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Research Article
Taxonomy and evolution history of two new litter-decomposing Ciliochorella (Amphisphaeriales, Sporocadaceae)
expand article infoJia-Yu Song‡, Hai-Xia Wu‡§, Jin-Chen Li‡, Wei-Feng Ding‡§, Cui-Ling Gong‡, Xiang-Yu Zeng|, Nalin N. Wijayawardene, Da-Xin Yang#
‡ International Fungal Research and Development Centre, Institute of Highland Forest Science, Chinese Academy of Forestry, Kunming, China
§ Key Laboratory of Breeding and Utilization of Resource Insects, National Forestry and Grassland Administration, Kunming, China
| Guizhou University, Guiyang, China
¶ Qujing Normal University, Qujing, China
# Kunming Branch (KMB), Chinese Academy of Sciences (CAS), Kunming, China

Corresponding author: Hai-Xia Wu ( aileen2008haixia@gmail.com )

Academic editor: Xinlei Fan
© 2023 Jia-Yu Song, Hai-Xia Wu, Jin-Chen Li, Wei-Feng Ding, Cui-Ling Gong, Xiang-Yu Zeng, Nalin N. Wijayawardene, Da-Xin Yang.
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: Song J-Y, Wu H-X, Li J-C, Ding W-F, Gong C-L, Zeng X-Y, Wijayawardene NN, Yang D-X (2023) Taxonomy and evolution history of two new litter-decomposing Ciliochorella (Amphisphaeriales, Sporocadaceae). MycoKeys 100: 95-121. https://doi.org/10.3897/mycokeys.100.108863
Open Access

Abstract

The genus Ciliochorella is a group of pestalotioid fungi, which typically occurs in subtropical and tropical areas. Species from the Ciliochorella genus play important roles in the decomposition of litter. In this study, we introduce two new species (Ciliochorella chinensis sp. nov. and C. savannica sp. nov.) that were found on leaf litter collected from savanna-like vegetation in hot dry valleys of southwestern China. Phylogenetic analyses of combined LSU, ITS and tub2 sequence datasets indicated that C. chinensis and C. savannica respectively form a distinct clade within the Ciliochorella genus. The comparison of the morphological characteristics indicated that the two new species are well differentiated within this genus species. Analysis of the evolutionary history suggests that Ciliochorella originated from the Eurasian continent during the Paleogene (38 Mya). Further, we find that both new species can produce cellulase and laccase, playing a decomposer role.

Key words

Ancestral biogeography, leaf litter degradation, morphology, new taxa, time dating

Introduction

Fungi thrive on diverse ecosystems and environments as pathogens, mutualists, and saprobes (Bucher et al. 2004; Schmit and Mueller 2007; Jobard et al. 2010; Hyde et al. 2020; Lai et al. 2021). As decomposers of nature, fungi are involved in the degradation of lignin and cellulose (Bisaria and Ghose 1981; Hatakka 1994; Adlini et al. 2014). The extracellular lignin-degrading enzymes of fungi mainly comprise two types, peroxidases and laccases (Pointing et al. 2005; Floudas et al. 2012). Some plant-specific pathogenic fungi use laccases to counter the effects of tannic acid, which also has anti-viral activities (Dong and Changsun 2021). As such, laccase activity is also considered a virulence factor in many fungal diseases.

Ciliochorella Sydow & Mitter (1935), typified by C. mangiferae Syd., is an important genus of pestalotioid fungi (Sutton 1980; Nag Raj 1993; Lee et al. 2006; Tanaka et al. 2011; Tangthirasunun et al. 2015; Wijayawardene et al. 2016; Liu et al. 2019a). Most taxa classified as pestalotioid fungi are phytopathogens that cause a variety of diseases in plants, some of which are saprobes or endophytes that are widely distributed in tropical and temperate regions (Benjamin and Guba 1961; Barr 1975; Nag Raj 1993; Maharachchikumbura et al. 2016). Liu et al. (2019a) and Wijayawardene et al. (2022a) placed this genus in Sporoca­daceae (Ascomycota, Sordariomycetes, Amphisphaeriales).

Ciliochorella is an asexually typified, coelomycetous genus with nine species listed in the Index Fungorum (2023). However, only six species are accepted in the Species Fungorum (2023) due to the following two reports: 1) Subramanian and Ramakrishnan (1956) proposed Shanoria Subram. & Ramakr., a new genus, to accommodate Ciliochorella bambusarum Shanor as Shanoria bambusarum (Shanor) Subram. & K. Ramakr; 2) Nag Raj (1993) synonymized Ciliochorella eucalypti T.S. Viswan. and Ciliochorella indica Kalani under C. mangiferae). The genus is characterized by cylindrical, straight, or slightly curved conidia with septate pale brown middle cells, and colorless end cells bearing a single, eccentric appendage (Nag Raj 1993; Allegrucci et al. 2011; Hyde et al. 2016; Wijayawardene et al. 2016).

There are few studies that focused on the divergence time estimation of Ciliochorella, whereas some published studies are based on a larger classification scale (such as the order and the class). Divergence time can provide insights into the history of a given group of fungi species and its taxonomic placement (Li et al. 2005; Vijaykrishna et al. 2006; Beimforde et al. 2014; Pérez-Ortega et al. 2016; Samarakoon et al. 2016; Li et al. 2023). Samarakoon et al. (2016; 2022) estimated the divergence time of the Xylariomycetidae, including one species of Ciliochorella (C. mangiferae), diverged approximately 201–252 Mya in the Early Mesozoic (Samarakoon et al. 2022). Chen et al. (2023) conducted detailed genomic studies on the divergence time of members in Sordariomycetes, which included nine species of Sporocadaceae. The results show that the divergence time of Sporocadaceae is about 90.56 Mya. In addition to estimating divergence times, ancestral state reconstruction is also a viable strategy for studying evolutionary history. Ancestral state reconstruction can reveal the origin and evolution of a species and provide a basis for species classification (Omland 1999; Ismail et al. 2016; Royer-Carenzi and Didier 2016; Gao and Wu 2022; Li et al. 2022). However, relevant research examining the ancestral reconstruction of Ciliochorella is lacking.

Studies on the litter decomposition of Ciliochorella have demonstrated oxidative enzymatic activity using in-vitro cultures of Ciliochorella buxifolia demonstrated by Troncozo et al. (2015). It is also worth noting that C. mangiferae is an important litter-decomposing taxon in tropical countries, especially in India (Masilamani and Muthumary 1994). This genus may be involved in the leaf decomposition process, but not all species in this genus have been verified to have this function (Saparrat et al. 2010).

The primary objectives of this study were: 1) to delineate the taxonomic status of newly collected Ciliochorella-like species; 2) to estimate the evolutionary history of Ciliochorella; and 3) to determine the litter-decomposing function of this genus species in nature based on the screening of cellulase and laccase production.

Methods

Morphological studies

Two Ciliochorella-like taxa were collected from leaf litter (dead leaves from an unidentified plant species) in the savanna-like vegetation of hot dry valleys in southwestern China. The samples were placed in paper bags and transported to the laboratory for further observation. Following Wu et al. (2014), the collected samples were processed and examined by microscopes: photographs of ascomata were taken by using a compound stereomicroscope (KEYENCE CORPORATION V.1.10 with camera VHZ20R). Hand sections were made under a stereomicroscope (OLYMPUS SZ61) and mounted in water and blue cotton Photomicrographs of fungal structures were taken with a compound microscope (Nikon ECLIPSE 80i).

The images used for the figures were processed using the software Adobe Photoshop CC v. 2015.5.0 software (Adobe Systems, San Jose, CA, USA).

The specimens were deposited in the herbarium of IFRD (International Fungal Research & Development Centre; Institute of Highland Forest Science, Chinese Academy of Forestry, Kunming, China) and the cultures were deposited in the International Fungal Research & Development Center Culture Collection (IFRDCC) at the Research Institute of Highland Forest Science, Chinese Academy of Forestry, Kunming, China.

Single spore isolation was performed following the procedure published by Choi et al. (1999) and Chomnunti et al. (2014). Germinated spores were individually transferred to potato dextrose agar (PDA) medium and incubated at 26 °C for 48 h. Colony characteristics were observed and measured after two weeks at 26 °C.

Newly introduced taxa were registered at Fungal Names (https://nmdc.cn/fungalnames/) and obtained identifiers.

DNA isolation, amplification and sequencing

Genomic DNA was extracted from mycelia growing on PDA at room temperature using the Forensic DNA Kit (OMEGA, USA) according to the manufacturer’s instructions. The primers LR0R and LR5 were used to amplify the 28S large subunit (LSU) rDNA (Vilgalys and Hester 1990). The internal transcribed spacer (ITS) rDNA was amplified and sequenced with the primers ITS5 and ITS4 (White et al. 1990). The primers T12 and T22 were used to amplify the β-tubulin (tub2) (O’Donnell and Cigelnik 1997). The following PCR protocol was used: initial denaturation at 98 °C for 2 min, then 30 cycles, i) 98 °C denaturation for 10 s, ii) 56 °C annealing for 10 s, and iii) 72 °C extension for 10 s (ITS) or 20 s (LSU and tub2) followed by a final extension at 72 °C for 1 min. All PCR products were sequenced by Biomed (Beijing, China).

Sequence alignments and phylogenetic analyses

BioEdit version 7.0.5.3 was used to re-assemble sequences generated from forward and reverse primers to obtain the integrated sequences (Hall 1999). The sequences used by literature and closely related taxa from NCBI BLAST results (Table 1). Sequence alignments were performed in MAFFT (https://mafft.cbrC.jp/alignment/server/) (Katoh et al. 2019), and alignments were manually adjusted where necessary using BioEdit version 7.0.5.3. The sequence data set for subsequent analyses were obtained with the sequence fragments using R-based ape package (Paradis and Schliep 2019).

Table 1.
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Selected taxa in this study with their corresponding GenBank accession numbers and distribution information.

Species Location Voucher/ Strains GenBank accession numbers Reference
LSU ITS tub2
Ciliochorella castaneae East Asia (Japan); South Asia (India) HHUF 28799 AB433277 – – Nag Raj 1993; Endo et al.2008
C. castaneae East Asia (Japan); South Asia (India) HHUF 28800 AB433278 – – Nag Raj 1993; Endo et al. 2008
C. chinensis East Asia (China) IFRD 9468 OP902256 OP902250 OQ918680 In this study
C. dipterocarpi Southeast Asia (Thailand) MFLUCC 22-0132 OP912990 OP912991 – Nethmini et al. 2023
C. mangiferae* Southeast Asia (Thailand); South Asia (India, Pakistan); America (Cuba); Africa (Nigeria, Sierra Leone); MFLUCC 12-0310 KF827445 KF827444 KF827478 Nag Raj 1993; Masilamani and Muthumary 1994; Tangthirasunun et al. 2015
C. phanericola Southeast Asia (Thailand) MFLUCC 14-0984 KX789681 KX789680 KX789682.1 Hyde et al. 2016
C. savannica East Asia (China) IFRD 9467 OP902279 OP902251 OQ926205 In this study
East Asia (China) IFRD 9473 OQ867459 OQ867475 OQ926206 In this study
Discosia aff. brasiliensis Unknown NBRC 104199 AB593707 AB594775 AB594185 Tanaka et al. 2011
D. aff. pleurochaeta Unknown KT2188 AB593713 AB594781 AB594179 Tanaka et al. 2011
D. artocreas* Unknown NBRC 8975 AB593705 AB594773 AB594172 Tanaka et al. 2011
D. brasiliensis Southeast Asia (Thailand) NTCL095 KF827437 KF827433 KF827470 Tangthirasunun et al. 2015
D. celtidis East Asia (China) MFLU 18-2581 MW114406 NR_174839 – Tennakoon et al. 2021
D. fagi Europe (Italy) MFLU 14-0299A KM678048 KM678040 – Li et al. 2015
D. fici East Asia (China) MFLU 19-2704 MW114409.1 NR_174840 – Tennakoon et al. 2021
D. italica Europe (Italy) MFLU 14-0298C KM678044 KM678041 – Li et al. 2015
D. macrozamiae Oceania (Australia) CPC 32113 MH327855 MH327819 MH327894 Crous et al. 2018
D. pini Unknown MAFF 410149 AB593708 AB594776 AB594174 Tanaka et al. 2011
D. pseudoartocreas Europe (Austria) CBS 136438 MH877640 NR_132068 MH554672 Crous et al. 2013
Unknown DUCC5154 MH844788 MH844763 – Tanaka et al. 2011
D. querci East Asia (China) MFLU 18-0097 MW114405 MW114326 – Tennakoon et al. 2021
D. tricellularis Unknown NBRC 32705 AB593728 AB594796 AB594188 Tanaka et al. 2011
D. yakushimensis East Asia (Japan) MAFF 242774 AB593721 AB594789 AB594187 Tanaka et al. 2011
Discostroma tosta Unknown HKUCC 1004 AF382380 – – Tang et al. 2007
Discost. fuscellum Europe (Italy) MFLUCC 14-0052 KT005514 KT005515 – Senanayake et al. 2015
Discost. stoneae Unknown NBRC 32690 AB593729 AB594797 – Tanaka et al. 2011
Immersidiscosia eucalypti* East Asia (Japan) NBRC 104195 AB593722 AB594790 – Tanaka et al. 2011
I. eucalypti* East Asia (Japan) NBRC 104196 AB593723 AB594791 – Tanaka et al. 2011
East Asia (Japan) NBRC 104197 AB593724.1 AB594792 – Tanaka et al. 2011
East Asia (Japan) MAFF 242781 AB593725 AB594793 – Tanaka et al. 2011
Unknown MFLU 16-1372 MF173608 MF173609 – Tennakoon et al. 2021
Neopestalotiopsis protearum* Africa (Zimbabwe) CBS 114178 JN712564 JN712498 KM199463 Maharachchikumbura et al. 2014
N. rosae Oceania (New Zealand) CBS 101057 KM116245 KM199359 KM199429 Maharachchikumbura et al. 2014
Pestalotiopsis knightiae Oceania (New Zealand) CBS 114138 KM116227 KM199310 KM199408 Maharachchikumbura et al. 2014
P. malayana Southeast Asia (Malaysia) CBS 102220 KM116238 KM199306 KM199411 Maharachchikumbura et al. 2014
P. spathuliappendiculata Oceania (Australia) CBS 144035 MH554366 MH554172 MH554845 Liu et al. 2019
Pseudopestalotiopsis cocos Southeast Asia (Indonesia) CBS 272.29 KM116276 KM199378 KM199467 Maharachchikumbura et al. 2014
Ps. theae* East Asia (China), Southeast Asia (Thailand) MFLUCC 12-0055 KM116282 JQ683727 JQ683711 Maharachchikumbura et al. 2014
Robillarda africana Africa (South Africa) CBS 122.75 KR873281 KR873253 MH554656 Crous et al. 2015
R. roystoneae East Asia (China) CBS 115445 KR873282 KR873254 KR873317 Crous et al. 2015
East Asia (China) MFLUCC 19-0060 MW114402 MW114323 – Tennakoon et al. 2021
R. sessilis* Europe (Germany) CBS 114312 KR873284 KR873256 KR873319 Crous et al. 2015
R. terrae South Asia (India) CBS 587.71 KJ710459 KJ710484 MH554734 Crous et al. 2015
Seimatosporium azaleae Unknown MAFF 237478 AB593730 AB594798 AB594189 Tanaka et al. 2011
S. biseptatum Oceania (Australia) CPC 13584 JN871208 JN871199 MH554749 Barber et al. 2011
S. botan America (Chile) HMUC 316PD – JN088483 – Díaz et al. 2012
S. cornicola Europe (Italy) MFLUCC 14-0448 – KU974967 – Wijayawardene et al. 2016
S. cornii Europe (Italy) MFLUCC 14-1208 KT868531 KT868532 – Perera et al. 2016
S. elegans Oceania (Australia) NBRC 32674 AB593733 AB594801 MH554683 Tanaka et al. 2011
S. eucalypti Africa (South Africa) CPC 156 JN871209 JN871200 MH704627 Barber et al. 2011
S. falcatum Oceania (Australia) CPC 13578 JN871213 JN871204 MH554668 Barber et al. 2011
S. grevilleae Africa (South Africa) ICMP 10981 AF382372 AF405304 – Jeewon et al. 2002
S. italicum Europe (Italy) MFULCC 14-1196 NG_064463 NR_157485 – Hyde et al. 2017
S. leptospermi Oceania (New Zealand) ICMP 11845 AF382373 – – Jeewon et al. 2002
S. obtusum Oceania (Australia) CPC 12935 JN871215 JN871206 MH554669 Barber et al. 2011
S. physocarpi Europe (Russia) MFLUCC 14-0625 KT198723 KT198722 MH554676 Norphanphoun et al. 2015
S. pistaciae West Asia (Iran) CBS 138865 KP004491 KP004463 MH554674 Norphanphoun et al. 2015
S. pseudorosae Europe (Italy) MFLUCC 14-0468 KU359035 – – Li et al. 2015
S. pseudorosarum Europe (Italy) MFLUCC 14-0466 KT281912 KT284775 – Ariyawansa et al. 2015
S. rosae* Europe (Russia) MFLUCC 14-0621 KT198727 KT198726 LT853253 Norphanphoun et al. 2015
S. rosicola Europe (Italy) MFLU 16-0239 MG829069 MG828958 – Wanasinghe et al. 2018
Europe (Italy) MFLUCC 15-0564 MG829070 MG828959 Wanasinghe et al. 2018
S. sorbi Europe (Italy) MFLUCC 14-0469 KT281911 KT284774 – Ariyawansa et al. 2015
S. tostum Unknown NBRC 32626 AB593727 AB594795 – Rossman et al. 2016
S. vaccinii Oceania (New Zealand) ICMP 7003 AF382374 – – Jeewon et al. 2002
S. vitis Europe (Italy) MFLUCC 14-0051 KR920362 NR_156595 – Senanayake et al. 2015
S. walkeri Oceania (Australia) CPC 17644 JN871216 JN871207 MH554769 Barber et al. 2011
Seiridium cancrinum Africa (Kenya) CBS 226.55 = IMI 052256 MH554241 LT853089 LT853236 Liu et al. 2019
Seir. cupressi Africa (Kenya) CBS 224.55 = IMI 052254 MH554240 LT853083 LT853230 Liu et al. 2019
Seir. eucalypti Oceania (Australia) CBS 343.97 MH554251 MH554034 MH554710 Liu et al. 2019
Seir. kartense Oceania (Australia) CBS 142629 = CPC 20183 – LT853100 LT853247 Liu et al. 2019
Seir. kenyanium Africa (Kenya) CBS 228.55 = IMI 052257 MH554242 LT853098 LT853245 Liu et al. 2019
Seir. marginatum* Europe (Austria) CBS 140404 – KT949916 – Jaklitsch et al. 2016
Europe (France) CBS 140403 MH554223 KT949914 LT853249 Liu et al. 2019
Seir. neocupressi Europe (Italy) CBS 142625 = CPC 23786 MH554329 LT853079 LT853226 Liu et al. 2019
Seir. papillatum Oceania (Australia) CBS 340.97 DQ414531 LT853102 LT853250 Liu et al. 2019
Seir. phylicae Tristan da Cunha (Atlantic islands) CBS 133587 = CPC 19964 – LT853091 LT853238 Liu et al. 2019
Seir. pseudocardinale Europe (Portugal) CBS 122613 = CMW 1648 MH554206 LT853096 LT853243 Liu et al. 2019
Seir. unicorne Oceania (New Zealand) CBS 538.82 = NBRC 32684 MH554269 LT853088 LT853235 Liu et al. 2019
Strickeria kochii* Europe (Austria) C143 KT949918 KT949918 – Jaklitsch et al. 2016
St. kochii* Europe (Austria) C149 KT949920 KT949920 – Jaklitsch et al. 2016
Phlogicylindrium uniforme Oceania (Australia) CBS 131312 JQ044445 JQ044426 MH704634 Crous et al. 2015

Type species are marked with an asterisk ‘*’. New species are given in bold.

Phylogenetic analyses were performed using the CIPRES Science Gateway V.3.3 (https://www.phylo.org/). For maximum likelihood (ML) analyses, we used RAxML-HPC2 on XSEDE (8.2.12). Phlogicylindrium uniforme (CBS 131312) was selected as the outgroup taxon. One thousand non-parametric bootstrap iterations were performed using the “GTRGAMMA” algorithm. For Bayesian analysis, jModelTest2 on XSEDE (2.1.6) was used to estimate the best-fitting model for the combined LSU, ITS and tub2 genes, and the GTR+I+G model was the best fit. In MrBayes on XSEDE (3.2.7a), four simultaneous Markov chains were run for 2,000,000 generations; trees were sampled and printed every 2,000 generations. The first 25% of all trees were submitted to the burn-in phase and discarded, while the remaining trees were used to compute posterior probabilities in the majority rule consensus tree (Cai et al. 2006, 2008; Wu et al. 2011; Zeng et al. 2019).

Divergence time estimations

In this study, two secondary calibration nodes for the divergence time estimation of Ciliochorella were implemented to calibrate the tree: Node 1 was composed of Phlogicylindrium (outgroup, Phlogicylindriaceae) and 10 genera from the Sporocadaceae, which diverged 76 Mya; for Node 2 we used Discosia, Robillarda and the other seven genera (Ciliochorella, Neopestalotiopsis, Pestalotiopsis, Pseudopestalotiopsis, Seimatosporium, Seiridium and Strickeria), which diverged 44 Mya (Samarakoon et al. 2016). A maximum likelihood (ML) tree was used as input data and the data were analyzed via R8S 1.81 (https://sourceforge.net/projects/r8s/). The divergence time of Ciliochorella was estimated based on the PL (Penalized likelihood) method and TN algorithm (truncated Newton algorithm) obtained via R8S (Fig. 2). The R8S program only needs the second calibration node to estimate divergence times, and some methods in this program, such as NPRS (Nonparametric rate smoothing) and PL, which were first proposed by the author, are currently challenging to implement in similar software programs (Sanderson 2003). The PL method and TN algorithm have been implemented to estimate divergence times using data from the ML tree and secondary calibration nodes (Sanderson 2003). The ancient map is based on the results of Peng et al. (2023).

Reconstruction of ancestral biogeographic

RASP (http://mnh.scu.edu.cn/soft/blog/RASP) was used to reconstruct the ancestral biogeography in this study. It is a tool to infer the ancestral state using S-DIVA (Statistical Dispersal-Vicariance Analysis), Lagrange (DEC), Bayes-Lagrange (S-DEC), BayArea, BBM (Bayesian Binary MCMC), Bayestraits and BioGeoBEARS packages (Yu et al. 2015, 2020). Members of Ciliochorella were coded based on their collection locality according to references (Table 1). Based on the distribution data in the table, six geographic regions were defined: A = Asia, B =America, C = Europe, D = Africa, E = Oceania, F = Tristan da Cunha, G = Unknown, using species from Asia, America, Europe, Africa, Oceania and Tristan da Cunha. In MrBayes on XSEDE (3.2.7a), chains were run for 2,000,000 generations; trees were sampled and printed every 2,000 generations. RASP 4.2 was used to reconstruct the ancestral state, and the most-optimal model was BAYAREALIKE.

Screening of cellulase and laccase production

Cellulase screening was performed by the Congo red test (Liu and Fan 2012). A fungal cake with a diameter of 8 mm was isolated from the edge of the 7-day old colony and inoculated on solid PDA medium. After 7 days of inoculation, the culture was stained with 1 mg/mL Congo red solution for 10 min, and washed and fixed with 1 mol/L NaCl for 30 min.

Screening for laccase activity in the lignin peroxidase system requires the use of guaiacol-PDA solid medium (Wang et al. 2016), including PDA medium 40.20 g, agar 3.00 g, guaiacol 0.40 mL and distilled water to 1 L with 121 °C sterilization 30 min. The obtained strain was cultured at 26 °C for 7 days, and the fungal cake with a diameter of 8 mm was taken from the growing mycelium at the edge of the colony and inoculated on solid guaiacol-PDA medium. The growth of the strain was observed for 7 days of inoculation.

The supernatant was incubated on a shaker (150 rpm) for 12 hours at 26 °C, followed by centrifugation at 12,000 rpm to obtain a crude enzyme solution. The Thermo Varioskan Flash multifunctional enzyme reader has a characterized absorption peak at 540 nm, which can be used to assess cellulase activity based on changes in absorbance values. Laccase activity was characterized by the change in absorbance at 420 nm and the enzyme activity of the crude enzyme liquid was determined using the Laccase Activity Detection Kit (www.boxbio.cn). The experiment was repeated three times.

Results

Phylogenetic analyses

We analyzed a three-locus (LSU, ITS, tub2) data set of Ciliochorella. This data set consists of 203 sequences, including 75 LSU sequences, 75 ITS sequences and 53 tub2 sequences from 80 taxa. The concatenated sequences have 2338 characters including gaps. The two topological trees obtained by maximum likelihood (ML) and Bayesian were found to be similar, and the best-scoring RAxML tree was used as the representative tree (Fig. 1). Bootstrap values of ML greater than 50% are shown on the phylogenetic tree, while values of Bayesian posterior probabilities greater than 0.5 are shown on the tree (Fig. 1).

Figure 1. 

Phylogenetic tree of maximum likelihood analyses showing the relationships of Ciliochorella species based on combined LSU, ITS and tub2 data set analysis. Bootstrap values of maximum likelihood values greater than 50% are shown on the left, while values for Bayesian posterior probabilities greater than 0.5 are shown on the right. Discostroma is the sexual morph of Seimatosporium. New species are shown in bold and red, followed by their strain number.

Phylogenetic analysis showed that Ciliochorella species formed a clade with bootstrap values of 70% (in ML analysis) and Bayesian posterior probability of 1.00 (as a result of new species, the genus forms a separate clade). Pestalotiopsis, Pseudopestalotiopsis, and Neopestalotiopsis formed a clade with bootstrap values of 100% and Bayesian posterior probabilities of 1.00. Notably, this clade was adjacent to the Ciliochorella clade. In addition, Ciliochorella was also close to Seiridium (Fig. 1).

Ciliochorella savannica is distinguished from other Ciliochorella in the phylogenetic tree and has a high support rate with 97% ML and 1.00 Bayesian posterior probabilities. Ciliochorella chinensis has a close relationship with C. castaneae (HHUF 28800).

Divergence time estimation

According to divergence time estimates (Fig. 2), the age of Ciliochorella is about 38 Mya in the Paleogene period and falling in the recommended divergence times of Xylariomycetidae by Samarakoon et al. (2016). The ten genera of Sporocadaceae were all originated in the Paleogene. The genus of Immersidiscosia initially diverged about 49 Mya. Discosia and Robillarda formed one clade, with a divergence of time about 35 Mya. The other seven genera formed one clade: Neopestalotiopsis diverged about at 25 Mya, divergence times of Pestalotiopsis in the analysis is about 28 Mya, Pseudopestalotiopsis diverged about at 25 Mya, Seimatosporium diverged about at 35 Mya, Seiridium diverged about at 41 Mya and Strickeria diverged about at 35 Mya.

Figure 2. 

Divergence time tree based on ML analysis. Divergence times of all nodes were estimated by R8S software using two calibration points. The blue circles and the red star indicate secondary points and the divergence time of Ciliochorella respectively. Ciliochorella species are shown in bold and green. Maps were adopted from Peng et al (2023).

Ancestral biogeographic reconstruction analysis for Ciliochorella

Analysis of ancestral biogeographic reconstructions revealed that Ciliochorella species originated in Asia (Fig. 3, node 139). Dispersal, vicariance, extinction, and other historical events affected the biogeographic distribution of individual species. The evolutionary history of the ancestors of the genus Ciliochorella showed that the species of this genus underwent 45 dispersals, 27 vicariances, and 2 extinctions (Fig. 3, the blue circle represents dispersal, the green circle represents vicariance, and the yellow circle represents extinction). From approximately the Middle Paleogene, dispersal and vicariance events were frequent. In the early Paleogene, dispersal and extinction events occurred among ancestors of Pestalotiopsis, Pseudopestalotiopsis, Neopestalotiopsis, and Ciliochorella. After these events, Ciliochorella began to evolve independently of other genera (Fig. 3, node 140). Pestalotiopsis, Pseudopestalotiopsis, and Neopestalotiopsis are predicted to share the same ancestral biogeographic area (Fig. 3, node 132). Dispersal events occurred two times with Ciliochorella in the late Paleogene (about 30 Mya), which was followed by a period where Ciliochorella began spreading in Africa and America (Fig. 3, node 135). The result of the ancestral biogeographic reconstruction supported the notion that the Eurasian continent was the center of origin for Ciliochorella: the estimated ancestral distributions for nodes of the complex and its clades included both Asia and Europe (Fig. 3, node 139).

Figure 3. 

Ancestral biogeographic reconstructions are based on Bayesian trees. Each event is represented by a node number. Bayesian posterior probabilities are shown (≥ 50). A colored circle near the number at the nodes indicates the following: blue represents dispersal, green represents vicariance, and yellow represents extinction. Ciliochorella species are shown in bold and green.

Taxonomy

Ciliochorella Syd., in Sydow & Mitter, Annls mycol. 33(1/2): 62 (1935)

Fungal Names: FN 7657

Type species

Ciliochorella mangiferae Syd., Annls Mycol. 33(1/2): 63 (1935). Fungal Names: FN 270484.

Notes

Ciliochorella is an asexually typified genus. Most species of this genus are saprophytic with the exception of Ciliochorella castaneae Munjal. The conidiomata of Ciliochorella species are generally round, semi-immersed, and longitudinally lenticular. A prominent feature observed during the early stage of germination is apical and basal cells of conidia-produced germ tubes, and a vacuolated state of the protoplasm (Masilamani and Muthumary 1994). Conidiophores arise from the thin-walled, and are almost colorless cells of the basal or basal and parietal tissue, mostly reduced to conidiogenous cells. Occasionally, they are sparsely septate, branched or unbranched, colorless, smooth, invested in mucus (Sutton 1980; Nag Raj 1993). Conidiogenous cells are discrete, ampulliform, or conical with a long neck, colorless, and smooth. Conidia are cylindrical, straight, or slightly curved with septate pale brown middle cells and colorless end cells with appendages at one or both ends (Lee et al. 2006; Allegrucci et al. 2011; Tangthirasunun et al. 2015; Hyde et al. 2016; Wijayawardene et al. 2016; Liu et al. 2019a).

There are four Ciliochorella species for which molecular data is available on the NCBI repository (i.e. C. castaneae; C. dipterocarpi Samaradiwakara, Lumyong & K.D. Hyde; C. mangiferae and C. phanericola Norph., T.C. Wen & K.D. Hyde). Ciliochorella mangiferae is the earliest recorded species and described by Sydow and Mitter (1935) as the type species of this genus. Tangthirasunun et al. (2015) discovered a new record of C. mangiferae in Thailand and provided some its molecular data for this species. The first discovery of C. castaneae was in India (Nag Raj 1993), but Endo et al. (2008) added a new record for this species in Japan and also added molecular data. Samaradiwakara et al. (2023) discovered C. dipterocarpi and analyzed the species molecularly. For the other species of this genus, there is still no molecular data available, and comprise C. splendida Nag Raj & R.F. Castañeda and C. buxifoliae Allegr., Ellegr. & Aramb (Nag Raj 1993; Allegrucci et al. 2011). The morphological characteristics of all Ciliochorella species are provided in Table 2.

Table 2.
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The comparison of micro-morphological characteristics of Ciliochorella.

Species Host-Substratum Conidiomata diam (μm) Conidiomata with a papillary Conidia (μm) Mean conidium length/width ratio Basal appendages number Reference
Ciliochorella buxifoliae Scutia buxifolia 300–500 – 19–21×2.5–2.7 7:1 1 Allegrucci et al. 2011
C. castaneae Castanea europaea 450–650 Yes 13–19×2.5–3.2 (Ave.16.0×3.0) 11.1:1 1 Nag Raj 1993; Endo et al. 2008
C. chinensis Unidentified leaf litter 894–1314 Yes 13.9–17.9×3.3–4.1 (Ave.15.7×3.6) 4.4:1 1 In this study
C. dipterocarpi Dipterocarpaceae alatus 650–800 No 9–18×1–3 (Ave.14×2) 7:1 1 Nethmini et al. 2023
C. mangiferae Mangifera indica 400–800 – 32–43×2.5–3.5 (Ave. 37×3) 12.3:1 1 Nag Raj 1993
C. phanericola Phanera purpurea 1000–1200 No 13–15×2.8–3.5 (Ave. 15×3.7) 4.1:1 1 Hyde et al. 2016
C. savannica Unidentified leaf litter 530–952 Yes 11–16×2–3 (Ave.14×2.6) 5.4:1 0 In this study
C. splendida Quercus oleoidessubsp. Sagrana – – 24–40×2.5–3 (Ave. 32×2.7) 11.8:1 1 Nag Raj 1993

Ciliochorella chinensis H.X. Wu & J.C. Li, sp. nov.

Fungal Names: FN 571291

Etymology

The species epithet reflects China where the species of Ciliochorella was first collected country.

Holotype

IFRD9468.

Description

Saprobic on leaf litter. Asexual morph: Coelomycetous. Conidiomata 894–1314 μm diameter (x¯ = 1055 μm, n = 14), unilocular, semi-immersed, circular areas, dark brown, mostly aggregated, sometimes solitary, forming a papilla in the center (Fig. 4a–c). Conidiomata wall comprises a few to several layers of cells of textura angularis, with the innermost layer thin, transparent, and precisely arranged, the outer layer dark brown to black (Fig. 4d). Conidiophores appear to be reduced to conidiogenous cells. Conidiogenous cells are enteroblastic phialidic, formed from the innermost layer of the wall, hyaline to pale brown, and smooth (Fig. 4e). Conidia 14–18 × 3–4 μm (x¯ = 15.7 × 3.6 μm, n = 12), excluding apical and basal appendages, mean conidium length/width ratio = 4.4:1, navicular to subcylindrical, slightly curved, 1-septate, wide middle two cells with apical cell transformed into two forked filiform cellular appendages, 9–16 μm (x¯ = 12.5 μm, n = 20), the narrow basal cell with basal appendage, 4–7 μm (x¯ = 5.4 μm, n = 11), colorless to light brown, with guttules on the conidia surface (Fig. 4f–i). Sexual morph: Unknown.

Figure 4. 

Ciliochorella chinensis (IFRD9468, holotype; IFRDCC3202, ex-type strain) a, b the specimen c surface of fruiting bodies d longitudinal section of the conidioma e peridium f–h mature conidia i mature conidia in cotton blue j, k colonies on PDA (k from below) l, m colonies on PDA (m from below) n fruiting bodies on PDA o fruiting bodies in PDA p peridium q–t mature conidia. Scale bars: 400 µm (c, n, o); 200 µm (d); 40 µm (p); 20µm (e); 10 µm (f–i, q–t).

Culture characteristics

Colonies on PDA, reaching 4.4 cm (n = 3) diam after 7 days at 26 °C, producing dense mycelium, irregular circular, margin rough, white (Fig. 4j, k). Conidia germinated and grew deep into the medium. There was a clear boundary between the center and the most marginal part. The culture grew fruiting bodies after about four months on PDA medium at 26 °C (Fig. 4l, m). The morphology of conidiophores and conidia in the semi-immersed or fully embedded medium was consistent with that found under natural conditions (Fig. 4n–t).

Material examined

China. Yunnan Province, Yuanjiang County, Yuanjiang National Nature Reserve (Xiaohedi), on dead leaves of an unidentified plant, 23°28'33"N, 102°21'1"E, elevation 423 m, June 2021, Hai-Xia Wu, Jin-Chen Li, and Xin-Hao Li (IFRD9468, holotype; IFRDCC3202, ex-type).

Notes

The phylogenetic tree shows that Ciliochorella chinensis has a close relationship with C. castaneae (HHUF 28800) (Fig. 1). A BLAST search conducted within GenBank, the match for LSU showed a 98.72% similarity to C. castaneae (HHUF 28800, this species only has LSU) across a query coverage of 95%. At present, the phylogenetic relationship in this genus is not comprehensive enough, so the classification depends greatly on their morphology. Morphologically, the conidiomata of C. chinensis have a papillary, which the conidiomata of C. phanericola lack. The conidiomata of both species display different sizes (Table 2).

Ciliochorella savannica H.X. Wu & J.Y. Song, sp. nov.

Fungal Names: FN 571290

Etymology

Epithet derived from the type locality (Yuanjiang Savanna Ecosystem Research Station).

Holotype

IFRD9467.

Description

Saprobic on leaf litter. Asexual morph: Coelomycetous. Conidiomata 530–950 μm diameter (x¯ = 758 μm, n = 23), unilocular, semi-immersed, circular areas, black, mostly aggregated, sometimes solitary, with a papilla central circular ostiole (Fig. 5a–c). Conidiomata wall comprises a few to several layers of cells of textura angularis, with the inner layer being mostly thin, brown, whereas the outer layer appears dark brown to black. The longitudinal section is lenticular, the base is well developed (Fig. 5d). Conidiophores are reduced to conidiogenous cells. Conidiogenous cells enteroblastic phialidic, formed from the innermost layer of the wall, hyaline to pale brown, smooth (Fig. 5e). Conidia 11–16 × 2–3 μm (x¯ = 14 × 2.6 μm, n = 22) excluding apical appendages, mean conidium length/width ratio = 5.4:1, navicular to subcylindrical, slightly curved, 1-septate, narrow basal cell, wide middle two cells with apical cell transformed into two forked filiform cellular appendages 7–13 μm (x¯ = 10 μm, n = 22), 2–4-guttulates on the surface of the conidia, without basal appendages (Fig. 5f–i). Sexual morph: Unknown.

Figure 5. 

Ciliochorella savannica (IFRD:9467, holotype; IFRDCC:3201, ex-type) a, b the specimen c surface of fruiting bodies d longitudinal section of the conidioma e peridium f–h mature conidia i mature conidia in cotton blue j, k colonies on PDA (k from below). Scale bars: 400 µm (c); 200 µm (d); 20µm (e); 10 µm (f–i).

Culture characteristics

Conidia germinated and hyphae grew in emission form the center to the outside (Fig. 5j, k). Colonies growing on PDA, reaching a diameter of 4.4 cm (n = 3) after 7 days at 26 °C, producing dense mycelium, circular, margin rough. Surface white from the surrounding of the mycelium on PDA and pale yellow in reverse.

Material examined

China. Yunnan Province, Yuanjiang County, Yuanjiang Savanna Ecosystem Research Station (Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences), 23°28'31"N, 102°10'38"E, 579 m, on dead leaves of an unidentified plant, June 2021, Hai-Xia Wu, Jin-Chen Li, and Xin-Hao Li (IFRD9467, holotype; IFRD9473, paratype; IFRDCC3201, ex-type).

Notes

Two strains of Ciliochorella savannica (holotype and paratype) correspond to Ciliochorella described by Sydow and Mitter (1935). The phylogenetic analysis showed that this species is only distantly related to other species in Ciliochorella. The number of different bases in ITS and LSU sequences of holotype and paratype was 7 (1033/1040) and 4 (1406/1410), respectively. These two strains of C. savannica formed a subclade within Ciliochorella, with 97% ML and 1.00 Bayesian posterior probabilities (Fig. 1). They differ morphologically from other species in conidiomata size (530–952 μm) and mean conidium length/width ratio (5.4:1) (Table 2). The significant characteristic is that C. savannica has conidia that lack basal appendages, whereas Ciliochorella species have this characteristic.

Enzyme activity screening

The temperature was maintained at 26 °C. After 7 days of inoculation, Congo red staining was used to determine whether the strain had cellulase production ability (Fig. 6a, d). The results showed that both C. chinensis and C. savannica produced discoloring circles on the solid medium, with the discoloration of C. savannica being more pronounced. This indicates that cellulase plays a role in the cellulose degradation of both species.

Figure 6. 

Screening of enzyme activity in culture a C. chinensis was cultured on solid PDA medium for 7 days and stained with Congo red stain b C. chinensis on solid guaiacol-PDA medium after 1 day c C. chinensis on solid guaiacol-PDA medium after 12 days d C. savannica was cultured on PDA solid medium for 7 days and stained with Congo red stain e C. savannica on guaiacol-PDA solid medium 1 day f C. savannica on solid guaiacol-PDA medium for 10 days g determination of enzyme activity.

Guaiacol-PDA solid medium was used to screen for laccase, and the temperature was set at 26 °C. The results were as follows: C. chinensis had a lighter color reaction on the solid medium until after 12 days (Fig. 6b, c) while C. savannica showed a color reaction obvious on the solid medium after 10 days (Fig. 6e, f).

The enzyme activity of the supernatant was determined by the Thermo Varioskan Flash enzyme marker. The average content of cellulose and laccase for C. savannica was 4.97 U/ml (n = 3) and 1.16 U/ml (n = 3); and for C. chinensis, the average cellulose content was 5.05 U/ml (n = 3) and laccase content was 1.71 U/ml (n = 3) (Fig. 6g). This suggests that laccase participates in lignin degradation of both species. There is no strong positive correlation between color reaction and numerical value, and the specific reasons need to be further explored.

Discussion

Ciliochorella species play important roles in the decomposition of litter (Saparrat et al. 2010), and as such are a part of the carbon cycle throughout the world. The main body of Ciliochorella research has focused on the phylogeny and morphology of these fungi (Kalani 1963; Seshadri et al. 1969; Nag Raj 1993; Endo et al. 2008; Allegrucci et al. 2011; Hyde et al. 2016; Samaradiwakara et al. 2023). By contrast, the evolutionary history of Ciliochorella, whether based on DNA sequence analysis or the ecosystem studies, has received less attention and has remained unclear.

Wijayawardene et al. (2022b) stated that the subtropical to tropical regions in Asia will be an important region for discovering new fungal taxa, specifically asexually typified taxa. In China, the savanna-like vegetation has a unique geography and complex topography, which has contributed to the formation of various habitats with high biodiversity (Zhu and Tan 2022). Investigations have been carried out in the savanna-like vegetation in hot dry valleys of southwestern China, and this site is referred to as the “Chinese savanna”. However, only a few reports have focused on fungi in this habitat, most of which have concentrated on endophytic and soil fungi (He et al. 2011; Ruan 2011; Yi et al. 2011). In addition, most Ciliochorella species were recorded from Asia except for C. buxifoliae and C. splendida, both of which occur in America (Nag Raj 1993; Endo et al. 2008; Allegrucci et al. 2011; Tangthirasunun et al. 2015; Hyde et al. 2016). According to the best of our knowledge, Ciliochorella species have not been recorded from China before. Our studies resulted in the discovery of two new Ciliochorella species: C. chinensis and C. savannica. This finding not only contributed two new species to the growing catalog of microfungal species found in the Chinese savanna, but also represents the first Ciliochorella specimens reported for China. The two new species in this paper have been characterized based on phylogenetic analysis (Fig. 1) and morphological characteristics (Table 2). They belong to the genus Ciliochorella, which is part of the Sporocadaceae family, and the result is consistent with previous studies (Samarakoon et al. 2016; Liu et al. 2019a; Tennakoon et al. 2021).

The study of fossil fungi has become an essential tool for understanding fungal evolution and diversification, as well as elucidating the relationships of fungi to other organisms in the historical context of a given ecosystem (Taylor et al. 2015; Liu et al. 2019b; Samarakoon et al. 2019; Li et al. 2023). Despite wide distribution and large population, the majority of fungi (mycelia) are readily decomposed after death, resulting in a scarcity of fungal fossils that can be utilized for research concerning evolution (Tao and Chen 2020). In this report, we used the r8s program based on molecular clocks and two secondary calibration nodes to assess divergence times, which allowed us to estimate the emergence of the Ciliochorella at around 38 Mya during the Paleogene (Fig. 2). The Cretaceous-Paleogene mass extinction caused the disappearance of numerous groups, and its aftermath saw the rapid diversification of surviving species (Klein et al. 2021). According to the results of this study, Ciliochorella appeared in the middle and late periods of the Paleogene explosion of species. In addition, recent phylogeny and genomic studies used for the divergence time of Sordariomycetes indicate that relying solely on genus-level estimations may lack sufficient evidence and could potentially introduce errors (Chen et al. 2023). However, the divergence time estimated in this study does not conflict with the results based on genomic data.

The ancestral biogeography of Ciliochorella was investigated for the first time in this study. The result showed that the ancestor of Ciliochorella species originated from the Eurasian continent during the late Cretaceous. From approximately the late Cretaceous to the early Paleogene, there were some dispersal, vicariance and extinction events, which may be related to extreme climate incidents (Hu and Liu 2003). At about 30 Mya, there are two dispersal events that occurred within Ciliochorella. Up to this point, Ciliochorella species have been only found in Asia, Africa and America (Nag Raj 1993; Masilamani and Muthumary 1994; Endo et al. 2008; Tangthirasunun et al. 2015; Hyde et al. 2016). The results of our study clarify the evolutionary history of Ciliochorella ancestors and also provide a reference for the estimation of the divergence times of similar genera.

Some pathogenic plant fungi eliminate the effects of plant antiviral and tannic acid via laccase activity (Dong and Changsun 2021). By screening Ciliochorella chinensis and C. savannica strains on the medium, we found that both new species produce laccase and cellulase. They are involved in the decomposition of lignin and cellulose of leaf litter in their natural habitat, but their decomposition efficiency needs further study. Hyde et al. (2016) identify C. phanericola as a pathogen. The present study also supports the idea that Ciliochorella may have a potential role as a pathogenic plant fungus.

Acknowledgements

The authors are deeply grateful to Prof. Kirst King-Jones (University of Alberta) for language improvement.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

This study was supported by the National Natural Science Foundation of China (grant No. 32170024) the Grant for Essential Scientific Research of National Nonprofit Institute (No. CAFYBB2019QB005), and the Yunnan Province Ten Thousand Plan of Youth Top Talent Project (No. YNWR-QNBJ-2018-267).

Author contributions

Methodology, H.-X. W., W.-F. D. and J.-Y. S.; formal analysis, H.-X. W. and J.-Y. S.; resources, H.-X. W., J.-C. L. and J.-Y. S.; sampling guidance, D.-X. Y.; data curation, J.-Y. S., J.-C. L., C.-L. G. and H.-X. W.; writing—original draft preparation, J.-Y. S.and H.-X. W.; writing—review and editing, J.-Y. S., H.-X. W., N. W. and X.-Y. Z.; project administration, H.-X. W.; funding acquisition, H.-X. W. All authors have read and agreed to the published version of the manuscript.

Author ORCIDs

Jia-Yu Song https://orcid.org/0000-0002-0884-7594

Hai-Xia Wu https://orcid.org/0000-0002-7169-6717

Jin-Chen Li https://orcid.org/0000-0001-8977-1829

Wei-Feng Ding https://orcid.org/0000-0002-2471-8071

Cui-Ling Gong https://orcid.org/0009-0005-9282-0974

Xiang-Yu Zeng https://orcid.org/0000-0003-1341-1004

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

Da-Xin Yang https://orcid.org/0009-0008-9985-4669

Data availability

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

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