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Research Article
Paramphibambusa bambusicola gen. et. sp. nov., Arecophila xishuangbannaensis and A. zhaotongensis spp. nov. in Cainiaceae from Yunnan, China
expand article infoLi-Su Han, Nalin N. Wijayawardene§, Chao Liu, Li-Hong Han, Itthayakorn Promputtha|, Qiang Li, Abdallah M. Elgorban, Salim Al-Rejaie, Kazuaki Tanaka#, Dong-Qin Dai
‡ Qujing Normal University, Qujing, China
§ Tropical Microbiology Research Foundation, Pannipitiya, Sri Lanka
| Chiang Mai University, Chiang Mai, Thailand
¶ King Saud University, Riyadh, Saudi Arabia
# Hirosaki University, Aomori, Japan
Open Access

Abstract

Morphological comparisons and multi locus phylogenetic analyses (base on the combined genes of ITS, LSU, rpb2 and tub) demonstrated that three new saprobic taxa isolated from bamboo belong to Cainiaceae. These taxa comprise a novel genus Paramphibambusa (P. bambusicola sp. nov.) and two new species, Arecophila xishuangbannaensis and A. zhaotongensis. The three new taxa belong to Cainiaceae (Xylariales, Sordariomycetes) a poorly studied family, which now comprises eight genera. Paramphibambusa can be distinguished from other Cainiaceae genera in having ascomata with a neck and ascospores lacking longitudinal striation, germ slits or germ pores. The two new Arecophila species clustered in a clade with Arecophila sp. and A. bambusae. Detailed morphological descriptions, illustrations, and an updated phylogenetic tree are provided for the new taxa.

Key words

Bambusicolous fungi, multilocus phylogeny, taxonomy, Xylariales

Introduction

During our continuous investigation of bambusicolous fungi in Yunnan, China, we have collected one new genus and two new Arecophila K.D. Hyde species in Cainiaceae J.C. Krug. The family Cainiaceae (Xylariales, Sordariomycetes) was established by Krug (1978), with Cainia Arx & E. Müll as the type genus. Hongsanan et al. (2017) and Wijayawardene et al. (2020) accommodated Cainiaceae in Xylariomycetidae family incertae sedis. However, Hyde et al. (2020), Samarakoon et al. (2021), and Wijayawardene et al. (2022a) accepted Cainiaceae in Xylariales.

Maharachchikumbura et al. (2015, 2016) accepted five genera (viz., Amphibambusa D.Q. Dai & K.D. Hyde, Arecophila, Atrotorquata Kohlm. & Volkm.-Kohlm, Cainia, and Seynesia Sacc.) in Cainiaceae based on morphology and phylogeny. Subsequently, Mapook et al. (2020) introduced Longiappendispora Mapook & K.D. Hyde as a new member of Cainiaceae. Konta et al. (2021) transferred Endocalyx Berk. & Broome from Apiosporaceae to Cainiaceae. Li et al. (2022) revisited the monospecific genus Alishanica Karun et al. and synonymized it under Arecophila. Hence, seven genera (Amphibambusa, Arecophila, Atrotorquata, Cainia, Endocalyx, Longiappendispora, Seynesia) are accepted in Cainiaceae according to Hyde et al. (2020), Mapook et al. (2020), Jiang et al. (2021), and Konta et al. (2021).

Members of Cainiaceae are often found in tropical and temperate regions as saprobic fungi, which are usually associated with monocotyledons (mainly grasses) and fabaceous dicotyledons. Some Cainia species have been reported as causative agents of plant diseases, e.g., C. desmazieri C. Moreau & E. Müll (Krug 1978). Cainiaceae is morphologically characterized by immersed ascomata with a papillate ostiole, unitunicate asci, with a unique J+, apical ring or series of rings, and hyaline to pigmented, 1-septate ascospores with longitudinal striations or germ slits or germ pores, and usually surrounded by a sheath or appendages (Maharachchikumbura et al. 2016; Hyde et al. 2020). Asexual morphs of this family were reported as coelomycetous taxa, viz., Cainia and Endocalyx, that are characterized by black, pycnidial conidiomata, denticulate, sympodially proliferating conidiophores, branched or simple, septate, and phialidic conidiogenous cells, and hyaline, fusiform, or falcate to lunate conidia (Maharachchikumbura et al. 2016; Hyde et al. 2020; Konta et al. 2021; Wijayawardene et al. 2021a).

Arecophila was introduced by Hyde (1996) with A. gulubiicola K.D. Hyde as the type species. The genus Arecophila was initially regarded as a member of Amphisphaeriaceae G. Winter based on the morphology. Subsequently, Kang et al. (1999) accepted Arecophila as a member of Cainiaceae. Afterwards, the placement of Arecophila within the Cainiaceae has been confirmed based on analyses of partial LSU gene sequences (Jeewon et al. 2003; Senanayake et al. 2015; Li et al. 2022). Currently, 18 epithets are listed under Arecophila based on morpho-molecular study (Li et al. 2022; Index Fungorum 2023), and 15 epithets are listed under Arecophila in Species Fungorum (2023).

According to Jiang et al. (2022) and previous studies (Eriksson and Yue 1998; Hyde et al. 2002a, b; Zhou and Hyde 2002; Cai et al. 2003), only four Cainiaceae species are associated with bamboo (Amphibambusa hongheensis H.B. Jiang & Phookamsak, Arecophila bambusae Umali & K.D. Hyde, A. coronata (Rehm) Umali & K.D. Hyde and A. nypae K.D. Hyde) in China. In this study, we aim to collect bamboo samples in Yunnan, China, describe and introduce a new genus Paramphibambusa to accommodate P. bambusicola, and two new species Arecophila xishuangbannaensis and A. zhaotongensis in the family of Cainiaceae. This study enriches the species diversity of bambusicolous Cainiaceae species in China.

Materials and methods

Sample collection, single spore isolation and morphological study

Bamboo culms were collected in northeastern (Zhaotong), northwestern (Shangri-La), and southwestern (Xishuangbanna) Yunnan Province, China, stored in disposable plastic Ziplock bags and brought back to the laboratory for examination and study. Morphological observation and single spore isolation were followed as described in Dai et al. (2017). The ascomata on the host surface were observed by Leica using a S8AP0 microscope and photographed by HDMI 200C. Micro-morphological features were observed using an Olympus BX53 compound microscope and captured with an Olympus DP74 camera (Olympus SZ61; Olympus Corporation, Tokyo, Japan). The asci were stained by Meltzer’s reagent to examine the J-/J+ ring at the tip of the asci. India ink was used to stain the ascospores for checking the mucilaginous sheath. The micro-morphological features and fruiting bodies were measured by Tarosoft (R) Image FrameWork (IFW). The photo plates were created by Adobe Photoshop CS6 software (Adobe Systems Inc., San Jose, CA, USA). Herbarium material and living cultures were deposited at the Herbarium of Guizhou Medical University (GMB), Guizhou Medical University Culture Collection (GMBCC) Guiyang, Zhongkai University of Agriculture and Engineering (ZHKU), Zhongkai University of Agriculture and Engineering Culture Collection (ZHKUCC) Guangdong, China, and the Guizhou Culture Collection (GZCC), Guiyang, China. MycoBank numbers were obtained from MycoBank database (https://www.mycobank.org/; accessed on 23 January 2024) to register the newly described taxa (MycoBank 2024).

DNA extraction, PCR amplification and sequencing

Fungal genomic DNA was extracted from fresh mycelium using the Biospin Fungus Genomic DNA Extraction Kit (BioFlux) according to the manufacturer’s instructions. When culture could not be obtained, fruiting bodies were used to extract genomic DNA by using E.Z.N.A. Forensic DNA Kit (BIO-TEK) followed the protocols. Genomic DNA was conducted by polymerase chain reaction (PCR). Four phylogenetic markers, internal transcribed spacer (ITS), large-subunit ribosomal RNA (LSU), RNA polymerase II (rpb2), and tub, were amplified using primer pairs ITS4/ITS5 (White et al. 1990), LR5/LR0R (Vilgalys and Hester 1990), RPB2-5F/RPB2-7cR (Liu et al. 1999), Bt2a/Bt2b (Hsieh et al. 2005), respectively. Amplification conditions were performed according to Dai et al. (2022) and Li et al. (2022). The purified PCR fragments were sequenced at Shanghai Myobio Biomedical Technology Co. and China UW Genetics Solutions (BGI-Tech), in Shanghai, China. The newly obtained sequence data were deposited in GenBank (https://www.ncbi.nlm.nih.gov).

Sequence alignment and phylogenetic analyses

The newly generated reverse and forward sequences were assembled with Geneious (Restricted) 9.1.2 (https://www.geneious.com, accessed on 20 May 2023) and subjected to BLAST searches in GenBank (https://blast.ncbi.nlm.nih.gov/, accessed on 20 May 2023) for revealing closely matched strains (Table 1). The related sequences of families in the order Xylariales were downloaded based on the latest article Li et al. (2022). The single gene matrix was aligned via the server version of MAFFT v. 7 (Katoh and Standley 2013) (https://mafft.cbrc.jp/alignment/server). The aligned sequence datasets were trimmed by trimAl.v1.2rev59. The alignments were combined via SequenceMatrix 1.9 (Vaidya et al. 2011). The AliView 1.26 (Larsson 2014) was used to obtain phylip and nexus format files for RAxML analysis and Bayesian analysis, respectively.

Table 1.

Sequences used for phylogenetic analyses in this study. The newly generated sequences are in bold. Type strains or type specimens are labelled with HT (holotype), ET (epitype), IT (isotype), and PT (paratype), T (Type), “N/A” indicates no available sequences.

Species Strain/voucher No. Status GenBank accession numbers
ITS LSU rpb2 tub
Amphibambusa bambusicola MFLUCC 11-0617 HT KP744433 KP744474 NA NA
Amphibambusa hongheensis KUN-HKAS 112723 HT MW892971 MW892969 NA NA
Amphibambusa hongheensis KUMCC 20-0334 HT MW892972 MW892970 NA NA
Amphirosellinia fushanensis HAST 91111209 HT GU339496 NA GQ848339 GQ495950
Amphirosellinia nigrospora HAST 91092308 HT GU322457 NA GQ848340 GQ495951
Annulohypoxylon atroroseum ATCC 76081 AJ390397 KY610422 KY624233 DQ840083
Annulohypoxylon stygium MUCL 54601 KY610409 KY610475 KY624292 KX271263
Apiospora arundinis CBS 464.83 KF144888 KF144933 NA KF144979
Apiospora hysteriana ICMP 6889 NA DQ368630 DQ368649 DQ368621
Apiospora kogelbergense CBS 117206 KF144895 KF144941 NA KF144987
Apiospora setosa ATCC 58184 NA AY346259 NA NA
Arecophila australis GZUCC0112 HT MT742126 MT742133 NA MT741734
Arecophila australis GZUCC0124 PT MT742125 MT742132 NA NA
Arecophila bambusae HKUCC 4794 NA AF452038 NA NA
Arecophila clypeata GZUCC0110 HT MT742129 MT742136 MT741732 NA
Arecophila clypeata GZUCC0127 PT MT742128 MT742135 NA NA
Arecophila miscanthi GZUCC0122 MT742127 MT742134 NA NA
Arecophila miscanthi MFLU 19-2333 HT NR_171235 MK503827 NA NA
Arecophila sp. HKUCC 6487 NA AF452039 NA NA
Arecophila xishuangbannaensis ZHKU 23-0280 OR995737 OR995744 NA NA
Arecophila xishuangbannaensis GMB-W1283 HT OR995736 OR995743 NA NA
Arecophila zhaotongensis GMBCC1145 HT OR995740 OR995747 OR995741 NA
Arecophila zhaotongensis ZHKU 23-0260 OR995738 OR995745 NA NA
Arecophila zhaotongensis ZHKU 23-0259 IT OR995735 OR995742 NA NA
Astrocystis concavispora MFLUCC 14-0174 HT KP297404 KP340545 KP340532 KP406615
Atrotorquata lineata HKUCC 3263 AF009807 NA NA NA
Atrotorquata spartii MFLUCC 13-0444 HT NA KP325443 NA NA
Barrmaelia rappazii CBS 142771 HT MF488989 MF488989 MF488998 MF489017
Barrmaelia rhamnicola CBS 142772 ET MF488990 MF488990 MF488999 MF489018
Cainia anthoxanthis MFLUCC 15-0539 HT NR_138407 KR092777 NA NA
Cainia desmazieri CAI KT949896 KT949896 NA NA
Cainia desmazieri CBS 137.62 MH858124 MH869702 NA NA
Cainia globosa MFLUCC 13-0663 HT NR_171724 KX822123 NA NA
Cainia graminis CBS 136.62 MH858123 AF431949 NA NA
Cainia graminis MFLUCC 15-0540 KR092793 KR092781 NA NA
Cainia sp. LSU0560 MT000421 MT000513 NA NA
Camillea obularia ATCC 28093 KY610384 KY610429 KY624238 KX271243
Camillea tinctor YMJ 363 JX507806 NA JX507790 JX507795
Collodiscula bambusae GZ 62 KP054279 KP054280 KP276675 KP276674
Collodiscula fangjingshanensis GZUH 0109 HT KR002590 KR002591 KR002592 KR002589
Coniocessia maxima CBS 593.74 HT NR_137751 MH878275 NA NA
Coniocessia nodulisporioides CBS 281.77 IT MH861061 AJ875224 NA NA
Creosphaeria sassafras STMA 14087 KY610411 KY610468 KY624265 KX271258
Daldinia bambusicola CBS 122872 HT KY610385 KY610431 KY624241 AY951688
Daldinia concentrica CBS 113277 AY616683 KT281895 KY624243 KC977274
Endocalyx cinctus NBRC 31306 MZ313191 MZ313152 NA NA
Endocalyx cinctus JCM 7946 LC228648 LC228704 NA NA
Endocalyx grossus JCM 5164 HT MZ313160 MZ313138 NA NA
Endocalyx grossus JCM 5165 MZ313159 MZ313158 NA NA
Endocalyx grossus JCM 5166 MZ313179 MZ313171 NA NA
Endocalyx indumentum JCM 5171 HT MZ313153 MZ313161 NA NA
Endocalyx indumentum JCM 8042 MZ313162 MZ313157 NA NA
Endocalyx melanoxanthus CBS147393 MW718204 MW718204 NA NA
Endocalyx melanoxanthus CBS147394 MW718203 MW718203 NA NA
Endocalyx ptychospermatis ZHKUCC 21-0008 HT MZ493352 OK513439 NA NA
Endocalyx ptychospermatis ZHKUCC 21-0009 HT MZ493353 OK513440 NA NA
Endocalyx ptychospermatis ZHKUCC 21-0010 HT MZ493354 OK513441 NA NA
Entoleuca mammata JDR 100 GU300072 NA GQ844782 GQ470230
Entonaema liquescens ATCC 46302 KY610389 KY610443 KY624253 KX271248
Entosordaria perfidiosa CBS 142773 ET MF488993 MF488993 MF489003 MF489021
Entosordaria quercina RQ/CBS 142774 HT MF488994 MF488994 MF489004 MF489022
Graphostroma platystomum CBS 270.87 HT JX658535 AY083827 KY624296 HG934108
Hypocopra rostrata NRRL 66178 KM067909 KM067909 NA NA
Hypocrea gelatinosa NBRC 104900 ET JN943358 JN941453 NA NA
Hypomontagnella barbarensis STMA 14081 HT MK131720 MK131718 MK135891 MK135893
Hypomontagnella monticulosa MUCL 54604 ET KY610404 KY610487 KY624305 KX271273
Hypoxylon fragiforme MUCL51264 ET KM186294 KM186295 KM186296 KX271282
Hypoxylon investiens CBS 118185 KC968924 KY610451 KY624260 KC977269
Jackrogersella multiformis CBS 119016 ET KC477234 KT281893 KY624290 KX271262
Kretzschmaria deusta CBS 163.93 KC477237 KY610458 KY624227 KX271251
Leiosphaerella chromolaenae CBS 125586 JF440976 JF440976
Longiappendispora chromolaenae MFLUCC 17-1485 HT NR_169723 NG_068714 NA NA
Lopadostoma americanum LG8 HT KC774568 KC774568 KC774525 NA
Lopadostoma dryophilum LG21 ET KC774570 KC774570 KC774526 MF489023
Lopadostoma fagi LF1 HT KC774575 KC774574 KC774531 NA
Lopadostoma quercicola LG27 HT KC774610 KC774610 KC774558 NA
Lopadostoma turgidum LT2 ET KC774618 KC774618 KC774563 MF489024
Monographella nivalis UPSC 3273 NA AF452030 NA NA
Nemania abortiva BISH 467 HT GU292816 NA GQ844768 GQ470219
Nemania bipapillata HAST 90080610 GU292818 NA GQ844771 GQ470221
Nemania maritima HAST 89120401 ET GU292822 NA GQ844775 GQ470225
Nemania primolutea HAST 91102001 HT EF026121 NA GQ844767 EF025607
Obolarina dryophila MUCL 49882 GQ428316 GQ428316 KY624284 GQ428322
Oxydothis frondicola HKUCC 1001 NA AY083835 NA NA
Paramphibambusa bambusicola GMBCC1142 HT OR995739 OR995746 OR995740 NA
Paramphibambusa bambusicola ZHKUCC 23-0976 OR995741 OR995748 OR995739 NA
Paraxylaria xylostei MFLU 17-1636 MW240640 MW240570 NA MW820914
Paraxylaria xylostei MFLU 17-1645 MW240641 MW240571 NA MW820915
Phylacia sagrana CBS 119992 AM749919 NA NA NA
Podosordaria mexicana WSP 176 GU324762 NA GQ853039 GQ844840
Podosordaria muli WSP 167 HT GU324761 NA GQ853038 GQ844839
Poronia pileiformis WSP 88113001 ET GU324760 NA GQ853037 GQ502720
Poronia punctata CBS 656.78 HT KT281904 KY610496 KY624278 KX271281
Pyrenopolyporus nicaraguensis CBS 117739 AM749922 KY610489 KY624307 KC977272
Rhopalostroma angolense CBS 126414 KY610420 KY610459 KY624228 KX271277
Rosellinia aquila MUCL 51703 KY610392 KY610460 KY624285 KX271253
Rosellinia corticium MUCL 51693 KY610393 KY610461 KY624229 KX271254
Rostrohypoxylon terebratum CBS 119137 HT DQ631943 DQ840069 DQ631954 DQ840097
Ruwenzoria pseudoannulata MUCL 51394 HT KY610406 KY610494 KY624286 KX271278
Sarcoxylon compunctum CBS 359.61 KT281903 KY610462 KY624230 KX271255
Seynesia erumpens SMH 1291 NA AF279410 AY641073 NA
Stilbohypoxylon quisquiliarum YMJ 172 EF026119 NA GQ853020 EF025605
Thamnomyces dendroideus CBS 123578 FN428831 KY610467 KY624232 KY624313
Vialaea mangiferae MFLUCC 12-0808 HT KF724974 KF724975 NA NA
Vialaea minutella BRIP 56959 KC181926 KC181924 NA NA
Xylaria hypoxylon CBS 122620 ET KY610407 KY610495 KY624231 KX271279
Zygosporium oscheoides MFLUCC 14-0402 MF621585 MF621589 NA NA

Maximum likelihood (ML) analysis was performed by RAxML-HPC2 on XSEDE (8.2.12) (Stamatakis et al. 2008; Stamatakis 2014) via the CIPRES Science Gateway V.3.3 web server (https://www.phylo.org/portal2/login!input. action) (Miller et al. 2010). The best model was GTRGAMMA, with 1000 replicates rapid bootstrapping. Bayesian inference (BI) analysis was performed by MrBayes on XSEDE (3.2.7a) in the website CIPRES Science Gateway (Ronquist et al. 2012). Markov Chain Monte Carlo (MCMC) was used to evaluate posterior probabilities (PP) (Rannala and Yang 1996; Zhaxybayeva and Gogarten 2002). The best model test for each gene was performed via MrMTgui (Ma 2016). Six simultaneous Markov chains were run for 1000000 generations, and trees were sampled every 100th generation (resulting in 10,000 total trees). The phylogenetic trees were visualized with FigTree v. 1.4.2 (http://tree.bio.ed.ac.uk software/figtree/) (Rambaut 2012), and edited by Adobe Illustrator CS v. 5.

Abbreviations

ATCC: American Type Culture Collection; BISH: Bishop Museum, Department of Natural Sciences; CAI: Cairo University, Botany Department; CBS: Culture Collection of the Westerdijk Fungal Biodiversity Institute, Utrecht, Netherlands; GMBCC: Guizhou Medical University Culture Collection, Guiyang, China; GZU: Karl-Franzens-Universitat Graz; GZUCC: Guizhou University Culture Collection, Guiyang, Guizhou, China; HAST: Research Center for Biodiversity, Academia Sinica; HKUCC: The University of Hong Kong Culture Collection, Hong Kong, P.R. China; JCM: Japan Collection of Microorganisms, Japan; JDR: J.D. Rogers; KUMCC: Kunming Institute of Botany Culture Collection; KUN-HKAS: Herbarium of Cryptogams Kunming Institute of Botany Academia Sinica; LF: Lopadostoma fagiL; LT: Lopadostoma turgidum; MFLU: Mae Fah Luang University Herbarium; MFLUCC: Mae Fah Luang University Culture Collection; MUCL: Agro-food & Environmental Fungal Collection; NBRC: Biological Resource Center IFO; NRRL: Agricultural Research Service Culture Collection; SMH: Sabine M. Huhndorf; KUN-HKAS: Herbarium of Cryptogams Kunming Institute of Botany Academia Sinica; STMA: HZI culture collection, Helmholtz Centre for Infection Research, Braunschweig, Germany; WSP: Washington State University, Plant Pathology Department; YMJ: YuMing, Ju; ZHKUCC: Zhongkai University of Agriculture and Engineering.

Results

Phylogenetic results

The combined dataset comprised 107 strains (Table 1). Hypocrea gelatinosa (NBRC 104900) was selected as the outgroup taxon. The alignment comprised 4195 bp in total (ITS 580 bp, LSU 736 bp, rpb2 1197 bp, and tub 1682 bp). The final ML optimization likelihood value of -68750.486429 and the matrix had 2603 bp distinct alignment patterns, with 45.50% of undetermined characters or gaps. Estimated base frequencies were as follows: A = 0.240607, C = 0.260776, G = 0.259542, T = 0.239075, AC = 1.358257, AG = 3.703167, AT = 1.354909, CG = 1.087664, CT = 6.069506, GT = 1.000000; proportion of invariable sites I = 0.378984; and gamma distribution shape parameter α = 0.817253.

The final RAxML tree (Fig. 1) is based on maximum likelihood (ML), and Bayesian inference analyses with similar topology. The RAxML tree showed that Paramphibambusa bambusicola (GMBCC1142, ZHKUCC 23-0976) formed a distinct, stable clade basal to the other genera of Cainiaceae with high statistical support (90% ML, 1.00 PP). Moreover, Arecophila strains form two clades (Fig. 1), which coincide with Li et al. (2022). Our new collections cluster with A. bambusae Umali & K.D. Hyde (HKUCC 4794) and Arecophila sp. (HKUCC 6487) forming a sister branch clustered in Clade 2 (Fig. 1).

Figure 1. 

The RAxML tree was generated based on the combined ITS, LSU, rpb2, and tub sequence data. Bootstrap support values for ML equal to or greater than 60%, and Bayesian posterior probabilities (BYPP) equal to or higher than 0.90 are indicated above the nodes as ML/PP. Type materials are indicated by superscript “T”, while the newly generated sequences are shown in red.

Taxonomy

Paramphibambusa L.S. Han & D.Q. Dai, gen. nov.

MycoBank No: MB851854

Etymology

In reference to a new genus is morphologically similar to Amphibambusa, but phylogenetically distinct.

Description

Saprobic on bamboo culms. Sexual morph: Ascomata deeply immersed beneath poorly developed clypeus, solitary, scattered, black, globose to subglobose, ostiolate, with a long neck. Peridium composed of several layers, thick-walled, hyaline to pale brown cells of textura angularis. Paraphyses hyaline, numerous, filiform to cylindrical, guttulate, branched, septate, tapering towards the apex. Asci 8-spored, rarely 6-spored, unitunicate, cylindrical, short pedicellate, straight or slightly curved, rounded at the apex, with an elliptical to trapezoidal, J+ sub-apical ring. Ascospores uniseriate or overlapping uniseriate, hyaline to golden brown, ellipsoidal, guttulate, 2–3-celled, tapering at the ends, slightly constricted at the septum, smooth-walled, surrounded by a mucilaginous sheath. Asexual morph: Undetermined.

Type species

Paramphibambusa bambusicola L.S. Han & D.Q. Dai

Notes

A monotypic genus Paramphibambusa is introduced based on its different morphological characteristics and the support of phylogenetic affinity with the other members in Cainiaceae. The morphological characteristics of Paramphibambusa resemble Amphibambusa in having dark clypeus, immersed, globose to subglobose ascomata, unitunicate, short pedicellate asci with a J+, and sub-apical ring, and 1-septate ascospores, surrounded by a thick mucilaginous sheath (Liu et al. 2015; Jiang et al. 2021). Paramphibambusa can be easily distinguished from Amphibambusa in having an ostiole, with a long neck, and ascospores lacking longitudinal wall ornamentations. In addition, Paramphibambusa forms a well-separated branch basal to other cainiaceous genera with 90% ML, and 1.00 PP statistical supports (Fig. 1). Paramphibambusa differs from the sexual members of Cainiaceae in ascomata with a long neck leading up to the ostiole, and in that the ascospores lack longitudinal striations or germ slits or germ pores Endocalyx is an asexually typified genus and lacks a sexual morph to compare its morphology with Paramphibambusa. However, in the phylogenetic analyses, Paramphibambusa resides in a distinct phylogenetic lineage to Endocalyx (Fig. 1). Therefore, we consider Paramphibambusa as a distinct genus.

Paramphibambusa bambusicola L.S. Han & D.Q. Dai, sp. nov.

MycoBank No: MB851857
Fig. 2

Etymology

With reference to its occurrence on host bamboo.

Holotype

GMB-W1350.

Description

Saprobic on dead culms of bamboo. Sexual morph: Ascomata 430–580 × 500–550 µm (x– = 474 × 519 µm, n = 20), deeply immersed beneath blackened poorly developed clypeus, solitary, scattered, black, globose to subglobose, ostiolate, with a long neck, 50–125 µm diam., 240–260 µm long. Peridium 15–25 µm thick, composed of several layers, thick-walled, hyaline to pale brown cells of textura angularis. Paraphyses 2–5.5 µm wide, hyaline, numerous, filiform to cylindrical, guttulate, branched, septate, tapering towards the apex. Asci 200–240 × 10–13.5 µm (x– = 215 × 11.5 µm, n = 20), 8-spored, rarely 6-spored, unitunicate, cylindrical, short pedicellate, straight or slightly curved, rounded at the apex, with a 3–4 µm wide, 1.5–2 µm high (x– = 3.6 × 1.7 µm, n = 20), elliptical to trapezoidal, J+, sub-apical ring. Ascospores 24–35 × 6–7.5 µm (x– = 27 × 6.6 µm, n = 20), uniseriate or overlapping uniseriate, hyaline to golden brown, ellipsoidal, 2–3-celled, tapering at the ends, slightly constricted at the septum, smooth-walled, surrounded by a 9–12 µm mucilaginous sheath. Asexual morph: Undetermined.

Culture characters

Ascospores germinating within 24 h. Colonies reaching 45 mm diam. in 20 days under dark and at 28 °C conditions, circular, flocculent, yellowish from above and below.

Figure 2. 

Paramphibambusa bambusicola (GMB-W1350, holotype) a bamboo specimen b black ostioles at the host surface c transverse section of ascomata d, e vertical section of ascomata with long necks and black clypeus f cells of peridium g paraphyses h–k asci l asci with J+, elliptical to trapezoidal, subapical ring (stained in Melzer’s reagent) m–s ascospores (s ascospore stained in Indian ink showing mucilaginous sheath) t a germinating ascospore u, v cultures on PDA after 20 days (u upper, v reverse). Scale bars: 300 µm (d, e); 15 µm (f, l–t); 30 µm (g); 50 µm (h–k).

Materials examined

China, Yunnan Province, Zhaotong, Zhenxiong town, 27°36′8"N, 104°56′34"E, 1673.07 m, on dead culms of bamboo, 29 July 2021, Dong-Qin Dai, Li-Su Han, DDQ02077, (GMB-W1350, holotype), GMBCC1142, ex-type; ibid. (ZHKU 23-0256, isotype), GZCC 23-0629, ex-isotype; Zhaotong, Zhenxiong town, Shanzhai, 27°62′52"N, 104°81′98"E, 1666.10 m, on dead culms of bamboo, 4 August 2023, Dong-Qin Dai, Li-Su Han, HLS0114 (ZHKU 23-0257), living culture ZHKUCC 23-0976.

Notes

In the phylogenetic tree, Paramphibambusa bambusicola formed a stable clade basal to the other species of Cainiaceae with 90% ML, and 1.00 PP statistical supports (Fig. 1). In morphology, Paramphibambusa bambusicola has Cainiaceae species typical characteristics that are cylindrical asci, with a J+, apical ring, and ellipsoidal ascospores surrounded by a mucilaginous sheath. However, the spores of Cainiaceae species have the ornamented walls with longitudinal striations or germ slits or germ pores. Paramphibambusa bambusicola differs from the current Cainiaceae species by having smooth-walled ascospores. Therefore, based on morphological and phylogenetic studies, P. bambusicola is introduced hereby as a new species occurring on bamboo in Yunnan, China.

Arecophila K.D. Hyde, Nova Hedwigia 63(1-2): 82 (1996)

MycoBank No: MB27653

Notes

The genus Arecophila is characterized by immersed ascomata, usually with a clypeus, unitunicate, cylindrical asci, commonly producing an apical ring, and ascospores with longitudinal striation or a verrucose wall, and surrounded by a mucilaginous sheath (Hyde 1996; Li et al. 2022). Li et al. (2022) provided a morphological comparison of the main characters of Arecophila species. The asexual morph of Arecophila has not been reported. According to Li et al. (2022), this genus is distributed across 12 countries and is reported from 16 host species.

Arecophila xishuangbannaensis L.S. Han & D.Q. Dai, sp. nov.

MycoBank No: MB851853
Fig. 3

Etymology

Named after the location “Xishuangbanna” where the new taxon was discovered.

Holotype

GMB-W1283.

Description

Saprobic on dead culms of bamboo. Sexual morph: Ascomata 540–700 × 320–450 µm (x– = 586 × 389 µm, n = 20), immersed beneath a black clypeus, forming white ring surrounding ostioles of ascomata, solitary or scattered, sometimes gregarious, globose to subglobose, dark brown to black. Ostioles papillate, central, black. Peridium 15–25 µm thick, comprised of several layers, thick-walled, dense, brown to hyaline, cells of textura angularis. Paraphyses 2.5–6 μm wide, hyaline, numerous, cylindrical, unbranched, septate. Asci 180–270 × 12–14 μm (x– = 213 × 12.8 μm, n = 20), 8-spored, unitunicate, cylindrical, pedicellate, straight or slightly curved, apically rounded, with a 3.7–4.7 μm wide, 2.5–3 μm high (x– = 4.3 × 2.7 μm, n = 20), wedge-shaped, J+, apical ring. Ascospores 23–27 × 8.5–9.5 μm (x– = 24.5 × 8.8 μm, n = 20), overlapping, uniseriate, initially hyaline, pale brown to dark brown when mature, ellipsoidal, medianly 1-septate, tapering towards both ends, slightly constricted at the septum, with longitudinal striation along entire length of the ascospore, surrounded by a 3.5–5 µm thick, distinct, globose to subglobose, mucilaginous sheath. Asexual morph: Undetermined.

Figure 3. 

Arecophila xishuangbannaensis (GMB-W1283, holotype) a bamboo specimen b, c appearance of ostioles on host surface d–f vertical sections of ascomata g peridium h paraphyses i–m asci n asci with J+, wedge-shaped rings (Stained in Melzer’s reagent) o–t ascospores (s showing ascospore with longitudinal striations t ascospore stained in Indian ink showing mucilaginous sheath). Scale bars: 300 μm (d–f); 20 μm (g); 30 μm (h); 50 μm (i–m); 15 μm (n–t).

Materials examined

China, Yunnan Province, Xishuangbanna, Jinghong, Manzhang, Mengla, 21°91′97"N, 101°20′42"E, 617.14 m, on dead culms of bamboo, 16 August 2020, Dong-Qin Dai, Li-Su Han, DDQ00993, (GMB-W1283 holotype), ibid. (ZHKU 23-0258, isotype), ibid. DDQ00993-1 (ZHKU 23-0280).

Notes

In the phylogenetic tree, our new collections of Arecophila xishuangbannaensis (GMB-W1283, ZHKU 23-0280) formed a well-separated sister branch with A. bambusae (HKUCC 4794) and Arecophila sp. (HKUCC 6487) with 92% ML, 0.94 PP statistical supports (Fig. 1). Based on a nucleotide base pair comparison, A. xishuangbannaensis differs from A. bambusae (HKUCC 4794) in LSU gene (15/736 bp, 2%). Morphologically, A. xishuangbannaensis is similar to A. bambusae, in having cylindrical asci and ellispoidal ascospores. However, our new taxon differs A. bambusae by forming a white ring surrounding ostioles of ascomata and having larger asci (180–270 × 12–14 μm vs. 132.5–140 × 7.5–8 µm) and larger ascospores (23–27 × 8.5–9.5 μm vs. 19–22.5 × 5.5–7 µm) (Umali et al. 1999; Li et al. 2022). Arecophila xishuangbannaensis also resembles A. notabilis K.D. Hyde, but it has larger ascomata (586 × 389 µm vs. 400 × 360 µm) (Hyde 1996). The spores of this species did not germinate on PDA or malt extract agar (MEA) media, thus no culture is available.

Arecophila zhaotongensis L.S. Han & D.Q. Dai, sp. nov.

MycoBank No: MB851836
Fig. 4

Etymology

Named after the location “Zhaotong” where the new taxon was discovered.

Holotype

GMB-W1353.

Description

Saprobic on dead culms of bamboo. Sexual morph: Ascomata 600–960 × 450–550 µm (x– = 710 × 500 µm, n = 20), immersed beneath blackened clypeus, clypeus well-developed, darkened raised discs, or as tiny ostiolar dots, solitary, scattered, sometimes gregarious, dark brown to black, globose to subglobose, papillate, with a central ostiole. Peridium 15–25 µm thick, comprising several layers, thick-walled, brown cells of textura angularis. Paraphyses 1–3 µm wide, hyaline, numerous, filiform, branched. Asci 190–240 × 10.5–14 µm (x– = 215 × 11.6 µm, n = 20), 4- or 8-spored, rarely 6-spored, cylindrical, unitunicate, short pedicellate, straight or slightly curved, rounded at the apex, with a 4–4.5 μm wide, 2–2.5 µm high (x– = 4.2 × 2.2 µm, n = 20), trapezoidal, J+, apical ring. Ascospores 21–30 × 6–8 µm (x– = 25.5 × 7 µm, n = 20), uniseriate or overlapping uniseriate, brown, ellipsoidal, 1-septate, septate at the centre, slightly tapering at the ends, with longitudinal and sulcate striations, surrounded by a 5–10.5 µm wide, distinct, oval to spherical, mucilaginous sheath. Asexual morph: Undetermined.

Culture characters

Ascospores germinating within 24 h. Colonies reach 20 mm diam. in 15 days under dark and at 28 °C conditions, circular, hairy, white from above, and yellow to yellowish from below.

Figure 4. 

Arecophila zhaotongensis (GMB-W1353, holotype) a bamboo specimen b, c appearance of ostioles at the host surface d, e vertical sections of ascomata with ostioles and black clypei f peridium g paraphyses h–m asci n, o asci with a J+ trapezoidal ring (stained in Melzer’s reagent) p–t ascospores surrounded by mucilaginous sheath (t ascospore with longitudinal striations) u a germinating ascospore v, w cultures on PDA after 15 days (v upper, w reverse). Scale bars: 300 µm (d, e); 30 µm (f, g); 50 µm (h–m); 15 µm (n–u).

Materials examined

China, Yunnan Province, Diqin, Shangri-La, Bigu Mountain, on dead culms of bamboo, 22 July 2020, 27°36′56.9"N, 99°42′6.4"E, 3460 m, Dong-Qin Dai DDQ00740 (ZHKU 23-0261); Zhaotong, Zhenxiong S302, 27°36′8"N, 104°56′34"E, 1673.07 m, on dead culms of bamboo, 29 July 2021, Dong-Qin Dai, Li-Su Han, DDQ02079, (GMB-W1353, holotype), GMBCC1145, ex-type; ibid. (ZHKU 23-0259, isotype), ZHKUCC 23-0975, ex-isotype; ibid. DDQ02105 (ZHKU 23-0260).

Notes

In the phylogenetic tree, the new species A. zhaotongensis (GMBCC 1145, ZHKU 23-0259, ZHKU 23-0260) formed a separated sister branch to A. bambusae (HKUCC 4794), Arecophila sp. (HKUCC 6487) and A. xishuangbannaensis (GMB-W1283, ZHKU 23-0280) with 89% ML, 0.99 PP statistical supports (Fig. 1). Based on a nucleotide pairwise comparison, A. zhaotongensis differs from A. bambusae (HKUCC 4794) in 26/736 bp of LSU (3.5%), and differs from A. xishuangbannaensis (GMB-W1283, ZHKU 22-0280) in 56/563 bp of ITS (9.9%), 18/736 bp of LSU (2.4%). Arecophila zhaotongensis has larger asci than A. bambusae (190–240 × 10.5–14 µm vs. 132.5–140 × 7.5–8 µm) and larger ascospores (21–30 × 6–8 µm vs. 19–22.5 × 5.5–7 µm) (Umali et al. 1999). Arecophila zhaotongensis differs from A. xishuangbannaensis (GMB-W1283, ZHKU 23-0280) in having narrower ascospores (21–30 × 6–8 µm vs. 23–27 × 8.5–9.5 µm). The new species also resembles A. muroiana (I. Hino & Katum.) You Z. Wang et al. (Wang et al. 2004). However, A. muroiana lacks a clypeus absent, while a blackened clypeus was observed in A. zhaotongensis.

Discussion

Paramphibambusa forms deeply immersed, dark ascomata, with a long neck, J+ asci and smooth-walled ascospores. Interestingly, genera in Cainiaceae usually form ascospores with longitudinal striations or germ slits or germ pores, however, these characters were not observed in our new collection (GMB-W1350). Hence, we introduced the new genus Paramphibambusa in Cainiaceae based on morphological characteristics and phylogenetic analyses (Fig. 1). Moreover, we introduced two new Arecophila species in Cainiaceae. The establishment of Paramphibambusa and the introduction of two new Arecophila species enriches the species diversity of the family Cainiaceae and the diversity of bambusicolous fungi.

Currently, some species in the Cainiaceae are monospecific, such as Longiappendispora (Mapook et al. 2020), and Paramphibambusa (this study), while Amphibambusa, and Atrotorquata each contain only two species (Kohlmeyer and Volkmann-Kohlmeyer 1993; Liu et al. 2015; Jiang et al. 2021). Hence, more samples are needed to better understand each genus. Wijayawardene et al. (2022b) mentioned that it is essential to carry out more studies on host plants (that have been extensively studied for fungi, such as bamboo) in biodiversity-rich regions to reveal more novel species. Yunnan is exceedingly rich in fungal diversity, especially in higher level taxa, such as ascomycetes and basidiomycetes (Wijayawardene et al. 2021b; Dai et al. 2022). Hence, we believe that future studies on bamboo-associated fungi in Yunnan Province would disclose more novel taxa.

Atrotorquata was introduced as a monotypic genus by Kohlmeyer and Volkmann-Kohlmeyer (1993) to accommodate A. lineata Kohlm. & Volkm.-Kohlm. Subsequently, Liu et al. (2015) introduced A. spartii Thambug et al. as the second species. These two species share similar morphology, but their phylogenetic relationship was not well-resolved by Liu et al. (2015). Due to a lack of sequence data in GenBank, Atrotorquata clusters outside of Cainiaceae. More sequences especially protein genes loci are needed, to clarify its family placement.

Eighteen epithets were listed in Arecophila (Li et al. 2022), but only four taxa and a unnamed species have available molecular data, viz., A. australis Q.R. Li et al. (GZUCC0112, GZUCC0124), A. bambusae (HKUCC 4794), A. clypeata Q.R. Li et al. (GZUCC0110, GZUCC0127), A. miscanthi Q.R Li & J.C. Kang (GZUCC0122, MFLU 19-2333), and Arecophila sp. (HKUCC 6487). Thus, it is necessary to recollect fresh specimens and designate epitypes or reference specimens. Li et al. (2022) divided Arecophila into two clades based on phylogenetic analyses. We obtained the same results in our study, probably because most species of Arecophila lack protein genes regions in GenBank. We may need to design more suitable primers for sequencing protein genes fragments of Arecophila to support phylogenetic study.

Acknowledgments

The authors are grateful to High-Level Talent Recruitment Plan of Yunnan Provinces (“Young Talents” Program and “High-End Foreign Experts” Program), National Natural Science Foundation of China (Grant No.31760013, 32100010 and 32060710), Mee-mann Chang Academician Workstation in Yunnan Province, (Grant No. 202205AF150002), and Science and technology plan project of Science and Technology Department of Yunnan Province (Grant No. 202305AC350252, 20210BA070001-076), Key Laboratory of Yunnan Provincial Department of Education of the Deep-Time Evolution on Biodiversity from the Origin of the Pearl River for support. We are grateful to Dr. Shaun Pennycook for suggestions of Latin names for the new taxa. Li-Su Han would like to thank Tian-Ye Du for helping with phylogenetic analyses. The authors extend their appreciation to the Researchers supporting Project Number (RSP2024R120) King Saud University, Riyadh, Saudi Arabia. Kazuaki Tanaka would like to thank the Japan Society for the Promotion of Science (JSPS, 23K05900).

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 (Grant No.31760013, 32100010 and 32060710), Mee-mann Chang Academician Workstation in Yunnan Province, (Grant No. 202205AF150002), Science and technology plan project of Science and Technology Department of Yunnan Province (Grant No. 202305AC350252, 20210BA070001-076), and Researchers Supporting Project Number (RSP2024R120), King Saud University, Riyadh, Saudi Arabia.

Author contributions

Data curation: QL, NNW, CL. Formal analysis: AME. Methodology: KT, LHH. Software: SAR. Writing - original draft: LSH. Writing - review and editing: DQD, IP.

Author ORCIDs

Li-Su Han https://orcid.org/0000-0001-5380-9928

Nalin N. Wijayawardene https://orcid.org/0000-0003-0522-5498

Chao Liu https://orcid.org/0000-0001-6811-2218

Li-Hong Han https://orcid.org/0000-0002-6127-0915

Itthayakorn Promputtha https://orcid.org/0000-0003-3376-4376

Qiang Li https://orcid.org/0000-0002-9735-8214

Abdallah M. Elgorban https://orcid.org/0000-0003-3664-7853

Salim Al-Rejaie https://orcid.org/0000-0002-9254-1087

Kazuaki Tanaka https://orcid.org/0000-0002-7037-0774

Dong-Qin Dai https://orcid.org/0000-0001-8935-8807

Data availability

All of the data that support the findings of this study are available in the main text.

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