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Taxonomy of two synnematal fungal species from Rhus chinensis, with Flavignomonia gen. nov. described
expand article infoNing Jiang, Qin Yang§, Ying-Mei Liang, Chengming Tian
‡ Beijing Forestry University, Beijing, China
§ Central South University of Forestry and Technology, Changsha, China
Open Access

Abstract

Rhus chinensis represents a commercially and ecologically important tree species in China, but suffers from canker diseases in Jiangxi Province. Synnemata, pycnidia and ascomata were discovered on cankered tissues. Strains were obtained from single ascospore or conidium within the fruiting bodies and identified based on morphological comparison and the phylogenetic analyses of partial ITS, LSU, tef1 and rpb2 gene sequences. As a result, two species were confirmed to represent two kinds of synnemata. One of these species is described herein as Flavignomonia rhoigena gen. et sp. nov.; and Synnemasporella aculeans is illustrated showing ascomata, pycnidia and synnemata. Flavignomonia is distinguished from Synnemasporella by the colour of the synnematal tips. Additionally, Flavignomonia can be distinguished from the other gnomoniaceous genera by the formation of synnemata.

Keywords

Diaporthales, Gnomoniaceae, systematics, taxonomy

Introduction

Many Diaporthales species are important branch canker pathogens, forming acervuli or pycnidia on diseased tissues (Rossman et al. 2007, Senanayake et al. 2017, Jiang et al. 2018, 2019, Wijayawardene et al. 2018, Yang et al. 2018, Voglmayr et al. 2019). However, two diaporthalean species with synnemata were reported to cause cankers, namely Synnemasporella aculeans (syn. Cryptodiaporthe aculeans) and S. toxicodendri (Fan et al. 2018). These two species differ from the other diaporthalean taxa in conidiomata and form a distinct clade phylogenetically, which was named Synnemasporellaceae and distinguished by Fan et al. (2018).

Gnomoniaceae was initially introduced with Gnomonia as the type (Winter 1886). Species in Gnomoniaceae formed upright perithecia, with or without long or short necks and presence or absence of stromatic tissues (Barr 1978, Sogonov et al. 2008, Walker et al. 2012). In the recent monograph of Diaporthales, 34 genera were accepted in the family Gnomoniaceae (Senanayake et al. 2018). Subsequently, Neognomoniopsis and Tenuignomonia were added based on both molecular and morphological evidence (Crous et al. 2019, Minoshima et al. 2019).

Chinese gall (Rhus chinensis Mill.) has a range of uses as source of medicine, dye and oil, and has a wide distribution in China (Wang et al. 2014). However, cankers were found to be associated with different ascomata during our fungal collection trips in Jiangxi Province, China. The objectives of the present study were to identify these fungi based on morphological and phylogenetic evidence.

Materials and methods

Sample collections and isolation

We conducted our fungal collection surveys from April to October in China, and found Rhus chinensis to be one of the major tree species in Jiangxi Province. Twigs, branches and stems were carefully checked, and diseased tissues were cut into small pieces and packed in paper bags. Isolates were obtained by transferring the ascospores or conidial masses from ascomata to sterile PDA plates, incubating at 25 °C until spores germinated. Single germinating spores were transferred onto new PDA plates, which were kept at 25 °C in darkness. Specimens were deposited in the Museum of the Beijing Forestry University (BJFC) and axenic cultures maintained in the China Forestry Culture Collection Centre (CFCC).

Morphological analysis

Recognition and identification of the fungal species on Rhus chinensis was based on fruiting bodies formed on the bark. Ascomata and conidiomata were sectioned by hand using a double-edged blade, and microscopic structures were observed under a dissecting microscope. At least 10 conidiomata/ascomata, 10 asci, and 50 conidia/ascospores were measured to calculate mean and standard deviation. Measurements are reported as maxima and minima in parentheses and the range representing the mean plus and minus the standard deviation of the number of measurements given in parentheses (Voglmayr et al. 2017). Microscopy photographs were captured with a Nikon Eclipse 80i compound microscope equipped with a Nikon digital sight DS-Ri2 high definition colour camera, using differential interference contrast illumination. Nomenclatural novelties and descriptions were deposited in MycoBank (Crous et al. 2004).

DNA extraction, PCR amplification and sequencing

Genomic DNA was extracted from colonies grown on cellophane-covered PDA plates using a modified CTAB method (Doyle and Doyle 1990). PCR amplifications were performed in a DNA Engine Peltier Thermal Cycler (PTC-200; Bio-Rad Laboratories, Hercules, CA, USA). The primer sets ITS1/ITS4 (White et al. 1990) were used to amplify the ITS region. The primer pair LR0R/LR5 (Vilgalys and Hester 1990) was used to amplify the LSU region. The primer pairs EF1-688F/EF1-986R or EF1-728F/TEF1-LLErev (Carbone and Kohn 1999; Jaklitsch et al. 2005; Alves et al. 2008) were used to amplify tef1 gene. The primer pair dRPB2-5f/dRPB2-7r (Voglmayr et al. 2016) was used to amplify the rpb2 gene. The polymerase chain reaction (PCR) assay was conducted as described by Fan et al. (2018). PCR amplification products were assayed via electrophoresis in 2 % agarose gels. DNA sequencing was performed using an ABI PRISM 3730XL DNA Analyzer with a BigDye Terminater Kit v.3.1 (Invitrogen, USA) at the Shanghai Invitrogen Biological Technology Company Limited (Beijing, China).

Phylogenetic analyses

The preliminary identities of the isolates sequenced in this study were obtained by conducting a standard nucleotide BLAST search using the sequences generated from the above primers of the different genomic regions (ITS, LSU, tef1 and rpb2). The BLAST results showed that three isolates were grouped in the family Gnomoniaceae, and five isolates in the genus Synnemasporella. The phylogenetic analyses for the three gnomoniaceous isolates were conducted based on Senanayake et al. (2018), supplemented by sequences of Tenuignomonia styracis and Neognomoniopsis quercina from Crous et al. (2019) and Minoshima et al. (2019). Melanconis marginalis (CBS 109744) in Melanconidaceae was selected as the out-group taxon. All sequences were aligned using MAFFT v. 6 (Katoh and Toh 2010) and edited manually using MEGA v. 6 (Tamura et al. 2013). Phylogenetic analyses were performed using PAUP v. 4.0b10 for maximum parsimony (MP) analysis (Swofford 2003), and PhyML v. 3.0 for Maximum Likelihood (ML) analysis (Guindon et al. 2010).

MP analysis was run using a heuristic search option of 1000 search replicates with random additions of sequences with a tree bisection and reconnection algorithm. Other calculated parsimony scores were tree length (TL), consistency index (CI), retention index (RI), and rescaled consistency (RC). ML analysis was performed using a GTR site substitution model including a gamma-distributed rate heterogeneity and a proportion of invariant sites (Guindon et al. 2010). The branch support was evaluated using a bootstrapping method of 1000 replicates (Hillis and Bull 1993). The matrix was partitioned for the different gene regions. Phylograms were shown using FigTree v. 1.4.3 (Rambaut 2016). Novel sequences generated in the current study were deposited in GenBank (Table 1) and the aligned matrices used for phylogenetic analyses in TreeBASE (accession number: S25047).

Strains used in the phylogenetic tree and their culture accession and GenBank numbers. Strains from this study are in bold.

Species Strains GenBank numbers
ITS LSU tef1 rpb2
Alnecium auctum CBS 124263 KF570154 KF570154 KF570200 KF570170
Ambarignomonia petiolorum CBS 116866 EU199193 AY818963 NA EU199151
CBS 121227 EU254748 EU255070 EU221898 EU219307
Amphiporthe tiliae CBS 119289 EU199178 EU199122 NA EU199137
Anisogramma anomala 529478 EU683064 EU683066 NA NA
Anisogramma virgultorum 529479 EU683062 EU683065 NA NA
Apiognomonia errabunda AR 2813 DQ313525 NG027592 DQ313565 DQ862014
Apiognomonia veneta MFLUCC 16-1193 MF190114 MF190056 NA NA
Apioplagiostoma populi 858501 KP637024 NA NA NA
Asteroma alneum CBS 109840 EU167609 EU167609 NA NA
Asteroma sp. Masuya 8Ah9-1 NA AB669035 NA NA
Cryptosporella hypodermia CBS 116866 EU199181 AF408346 NA EU199140
Discula destructiva MD 254 AF429741 AF429721 AF429732 NA
Ditopella biseptata MFLU 15-2661 MF190147 MF190091 NA MF377616
Ditopella ditopa CBS 109748 DQ323526 EU199126 NA EU199145
Ditopellopsis sp. CBS 121471 EU254763 EU255088 EU221936 EU219254
Flavignomonia rhoigena CFCC 53118 MK432674 MK429917 NA MK578102
CFCC 53119 MK432675 MK429918 NA MK578103
CFCC 53120 MK432676 MK429919 NA MK578104
Gnomonia gnomon CBS 199.53 DQ491518 AF408361 EU221885 EU219295
CBS 829.79 AY818957 AY818964 EU221905 NA
Gnomoniopsis alderdunensis CBS 125680 GU320825 NA NA NA
Gnomoniopsis chamaemori CBS 803.79 EU254808 EU255107 NA NA
Gnomoniopsis racemula AR 3892 EU254841 EU255122 EU221889 EU219241
Mamianiella coryli BPI 877578 EU254862 NA NA NA
Marsupiomyces quercina MFLUCC 13-0664 MF190116 MF190061 NA NA
Marsupiomyces epidermoidea MFLU 15-2921 NA MF190058 NA NA
Melanconis marginalis CBS 109744 EU199197 AF408373 EU221991 EU219301
Neognomoniopsis quercina CBS 145575 MK876399 MK876440 NA NA
Occultocarpon ailaoshanense LCM 524.01 JF779849 JF779853 NA JF779856
LCM 522.01 JF779848 JF779852 JF779862 JF779857
Ophiognomonia melanostyla LCM 389.01 JF779850 JF779854 NA JF779858
Ophiognomonia vasiljevae AR 4298 EU254977 EU255162 EU221999 EU219331
Plagiostoma aesculi AR 3640 EU254994 EU255164 NA EU219269
Linospora capreae CBS 372.69 NA AF277143 NA NA
Pleuroceras oregonense AR 4333 EU255060 EU255196 EU221931 EU219313
Pleuroceras pleurostylum CBS 906.79 EU255061 EU255197 EU221962 EU219311
Phragmoporthe conformis AR 3632 NA AF408377 NA NA
Valsalnicola oxystoma AR 5137 JX519561 NA NA NA
AR 4833 JX519559 JX519563 NA NA
Sirococcus tsugae AR 4010 EF512478 EU255207 EU221928 EU219289
CBS 119626 EU199203 EU199136 EF512534 EU199159
Synnemasporella aculeans CFCC 52094 MG682086 MG682026 MG682066 MG682046
Synnemasporella aculeans CFCC 53123 MK432679 MK429920 MK578148 MK578105
CFCC 53124 MK432680 MK429921 MK578149 MK578106
CFCC 53125 MK432681 MK429922 MK578150 MK578107
CFCC 53126 MK432682 MK429923 MK578151 MK578108
CFCC 53127 MK432683 MK429924 MK578152 MK578109
Synnemasporella toxicodendri CFCC 52097 MG682089 MG682029 MG682069 MG682049
Tenuignomonia styracis BPI 89278 NA LC379288 LC379282 LC379294

Results

Phylogenetic analyses

The alignment based on the combined sequence dataset (ITS, LSU, tef1, and rpb2) included 42 in-group taxa and one out-group taxon, comprising 3368 characters in the aligned matrix. Of these, 2201 characters were constant, 224 variable characters were parsimony-uninformative and 943 characters were parsimony informative (282 from the ITS-LSU, 280 from tef1, 381 from rpb2). The MP analysis resulted in nine equally most parsimonious trees with identical tree backbone. The best ML tree (lnL = −20604.0384) was compatible with the MP strict consensus tree, except for unsupported clades in Fig. 1. As the trees obtained from different analytical methods were similar, only the ML tree was present in Fig. 1. The phylogram based on the four gene sequence matrix indicated that the three strains from the present study represent a novel genus in Gnomoniaceae.

Figure 1. 

Phylogenetic tree based on an ML analysis of a combined DNA dataset of ITS, LSU, tef1 and rpb2 gene sequences for all genera with DNA data and some species of Gnomoniaceae. Bootstrap values ≥ 50 % for MP and ML analyses are presented at the branches. The scale bar represents the number of changes per site.

Taxonomy

Flavignomonia C.M. Tian, Q. Yang & N. Jiang, gen. nov.

MycoBank No: 829530

Diagnosis

Flavignomonia is distinguished from Synnemasporella by the orange tips of its synnemata.

Type species

Flavignomonia rhoigena C.M. Tian & Q. Yang

Etymology

The generic name is derived from the colour of synnemata (flavus = yellow) and the genus name Gnomonia.

Description

Sexual morph: not observed. Asexual morph: Conidiomata synnematal. Synnemata long and determinate, growing from host tissue, with brown base and orange tip, straight to curved, parallel, with flat to slightly concave and dark zone of conidiogenous cells and host tissue at their bases. Conidiophores reduced to conidiogenous cells. Conidiogenous cells phialidic, aggregated, hyaline, straight to curved, cylindrical, arranged adjacent to one another at the end of the synnema, producing a single conidium. Conidia cylindrical to oblong, smooth, multiguttulate, hyaline.

Notes

Flavignomonia is included in Gnomoniaceae based on DNA sequences data. Flavignomonia is morphologically similar to Synnemasporella in forming synnemata (Wehmeyer 1933, Fan et al. 2018). However, Flavignomonia, typified with Flavignomonia rhoigena, is distinguished from Synnemasporella species by its orange synnematal tips and hyaline conidia (Fan et al. 2018).

Flavignomonia rhoigena C.M. Tian & Q. Yang, sp. nov.

MycoBank No: 829531
Figure 2

Diagnosis

Flavignomonia rhoigena can be distinguished from other gnomoniaceous species by the formation of synnemata.

Etymology

Named after the host genus, Rhus.

Description

Sexual morph: not observed. Asexual morph: Conidiomata synnematal. Synnemata (650–)750–1100 µm high, 150–300 µm diam, determinate, growing from host tissue, with brown base and orange tip, straight to curved, parallel, with flat to slightly concave and dark zone of conidiogenous cells and host tissue at their bases. Conidiophores reduced to conidiogenous cells. Conidiogenous cells (12.5–)16–22(–25) × 2 μm, phialidic, aggregated, hyaline, straight to curved, cylindrical, arranged adjacent to one another at the end of the synnema, producing a single conidium. Conidia cylindrical to oblong, smooth, multiguttulate, hyaline, (5–)5.5–7(–8) × 1.5–2 µm.

Culture characters

On PDA at 25 °C in darkness, initially white, becoming olive-green to black after 3 wk, zonate with 3–4 well defined zones. Conidiomata distributed concentrically over agar surface.

Specimen examined

CHINA, Jiangxi Province, Ganzhou City, Xunwu County, 24°52'31.34"N, 115°35'39.53"E, on branches of Rhus chinensis, 14 May 2018, Q. Yang, Y. Liu & Y.M. Liang (holotype BJFC-S1766, ex-type living cultures CFCC 53118, CFCC 53119 and CFCC 53120).

Notes

Flavignomonia rhoigena is the type species of Flavignomonia in the family Gnomoniaceae. It can be easily distinguished from the other gnomoniaceous genera by its unique conidiomata (Walker et al. 2004, Senanayake et al. 2018, Crous et al. 2019, Minoshima et al. 2019).

Figure 2. 

Flavignomonia rhoigena on Rhus chinensis (BJFC-S1766, holotype) A–C habit of conidiomata on twigs D transverse section through synnema E longitudinal section through synnema F, I conidiogenous cells attached with conidia G conidiomata on PDA H condia J the colony on PDA. Scale bars: 1 mm (B); 500 μm (C); 100 μm (D); 10 μm (F, H–I); 200 μm (G).

Synnemasporella aculeans (Schwein.) X.L. Fan & J.D.P. Bezerra, Persoonia 40: 130. 2018.

Figure 3, 4

Description

Sexual morph: See Wehmeyer (1933) and Fan et al. (2018). Asexual morph: See Fan et al. (2018).

Specimens examined

CHINA, Jiangxi Province, Ganzhou City, Xunwu County, 24°52'31.34"N, 115°35'39.53"E, on branches of Rhus chinensis, 14 May 2018, Q. Yang, Y. Liu & Y.M. Liang (BJFC-S1740, living culture CFCC 53123); Ganzhou City, Fengshan forest park, 25°44'32.14"N, 114°59'25.54"E, on branches of Rhus chinensis, 15 May 2018, Q. Yang, Y. Liu & Y.M. Liang (BJFC-S1753, living culture CFCC 53124 and CFCC 53125). 24°38'38.18"N, 115°33'58.45"E, on branches of Rhus chinensis, 16 May 2018, Q. Yang, Y. Liu & Y.M. Liang (BJFC-S1745, living culture CFCC 53126 and CFCC 53127).

Notes

Synnemasporella aculeans was proposed as a new combination in the new genus Synnemasporella based on the description of Cryptodiaporthe aculeans (Fan et al. 2018), which was introduced producing perithecial ascomata, and an asexual morph producing sporodochial and/or pycnidial conidiomata (Wehmeyer 1933). In the present study, five isolates from canker tissues on Rhus chinensis were congruent with S. aculeans based on morphology and DNA sequences data. This was the first time that the sexual morph of Synnemasporella aculeans in China had been collected.

Figure 3. 

Asexual morphology of Synnemasporella aculeans on Rhus chinensis (BJFC-S1740) A, B habit of pycnidia on twigs C transverse section of pycnidium D longitudinal section through pycnidium E conidia F, G conidiogenous cells and conidia H, I habit of synnemata on twigs J longitudinal section through synnema K the colony on PDA L, N conidiogenous cells bearing conidia M conidia. Scale bars: 500 μm (B–D, I, J); 10 μm (E–G, L–N).

Figure 4. 

Sexual morphology of Synnemasporella aculeans on Rhus chinensis (BJFC-S1745) A, B habit of ascomata on twigs C transverse section of ascomata D longitudinal section through ascomata E, F asci G ascospores. Scale bars: 500 μm (B–D); 10 μm (E–G).

Discussion

In this study, two diaporthalean species forming synnemata on Rhus chinensis were identified based on morphology and ITS, LSU, tef1, and rpb2 sequence datasets. As a result, Flavignomonia typified with F. rhoigena is proposed as a new genus in Gnomoniaceae for its distinct phylogenic position and distinctive asexual fruiting body, Also, Synnemasporella aculeans strains were successfully isolated from perithecia, pycnidia and synnemata, which was confirmed by molecular data.

Nineteen fungal species have been recorded from the commercially and ecologically important tree species in China, including Cladosporium cladosporioides, Cronartium quercuum, Mycosphaerella fushinoki, Pestalotiopsis diospyri, P. guepinii, P. mangiferae, P. sorbi, Phaeoramularia rhois, Phyllactinia corylea, Ph. rhoina, Pileolaria klugkistiana, Pi. shiraiana, Pseudocercospora rhoina, Ps. toxicodendri, Septoria sp., Tubercularia phyllophila, Uncinula verniciferae, and two synnematal species from branch cankers in this study (Farr and Rossman 2019). Flavignomonia rhoigena and Synnemasporella aculeans, described and illustrated in the present study can be easily recognized by the asexual fruiting bodies, and they differ from each other in the colour of the synnematal tips.

Gnomoniaceae is a globally distributed fungal family on diverse plant hosts (Mejía et al. 2008, 2011a, 2011b, 2012, Sogonov et al. 2008, Walker et al. 2012, Senanayake et al. 2017, 2018). Host specificity of this family has been confirmed to be important in the evolution (Walker et al. 2014). Our newly discovered genus Flavignomonia was only found on Rhus chinensis, and more Flavignomonia species might be collected from the plant family Anacardiaceae in the future.

Acknowledgements

This study is financed by National Natural Science Foundation of China (Project No.: 31670647). We are grateful to Chungen Piao, Minwei Guo (China Forestry Culture Collection Center (CFCC), Chinese Academy of Forestry, Beijing.

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