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Biodiversity Data Journal 10: e80122
doi: 10.3897/BDJ.10.e80122
Taxonomic Paper
Curvicladiella paphiopedili sp. nov. (Hypocreales,
Nectriaceae), a new species of orchid
(Paphiopedilum sp.) from Guizhou, China
Lian-chai Song , Lu Huang , Ling-ling Liu , Yao Feng , Li-li Wang , Zuo-yi Liu
‡ College of Agriculture, Guizhou University, Guiyang, China
§ Scientific research administration office, Guizhou Academy of Agricultural Sciences, Guiyang, China
| Institute of Plant Protection, Guizhou Academy of Agricultural Sciences, Guiyang, China
¶ Guizhou Institute of Soil and Fertilizer, Guizhou Academy of Agricultural Sciences, Guiyang, China
# School of Ethnic Medicine, Guizhou Minzu University, Guiyang, China
¤ Guizhou Key Laboratory of Agricultural Biotechnology, Guizhou Academy of Agricultural Sciences, Guiyang, China
Corresponding author: Zuo-yi Liu (gzliuzuoyi@163.com)
Academic editor: Ning Jiang
Received: 05 Jan 2022 | Accepted: 18 Mar 2022 | Published: 05 Apr 2022
Citation: Song L-c, Huang L, Liu L-l, Feng Y, Wang L-l, Liu Z-y (2022) Curvicladiella paphiopedili sp. nov.
(Hypocreales, Nectriaceae), a new species of orchid (Paphiopedilum sp.) from Guizhou, China. Biodiversity
Data Journal 10: e80122. https://doi.org/10.3897/BDJ.10.e80122
Abstract
Background
An asexual fungus, collected from diseased leaves of Paphiopedilum sp. from Guizhou
Province, China, and based on the phylogenetic analyses and morphological characters, it
was identified as a new species in Curvicladiella. The genus Curvicladiella are recorded for
the first time for China.
New information
The morphology of Curvicladiella paphiopedili sp. nov. is characterised by penicillate
conidiophores with a stipe, dull, tapering towards the apex, the curved stipe extension and
cylindrical conidia. In the phylogenetic analyses of combined cmdA, his3, ITS, LSU, tef1
‡,§ | ¶ # § ¤
© Song L et al. 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.
and tub2 sequence data, this taxon was clustered as sister to Curvicladiella cignea within
Nectriaceae.
Keywords
Curvicladiella, morphology, phylogeny, Paphiopedilum, taxonomy
Introduction
Nectriaceae (order Hypocreales) includes many important plant and human pathogens and
some species have been used as biodegrading and biocontrol agents in industrial and
commercial applications (Lombard et al. 2015). Based on molecular studies, many sexual
genera in Nectriaceae were placed in Nectria sensu lato ( Rehner and Samuels 1995,
Rossman et al. 1999). However, Nectria sensu stricto is restricted to the type species N.
cinnabarina (Tode) Fr et al. with tubercularia-like asexual morphs (Rossman 2000, Hirooka
et al. 2012). A number of studies have treated taxonomic concepts within Nectriaceae,
based on multi-gene phylogenetic inference (Lombard et al. 2010a, Lombard et al. 2010b,
Chaverri et al. 2011, Gräfenhan et al. 2011, Schroers et al. 2011, Hirooka et al. 2012,
Lombard and Crous 2012a, Lombard and Crous 2012b, Lombard et al. 2014a, Lombard et
al. 2014b). Lombard et al. (2015) provided a phylogenetic backbone tree for Nectriaceae,
based on combined sequence data of 10 gene regions. Curvicladiella is one of the genera
in the Nectriaceae.
Decock and Crous (1998) established Curvicladium (as Curvicladiella) with C. cigneum (as
Curvicladiella cignea) as the type species. The genus is distinct from morphologically-
similar genera, such as Cylindrocladium Morgan, Cylindrocladiella Boesew, Gliocladiopsis
Saksena, Falcocladium Silveira, Alfenas, Crous, Wingf and Xenocylindrocladium Decock,
Hennebert, Crous by having cylindrical conidia and stipe extensions (Decock and Crous
1998). Curvicladiella cignea is the only species in the genus.
Based on the phylogenetic analyses and morphological characters, the fungus collected
from diseased leaves of Paphiopedilum sp. is identified as a new species in Curvicladiella,
the artificial infection test shows that it is a pathogen and the specific infection process has
been described by Song et al. (Song et al. 2020). Paphiopedilum is known as“slipper
orchids”, has a high ornamental value and can be used as household bonsai and garden
plants(Luan et al. 2019).
Materials and methods
Sample collection and isolation
Diseased orchid leaves were collected from Guizhou Botanical Garden, Guizhou Province,
China (in August 2019). The samples were brought to the laboratory in envelopes,
photographed and identified. Pieces of leaves (5 × 5 mm), half of which were diseased and
2Song L et al
half healthy, were sterilised by 75% ethanol for 5–10 s, rinsed three times with sterilised
distilled water, placed on potato dextrose agar (PDA) and incubated at 25°C for two days
(Fang 2001). Mycelia were transferred to PDA and incubated for ten days at 25°C to obtain
the pure cultures. The morphological characters of the fungi obtained from the diseased
leaves collected in the field and cultured with PDA, and the fungi obtained from the
diseased leaves after an artificial infection test were observed using a Nikon SMZ 745
stereomicroscope. Measurements were made using Image Frame Work.
Pure cultures were deposited in Guizhou Culture Collection (GZCC) Guizhou, China and
Mae Fah Luang University Culture Collection (MFLUCC), Chiang Rai, Thailand. Herbarium
specimens were deposited in the Guizhou Academy of Agricultural Sciences (GZAAS),
Guiyang, China and the Herbarium of Mae Fah Luang University (MFLU), Chiang Rai,
Thailand.
DNA extraction, PCR amplification and sequencing
The fungal mycelia were scraped from the pure culture growing on PDA for ten days at
25ºC. DNA was extracted using the Ezup Column Fungi Genomic DNA Purification Kit
(Sangon Biotech, China). Six gene regions, the 28S large subunit rDNA (LSU), calmodulin
(cmdA), histone H3 (his3), internal transcribed spacer region and intervening 5.8S nrRNA
gene (ITS), translation elongation factor 1-alpha (tef1) and β-tubulin (tub2) gene were
amplified by the primer pairs LR0R and LR5(Vilgalys and Hester 1990, Rehner and
Samuels 1994), CAL-228F and CAL2Rd (Carbone and Kohn 1999, Groenewald et al.
2013), CYLH3F and CYLH3R ( Crous et al. 2004), ITS5 and ITS4 (White et al. 1990),
EF1-728F and EF2 (O'Donnell et al. 1998, Carbone and Kohn 1999), T1 and CYLTUB1R
(O'Donnell and Cigelnik 1997, Crous et al. 2004), respectively. Polymerase chain reaction
(PCR) was carried out in 25 µl reaction volume containing 12.5 µl 2 × PCR Master Mix
(Sangon Biotech, China), 9.5 µl ddH O, 1µl of each primer and 1µl DNA template. The
PCR products were examined by using 1.2% agarose electrophoresis gel, stained with
ethidium bromide and were purified and sequenced by Sangon Biotech (Shanghai) Co.
Ltd, China. The nucleotide sequences were submitted in GenBank.
Phylogenetic analyses
Phylogenetic analyses were performed using combined sequence data with six gene
regions, LSU, cmdA, his3, ITS, tef1 and tub2. Related strains of Curvicladiella (Table 1)
were referred to Lombard et al. (2015). Sequences were obtained from GenBank. The
sequences were aligned using the online multiple alignment programme MAFFT v.7 (http://
mafft.cbrc.jp/alignment/server) (Standley 2013). The alignments were checked visually and
optimised manually by using BioEdit v. 7.2.6.1.
Maximum Likelihood (ML) analysis was performed using RaxmlGUI 1.3.1 (Silvestro and
Michalak 2012). The optimal RAxML tree search was conducted with 1000 bootstrap
replicates and the default algorithm was used from a random starting tree for each
replicate. The final tree was selected from amongst suboptimal trees from each replicate
by comparing likelihood scores under the GTR+GAMMA substitution model.
2
Curvicladiella paphiopedili sp. nov. (Hypocreales, Nectriaceae), a new ... 3
Taxa Isolate
numbers
GenBank Accession numbers
LSU CMDA HIS3 ITS TEF1 TUB2
Aquanectria
penicillioides
CBS 257.54 KM231613 KM231275 –KM231743 KM231865 KM232000
Aquanectria
submersa
CBS 394.62 KM231612 –KM231458 HQ897796 –KM231999
Calonectria brassicae CBS 111869 GQ280698 GQ267382 DQ190720 GQ280576 FJ918567 AF232857
Calonectria ilicicola CBS 190.50 GQ280727 AY725764 AY725676 GQ280605 AY725726 AY725631
Calonectria
naviculata
CBS 101121 GQ280722 GQ267399 GQ267252 GQ280600 GQ267317 GQ267211
Campylocarpon
fasciculare
CBS 112613 HM364313 KM231297 JF735502 AY677301 JF735691 AY677221
Campylocarpon
pseudofasciculare
CBS 112679 HM364314 KM231298 JF735503 AY677306 JF735692 AY677214
Corallonectria
jatrophae
CBS 913.96 KM231611 KM231273 KM231457 KC479758 KM231863 KC479787
Curvicladiella cignea CBS 101411 JQ666075 KM231285 KM231459 KM231744 KM231866 KM232001
Curvicladiella cignea CBS 109168 JQ666074 KM231286 KM231460 KM231745 KM231868 KM232003
Curvicladiella cignea CBS 109167 AY793431 KM231287 KM231461 AF220973 KM231867 KM232002
Curvicladiella
paphiopedili
MFLUCC
20-0110
MT279199 MT294104 MT294105 MT279198 MT294103 MT294102
Curvicladiella
paphiopedili
GZCC22-0001 OM899803 – – OM903885 – –
Cylindrocarpostylus
gregarius
CBS 101074 KM231614 KM231291 –KM231746 KM231869 KM232004
Cylindrocarpostylus
gregarius
CBS 101072 JQ666084 KM231292 –KM231747 KM231870 KM232005
Cylindrocarpostylus
gregarius
CBS 101073 JQ666083 KM231293 KM231465 KM231748 KM231871 KM232006
Cylindrocladiella
camelliae
CPC 234 JN099249 KM231280 AY793509 AF220952 JN099087 AY793471
T
T
T
T
T
T
T
T
T
T
Table 1.
Taxa or selected taxa used in this study and their GenBank accession numbers. The type species
have T as superscript and the newly-generated sequences have been highlighted in bold.
4Song L et al
Taxa Isolate
numbers
GenBank Accession numbers
LSU CMDA HIS3 ITS TEF1 TUB2
Cylindrocladiella
lageniformis
CBS 340.92 JN099165 KM231279 AY793520 AF220959 JN099003 AY793481
Cylindrocladiella
parva
CBS 114524 JN099171 KM231281 AY793526 AF220964 JN099009 AY793486
Dematiocladium
celtidis
CBS 115994 AY793438 KM231274 –AY793430 KM231864 –
Gliocephalotrichum
bulbilium
CBS 242.62 AY489732 KM231283 KF513326 – KM231892 DQ377831
Gliocephalotrichum
cylindrosporum
CBS 902.70T JQ666077 KM231284 KF513353 DQ366705 KF513408 DQ377841
Gliocephalotrichum
longibrachium
CBS 126571 KM231686 KM231282 KF513367 DQ278422 KF513435 DQ377835
Gliocladiopsis
irregularis
CBS 755.97 JQ666082 KM231278 JQ666023 AF220977 KF513449 JQ666133
Gliocladiopsis
pseudotenuis
CBS 116074 JQ666080 KM231277 JQ666030 AF220981 JQ666099 JQ666140
Gliocladiopsis
sagariensis
CBS 199.55 JQ666078 KM231276 JQ666031 JQ666063 JQ666106 JQ666141
Penicillifer
bipapillatus
CBS 420.88 KM231608 KM231270 KM231454 KM231740 KM231860 KM231996
Penicillifer
diparietisporus
CBS 376.59 KM231609 KM231271 KM231455 KM231741 KM231861 KM231997
Penicillifer penicilliferi CBS 423.88 KM231607 KM231269 KM231453 KM231739 KM231859 KM231995
Penicillifer pulcher CBS 560.67 KM231610 KM231272 KM231456 KM231742 KM231862 KM231998
Rugonectria
neobalansae
CBS 125120 HM364322 KM231294 KM231466 KM231750 KM231874 HM352869
Rugonectria rugulosa CBS 129158 JF832761 KM231295 KM231467 JF832661 KM231872 JF832911
Rugonectria rugulosa CBS 126565 KM231615 KM231296 KM231468 KM231749 KM231873 KM232007
Thelonectria
discophora
CBS 125153 HM364307 KM231327 KM231489 HM364294 KM231897 HM352860
Thelonectria olida CBS 215.67 HM364317 KM231325 KM231487 AY677293 HM364345 KM232024
Thelonectria trachosa CBS 112467 HM364312 KM231326 KM231488 AY677297 KM231896 AY677258
Xenocylindrocladium
guianense
CBS 112179 JQ666073 KM231289 KM231463 AF317348 KM231895 AF320197
T
T
T
T
T
T
T
T
T
T
T
T
T
T
T
Curvicladiella paphiopedili sp. nov. (Hypocreales, Nectriaceae), a new ... 5
Taxa Isolate
numbers
GenBank Accession numbers
LSU CMDA HIS3 ITS TEF1 TUB2
Xenocylindrocladium
serpens
CBS 128439 KM231688 KM231290 KM231464 AF220982 KM231894 AF320196
Xenocylindrocladium
subverticillatum
CBS 113660 KM231687 KM231288 KM231462 AF317347 KM231893 AF320196
T Ex-type and ex-epitype cultures. CBS: CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands; CPC:
P.W. Crous collection.
Bayesian analyses were carried out using MrBayes 3.2 (Huelsenbeck 2012). MrModeltest
2.2 was used to choose the best-fit evolutionary model (Nylander 2004). Posterior
probabilities (PP) (Rannala and Yang 1996, Zhaxybayeva and Gogarten 2002) were
determined by Markov Chain Monte Carlo sampling (MCMC) in MrBayes v. 3.2. Six
simultaneous Markov chains were run for 10 million generations and trees were sampled
every 1000 generation. The temperature values were lowered to 0.15, burn-in was set to
0.25 and the run was automatically stopped as soon as the average standard deviation of
split frequencies reached below 0.01.
The resulting trees of Maximum Likelihood and Bayesian were visualised with Fig Tree v.
1.4.0. The layouts were undertaken using Microsoft Powerpoint 2010 and Adobe
Photoshop CS6.
Taxon treatment
Curvicladiella paphiopedili Lian-Chai Song,Jing Yang, Zuo-Yi Liu, 2019, sp.
nov.
• IndexFungorum http://www.indexfungorum.org/names:IF558310
• Species-ID Facesoffungi number:FOF 09697
Materials
Holotype:
a. scientificName: Curvicladiella paphiopedili; class: Sordariomycetes; order: Hypocreales;
family: Nectriaceae; genus: Curvicladiella; locationRemarks: China, Gui Zhou Province,
Guiyang City, Guizhou Botanical Garden, 26°37'N, 106°43'E, 13 August 2019; habitat:
Terrestrial; fieldNotes: diseased leaves of Paphiopedilum sp.; recordNumber: zwy-dl4-2;
recordedBy: Lian Chai Song; type: Stilllmage; language: English; collectionID: MFLU
20-0203
Isotype:
a. scientificName: Curvicladiella paphiopedili; class: Sordariomycetes; order: Hypocreales;
family: Nectriaceae; genus: Curvicladiella; locationRemarks: China, Gui Zhou Province,
Guiyang City, Guizhou Botanical Garden, 26°37'N, 106°43'E, 13 August 2019; habitat:
Terrestrial; fieldNotes: diseased leaves of Paphiopedilum sp.; recordNumber: zwy-dl4-2;
T
T
th
6Song L et al
recordedBy: Lian Chai Song; type: Stilllmage; language: English; collectionID: GZAAS
19-2061
Description
The characters of pathogenic fungi on the leaves were identified through an artificial
infection test. Asexual morph: Conidiomata white, scattered, hairy. Conidiophores
straight to flexuous, consisting of a stipe bearing a penicillate arrangement of fertile
branches, stipe septate, hyaline, smooth; stipe extensions septate, straight or curved,
dull and tapering towards the apex, 128.5–549.9 µm long, (x= 288.1 µm, n = 20).
The
primary branches of conidiogenous apparatus aseptate, 9.3–17.5 × 2.6–3.7 μm;
secondary branches aseptate, 9.9–19.1 × 2.5–3.9 μm; tertiary branches aseptate, 9.5–
17.6 × 2.6–3.7 μm; quaternary and additional branches (–6) aseptate, 11–16.3 × 2.5–
3.9 μm, each terminal branch producing 2–4 phialides; phialides doliiform to reniform,
hyaline, aseptate, apex with minute periclinal thickening and inconspicuous collarette.
Conidia cylindrical, rounded at both ends, straight, 1-septate, hyaline, (30.5–) 31.2–
37.2 (–42.0) × (2.6–) 2.9–3.5 (–3.9) µm, (x= 34.2 × 3.2 µm, n = 20) (Fig. 1). Sexual
morph: not observed.
Figure 1.
Curvicladiella paphiopedili. a The diseased leaves were withered; b, c Conidiomata; d–g
Stipes extension and conidiogenous cells; h–j Conidiogenous cells and conidiophores; k–n
Conidia. Scale bars: d–g=50 µm, h–j=20 µm, k–n=10 µm.
Curvicladiella paphiopedili sp. nov. (Hypocreales, Nectriaceae), a new ... 7
The characters of fungus obtained from the diseased leaves collected in the field
that
were cultured with PDA: after 10 days at 25°C on PDA, colonies reached 47 mm in
diam. Beige to pale yellow colony on the surface, brown in reverse with irregular
margins, extensive sporulation on the medium surface. Conidiophores straight to
flexuous, consisting of a stipe bearing a penicillate arrangement of fertile branches,
stipe extensions septate, straight or slightly flexuous, 104.4–153.0 µm long, (x= 128.7
µm, n = 10). The primary branches of conidiogenous apparatus aseptate, 8.9–17.8 ×
2.7–3.4 μm; secondary branches aseptate, 7.8–14.0 × 2.5–5.9 μm; tertiary branches
aseptate, 8.9–17.7 × 2.3–3.5 μm; quaternary and additional branches (–6) aseptate,
9.3–16.7 × 2.3–3.7 μm, each terminal branch producing 2–4 phialides; phialides
doliiform to reniform, hyaline, aseptate, apex with minute periclinal thickening and
inconspicuous collarette. Conidia cylindrical, rounded at both ends, straight, 1-septate,
hyaline, (38.5–) 45.2–56.6 (–63.2) × (2.2–) 2.9–4.2 (–4.9) µm, (x= 50.9 × 3.5 µm, n =
40). Chlamydospores thick-walled, ellipsoidal or sphaeropedunculate, brown to hyaline,
Figure 2.
Curvicladiella paphiopedili. (MFLU 20-0203, holotype) a Paphiopedilum diseased leaf in the
field; b The healthy leaves diseased after inoculating the mycelial PDA plug of Curvicladiella
paphiopedili ; c The healthy leaves did not become infected after being inoculated with free
PDA plug as control; d Colonies on PDA producing conidia masses; e–j Conidiophores,
conidiogenous cells and stipes extension; k Chlamydosporae; l, m Conidia; n, o Culture on
PDA; (n) from above, (o) from below. Scale bars: e–g=50 µm, h–k=20 µm, l, m=10 µm.
8Song L et al
(9.0–) 11.9–20.7 (–23.1) × (8.1–) 8.9–12.8 (–15.4) µm, (x= 16.3 × 10.8 µm, n = 20)
(Fig. 2).
Material: ex-type living culture, MFLUCC 20-0110.
Etymology
Refers to the genus name Paphiopedilum.
Analysis
Phylogenetic analyses
The final alignment consists of the new species and the fungus obtained from the diseased
leaves after use of the new species to infect the heathy Paphiopedilum and other genera of
the families Nectriaceae. Additionally, the alignment of combined cmdA, his3, ITS, LSU,
tef1 and tub2 sequence data comprised a total of 3877 characters with gaps (734bp for
cmdA, 529bp for his3, 616bp for ITS, 840bp for LSU, 548bp for tef1 and 610bp for tub2).
Figure 3.
The RAxML tree, based on analysis of cmdA, his3, ITS, LSU, tef1 and tub2 sequences data.
Bootstrap support values for ML and Bayesian greater than 75% and 0.95 were given near
nodes, respectively. The tree was rooted with Campylocarpon fasciculare and Campylocarpon
pseudofasciculare. The new isolate are shown in bold.
Curvicladiella paphiopedili sp. nov. (Hypocreales, Nectriaceae), a new ... 9
The dataset comprised 39 taxa with Campylocarpon fasciculare and C. pseudofasciculare
as the outgroup taxa. The best scoring RAxML tree is shown in Fig. 3, with the Bayesian
tree (not shown) having a similar topology with the ML tree. Curvicladiella paphiopedili was
clustered as sister taxon to C. cignea within Nectriaceae with high support (99/1.00)
(Fig. 3).
Discussion
Morphologically, Curvicladiella paphiopedili is similar to species in Calonectria,
Cylindrocladium and Xenocylindrocladium, but distinct in having ellipsoidal or
sphaeropedunculate chlamydospores (Fig. 2k), dull, tapering towards the apex (Fig. 1d
and e, Fig. 2e–g) and curved extension stipes (Fig. 1f and g), without obpyriform, ovoid,
ellipsoidal or sphaeropedunculate vesicles (Lombard et al. 2010a, Pham et al. 2019) or
coiled stipes (Decock et al. 1997). The morphology of Curvicladiella paphiopedili is
different from the type species Curvicladiella cignea in the size of stipe extensions and
conidia, without the swollen cell below the apical septum; on the other hand, the stipe
extensions of Curvicladiella cignea is curved obviously, while Curvicladiella paphiopedili is
not. The stipe extensions of Curvicladiella paphiopedili are 128.5–549.9 µm long, the
Curvicladiella cignea is 110-200 µm long. The conidia of Curvicladiella paphiopedili are
(38.5–) 45.2–56.6 (–63.2) × (2.2–) 2.9–4.2 (–4.9) µm, the Curvicladiella cignea are (28–)
33–36 (–38) × 2.5–3µm. In the phylogenetic analyses, the two taxa of Curvicladiella formed
a well-supported monoclade and Curvicladiella aphiopedili represented a distinct lineage
(Fig. 3).
Acknowledgements
This research is supported by the following projects: National Natural Science Foundation
of China (31660011),Guizhou Graduate Research Funding:Taxonomic and
Phylogenetic studies of microfungi from Bamboo in Guizhou (Qianjiaohe YJSCXJH [2019]
022). Lian-chai Song thanks Jing Yang for guiding the experiments and modifing the
articles.
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