers (ibid.) and modified for amplification of ITS (Sulzbacher et al. 2016). Amplifications were done in a GeneAmp® PCR System 9700 thermal cycler (Applied Biosystems, Foster City, CA, USA). Prior to sequencing, PCR products were purified from agarose gel using the Wizard SV Genomic DNA Purification System (Promega Corporation, Madison, WI, USA). Both strands were sequenced separately at Macrogen Korea (Seoul, Korea) with the same primers used in the amplification. Sequencher 5.1 (Gene Codes Corporations, Ann Arbor, MI, USA) was used to assemble the consensus sequence from the two strands of each isolate.
2.3 Molecular analyses
The new sequences generated were compared to those available at GenBank (Altschul et al. 1997); the accession numbers are indicated in Tables S1 and S2. Two datasets were aligned in Mafft v6.859b (Katoh et al. 2005) using a default alignment approach.
To assess the phylogenetic position of the new species, concatenated partial atp6 and EF-1α sequences from GenBank were included (Table S1), mainly from Hosaka et al. (2008); Phallus hadriani and Ramaria flavobrunnescens were used as outgroups (ibid.). Analyses were conducted using Maximum Parsimony (MP) and maximum likelihood (ML). The Maximum Parsimony (MP) phylogenetic reconstruction with Subtree-Pruning-Regrafting MP search method using all sites, and 1000 bootstrap repetitions (MPbs); while for Maximum Likelihood (ML), the General Time Reversible with a discrete Gamma distribution, and assuming invariable sites (+I) was selected after ModelTest in MEGA7.0.18 (Kumar et al. 2016), and 1000 bootstrap repetitions (MLbs), with a partial deletion of gaps/missing data (95% site coverage cutoff).
For the molecular identification of the EcM in the second dataset, ITS nrDNA sequences from basidiomes of the new species, and from the EcM of Coccoloba species were compared with partial homologous sequences belonging to genus Hysterangium retrieved from GenBank on January 15, 2018 (Table S2); Gallacea spp. were included as outgroup (Giachini et al. 2010). The MP analysis was done using the same parameters as mentioned above, and the ML analysis with the Tamura-2-parameter substitution model with a discrete Gamma distribution of sites, as selected by ModelTest; 1000 bootstrap repeats were run with complete selection of data to MP and ML analyses.
All phylogenetic analyses were run in MEGA7.0.18. Phylogenetic trees were drawn and annotated in the same software and subsequently edited in Inkscape 0.91.
3 Results
3.1 Molecular analyses
For reconstruction of the Hysterangiales phylogeny and taxonomic positioning of the new hypogeous species, LSU and complete ITS sequences were not included in the analysis because LSU sequences were poorly represented in nucleotide databases for a relevant analysis, and the complete ITS region was too heterogeneous within Hysterangiales to be aligned with confidence. As a result, a concatenated dataset (atp6/EF-1α) was prepared. The matrix contained 108 taxa (Table S1) and 1314 positions. The Maximum Parsimony (data not shown) and Maximum Likelihood analyses (Fig. 1) resulted in trees with similar topologies, where the new species forms a well-supported terminal clade (MPbs = 88; MLbs = 88), sister group to three sequences of Hysterangium sp., e.g.: SM10007 (DQ218869), SM10166 (DQ218871), and SM10100 (DQ218870). The latter sequences were collected in tropical forest of Guyana (Hosaka et al. 2008). All these sequences form the sister group of three Hysterangium sp.: Hysterangium sp. H5573 (DQ218863), Hysterangium sp. T17501 (DQ218841), and Hysterangium sp. T13345 (DQ218872), all from Asia (Hosaka et al. 2008).
In the second dataset, the ITS matrix contained 51 taxa and 609 positions. Sequences from the basidiomata of H. atlanticum sp. nov. (ITS sequence GenBank LT623204; LT623205; LT623206), and from EcM rootips of Coccoloba (ITS sequence GenBank LT623207; LT623208; LT623209; LT623210) were identical (Fig. 2); thus, the identity of H. atlanticum sp. nov. as the fungal symbiont of the EcM rootips collected was confirmed.
3.2 Taxonomy
Hysterangium atlanticum Sulzbacher, Grebenc, Baseia et Nouhra, sp. nov.
MycoBank MB 817856.
Diagnosis – The combination of basidiomes up to 25 mm in diam., the white peridium that rapidly turns greyish orange to pale red where bruised or exposed to air, basidiospores 11–15 × 5–7 μm, ellipsoid, utricle present, are the main features that characterize this species growing under Coccoloba spp.
Holotype – BRAZIL. Paraíba. Mamanguape, Guaribas Biological Reserve, under Coccoloba, 27 Jul 2012, leg. Sulzbacher 412 (UFRN-Fungos 2115 holotype! URM 88220 isotype!; ITS sequence GenBank LT623204; LT623205; LT623206, atp6 sequence Number LT635647; LT635648, EF-1α sequence LT635645; LT635646).
Etymology – The epithet refers to the Atlantic rainforest type of habitat.
Description – Basidiomata (4–7) 11–25 mm diam., (3–6) 8–19 mm high, globose to somewhat depressed, reniform, with a distinct rhizomorphic base (Fig. 3b). Peridium <1 mm thick, white (1A1) to yellowish white (1A2), yellowish grey (2B2), rapidly turns greyish orange (6B3) to reddish grey (7B2) or pale red (9A3) where bruised or exposed to air. Peridium surface tomentose under hand lens at immature stages, smooth and glabrous at maturity, covered by scattered to numerous rhizomorphs, roots or debris are frequently attached to the peridium (Fig. 3a, b). Gleba finely loculate, gelatinized, compacted, olive (3F3, 3F8) to olive brown (4F4), with rounded to irregular locules (<1 mm diam.) radially arranged. Columella dendroid and irregular in shape, 1–3 mm wide, 3–7 mm high, distinctly gelatinous, translucent, yellowish grey (3D2), to greyish beige (4C2), arising from a sterile base (Fig. 3c). Rhizomorphs 0.1–1.5 mm diam., white (1A1), yellowish grey (3B2) to greyish yellow (4B3), short and numerous going into the ground, at the base of the basidiomata. – Microscopic characters: Rhizomorphs 2–4 μm diam., constituted by hyaline, thin-walled hyphae, ramified and frequently encrusted by irregular shaped crystals 2–4.5 μm diam., which dissolve in 5% KOH (Fig. 5a–c), clamps frequent at the septa, with ampullated or inflated hyphal portions (4–8 μm diam.). The hyphae at the core of the rhizomorph are smooth, thick walled (up to 1.5 μm diam.), clamped, with brown contents, 2–3.5 μm diam. (Fig. 5c). Peridium (Fig. 3f, 4a) easily separable from gleba, 2-layered; external layer plectenchymatous (25–50 μm thick) formed by cylindrical yellowish interwoven hyphae 1–5 μm diam., slightly thickened walls, encrusted with crystalline particles, clamp connections present; internal layer (230–307 μm thick) pseudoparenchymatous, composed by subglobose or angular in shape, more or less elongated hyaline hyphae, smooth and thin-walled, 7–20 μm diam., clamp connections present. Tramal plates of 38–140 μm thick, constituted by hyaline, mostly collapsed, subparallel to interwoven hyphae, smooth and thin-walled from 1 to 8 μm diam. (Fig. 3e). Basidioles 21–38 × 3–9 μm, clavate, hyaline. Basidia 28–45 × 6–9 μm, cylindrical to clavate, 1–4 spored, hyaline (Fig. 4c). Basidiospores (10–) 11–15 × 5–7 μm (ornamentation and sterigmal attachment base excluded), L = 13 μm, W = 6 μm, Q = 1.8–2.6, Qm = 2.2; or 13–17 × 5–7 μm (attachment base included), L = 15.2 μm, W = 6.3 μm, Q = (1.8–)1.9–3.0, Qm = 2.4, ellipsoid to suboblong, smooth, apex and base tapered, hyaline in KOH, slightly thickened wall 0.2–1.5(−2) μm thick, with a sterigmal attachment base (up to 3 μm high), utricle present and heavily wrinkled under SEM (Fig. 3g, h).
Ectomycorrhiza description: mycorrhizal root tips simple, monopodial-pinnate to irregularly pinnate, terminal tips of various lengths, the whole EcM system up to 20 mm long, white, the older parts yellowish white; ectomycorrhizae shiny with wooly surface, abundant and with a closed distribution in substrate. – Rhizomorphs abundant, especially in well-developed mycorrhizal systems, shiny, white to whitish, when handled turning ochre, frequently ramified, rhizomorphs connection to mantle oblique and in places not clearly visible (Fig. 3a). – Margin cottony. – Exploration type long distance. – Sclerotia absent. – Morphology of the unramified ends curved to bent, not inflated, tips very straight, white, shiny; older parts ochre to yellowish ochre. – Anatomical characters of mantle in plan views. Mantle not transparent, no latex, no dots, not carbonizing, with a lot of emanating hyphae over all of the surface. – Anatomical characters of the outer mantle layer plectenchymatous (Fig. 6b), inner mantel layers densely plectenchymatous, hyphae of the same diameter (3–5 μm diam.), septate, walls thin to slightly thickened (0.5–1 μm diam.) hyphae from which emanating hyphae and rhizomorphs originate, colorless, crystals on the surface and septa with clamp connections frequent. Matrix absent. Hartig net present. Emanating hyphae present, abundant, all over the mantle, white. – Anatomical characters of emanating elements: Rhizomorphs abundant, not differentiated, thin-walled, clamp connection frequent, no central hyphae observed, very similar to those of basidiomata, ramarioid (Fig. 6a, b), ampullated hyphae frequent (4–8 μm diam.), with open anastomoses; Emanating hyphae present, frequent, smooth, covered by numerous angular, irregular shaped crystals 1.5–5 μm diam., hyaline, cell walls thin, not filled, 3–7 μm diam., septate, septa clamped (Fig. 5d); Cystidia present (oleoacanthocystidia ‘Hysterangium-type’ sensu Agerer 2006), frequently with short lateral outgrowths, roundish cells filled with yellowish or opaque contents, thick walled (0.4–1 μm diam.), (Fig. 5e, f, 6a).
Additional basidiomata examined: BRAZIL. Paraíba. Mamanguape, Guaribas Biological Reserve, SEMA II, 06°44.389′ S, 35°08.386′ W, under Coccoloba alnifolia 27 Jul 2012, leg. Sulzbacher 408 (UFRN-Fungos 2112, URM 88222; paratypes); idem, under Coccoloba sp., 14 Jul 2012, leg. Sulzbacher 396 (UFRN-Fungos 2207; paratype); idem, under Coccoloba laevis, 12 Sep 2012, leg. Sulzbacher 438 (UFRN-Fungos 2205; paratype); idem, under Coccoloba laevis 30 Jul 2013, leg. Sulzbacher 455 (UFRN-Fungos 1750; paratype).
Additional EcM examined: deposited at the Mycotheca and herbarium GIS at the Slovenian Forestry Institute under accession numbers: LJU-SFI-MAS001; LJU-SFI-MAS002; LJU-SFI-MAS003; LJU-SFI-MAS004.
Habitat and distribution: Hypogeous, under organic soil and forest debris, occurring either in large groups (±25 basidiomata was observed per single nest) or in small groups, and/or isolated in sandy soil (Quartzarenic Neosoil), fixed to roots; associated with Coccoloba alnifolia Casar. and C. laevis Casar.; known only from the type locality.
4 Discussion
Hysterangium atlanticum is a newly discovered hypogeous species from the Neotropics in northeastern Brazil. Its habitat is quite unique, since it occurs in coastal sand habitats colonized by ectomycorrhizal Coccoloba alnifolia and C. laevis, among other tropical plant species. Macroscopically, H. atlanticum resembles the description of Montecchi and Sarasini (2000) of the European species H. stoloniferum Tul. & C. Tul., specifically by the size of basidiomata (10–20 mm diam.), its smooth, whitish to reddish peridium and the presence of numerous ramified whitish rhizomorphs connecting other basidiomes. However, H. stoloniferum has larger hyaline spores (19–26 × 6–7 μm), shortly pedicellate at the base, and the peridiopellis is pseudoparenchymatous, composed of hyaline cells, with an external layer formed by prostrate and brownish hyphae, growing under deciduous trees (Quercus spp.), as indicated by Tulasne and Tulasne (1843).
Multi-locus molecular data support the separation of the new species, indicating its close relation to several unnamed Hysterangium species including one from Guyana (Fig. 2).
Based on the morphology, Hysterangium hallingi Castellano & J.J. Muchovej and H. spegazzinii Castellano & J.J. Muchovej, both from southern South America (Argentina, Chile and Uruguay), are similar to H. atlanticum. However, H. hallingi has spore wall thickness of ±1 μm thick, narrower basidiospores (4.5–5.5 μm diam.), and a three-layered peridium (Castellano and Muchovej 1996), and H. spegazzinii presents spores minutely verrucose with walls thinner than 0.5 μm. The only available sequence for H. hallingi out of the two species is significantly different from H. atlanticum (Fig. 1). Moreover, H. hallingi putative EcM host plants are Nothofagus betuloides and N. pumilio, and for H. spegazzinii, Eucalyptus sp. and Nothofagus dombeyi; however, we confirmed that H. atlanticum forms EcM with Coccoloba species in the native Atlantic rainforest. In agreement with Castellano (1988), and considering the EcM host specificity displayed by Hysterangium, the natural geographic distribution of fungi and their hosts is a reliable character for species differentiation and identification in this genus.
Recently, some new Hysterangium species have been found in the Neotropics, associated with native tropical taxa. For example two undescribed Hysterangium species growing on a Dicymbe-dominated forest in the Guyana Shield region (Henkel et al. 2012), as part of an ectomycorrhizal community, previously unknown to occur in those latitudes (Hosaka et al. 2008; Henkel et al. 2010; Castellano et al. 2012). Similarly, our studies showed an undocumented community of EcM fungi, including some hypogeous taxa, co-occurring in native fragments of the Atlantic rainforest in northeast Brazil (Sulzbacher et al. 2013; Sulzbacher et al. 2016; Sulzbacher et al. 2017). It is possible that this ectotrophic sand dune forest along the Brazilian Atlantic coast is home for a unique community of EcM taxa (Menolli et al. 2009; Gurgel et al. 2008; Pinheiro and Wartchow 2013; Sá et al. 2013; Wartchow et al. 2015). However, tropical forest types in northeast Brazil do not have EcM tree hosts such as Aldina (Benth.) Endl. and Dicymbe Spruce ex Benth. (Freire 1990; Oliveira-Filho and Carvalho 1993; Barbosa et al. 2011); instead, as shown in this work, the putative EcM partners are represented by trees species in the Polygonaceae (e.g. Coccoloba spp.), and likely also in the Fabaceae (Caesalpinioideae), Nyctaginaceae (Guapira spp.), which are confirmed EcM genera (Smith and Read 2008; Tedersoo et al. 2010; Põlme et al. 2017; Séne et al. 2018).
The EcM status for the Hysterangiales members has not been investigated for all taxa (Hosaka et al. 2006); however, in Hysterangium, the symbiosis was described for Hysterangium crassirhachis Zeller & C. W. Dodge and H. stoloniferum, based on morpho-anatomical studies (Agerer and Iosifidou 2004; Agerer and Rambold 2004–2017; Agerer 2006). The most prominent difference of H. atlanticum compared to other Hysterangium ectomcorrhizae is the unique presence of oleoacanthocystidia and rhizomorphs which are cottony and not differentiated, compared to slightly differentiated rhizomorphs with central hypha present in H. stoloniferum (Raidl and Agerer 1998), and a combination of slightly differentiated and undifferentiated rhizomorphs in H. crassirhachis (Müller and Agerer 1996).
The description of Hysterangium atlanticum sp. nov. and its ectomycorrhizae is a new contribution unveiling a fungal community of the Atlantic rainforest biodiversity hotspot area. The Atlantic rainforest spans a considerable area in Brazil and the ectomycorrhizal fungal diversity is just starting to be discovered.
References
Agerer R (1991) Characterization of ectomycorrhiza. In: Norris JR, Read DJ, Varma AK (eds) Techniques for the study of mycorrhiza. (methods in microbiology, vol 23). Academic, London, pp 25–73
Agerer R (2001) Exploration types of mycorrhizae - a proposal to classify ectomycorrhizal mycelia systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11:107–114. https://doi.org/10.1007/s005720100108
Agerer R (2006) Fungal relationships and structural identity of their ectomycorrhizae. Mycol Prog 5:67–107. https://doi.org/10.1007/s11557-006-0505-x
Agerer R, Iosifidou P (2004) Rhizomorph structure of Hymenomycetes: a possibility to test DNA-based phylogenetic hypotheses. In: Agerer R, Piepenbring M, Blanz P (eds) Frontiers inbasidiomycote mycology. IHW, Eching, pp 249–302
Agerer R, Rambold G (2004–2017) DEEMY—an information system for characterization and determination of ectomycorrhizae. München, Germany. http://www.deemy.de. Accessed 20 May 2017
Alexander IJ (1989) Mycorrhizas in tropical forests. In: Proctor J (ed) Mineral nutrients in tropical forest and savanna ecosystems. Blackwell Scientific Publications, Oxford, pp 169–188
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 http://nar.oxfordjournals.org/content/25/17/3389.long. Accessed 10 July 2017
Barbosa MRB, Thomas WW, Zárate ELP, Lima RB, Agra MF, Lima IB, Pessoa MCR. Lourenço AR., Delgado-Junior GD, Pontes RAS, Chagas ECO, Viana JL, Gadelha-Neto PC, Araújo CMR, Freitas GB, Lima JR, Silva FO, Vieira LAF, Costa RMT, Duré RC, Sá MGV (2011) Checklist of the vascular plants of the Guaribas biological reserve, Paraíba, Brazil. 16 rev Nord biol 20:79–106. http://periodicos.ufpb.br/ojs/index.php/revnebio/article/view/11912. Accessed 18 Sep 2017
Beaton G, Pegler DN, Young TWK (1985) Gasteroid Basidiomycota of Victoria state, Australia: 4. Hysterangium. Kew Bull 40:435–444 http://www.jstor.org/stable/4108269. Accessed 10 Aug 2017
Béreau M, Gazel M, Garbaye J (1997) Les symbioses mycorhiziennes des arbres de la forêt tropicale humide de Guyane française. Can J Bot 75:711–716
Castellano MA (1988) The taxonomy of the genus Hysterangium (Basidiomycotina, Hysterangiaceae) with notes on its ecology. PhD. Thesis, Oregon State University, Corvallis, OR. p 238. http://hdl.handle.net/1957/13508. Accessed 09 May 2017
Castellano MA (1999) Hysterangium. In: Cairney JWG, Chambers SM (eds) Ectomycorrhizal fungi: key genera in profile. Springer, Berlin, pp 311–323
Castellano MA, Muchovej JJ (1996) Truffle-like fungi from South America: Hysterangium sensu lato. Mycotaxon 57:329–345
Castellano MA, Trappe JM, Luoma DL (2004) Sequestrate fungi. In: Foster MS, Mueller GM, Bills GF (eds) Biodiversity of fungi: inventory and monitoring methods. Academic Press, Burlington, pp 197–213
Castellano MA, Henkel TW, Miller SL, Smith ME, Aime MC (2012) New Elaphomyces species (Elaphomycetaceae, Eurotiales, Ascomycota) from Guyana. Mycologia 104:1244–1249. https://doi.org/10.3852/12-061
Corrales A, Henkel TW, Smith ME (2018) Ectomycorrhizal associations in the tropics – biogeography, diversity patterns and ecosystem roles. New Phytol 220:1076–1091. https://doi.org/10.1111/nph.15151
Cortez VG, Sulzbacher MA, Baseia IG, Antoniolli ZI, Silveira RMB (2011) New records of Hysterangium (Basidiomycota) in Eucalyptus plantations of South Brazil. Rev Bras Bioc 9:220–223 http://www.ufrgs.br/seerbio/ojs/index.php/rbb/article/view/1661. Accessed 09 Jun 2017
Elliott TF, Trappe JM, Weise A (2015) Australasian sequestrate fungi 19: Hysterangium colossum sp. nov. IMA Fungus 6:115–117. https://doi.org/10.5598/imafungus.2015.06.01.05
Entry J, Rose C, Cromack K (1991) Litter decomposition and nutrient release in ectomycorrhizal mat soils of Douglas-fir ecosystem. Soil Biol Biochem 23:285–290. https://doi.org/10.1016/0038-0717(91)90065-R
Entry J, Rose C, Cromack K (1992) Microbial biomass and nutrient concentration in hyphal mats of the ectomycorrhizal fungus Hysterangium setchellii in a coniferous forest soil. Soil Biol Biochem 24:447–453. https://doi.org/10.1016/0038-0717(92)90207-E
Freire SMB (1990) Levantamento florístico do Parque estadual das dunas de Natal. Acta Bot Bras 4:41–59 https://doi.org/10.1590/S0102-33061990000300006
Giachini AJ, Oliveira VL, Castellano MA, Trappe JM (2000) Ectomycorrhizal fungi in Eucalyptus and Pinus plantations in southern Brazil. Mycologia 92:1166–1177. https://doi.org/10.2307/3761484
Giachini AJ, Hosaka K, Nouhra E, Spatafora J, Trappe JM (2010) Phylogenetic relationships of the Gomphales based on nuc-25S-rDNA, mit-12S-rDNA, and mit-atp6-DNA combined sequences. Fungal Biology 114:224–234
Griffiths RP, Baham J, Caldwell B (1994) Soil solution chemistry of ectomycorrhizal mats in forest soils. Soil Biol Biochem 26:331–337 http://andrewsforest.oregonstate.edu/pubs/pdf/pub1468.pdf
Guerrero GG, Castellano MA, Jiménez JG, González EC, Trappe JM (2008) Hysterangium (Hysterangiales, Hysterangiaceae) del norte de México. Rev Mex Micol 28:95–100 http://www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S0187-31802008000300012. Accessed 05 Jul 2017
Gurgel FE, Silva BDB, Baseia IG (2008) New records of Scleroderma from northeastern Brazil. Mycotaxon 105:399–405
Henkel TW, Smith ME, Aime CM (2010) Guyanagaster, a new wood-decaying sequestrate fungal genus related to Armillaria Agaricales, Basidiomycota. Amer Jour Bot 97:1–11. https://doi.org/10.3732/ajb.1000097
Henkel TW, Aime MC, Chin MML, Miller SL, Vilgalys R, Smith ME (2012) Ectomycorrhizal fungal sporocarp diversity and discovery of new taxa in Dicymbe monodominat forests of the Guiana shield. Biodivers Conserv 21:2195–2220. https://doi.org/10.1007/s10531-011-0166-1
Hosaka K, Bates ST, Beever RE, Castellano MA, Colgan WIII, Domínguez LS, Nouhra ER, Geml J, Giachini AJ, Kenney SR, Simpson NB, Spatafora JW, Trappe JM (2006) Molecular phylogenetics of the gomphoid-phalloid fungi with an establishment of the new subclass Phallomycetidae and two new orders. Mycologia 98:949–959. https://doi.org/10.3852/mycologia.98.6.949
Hosaka K, Castellano MA, Trappe JM (2007) NATS truffle and truffle-like fungi 16: Hysterangium pavelekii sp. nov. (Hysterangiaceae, Basidiomycota). Mycotaxon 93:345–353 https://nature.berkeley.edu/brunslab/papers/grubisha2005c.pdf. Accessed 05 May 2017
Hosaka K, Castellano MA, Spatafora JW (2008) Biogeography of Hysterangiales (Phallomycetidae, Basidiomycota). Mycol Res112: 448–462. doi: https://doi.org/10.1016/j.mycres.2007.06.004
Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518 http://nar.oxfordjournals.org/content/33/2/511.long. Accessed 15 Jun 2017
Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the Fungi.10th edn. CABI, Wallingford, p 771
Kornerup A, Wanscher JE (1978) Methuen handbook of colour, 3rd edn. Methuen, London
Kretzer AM, Bruns TD (1999) Use of atp6 in fungal phylogenetics: an example from the Boletales. Mol Phylogenet Evol 13:483–492 https://nature.berkeley.edu/brunslab/papers/kretzer1999.pdf. Accessed 14 May 2017
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Menolli N, Capelari M, Baseia IG (2009) Amanita viscidolutea, a new species from Brazil with a key to central and south American species of Amanita section Amanita. Mycologia 101:391–396. https://doi.org/10.3852/07-079
Montecchi A, Sarasini M (2000) Fungi ipogei d’Europa. Trento, Italy, Associazione Micologica Bresadola, p 714
Moyersoen B, Weiß M (2014) New Neotropical Sebacinales species from a Pakaraimaea dipterocarpacea Forest in the Guayana region, southern Venezuela: structural diversity and Phylogeography. PLoS ONE 9:e103076. https://doi.org/10.1371/journal.pone.0103076
Moyersoen B, Fitter AH, Alexander IJ (1998) Spatial distribution of ectomycorrhizas and arbuscular mycorrhizas in Korup National Park rain forest, Cameroon, in relation to edaphic parameters. New Phytol 139:311–320
Müller WR, Agerer R (1996) Hysterangium crassirhachis. In: Agerer R (ed) Colour atlas of Ectomycorrhizae, plate 93. Einhorn-Verlag, Schwäbisch Gmünd
Oliveira-Filho AT, Carvalho DA (1993) Florística e fisionomia da vegetação no extremo norte do litoral da Paraíba. Rev Bras Bot 16:115–130 http://prof.icb.ufmg.br/treeatlan/Downloads/a17.pdf. Accessed 10 Jul 2017
Pinheiro FGB, Wartchow F (2013) Cantharellus protectus — a new species from Paraíba, Brazil. Sydowia 65:27–31
Põlme S, Bahram M, Kõljalg U, Tedersoo L (2017) Biogeography and specificity of ectomycorrhizal fungi of Coccoloba uvifera. In: Tedersoo L (ed) Biogeography of mycorrhizal symbiosis. Springer, Berlin, pp 345–359
Raidl S, Agerer R (1998) Hysterangium stoloniferum Tul. & Tul. + Picea abies (L.) Karst. Descr Ectomyc 3:31–35
Rehner SA, Buckley E (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1-a sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97:84–98. https://doi.org/10.3852/mycologia.97.1.84
Rick J (1961) Basidiomycetes Eubasidii in Rio Grande do Sul, Brasilia - 6. Iheringia. Sér Bot 9:451–489
Roy M, Vasco-Palacios A, Geml J, Buyck B, Delgat L, Giachini A, Grebenc T, Harrower E, Kuhar F, Magnago A, Rinaldi AC, Schimann H, Selosse M-A, Sulzbacher MA, Wartchow F, Neves M-A (2017) The (re)discovery of ectomycorrhizal symbioses in Neotropical ecosystems sketched in Florianópolis. New Phytol 214:920–923
Sá MCA, Baseia IG, Wartchow F (2013) Lactifluus dunensis, a new species from Rio Grande do Norte, Brazil. Mycosphere 4:261–264
Séne S, Selosse MA, Forget M, Lambourdière J, Cissél K, Diédhiou AG, Rivera-Ocasio E, Kodja H, Kameyama N, Nara K, Vincenot L, Mansot J-L, Weber J, Roy M, Sylla SN, Bâ A (2018) A pantropically introduced tree is followed by specific ectomycorrhizal symbionts due to pseudo-vertical transmission. The ISME Journal 12:1806–1816
Smith SE, Read DJ (2008) Mycorrhizal Symbiosis. 3 ed. Academic Press, p 800
Smith ME, Henkel TW, Uehling JK, Fremier AK, Clarke HD, Vilgalys R (2013) The ectomycorrhizal fungal community in a neotropical forest dominated by the endemic dipterocarp Pakaraimaea dipterocarpacea. PLoS One 8:e55160. https://doi.org/10.1371/journal.pone.0055160
Sulzbacher MA, Giachini AJ, Grebenc T, Silva BDB, Gurgel FE, Loiola MIB, Neves MA, Baseia IG (2013) A survey of an ectotrophic sand dune forest in the Northeast Brazil. Mycosphere 4:1106–1116. https://doi.org/10.5943/mycosphere/4/6/8
Sulzbacher MA, Grebenc T, Cabral TS, Giachini AJ, Goto BT, Smith ME, Baseia IG (2016) Restingomyces, a new sequestrate genus from the Brazilian Atlantic rainforest that is phylogenetically related to early-diverging taxa in Trappeaceae (Phallales). Mycologia 108:954–966
Sulzbacher MA, Grebenc T, Giachini AJ, Baseia IG, Nouhra ER (2017) Hypogeous sequestrate fungi in South America – how well do we know them? Symbiosis 71:9–17
Suz LM, Azul AM, Morris MH, Bledsoe CS, Martín MP (2008) Morphotyping and molecular methods to characterize ectomycorrhizal roots and hyphae in soil. In: Nautiyal PDCS, Dion PDP (eds) Molecular mechanisms of plant and microbe coexistence soil biology- springer. Berlin, Heidelberg, pp 437–474
Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20:217–263. https://doi.org/10.1007/s00572-009-0274-x
Trappe MJ, Cromack K Jr, Caldwell BA, Griffiths RP, Trappe JM (2012) Diversity of mat-forming fungi in relation to soil properties, disturbance, and forest ecotype at crater lake National Park, Oregon, USA. Diversity 4:196–223. https://doi.org/10.3390/d4020196
Tulasne L-R, Tulasne C (1843) Champignons hypogés de la famille des Lycoperdacées. Annales des Sciences Naturelles Botanique 19:373–381
Tulloss RE, Ovrebo CL, Halling RE (1992) Studies on Amanita (Amanitaceae) from Andean Colombia. Mem New York Bot Gard 66:1–46
van der Heijden MGA, Matin F, Selosse M-A, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423. https://doi.org/10.1111/nph.13288
Wartchow F, Sulzbacher MA, Baseia IG (2015) Amanita psammolimbata, a new species from northeastern Brazilian sand dunes. Mycosphere 6:260–265. https://doi.org/10.5943/mycosphere/6/3/3
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols. A Guide to Methods and Applications. Academic Press, San Diego, CA, pp 315–322
Xu AS, Liu B (2003) A new species in the genus Hysterangium from China. Mycosystema 22:16–18
Zeller SM, Dodge CW (1929) Hysterangium in North America. Ann Mo Bot Gdn 16:83–128
Acknowledgements
We thank to Dr. Reinhard Agerer by his guidance in the studies of ectomycorrhizae and to Dr. Marian Glenn for her kind English revision. This work was supported by CAPES (scholarships No PDSE 99999.004997/2014-00 to the senior author), and also co-financed by the Brazil – Slovenia bilateral project (BI-BR/11-13-005(SRA) / 490648/2010-0 (CNPq)) and the Research Programme Forest Biology, Ecology and Technology (P4-0107) of the Slovenian Research Agency. IGB and MPM thanks to CNPq project PVE 407474/2013-7 and EN CONICET for financial support.
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Sulzbacher, M.A., Grebenc, T., Nouhra, E.R. et al. Hysterangium atlanticum sp. nov., forms ectomycorrhizae with Coccoloba species (Polygonaceae) from the Atlantic rainforest of Northeastern Brazil. Symbiosis 78, 275–286 (2019). https://doi.org/10.1007/s13199-019-00617-3
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DOI: https://doi.org/10.1007/s13199-019-00617-3