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Research Article
Multi-gene phylogenetic and taxonomic contributions to Xylaria (Ascomycota) associated with fallen fruits from China
expand article infoAn-Hong Zhu‡§|, Zi-Kun Song§‡, Jun-Fang Wang§#‡, Hao-Wen Guan§¤‡, Zhi Qu§‡, Hai-Xia Ma§«‡
‡ Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, China
§ Hainan Institute for Tropical Agricultural Resources, Haikou, China
| Beijing Forestry University, Beijing, China
¶ Coconut Research Institute, Chinese Academy of Tropical Agricultural Sciences, Wenchang, China
# Jilin Agricultural University, Changchun, China
¤ Liaoning University, Shenyang, China
« Chongzuo Key Laboratory for Protection and Utilization of Edible and Medicinal Fungi, Fusui, China

Corresponding author: Hai-Xia Ma ( mahaixia@itbb.org.cn )

Academic editor: Jennifer Luangsa-ard
© 2024 An-Hong Zhu, Zi-Kun Song, Jun-Fang Wang, Hao-Wen Guan, Zhi Qu, Hai-Xia Ma.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Zhu A-H, Song Z-K, Wang J-F, Guan H-W, Qu Z, Ma H-X (2024) Multi-gene phylogenetic and taxonomic contributions to Xylaria (Ascomycota) associated with fallen fruits from China. MycoKeys 106: 23-41. https://doi.org/10.3897/mycokeys.106.124944
Open Access

Abstract

Morphological and phylogenetic analyses on samples of Xylaria species associated with fallen fruits from China were carried out, and two new species were described, namely X. aleuriticola and X. microcarpa. Xylaria aleuriticola is found on fallen fruits of Aleurites moluccana, and characterized by stromata dichotomously branched several times with long acute sterile apices, fertile parts roughened with perithecia and tomentose, and ellipsoid to fusiform ascospores. Xylaria microcarpa differs in its very small stromata with dark brown tomentum, light brown ascospores with an inconspicuous straight germ slit, and grows on leguminous pods. The differences between the new species and morphologically similar species are discussed. Phylogenetic analyses on ITS-RPB2-TUB sequences confirmed that the two species are clearly separated from other species of the genus Xylaria. Xylaria liquidambaris is reported as a new record from China. A key to the Xylaria species associated with fallen fruits and seeds reported from China is provided to facilitate future studies of the genus.

Key words

Ascomycota, fructicolous fungi, new species, seminicolous fungi, Xylariaceae

Introduction

Xylaria Hill ex Schrank, with more than 878 epithets listed in Index Fungorum (http://www.indexfungorum.org/Names/Names.asp, accessed on 22 November 2023), was currently the largest genus in the family Xylariaceae (Hsieh et al. 2010; Fournier et al. 2018a). The members of Xylaria have a worldwide distribution, but they are highly diverse in the tropics and subtropics (Dennis 1956; Ju and Rogers 1999; Ju and Hsieh 2007; Lodge et al. 2008; Fournier et al. 2011; Wangsawat et al. 2021). Species of Xylaria are saprobic, pathogenic, or endophytic and associated with a wide range of host (Rogers 1979a; Vannini et al. 1996; Whalley 1996; Crozier et al. 2006; Thomas et al. 2008; U’Ren et al. 2009; de Vega et al. 2010). According to the substrate in which these fungi grow, the taxa of the genus can be divided into four different ecological types, viz., wood-inhabiting type, termite nests inhabiting type, foliicolous type, and fructicolous/seminicolous type. The Xylaria species associated with fallen fruits and seeds preferred to somewhat substrate-specific (Rogers 1979b; Læssøe and Lodge 1994; Ju et al. 2018; Perera et al. 2020).

The generic concept of Xylaria was traditionally based on morphological studies (Dennis 1957, 1958; Rogers et al. 1987, 1988; San Martín and Rogers 1989; Fournier 2014; Fournier et al. 2020). In the past two to three decades, molecular phylogenetic analysis was carried out on the family Xylariaceae by using a single-gene to multi-gene (Lee et al. 2000; Bahl et al. 2005; Ju et al. 2004, 2007; Peláez et al. 2008; Hsieh et al. 2010; Læssøe et al. 2013; Wangsawat et al. 2021). Nuclear ribosomal DNA, ITS-5.8S, and protein-coding gene are commonly used for inferring phylogenetic relationships (Tang et al. 2009; Visser et al. 2009). The new genus Neoxylaria was segregated from Xylaria based on morphological and phylogenetic evidence (Konta et al. 2020). The genus Xylaria is quite common in China, however, molecular studies on the Xylaria are still poorly used (Teng 1963; Tai 1979; Li and Li 1994; Xu 1999; Zhu and Guo 2011; Ma et al. 2011, 2013). Especially, the phylogenetic relationships inferring from multi-gene between Xylaria species associated with fruits and other Xylaria species as well as other genera in the Xylariaceae remain unsolved, and the species diversity and geographical distribution in China are unclear.

During the investigation of xylariaceous taxa from China, 18 samples belonging to 3 species of Xylaria associated with fruits were collected. Based on morphological and multi-gene phylogenetic evidences, two new species and one new Chinese record are introduced in this study.

Materials and methods

Sample collection and morphological studies

The studied samples were collected from south China during 2013–2020. The fallen fruits bearing xylariaceous stromata were dried with a SX-770 portable drier of Foshan Taomeihui Electric Appliance Co., Ltd (Guangdong, China), and deposited in the Fungarium of Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences (FCATAS). Macro- and micro-morphological studies were carried out in this study and followed Ma et al. (2022). Stromatal surface and perithecia were observed and measured by using a VHX-600E 3D microscope of the Keyence Corporation (Osaka, Japan). Microscopic observations and examinations were performed by using an Olympus IX73 inverted fluorescence microscope (Tokyo, Japan) and the CellSens Dimensions Software (Olympus, Tokyo, Japan). In presenting ascospore size variation, 5% of measurements were excluded from each end of the range and given in parentheses. The following abbreviations were used: KOH = 5% potassium hydroxide, SDS = 1% sodium dodecyl sulfate, M = mean ascospore length × mean ascospore width, Q = the ration of mean ascospore length / mean ascospore width, n (a/b) = number of ascospores (a) measured from number of specimens (b). Colour terms followed Rayner (1970).

DNA extraction, amplification, and sequencing

Total genomic DNA was extracted from dried specimens using a cetyltrimethylammonium bromide (CTAB) rapid extraction kit (Aidlab Biotechnologies, Beijing) following its instruction with some modifications as in Song et al. (2022). Three DNA gene fragments, the internal transcribed spacer (ITS) region, RNA polymerase II subunit (RPB2) gene, and β-tubulin (TUB) were amplified using the primer pairs ITS5/ITS4 (White et al. 1990), fRPB2-5F/fRPB2-7cR (Liu et al. 1999), and T1/T22 (O’ Donnell et al. 1997), respectively. The PCR procedures for the three sequences followed Pan et al. (2022). Newly generated sequences were uploaded on GenBank and listed in Table 1.

Table 1.
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List of taxa used for the phylogenetic reconstruction. GenBank accession numbers, specimen numbers, origin and host are given. Holotype specimens are labelled with HT. Species highlighted in bold were derived from this study. N/A: not available.

Species Specimen No. Origin Host GenBank Accession Number
ITS RPB2 ß-tubulin
Amphirosellinia fushanensis HAST91111209(HT) China dead twigs GU339496 GQ848339 GQ495950
A. nigrospora HAST91092308(HT) China dead twigs GU322457 GQ848340 GQ49595
Astrocystis bambusae HAST89021904 China bamboo culms GU322449 GQ844836 GQ495942
As. mirabilis HAST94070803 China bamboo culms GU322448 GQ844835 GQ49594
Kretzschmaria clavus JDR114 French Guiana wood EF026126 GQ844789 EF025611
K. guyanensis HAST89062903 China bark GU300079 GQ844792 GQ478214
K. neocaledonica HAST94031003 China bark GU300078 GQ844788 GQ478213
Nemania abortiva BiSH467(HT) USA – GU292816 GQ844768 GQ470219
N. diffusa HAST91020401 China bark GU292817 GQ844769 GQ470220
N. sphaeriostomum JDR261 USA wood GU292821 GQ844774 GQ470224
Podosordaria mexicana WSP176 Mexico horse dung GU324762 GQ853039 GQ844840
P. muli WSP167(HT) Mexico mule dung GU324761 GQ853038 GQ844839
Poronia pileiformis WSP88113001(ET) China cow dung GU324760 GQ853037 GQ502720
Rosellinia merrillii HAST89112601 China bark GU300071 GQ844781 GQ470229
R. sanctacruciana HAST90072903 China fronds of Arenga engleri GU292824 GQ844777 GQ470227
Xylaria adscendens HAST570 Guadeloupe wood GU300101 GQ844817 GQ487708
X. aethiopica YMJ1136 Ethiopia pods of Millettia ferruginea MH790445 MH785222 MH785221
X. aleuriticola FCATAS858(HT) China fruits of Aleurites moluccana MZ648856 MZ707101 MZ695778
X. aleuriticola FCATAS859 China fruits of Aleurites moluccana MZ648857 MZ707102 MZ695779
X. aleuriticola FCATAS862 China fruits of Aleurites moluccana MZ648858 N/A MZ695780
X. aleuriticola FCATAS863 China fruits of Aleurites moluccana MZ648859 N/A MZ695781
X. aleuriticola FCATAS864 China fruits of Aleurites moluccana MZ648860 MZ707103 N/A
X. allantoidea HAST94042903 China trunk GU324743 GQ848356 GQ502692
X. amphithele HAST529 Guadeloupe dead leaves GU300083 GQ844796 GQ478218
X. apoda HAST90080804 China bark GU322437 GQ844823 GQ495930
X. arbuscula HAST89041211 China bark GU300090 GQ844805 GQ478226
X. atrosphaerica HAST91111214 China bark GU322459 GQ848342 GQ495953
X. berteri HAST90112623 China wood GU324749 GQ848362 AY951763
X. brunneovinosa HAST720(HT) China ground of bamboo plantation EU179862 GQ853023 GQ502706
X. cirrata HAST664(ET) China ground of vegetable farm EU179863 GQ853024 GQ502707
X. cranioides HAST226 China wood GU300075 GQ844785 GQ478210
X. cubensis JDR860 USA wood GU991523 GQ848365 GQ502700
X. culleniae JDR189 Thailand pod GU322442 GQ844829 GQ495935
X. curta HAST92092022 China bark GU322443 GQ844830 GQ495936
X. digitata HAST919 Ukraine wood GU322456 GQ848338 GQ495949
X. enterogena HAST785 French Guiana wood GU324736 GQ848349 GQ502685
X. escharoidea HAST658(ET) China ground of mango orchard EU179864 GQ853026 GQ502709
X. fabacearum MFLU16-1061(HT) Thailand seed pods of Fabaceae NR171104 MT212202 MT212220
X. fabaceicola MFLU16-1072(HT) Thailand seed pods of Fabaceae NR171103 MT212201 MT212219
Xylaria sp. FCATAS917 China pericarps of Fagus longipetiolata MZ621171 MZ707122 MZ695801
X. feejeensis HAST92092013 China bark GU322454 GQ848336 GQ495947
X. fimbriata HAST491 Martinique termite nest GU324753 GQ853022 GQ502705
X. fissilis HAST367 Martinique bark GU300073 GQ844783 GQ470231
X. frustulosa HAST92092010 China bark GU322451 GQ844838 GQ495944
X. cf. glebulosa HAST431 Martinique Fruits of Swietenia macrophylla GU322462 GQ848345 GQ495956
X. globosa HAST775 Guadeloupe bark GU324735 GQ848348 GQ502684
X. grammica HAST479 China wood GU300097 GQ844813 GQ487704
X. griseosepiacea HAST641(HT) China ground of mango orchard EU179865 GQ853031 GQ502714
X. haemorrhoidalis HAST89041207 China bark GU322464 GQ848347 GQ502683
X. hedyosmicola FCATAS856(HT) China leaves of Hedyosmum orientale MZ227121 MZ221183 MZ683407
X. hypoxylon HAST95082001 China wood GU300095 GQ844811 GQ487703
X. intracolorata HAST90080402 China bark GU324741 GQ848354 GQ502690
X. ianthinovelutina HAST553 Martinique fruit of Swietenia macrophylla GU322441 GQ844828 GQ495934
X. intraflava HAST725(HT) China ground of bamboo plantation EU179866 GQ853035 GQ502718
X. juruensis HAST92042501 China Arenga engleri GU322439 GQ844825 GQ495932
X. laevis HAST95072910 China bark GU324747 GQ848360 GQ502696
X. lindericola FCATAS852 China leaves of Lindera robusta MZ005635 MZ031982 MZ031978
X. liquidambaris HAST93090701 China fruits of Liquidambar formosana GU300094 GQ844810 GQ487702
X. liquidambaris FCATAS872 China fruits of Liquidambar formosana MZ620273 MZ707106 N/A
X. liquidambaris FCATAS874 China fruits of Liquidambar formosana MZ620275 MZ707107 MZ695775
X. liquidambaris FCATAS877 China fruits of Liquidambar formosana MZ620276 MZ707109 N/A
X. liquidambaris FCATAS879 China fruits of Liquidambar formosana MZ620278 MZ707110 N/A
X. meliacearum JDR148 Puerto Rico petioles and infructescence of Guarea guidonia GU300084 GQ844797 GQ478219
X. microcarpa FCATAS883(HT) China pods of legume MZ648823 MZ707111 MZ695776
X. microcarpa FCATAS885 China pods of legume MZ648824 N/A MZ695777
X. microceras HAST414 Guadeloupe wood GU300086 GQ844799 GQ478221
X. montagnei HAST495 Martinique wood GU322455 GQ848337 GQ495948
X. multiplex JDR259 USA wood GU300099 GQ844815 GQ487706
X. muscula HAST520 Guadeloupe dead branch GU300087 GQ844800 GQ478222
X. nigripes HAST653 China ground of mango orchard GU324755 GQ853027 GQ502710
X. ochraceostroma HAST401(HT) China ground of mango orchard EU179869 GQ853034 GQ502717
X. oligotoma HAST784 French Guiana wood GU300092 GQ844808 GQ487700
X. ophiopoda HAST93082805 China bark GU322461 GQ848344 GQ495955
X. oxyacanthae JDR859 USA seeds of Crataegus monogyna GU322434 GQ844820 GQ495927
X. palmicola PDD604 New Zealand fruits of palm GU322436 GQ844822 GQ495929
X. papulis HAST89021903 China wood GU300100 GQ844816 GQ487707
X. phyllocharis HAST528 Guadeloupe dead leaves GU322445 GQ844832 GQ495938
X. plebeja HAST91122401 China trunk of Machilus zuihoensis GU324740 GQ848353 GQ502689
X. polymorpha JDR1012 USA wood GU322460 GQ848343 GQ495954
X. polysporicola FCATAS848(HT) China leaves of Polyspora hainanensis MZ005592 MZ031980 MZ031976
X. reevesiae HAST90071609(HT) China fruits of Reevesia formosana GU322435 GQ844821 GQ495928
X. regalis HAST920 India log of Ficus racemosa GU324745 GQ848358 GQ502694
X. rogersii FCATAS915(HT) China fruits of Magnolia sp. MZ648827 MZ707121 MZ695800
X. schimicola FCATAS896(HT) China fruits of Schima noronhae MZ648850 MZ707114 MZ695787
X. schweinitzii HAST92092023 China bark GU322463 GQ848346 GQ495957
X. scruposa HAST497 Martinique wood GU322458 GQ848341 GQ495952
X. sicula HAST90071613 China fallen leaves GU300081 GQ844794 GQ478216
Xylaria sp. 6 JDR258 USA leaves of Tibouchina semidecandra GU300082 GQ844795 GQ478217
X. striata HAST304 China branch of Punica granatum GU300089 GQ844803 GQ478224
X. telfairii HAST90081901 China bark GU324738 GQ848351 GQ502687
X. theaceicola FCATAS903(HT) China fruits of Schima villosa MZ648848 MZ707115 MZ695788
X. tuberoides HAST475 Martinique wood GU300074 GQ844784 GQ478209
X. venustula HAST 88113002 China bark GU300091 GQ844807 GQ487699
X. vivantii HAST519(HT) Martinique fruits of Magnolia sp. GU322438 GQ844824 GQ495931
X. wallichii FCATAS923(HT) China fruits of Schima wallichii MZ648861 MZ707118 MZ695793

Phylogenetic analyses

Xylaria species associated with fallen fruits and seeds were subjected to phylogenetic analyses in other various species of Xylaria and closely related genera including Amphirosellinia, Astrocystis, Kretzschmaria, Nemania, Podosordaria, and Rosellinia (Table 1). Poronia pileiformis (Berk.) Fr. was selected as an outgroup (Wangsawat et al. 2021; Ma et al. 2022).

The sequences of ITS, RPB2 and TUB2 were aligned individually using the online MAFFT tool (http://mafft.cbrc.jp/alignment/server/index.html), and improved manually using BioEdit 7.0.5.3 (Hall 1999) and ClustalX 1.83 (Thompson et al. 1997). The individual gene data sets were concatenated using the MEGA 6.0 (Tamura et al. 2011). The concatenated data set of ITS, RPB2 and TUB (ITS-RPB2-TUB) data set of studied species were carried out using Bayesian inference (BI) and maximum likelihood (ML) analyses. Maximum likelihood (ML) analysis was conducted by raxmlGUI 2.0 using rapid bootstrapping with 1000 replicates, and GTRGAMMA+G as a substitution model (Felsenstein 1981). Bayesian inference (BI) analysis was performed in MrBayes 3.2.6 with jModelTest 2 conducting model discrimination (Huelsenbeck and Ronquist 2001). Six simultaneous Markov chains were run from random starting trees for 1 million generations, and trees were sampled every 1000th generations. The first 25% of sampled trees were discarded as burn-in, and the remaining were used to calculate the posterior probability (PP) of each branch (Larget and Simon 1999). The combined alignment and phylogenetic tree were deposited in Figshare (https://figshare.com/s/e1c181f1e3a56164ecc3).

Results

Molecular phylogeny

Eighteen Xylaria species associated with fallen fruits and seeds were subjected to phylogenetic analyses based on ITS-RPB2-TUB dataset in Xylariaceae. The BI and ML analyses generated highly similar topologies, the ML tree is presented with bootstrap values ≥ 75% and Bayesian posterior probabilities ≥ 0.90 respectively (Fig. 1).

Figure 1. 

Phylogenetic tree of Xylaria based on the multigene alignment of ITS-RPB2-TUB2 in the ML tree. ML bootstrap support (BS) ≥ 75% and Bayesian posterior probabilities (PP) ≥ 0.90 are given at the nodes in this order. New species in this study are indicated in bold.

In the phylogenetic tree (Fig. 1), the genus Podosordaria separated from other genera, Amphirosellinia, Astrocystis, Kretzschmaria, Nemania, and Rosellinia were nested within Xylaria clade. All Xylaria species associated with fallen fruits and seeds were distributed within clade HY or clade PO as shown in Hsieh et al. (2010) and Ma et al. (2022). In HY clade, a Xylaria species on fruits of Fagus longipetiolata and four known Xylaria species associated with pericarps of fruits, including X. schimicola Hai X. Ma & Yu Li, X. theaceicola Hai X. Ma & Yu Li, X. wallichii Hai X. Ma & Yu Li and X. liquidambaris J.D. Rogers, Y.M. Ju & F. San Martín, formed a subclade with high support values (BS = 88, PP = 1.00). In the PO clade, the new species X. aleuriticola on fruits of Aleurites moluccana and X. microcarpa on pods grouped with six fructicolous Xylaria species including X. aethiopica J. Fourn., Y.M. Ju, H.M. Hsieh & U. Lindem., X. ianthinovelutina (Mont.) Fr., X. culleniae Berk. & Broome, X. fabaceicola R.H. Perera, E.B.G. Jones & K.D. Hyde, X. vivantii Y.M. Ju, J.D. Rogers, J. Fourn. & H.M. Hsieh, X. rogersii Hai X. Ma & Yu Li, and X. juruensis Henn. on Arenga engleri in a subclade with high support values (BS = 100, PP = 1.00).

Taxonomy

Xylaria aleuriticola Hai X. Ma, A.H. Zhu & Yu Li, sp. nov.

MycoBank No: 840908
Fig. 2

Type

China. Yunnan Province, Jinghong City, Xishuangbanna Primeval Forest Park, on buried fruits of Aleurites moluccana (L.) Willd (Euphorbiaceae), 22 October 2013, Ma HaiXia, FCATAS 858 (Col. 11).

Etymology

Aleuriticola (Lat.): referring to the host which the fungus inhabits.

Teleomorph

Stromata upright or prostrate, solitary to often densely clustered, dichotomously branched several times, or unbranched infrequently, 2–11 cm total height, long-stipitate; fertile parts 7–30 mm high × 1.0–2.5 mm broad, narrowly fusiform to cylindrical, often flattened, with acute sterile apices up to 8 mm long, strongly nodulose, particularly tomentose; stipes 12–90 mm high × 0.7–2.6 mm broad, terete to rarely flattened, most often contorted, usually ill-defined, with conspicuously tomentose, arising from a slightly enlarged pannose base; surface roughened with perithecial mounds and tomentose except for stromatal apices, black brown to black; interior white to cream, tan at center, solid, woody. Perithecia subglobose, 300–500 µm. Ostioles conic-papillate. Asci eight-spored arranged in uniseriate manner, cylindrical, long-stipitate, (90–)110–135(–150) µm total length, the spore-bearing parts (55–)60–70(–75) µm long × (5.5–)6.0–7.0(–7.5) µm broad, the stipes 30–70 µm long, with apical ring bluing in Melzer’s reagent, urn-shaped, 2.0–2.8 µm high × 1.0–1.8 µm diam. Ascospores brown to dark brown, unicellular, ellipsoid to fusiform, inequilateral, with narrowly rounded ends, occasionally one end slightly pinched, smooth, (7.1–)7.5–9.5(–10.5) × (3–)3.5–4(–4.5) µm (M = 8.1 × 3.6 µm, Q = 2.3, n = 60/2), with a conspicuous straight germ slit spore-length or slightly less than spore-length, lacking a hyaline sheath or appendages visible in india ink or 1% SDS.

Figure 2. 

Xylaria aleuriticola (FCATAS858, holotype) a, b stromata on fallen fruits c stromatal surface d, e section through stroma, showing perithecia f asci in Melzer’s reagent g asci in water h ascospores in Melzer’s reagent i ascal apical ring in Melzer’s reagent j, k ascospore in 1% SDS l ascospore in India ink m ascospore with germ slit in India ink. Scale bars: 2 cm (a, b); 100 µm (c, e); 200 µm (d); 10 µm (f–m).

Additional specimen examined

China. Yunnan Province, Jinghong City, Xishuangbanna Primeval Forest Park, on buried fruits of Aleurites moluccana (Euphorbiaceae), 22 October 2013, Ma HaiXia, FCATAS 859 (Col. 23); 22 January 2015, Ma Haixia, FCATAS 862 (Col. 231), FCATAS 863 (Col. 232), FCATAS 864 (Col. 238), FCATAS 865 (COL. 270).

Notes

Xylaria aleuriticola, associated with the pericarps of A. moluccana (Euphorbiaceae), is characterized by stromata dichotomously branched several times with long acute sterile apices, fertile parts roughened with perithecia and tomentose, and tomentose stipes. It is similar to X. culleniae Berk. & Broome by having dichotomously branched stromata and ascospores dimensions, but the latter species branches dichotomously only once in fertile parts, ascospores surrounded with a hyaline sheath and non-cellular appendages, and grows on capsules of Cullenia excelsa (Malvaceae) (Rogers et al. 1988; Ju et al. 2018). Xylaria euphorbiicola Rehm was described on fruits of Euphorbia (Euphorbiaceae) from Brazil, but it has unbranched stromata, lacking perithecial mounds, overlain with a brown striped outermost layer, and smaller discoid apical ring 1µm high × 1.5–2 µm broad (Ju et al. 2018). Xylaria ianthinovelutina somewhat resembles X. aleuriticola in stromatal morphology, but it has stronger stromata, larger ascospores (9–)9.5–11(–12) × (3.5–)4–4.5(–5) µm (M = 10.3 × 4.0 µm), and often associated with leguminous pods (Dennis 1956, 1957; Ju et al. 2018), while stromata of the new speices has sharper and longer sterile apices, more forked. Xylaria luzonensis Henn. differs from X. aleuriticola by its smaller stromata (1.5–3 cm long × 0.5–1 mm diam), smaller perithecia (200–300 µm diam), slightly smaller apical ring (1–1.5 µm high × 1.5 µm broad), light brown ascospores, and grows on pod of Bauhinia cumingiana (Fabaceae) (Ju et al. 2018). Xylaria apeibae Mont. is close to X. aleuriticola in stromatal morphology, from which it differs mainly by having smaller stromata 4 cm long × 0.8–1.5 mm diam, light brown and larger ascospores (9.5–)10–12(–13) × (3–)3.5–4(–4.5) µm (M = 11.0 × 3.7 µm), and grows on fruits of Apeiba species (Tiliaceae) (Ju et al. 2018). In the phylogenetic analysis (Fig. 1), X. aleuriticola clustered together with high support values (BS = 98, PP = 1.00) with X. fabaceicola, but the latter species is distinguished by its smaller stromata 13–25 mm long, pale brown to brown ascospores with a hyaline sheath and appendages, and the fact that it grows on decaying pods of Fabaceae (Perera et al. 2020).

Xylaria microcarpa Hai X. Ma & Yu Li, sp. nov.

MycoBank No: 840911
Fig. 3

Type

China. Yunnan Province, Xishuangbanna Prefecture, Dadugang Town, Guanping Village, on legume pods, 21 January 2015, Haixia Ma, FCATAS 883 (Col. 233).

Etymology

Microcarpa (Lat.): referring to its stroma that it is very small.

Teleomorph

Stromata upright or prostrate, often densely gregarious in large groups, unbranched, cylindrical to filiform, with acute sterile apices, on tomentose stipes, 3.5–9 mm total height; fertile parts 2–6 mm high × 0.6–1.5 mm broad, filiform to cylindrical, brown tomentose dense or sparse, nodulose with perithecial contours exposed; stipes 1.5–4 mm high × 0.3–0.5 mm broad, terete, with conspicuously dark brown tomentose, arising from slighly enlarged base; surface black, interior light yellow, solid, woody. Perithecia subglobose, 300–500 µm. Ostioles conic-papillate. Asci eight-spored arranged in uniseriate manner, cylindrical, long-stipitate, (96–)105–125(–140) µm total length, the spore-bearing parts (56–)60–70(–75) µm long ×(6.0–)6.4–7.1(–7.6) µm broad, the stipes 30–56 µm long, with apical ring bluing in Melzer’s reagent, tubular or urn-shaped, 1.5–2.5 (–2.9) µm high × 1.4–1.8 µm diam. Ascospores light brown, unicellular, ellipsoid-inequilateral, with narrowly rounded ends, sometimes with pinched on one end, smooth, (9.5–)10–11(–11.5) ×(4.5–) 5–6(–6.2) µm (M = 10.5 × 5.5 µm, Q = 1.9, n = 60/2), with a inconspicuous straight germ slit almost spore-length, lacking a sheath or appendages visible in india ink or 1% SDS.

Figure 3. 

Xylaria microcarpa (FCATAS883, holotype) a stroma on fallen pod b stromatal surface c section through stroma, showing perithecia d asci with ascal apical ring in Melzer’s reagent e asci in India ink f, g ascospores in water h ascospores in Melzer’s reagent i ascospore with germ slit in India ink j ascospore in India ink k ascospores in Melzer’s reagent l ascal apical ring in Melzer’s reagent. Scale bars: 0.3 mm (a); 200 µm (b, c); 10 µm (d–l).

Additional specimen examined

China. Yunnan Province, Xishuangbanna Prefecture, Xishuangbanna Tropical Botanical Garden, on legume pods, 20 January 2015, Haixia Ma, FCATAS 885 (Col. 239).

Notes

Xylaria microcarpa is characterized by very small stromata growing in groups, overlain with a dark brown tomentum, ascospores light brown with an inconspicuous straight germ slit, lacking a sheath or appendages, and grows on leguminous pods. The new species resembles X. fabacearum R.H. Perera, E.B.G. Jones & K.D. Hyde by sharing small stromata and ascospores length dimensions, but differs from the latter species in having stromata branched sometimes, stromatal surface without tomentose, brown to dark brown ascospores with conspicuous straight germ slit (Perera et al. 2020). Xylaria luzonensis on Bauhinia cumingiana (Fabaceae) differs from X. microcarpa by having branched and larger stromata, smaller perithecia, and smaller ascospores (8–)8.5–9.5(–10) × 3–3.5(–4) µm (M = 8.9 × 3.4 µm) (Ju et al. 2018). Xylaria microcarpa is somewhat similar to X. ianthinovelutina and X. culleniae in stromatal surface with tomentum and grow on leguminous pods, but the later two taxa differ in larger stromata, ascospores with a straight germ slit slightly less than spore-length, surrounded with a hyaline sheath and non-cellular appendages (Ju et al. 2018). The phylogenetic tree showed that Xylaria microcarpa and X. aethiopica J. Fourn., Y.M. Ju, H.M. Hsieh & U. Lindem are sister taxa with a strong supported branch in BI tree (BS=0.98), but X. aethiopica is distinct morphologically with larger stromata 15–30 mm total height, brown to dark brown and slightly larger ascospores (9.7–)11–13(–13.5) × (3.5–)3.8–4.5(–4.9) µm (M = 11.9 × 4.1 µm) with a conspicuous straight germ and appendages, and grows on fallen woody pods of Millettia ferruginea (Fabaceae) (Fournier et al. 2018b).

Xylaria liquidambaris J.D. Rogers, Y.M. Ju & F. San Martín, Sydowia 54(1): 92. 2002

Fig. 4

Teleomorph

Stromata upright, solitary or sometimes clustered, unbranched or occasionally branched, 1.2–8.0 cm total height; fertile parts 6–25 mm high × 1.5–5.0 mm broad, cylindrical with acute sterile apices, at times longitudinally furrowed, with wrinkles isolating somewhat prominent perithecia; stipes 6–55 mm high × 1.0–2.5 mm broad, glabrous to pubescent arising from a pannose base; surface dark brown to black, interior white, with dark brown to black a circle, and white at center. Texture solid, soft, woody. Perithecia subglobose, 250–400 µm. Ostioles conic-papillate. Asci eight-spored arranged in uniseriate manner, cylindrical, long-stipitate, (110–)125–145(–165) µm total length, the spore-bearing parts (80–)90–105(–115) µm long × (6–)7–8(–8.5) µm broad, the stipes 30–60 µm long, with apical ring bluing in Melzer’s reagent, inverted hap-shaped to more or less rectangular, 2.5–3.5 µm high × 2.0–2.5 µm diam. Ascospores brown, unicellular, ellipsoid-inequilateral with narrowly to broadly rounded ends, smooth, (12.5–)13–14(–15) × (4.8–)5.5–6.5(–6.8) µm (M = 13.5 × 6.1 µm, Q = 2.2, n = 90/3), with spiraling germ slit, lacking a sheath or appendages in india ink or 1% SDS.

Specimens examined

China. Guangdong Province, Chebaling Nature Reserve, on fruits of Liquidambar formosana, 26 June 2010, Ma Haixia, Col. 10062607; Fengkai County, Heishiding Nature Reserve, on fruits of L. formosana, 2 July 2010, Ma Haixia, Col. 10070206; Jiangxi Province, Guanshan Nature Reserve, on fruits of L. formosana, 21 June 2013, Ma Haixia, FCATAS 873 (Col. 16); Fuzhou City, Tang Xianzu Museum, on fruits of L. formosana, 17 June 2013, Ma Haixia, FCATAS 877 (Col. 36); Anyuan County, Sanbai Mountain Nature Reserve, on fruits of L. formosana, 15 August 2016, Ma Haixia, FCATAS 878 (Col. O37); Zhejiang Province, Tianmu Mountain Nature Reserve, on fruits of L. formosana, 6 August 2013, Ma Haixia, FCATAS 872 (Col. 10); Gutian Mountain Nature Reserve, on fruits of L. formosana, 13 August 2013, Ma Haixia, FCATAS 496 (Col. 29); Anhui Province, Huangshan City, Qiman County, Guniujiang Nature Reserve, on fruits of L. formosana, 8 August 2013, Ma Haixia, FCATAS 874 (Col. 19); Huangshan Nature Reserve, on fruits of L. formosana, 27 June 2019, Ma Haixia, FCATAS 879 (Col. P6); Hainan Province, Diaoluoshan Nature Reserve, on fruits of L. formosana, 31 December 2020, Ma Haixia, FCATAS 880 (Col. Z211).

Figure 4. 

Xylaria liquidambaris (a from Col.10062607 b–m from FCATAS874) a, b stromata on fallen fruits c stromatal surface d, e section through stroma, showing perithecia f asci in Melzer’s reagent g, l ascospore in water h ascospores with germ slit in India ink i, j ascal apical ring in Melzer’s reagent k ascospores with germ slit in Melzer’s reagent m asci in water. Scale bars: 1.5 cm (a, b); 100 µm (c, d, e); 20 µm (f); 10 µm (g–m).

Notes

Xylaria liquidambaris was originally described by Rogers et al. (2002) from USA, and has high specificity to fruits of Liquidambar (Altingiaceae). It is characterized by unbranched stromata with acute sterile apex, embedded to slightly prominent perithecia with longitudinal striations, brown ascospores with long spiraling germ slit (Rogers et al. 2002). These Chinese materials well fit the descriptions and illustrations of X. liquidambaris by Rogers et al. (2002).

Discussion

In the present study, two new Xylaria species associated with fallen fruits were described and compared with closely related species based on morphological and molecular data. In addition, X. liquidambaris has been reported from China for the first time. We included eighteen Xylaria species on fallen fruits and seeds in the phylogenetic trees based on a combined ITS-RPB2-TUB2 dataset. The phylogenetic analyses showed that seventeen species are mainly distributed in three different subclades, while Xylaria cf. gleculosa clustered with Xylaria species on wood, which is consistent with the previous studies (Hsieh et al. 2010; Perera et al. 2020; Ma et al. 2022).

By inclusion of the two new species we described here, thirty-seven species on fallen fruits and seeds are now recognized in the genus Xylaria (Rogers 1979b; Stowell and Rogers 1983; Rogers et al. 2002; Pande and Waingankar 2004; Rönsch et al. 2010; Hsieh et al. 2010; Dillon et al. 2018; Ju et al. 2018; Fournier et al. 2018b; Perera et al. 2020; Ma et al. 2022). Compared to the number of Xylaria species on fruits and seeds, the available sequences of these species in NCBI are relatively fewer. Most species in this group are lacking DNA sequences, and some species only have one or two sequences, for X. carpophila just has ITS sequences, and X. karyophthora from Guyana with ITS and RPB2 sequences available (Dillon et al. 2018; Vu et al. 2019). Moreover, almost half the taxa, e.g., X. apeibae Mont., X. clusiae K.F. Rodrigues, X. duranii San Martín & Vanoye, X. euphorbiicola Rehm, X. guazumae San Martín & J.D. Rogers, X. heloidea Penz. & Sacc., X. himalayensis Narula & Rawla, X. jaliscoensis San Martín, J.D. Rogers & Y.M. Ju, X. luzonensis Henn., X. magnolia J.D. Rogers, X. magnolia var. microspora J.D. Rogers, Y.M. Ju & Whalley, X. patrisiae Henn., X. psidii J.D. Rogers & Hemmes, X. rhizocola (Mont.) Fr., X. rossmanae Y.M. Ju, J.D. Rogers, X. terminaliae-bellericae Pande & Waingankar, X. terminaliae-crenulatae Pande & Waingankar, and X. warburgii Henn., still have no available sequences. The current molecular study of Xylaria usually uses ITS, RPB2, TUB, and α-ACT (Hsieh et al. 2010; Fournier et al. 2018b; Perera et al. 2020; Ma et al. 2022), which is not so sufficient. In recent years, genome sequencing, sanger sequencing and next-generation sequencing have been used in some macrofungi groups for inferring phylogenetic relationships (Wibberg et al. 2021; Wang et al. 2023). To further understand the taxonomy and phylogeny of Xylaria associated with fruits and seeds, newly collected specimens from their original regions, more taxa and more DNA sequences need to be included in future study.

Dichotomous key to species of Xylaria associated with fruits and seeds in China

1 Ascospores pale or subhyaline 2
– Ascospores brown to dark brown 5
2 Ascospores with a conspicuous straight germ slit X. theaceicola
– Ascospores without a germ slit or inconspicuous germ slit 3
3 Stromata with half- to fully exposed perithecial mounds, frequently dichotomously branched X. wallichii
– Stromata with inconspicuous perithecial mounds, unbranched in most cases 4
4 Stromata associated with fruits of Magnolia (Magnoliaceae); ascospores (13.0–)13.8–15.0(–15.6) × (3.3–) 3.6–4.0(–4.4) µm X. rogersii
– Stromata associated with fruits of Schima noronhae (Theaceae); ascospores (9.5–)10.5–12.0(–13.0) × (1.6–)1.9–2.5(–3.0) µm X. schimicola
5 Stromata glabrous on the fertile part 6
– Stromata tomentose on the fertile part 10
6 Ascospores with a spiral germ slit, (12.5–)13–14(–15) × (4.8–)5.5–6.5(–6.8) µm X. liquidambaris
– Ascospores with a straight germ slit 7
7 Stromata associated with pericarps of fruits 8
– Stromata associated with endocarps of fruits 9
8 Stromata associated with fruits of Fagus longipetiolata (Fagaceae); ascospores (11.0–)11.8–13.5(–15) × (6–)6.5–7.5(–8) µm Xylaria sp.
– Stromata associated with fruits of Sloanea (Elaeocarpaceae); ascospores (9.5–)10–11.5(–12.5) × (3.5–)4–4.5(–5) µm X. warburgii
9 Stromata on fallen fruits of Reevesia formosana (Sterculiaceae); ascospores (8.5–)9–10.5(–11) × (4–)4.5–5.5(–6) µm X. reevesiae
– Stromata on seeds of Crataegus oxyacantha (Rosaceae); ascospores (10–)11–12(–12.5) × (4.5–)5.0–5.5(–6) µm X. oxyacanthae
10 Stromata unbranched; ascospores (9.5–)10–11(–11.5) × (4.5–) 5–6(–6.2) µm, with an inconspicuous straight germ slit X. microcarpa
– Stromata branched 11
11 Stromata on buried fruits of Aleurites moluccana (Euphorbiaceae); ascospores (7.1–)7.5–9.5(–10.5) × (3–)3.5–4(–4.5) µm X. aleuriticola
– Stromata on fruits of legume pods (Fabaceae); ascospores (9.6–)10.5–13(–14) × (3.9–)4.3–5.0(–5.5) µm X. ianthinovelutina

Acknowledgments

We wish to thank Dr. Wan-Jin Liao (Beijing Normal University) who helped us to identify the host.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

National Natural Science Foundation of China (Project Nos. 31972848); Central Public-interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences (No. 1630032022003); Yazhou Bay Scientific and Technological Project for Trained Talents of Sanya City (SCKJ-JYRC-2023-74).

Author contributions

Conceptualization and supervision, H.-X. M.; Resources, H.-X. M., Z. Q., and A.-H.Z.; Investigation, methodology and data curation, A.-H. Z., and S.-Z. K.; Software, J.-F. W. and H.-W. G.; Writing – original draft preparation, A.-H. Z.; Writing – review and editing, H.-X. M.; Project administration, H.-X. M.; Funding acquisition, H.-X. M. All authors have read and agreed to the published version of the manuscript.

Author ORCIDs

An-Hong Zhu https://orcid.org/0000-0002-2812-8108

Zi-Kun Song https://orcid.org/0000-0001-9532-2536

Jun-Fang Wang https://orcid.org/0009-0007-1197-6008

Hao-Wen Guan https://orcid.org/0009-0000-2714-4061

Hai-Xia Ma https://orcid.org/0000-0001-6699-7454

Data availability

Publicly available datasets were analyzed in this study. All newly generated sequences were deposited in GenBank (https://www.ncbi.nlm.nih.gov/genbank/; accessed on 26 July 2021; Table 1). All new taxa were deposited in MycoBank (https:www.mycobank.org/; accessed on 19 January 2024; MycoBank identifiers follow new taxa).

References

  • Crozier J, Thomas SE, Aime MC, Evans HC, Holmes KA (2006) Molecular characterization of fungal endophytic morphospecies isolated from stems and pods of Theobroma cacao. Plant Pathology 55(6): 783–791. https://doi.org/10.1111/j.1365-3059.2006.01446.x
  • de Vega C, Arista M, Ortiz PL, Talavera S (2010) Anatomical relations among endophytic holoparasitic angiosperms, autotrophic host plants and mycorrhizal fungi: A novel tripartite interaction. American Journal of Botany 97(5): 730–737. https://doi.org/10.3732/ajb.0900147
  • Dennis RWG (1958) Some Xylosphaeras of tropical Africa. Revista de Biologia (Lisboa) 1: 175–208.
  • Felsenstein J (1981) Evolutionary trees from DNA sequences: A maximum likelihood approach. Journal of Molecular Evolution 17(6): 368–376. https://doi.org/10.1007/BF01734359
  • Fournier J (2014) Update on European species of Xylaria.
  • Fournier J, Lechat C, Courtecuisse R (2018a) The genus Xylaria sensu lato (Xylariaceae) in Guadeloupe and Martinique (French West Indies) I. Taxa with penzigioid stromata. Ascomycete. Org 10(4): 131–176. https://doi.org/10.25664/ART-0239
  • Fournier J, Ju YM, Hsieh HM, Lindermann U (2018b) Xylaria aethiopica sp. nov. – a new pod-inhabiting species of Xylaria (Xylariaceae) from Ethiopia. Ascomycete. Org 10(5): 209–215.
  • Fournier J, Lechat C, Courtecuisse R (2020) The genus Xylaria sensu lato (Xylariaceae) in Guadeloupe and Martinique (French West Indies) III. Taxa with slender upright stromata. Ascomycete. Org 12(3): 81–164. https://doi.org/10.1128/jb.172.8.4238-4246.1990
  • Hsieh HM, Lin CR, Fang MJ, Rogers JD, Fournier J, Lechat C, Ju YM (2010) Phylogenetic status of Xylaria subgenus Pseudoxylaria among taxa of the subfamily Xylarioideae (Xylariaceae) and phylogeny of the taxa involved in the subfamily. Molecular Phylogenetics and Evolution 54(3): 957–969. https://doi.org/10.1016/j.ympev.2009.12.015
  • Ju YM, Rogers JD (1999) The Xylariaceae of Taiwan (excluding Anthostomella). Mycotaxon 73: 343–440.
  • Konta S, Hyde KD, Phookamsak R, Xu JC, Maharachchikumbura SSN, Daranagama DA, McKenzie EHC, Boonmee S, Tibpromma S, Eungwanichayapant PD, Samarakoon MC, Lu YZ (2020) Polyphyletic genera in Xylariaceae (Xylariales): Neoxylaria gen. nov. and Stilbohypoxylon. Mycosphere 11(1): 2629–2651. https://doi.org/10.5943/mycosphere/11/1/17
  • Læssøe T, Srikitikulchai P, Luangsa-ard JJD, Stadler M (2013) Theissenia reconsidered, including molecular phylogeny of the type species T. pyrenocrata and a new genus Durotheca (Xylariaceae, Ascomycota). IMA Fungus 4(1): 57–69. https://doi.org/10.5598/imafungus.2013.04.01.07
  • Li YL, Li HJ (1994) A novel species of Xylaria. Journal of Nanjing Agricultural University 17(3): 145–147.
  • Ma HX, Vasilyeva L, Li Y (2013) The genus Xylaria in the south of China – 7. Two penzigioid Xylaria species. Sydowia 65(2): 329–335.
  • Ma HX, Song ZK, Pan XY, Qu Z, Yang ZE, Li Y, Zhu AH (2022) Four new pale-spored species of Xylaria (Xylariaceae, Xylariales) with a key to worldwide species on fallen fruits and seeds. Biology 11(6): 885. https://doi.org/10.3390/biology11060885
  • O’ Donnell K, Cigelnik E (1997) Two Divergent Intragenomic rDNA ITS2 Types within a Monophyletic Lineage of the Fungus. Molecular Phylogenetics and Evolution 7(1): 103–116. https://doi.org/10.1006/mpev.1996.0376
  • Pan XY, Song ZK, Qu Z, Liu TD, Ma HX (2022) Three new Xylaria species (Xylariaceae, Xylariales) on fallen leaves from Hainan Tropical Rainforest National Park. MycoKeys 86: 47–63. https://doi.org/10.3897/mycokeys.86.71623
  • Peláez F, González V, Platas G, Sánchez-Ballesteros J, Rubio V (2008) Molecular phylogenetic studies within the Xylariaceae based on ribosomal DNA sequences. Fungal Diversity 31: 111–134.
  • Perera RH, Hyde KD, Maharachchikumbura SSN, Jones EBG, McKenzie EHC, Stadler M, Lee HB, Samarakoon MC, Ekanayaka AH, Camporesi E et al. (2020) Fungi on wild seeds and fruits. Mycosphere 11(1): 2108–2480. https://doi.org/10.5943/mycosphere/11/1/14
  • Rayner RW (1970) A mycological color chart. Cmi. & British Mycological Society Kew, London, UK.
  • Rogers JD (1979b) Xylaria magnoliae sp. nov. and comments on several other fruit-inhabiting species. Canadian Journal of Botany 57(8): 941–945. https://doi.org/10.1139/b79-115
  • Rogers JD, Callan BE, Samuels GJ (1987) The Xylariaceae of the rain forests of North Sulawesi (Indonesia). Mycotaxon 29: 113–172.
  • Rogers JD, Callan BE, Rossman AY, Samuels GJ (1988) Xylaria (Sphaeriales, Xylariaceae) from Cerro de la Neblina, Venezuela. Mycotaxon 31: 103–153.
  • Rogers JD, San Martín F, Ju YM (2002) A reassessment of the Xylaria on Liquidambar fruits and two new taxa on Magnolia fruits. Sydowia 54: 91–97.
  • Rönsch P, Rönsch S, Reiher A, Otto P (2010) Investigations on the fructicolous Xylaria delitschii and Xylaria oxyacanthae. Boletus 32: 106–122.
  • San Martín F, Rogers JD (1989) A preliminary account of Xylaria of Mexico. Mycotaxon 34: 283–373.
  • Song ZK, Zhu AH, Liu ZD, Qu Z, Li Y, Ma HX (2022) Three new species of Hypoxylon (Xylariales, Ascomycota) on a multigene phylogeny from Medog in southwest China. Journal of Fungi 8(5): 500. https://doi.org/10.3390/jof8050500
  • Stowell EA, Rogers JD (1983) Studies on Xylaria oxyacanthae. Mycotaxon 17: 433–444.
  • Tai FL (1979) Sylloge fungorum Sinicorum. Science Press, Peking.
  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28(10): 2731–2739. https://doi.org/10.1093/molbev/msr121
  • Tang AMC, Jeewon R, Hyde KD (2009) A re-evaluation of the evolutionary relationships within the Xylariaceae based on ribosomal and protein-coding gene sequences. Fungal Diversity 34: 127–155.
  • Teng SQ (1963) Fungi of China. Science Press, Peking.
  • Thomas SE, Crozier J, Aime MC, Evans HC, Holmes KA (2008) Molecular characterisation of fungal endophytic morphospecies associated with the indigenous forest tree, Theobroma gileri, in Ecuador. Mycological Research 112(7): 852–860. https://doi.org/10.1016/j.mycres.2008.01.008
  • Thompson JD, Gibson TJ, Plewniak F, Franois J, Higgins DG (1997) The CLUSTAL X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25(24): 4876–4882. https://doi.org/10.1093/nar/25.24.4876
  • U’Ren JM, Dalling JW, Gallery RE, Maddison DR, Davis EC, Gibson CM, Arnold AE, U’Ren JM (2009) Diversity and evolutionary origins of fungi associated with seeds of a neotropical pioneer tree: A case study for analysing fungal environmental samples. Mycological Research 113(4): 432–449. https://doi.org/10.1016/j.mycres.2008.11.015
  • Vannini A, Valentini R, Luisi N (1996) Impact of drought and Hypoxylon mediterraneum on oak decline in the Mediterranean region. Annales des Sciences Forestieres 53(2–3): 753–760. https://doi.org/10.1051/forest:19960251
  • Visser AA, Ros VID, de Beer ZW, Debets AJM, Hartog E, Kuyper TW, Læssøe T, Slippers B, Aanen DK (2009) Levels of specificity of Xylaria species associated with fungus-growing termites: A phylogenetic approach. Molecular Ecology 18(3): 553–567. https://doi.org/10.1111/j.1365-294X.2008.04036.x
  • Vu D, Groenewald M, de Vries M, Gehrmann T, Stielow B, Eberhardt U, Al-Hatmi A, Groenewald JZ, Cardinali G, Houbraken J, Boekhout T, Crous PW, Robert V, Verkley GJM (2019) Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdon fungi and reveals thresholds for fungal species and higher taxon delimitation. Studies in Mycology 92(1): 135–154. https://doi.org/10.1016/j.simyco.2018.05.001
  • Wang GS, Cai Q, Hao YJ, Bau T, Chen ZH, Li MX, Kraisitudomsook N, Yang ZL (2023) Phylogenetic and taxonomic updates of Agaicales, with an emphasis on Tricholomopsis. Mycology 14: 1–30. https://doi.org/10.1080/21501203.2023.2263031
  • Wangsawat N, Ju YM, Phosri C, Whalley AJS, Suwannasai N (2021) Twelve new taxa of Xylaria associated with termite nests and soil from Northeast Thailand. Biology 10(7): 575. https://doi.org/10.3390/biology10070575
  • White TJ, Burns 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, 315−322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
  • Wibberg D, Stadler M, Lambert C, Bunk B, Sprӧer C, Rückert C, Kalinowski J, Cox RJ, Kuhnert E (2021) High quality genome sequences of thirteen Hypoxylaceae (Ascomycota) strengthen the phylogenetic family backbone and enable the discovery of new taxa. Fungal Diversity 106(1): 7–28. https://doi.org/10.1007/s13225-020-00447-5
  • Xu AS (1999) A new species of Xylaria. Mycosystema 18(2): 137–140.
  • Zhu YF, Guo L (2011) Xylaria hainanensis sp. nov. (Xylariaceae) from China. Mycosystema 30(4): 526–528.
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