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Redisposition of apiosporous genera Induratia and Muscodor in the Xylariales, following the discovery of an authentic strain of Induratia apiospora
Botanical Studies volume 64, Article number: 8 (2023)
Abstract
Background
The genus Induratia is based on Induratia apiospora, a xylarialean pyrenomycete from New Zealand with clypeate uniperitheciate stromata, hyaline apiospores and a nodulisporium-like anamorph. However, because of the lack of DNA data from the generic type, its phylogenetic affinities have remained unresolved. Recently, two fungal species with teleomorphs strikingly similar to Induratia were discovered in Thailand. However, they did not produce an anamorph and were found to be phylogenetically close to the species classified within the hyphomycete genus Muscodor, which was described after Induratia. Therefore, in 2020 the species of Muscodor were transferred to Induratia, and a new family Induratiaceae was proposed.
Results
We have encountered an unpublished ex-holotype strain of Induratia apiospora among the holdings of the ATCC collection, enabling detailed morphological and molecular phylogenetic investigations. We observed the characteristic nodulisporium-like anamorph described in the original publication. Phylogenetic analyses of multigene sequence data revealed a close relationship of Induratia apiospora to the Barrmaeliaceae, while a close relationship to the Induratia species formerly classified within Muscodor was rejected.
Conclusions
We here classify Induratia apiospora within the Barrmaeliaceae and consider Induratiaceae to be synonymous with the former. As the holotype specimen of Induratia apiospora is apparently lost, an isotype specimen from WSP is selected as lectotype. We also propose that the genus Muscodor is resurrected within the Xylariaceae, and formally transfer several Induratia species to Muscodor.
Background
The taxonomy of the Sordariomycetes and other Ascomycota has changed drastically in the past decade, owing to the advent of multi-locus phylogenies, which were often combined in polyphasic studies, using morphological and chemotaxonomic data as additional evidence. The currently proposed classification of genera and higher taxa (cf. Hyde et al. 2020; Wijayawardene et al. 2022) is steadily changing as new evidence becomes available, in particular when the species that have been first described in the pre-molecular era are cultured and sequenced for the first time. A fair example are genera of the Xylariales, and especially so the Xylariaceae s. lat. where it has become evident due to the availability of molecular data that the classical discrimination of higher taxa based on ascus structure (uni-, bitunicate), fruiting bodies, anamorph-teleomorph connections and ascospore morphology alone is not feasible. This has been reflected by the recent re-organization of the families (Wendt et al. 2018), where the results of a four-locus genealogy were better in agreement with chemotaxonomy and anamorphic morphology than with the classical concept based on ascospore shape. Interestingly, the aforementioned phylogeny was even backed up at genus level by a concurrent phylogenomic study using the amino acid sequences of 4912 orthologue genes for the core genera of the Hypoxylaceae (Wibberg et al. 2021). Other families and genera of Xylariales, for which by far not that many data are available, are in bad need of further studies. It is to be expected that it will take several years more to generate sufficient amounts of data to attain a stable phylogeny. Numerous taxa are still only known from old morphological descriptions (often restricted to the teleomorphs), or have only recently been recollected and cultured to generate molecular data and study their anamorphs for the first time. These studies sometimes revealed rather unexpected phylogenetic affinities but also showed the limits of a morphocentric approach for phylogenetic assessments (Jaklitsch et al. 2014; 2016; Voglmayr et al. 2022).
Aside from attempts to re-discover fresh specimens corresponding to the old fungal taxa, it may at times also be feasible to screen the inventories of the large culture collections, since those may contain valuable reference or ex-type strains that have not been reported in the original literature. The current paper describes such a case.
The genus Induratia was originally described by Samuels et al. (1987) based on a single specimen from New Zealand that featured uniperitheciate stromata, asci with an amyloid ascal apparatus and apiosporous ascospores. The authors also observed a nodulisporium-like conidial stage in the mycelial culture they obtained, and this new combination had at that time given rise to the erection of a new monotypic genus. In the following decades the genus almost remained forgotten, except that Miller and Huhndorf (2005) included a specimen they referred to as “Induratia sp. SMH 1255” originating from Puerto Rico in their phylogenetic study of Sordariales and other Sordariomycetes. However, Miller and Huhndorf (2005) neither included any morphological data of the specimen (which is housed in the fungarium of the University of Illinois as ILLS 82598), nor cultured it nor studied the anamorph. Samarakoon et al. (2020) later included the DNA sequences derived from this collection and provided microscopic details of the stromata and ascogenic structures. These morphological features resembled the drawings of Induratia apiospora by Samuels et al. (1987), even though the holotype specimen of this species has apparently been lost and could neither be located at the ZT nor the PDD herbarium. The molecular data of Induratia sp. SMH 1255 resembled those derived from two specimens that were freshly collected from Thailand. Moreover, they also clustered with the sequences of all hitherto described species of the genus Muscodor. This gave rise to the synonymisation of Induratia and Muscodor, with the former, older name taking priority over the younger Muscodor, and the erection of the new family Induratiaceae, which also included the similar genus Emarcea (Samarakoon et al. 2020).
However, we have recently encountered a culture labeled Induratia apiospora in the catalogue of the ATCC (Manassas, USA) via a random Google search on information on the genus on the Internet and decided to order and study it for comparison. The current paper is dedicated to the description of its characteristics and the necessary changes in the taxonomy of the Xylariales.
Methods
Morphological studies on strain ATCC 60639
A Google search for Induratia apiospora revealed a culture deposited as ATCC 60639 by G.J. Samuels not mentioned by Samuels et al. (1987). From discussions with two of the authors of the original paper, it was confirmed that this strain was indeed derived from the holotype specimen (O. Petrini and G.J. Samuels, personal communications). The strain Induratia apiospora (Samuels et al. 1987) was thus purchased from the American Type Culture Collection (ATCC, Mannassas, Virginia) under the accession ATCC 60639 and cultured on Yeast-Malt agar (10 g/L malt extract, 4 g/L D-glucose, 4 g/L yeast extract, supplemented with 20 g/L agar and adjusted to pH 6.3 prior to sterilization). The mycelia were transferred to a new plate once the strain had covered the medium by excision of a 5 mm2 square overgrown with mycelium on a regular basis (2–4 weeks). Plates were frequently monitored for sporulation.
For the morphological analysis of strain ATCC 60639, a small piece of sporulating mycelium was extracted and the dimensions of conidiogenous structures measured in distilled water and lactic acid. To observe the macro-morphology of the cultures, the strains were grown on Yeast-Malt agar (YM6.3; malt extract 10 g/L, yeast extract 4 g/L, D-glucose 4 g/L, agar 20 g/L, pH 6.3 before autoclaving), 2% Malt Extract Agar (MEA), Oatmeal Agar (OA, Sigma-Aldrich, Steinheim, Germany), and potato dextrose agar (PDA, Himedia, Mumbai, India) and the cultures checked at four weeks after inoculation. Photomicrographs were obtained using a DS-Fi3 camera connected to a Nikon eclipse Ni-U microscope (Nikon Europe BV, Amsterdam, Netherlands).
DNA extraction, PCR amplification and sequencing
The DNA extraction protocol and the solutions used for PCR amplification followed the description of Wendt et al. (2018). PCR programs followed Samarakoon et al. (2020), with the exemption of using the primer pair ITS1f and ITS4 (White et al. 1990) instead of ITS5 and ITS4. Briefly, the following settings were used: ITS: 94 °C for 30 s, 56 °C for 50 s, 72 °C for 60 s; LSU: LR0R/LR5: 94 °C for 30 s, 55 °C for 50 s, 72 °C for 60 s (Vilgalys and Hester 1990); SSU: NS1/NS4: 94 °C for 30 s, 54 °C for 50 s, 72 °C for 60 s (White et al. 1990); rpb2: fRPB2-5F/fRPB2-7cR: 95 °C for 45 s, 57 °C for 50 s, 72 °C for 90 s (Liu et al. 1999); tub2: T1/T22: 95 °C for 60 s, 54 °C for 110 s, 72 °C for 120 s (O’Donnell and Cigelnik 1997). PCR amplicons were purified as described in Wendt et al. (2018) and sequences generated with the Sanger sequencing method at the Microsynth sequencing company, using respective forward and reverse primers (Microsynth SeqLab GmbH, Göttingen, Germany). Sequences were assembled as a consensus sequence from both reads by using the de-novo assembly program contained in Geneious® R7.1.9 (Kearse et al. 2012). The generated and further used sequences in this study are listed with their respective GenBank Acc. No. in Table 1.
Taxon selection and molecular phylogenetic inference
To assess the affinities of the newly generated sequences within the order Xylariales, the manually curated alignment and taxon set recently presented by Voglmayr et al. 2022 was used, further restricting sequences derived from Xylariaceae from 154 to 94 taxa. The newly generated sequences of the ITS, LSU, rpb2 and tub2 loci were inserted into the data matrix and manually checked for consistency. The different loci were subjected to IQTree2 (Minh et al. 2020) for molecular phylogenetic inference using Maximum-Likelihood criterion with options for a partitioned analysis (Chernomor et al. 2016) of the supermatrix with prior testing for the optimal nucleotide substitution model by using ModelFinder (Kalyaanamoorthy et al. 2017) following BIC criterion and 1000 non-parametric bootstrap (Felsenstein 1985) replicates. Concurrently, the optimal nucleotide substitution models for each locus were calculated with PartitionFinder2 (Lanfear et al. 2016) as implemented in the PhyloSuite V.1.2.2 (Zhang et al. 2020) program package and to-be-tested models restricted to the ones available in MrBayes 3.2.7a (Ronquist et al. 2012). Partitions were regarded as unlinked and testing options set to BIC optimality criterion and test strategy set to test all. A phylogenetic inference using MrBayes 3.2.7a followed, with settings used and described by Kemkuignou et al. (2022). Briefly, a random starting tree was used to calculate 200.000.000 generations with convergence controlled to arrive at an average split frequency of 0.01. Tree sampling was done every 1000 generations, of which the first 25% were discarded as “burn-in”. Four incrementally heated chains were used for the Markov Chain Monte Carlo (MCMC), with temperature set to 0.15. The BEAGLE library (Ayres et al. 2012) and a parallel Metropolis coupling for the MCMC (Altekar et al. 2004) were used to calculate in total four chains in parallel. The resulting bootstrap (bs) ≥ 70% and posterior probabilities ≥ 0.95 were mapped on the respective bipartition on the found maximum-likelihood tree.
Results
Morphological studies on strain ATCC 60639
The culture we obtained from ATCC showed the following characteristics (Fig. 1):
Colonies of Induratia apiospora (ATCC 60639) after four weeks A, B on MEA; C, D on OA; E, F on PDA; G, H on YM6.3
Culture characteristics: On YM6.3 and PDA: 2.6 cm in four weeks. Mycelium white, wavy or cottony hyphal growth, margin filiform to slightly undulate, flat to slightly elevate. Reverse white to pale. On MEA: 4.2 cm in four weeks, differs by having a mycelium with a margin slightly undulate, flat. On OA: 5.8 cm in four weeks, differing to have a margin entire. The information is summarized in Table 2. Sporulating regions: in patches, citrine (13) olivaceous (48). Conidiogenous structure nodulisporium-like, abundant, smooth to slightly roughened. Conidiogenous cells: melanized, smooth to slightly roughened, 34.5–66.5 × 2–3 µm (n = 23). Conidia: hyaline with cytoplasm content melanized, smooth, ellipsoidal to obovoid, 4–6 × 2–4 µm (n = 41).
These characteristics (see also Fig. 2) are indeed well in accordance with what Samuels et al. (1987) had reported for Induratia apiospora. According to the description by Samuels et al. (1987), the anamorph is nodulisporium-like, conidiogenous cells are light brown, slightly roughened, conidia are hyaline, ellipsoidal to obovoid, 4–6 × 2–4 µm.
Morphology of the anamorph of the ex-type strain of Induratia apiospora (ATCC 60639) on YM6.3. A Conidiophore on surface mycelium. B Single nodulisporium-like conidiophore. C, D Conidiogenous cells. E, F Conidia. Scale bars: B 20 µm, E, F 10 µm
Molecular phylogenetic inference
The alignment subjected to IQTree and MrBayes consisted of 4679 sites in total, distributed among loci corresponding to the ITS (584 sites), LSU (1329 sites), rpb2 (1235 sites) and tub2 (1531 sites). The generated sequence of the SSU for Induratia apiospora ATCC 60639 has not been used for phylogenetic reconstruction, but has been deposited under the GenBank Acc. No. OQ748100 for the scientific community to use. A detailed list of alignment features and the tested models per partition, as well as the alignments can be found in the (Additional file 1: Tables S1–S3). The final inferred tree following maximum-likelihood analysis had an lLn of − 89939.9947 (Fig. 3). The topology of trees generated from the ML and Bayesian approach were identical, showing a similar arrangement of the taxa as previously presented by Voglmayr et al. (2022). Briefly, the Hypoxylaceae, Diatrypaceae, Lopadostomataceae, Graphostromataceae, Xylariaceae and Barrmaeliaceae received maximum support. The position of the latter was not resolved. Sequences derived from Induratia sensu Samarakoon et al. (2020; given as Muscodor in Fig. 3), Spiririma gaudefroyi and Emarcea received maximum support in a clade nested inside the Xylariaceae. Surprisingly, the sequences of Induratia apiospora ATCC 60639 clustered in a basal position to a clade formed by Entosordaria and Barrmaelia representing the Barrmaeliaceae, each clade receiving maximum support.
Maximum Likelihood Tree (lLn = − 89939.9947) inferred from a manually edited alignment of ITS, LSU, rpb2 and tub2 sequences featuring sequences derived from Hypoxylaceae, Diatrypaceae, Lopadostomataceae, Graphostromataceae, Barrmaeliaceae and Xylariaceae. The position of the newly generated and concatenated sequences of Induratia apiospora are marked in bold. Bootstrap and Bayesian posterior probabilities ≥ 70% and ≥ 0.95, respectively, are given at bipartitions
Taxonomy
Our phylogenetic study showed that the ex-type strain of Induratia resolves within the Barrmaeliaceae. The Induratiaceae are thus regarded as a synonym of Barrmaeliaceae and Muscodor is resurrected. The holotype specimen of Induratia could still not be recovered, hence the isotype (WSP73242; MyCoPortal 2022) located at Shaw Mycology Herbarium (WSP; Washington State University) is chosen as lectotype. The genera Emarcea and Muscodor, which were previously classified within Induratiaceae, are now formally accommodated in the Xylariaceae.
Barrmaeliaceae Voglmayr & Jaklitsch, Mycol. Progr. 17(1–2): 162 (2017) [2018], emend. Cedeño-Sanchez, M. Stadler, Voglmayr & C. Lambert.
MycoBank MB 822042
Type genus: Barrmaelia Rappaz
≡ Induratiaceae Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Diversity 101: 188 (2020) [MB833443], syn. nov.
Other genera in the family: Entosordaria Höhn. (see Voglmayr et al. 2018), Induratia Samuels, E. Müll. & Petrini (see below).
Saprobic on wood or bark. Stroma if present mostly in wood and blackening the surface in wide areas or in elongate bands, sometimes darker or carbonized around the ostioles; entostroma prosenchymatous, poorly developed, sometimes delimited by a black carbonized line (Induratia), without KOH-extractable pigments; ectostroma variable, from virtually absent, poorly developed to strongly carbonized and clypeus-like. Ascomata (perithecia) globose, sometimes raising the substrate, singly, in small groups or gregarious. Peridium melanized, pseudoparenchymatous to prosenchymatous. Hamathecium of numerous persistent, hyaline, septate paraphyses. Asci eight-spored, cylindrical, persistent, with inamyloid or amyloid apical ascus apparatus. Ascospores hyaline, yellow to dark brown; unicellular with or without germ slit (Barrmaelia), or two-celled with septum near one end, the small cell hyaline, the large cell dark brown and with an apical germ apparatus consisting of radial slits (Entosordaria), or hyaline, two-celled, apiosporous without germ slit (Induratia); allantoid, ellipsoid or fusoid, inequilateral, slightly inequilateral or nearly equilateral, with narrowly or broadly rounded ends. Anamorph, where known, libertella-like (Barrmaelia; Rappaz 1995), or nodulisporium-like (Induratia).
Key to the genera of Barrmaeliaceae
1. Ascospores one-celled, asymmetrically ellipsoid to allantoid, uniformly light to dark brown, with or without a longitudinal germ slit, without appendages; anamorph libertella-like……………….……………Barrmaelia.
1. Ascospores two-celled, apiosporous, germ locus absent or consisting of apical radial slits, with or without appendages…………………………………2
2. Ascospores with submedian septum, entirely hyaline, without germ locus, with hyaline cellular appendages at each end while still in the ascus; anamorph nodulisporium-like………………………………………Induratia.
2. Ascospores with septum near one end, small ascospore cell hyaline, large ascospore cell dark brown and with an apical germ apparatus consisting of radial slits, without appendages; anamorph unknown………………………………………………Entosordaria.
Induratia Samuels, E. Müll. & Petrini, Mycotaxon 28(2): 484 (1987).
Type species: Induratia apiospora Samuels, E. Müll. & Petrini, Mycotaxon 28(2): 484 and Fig. 5 (1987).
MycoBank MB 130900
Holotype: New Zealand, North Island, Hokianga Co., Waipoua State Forest, near Yakas Track, on decorticated wood, 30 May 1982, G.J. Samuels and P. Johnston (PDD 44399, lost). Lectotype: (designated here, MBT 10010382) New Zealand North Island, Hokianga Co., Waipoua State Forest, near Yakas Track, on decorticated wood, 30 May 1982, G.J. Samuels and P. Johnston (WSP73242).
Ex-type culture: ATCC 60639, deposited by G.J. Samuels; duplicates sent to CBS under accession CBS 149733 and ICMP 24754.
Resurrection of Muscodor
The genus Muscodor is now placed in the Xylariaceae, where it had originally been accommodated based on phylogenetic relationship, however anamorph morphology, a traditionally important character for the characterization of Xylariales, is still lacking. Below we list all species that were formerly accepted in Muscodor, including those that have been invalidly described in the original publications. The typifications have already been corrected and changed by Samarakoon et al. (2020) according to the rules of the International Code of Nomenclature for Algae, Fungi, and Plants (ICN), when those designations were validated in Induratia. We here introduce new combinations for these Induratia names in Muscodor.
Muscodor Worapong, Strobel & W.M. Hess, Mycotaxon 79: 71 (2001).
Type species: Muscodor albus Worapong, Strobel & W.M. Hess, Mycotaxon 79: 71 (2001).
≡ Induratia alba (Worapong, Strobel & W.M. Hess) Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 193 (2020).
Other accepted species
Muscodor brasiliensis (L.C. Pena, Servienski & V. Kava ex Samarak., Thongbai, K.D. Hyde & M. Stadler) Cedeño-Sanchez, M. Stadler, Voglmayr & C. Lambert, comb. nov.
MycoBank MB 846432
Basionym: Induratia brasiliensis L.C. Pena, Servienski & V. Kava ex Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 196 (2020).
[originally described as: Muscodor brasiliensis L.C. Pena, Servienski & V. Kava, Microbiol. Res. 221: 32 (2019), nom. inval., Art. 40.7 (Shenzhen)]
Muscodor camphorae Meshram, N. Kapoor, G. Chopra & S. Saxena [as ‘camphora’], Mycosphere 8(4): 571 (2017).
≡ Induratia camphorae (Meshram, N. Kapoor, G. Chopra & S. Saxena) Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 193 (2020).
Muscodor cinnamomi Suwannar., Bussaban, K.D. Hyde & Lumyong, Mycotaxon 114: 19 (2011) [2010].
≡ Induratia cinnamomi (Suwannar., Bussaban, K.D. Hyde & Lumyong) Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 193 (2020).
Muscodor coffeanus A.A.M. Gomes, Pinho & O.L. Pereira [as ‘coffeanum’], in Hongsanan et al., Cryptog. Mycol. 36(3): 368 (2015).
≡ Induratia coffeana (A.A.M. Gomes, Pinho & O.L. Pereira) Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 193 (2020).
Muscodor crispans A.M. Mitch., Strobel, W.M. Hess, Pérez-Vargas & Ezra, Fungal Divers. 31: 41 (2008).
≡ Induratia crispans (A.M. Mitch., Strobel, W.M. Hess, Pérez-Vargas & Ezra) Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 193 (2020).
Muscodor darjeelingensis (Meshram, N. Kapoor & S. Saxena ex Samarak., Thongbai, K.D. Hyde & M. Stadler) Cedeño-Sanchez, M. Stadler, Voglmayr & C. Lambert, comb. nov.
MycoBank MB 846443
Basionym: Induratia darjeelingensis Meshram, N. Kapoor & S. Saxena ex Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 198 (2020).
[originally described as: Muscodor darjeelingensis Meshram, N. Kapoor & S. Saxena, Sydowia 66(1): 61 (2014), nom. inval., Art. 40.7 (Shenzhen)]
Muscodor equiseti Suwannar. & Lumyong, in Suwannarach, Kumla, Bussaban, Hyde, Matsui & Lumyong, Ann. Microbiol. 63(4): 1350 (2013).
≡ Induratia equiseti (Suwannar. & Lumyong) Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 193 (2020).
Muscodor fengyangensis (Chu L. Zhang ex Samarak., Thongbai, K.D. Hyde & M. Stadler) Cedeño-Sanchez, M. Stadler, Voglmayr & C. Lambert, comb. nov.
MycoBank MB 846442
Basionym: Induratia fengyangensis Chu L. Zhang ex Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 198 (2020).
[originally described as: Muscodor fengyangensis Chu L. Zhang, Fungal Biol. 114(10): 801 (2010), nom. inval., Art. 40.1 (Shenzhen)]
Muscodor ghoomensis S. Saxena, M. Gupta & Meshram, Sydowia 67: 136 (2015).
≡ Induratia ghoomensis (S. Saxena, M. Gupta & Meshram) Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 193 (2020).
Muscodor heveae (Siri-Udom & Lumyong ex Samarak., Thongbai, K.D. Hyde & M. Stadler) Cedeño-Sanchez, M. Stadler, Voglmayr & C. Lambert, comb. nov.
MycoBank MB 846436
Basionym: Induratia heveae Siri-Udom & Lumyong ex Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 199 (2020).
[originally described as: Muscodor heveae Siri-Udom & Lumyong, Ann. Microbiol. 66(1): 442 (2015), nom. inval., Art. 40.7 (Shenzhen)]
Muscodor indicus S. Saxena, M. Gupta & Meshram [as ‘indica’], Sydowia 67: 136 (2015).
≡ Induratia indica (S. Saxena, M. Gupta & Meshram) Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 193 (2020).
Muscodor kashay (Meshram, N. Kapoor & S. Saxena ex Samarak., Thongbai, K.D. Hyde & M. Stadler) Cedeño-Sanchez, M. Stadler, Voglmayr & C. Lambert, comb. nov.
MycoBank MB 846437
Basionym: Induratia kashay Meshram, N. Kapoor & S. Saxena ex Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 199 (2020).
[originally described as: Muscodor kashayum Meshram, N. Kapoor & S. Saxena, Mycology 4(4): 198 (2013), nom. inval., Art. 40.7 (Shenzhen)]
Muscodor musae Suwannar. & Lumyong, in Suwannarach, Kumla, Bussaban, Hyde, Matsui & Lumyong, Ann. Microbiol. 63(4): 1347 (2013).
≡ Induratia musae (Suwannar. & Lumyong) Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 193 (2020).
Muscodor oryzae Suwannar. & Lumyong, in Suwannarach, Kumla, Bussaban, Hyde, Matsui & Lumyong, Ann. Microbiol. 63(4): 1349 (2013).
≡ Induratia oryzae (Suwannar. & Lumyong) Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 194 (2020).
Muscodor roseus Worapong, Strobel & W.M. Hess, Mycotaxon 81: 467 (2002).
≡ Induratia rosea (Worapong, Strobel & W.M. Hess) Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 194 (2020).
Muscodor strobelii Meshram, S. Saxena & N. Kapoor, Mycotaxon 128: 96 (2014).
≡ Induratia strobelii (Meshram, S. Saxena & N. Kapoor) Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 194 (2020).
Muscodor suthepensis Suwannar. & Lumyong, in Suwannarach, Kumla, Bussaban, Hyde, Matsui & Lumyong, Ann. Microbiol. 63(4): 1349 (2013).
≡ Induratia suthepensis (Suwannar. & Lumyong) Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 194 (2020).
Muscodor suturae Kudalkar, Strobel & Riy.-Ul-Hass. [as ‘sutura’], Mycoscience 53(4): 322 (2012).
≡ Induratia suturae (Kudalkar, Strobel & Riy.-Ul-Hass.) Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 194 (2020).
Muscodor thailandicus (Samarak., Thongbai, K.D. Hyde & M. Stadler) Cedeño-Sanchez, M. Stadler, Voglmayr & C. Lambert, comb. nov.
MycoBank MB 846434
Basionym: Induratia thailandica Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 194 (2020).
Muscodor tigerensis (S. Saxena, Meshram & N. Kapoor ex Samarak., Thongbai, K.D. Hyde & M. Stadler) Cedeño-Sanchez, M. Stadler, Voglmayr & C. Lambert, comb. nov.
MycoBank MB 846438
Basionym: Induratia tigerensis S. Saxena, Meshram & N. Kapoor ex Samarak., Thongbai, K.D. Hyde & M. Stadler Fungal Divers. 101(1): 199 (2020).
[originally described as: Muscodor tigerensis S. Saxena, Meshram & N. Kapoor, Ann. Microbiol. 65(1): 53 (2014) [2015], [as ‘tigerii’], nom. inval., Art. 40.7 (Shenzhen)].
Muscodor vitigenus Daisy, Strobel, Ezra & W.M. Hess, in Daisy, Strobel, Ezra, Castillo, Baird & Hess, Mycotaxon 84: 45 (2002).
≡ Induratia vitigena (Daisy, Strobel, Ezra & W.M. Hess,) Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 196 (2020).
Muscodor yucatanensis M.C. González, A.L. Anaya, Glenn & Hanlin, Mycotaxon 110: 365 (2009).
≡ Induratia yucatanensis (M.C. González, A.L. Anaya, Glenn & Hanlin) Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 196 (2020).
Muscodor yunnanensis (C.L. Zhang ex Samarak., Thongbai, K.D. Hyde & M. Stadler) Cedeño-Sanchez, M. Stadler, Voglmayr & C. Lambert, comb. nov.
MycoBank MB 846435
Basionym: Induratia yunnanensis C.L. Zhang ex Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 199 (2020).
[originally described as: Muscodor yunnanensis C.L. Zhang, in Chen et al., Mycosphere 10(1): 193 (2019), nom. inval., Art. 40.8 (Shenzhen)]
Muscodor ziziphi (Samarak., Thongbai, K.D. Hyde & M. Stadler) Cedeño-Sanchez, M. Stadler, Voglmayr & C. Lambert, comb. nov.
MycoBank MB 846433
Basionym: Induratia ziziphi Samarak., Thongbai, K.D. Hyde & M. Stadler, Fungal Divers. 101(1): 196 (2020).
Notes
The specimen SMH 1255 from Puerto Rico, originally studied by Miller and Huhndorf (2005) and later by Samarakoon et al. (2020), has so far been treated as a member of the genus Induratia. It should henceforth be treated as a species of Muscodor, as its phylogenetic affinities are with the latter genus. Even though the species has not been formally described, the taxonomic name associated with the GenBank Acc. Nos for its DNA sequences ought to be changed.
Emarcea Duong, Jeewon & K.D. Hyde, Stud. Mycol. 50(1): 255 (2004).
MycoBank MB 500070.
Type species: Emarcea castanopsidicola Duong, Jeewon & K.D. Hyde, Stud. Mycol. 50(1): 255 (2004).
Notes
Since the genus Emarcea is phylogenetically closely related to the species in the Muscodor clade, it is again classified within the Xylariaceae, together with the Muscodor species discussed above.
Discussion
Multi-locus molecular phylogenetic analysis proved to serve as a powerful tool to emend placements of taxonomic groups in the Xylariales over the last years, exemplified by the erection of the Barrmaeliaceae to accommodate a phylogenetically distinct and well-supported clade of Barrmaelia and Entosordaria (Voglmayr et al. 2018). Other examples include the emendation of the Hypoxylaceae in concordance with chemotaxonomic information (Wendt et al. 2018) or the resurrection of Dematophora, distinguished from Rosellinia species by its synnematal geniculosporium-like anamorph and often a phytopathogenic lifestyle (Wittstein et al. 2020). Regarding the recent synonymisation of Muscodor with Induratia (Samarakoon et al. 2020), some doubts remained on the validity of that approach, e.g., because the anamorph described by Samuels et al. (1987) was hitherto not observed in the Muscodor cultures, which seem to be unable to sporulate. The proposed taxonomy of Samarakoon et al. (2020) was based on the rather similar teleomorphs of M. thailandicus (≡ I. thailandica) and M. ziziphi (≡ I. ziziphi) and the Muscodor sp. (≡ Induratia sp.) specimen reported by Miller and Huhndorf (2005) and characterized by Samarakoon et al. (2020), featuring typical xylariaceous asci and apiospores. The results of the corresponding phylogenies unfortunately did not include any sequences of Induratia before erection of its eponymous family, due to a lack of access to molecular data to compare (Samarakoon et al. 2020). Only two years later, Voglmayr et al. (2022) found that DNA sequences of Spiririma (≡ Helicogermslita) gaudefroyi, clustered within the Induratiaceae clade. Since S. gaudefroyi features dark ascospores, this gave reason to challenge the concept of restricting apiosporous Xylariales to the Induratiaceae. In our study, the ex-holotype culture of Induratia apiospora isolated by Samuels et al. (1987) clustered in a basal position with Barrmaelia and Entosordaria, while the position of the Barrmaeliaceae remained unchanged. As the Induratia spp. transferred from Muscodor showed no relationship with the ex-holotype culture of I. apiospora, the genus Muscodor is resurrected. Furthermore, this implied that the Induratiaceae cannot be retained as an own family, from a phylogenetic perspective, but should be merged with Barrmaeliaceae (Voglmayr et al. 2022). Morphological characters formerly used to segregate the Induratiaceae from other members of the Xylariaceae, i.e. the presence of apiosporous ascospores, can apparently not serve beyond species discrimination. The resurrected Muscodor still showed a paraphyletic structure, indicated by a clade formed by Spiririma and Muscodor fengyangensis, which may result in further re-arrangements in the future, e.g., when a larger number of anamorph/teleomorph relationships has been established.
Serious degrees of synapomorphies are well documented within the Xylariaceae, illustrated by the paraphyly of the genus Xylaria, and so far it has not been possible to resolve this problem even by extensive taxon sampling (Hsieh et al. 2010; Voglmayr et al. 2018, 2022; Voglmayr and Beenken 2020). A similar situation was previously encountered for another family in the Xylariales, the Hypoxylaceae. An important feature of the Hypoxylaceae is the prolific secondary metabolism of its members, which has long been exploited for chemotaxonomic purposes. Recently, it was possible to match chemotaxonomic data by performing genome mining for secondary metabolite-encoding biosynthesis gene clusters (Wibberg et al. 2021; Kuhnert et al. 2021) after sequencing of the full genomes of some representative strains using 3rd generation techniques with phylogenomic approaches. This example indicates the feasibility to sample for additional phenotypic data, i.e. data about the secondary metabolism, and attempting to link it with phylogenetic data on a larger scale to explore taxonomic affinities. Almost all Xylariales are well-known to be very prolific secondary metabolite producers, and in particular Muscodor species are known to produce volatile antibiotics. Therefore, following the previously presented example of the Hypoxylaceae, we suggest the inclusion of chemotaxonomic data and in particular studies on the non-volatile metabolites, combined with robust synthetic chemistry enabling the identification of the produced metabolites for the future.
Data availability
All data except for the DNA sequences, which are deposited in GenBank (https://www.ncbi.nlm.nih.gov/genbank/) are available in the manuscript or the Additional file 1.
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Acknowledgements
We thank Anke Skiba for expert technical assistance and, Adrienne Stanton, Peter Johnston, Gary J. Samuels, Orlando Petrini, for valuable correspondence in the course of our search for the type of Induratia apiospora. Monique H. Slipher is thanked for providing information and images about the state of the isotype of I. apiospora located in WSP.
This article is dedicated to the memory of Prof. Jack D. Rogers
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Open Access funding enabled and organized by Projekt DEAL. MCS gratefully acknowledges a PhD stipend from The National Secretariat of Science, Technology and Innovation of the Republic of Panama (SENACYT) and the Institute for the Development of Human Resources (IFARHU). We are also grateful to the LifeScience Foundation (Munich) for a PhD stipend for CL. MS would like to thank the Deutsche Forschungsgemeinschaft for a Research Unit grant in the SPP 1991 (TaxonOmics).
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CL: conceptualization, supervision, analysis, writing—original draft preparation; HV: analysis; MCS: methods and analysis; RS: methods and analysis; MS: analysis, writing—original draft preparation, resources; KB: analysis, writing—review and editing. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Images of the isotype located in the Shaw Mycological Herbarium (WSP), provided by Monique H. Slipher, are shown in Fig. S1. Auxilliary information and characteristics covering the molecular phylogenetic analysis as well as the alignment are given in the Tables S1–S3.
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Cedeño-Sanchez, M., Schiefelbein, R., Stadler, M. et al. Redisposition of apiosporous genera Induratia and Muscodor in the Xylariales, following the discovery of an authentic strain of Induratia apiospora. Bot Stud 64, 8 (2023). https://doi.org/10.1186/s40529-023-00372-1
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DOI: https://doi.org/10.1186/s40529-023-00372-1