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287
Unveiling species diversity within early-diverging fungi from
China III: Six new species and a new record of Gongronella
(Cunninghamellaceae, Mucoromycota)
Yi-Xin Wang1, Heng Zhao2, Yang Jiang1, Xin-Ye Liu1, Meng-Fei Tao1, Xiao-Yong Liu1,3
1 College of Life Sciences, Shandong Normal University, Jinan 250358, China
2 School of Ecology and Nature Conservation, Beijing Forestry University, Beijing 100083, China
3 State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China
Corresponding author: Xiao-Yong Liu (liuxy@sdnu.edu.cn)
Copyright: © Yi-Xin Wang et al.
This is an open access article distributed under
terms of the Creative Commons Attribution
License (Attribution 4.0 International – CC BY 4.0).
Research Article
Abstract
Gongronella had accommodated only two species for more than half a century and as
many as 17 new species have been described in this genus since 2015. However, no
systematic studies were conducted for this genus so far. The distribution, substrate
and morphology of all known species in Gongronella are analysed herein. Meanwhile,
with the support of phylogenetic and morphological evidence, six new species (G. abor-
tosporangia sp. nov., G. apophysata sp. nov., G. bawanglingensis sp. nov., G. inconstans
sp. nov., G. pingtangensis sp. nov. and G. reniformis sp. nov.) are proposed and G. pam-
philae
using ITS+LSU+TEF+ACT+RPB1 and the results were basically the same as ITS+LSU.
All species of Gongronella, except G. namwonensis from fresh water, were isolated from
soil. The genus is distributed worldwide, mainly in tropical and subtropical regions.
A synoptic key is provided for a total of 24 species (18 species previously published and
six species newly described herein), except for G. banzhaoae due to unavailable proto-
logue, type and living culture. No morphologies were described when G. pamphilae was
proposed. Thanks to the strains isolated in this study, G. pamphilae is included in the key
phylogeny of the genus Gongronella.
Key words: Mucoromycota, molecular phylogeny, new taxa, soil-borne fungi, taxonomy
Introduction
The genus Gongronella Ribaldi has a great potential in biological applications
due to the ability of producing bioactive substance such as chitosan (Wang et al.
2008; Zhou et al. 2008), dissolving phosphate and degrading metalaxyl (Doilom
et al. 2020; Martins et al. 2020). Gongronella sp. w5, a well-known strain in this
genus, can induce fungi Panus rudis (Wei et al. 2010) and Coprinopsis cinerea
(Pan et al. 2014; Hu et al. 2019; Liu et al. 2022) to produce laccase, secrete organ-
ic acids for improving the acquisition of phosphate in plants and thus promote
their growth (Dong et al. 2018; Wang et al. 2021) and synthesise various bioactive
Academic editor: Thorsten Lumbsch
Received:
22 June 2024
Accepted:
4 November 2024
Published:
20 November 2024
Citation: Wang Y-X, Zhao H, Jiang
Y, Liu X-Y, Tao M-F, Liu X-Y (2024)
Unveiling species diversity within
early-diverging fungi from China III:
Six new species and a new record of
Gongronella (Cunninghamellaceae,
Mucoromycota). MycoKeys 110:
287–317. https://doi.org/10.3897/
mycokeys.110.130260
MycoKeys 110: 287–317 (2024)
DOI: 10.3897/mycokeys.110.130260
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MycoKeys 110: 287–317 (2024), DOI: 10.3897/mycokeys.110.130260
Yi-Xin Wang et al.: Unveiling species diversity within early-diverging fungi from China III
Gongronella urceo-
lifera Ribaldi (Ribaldi 1952). It belongs to Mucoromycota Doweld, Mucoro-
mycetes Doweld, Mucorales Dumort, Cunninghamellaceae Naumov ex R.K.
Benj. (Tedersoo et al. 2018). Before 2015, the taxonomy of Gongronella was
stagnant, accommodating only two species G. urceolifera (= G. butleri) and
G. lacrispora. Since 2015, as many as 17 species have been described suc-
cessively (Hesseltine and Ellis 1961; Adamcik et al. 2015; Ariyawansa et al.
2015; Li et al. 2016; Tibpromma et al. 2017; Dong et al. 2019; Zhang et al.
2019; Crous et al. 2020; de Freitas et al. 2020; Doilom et al. 2020; Martins et
al. 2020; Wang et al. 2023a; Zhao et al. 2023). At present, Gongronella con-
tains 19 species, nearly half of which were initially found from China (Table
1). In the GlobalFungi database, there are a total of 3,039 sample records for
the genus Gongronella covering Asia (1,566, 51.53%), North America (571,
18.79%), Europe (433, 14.58%), South America (261, 8.59%), Africa (123,
4.05%), Australia (64, 2.11%) and Atlantic Ocean (1, 0.03%) (https://globalfun-
gi.com/, accessed on 18 October 2024). Considering geographical climate,
most samples were collected from tropical and subtropical regions (https://
globalfungi.com/, accessed on 17 October 2024). In conclusion, the species
of Gongronella were distributed worldwide and mainly concentrated in tropi-
cal and subtropical regions in Asia.
Regarding substrate of nomenclatural types within the genus Gongronel-
la, G. namwonensis was isolated from fresh water and the other 18 species
were all isolated from soil (Crous et al. 2020; Doilom et al. 2020). According
to the GlobalFungi database, substrates include soil (1852, 60.94%), topsoil
(475, 15.63%), root (403, 13.26%), rhizosphere soil (204, 6.71%), root + rhi-
zosphere soil (52, 1.71%), litter (22, 0.72%), sediment (10, 0.33%), shoot (9,
0.3%) and deadwood (7, 0.23%), (https://globalfungi.com/, accessed on 19
October 2024). Although the GlobalFungi database showed more kinds of
substrates of Gongronella, most strains were still isolated from a variety of
soil samples.
In this study, 14 strains of the genus Gongronella were isolated from soil
in Hainan, Yunnan, Sichuan and Guizhou Provinces from China. According
to ITS+LSU+TEF+RPB1 molecular phylogenetic analyses and morphological
described species of Gongronella was reviewed and compared.
Table 1. The origin of taxonomic types in Gongronella.
Countries Type numbers Percentage (%)
China 9 47.4
Korea 3 15.8
Brazil 3 15.8
Australia 2 10.5
Portugal 1 5.3
UK 1 5.3
Note: These data are from the Index Fungorum (http://www.indexfungorum.org/, accessed on 9 December 2023)
and Wang et al. (2023).
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MycoKeys 110: 287–317 (2024), DOI: 10.3897/mycokeys.110.130260
Yi-Xin Wang et al.: Unveiling species diversity within early-diverging fungi from China III
Materials and methods
Isolation and morphology
Soil samples were collected in Hainan Province (April 2023 and October 2023),
Sichuan Province (June 2023) and Guizhou Province (August 2023). Strains
were isolated from the soil samples by a combination of soil dilution and single
spore isolation.
About 1 g soil sample was mixed with 10 ml sterile water to prepare 10-1
soil suspension. One millilitre of 10-1 suspension was transferred to 9 ml of
sterile water to obtain a 10-2 soil suspension. In the same way, 10-3 and 10-4
-3 and 10-4 soil suspensions (200 ml)
were pipetted on the surface of Rose-Bengal Chloramphenicol Agar (RBC: pep-
tone 5.00 g/l, glucose 10.00 g/l, KH2PO4 1.00 g/l, MgSO4·7H2O 0.50 g/l, rose red
0.05 g/l, chloramphenicol 0.10 g/l, agar 15.00 g/l) (Corry et al. 1995), dispersed
evenly with sterilised coating rods and cultured at 25 °C in the dark for 2–5
days. Upon colonies were visible, they were transferred onto Potato Dextrose
Agar (PDA: glucose 20.00 g/l, potato 200.00 g/l, agar 20.00 g/l, pH 7). When
sporangia were produced, sporangiospores were suspended with sterile water
and streaked with a sterilised inoculation ring. The plates were cultured at 25 °C
in darkness and single spore colonies were transferred on to a new PDA plate
for subculturing. To ensure the formation of zygospores, pairing experiments
were carried out by adding 0.1% lecithin to PDA and sealing Petri dishes to
retain moisture. The microscopic morphological characteristics of fungi were
observed with an optical microscope (Olympus BX53) and photographed with
with 10% sterilised glycerine at 4 °C. Each morphological character was statis-
tically calculated from 30 measurements (Zhang et al. 2022). Cultures were de-
posited in the China General Microbiological Culture Collection Center, Beijing,
China (CGMCC) and the Shandong Agricultural University Culture Collection,
Taian, China (SAUCC). Specimens were deposited in the Herbarium Mycolog-
icum Academiae Sinicae, Beijing, China (HMAS). Taxonomic information for
the new taxa was registered in the Fungal Name repository (https://nmdc.cn/
fungalnames/).
DNA extraction and amplication
Genomic DNA was extracted from mycelia using the CTAB method and Beaver-
Beads Plant DNA Kit (Cat. No.: 70409-20; BEAVER Biomedical Engineering Co.,
Ltd.) (Doyle et al. 1990; Guo et al. 2000; Wang et al. 2023b). ITS, LSU, TEF, ACT
LR7, EF1-728F/EF1-986R, ACT-512F/ACT-783R and RPB1-Af/RPB1-Cr primer
® Plus PCR Master Mix (Yeasen Biotech-
distilled deionised water. Molecular loci, PCR primers and programmes used in
this study are listed in Table 2. The PCR products were electrophoresed with 1%
agarose gel. The DNA fragments were stained with GelRed and observed under
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MycoKeys 110: 287–317 (2024), DOI: 10.3897/mycokeys.110.130260
Yi-Xin Wang et al.: Unveiling species diversity within early-diverging fungi from China III
ultraviolet light. Then a gel extraction kit (Cat# AE0101-C; Shandong Sparkiade
Biotechnology Co., Ltd.) was used for gel recovery. Sanger sequencing was car-
ried out by Biosune Company Limited (Shanghai, China). Consensus sequences
were assembled using MEGA v.7.0 (Kumar et al. 2016). All sequences generated
in this study were deposited at GenBank under the accession numbers in Table 3.
Relative sequences were obtained by BLAST search in the GenBank nucleo-
tide database of NCBI website (Kumar et al. 2016). Sequences both generated
herein and retrieved from GenBank (Table 3) were aligned using MAFFT 7 on-
line service (http://mafft.cbrc.jp/alignment/server/, 20 October 2023) (Katoh et
al. 2019). The ITS, LSU, TEF, ACT and RPB1 sequences were analysed individ-
ually and jointly. The optimal evolutionary model for each partition was deter-
mined and included in the analysis using MrModelTest v.2.3 (Nylander 2004).
Phylogenetic history was reconstructed using Maximum Likelihood (ML) algo-
rithm with RaxML-HPC2 on XSEDE 8.2.12 (Stamatakis 2014; Zhao et al. 2024)
and Bayesian Inference (BI) algorithm with MrBayes 3.2.7a (Huelsenbeck and
Ronquist 2001; Ronquist and Huelsenbeck 2003; Ronquist et al. 2012). ML was
performed for 1,000 bootstrap replicates with the GTRGAMMA model of nucle-
otide evolution. BI was performed using a quick start algorithm with an auto-
matic stop option. The Bayesian analysis consisted of 5,000,000 generations
with four parallel runs with the option of stopping rules and a sampling frequen-
cy of 100 generations. The burn-in score was set to 0.25 and the posterior prob-
ability (PP) was determined from the remaining trees. Initial adjustments of
phylogenetic trees were made using FigTree v.1.4.4 (http://tree.bio.ed.ac) and
https://
adobe.com/products/illustrator).
Results
Phylogenetic analyses
The sequence matrix included 43 strains in 25 species of Gongronella, with
Cunninghamella echinulata CBS 156.28 as outgroup. A total of 4,080 charac-
ters comprised ITS rDNA (1–989), LSU rDNA (990–1967), TEF (1968–2172),
ACT (2173–2948) and RPB1 (2949–4080). Amongst these characters, 2,866
were constant, 562 variable, but parsimony non-informative and 652 parsimony
Table 2. Molecular loci, PCR primers and programmes used in this study.
Loci PCR primers Sequence (5’–3’) PCR cycles References
ITS ITS5 GGA AGT AAA AGT CGT AAC AAG G 95 °C 5 min; (95 °C 30 s, 55 °C 30 s, 72 °C 1 min)
White et al. (1990)
ITS4 TCC TCC GCT TAT TGA TAT GC
LSU LR0R GTA CCC GCT GAA CTT AAG C 95 °C 5 min; (95 °C 50 s, 47 °C 30 s, 72 °C 1.5 min)
Vilgalys and Hester (1990)
LR7 TAC TAC CAC CAA GAT CT
TEF EF1-728F CAT CGA GAA GTT CGA GAA GG
30 cycles; 72 °C 10 min
Carbone and Kohn (1999);
O’Donnell et al. (1998)
EF2 GGA RGT ACC AGT SAT CAT GTT
RPB1 RPB1-Af GAR TGY CCD GGD CAY TTY GG 95 °C 3 min; (94 °C 40 s, 60 °C 40 s, 72 °C 2 min)
37 cycles; 72 °C 10 min
Stiller and Hall (1997)
RPB1-Cr CCN GCD ATN TCR TTR TCC ATR TA
ACT ACT-512F ATG TGC AAG GCC GGT TTC GC 95 °C 3 min; (95 °C 1 min, 55 °C 1 min,
Voigt and Wostemeyer (2000)
ACT-783R TAC GAG TCC TTC TGG CCC AT
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Yi-Xin Wang et al.: Unveiling species diversity within early-diverging fungi from China III
Table 3. Information of strains used in this study.
Species Strains Substrates Countries GenBank accession numbers
ITS LSU ACT TEF RPB1
Gongronella
abortosporangia
CGMCC 3.27028* Soil China PP195847 PP195948 PP933938 PP850088 PP842883
SAUCC 4064-2 Soil China PP195848 PP195949 PP933939 PP850089 PP842882
G. apophysata CGMCC 3.27031* Soil China PP195853 PP195954 PP933947 PP850099PP842878
SAUCC 4846-3 Soil China PP195854 PP195955PP933948 PP850100 PP842877
G. banzhaoae BRIP 75171a* Soil Australia OR271908 OR259049 n.a. n.a. n.a.
G. bawanglingensis CGMCC 3.27033* Soil China PP195857 PP195958 PP933951 PP850103 PP883965
SAUCC 6946-1 Soil China PP195858 PP195959 PP933952 PP850104 PP883964
G. brasiliensis URM 7487* Soil Brazil NR_155148 KY114932 n.a. n.a. n.a.
URM 7488 Soil Brazil KY114931 KY114933 n.a. n.a. n.a.
G. butleri CBS 216.58* Soil UK JN206285 MH869292 n.a. n.a. n.a.
G. chlamydospora CGMCC 3.16118* Soil China OL678157 n.a. n.a. n.a. PP898292
G. eborensis MUM 10.262* Soil Portugal KT809408 MN947301 n.a. n.a. n.a.
MUM 10.263 Soil Portugal GU244500 MN947302 n.a. n.a. n.a.
G. guangdongensis CGMCC 2.15212* Soil China NR_158464 MN947303 n.a. n.a. n.a.
CGMCC 2.15213 Soil China KC462740 MN947304 n.a. n.a. n.a.
G. hydei KUMCC 18.0198* Rhizosphere soil China NR_171964 MT907273 n.a. n.a. n.a.
G. inconstans CGMCC 3.27029* Soil China PP195849 PP195950 PP933941 PP850091 PP842874
SAUCC 4113-3 Soil China PP195850 PP195951 PP933942 PP850092 PP842873
G. koreana EML-TS2Bp* Soil Korea KP636529 KP636530 KP636527 n.a. n.a.
EML-TS2Bp-2 Soil Korea KP835545 KP835542 KP835543 n.a. n.a.
G. lacrispora ATCC 24412* Soil Brazil GU244498 JN206609 n.a. n.a. n.a.
G. multiramosa CGMCC 3.26216* Soil China OR733546 OR733611 PP933937 PP850087 PP842881
SAUCC 4056-4 Soil China OR733545 OR733610 n.a. n.a. n.a.
G. multispora CGMCC 3.16119* Soil China OL678158 n.a. n.a. n.a. pm
G. namwonensis CNUFC WW2-12* Fresh water Korea NR_175640 MN658482 n.a. n.a. n.a.
G. oleae CGMCC 3.26217* Soil China OR742078 OR733608 PP933945 PP850097 PP850080
SAUCC 4164-2 Soil China OR742079 OR733609 PP933946 PP850098 PP850079
G. orasabula EML-QF12-1* Soil Korea NR_148087 KT936263 KT936265 n.a. n.a.
EML-QF12-2 Soil Korea KT936270 KT936264 n.a. n.a. n.a.
G. pamphilae BRIP 74936a* Soil Australia OR271909 OR259050 n.a. n.a. n.a.
CGMCC 3.27027 Soil China PP195845 PP195946 PP933935 PP850086 PP850081
SAUCC 4031-2 Soil China PP195846 PP195947 PP933936 PP850085 PP850082
G. pedratalhadensis URM 8182* Soil Brazil MN912512 MN912508 n.a. n.a. n.a.
G. pingtangensis CGMCC 3.27032* Soil China PP195855 PP195956 PP933949 PP850101 PP842880
SAUCC 5676-2 Soil China PP195856 PP195957 PP933950 PP850102 PP842879
G. qichaensis CGMCC 3.26218* Soil China OR733544 OR733607 n.a. PP850093 PP850084
SAUCC 4137-3 Soil China OR733543 OR733606 n.a. PP850094 PP850083
G. reniformis CGMCC 3.27030* Soil China PP195851 PP195952 PP933943 PP850095 PP842875
SAUCC 4142-5 Soil China PP195852 PP195953 PP933944 PP850096 PP842876
G. sichuanensis CGMCC 3.19651* Soil China MK813373 MK813855 MK820625 n.a. n.a.
CGMCC 3.19652 Soil China MK813374 MK813856 MK820626 n.a. n.a.
G. zunyiensis CGMCC 3.19899* Soil China MN453856 MN453853 n.a. n.a. n.a.
CGMCC 3.19900 Soil China MN453857 MN453854 n.a. n.a. n.a.
Cunninghamella
echinulata
CBS 156.28* n.a. n.a. JN205895 MH877699 n.a. n.a. n.a.
Notes: New species established in this study are in bold. Ex-type or ex-holotype strains are labelled with a star mark “*”. The abbreviation “n.a.” stands for
“not available”
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Yi-Xin Wang et al.: Unveiling species diversity within early-diverging fungi from China III
informative characters (Suppl. material 1). MrModelTest suggested that the
Dirichlet fundamental frequency and GTR+I+G evolution pattern for both par-
titions were adopted in Bayesian Inference. The topology of the Bayesian tree
was consistent with that of the ML tree and, therefore, was used as a repre-
sentative to summarise the evolutionary history within the genus Gongronella
(Fig. 1). G. abortosporangia was closely related to G. multiramosa with a high
support (BIPP = 0.95). G. pingtangensis was closely related to G. namwonensis
with a high support (BIPP = 1). G. reniformis was closely related to G. pam-
philae and G. brasiliensis with a high support (MLBV = 75, BIPP = 0.99). The
G. bawanglingensis (MLBV = 100, BIPP = 1) is closely related to G. qichaensis
and G. inconstans. G. inconstans (MLBV = 99, BIPP = 1) is closely related to G.
qichaensis with a high support (BIPP = 0.96). G. apophysata is closely related
to G. zunyiensis.
Taxonomy
Gongronella abortosporangia Yi Xin Wang, H. Zhao & X.Y. Liu, sp. nov.
Fungal Names: FN 571253
Fig. 2
Etymology. The epithet “abortosporangia” (Latin) refers to the abortive sporangia.
Type. • Hainan Province, Lingshui Li Autonomous County, Qixian Yaoc-
hi Yexi Hot Spring (18.70161°N, 109.69318°E), from soil sample, 10 April 2023,
Yi-Xin Wang (holotype HMAS 352726, ex-holotype strain CGMCC 3.27028).
Description. Colonies growing slowly on PDA in darkness at 25 °C, reaching
49.2–52.4 mm in diameter in seven days, white, regular at edge and cottony in the
centre, reversely milky white. Rhizoids hyaline, branched, irregularly shaped, with
oil droplets. Stolons absent. Sporangiophores on aerial mycelia, erect or slightly
smooth, mostly aseptate, sometimes one-septate and rarely two-septate, occa-
sionally containing a line of oil droplets. Sterile (aborted) sporangia abundant,
mainly on the top of short lateral branches of sporangiophores, mostly gourd-
deliquescent-walled, leaving a collar after releasing sporangiospores. Columel-
-
Additional specimen examined. • Hainan Province, Lingshui Li Auton-
omous County, Benhao Town (18.70161°N, 109.69318°E), from soil sample, 10
April 2023, Yi-Xin Wang (living culture SAUCC 4064-2).
GenBank accession numbers. CGMCC 327028 (ITS, PP195847; LSU, PP195948;
TEF, PP850088; ACT, PP933938; RPB1, PP842883), SAUCC 4064-2 (ITS, PP195848;
LSU, PP195949; TEF, PP850089; ACT, PP933939; RPB1, PP842882).
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Yi-Xin Wang et al.: Unveiling species diversity within early-diverging fungi from China III
Notes. Based on phylogenetic analyses of ITS+LSU+TEF+ACT+RPB1 sequenc-
es, the two isolates of the new species Gongronella abortosporangia formed an in-
dependent clade with high supports (MLBV = 100; Fig. 1), which is closely related
to G. multiramosa (BIPP = 0.95; Fig. 1). This new species differs morphologically
Figure 1. A Maximum Likelihood (ML) phylogenetic consensus tree inferred from DNA sequences of ITS, LSU, TEF, ACT
and RPB1, showing relationships amongst species of Gongronella with Cunninghamella echinulata CBS 156.28 as out-
group. The Maximum Likelihood bootstrap value (MLBV) and Bayesian Inference posterior probability (BIPP) are suc-
cessively shown at the nodes and separated by a slash “/”. Strains marked with a star “*” are ex-types or ex-holotypes.
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Yi-Xin Wang et al.: Unveiling species diversity within early-diverging fungi from China III
from G. multiramosa in sporangium, septum, columella, collar and apophysis
(Wang et al. 2023a). The G. abortosporangia is different from G. multiramosa in
shape and size of sterile sporangia, the former being variously shaped, mostly
Figure 2. Gongronella abortosporangia ex-holotype CGMCC 3.27028 a, b colonies on PDA (a obverse b reverse) c an
unbranched sporangiophore with a mature sporangium d an unbranched sporangiophore with an immature sporangium
e an aborted sporangium with two septa f columellae, collars and apophyses g, h, j branched sporangiophores with
sterile (aborted) sporangia i a branched sporangiophore with a mature sporangium, columellae, collars and apophyses
k rhizoids l, m giant cells nc–n).
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Yi-Xin Wang et al.: Unveiling species diversity within early-diverging fungi from China III
G. abor-
tosporangia has a smaller minimum diameter than G. multiramosa
G. abortosporangia has more septa on sporangiophores compared to
G. multiramosa (0–2 vs. 0–1). Although G. abortosporangia is similar in shape of
columellae to G. multiramosa
G. abortospo-
rangia has shorter collars than G. multiramosa
G. abortosporangia is similar in shape of apophyses to G. multiramosa. However,
they are different from each other in main pattern and size: The former mostly
-
two isolates as a new species G. abortosporangia allied to G. multiramosa.
Gongronella apophysata Yi Xin Wang, H. Zhao & X.Y. Liu, sp. nov.
Fungal Names: FN 571631
Fig. 3
Etymology. The epithet “apophysata” (Latin) refers to various shapes of apophyses.
Type. • Sichuan Province, Emeishan City, Leshan City, Ehong Road,
near the Xu family residence (29.59211°N, 103.37776°E), from soil sample, 25
June 2023, Yi-Xin Wang (holotype HMAS 352728, ex-holotype strain CGMCC
3.27031).
Description. Colonies growing slowly on PDA in darkness at 25 °C, reaching
35.8–42.4 mm in diameter in seven days, white, irregular at edge and cottony in
the centrr, reversely milky white. Rhizoids hyaline, branched, irregularly shaped.
Stolons absent. Sporangiophores on aerial mycelia, erect or slightly curved,
-
line, smooth, mostly aseptate or one-septate, occasionally two-septate. Sterile
(aborted) sporangia predominantly on the top of short lateral branches of spo-
-
yses hyaline, smooth, variously shaped, mostly ellipsoidal to olive-shaped,
-
Additional specimen examined. • Sichuan Province, Emeishan City, Le-
shan City, Ehong Road, near the Xu family residence (29.59211°N, 103.37776°E),
from soil sample, 25 June 2023, Yi-Xin Wang (living culture SAUCC 4846-3).
GenBank accession numbers. CGMCC 3.27031 (ITS, PP195853; LSU,
PP195954; TEF, PP850099; ACT, PP933947; RPB1, PP842878), SAUCC 4846-3 (ITS,
PP195854; LSU, PP195956; TEF, PP850100; ACT, PP933948; RPB1, PP842877).
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Yi-Xin Wang et al.: Unveiling species diversity within early-diverging fungi from China III
Notes. Based on phylogenetic analyses of ITS+LSU+TEF+ACT+RPB1 se-
quences, the two isolates of the new species Gongronella apophysata form
an independent clade with high support (MLBV = 98; Fig. 1), which is closely
related to G. zunyiensis. In ITS, G. apophysata differs from the type species
of G. zunyiensis by 13 base pairs. This new species differs morphologically
Figure 3. Gongronella apophysata ex-holotype CGMCC 3.27031 a, b colonies on PDA (a obverse b reverse) c an un-
branched sporangiophore with a fertile sporangium d an unbranched sporangiophore with an immature sporangium
e–g columellae, collars, apophyses and septa h branched sporangiophores with columellae, collars and apophyses
i branched sporangiophores with columellae, collars and apophyses j–l chlamydospores m giant cells n, o rhizoids p
c–p).
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from G. zunyiensis in sporangium, columellae, apophyses and chlamydospore
(Dong et al. 2019). G. apophysata has larger sporangia than G. zunyiensis
G. apophysata differs from G. zunyiensis
in the shape of columellae, the former being elliptic and the latter being hemi-
spherical and globose. As for apophyses, G. apophysata and G. zunyiensis are
remarkably different in shape and size, the former variously shaped, mostly
-
G. apophysata is remarkably different from
G. zunyiensis in shape and size of chlamydospores, the former being not uni-
-
species G. apophysata allied to G. zunyiensis.
Gongronella bawanglingensis Yi Xin Wang, H. Zhao & X.Y. Liu, sp. nov.
Fungal Names: FN 571903
Fig. 4
Etymology. The epithet “bawanglingensis” (Latin) refers to the location where
the type was collected, Bawangling National Forest Park.
Type. • Hainan Province, Changjiang Li Autonomous County, Bawan-
gling National Forest Park (19.08593°N, 109.12275°E), from soil sample,
14 October 2023, Yi-Xin Wang (holotype HMAS 352730, ex-holotype strain
CGMCC 3.27033).
Description. Colonies growing slowly on PDA in darkness at 25 °C, reaching
45.6–48.8 mm in diameter in seven days, white, cottony in the centre, on the
reverse milky white. Rhizoids hyaline, branched, irregularly shaped. Stolons ab-
sent. Sporangiophores on aerial mycelia, erect or slightly curved, unbranched
hyaline, smooth, mostly aseptate or one-septate, no more than four-septate.
Sterile (aborted) sporangia mainly on the top of short lateral branches of spo-
rangiophores, mostly gourd-shaped. Fertile sporangia hyaline or light yellow,
a collar after releasing sporangiospores. Columellae mostly hemispherical,
-
-
-
casionally gourd-shaped. Sporangiospores not uniform, hyaline, smooth, most-
-
Additional specimen examined. • Hainan Province, Changjiang Li Au-
tonomous County, Bawangling National Forest Park (19.08593°N, 109.12275°E),
from soil sample, 14 October 2023, Yi-Xin Wang (living culture SAUCC 6946-1).
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GenBank accession numbers. CGMCC 3.27033 (ITS, PP195857; LSU, PP195958;
TEF, PP50103; ACT, PP933951; RPB1, PP883965), and SAUCC 6946-1 (ITS,
PP1195858; LSU, PP195959; TEF, PP850104; ACT, PP933952; RPB1, PP883964).
Notes. Based on phylogenetic analyses of ITS+LSU+TEF+ACT+RPB1 sequenc-
es, the two isolates of the new species Gongronella bawanglingensis form an in-
dependent clade with full support (MLBV = 100, BIPP = 1; Fig. 1), which is closely
Figure 4. Gongronella bawanglingensis ex-holotype CGMCC 3.27033 a, b colonies on PDA (a obverse b reverse) c, d an un-
branched sporangiophore with a fertile sporangium e branched sporangiophores with sterile (aborted) sporangia f branched
sporangiophores with immature sporangia g–i columellae, collars, apophyses and septa j, k branched sporangiophores with
columellae, collars and apophyses l, m chlamydospores n giant cells o rhizoids pc–p).
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related to G. inconstans and G. qichaensis. In ITS, G. bawanglingensis differs from
G. inconstans by 21 base pairs. This new species differs morphologically from
G. inconstans in columella, apophysis, colour and sporangiospore. G. bawan-
glingensis and G. inconstans are similar in the dominant shape of columellae, but
apophyses, G. bawanglingensis and G. inconstans are remarkably different from
G. incon-
stans are more distinct than G. bawanglingensis
for sporangiospores, G. bawanglingensis and G. inconstans are similar in dominant
Additionally, the G. inconstans has more shapes, except ovoid and reniform. In ITS,
G. bawanglingensis differs from G. qichaensis by 28 base pairs. This new species
differs morphologically from G. qichaensis in sporangium, columellae and apoph-
ysis (Wang et al. 2023a). The G. bawanglingensis has evidently smaller sporangia
than G. qichaensis
the two species have evident differences in shape. Combining morphological and
species G. bawanglingensis allied to G. inconstans and G. qichaensis.
Gongronella inconstans Yi Xin Wang, H. Zhao & X.Y. Liu, sp. nov.
Fungal Names: FN 571905
Fig. 5
Etymology. The epithet “inconstans” (Latin) refers to the inconstant shape of
apophyses.
Type. • Hainan Province, Lingshui Li Autonomous County (18.69850°N,
109.88098°E), from soil sample, 7 Apr 72023, Yi-Xin Wang (holotype HMAS
352731, ex-holotype strain CGMCC 3.27029).
Description. Colonies growing slowly on PDA in darkness at 25 °C, reaching
31.2–36.8 mm in diameter in seven days, white, regular at edge and cottony,
reversely milky white. Rhizoids hyaline, branched, irregular, ubiquitous. Stolons
absent. Sporangiophores on aerial mycelia, erect or slightly curved, unbranched
diameter, smooth and deliquescent-walled, leaving a collar after releasing
-
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Additional specimen examined. • Hainan Province, Lingshui Li Auton-
omous County (18.69850°N, 109.88098°E), from soil sample, 7 April 2023, Yi-
Xin Wang (living culture SAUCC 4113-1).
GenBank accession numbers. CGMCC 3.27029 (ITS, PP1955849; LSU,
PP195950; TEF, PP850091; ACT, PP933941; RPB1, PP842874), and SAUCC 4113-1
(ITS, PP105850; LSU, PP195951; TEF, PP850092, ACT, PP933942; RPB1, PP842873).
Figure 5. Gongronella inconstans ex-holotype CGMCC 3.27029 a, b colonies on PDA (a obverse b reverse) c, d an un-
branched sporangiophore with a fertile sporangium e an unbranched sporangiophore with a premature sporangium
f branched sporangiophores with aborted sporangia g–i columellae, collars, apophyses j–l branched sporangiophores
with fertile sporangia, columellae, collars and apophyses n fertile sporangium with protuberance o, p chlamydospores
m giant cells q rhizoids rc–r).
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Note. Based on phylogenetic analyses of ITS+LSU+TEF+ACT+RPB1 sequenc-
es, the two isolates of the new species Gongronella inconstans form an inde-
pendent clade with full support (MLBV = 100, BIPP = 1; Fig. 1), which is closely
related to G. qichaensis with high support (BIPP = 0.96; Fig. 1). In ITS, G. incon-
stans differs from G. qichaensis by 28 base pairs. This new species differs mor-
phologically from G. inconstans in sporangium, columellae and apophysis. As
for sporangium, the G. inconstans is smaller than the G. qichaensis
G. inconstans and G. qichaensis are different in size and
shape of columellae (Wang et al. 2023a). The G. inconstans mostly hemispher-
-
tionally, the columellae of G. qichaensis
G. incon-
stans and G. qichaensis are evidently different in apophysis shape. The former
mostly long fusiform, sometimes oval-shaped and rarely egg shaped. The latter
mostly pear-shaped to oval, partially elliptical or sub-globose. Combining mor-
together as a new species: G. inconstans allied to G. qichaensis.
Gongronella pamphilae Y.P. Tan, Bishop-Hurley & R.G. Shivas
Fungal Names: FN 900776
Fig. 6
Etymology. Named after Pamphilae of Epidaurus (ca. 1st century AD), a histori-
an of Egyptian descent who lived in Greece.
Description. Colonies growing slowly on PDA in darkness at 25 °C, reaching
36.6–44.6 mm in diameter in seven days, white, regular at edge and cottony in
the centre, reversely milky white. Rhizoids hyaline, branched, irregular. Stolons
absent. Sporangiophores on aerial mycelia, erect or slightly curved, unbranched
mostly aseptate, no more than two-septate. Fertile sporangia hyaline or light
leaving a collar after releasing sporangiospores. Columellae mostly hemispher-
-
-
Additional specimen examined. • Hainan Province, Lingshui Li Auton-
omous County, Shizhi Village Road (18.70178°N, 109.83679°E), from soil sam-
ple, 10 April 2023, Yi-Xin Wang (specimen HMAS 352732, living culture CGMCC
3.27027, SAUCC 4031-2).
GenBank accession numbers. CGMCC 3.27027 (ITS, PP195845; LSU, PP195946;
TEF, PP850086; ACT, PP933935; RPB1, PP850081), and SAUCC 4031-2 (ITS,
PP195846; LSU, PP195947; TEF, PP850085; ACT, PP933936; RPB1, PP850082).
Note. Based on phylogenetic analyses of ITS+LSU+TEF+ACT+RPB1 DNA se-
quences, the two isolates of the new record species Gongronella pamphilae form
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an independent clade with full support (MLBV = 100; Fig. 1), which is closely
related to G. pamphilae (MLBV = 100; BI = 1, Fig. 1). In ITS, the two isolates differ
from G. pamphilae by only 2 base pairs. As no morphological descriptions were
provided for the G. pamphilae-
gether as members of G. pamphilae just based on molecular phylogenetic analy-
ses. Consequently, we provide herein a supplemental description for the species.
Figure 6. Gongronella pamphilae ex-living culture CGMCC 3.27027 a, b colonies on PDA (a obverse b reverse) c an un-
branched sporangiophore with a fertile sporangium d an unbranched sporangiophore with an aborted sporangium e, f an
unbranched sporangiophore with columellae, apophyses and collars g, h branched sporangiophores with columellae,
collars, apophyses i Rhizoids j, k giant cells lc–l).
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Gongronella pingtangensis Yi Xin Wang, H. Zhao & X.Y. Liu, sp. nov.
Fungal Names: FN 571904
Fig. 7
Etymology. The epithet “pingtangensis” (Latin) refers to the location where the
type was collected, Pingtang County.
Type. • Qiannan Buyi and Miao Autonomous Prefecture, Pingtang Coun-
ty, Kapu Maonan Town (25.79510°N, 107.38631°E), from soil sample, 7 August 7
2023, Yi-Xin Wang (holotype HMAS 352732, ex-holotype strain CGMCC 3.27032).
Description. Colonies growing slowly on PDA in darkness at 25 °C, reaching
38.8–45.6 mm in diameter in seven days, white, cottony, in reverse milky white.
Rhizoids hyaline, branched, irregular. Stolons absent. Sporangiophores on ae-
rial mycelia, erect or slightly curved, unbranched, or slightly branched (1–4
aseptate or one-septate. Sterile (aborted) sporangia predominantly on the top
of short lateral branches of sporangiophores. Fertile sporangia hyaline or light
leaving a collar after releasing sporangiospores. Columellae mostly hemispher-
-
-
Additional specimen examined. • Qiannan Buyi and Miao Autonomous
Prefecture, Pingtang County, Kapu Maonan Town (25.79510°N, 107.38631°E),
from soil sample, 7 August 2023, Yi-Xin Wang (living culture SAUCC 5676-2).
GenBank accession numbers. CGMCC 3.27032 (ITS, PP195855; LSU, PP195956;
TEF, PP850101; ACT, PP933949; RPB1, PP842880), and SAUCC 5676-4 (ITS,
PP195856; LSU, PP195957; TEF, PP850102; ACT, PP933950; RPB1, PP842879).
Note. Based on phylogenetic analyses of ITS+LSU+TEF+ACT+RPB1 sequenc-
es, the two isolates of the new species G. pingtangensis form an independent
clade with high support (MLBV = 100, BIPP = 0.84; Fig. 1), which is closely relat-
ed to G. namwonensis with high support (BIPP = 1; Fig. 1). In ITS, G. pingtangen-
sis differs from G. namwonensis by 14 base pairs. This new species differs
morphologically from G. namwonensis in columellae, apophysis and giant cell
(Crous et al. 2020). G. pingtangensis and G. namwonensis greatly differ from
each other in shape of columellae, the former being mostly hemispherical, par-
tially arch-shaped, rarely spherical and the latter being globose, subglobose,
hemispherical, nipple-like and ellipsoidal. As for apophyses, G. pingtangensis
and G. namwonensis obviously differ from each other in shape, the former be-
ing mostly oval, partially bowling pin-shaped, rarely egg-shape and the latter
being subglobose and ellipsoid, sometimes with a truncated base. As for giant
cells, the G. namwonensis varies in shape more than G. pingtangensis. Combin-
isolates together as a new species G. pingtangensis allied to G. namwonensis.
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Gongronella reniformis Yi Xin Wang, H. Zhao & X.Y. Liu, sp. nov.
Fungal Names: FN 571630
Fig. 8
Etymology. The epithet “reniformis “ (Latin) refers to the reniform sporangiospores.
Type. • Hainan Province, Changjiang Li Autonomous County, Qicha
Town (19.11750°N, 109.15000°E), from soil sample, 11 April 2023, Yi-Xin Wang
(holotype HMAS 352727, ex-holotype strain CGMCC 3.27030).
Figure 7. Gongronella pingtangensis ex-holotype CGMCC 3.27032 a, b colonies on PDA (a obverse b reverse) c, d an un-
branched sporangiophore with a fertile sporangium e–g columellae, collars, apophyses and septa h–j branched sporan-
giophores with fertile sporangia, columellae, collars, apophyses and septa k giant cells i–n rhizoids o sporangiospores.
c–o).
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Description. Colonies on PDA in darkness at 25 °C growing slowly, reaching
39.4–41.8 mm in diameter in seven days, white, regular at edge and cottony in
the centre, on reverse milky white. Rhizoids hyaline, branched, irregular, some-
times with giant cells in the terminal. Stolons absent. Sporangiophores on aerial
mycelia, erect or slightly curved, unbranched or slightly branched (1–3 times),
than two-septate. Sterile (aborted) sporangia predominantly on the top of short
smooth and deliquescent-walled, leaving a collar after releasing sporangio-
-
Zygospores not found.
Additional specimen examined. • Hainan Province, Changjiang Li Au-
tonomous County, Qicha Town (19.11750°N, 109.15000°E), from soil sample,
11 April 2023, Yi-Xin Wang (living culture SAUCC 4142-5).
GenBank accession numbers. CGMCC 3.27030 (ITS, PP195851; LSU,
PP195952; TEF, PP850095; ACT, PP933943; RPB1, PP84875), SAUCC 4142-5 (ITS,
PP195852; LSU, PP195953; TEF, PP850096; ACT, PP933944; RPB1, PP842876).
Notes. Based on phylogenetic analyses of ITS+LSU+TEF+ACT+RPB1 se-
quences, the two isolates of the new species Gongronella reniformis form an in-
dependent clade with full support (MLBV = 100, BIPP = 1; Fig. 1), which is close
to G. pamphilae and G. brasiliensis with a high support (MLBV = 89, BIPP = 1;
Fig. 1). Comparing ITS sequences showed that G. reniformis is relatively close-
ly related to G. pamphilae (44 bp of dissimilarity) and G. brasiliensis (40 bp of
dissimilarity). There were no morphological descriptions of G. pamphilae in its
protologue, so the morphological comparison was made between G. reniformis
and the G. pamphilae
morphologically from G. pamphilae in sporangium, columellae, apophysis, spor-
angiospore. The sporangium of G. reniformis is smaller than that of G. pamphilae
G. reniformis and G. pamphilae are different
from each other mainly in shape and size of columellae, the former being mostly
G. reniformis and G. pamphilae are differ-
ent from each other in dominant shape and size of apophyses, the former being
G. reniformis are smaller than those of G. pamphi-
lae
from G. brasiliensis in sporangiophore, columellae and giant cells (Tibpromma et
al. 2017). In sporangiophores, the G. renformis differs from the G. brasiliensis in
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the G. renformis and G. brasiliensis are different in shape. The former mostly el-
liptic, sometimes sub-hemispherical. The latter globose, subglobose and coni-
cal-cylindrical. The G. renformis is evidently smaller than G. brasiliensis in giant
-
G. reniformis.
Figure 8. Gongronella reniformis ex-holotype CGMCC 3.27030 a, b colonies on PDA (a obverse b reverse) c an unbranched
sporangiophore with a fertile sporangium d an unbranched sporangiophore with an immature sporangium e, f columel-
lae, collars and apophyses g branched sporangiophores with shedding sporangia, columellae, collars, apophyses and
septa h branched sporangiophores with fertile sporangia and sterile (aborted) sporangia i giant cells j chlamydospore
k rhizoids lc–l).
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Morphological comparisons and key to the species of Gongronella
Together with the six new species proposed in this study, a total of 25 species
of Gongronella have been described worldwide. Except G. banzhaoae, morpho-
logical comparisons were made amongst 18 species published before and six
species newly proposed in this study (Table 4). We provide herein a synoptic key
for these species. Characteristics adopted in the key include colonies, sporan-
giophores, sporangia, columellae, apophyses, sporangiospores and giant cells.
1 Giant cells known ..........................................................................................2
– Giant cells unknown ....................................................................................15
2 Aborted sporangia known .............................................................................3
– Aborted sporangia unknown ............................................................ G. hydei
.............................................................4
...........................................................10
4 Sporangiospores mainly not reniform .........................................................5
– Sporangiospores mainly reniform ................................................................7
5 Columellae mainly ellipsoidal .................................................. G. qichaensis
– Columellae mainly not ellipsoidal ................................................................6
.........................................G. pingtangensis
...............................................G. lacrispora
......................................................................8
....................................................................10
................................ G. namwonensis
– Sporangiophores branched < 3 times ..........................................................9
.....G. brasiliensis
...... G. pamphilae
................ G. reniformis
.............. G. apophysata
11 Sporangiophores branched > 3 times ........................................................12
........................................................14
........................................................................13
........................................... G. abortosporangia
.....G. oleae
..... G. multiramosa
14 Apophyses oval, subglobose and gourd-shaped.......... G. bawanglingensis
– Apophyses long fusiform, oval and egg-shaped .................... G. inconstans
...........................................................16
...........................................................17
............G. pedratalhadensis
......................
............................................................................................... G. sichuanensis
17 Columellae hemispherical ..........................................................................18
– Columellae not hemispherical ....................................................................19
................
............................................................................................G. chlamydospora
...........................................G. butleri
.................................................................20
..................................................................21
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..... G. eborensis
... G. multispora
........................22
...............................23
....
..........................................................................................G. guangdongensis
...................
....................................................................................................G. zunyiensis
...................................G. orasabula
......................................G. koreana
Discussion
Southern China is located in tropical and subtropical areas, which belong to trop-
ical monsoon climate and subtropical monsoon climate. All the samples used in
this study were collected from these areas, including Hainan, Sichuan, Yunnan
and Guizhou Provinces. This is consistent with the geographical distribution of
the species of Gongronella, mainly inhabiting tropical and subtropical regions.
The genus Gongronella was established in 1952 and its type Gongronella ur-
ceolifera was synonymised with Gongronella butleri whose basionym is Absidia
butleri (Ribaldi 1952). Numbers of this genus have increased rapidly recently, with
as many as 17 species being described between 2015 and 2024 and the genus
currently has a total of 25 members including the six new species proposed here-
in, all of which are listed in Table 3. However, there are no systematic analyses of
the morphological characteristics of the species of Gongronella. In this study, the
morphological characteristics of the 24 species of Gongronella were compara-
tively analysed (Table 4), except G. banzhaoae. Since G. banzhaoae only has mo-
lecular data and no morphological description, it is not compared in this study.
Since 2019, phylogenetic analyses of Gongronella have mainly been con-
ducted on the basis of morphological characteristics and ITS+LSU sequence
(Zhang et al. 2019). In this study, new TEF, ACT and RPB1 protein-coding se-
quences were added for the construction of phylogenetic trees and the results
were basically consistent with previous studies based on ITS+LSU. Twelve
strains were grouped into six individual clades and two strains were grouped
along with G. pamphilae. Compared with G. multiramosa, G. abortosporangia
has more abundant and various aborted sporangia, smaller fertile sporangia
and smaller columellae (Wang et al. 2023a). Compared with G. pamphilae, G.
reniformis has smaller sporangia and sporangiospores, as well as different
shapes of columellae and apophyses. Compared with G. brasiliensis, G. reni-
formis has smaller sporangiophores, different columella shapes and smaller gi-
ant cells (Tibpromma et al. 2017). Compared with G. zunyiensis, G. apophysata
has larger sporangia, as well as different shapes of columellae, apophyses and
chlamydospores (Dong et al. 2019). Compared with G. inconstans, G. bawan-
glingensis has smaller sporangiospores, larger columellae, different shapes
and sizes of apophyses. Compared with G. qichaensis, the G. bawanglingen-
sis has smaller sporangia, different columellae and apophysis shapes (Wang
et al. 2023a). G. pingtangensis and G. namwonensis are different in size and
shape of columellae (hemispherical vs. globose) and apophyses (oval vs. sub-
globose). G. namwonensis has more shapes of giant cells (Crous et al. 2020).
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Table 4. Morphological comparisons of Gongronella species.
Species Colonies Sporangiophores Sporangia Columellae Apophyses Sporangiospores Giant cell Reference
G. abortosporangia PDA: dark 25 °C 7 d
24.6–26.2 mm diam.,
white, regular at edge
and cottony in the
centre, in reverse milky
white
unbranched or branched
partially 1-septate, rarely
2-septate, occasionally
containing a line of oil
droplets
Aborted: mostly gourd-
elliptical with slight
6.7–10.6, occasionally
mostly hemispherical,
hemispherical, 1.3–3.9
mostly cup-shaped, 1.9–8.6
intercalary, globular,
subglobular, 2.6–4.6
This study
G. apophysata PDA: dark 25 °C 7 d
17.9–21.2 mm in diam.,
white, irregular at edge
and cottony in centre, in
reverse milky white
unbranched or branched
or 1-septate, occasionally
2-septate
Aborted: gourd-shape,
spherical, 12.5–
hemispherical, 1.4–2.7
mostly ellipsoidal to olivary,
partially subglobose,
occasionally gourd-shaped,
mostly reniform, 3.2–5.5
intercalary, globular,
This study
G. bawanglingensis PDA: dark 25 °C 7 d
22.8–24.4 mm diam.,
white, cottony in centre,
in reverse milky white
unbranched or sympodially
branched 1–3 times,
aseptate or 1-septate,
occasionally up to 4-septate
Aborted: mostly
gourd-shaped; Fertile:
diam.
mostly hemispherical,
some arch-shaped,
shaped
intercalary, globular,
This study
G. brasiliensis MEA: 25 °C 7 d 1.0–2.0
mm high 60.0 mm
diam., white, cottony,
irregular at edge,
reverse cream to buff
solitary, arising from stolons
or in whorls of two, often
with a single branch, 1- or
2-septate below apophyses
Aborted: globose, 5.0–
globose, subglobose,
globose, subglobose,
(3.0–)4.0–8.0(–9.0)
some very small, up to
globose, (3.0–)4.0–5.0(–6.0)
globose, subglobose,
ovoid, some hypha-like,
irregularly swollen, up
Tibpromma
et al. (2017)
G. butleri White turf simply or irregularly
always 1-septate
Fertile: globose, 16.5–
swollen, oval-shaped, 7.0–10
side to reniform, 2.5–7.2
Ribaldi
(1952), Babu
et al. (2015)
G. chlamydospora PDA: 27 °C 11 d 90.0
grey
unbranched or simply
branched, hyaline, slightly
constricted at top
Fertile: globose, 8.5–
ovoid to depressed
urn-shaped to subglobose,
ellipsoid, reniform
Zhao et al.
(2023)
G. eborensis PDA: 25 °C 5 d 28.0–
32.0 mm diam.
branched, always 1-septate
under apophyses
Fertile: globose to
hemispherical to
globose to subglobose,
reniform to fusiform-
Martins et
al. (2020)
G. guangdongensis PDA: 25 °C 13 d 1–2
mm high, 50.0 mm
diam., white or pale,
irregular at edge; in
reverse buff to honey
irregularly or simply
branched, 28.0–100.0
1-septate
Aborted: sometimes
present; Fertile: always
diam.
hemispherical,
spherical or ovoid, 2.5–
in diam.
diam.
Adamcik et
al. (2015)
310
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Yi-Xin Wang et al.: Unveiling species diversity within early-diverging fungi from China III
Species Colonies Sporangiophores Sporangia Columellae Apophyses Sporangiospores Giant cell Reference
G. hydei PDA: 25 °C 7 d 60.0–
65.0 mm diam., circular,
effuse, dense, white;
unbranched, occasionally
branched, mostly 1-septate
Fertile: globose to
subglobose, 10.5–18.8
hemispherical,
sometimes tiny, 1.7–
cuboid-shaped with truncate
rounded at the base, 2.7–6.2
truncate at the base, 3.7–7.3
globose, guttulate, up
Doilom et al.
(2020)
G. inconstans PDA: dark 25 °C 7 d
15.6–18.4 mm diam.,
white, regular at edge,
cottony, in reverse milky
white
unbranched or branched
mostly aseptate
Aborted: existence;
Fertile: spherical,
mostly hemispherical,
sometimes spherical,
variously shaped, mostly long
occasionally irregular,
intercalary, globular,
This study
G. koreana PDA: 25 °C 7 d 31.5–
33.0 mm diam., light
white with age, reverse
from light-coloured to
white
branched, 1-septate
Fertile: globose,
hemispherical, 1.2–2.3
mostly bean-shaped,
Ariyawansa
et al. (2015)
G. lacrispora 25 °C 13 d 50.0 mm in
diam., 1–3 mm high,
white, then grey or pale
grey, later pale wine
colour
septate
Aborted: sometimes
present; Fertile:
typically perfectly
diam
in diam.
lacrymoid to narrowly
intercalary, globose
to irregular, often with
vacuoles or oil droplets,
Hesseltine
and Ellis
(1961)
G. multiramosa PDA: dark 25 °C 7 d
21.6–25.6 mm diam.,
white, regular at edge,
cottony in centre,
reverse milky white
unbranched or sympodially
branched up to 7 times,
4.7–128.4 × 2.6–3.9
occasionally containing a
line of oil droplets
spherical, 15.5–23.2
mostly hemispherical,
hemispherical, 3.0; –3.9
mostly hemispherical,
partially cup-shaped,4.6–7.0
subspherical, 1.7–2.6
globular, sub-spherical,
Wang et al.
(2023a)
G. multispora PDA: 27 °C 10 d 80.0
mm diam., 10.0 mm
high, from white to
yellowish, in reverse
crusty, yellow
unbranched or sympodially
branched, 2–3 in whorls and
swollen on the base, 1 to
several septate
Fertile: globose, 12.0–
hemispherical, 2.0–4.5
pyriform to subglobose,
ellipsoid, fusiform,
cylindrical, reniform
subglobose to globose
Zhao et al.
(2023)
G. namwonensis MEA:25 °C 7 d 55.0
mm diam. (28 °C 5 d
90.0 mm diam), white,
in reverse cream
simply or sympodially or
monopodially branched, up
wide, in whorls of 2 or 3
times, mostly 1-septate
Aborted: sometimes
formed; Fertile:
diam.
globose, subglobose,
hemispherical,; 1.8–5.5
like, ellipsoidal, 2.0–3.8
globose (2.5–)5.0–9.5(–
and ellipsoid, some with a
reniform, ellipsoidal,
some ovoid, 2.5–3.5
globose, subglobose
and branched
Crous et al.
(2020)
G. oleae PDA: dark 25 °C 7 d,
16.3–17.0 mm diam.,
white, regular at edge,
cottony in centre,
inreverse milky white
unbranched or branched
sometimes 1-septate
diam.; Fertile: spherical,
mostly sub-spherical
hemi-spherical, 0.4–3.3
ovoid, 2.40–3.34
×
reniform, 2.58–4.99 ×
terminal, globular, sub-
diam.
Wang et al.
(2023a)
311
MycoKeys 110: 287–317 (2024), DOI: 10.3897/mycokeys.110.130260
Yi-Xin Wang et al.: Unveiling species diversity within early-diverging fungi from China III
Species Colonies Sporangiophores Sporangia Columellae Apophyses Sporangiospores Giant cell Reference
G. orasabula SMA: 25 °C 5 d, 33.0–
35.0 mm, initial white,
later off-white, irregular
at edge, in reverse
white
simply branched 1–3 times
Fertile: globose
to subglobose or
calabash vase-
hemispherical, 2.0–3.0
globose, subglobose
mostly bean-shaped,
Li et al.
(2016)
G. pamphilae PDA: dark 25 °C 7 d
18.3–22.3 mm in diam.,
white, regular at edge
and cottony in centre, in
reverse milky white
unbranched or branched
1–2 times, 3.7–154.9
aseptate, occasionally 1- or
2-septate
Aborted: existence;
Fertile: spherical, 13.8–
mostly hemispherical,
sometimes arc-shaped,
intercalary, globular,
This study
G. pedratalhadensis PDA: 25 °C 7 d 5.5 mm
high, 45.0 mm diam.,
white, irregular at edge,
in reverse pale
sympodially branched 1–2
sporangia, rarely two or
more septate
Aborted: existence;
Fertile: globose 17.0–
mostly hemispherical,
some short
hemispherical or
vasiform, short or long,
bean-shaped, 2.5–3.5
de Freitas et
al. (2020)
G. pingtangensis PDA: dark 25 °C 7 d
19.4–22.8 mm diam.,
white, cottony, in
reverse milky white
unbranched or sympodially
branched 1–4 times,
or 1-septate
Aborted: existence;
Fertile: spherical, 14.2–
mostly hemispherical,
some arch-shaped,
mostly oval-shaped, 7.1–19.8
mostly ovoid, 2.8–3.9
large irregularly shaped,
intercalary, globular,
This study
G. qichaensis PDA: dark, 25 °C 7 d
20.3–22.7 mm diam.,
white, cottony, regular
at edge, in reverse
milky white
unbranched or branched
1–2 times, 17.3–141.2
aseptate, occasionally
2-septate
Aborted:
diam.; Fertile: spherical,
sub-hemispherical
mostly pear-shaped to
mostly ellipsoidal,
sometimes reniform,
intercalary or terminal,
globular, sub-spherical,
Wang et al.
(2023a)
G. reniformis PDA: dark 25 °C 7 d
19.7–20.9 mm diam.,
white, regular at edge
and cottony in centre in
reverse milky white
unbranched or branched
1–3 times, 3.4–157.9
aseptate, occasionally 1- or
2-septate
Aborted: gourd-shape,
mostly elliptic,
hemispherical, 1.4–2.6
mostly reniform, 2.8–3.5
intercalary, globular,
This study
G. sichuanensis PDA: 25 °C 14 d
4.0–5.0 mm high,
67.0–68.0 mm diam.,
white, regular at edge,
in reverse grey
solitary or simply branched,
or 2-septate
Fertile: globose,
subglobose, 10.5–26.5
hemispherical, 1.5–3.5
ellipsoidal to subglobose,
diam.
reniform, ovoid or
Zhang et al.
(2019)
G. zunyiensis PDA: 25 °C 14 d
3.0–6.0 mm high,
70.0–75.0 mm diam.,
white, villiform, irregular
at edge, in reverse
grey-white
several times, usually
aseptate
Fertile: subglobose to
diam.
hemispherical and
subglobose, reniform,
Dong et al.
(2019)
312
MycoKeys 110: 287–317 (2024), DOI: 10.3897/mycokeys.110.130260
Yi-Xin Wang et al.: Unveiling species diversity within early-diverging fungi from China III
-
ically independent clades, ensure their novelty (Wang et al. 2023a). As for
G. pamphilae, two strains were grouped into an independent separate clade
and there are only two base pairs of difference in ITS rDNA sequences. As no
morphological descriptions were provided for G. pamphilae in its protologue,
G. pamphi-
lae only based on molecular phylogenetic analyses.
In summary, the molecular phylogenetic and morphological results support
namely G. abortosporangia, G. reniformis, G. apophysata, G. bawanglingen-
sis, G. pingtangensis, G. inconstans and two strains as new record species of
G. pamphilae, complementing the morphological description of G. pamphilae.
TFE, ACT and RPB1 protein-coding sequences were newly added to construct
the phylogenetic evolutionary tree and the results were basically consistent
with ITS+LSU results. The morphology of members of the genus Gongronella
was systematically described herein, with a morphological description table
being established for the described strains of Gongronella and the new strains
described in this study (Table 4).
Acknowledgements
We thank Zhao-Xue Zhang (Shandong Agricultural University), Xin-Yi Wang
(Shandong Normal University) and Shu-Bin Liu (Beijing Forestry University) for
soil collection.
Additional information
Conict 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 (Nos.
32170012, 32300011, 32470004), Ji’nan City’s ‘New University 20 Policies’ Initiative
for Innovative Research Teams Project (202228028), Innovative Agricultural Applica-
tion Technology Project of Jinan City (CX202210) and Key Technological Innovation
Program of Shandong Province, China (2022CXGC020710)
Author contributions
Y.X. Wang took charge of the microscopy, DNA sequencing, data analyses and drafted
the paper; H. Zhao made specimens, proposed new species and revised the paper; Y.
Jiang, Xin-Y. Liu and M.F. Tao collected samples and isolated cultures; Xiao-Y. Liu pro-
posed new species, revised the paper and provided funding.
Author ORCIDs
Yi-Xin Wang https://orcid.org/0009-0001-5231-914X
Heng Zhao https://orcid.org/0000-0003-2938-5613
313
MycoKeys 110: 287–317 (2024), DOI: 10.3897/mycokeys.110.130260
Yi-Xin Wang et al.: Unveiling species diversity within early-diverging fungi from China III
Yang Jiang https://orcid.org/0009-0003-1292-610X
Xin-Ye Liu https://orcid.org/0009-0004-9396-1763
Xiao-Yong Liu https://orcid.org/0000-0002-8808-010X
Data availability
The sequences were deposited in the GenBank database.
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Supplementary material 1
The combined ITS+LSU+TEF+ACT+RPB1 sequence matrix used in this study
Authors: Yi-Xin Wang
Data type: fas
Explanation note: The sequence matrix included 43 strains in 25 species of Gongronella,
with Cunninghamella echinulata CBS 156.28 as outgroup. A total of 4,080 characters
comprised ITS rDNA (1–989), LSU rDNA (990–1967), TEF rDNA (1968–2172), ACT
rDNA (2173–2948) and RPB1 rDNA (2949–4080). Among them, there were 2866
constant, 562 variable but parsimony non-informative and 652 parsimony informa-
tive characters.
Copyright notice: This dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/mycokeys.110.130260.suppl1
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