1urn:lsid:arphahub.com:pub:F9B2E808-C883-5F47-B276-6D62129E4FF4urn:lsid:zoobank.org:pub:245B00E9-BFE5-4B4F-B76E-15C30BA74C02Biodiversity Data JournalBDJ1314-28361314-2828Pensoft Publishers10.3897/BDJ.9.e590015900114840Taxonomic PaperFungiBiodiversity & ConservationCenozoicAsiaOne new species and one new record of Zasmidium in ChinaAnYuan-Yanhttps://orcid.org/0000-0001-5549-10281ZengXiang-Yuhttps://orcid.org/0000-0003-1341-1004123GengKun4HydeKevin David23WangYongyongwangbis@aliyun.com1Department of Plant Pathology, Agriculture College, Guizhou University, Guiyang, ChinaDepartment of Plant Pathology, Agriculture College, Guizhou UniversityGuiyangChinaCenter of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai, ThailandCenter of Excellence in Fungal Research, Mae Fah Luang UniversityChiang RaiThailandSchool of Science, Mae Fah Luang University, Chiang Rai, ThailandSchool of Science, Mae Fah Luang UniversityChiang RaiThailandGuiyang plant protection and inspection station, Guiyang, ChinaGuiyang plant protection and inspection stationGuiyangChina
Corresponding author: Yong Wang (yongwangbis@aliyun.com).
Academic editor: Danny Haelewaters
2021070120219e5900184A2745A-88C0-5EFA-8684-92DA9208063944414092609202008122020Yuan-Yan An, Xiang-Yu Zeng, Kun Geng, Kevin David Hyde, Yong WangThis 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.Background
Two hyphomycetous species were collected from leaves of Smilaxchina (Liliales, Smilacaceae) and Cremastraappendiculata (Asparagales, Orchidaceae). ITS barcoding indicated that they belong to the genus Zasmidium.
New information
Morphological data in combination with molecular phylogenetic analyses based on ITS, LSU and rpb2 confirmed that our Chinese strains represented a new species, Zasmidiumliboense and a new record of Z.citri-griseum.
one new speciesasexual morphDothideomycetesMycosphaerellaceaetaxonomyIntroduction
The fungi of southern Asian are extremely diverse (Hyde et al. 2018, Cheek et al. 2020). During a survey of fungal diversity in ornamental plants in south-western China from 2017 to 2019, more than 2000 strains were obtained, which represented asexual morphs of both Ascomycota and Basidiomycota. Some new taxa were previously described by our research group as pathogens or endophytes (e.g. Liang et al. 2018, Long et al. 2019, Sun et al. 2020, Wijesinghe et al. 2020, Zhang et al. 2020).
The genus Zasmidium was established by Fries (1849) with Z.cellare (Pers.) Fr. as the type species. It is currently placed in the order Capnodiales within the Dothideomycetes (Hongsanan et al. 2020, Wijayawardene et al. 2020). Arzanlou et al. (2007) showed that Zasmidium was the oldest name for Stenella-like hyphomycetes within Mycosphaerellaceae, which are characterised by conidiogenous loci and conidia with truncate hila (Bensch et al. 2012). Hence, many former Stenella species were transferred to Zasmidium (Braun et al. 2010, Kamal 2010). Up to now, the number of accepted species in the genus is about 150 (Wijayawardene et al. 2020).
In this paper, we report on Zasmidium species found on medicinal plants in China. One new species (Zasmidiumliboense) and one new Chinese record (Z.citri-griseum) are reported, based on evidence from morphology and molecular phylogeny.
Materials and methodsSamples collection and fungal strains isolation
The samples were collected in Xishuangbanna City, Yunnan Province, China. In order to obtain pure cultures, diseased leaf pieces of Smilaxchina (Liliales, Smilacaceae) and Cremastraappendiculata (Asparagales, Orchidaceae) were surface-disinfected following the method of Zhang et al. (2020). The strains were isolated using the single-spore method (Chomnunti et al. 2014). Colonies growing from single spores were transferred to potato-dextrose agar (PDA) and incubated at room temperature (28ºC). The holotype was deposited in the Herbarium of Department of Plant Pathology, Agricultural College, Guizhou University (HGUP). The ex-type cultures were deposited in the Culture Collection at the Department of Plant Pathology, Agriculture College, Guizhou University, P.R. China (GUCC) and the Mae Fah Luang University Culture Collection (MFLUCC) in Thailand.
Morphological description
Morphological culture characters were recorded after 2–3 weeks of growth on PDA. Microscopic slides were prepared in lactophenol. Light microscopy observations were made using a BX53 compound microscopy (Olympus, Tokyo, Japan) at 1000× magnification. The morphology was observed using a compound microscope (OLYMPUS BX53) showing all necessary details of morphology and ontogeny of reproductive propagules. Measurements were made of 30 structures for conidia, hila and conidiophores. The new species name was submitted to MycoBank (www.mycobank.org).
DNA extraction, PCR amplification and sequencing
Fungal cultures were grown on PDA at 28°C. When the whole Petri-dish (90 mm diam.) was nearly covered, fresh mycelia were scraped from the surface with sterilised scalpels. Genomic DNA was extracted using Fungus Genomic DNA Extraction Kit (Biomiga #GD2416, San Diego, California, USA) and following the manufacturer's instructions. PCR amplification of the internal transcribed spacer (ITS) region and the large subunit (LSU) of the ribosomal RNA gene was performed in a 25-μl reaction volume system as in Liang et al. (2018). Primers V9G and ITS4 (White et al. 1990, de Hoog and van den Ende 1998) were used to amplify the ITS and LSU1Fd and LR5 for the LSU (Vilgalys and Hester 1990, Crous et al. 2009). In addition, one protein-coding gene fragment, RNA polymerase II second largest subunit (rpb2), was amplified with the primers fRPB2-5F and fRPB2-7cR (Liu et al. 1999). Purification and sequencing of the PCR amplicons were undertaken by SinoGenoMax (Beijing, China). The resulting DNA sequences were submitted to NCBI GenBank (https://www.ncbi.nlm.nih.gov/genbank/) and their accession numbers are provided in Table 1.
Phylogenetic analyses
Our newly-generated sequences were aligned by locus with ex-type and other representative sequences of Zasmidium species, which were downloaded from GenBank (Table 1). Alignments were made using the online version of MAFFT v. 7.307 (Katoh and Standley 2016) and manually improved, where necessary, using MEGA v. 6.06 (Tamura et al. 2013). Mesquite v. 2.75 (Maddison 2008) was used to concatenate the aligned sequences of the different loci. Ambiguous regions were excluded from analyses using AliView (Larsson 2014) and gaps were treated as missing data. DNA base differences of different gene loci between our strains and ex-type or representative strains of relative taxa are shown in Table 2. The alignment document is available in TreeBASE under the study ID 27250.
Maximum Parsimony (MP) analyses were performed in PAUP v. 4.0b10 (Swofford 2002), using the heuristic search option with 1,000 random sequence addition replicates and tree bisection-reconnection (TBR) as the branch swapping algorithm. Maxtrees was set at 10,000. The Tree Length (TL), Consistency Indices (CI), Retention Indices (RI), Rescaled Consistency Indices (RC) and Homoplasy Index (HI) were calculated for each tree generated.
Maximum Likelihood (ML) was inferred using the IQ-tree (Nguyen et al. 2015, Chernomor et al. 2016) under the Edge-linked partition model. Bootstrapping was done under 10000 ultrafast replicates (Hoang et al. 2018). ModelFinder (Kalyaanamoorthy et al. 2017) was used to select the best-fit partition model (Edge-linked) using BIC criterion. The best-fit model, according to BIC was: ITS: TNe+I+G4, LSU: TN+F+I+G4, rpb2: TN+F+I+G4.
For Bayesian Inference (BI), GTR+I+G was selected as the best model for all three loci (ITS, LSU and rpb2) as determined by MrModeltest v2 (Nylander 2004). BI analysis was undertaken using MrBayes v. 3.2.6 (Ronquist et al. 2012). Six Markov Chain Monte Carlo runs were launched with random starting trees for 1,000,000 generations and sampling every 1,000 generations. The first 25% resulting trees were discarded as burn-in.
Taxon treatmentsD97D94FD-E802-51FF-B7FC-2455428769D8ZasmidiumliboenseY.Y. An, Yong Wang bis & K.D. Hydesp. nov.Materials
Pathogenic on the leaf spot of Smilaxchina (Liliales, Smilacaceae). Lesions on the upper leaf surface, scattered, distinct, irregular, rather large, the maximum length of the spot more than 20 mm, the edges of the disease reddish-brown, the centre dead to greyish-white, on the lower leaf surface similar. Colonies on PDA 10–15 mm diam. in 2 weeks, with an even, dark coffee margin. Mycelium composed of hyaline and pale brown to dark blackish-brown hyphae, verruculose, septate, branching, uniform in width, 2.5 μm. Conidiophores arising from hyphae, pale olivaceous brown to pale blackish-brown, finely verruculose, straight or slightly curved, dendritic rugged or rugose on the surface 20–350 × 1.5–3.5 μm. Conidiogenous cells integrated, apical, polyblastic, proliferating sympodially, with rim-like conidiogenous loci, thickened and darkened, located apically and lateraly as in a short rachis 1.5–2.5 μm diam. Conidia solitary, occasionally catenate, pale blackish-brown to pale olivaceous brown, verruculose, ellipsoidal, cylindrical to obclavate, base obconically truncate and apex rounded, straight or curved, 6–21 × 2–4 μm, 0–1-septate, sometimes constricted at septa, with hila thickened and darkened, 1–1.5 μm diam. (Fig. 1)
MycoBank Number
MB836278
Etymology
In reference to the location (Libo county, Guizhou Province), where the holotype was isolated.
6940A98C-A2F7-5387-B8E6-56FC1C1650A1Zasmidiumcitri-griseum(F.E. Fisher) U. Braun & Crous, IMA Fungus 5 (2): 337 (2014)Materials
Type status:Other material. Occurrence: catalogNumber: HGUP 1507.3; recordedBy: An Yuan-Yan; occurrenceID: living culture GUCC 1507.3 and MFLUCC 20-0138; Taxon: scientificName: Zasmidiumcitri-griseum; kingdom: Fungi; class: Dothideomycetes; order: Capnodiales; family: Mycosphaerellaceae; genus: Zasmidium; Location: country: China; stateProvince: YunNan; locality: Xishuangbanna Dai Autonomous Prefecture; Identification: identifiedBy: Yuan-Yan An; dateIdentified: 2020; Record Level: language: en
Description
Pathogenic on leaf spot of Cremastraappendiculata (Asparagales, Orchidaceae). Lesions on the upper leaf surface, scattered to confluent, distinct, angular, spots elliptic to suborbicular, reddish-brown to dark brown, 2–5 mm, on the lower leaf surface similar. Colonies on PDA 10–15 mm diam. in 2 weeks, with an even, dark-brown margin. Surface fold, with gully shape. Conidiophores arising singly as lateral branches of superficial hyphae, semi-macronematous to macronematous, mononematous, erect to flexuous, sometimes curved, unbranched, thick-walled, non-smooth surface, 1–3-septate, cylindrical, geniculate, brown, 35–135 × 5–7 µm. Conidiogenous cells integrated, terminal, 5–10 µm long, sympodial, polyblastic, cylindrical, geniculate, scars slightly thickened and darkened, 0.5–1.5 µm in diam. Conidia solitary in simple or occasionally branched chains, short to long cylindrical, some ends swollen straight to somewhat curved, 8–41 × 2–5 µm, unseptate, light brown, thin-walled, verruculose, 2–3.5 µm wide. (Fig. 2)
Analysis
Our final concatenated alignment included 2407 characters , viz. (ITS: 1–537, LSU: 538–1354, rpb2: 1355–2407), of which 645 were parsimony-informative characters. MP inference resulted in two equally-parsimonious trees (TL = 3705, CI = 0.35, RC = 0.59, HI = 0.20, RC = 0.65) and one of them was selected to show the topology (Fig. 3). Forty-eight Zasmidium strains clustered together as a clade, which received maximum support from both ML and BI analyses. Zasmidiumliboense sp. nov. (GUCC 1720.2) was retrieved as sister taxon of Z.cellare (Pers.) Fr. (CBS 146.36) with high support (94 MP/89 ML/1.00 PP). Strain GUCC1507.3 grouped with a lineage consisting of Z.anthuriicola (U. Braun & C.F. Hill) Crous & U. Braun, Z.citri-griseum (F.E. Fisher) U. Braun & Crous and Z.suregadae Phengs., K.D. Hyde & U. Braun, with high support (99 MP/99 ML/1.00 PP). It was placed sister to Z.citri-griseum (CBS 122455) (86 ML).
A comparison of DNA bases (Table 2) demonstrated that, between Z.liboense (GUCC 1720.2) and Z.cellara (CBS 146.36), there were 23 bp differences in the ITS region, 19 in the LSU and 72 in the rpb2. The ITS sequence of GUCC 1507.3 differed in 8 bp from Z.citri-griseum (CBS 122455). Their LSU sequences were identical, whereas a single base pair difference was found in the rpb2.
Discussion
Our phylogenetic analyses pointed out that Zasmidiumliboense is different from Z.cellare. Morphologically, both species can be separated as well (Arzanlou et al. 2007). Zasmidiumliboense produces conidia with 0-1 septa, whereas those of Z.cellare possess 0–1(–4) septa. Conidia of Z.cellare arise terminally or laterally and are subhyaline, whereas those of Z.liboense arise terminally and are pale blackish-brown to pale olivaceous brown. In addition, conidia of Z.liboense (6–21 × 2–4 μm) generally have larger dimensions compared to those of Z.cellare (6–9 × 1.8–2.5 µm). We also compared micro-morphology of our new taxon with 74 Zasmidium species, for which no sequence data are available. Most of those, 64 species, produce larger conidia with more septa compared to Z.liboense. In addition, Z.araliae, Z.cerophilum and Z.litseae all possess smaller conidia than Z.liboense. The conidia of Z.capparacearum, Z.eriolobi, Z.gahniicola and Z.mitellae have more septa compared to those of Z.liboense. Zasmidiumclusiae produces conidia with basal unthickened hilum, whereas the conidia of Z.liboense, Z.deightonianum and Z.oxycocci have slightly or obviously thickened conidia. For these three species, the length of conidiophores can be used to distinguish amongst species: Z.liboense (20–350 μm), Z.deightonianum (10–30 μm) and Z.oxycocci (50–100 μm).
For strain GUCC 1507.3, our molecular phylogenetic data (Fig. 3, Table 2) showed that it was very close to Z.anthuriicola, Z.citri-griseum and Z.suregadae. Rbp2 sequences of strain GUCC 1507.3 and Z.citri-griseum (CBS 122455) are identical, but different from Z.anthuriicola (CBS 118742). Currently, no rpb2 sequences are available for Z.suregadae. Morphological comparison shows that conidia of our material (GUCC 1507.3) agree with the description of Z.citri-griseum; they are somewhat shorter although still in the range of measurements [Z.citri-griseum: 6–70(–120) × 2–4.5 μm] and they are aseptate [Z.citri-griseum: 0–1–(–6)-septate] (Braun et al. 2014). Zasmidiumcitri-griseum is one of the few species of Zasmidium with a wider host range. Braun et al. (2014) listed hosts in the Fabaceae, Musaceae and Rutaceae. The host of our Chinese material, Cremastraappendiculata (Orchidaceae), represents a new host family for this fungus.
Acknowledgements
This research was supported by the following sources: National Natural Science Foundation of China (No. 31972222, 31560489), Program of Introducing Talents of Discipline to Universities of China (111 Program, D20023), Talent Project of Guizhou Science and Technology Cooperation Platform ([2017]5788-5 and [2019]5641), Guizhou Science, Technology Department of International Cooperation Base Project ([2018]5806) and Guizhou Science and Technology Innovation Talent Team Project ([2020]5001).
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Zasmidiumliboense (GUCC 1720.2). a. Leaf spot symptoms on the host; b. Culture on PDA; c, d. hyphae and conidiophores on PDA; e–m. Conidiophores and conidia; n, o. Conidiogenous cells and conidia; p. Conidia. Scale bars: c, d = 50 µm, e–j = 10 µm, k = 5 µm, l–p = 10 µm.
Zasmidiumcitri-griseum (GUCC 1507.3) a. Leaf spot symptoms on host; b. Culture on PDA; c. Hyphae and conidiophores on PDA culture; d–h. Conidiophores, conidiogenous cells and conidia; i. Conidia; j, k. Conidiogenous cells and conidia; l–p. Conidia. Scale bars: c = 100 µm, d–g =10 µm, h=5 µm, i, j = 10 µm, k–p = 5 µm.
MP phylogeny of Zasmidium reconstructed from a three-locus dataset (ITS, LSU, rpb2). MP and ML bootstraps > 70 and BI posterior probabilities (PP) > 0.9 are placed close to topological nodes and separated by “/”. Nothopericoniellaperseamacranthae (CBS 122097) was selected as outgroup.
https://binary.pensoft.net/fig/477387
Taxa used for molecular phylogenetic analyses and their GenBank accession numbers. (T) = ex-type strain.