Abstract
Jaapia is a wood-saprobic genus of corticioid fungi for which two species have been recognized: J. argillacea Bres. and J. ochroleuca (Bres.) Nannf. & J. Erikss. Whereas the first one is easily recognized by its characteristic spores, the descriptions of the second indicated variable spores, which once led us to believe that J. ochroleuca could be a species complex rather than a single species. Eleven new ITS nrDNA sequences of J. ochroleuca were aligned with two obtained from GenBank and four of J. argillacea. The molecular results, parsimony analysis and KP2 distances clearly delimitate one highly supported Jaapia clade, with two subclades that correspond to the two described species. Morphological studies, including the holotype and isotype of J. ochroleuca, show significant differences between the clades concerning the size and shape of spores. The present study corroborates two species in this genus and also confirms that J. ochroleuca is a well-defined species in which spores show great morphological variability. Based on the Jaapia “species hypothesis”, the J. ochroleuca reference sequence has been selected. A comprehensive key to two Jaapia species is also provided.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Jaapia was described by Bresadola (1911) to accommodate J. argillacea Bres., and for 20 years, this monotypic genus was accepted by several authors (von Höhnel 1912; Wakefield and Pearson 1920; Bourdot and Galzin 1923, 1928; Rogers 1935). Nannfeldt and Eriksson (1953) considered Coniophora ochroleuca Bres. as the second species of Jaapia, and the genus was emended by them as “Fructifications effuse, resupinate, with indefinite margin, whitish or pale yellowish, loose and floccose; hyphae clamped and richly branching; cystidia present; basidia long, slightly sinuous and often constricted with four sterigmata,” and its characteristic spores as: “… relatively large and more or less fusiform, with a very conspicuous, more or less peg-like apiculus; spore-wall at least after detachment becoming thick and two-layered, the inner layer staining strongly with Cotton Blue and Congo Red; in one species (J. argillacea) the inner layer finally surrounds as chlamidospore-like body, which does not fill out the spore completely but leaves an empty space at each (or one) end; in the other species (J. ochroleuca) there is generally no inter-membranal space.”
On the basis of the peculiar morphology of its spores, Jaapia was considered to be closely related to Coniophora DC. (von Höhnel 1912), Pellicularia Cooke (Rogers 1935) or even Coniobotrys Pouzar, a new genus described by Pouzar (1958) with Coniophora ochroleuca as type species. Nannfeldt and Eriksson (1953) and Donk (1964) referred it to Coniophoraceae, and Eriksson and Ryvarden (1976) regarded Jaapia as member of the broad concept of the family Cortiaceae. Larsson (2007), in his phylogenetic classification for corticioid fungi, included it in an “incertae sedis” as Jaapia family. Binder et al. (2010) described the family Jaapiaceae in Jaapiales, an order for the lone genus Jaapia; according to these authors, Jaapiales was supported as the sister group of the remainder of the Agaricomycetidae.
Nowadays, this wood-saprobic fungal genus includes two taxa, Jaapia argillacea and J. ochroleuca (Bres.) Nannf. & J. Erikss. Jaapia argillacea seems to be a rare species with a wide distribution (Nannfeldt and Eriksson 1953); known in Europe from Denmark, France, Germany, Norway, Sweden, and the United Kingdom, (Bresadola 1911; Wakefield and Pearson 1920; Nannfeldt and Eriksson 1953; Chistiansen 1960; Eriksson and Ryvarden 1976; Boidin and Gilles 1990; Legon et al. 2005), as well as USA (Rogers 1935; Nannfeldt and Eriksson 1953; Ginns and Lefebvre 1993), and Canada (Eriksson and Ryvarden 1976; Ginns and Lefebvre 1993). Jaapia ochroleuca is even rarer than J. argillacea (Nannfeldt and Eriksson 1953; Eriksson and Ryvarden 1976), but also seems to be widely distributed. It is known in Europe from Austria, Belgium, Caucasus, Czechoslovakia, Denmark, Estonia, France, Finland, Germany, Italy, Macedonia, Norway, Portugal, Spain, Sweden, Ukraine, and the United Kingdom (Bresadola 1911; Bourdot and Galzin 1928; Rogers 1943; Nannfeldt and Eriksson 1953; Eriksson and Ryvarden 1976; Hjortstam et al. 1981; Dueñas and Telleria 1984; Boidin and Gilles 1990; Melo and Telleria 1991; Legon et al. 2005; Bernicchia and Gorjón 2010) as well as the Azores Archipelago (Telleria et al. 2009). Moreover, it has been reported from America: USA (Rogers 1943; Nannfeldt and Eriksson 1953; Ginns and Lefebvre 1993), Canada (Rogers 1943; Nannfeldt and Eriksson 1953) and Argentina (Gorjón et al. 2012); as well as from Africa, in Kenya (Hjortstam 1987), and Asia, in China (Dai 2011).
Whereas Jaapia argillacea is easily recognized by its characteristic spores narrowly fusiform, 16–25 × 5–7 μm, at first thin-walled but later with a thick and cyanophilous secondary wall, with the ends empty (Eriksson and Ryvarden 1976), the descriptions of the spores of J. ochroleuca show great morphological variability, particularly in spore width and therefore in length/width ratios (Brinkmann 1898; Bourdot and Galzin 1928; Rogers 1943; Nannfeldt and Eriksson 1953; Eriksson and Ryvarden 1976; Boidin and Gilles 1990; Bernicchia and Gorjón 2010) which once led us to believe that J. ochroleuca could be a species complex rather than a single one.
In corticioid fungi, the spore size has been considered to be a useful character with high diagnostic value; such is the case in separating several species pairs, such as Corticium roseum Pers. vs. Corticium meridioroseum Boidin & Lanq. (Boidin and Lanquetin 1983) or Hyphoderma argillaceum (Bres.) Donk vs. Hyphoderma magnargillaceum Boidin & Gilles (Boidin and Gilles 1991) or the species in the genus Vuilleminia (Boidin and Lanquetin 1983; Ghobad-Nejhad et al. 2010) and the genus Hyphodermella (Telleria et al. 2010).
Nevertheless, the delimitation of corticioid species is sometimes difficult, since morphological characters do not always help to distinguish species. Nowadays, molecular data are considered as effective tool for species discrimination and, recently, the ITS region was proposed (Schoch et al. 2012) as the first barcoding for fungi. However, the taxonomic coverage of the International Nucleotide Sequence Databases (INSD: EMBL/GenBank/DDBJ) (Cochrane et al. 2011) needs to be improved (Brock et al. 2009), and only when all described species of fungi are represented on GenBank (currently it has less than 7 % of the circa 1.5 million estimated species), will researchers be able to judge a “known” or “unknown” species. It has also been pointed out (Brock et al. 2009) that the number of insufficiently identified sequences in the INSD, lacking voucher information and named as “environmental unknowns,” has increased greatly within the last 5 years (Kõljag et al. 2013).
For improving the molecular identification of fungi, new tools have been developed in the UNITE database (http://unite.ut.ee), based on a two-tier clustering process on different similarity thresholds (97–99 %); both levels represent molecular operational taxonomic units (MOTUs). The first clustering represents the genus level, and the second represents the species range. Kõljag et al. (2013) introduced the term “species hypothesis” (SH) for the second cluster, and for each SH cluster, a sequence was chosen as a reference sequence.
The aims of this study were to use morphological and molecular data to characterize and identify the voucher specimens under Jaapia argillacea and J. ochroleuca all over the world, as well as to analyze the significance of spore size and shape in the taxonomy of this genus. Also, based on the Jaapia “species hypothesis,” the J. ochroleuca reference sequence was selected.
Materials and methods
Sampling and morphological studies
A total of 40 specimens, five of Jaapia argillacea and 35 of J. ochroleuca, from BIO-Fungi, GB, LISU, MA-Fungi, O, PC, and UPS herbaria were studied, including the holotype (S) and isotype (UPS) of J. ochroleuca (Table 1). Measurements were made from microscopic sections mounted in 3 % aqueous solutions of KOH and examined at magnifications up to 1250× using an Olympus BX51 microscope. The length and width of 30 spores were measured from each sample, and mean values and length/width ratios (Q) were calculated (Table 1). Type specimens of J. ochroleuca were studied in order to compare their spore data with those of the specimens included in this study.
DNA extraction, amplification and sequencing
DNA was isolated from herbarium specimens using the DNeasy™ Plant Mini Kit (Qiagen, Valencia, California, USA), following the instructions of the manufacturers. Lysis buffer incubation was done overnight at 55 °C following Whiting et al. (1997). The primer pair ITS1F and ITS4 was used to obtain amplifications of both ITS regions, including the 5.8S of the ribosomal RNA gene cluster and small flanking parts of the SSU and LSU genes (White et al. 1990; Gardes and Bruns 1993). Amplifications were done using illustra™ PuReTaq™ Ready-To-Go™ PCR beads (GE Healthcare, Buckinghamshire, UK) as described in Winka et al. (1998), following thermal cycling conditions in Martín and Winka (2000). Negative controls lacking fungal DNA were run for each experiment to check for contamination of reagents. Results of amplifications were assayed from 5 μl aliquots by gel electrophoresis of 2 % Pronadisa D-1 Agarose (Lab. Conda, Spain). For enhancing PCR amplification of those recalcitrant specimens, new DNA isolation was done using FTA® Indicating Micro Cards (Cat N° WB120211, Whatman, Maidstone, England) as described in Telleria et al. (2014).
Prior to sequencing, the amplification products were cleaned using a QIAquick gel PCR purification kit (QIAGEN, Valencia, California, USA). Both strands were sequenced separately using the primers mentioned above at Macrogen (South Korea). Sequences were edited and assembled using Sequencher™ version 4.2 (Gene Codes Corporations, Ann Arbor, Michigan, USA). BLASTN searches (Altschul et al. 1997) with the MEGABLAST option were used to compare the obtained sequences against the sequences in the National Center of Biotechnology Information (NCBI) nucleotide database. Moreover, a preliminary identification of the new sequences was done through UNITE database (http://unite.ut.ee) species hypotheses (SHs) search (Kõljag et al. 2013). The consensus sequences have been lodged in the EMLB/GenBank/DDBJ databases with the accession numbers indicated in Table 1.
Molecular identification
An automatic Jaapia PlutoF multiple sequence alignment was obtained through UNITE. The SH clusters were merged with the new sequences obtained in this study and manually adjusted using Se-Al v.2.0a11 (Rambaut 2002). Alignment gaps were indicated as “−” and ambiguous nucleotides were marked as “N”. Sequences under Gloeophyllum abietinum (Bull.) P. Karst. (AJ420948, Germany; KM098122 and JX524620, China) were included as outgroup, since in the BLASTN search, Gloeophyllum sequences scored next highest after the Jaapia sequences mentioned above; moreover, according to the 5.8S and LSU nrDNA analyses (Larsson 2007), species of Gloeophyllaceae are closely related to Jaapia species.
The alignment was analyzed under a heuristic search, using the program PAUP 4.0b10 (Swofford 2003). Branch lengths equal to zero were collapsed to politomies. Nonparametric bootstrap support (Felsenstein 1985) for each clade was tested with the fast-step option, using 10,000 replicates. The phylogenetic tree was viewed with the program FigTree 1.3.1 (http://tree.bio.ed.ac.uk/software/figtree/) and edited with Adobe Illustrator CS3 11.0.2. (Adobe Systems Incorporated).
From Jaapia sequences, genetic distances were also calculated in PAUP*4.0b10 using the Kimura 2-Parameter model (Kimura 1980), which is widely used in DNA barcoding analyses (e.g., Neigel et al. 2007); interspecific and intraspecific genetic divergences were obtained and the quotient between these distances was calculated to determine whether a barcoding gap exists (Hebert et al. 2004). Nonparametric bootstrap support for each clade was calculated as indicated above.
Results
In this study, eleven sequences were generated from the specimens studied using the primer pair ITS1F/ITS4. On the other hand, the automatic Jaapia PlutoF multiple sequence alignment (UCL7_001618) obtained through UNITE has six sequences distributed in two SH clusters. The sequence GU187524 (J. argillacea) published in Binder et al. (2010) is the reference sequence of the species hypothesis SH235459.06FU cluster; recently this sequence (GU187524) was also selected as the reference sequence of the species J. argillacea, and it appears in the INSD database with the number NR_119766 (Schoch et al. 2014). The SH235459.06FU cluster also includes the sequences EU118636 (J. argillacea) and EU118637 (J. ochroleuca) from Larsson (2007), and the sequence KC514904 (J. argillacea) from an unpublished paper. The second SH cluster, SH190037.07FU, includes two sequences from environmental samples, JX981904 and JX981905, identified as “uncultured fungus.”
The final alignment had 20 sequences, including the Jaapia sequences from the UNITE databases (all sequences in EMLB/GenBank/DDBJ), and the three Gloeophyllum abietinum sequences as outgroup. After heuristic search, 100 trees were retained (tree length = 117; consistency index, CI = 0.9402; homoplasy index, HI = 0.0598; retention index, RI = 0.9676); one of the 100MPTs is shown in Fig. 1, with bootstrap values above the branches. The Jaapia sequences formed a highly supported clade (BS = 100 %). Two main subclades were detected, both with very high bootstrap values. Subclade A (BS = 88 %) included the four sequences that grouped in the SH235459.06FU cluster, under J. argillacea (three sequences) and under J. ochroleuca (one sequence). Subclade B (BS = 96 %) consisted of the 11 sequences generated in this study and two environmental sequences that formed the SH cluster SH190037.07FU; these environmental sequences were isolated in China from the permafrost layer.
On the other hand, the K2P pairwise distance among the Jaapia sequences (517 positions) shows more genetic variability (range 0.00198–0.03028, average distance 0.01641) within sequences from the subclade A; whereas it shows a low value within the sequences of subclade B (range 0.00000–0.00983, average distance 0.0012). The average intraspecific K2P value for all specimens is 0.00274 and the average of interspecific value is 0.03811 (range 0.02832–0.05137). The quotient between the averages of interspecific and intraspecific distances is 13.91, which is greater than the widely used threshold for barcoding studies (10×, Hebert et al. 2004).
Morphological studies show significant differences between the clades concerning the size and shape of spores (Table 1, Fig. 2). The specimens of Jaapia argillacea in clade A show long and homogeneous fusiform spores, (16−)18 − 27 × (5−)6 − 8(−9) μm, Q = 2.52 − 3.15, always with protoplasm contracting in very conspicuous apical ends (Fig. 3). The specimens of J. ochroleuca in clade B exhibit a wide range of spore sizes, 10–20 × 5.5 − 9 μm [12–16 (−18) × 7.5 − 9 (−10) μm in Bresadola’s holotype, S, F88243]. Concerning spore shape, the specimens also show some variability with fusiform (Q = 2.08 − 2.55) or broadly fusiform (Q = 1.68 − 1.98) spores, sometimes with protoplasm contracting leaving the spore ends collapsed, as in the UPS (F-176765) 498999 collection (Fig. 4a).
From the present study, two species are confirmed, and morphological characters are summarized in the following comprehensive key.
Key to species
1. Basidioma resupinate, effuse, argillaceous to yellowish, soft; hymenophore flocculose; margin indeterminate. Hyphal system monomitic, hyphae with clamps, thin-walled, 5–6.5 μm wide; cystidia cylindrical, projecting, thick-walled in the basal part thinner in apical direction, 125–160 × (7−)8 − 11 μm; basidia cylindrical, sinuous, long, 45–60 × 8.5 − 10 μm, with four sterigmata; old basidia often with adventitious septa; spores (16−)18 − 27 × (5−)6 − 8(−9) μm, fusiform (Q = 2.52 − 3.15), smooth, cyanophilous, first thin-walled and after the protoplasm contracts, surrounding itself with a secondary thick wall and leaving the spore ends empty.
J. argillacea
1. Basidioma resupinate, effuse, yellowish to ocraceous, soft; hymenophore flocculose to pilose; margin indeterminate. Hyphal system monomitic; hyphae with clamps, thin- to thick-walled, (5−)6 − 11 μm wide; cystidia cylindrical, projecting, thick-walled in the basal part thinner in apical direction, 150 − 200 − 350 × 7 − 13(−17) μm; basidia claviform to cylindrical, sinuous 27–50 × 6.5 − 8.5 μm, with four sterigmata; old basidia often with adventitious septa; spores 10–20 × 5.5 − 9 μm, fusiform (Q = 2.08 − 2.55) or broadly fusiform (Q = 1.68 − 1.98), smooth, cyanophilous, thick-walled, sometimes with protoplasm contracting leaving the spore ends collapsed.
J. ochroleuca
Discussion
Parsimony analysis, as well as the KP2 distances, clearly delimitate two well-defined and highly supported clades (Fig. 1). Both clades are supported by morphology, specifically by the spore size (Fig. 2) and correspond to the two described species in the Jaapia genus.
Whereas Jaapia argillacea (Bresadola 1911) is a well-defined species with characteristic spores, J. ochroleuca has been described with a broad range of spore width. The protologue of Coniophora ochroleuca (Brinkmann 1898) describes the spores as “subamygdaliformes, 13–16 × 6–8 μm,” which accords with the data on Bresadola’s holotype label. Rogers (1943), based on the European and American specimens, holotype included, characterized the spores as “navicular-fusiform, obliquely apiculate, 9.5 − 18 × 4–8 μm.” Nannfeldt and Eriksson (1953) concluded that they are “fusiform, with a two-layered thick wall, 12–18 × 4–6 μm,” likely a mistake because they studied a lot of specimens, even the holotype. Unfortunately, these wide values will remain an enduring mistake, passed on from one author to the next (Eriksson and Ryvarden 1976; Bernicchia and Gorjón 2010), with the exception of Boidin and Gilles (1990), who defined it as “largement fusiforme, 11–15 × 6–8 μm.”
Our study confirms, based on morphological and molecular data, that Jaapia ochroleuca is a well-defined species with variable spores: fusiform or broadly fusiform, 10–20 × 5.5 − 9 μm.
The barcode for fungi (Schoch et al. 2012), ITS nrDNA sequences, allowed us to evaluate the accuracy of the identification of Jaapia specimens made by early authors. Sequences obtained in this study are based on well-identified specimens and are named not only through BLAST search; they show a good match to the two molecular operational taxonomic units (MOTUs) detected through UNITE search, and to the species level, allowing distinction between J. argillacea (Fig. 1 subclade A: SH235459.06FU cluster) and J. ochroleuca (Fig. 1 subclade B: species hypothesis SH190037.07FU cluster). A reference sequence already exists for J. argillacea (GU187524 in INSD and UNITE databases; named NR119766 as proposed in Schoch et al. 2014). ITS sequences generated from MA-Fungi 23942 will be proposed for deposit in the RefSeq Targeted Loci (RTL) database at NCBI (http://www.ncbi.nlm.nih.gov/bioproject/177353).
Sequences from well-identified isolates are master keys for identifying unknown and/or “environmental” sequences located in international sequence databases, giving a more accurate estimation of worldwide fungal diversity. For example, sequences JX981904 and JX981905 isolated from permafrost soil in China clearly belong to the species J. ochroleuca.
References
Altschul SF, Madden TL, Schäffer 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
Bernicchia AR, Gorjón SP (2010) Corticiaceae s.l. Fungi Europaei 12. Edizioni Candusso, Italy
Binder M, Larsson K-H, Matheny PB, Hibbett DS (2010) Amylocorticiales ord. nov. and Jaapiales ord. nov.: early diverging clades of Agaricomycetidae were dominated by corticioid forms. Mycologia 102:865–880
Boidin J, Gilles G (1990) Corticiés s.l. intéressants ou nouveaux pour la France (Basidiomycotina). Bull Soc Mycol France 106:135–167
Boidin J, Gilles G (1991) Basidiomycètes Aphyllophorales de l’Ile de la Réunion. XVI. Le genres Hyphoderma, Hyphodermopsis, Chrysoderma nov. gen. et Crustoderma. Cryptogam Mycol 12:97–132
Boidin J, Lanquetin P (1983) Les genres Vuilleminia et Corticium sensu stricto (Basidiomycètes) en France. Bull Soc Mycol France 99:269–279
Bourdot H, Galzin A (1923) Hyménomycètes de France IX. Méruliés. Bull Soc Mycol France 39:96–118
Bourdot H, Galzin A (1928) Hyménomycètes de France. Hetérobasidiés—Homobasidiés Gymnocarpes. Reprint 1969. Biblioth Mycol 23. J. Cramer, Lehre
Bresadola G (1911) Adnotanda mycological. Ann Mycol 9:425–428
Brinkmann W (1898) Vorarbeiten zu einer Pilzflora Westfalens. Jahres-Ber Westfäl Prov-Vereins Wiss 26:126–133
Brock PM, Doring H, Bidartondo MI (2009) How to know unknown fungi; the role of a herbarium. New Phytol 181:719–724
Chistiansen MP (1960) Danish resupinate fungi. Part II. Homobasidiomycetes. Dansk Bot Ark 19:57–388
Cochrane G, Karsch-Mizrachi I, Nakamura Y (2011) The international nucleotide sequence database collaboration. Nucleic Acids Res 39:D15–D18
Dai YC (2011) A revised checklist of corticioid and hydnoid fungi in China for 2010. Mycoscience 52:69–79
Donk MA (1964) A conspectus of the families of Aphyllophorales. Persoonia 3:199–324
Dueñas M, Telleria MT (1984) Notas sobre algunos Aphyllophorales procedentes del Norte de España. Bol Soc Micol Castellana 8:61–78
Eriksson J, Ryvarden L (1976) The Corticiaceae of North Europe, vol. 4. Hyphodermella-Mycoacia. Fungiflora, Oslo
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Gardes M, Bruns TD (1993) ITS Primers with enhanced specificity for Basidomycetes—applications to the identification of mycorrhizae and rusts. Mol Ecol 1:113–118
Ghobad-Nejhad M, Nilsson RH, Hallenberg N (2010) Phylogeny and taxonomy of Vuilleminia (Basidiomycota) based on molecular and morphological evidence, with new insights into Corticiales. Taxon 59:1519–1534
Ginns J, Lefebvre MNL (1993) Lignicolous corticioid fungi (Basidiomycota) of North America. Mycol Mem 19:1–247
Gorjón SP, Greslebin AG, Rajchenberg M (2012) Uncobasidium roseocremeum sp. nov. and other corticioid basidiomycetes from Patagonian Andes of Argentina. Mycotaxon 121:349–364
Hebert PDN, Stoeckle MY, Zemlak TS, Francis M (2004) Identification of birds through DNA barcodes. PLoS Biol 2, e312
Hjortstam K (1987) Studies in tropical Corticiaceae (Basidiomycetes) VII. Specimens from East Africa, collected by L. Ryvarden. II. Mycotaxon 28:19–37
Hjortstam K, Telleria MT, Ryvarden L, Calonge FD (1981) Notes on the Aphyllophorales of Spain. II. Nova Hedwigia 34:525–538
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:11–120
Kõljag U, Nilsson H, Abarenkov K, Tedersoo L, Taylor AFS et al (2013) Towards a unified paradigm for sequence-based identification of Fungi. Mol Ecol 22:5271–5277
Larsson K-H (2007) Re-thinking the classification of corticioid fungi. Mycol Res 111:1040–1063
Legon N, Henrici A, Roberts PJ, Spooner BM, Watling R (2005) Checklist of the British and Irish Basidiomycota. Royal Botanic Gardens, Kew
Martín MP, Winka K (2000) Alternative methods of extracting and amplifying DNA from lichens. Lichenologist 32:189–196
Melo I, Telleria MT (1991) Alguns fungos lenhícolas do Parque Nacional de Peneda-Geês, novos para Portugal. Bol Soc Brot, sér. 2, 63:349–378
Nannfeldt JA, Eriksson J (1953) On the Hymenomycetous genus Jaapia Bres. and its taxonomical position. Sven Bot Tidskr 47:177–189
Neigel J, Domingo A, Satke J (2007) DNA barcoding as a tool for coral reef conservation. Coral Reefs 26:487–499
Pouzar Z (1958) Nova genera macromycetum II. Ceská Mykol 12:31–36
Rambaut A (2002) Se-Al: sequences alignment editor v2.0a11. Edinburgh: Institute of Evolutionary Biology, University of Edinburgh. http://tree.bio.ed.ac.uk/software/
Rogers DP (1935) Notes on the lower basidiomycetes. Stud Nat Hist Iowa Univ 17:3–43
Rogers DP (1943) The genus Pellicularia (Thelephoraceae). Farlowia 1:95–118
Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Fungal Barcoding Consortium (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. PNAS 109(16):6241–6246
Schoch CL, Robbertse B, Robert V, Vu D, Cardinali G et al (2014) Finding needles in haystacks: linking scientific names, reference specimens and molecular data of Fungi. Database-Oxford 2014:1–21. doi:10.1093/database/bau061
Swofford DL (2003) PAUP* Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer, Sunderland
Telleria MT, Melo I, Dueñas M, Rodríguez-Armas JL, Beltrán-Tejera E, Cardoso J, Salcedo I (2009) Diversity and richness of corticioid fungi (Basidiomycota) on Azores Islands: a preliminary survey. Nova Hedwigia 88:285–308
Telleria MT, Dueñas M, Melo I, Martín MP (2010) Morphological and molecular studies of Hyphodermella in the western Mediterranean area. Mycol Prog 9:585–596
Telleria MT, Dueñas M, Martín MP (2014) Sistotremastrum chilensis (Trechisporales, Basidiomycota), a new species from Chilean Patagonia. Phytotaxa 158:093–098
von Höhnel F (1912) Fragmente zur Mykologie 14. Sitzungsber Kaiserl Akad Wiss Math-Naturwiss Cl Abt I 121:339–424
Wakefield EM, Pearson AA (1920) Record of surrey resupinate hymenomycetes. Trans Br Mycol Soc 6:317–321, 1919
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, San Diego, pp 315–322
Whiting MF, Carpenter JC, Wheeler QD, Wheeler WC (1997) The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Syst Biol 46:1–68
Winka K, Ahlberg C, Eriksson OE (1998) Are there lichenized Ostropales? Lichenologist 30:455–462
Acknowledgments
Financial support was provided by Plan Nacional I+D+i projects CGL2006-12732-CO2-01/BOS and CGL2012-35559. We are grateful to Marian Glenn (Seton Hall University, New Jersey) for checking the English, and Fátima Durán (RJB-CSIC) for providing technical assistance, as well as to the curators of BIO-Fungi, LISU, MA-Fungi, O, PC, S, UPS for their invaluable help.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
About this article
Cite this article
Telleria, M.T., Dueñas, M., Melo, I. et al. Spelling out Jaapia species. Mycol Progress 14, 57 (2015). https://doi.org/10.1007/s11557-015-1081-8
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11557-015-1081-8