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Article

Morphological and Phylogenetic Analyses Reveal Four New Species of Gnomoniopsis (Gnomoniaceae, Diaporthales) from China

by
Shi Wang
1,2,
Zhaoxue Zhang
2,
Rongyu Liu
2,
Shubin Liu
2,
Xiaoyong Liu
1,* and
Xiuguo Zhang
1,2,*
1
College of Life Sciences, Shandong Normal University, Jinan 250358, China
2
Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Taian 271018, China
*
Authors to whom correspondence should be addressed.
J. Fungi 2022, 8(8), 770; https://doi.org/10.3390/jof8080770
Submission received: 27 June 2022 / Revised: 16 July 2022 / Accepted: 21 July 2022 / Published: 25 July 2022
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Abstract

:
The fungal genus Gnomoniopsis (Gnomoniaceae, Diaporthales) has been reported all around the world and isolated from multiple plant hosts. Based on multilocus phylogenies from a combined dataset of internal transcribed spacer (ITS) region, the ribosomal RNA gene cluster, and partial regions of translation elongation factor 1 alpha (tef1) and partial beta-tubulin (tub2), in conjunction with morphological characteristics, we describe and illustrate herein four new species, including Gnomoniopsis diaoluoshanensis sp. Nov., G. lithocarpi sp. Nov., G. mengyinensis sp. Nov. and G. yunnanensis sp. Nov. Alongside this, their similarity and dissimilarity to morphologically-allied and phylogenetically-related species are annotated and discussed. For facilitating future identification, we update the key to all species currently recognized in this genus.

1. Introduction

Diaporthales Nannf. is an important order in the perithecial ascomycetes Sordariomycetes Erikss. & Winka, accommodating not only saprophytes but also endophytes or phytopathogens on various hosts [1,2,3,4,5]. Gnomoniaceae Winter, which contains 60 genera and 919 species, the second largest family in this order, occurs on growing and overwintering leaves and twigs of hardwood trees, shrubs, and herbaceous plants [6,7]. This family was first established in 1886 [8] and conserved by Hawksworth and Eriksson in 1988 [9,10]. Gnomoniaceae was circumscribed by Sogonov et al. in 2008 [11], and since then, their concept has been followed by others. At the present time, besides morphology and molecular data, host specificity has become a key characteristic for species identification and a single species in the Gnomoniaceae is often associated with a single host genus or species [6,12,13,14,15,16,17].
Gnomoniopsis Berl. was initially described as a subgenus within Gnomonia Ces. & De Not. for species with multi-septate ascospores [11]. Subsequently, multiple septa were found not to be a stable characteristic; thus, the Gnomoniopsis was synonymized with Gnomonia [17]. Currently, Gnomoniopsis is accepted as a separate genus in the Gnomoniaceae and typified by Gnomoniopsis chamaemori (Fr.) Berl. This genus is characterized by having small, black perithecia immersed in the host tissue and one-septate, oval to fusiform ascospores [4]. Species in this genus are delimitated by a combination of morphological and molecular data, and are known to inhabit three plant families only, viz. Fagaceae, Onagraceae and Rosaceae [4,5,11,15,18]. A total of 36 names are documented for Gnomoniopsis in the Index Fungorum (accessed on 20 June 2022) and 26 species possess sequence data.
Fungi associated with leaf spots were collected from Castanea mollissima Bl. (Fagaceae), Castanopsis chinensis Hance (Fagaceae), and Lithocarpus fohaiensis (Hu) A. Camus (Fagaceae). We obtained their respective morphological characteristics by separation and purification, using sequences of three molecular markers, including the internal transcribed spacer of ribosomal RNA gene (ITS rDNA), the translation elongation factor 1 alpha gene (tef1), and the beta-tubulin gene (tub2); we identified these fungi as four species of the genus Gnomoniopsis, and proposed them herein.

2. Materials and Methods

2.1. Isolation and Morphology

Samples of Castanea mollissima, Castanopsis chinensis and Lithocarpus fohaiensis showing necrotic spots were collected from Hainan, Shandong and Yunnan Provinces in China during 2020 and 2021. We obtained a single strain using tissue isolation and single spore isolation. Fragments (5 × 5 mm) were taken from the edges of leaf lesions, surface-sterilized by immersing consecutively in 75% ethanol solution for 1 min and rinsed in sterile distilled water for 30 s, and in 5% sodium hypochlorite solution for 30 s, and then rinsed three times in sterile distilled water for 30 s. The sterilized pieces were placed on sterile filter paper to absorb moisture and then placed on the PDA (PDA: 200 g potato, 20 g dextrose, 20 g agar, 1000 mL distilled water, pH 7.0) and incubated at 25 °C for 2–4 days. Subsequently, portions of agar with fungal mycelia from the periphery of the colonies were transferred onto new PDA plates and photographed on the 7th and 15th days by a digital camera (Canon Powershot G7X).
Micromorphological characters from structures produced in culture were observed using an Olympus SZX10 stereomicroscope and Olympus BX53 microscope, all fitted with an Olympus DP80 high-definition color digital camera to photo-document fungal structures. All fungal strains were stored in 10% sterilized glycerin at 4 ℃ for further studies. Structural measurements were taken using the Digimizer software (https://www.digimizer.com/, accessed on 20 June 2022), with 30 measurements taken for each character [19]. Voucher specimens were deposited in the Herbarium of the Department of Plant Pathology, Shandong Agricultural University, Taian, China (HSAUP) and Herbarium Mycologicum Academiae Sinicae, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China (HMAS). Ex-holotype living cultures were deposited in the Shandong Agricultural University Culture Collection (SAUCC). Taxonomic information of the new taxa was submitted to MycoBank (http://www.mycobank.org, accessed on 20 June 2022).

2.2. DNA Extraction and Amplification

Genomic DNA was extracted from mycelia grown on PDA using a CTAB (cetyltrimethylammonium bromide) method [20,21]. Three molecular markers, including an entire internal transcribed spacer region with intervening 5.8S rRNA gene (ITS), partial translation elongation factor 1-alpha gene (tef1) and partial beta-tubulin gene (tub2), were amplified with the primer pairs and polymerase chain reaction (PCR) programs listed in Table 1. PCR products were separated using the 1% agarose gel with GelRed and UV light was used to visualize the fragments [19]. Sequencing was carried out bidirectionally by the Biosune Company Limited (Shanghai, China). Consensus sequences were obtained using MEGA v. 7.0 [22]. All sequences generated in this study were deposited in GenBank under the accession numbers in Table 2.

2.3. Phylogenetic Analyses

The generated sequences for each gene were subjected to BLAST searches for identifying closely related sequences in the NCBI’s GenBank nucleotide database [27]. For the ITS-tef1-tub2 analysis, subsets of sequences from the alignments of Jiang et al. [4] were used as backbones. Newly generated sequences in this study were aligned with additional related sequences downloaded from GenBank (Table 1), using MAFFT 7 online service with the auto strategy (http://mafft.cbrc.jp/alignment/server/, accessed on 20 June 2022) [28]. To establish the identity of the isolates at species level, phylogenetic analyses were conducted first individually for each marker and then combinedly (ITS-tef1-tub2) (Supplementary File S1).
Phylogenetic analyses were conducted for the multi-marker data based on maximum likelihood (ML) and Bayesian inference (BI) algorithms. For BI, the best evolutionary model for each partition was determined using MrModeltest v. 2.3 [29] and incorporated into the analyses. ML and BI run on the CIPRES Science Gateway portal (https://www.phylo.org/, accessed on 20 June 2022) [30]. ML was performed in RaxML-HPC2 on XSEDE (8.2.12) [31] and 1000 rapid bootstrap replicates were run with the GTRGAMMA model of nucleotide evolution. BI was performed in MrBayes on XSEDE (3.2.7a) [32,33,34]. For ML analyses, the default parameters were used and BI was carried out using the rapid bootstrapping algorithm with the automatic halt option. Bayesian analyses included 4 parallel runs of 5,000,000 generations, with the stop rule option and a sampling frequency of 100 generations. The burn-in fraction was set to 0.25 and posterior probabilities (PP) were determined from the remaining trees. All resulted trees were plotted using FigTree v. 1.4.4 (http://tree.bio.ed.ac.uk/software/figtree, accessed on 20 June 2022) and the layout of the trees was carried out in Adobe Illustrator CC 2019.

3. Results

3.1. Phylogenetic Analyses

The alignment contained 50 isolates representing Gnomoniopsis and allied taxa, and the strain CBS 109778 of Melanconis stilbostoma was used as the outgroup. A total of 1751 characters were used for phylogenetic analyses, viz. 1–550 (ITS), 551–1222 (tef1), 1223–1751 (tub2). Of these characters, 979 were constant, 69 were variable and parsimony-uninformative and 703 were parsimony-informative. MrModelTest recommended that the Bayesian inference should use the Dirichlet base frequencies and the GTR+I+G evolutionary mode for all the three partitions. The topology of the Bayesian tree was consistent with that of the ML tree, and therefore is shown as a representative for recapitulating evolutionary history within the genus Gnomoniopsis (Figure 1). The final ML optimization likelihood was -13036.518679. The 50 strains were assigned to 28 species clades on the phylogram (Figure 1).
Based on the phylogenetic resolution and morphological analyses, the present study reports four new species of the Gnomoniopsis species, viz. Gnomoniopsis diaoluoshanensis sp. nov., G. lithocarpi sp. nov., G. mengyinensis sp. nov. and G. yunnanensis sp. nov.

3.2. Taxonomy

3.2.1. Gnomoniopsis diaoluoshanensis S. Wang, Z.X. Zhang, X.Y. Liu and X.G. Zhang, sp. nov.

MycoBank—No: MB844512
Etymology—The epithet diaoluoshanensis pertains to the location of the holotype, Diaoluoshan National Silva Park.
Type—China, Hainan Province, Diaoluoshan National Silva Park (18°38′42″–18°50′22″ N, 109°41′38″–110°4′46″ E), on diseased leaves of Castanopsis chinensis (Fagaceae), 21 May 2021, Z.X. Zhang, holotype HMAS 352166, ex-holotype living culture SAUCC DL0963.
Description—Leaf is endogenic and associated with leaf spots. Conidiomata (pycnothyria) are buried or attached to mycelia, aggregated or solitary, erumpent, exuding creamy yellow conidia after 7 days at 25 ℃ in dark. Conidiophores are indistinct, often reduced. Conidiogenous cells are hyaline, smooth, multi-guttulate, cylindrical to ampulliform, attenuate towards apex, phialidic, 8.0–12.0 × 1.0–2.0 μm. Conidia are hyaline, smooth, multi-guttulate, ellipsoid to broadly ellipsoid, base truncate, 3.8–7.0 × 1.2–2.0 μm, mean = (5.2 ± 0.7) × (1.6 ± 0.2) μm, see Figure 2. Sexual morph was not observed.
Culture characteristics—Colonies on PDA entirely occupy a 90 mm petri dish in 14 days at 25 °C in dark, with a growth rate of 6.0–6.5 mm/day, are grey-white to creamy white with an irregular margin, spreading out in circles in a similar way to petals and the reverse is similar in color.
Additional specimen examined—China, Hainan Province, Diaoluoshan National Silva Park, on diseased leaves of Castanopsis chinensis (Fagaceae), 21 May 2021, Z.X. Zhang, paratype HMAS 352168, ex-paratype living culture SAUCC DL0961; on diseased leaves of Castanopsis chinensis (Fagaceae), 21 May 2021, Z.X. Zhang, paratype HMAS 352167, ex-paratype living culture SAUCC DL0964.
Notes—Phylogenetic analyses of a combined three genes (ITS, tef1 and tub2) showed that Gnomoniopsis diaoluoshanensis sp. nov. formed an independent clade and is phylogenetically closely related to G. daii, G. mengyinensis sp. nov. and G. yunnanensis sp. nov. (Figure 1). In detail, G. diaoluoshanensis is distinguished from G. daii by 14/496, 25/314 and 32/445 characters in ITS, tef1 and tub2 sequences, respectively. It is distinguished from G. mengyinensis by 17/511, 46/638 and 27/467 characters, and from G. yunnanensis by 10/508, 28/638 and 6/466. Morphologically, G. diaoluoshanensis differs from G. daii, G. mengyinensis sp. nov. and G. yunnanensis sp. nov. mainly in conidia (3.8–7.0 × 1.2–2.0 μm vs. 5.5–7.0 × 2.1–2.5 μm vs. 4.5–6.5 × 1.8–2.8 μm vs. 4.1–5.5 × 1.3–2.0 μm) [4,35].

3.2.2. Gnomoniopsis lithocarpi S. Wang, Z.X. Zhang, X.Y. Liu and X.G. Zhang, sp. nov.

MycoBank—No: MB844513
Etymology—The epithet lithocarpi pertains to the generic name of the host plant Lithocarpus fohaiensis.
Type—China, Yunnan Province, Xishuangbanna Tropical Botanical Garden (21°41′ N, 101°25′ E), Chinese Academy of Sciences, on diseased leaves of Lithocarpus fohaiensis (Fagaceae), 11 Sep 2020, Z. X. Zhang, holotype HMAS 352165, ex-holotype living culture SAUCC200743.
Description—Leaf is endogenic and associated with leaf spots. Conidiomata (pycnothyria) are buried or attached to mycelia, aggregated or solitary, erumpent, exuding pale yellow conidia after 14 days at 25 °C in dark. Conidiophores are indistinct, often reduced. Conidiogenous cells are hyaline, smooth, multi-guttulate, cylindrical to ampulliform, attenuate towards apex, phialidic, 6.0–13.0 × 1.5–2.5 μm. Conidia are hyaline, smooth, multi-guttulate, ellipsoid to ovoid, base circular, 4.0–5.8 × 1.7–2.4 μm, mean = (4.6 ± 0.5) × (2.1 ± 0.2) μm, see Figure 3. Sexual morph was not observed.
Culture characteristics—Colonies on PDA at 25 °C for 14 days in dark reach 75–80 mm in diameter, are circular, with moderate aerial mycelia on the surface, light brown and sparse in the center, white and dense at the edge and the reverse is similar in color.
Additional specimen examined—China, Yunnan Province, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences on diseased leaves of Lithocarpus fohaiensis (Fagaceae), 11 Sep 2020, Z.X. Zhang, paratype HMAS 352164, ex-paratype living culture SAUCC YN0742.
Notes—Phylogenetic analyses of three combined genes (ITS, tef1 and tub2) showed that Gnomoniopsis lithocarpi formed an independent clade closely related to G. castanopsidis and G. silvicola. The G. lithocarpi sp. nov. is distinguished from G. castanopsidis by 35/513, 41/325 and 48/478 characters in ITS, tef1 and tub2 sequences, respectively, and from G. silvicola by 38/517, 42/325 and 58/470 characters. Morphologically, G. lithocarpi differs from G. castanopsidis and G. silvicola in conidia (4.0–5.8 × 1.7–2.4 μm vs. 4.5–5.3 × 2.2–2.7 μm vs. 4.6–5.1 × 2.1–2.5 μm), and in colony texture (light brown to white on PDA and dense at the edge vs. dirty-white to fawn on PDA and undulate margin vs. dirty-white on PDA and undulate margin) [4,35].

3.2.3. Gnomoniopsis mengyinensis S. Wang, Z.X. Zhang, X.Y. Liu and X.G. Zhang, sp. nov.

MycoBank No.: MB844514
Etymology—The epithet mengyinensis pertains to the location where the holotype was collected, Mengyin County.
Type—China, Shandong Province, Mengyin County (35°71′ N, 117°94′ E), on diseased leaves of Castanea mollissima (Fagaceae), 25 July 2020, Z.X. Zhang, holotype HMAS 352160, ex-holotype living culture SAUCC MY0293.
Description—Leaf is endogenic and associated with leaf spots. Conidiomata (pycnothyria) are aggregated or solitary, erumpent, globose to pulvinate, light brown, exuding creamy white or hyaline conidial after 10 days at 25 °C in dark. Conidiophores are indistinct, often reduced. Conidiogenous cells are hyaline, cylindrical, attenuate towards apex, phialidic, 8.0–11.5 × 1.3–2.2 μm. Conidia are hyaline, smooth, multi-guttulate, cylindrical, oval to fusoid, straight or slightly curved, truncate at the base, 4.5–6.5 × 1.8–2.8 μm, mean = (5.4 ± 0.4) × (2.2 ± 0.2) μm, see Figure 4. Sexual morph is unknown.
Culture characteristics—Cultures incubated on PDA at 25 °C in dark attain 82.0–86.0 mm in diameter after 14 days, with a growth rate of 5.8–6.2 mm diam/day and the colonies are flat, spreading with moderate aerial mycelia and lobate to undulate margins, grey-white to creamy, spreading out in a similar way to petals and the reverse is similar in color.
Additional specimen examined—China, Shandong Province, Mengyin County, on diseased leaves of Castanea mollissima (Fagaceae), 25 July 2020, Z.X. Zhang, paratype HMAS 352159, ex-prartype living culture SAUCC MY0296.
Notes—In the phylogenetic tree (Figure 1), Gnomoniopsis mengyinensis sp. nov. is closely related to G. daii (BIPP = 0.97, MLBS = 95%). This new species is distinguished from G. daii by a total of 65 characters in the concatenated sequence alignment (5/509 in the ITS, 29/313 in the tef1 and 22/442 in the tub2). Morphologically, Gnomoniopsis mengyinensis differs from G. daii in conidia (4.5–6.5 × 1.8–2.8 μm vs. 5.1–6.3 × 2.8–3.2 μm), conidiogenous cells (4.5–6.5 × 1.8–2.8 μm vs. 5.6–6.1 × 2.8–3.2 μm), as well as conidiomatum color (light brown vs. dark brown) [4,35].

3.2.4. Gnomoniopsis yunnanensis S. Wang, Z.X. Zhang, X.Y. Liu and X.G. Zhang, sp. nov.

MycoBank—No: MB844515
Etymology—The epithet yunnanensis pertains to the location where the holotype was collected, Yunnan Province.
Type—China, Yunnan Province, Xishuangbanna Tropical Botanical Garden (21°41′N, 101°25′E), Chinese Academy of Sciences, on diseased leaves of Castanea mollissima (Fagaceae), 11 Sep 2020, Z. X. Zhang, holotype HMAS 352161, ex-holotype living culture SAUCC YN1659.
Description—Leaf is endogenic and associated with leaf spots. Conidiomata (pycnothyria) are aggregated or solitary, erumpent, globose to pulvinate, light yellow, exuding creamy white or hyaline conidia after 14 days at 25 °C in dark. Conidiophores are indistinct, often reduced. Conidiogenous cells are hyaline, cylindrical, attenuate towards apex, phialidic, 9.0–18.0 × 0.5–1.57 μm. Conidia are hyaline, smooth, multi-guttulate, cylindrical, oblong to ellipsoid, straight or slightly curved, truncate at the base, 4.1–5.5 × 1.3–2.0 μm, mean = (4.9 ± 0.4) × (1.6 ± 0.2) μm, see Figure 5. Sexual morph is unknown.
Culture characteristics—Cultures incubated on PDA at 25 °C for 14 days in dark attain 69.0–72.0 mm in diameter, with a growth rate of 4.9–5.2 mm diam/day, with moderate aerial mycelia and a lobate to undulate margin, grey-white to creamy, spreading out in a similar way to petals and the reverse is similar in color.
Additional specimen examined—China, Yunnan Province, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, on diseased leaves of Castanea mollissima (Fagaceae), 11 Sep 2020, Z.X. Zhang, paratype HMAS 352162, ex-paratype living culture SAUCC YN1657; on diseased leaves of Castanea mollissima (Fagaceae), 11 Sep 2020, Z.X. Zhang, paratype HMAS 352163, ex-paratype living culture SAUCC YN1641.
Notes—Strains SAUCC YN1659, SAUCC YN1657 and SAUCC YN1641 are identified to the same species Gnomoniopsis yunnanensis sp. nov. on the basis of similar morphology and molecular monophyly. For details, one can refer to the notes for G. diaoluoshanensis.

3.3. Key to the Species of Gnomoniopsis

Together with the 4 new species proposed in this study, we have currently accepted a worldwide total of 30 species in the genus Gnomoniopsis. In order to facilitate identification in the future, a key to the species of Gnomoniopsis is provided herein. Characteristics adopted in the key include perithecia, septa, asci, ascospores, conidiogenous cells, conidia, and chlamydospores.
1. Sexual morph known------------------------------------------------------------------------------------2
1. Sexual morph unknown-------------------------------------------------------------------------------16
2. Asci cylindrical--------------------------------------------------------------------------------------------3
2. Asci fusiform-----------------------------------------------------------------------------------------------4
3. Ascospores size 10.0–13.0 × 2.0–3.0 μm---------------------------------------------G. chamaemori
3. Ascospores size 4.0–12.0 × 1.0–3.0 μm----------------------------------------------G. smithogilvyi
4. Perithecia without stroma-------------------------------------------------------------------------------5
4. Perithecia with stroma-----------------------------------------------------------------------------------7
5. Perithecia immersed--------------------------------------------------------------------G. sanguisorbae
5. Perithecia superficies-------------------------------------------------------------------------------------6
6. Perithecia size 110.0–150.0 × 120.0–140.0 μm-----------------------------------G. clavulata
6. Perithecia size 139.0–180.0 × 156.0–241.0 μm-----------------------------G. paraclavulata
7. Ascospores aseptate--------------------------------------------------------------------------------------8
7. Ascospores septate--------------------------------------------------------------------------------------10
8. Perithecia groups----------------------------------------------------------------------------G. racemula
8. Perithecia solitary-----------------------------------------------------------------------------------------9
9. Ascospores size 6.0–10.0 × 1.5–3.0 μm----------------------------------------------G. tormentillae
9. Ascospores size 7.0–8.0 × 1.8–2.2 μm-------------------------------------------------G. agrimoniae
10. Perithecia surfaced on the host---------------------------------------------------------------------11
10. Perithecia immersed in the host--------------------------------------------------------------------12
11. Perithecia size 280.0–375.0 × 327.0–490.0 μm----------------------------------G. alderdunensis
11. Perithecia size 112–330.0 × 125–500.0 μm-----------------------------------------------G. comari
12. Perithecia immersed in stem------------------------------------------------------------------------13
12. Perithecia immersed in leaves----------------------------------------------------------------------14
13. Asci size 30.0–48.5 × 5.0–10.0-------------------------------------------------------------G. idaeicola
13. Asci size 30.0–38.0 × 4.0–8.5--------------------------------------------------------------G. macounii
14. Perithecia aggregated 2–4----------------------------------------------------------------G. guttulata
14. Perithecia solitary--------------------------------------------------------------------------------------15
15. Perithecia size 150.0–475.0 × 200.0–475.0 μm----------------------------------------G. fragariae
15. Perithecia size 129.0–340.0 × 147.0–428.0 μm-------------------------------------------G. occulta
16. Conidiogenous cells guttulate----------------------------------------------------------------------17
16. Conidiogenous cells no guttulate------------------------------------------------------------------24
17. Conidia base circular--------------------------------------------------------G. lithocarpi sp. nov.
17. Conidia base truncate---------------------------------------------------------------------------------18
18. Conidia ellipsoid or cylindrical---------------------------------------------------------------------19
18. Conidia oval or fusoid--------------------------------------------------------------------------------20
19. Conidiogenous cells size 8.0–12.0 × 1.0–2.0 μm-------------G. diaoluoshanensis sp. nov.
19. Conidiogenous cells size 12.5–24.0 × 1.5–3.0 μm---------------------------G. guangdongensis
20. Conidia 1-septate-------------------------------------------------------------------------G. rossmaniae
20. Conidia aseptate----------------------------------------------------------------------------------------21
21. Conidia maximum length < 6.0 μm----------------------------------------------------------------22
21. Conidia maximum length > 6.0 μm----------------------------------------------------------------23
22. Conidiogenous cells 6.5–13.0 × 1.5–3.0 μm--------------------------------------G. castanopsidis
22. Conidiogenous cells 7.0–15.0 × 1.5–2.5 μm--------------------------------------------G. silvicola
23. Conidiogenous cells 16.0–33.5 × 2.0–5.0--------------------------------------------G. fagacearum
23. Conidiogenous cells 16.5–26.0 × 2.5–4.5-------------------------------------------G. hainanensis
24. Conidiogenous cells one-celled---------------------------------------------------------------------25
24. Conidiogenous cells multi-celled------------------------------------------------------------------26
25. Conidia 1-septate---------------------------------------------------------------------------G. chinensis
25. Conidia aseptate-----------------------------------------------------------------------------------G. daii
26. Conidiogenous cells branched-------------------------------------------------------G. xunwuensis
26. Conidiogenous cells unbranched------------------------------------------------------------------27
27. Conidia maximum length < 10.0 μm--------------------------------------------------------------28
27. Conidia maximum length > 10.0 μm--------------------------------------------------------------29
28. Conidia oval to fusoid--------------------------------------------------G. mengyinensis sp. nov.
28. Conidia oblong to ellipsoid---------------------------------------------G. yunnanensis sp. nov.
29. Conidia subcylindrical------------------------------------------------------------------G. angolensis
29. Conidia fusoid-----------------------------------------------------------------------------------G. rosae

4. Discussion

In the present study, four new species (Gnomoniopsis diaoluoshanensis, G. lithocarpi, G. mengyinensis, and G. yunnanensis) from three hosts (Castanea mollissima, Castanopsis chinensis, and Lithocarpus fohaiensis) in three provinces of China were described and illustrated (Figure 2, Figure 3, Figure 4 and Figure 5), and all these three hosts belong to the family Fagaceae. Currently, Gnomoniopsis species were found from hosts that belong to three plant families (Fagaceae, Onagraceae and Rosaceae). Sixteen Gnomoniopsis species (including the four new species herein) were described from fagaceous hosts. Only one species (G. racemula) was described from the Onagraceae family [11,15,36]. The remaining 11 species were from the family Rosaceae. The Fagaceae, Onagraceae and Rosaceae plants are widely distributed in China, suggesting abundant potentially new Gnomoniopsis species.
Driven by recent developments in DNA sequence analyses, taxonomists have combined phylogenetic data to gain insights into evolutionary relationships [37,38,39]. Jiang et al. [4] introduced six species in Gnomoniopsis, based on three gene loci encoding the internal transcribed spacer of ribosomal RNA (ITS), translation elongation factor 1 alpha (tef1), and beta-tubulin (tub2). They described and illustrated the Gnomoniopsis species from seven regions (Fujian, Guangdong, Hainan, Henan, Jiangxi and Shaanxi) in China. In sum, 13 species of Gnomoniopsis were recorded in more than 10 regions of China, and they are Gnomoniopsis castanopsidis, G. chinensis, G. daii, G. diaoluoshanensis, G. fagacearum, G. guangdongensis, G. hainanensis, G. lithocarpi, G. mengyinensis, G. rossmaniae, G. silvicola, G. xunwuensis and G. yunnanensis.
The Gnomoniopsis species were reported with 200 records in Fungal Databases (https://nt.ars-grin.gov/fungaldatabases/index.cfm, accessed on 20 June 2022). Among these, G. daii and G. chinensis were determined to be phytopathogenic, causing fruit rot and leaf spot diseases and branch canker of Chinese chestnut, respectively [40,41]. Gnomoniopsis smithogilvyi were illustrated and described in 12 countries (Australia, New Zealand, Chile, France, India, Ireland, Italy, Portugal, Spain, Switzerland, United Kingdom and USA) with 30 records in Fungal Databases, causing sweet chestnut branch canker and fruit rot in Australia, Europe and USA [42,43,44]. Apart from this, Linaldeddu et. al. revealed some fungi associated with branch diseases of hazelnut in Sardinia (Italy), including Dothiorella iberica, Do. omnivora, Do. symphoricarposicola and G. smithogilvyi. Gnomoniopsis smithogilvyi was isolated from rotting chestnut kernels as an endophyte from asymptomatic flowers, leaves and stems of the genus Chestnut [45]. The descriptions, pathogenicity testing and molecular data for species of Gnomoniopsis by taxonomists represent an important resource for plant pathologists and plant quarantine officials.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jof8080770/s1, Supplementary File S1: The combined ITS, tef1 and tub2 sequences.

Author Contributions

Conceptualization, S.W. and X.L.; methodology, S.L.; software, Z.Z.; validation, S.W.; formal analysis, X.L.; investigation, R.L.; resources, Z.Z.; data curation, S.W.; writing—original draft preparation, S.W.; writing—review and editing, X.L.; visualization, X.L.; supervision, X.Z.; project administration, X.Z.; funding acquisition, X.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by National Natural Science Foundation of China (nos. U2002203, 31750001 and 31900014).

Institutional Review Board Statement

Not applicable for studies involving humans or animals.

Informed Consent Statement

Not applicable.

Data Availability Statement

The sequences from the present study were submitted to the NCBI database (https://www.ncbi.nlm.nih.gov/, accessed on 20 June 2022) and the accession numbers were listed in Table 2.

Conflicts of Interest

The authors declare no conflict of interest.

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Jof 08 00770 g001 550
Figure 1. A Bayesian inference phylogram of Gnomoniopsis based on combined ITS, tef1 and tub2 gene sequences with CBS 109778 of Melanconis stilbostoma as the outgroup. At the nodes, the Bayesian inference posterior probability (left, BIPP ≥ 0.90) and the maximum likelihood bootstrap value (right, MLBV ≥ 50%) are separated by a slash. Strains marked with “*” are ex-types or ex-epitypes. Strains from the present study are in red. Some branches are shortened to fit to the page, which are indicated by double slashes and the number of fold times. The scale bar at the bottom middle indicates 0.03 substitutions per site.
Figure 1. A Bayesian inference phylogram of Gnomoniopsis based on combined ITS, tef1 and tub2 gene sequences with CBS 109778 of Melanconis stilbostoma as the outgroup. At the nodes, the Bayesian inference posterior probability (left, BIPP ≥ 0.90) and the maximum likelihood bootstrap value (right, MLBV ≥ 50%) are separated by a slash. Strains marked with “*” are ex-types or ex-epitypes. Strains from the present study are in red. Some branches are shortened to fit to the page, which are indicated by double slashes and the number of fold times. The scale bar at the bottom middle indicates 0.03 substitutions per site.
Jof 08 00770 g001
Jof 08 00770 g002 550
Figure 2. Gnomoniopsis diaoluoshanensis (holotype HMAS 352166. (a) Leaves of host plant; (b,c) inverse and reverse sides of colony after 15 days on PDA; (d) colony overview; (e,f) conidiogenous cells and conidia; (g,h) conidia. Scale bars: (e–h) 10 μm.
Figure 2. Gnomoniopsis diaoluoshanensis (holotype HMAS 352166. (a) Leaves of host plant; (b,c) inverse and reverse sides of colony after 15 days on PDA; (d) colony overview; (e,f) conidiogenous cells and conidia; (g,h) conidia. Scale bars: (e–h) 10 μm.
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Figure 3. Gnomoniopsis lithocarpi (holotype HMAS 352165). (a) Leaves of host plant; (b,c) inverse and reverse sides of colony after 15 days on PDA; (d) colony overview; (e–g) conidiogenous cells and conidia; (h,i) conidia. Scale bars: (e–i) 10 μm.
Figure 3. Gnomoniopsis lithocarpi (holotype HMAS 352165). (a) Leaves of host plant; (b,c) inverse and reverse sides of colony after 15 days on PDA; (d) colony overview; (e–g) conidiogenous cells and conidia; (h,i) conidia. Scale bars: (e–i) 10 μm.
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Figure 4. Gnomoniopsis mengyinensis (holotype HMAS 352160). (a) Leaves of host plant; (b,c) inverse and reverse sides of colony after 14 days on PDA; (d) colony overview; (e–h) conidiogenous cells and conidia; (i) conidia. Scale bars: (e–i) 10 μm.
Figure 4. Gnomoniopsis mengyinensis (holotype HMAS 352160). (a) Leaves of host plant; (b,c) inverse and reverse sides of colony after 14 days on PDA; (d) colony overview; (e–h) conidiogenous cells and conidia; (i) conidia. Scale bars: (e–i) 10 μm.
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Figure 5. Gnomoniopsis yunnanensis (holotype HMAS 352161). (a) Leaves of host plant; (b,c) inverse and reverse sides of colony after 15 days on PDA; (d) colony overview; (e–g) conidiogenous cells and conidia; (h,i) conidia. Scale bars: (e–i) 10 μm.
Figure 5. Gnomoniopsis yunnanensis (holotype HMAS 352161). (a) Leaves of host plant; (b,c) inverse and reverse sides of colony after 15 days on PDA; (d) colony overview; (e–g) conidiogenous cells and conidia; (h,i) conidia. Scale bars: (e–i) 10 μm.
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Table
Table 1. Molecular markers and their PCR primers and programs used in this study.
Table 1. Molecular markers and their PCR primers and programs used in this study.
LociPCR PrimersSequence (5′—3′)PCR CyclesReferences
ITSITS5
ITS4		GGA AGT AAA AGT CGT AAC AAG G
TCC TCC GCT TAT TGA TAT GC		(95 °C: 30 s, 55 °C: 30 s, 72 °C: 1 min) × 35 cycles[23]
tef1EF1-728F
EF-2		CAT CGA GAA GTT CGA GAA GG
GGA RGT ACC AGT SAT CAT GTT		(95 °C: 30 s, 48 °C: 30 s, 72 °C: 1 min) × 35 cycles[24,25]
tub2Bt-2a
Bt-2b		GGT AAC CAA ATC GGT GCT GCT TTC
ACC CTC AGT GTA GTG ACC CTT GGC		(95 °C: 30 s, 53 °C: 30 s, 72 °C: 1 min) × 35 cycles[26]
Table
Table 2. Information of specimens used in this study.
Table 2. Information of specimens used in this study.
SpeciesVoucherHostCountryGenBank Accession Number
ITStef1tub2
Gnomoniopsis alderdunensisCBS 125680 *Rubus parviflorus (Rosaeace)USAGU320825GU320801GU320787
CBS 125681Rubus parviflorus (Rosaeace)USAGU320827GU320802GU320789
G. castanopsidisCFCC 54437 *Castanopsis hystrix (Fagaceae)ChinaMZ902909MZ936385–
CFCC 54438Castanopsis hystrix (Fagaceae)ChinaMZ902910MZ936386–
G. chamaemoriCBS 804.79Rubus chamaemorus (Rosaeace)FinlandGU320817GU320809GU320777
G. chinensisCFCC 52286 *Castanea mollissima (Fagaceae)ChinaMG866032MH545370MH545366
CFCC 52288Castanea mollissima (Fagaceae)ChinaMG866034MH545372MH545368
CFCC 52287Castanea mollissima (Fagaceae)ChinaMG866033MH545371MH545367
G. clavulataCBS 121255Quercus falcata (Fagaceae)USAEU254818EU221934EU219211
G. comariCBS 806.79Oryza sativa (Rosaeace)UKEU254821GU320810EU219156
G. daiiCFCC 54043 *Castanea mollissima (Fagaceae)ChinaMZ902911MZ936387MZ936403
CFCC 55517Castanea mollissima (Fagaceae)ChinaMN598671MN605517MN605519
G. diaoluoshanensisSAUCC DL0963 *Castanopsis chinensis (Fagaceae)ChinaON753744ON759769ON759777
SAUCC DL0964Castanopsis chinensis (Fagaceae)ChinaON753743ON759768ON759776
SAUCC DL0961Castanopsis chinensis (Fagaceae)ChinaON753745ON759770ON759778
G. fagacearumCFCC 54316 *Lithocarpus glaber (Fagaceae)ChinaMZ902916MZ936392MZ936408
CFCC 54288Castanopsis faberi (Fagaceae)ChinaMZ902913MZ936389MZ936405
G. fragariae = G. fructicolaCBS 208.34Fragaria sp. (Rosaeace)USAEU254826EU221968EU219149
CBS 121226Fragaria vesca (Rosaeace)USAEU254824EU221961EU219144
G. guangdongensisCFCC 54443 *Castanopsis fargesii (Fagaceae)ChinaMZ902918MZ936394MZ936410
CFCC 54331Castanopsis fargesii (Fagaceae)ChinaMZ902919MZ936395MZ936411
G. guttulataMS 0312Agrimonia eupatoria (Rosaeace)BulgariaEU254812––
G. hainanensisCFCC 54376 *Castanopsis hainanensis (Fagaceae)ChinaMZ902921MZ936397MZ936413
CFCC 55877Castanopsis hainanensis (Fagaceae)ChinaMZ902922MZ936398MZ936414
G. idaeicolaCBS 125672Rubus sp. (Rosaeace)USAGU320823GU320797GU320781
CBS 125673Rubus pedatus (Rosaeace)USAGU320824GU320798GU320782
CBS 125674Rubus sp. (Rosaeace)FranceGU320820GU320796GU320780
G. lithocarpiSAUCC YN0743 *Lithocarpus fohaiensis (Fagaceae)ChinaON753749ON759765ON759783
SAUCC YN0742Lithocarpus fohaiensis (Fagaceae)ChinaON753750ON759764ON759782
G. macouniiCBS 121468Spiraea sp. (Rosaeace)USAEU254762EU221979EU219126
G. mengyinensisSAUCC MY0293 *Castanea mollissima (Fagaceae)ChinaON753741ON759766ON759774
SAUCC MY0296Castanea mollissima (Fagaceae)ChinaON753742ON759767ON759775
G. occultaCBS 125677Potentilla sp. (Rosaeace)USAGU320828GU320812GU320785
CBS 125678Potentilla sp. (Rosaeace)USAGU320829GU320800GU320786
G. paraclavulataCBS 123202Agrostis sp. (Fagaceae)USAGU320830GU320815GU320775
G. racemulaCBS 121469 *Triticum aestivum (Onagraceae)USAEU254841EU221889EU219125
G. rossmaniaeCFCC 54307 *Castanopsis hainanensis (Fagaceae)ChinaMZ902923MZ936399MZ936415
CFCC 55876Castanopsis hainanensis (Fagaceae)ChinaMZ902924MZ936400MZ936416
G. sanguisorbaeCBS 858.79Sanguisorba minor (Rosaeace)SwitzerlandGU320818GU320805GU320790
G. silvicolaCFCC 54304Castanopsis hystrix (Fagaceae)ChinaMZ902925MZ936401MZ936417
CFCC 54418 *Quercus serrata (Fagaceae)ChinaMZ902926MZ936402MZ936418
G. smithogilvyiCBS 130190 *Castanea sp. (Fagaceae)AustraliaJQ910642JQ910645JQ910639
CBS 130189Castanea sp. (Fagaceae)AustraliaJQ910644JQ910647JQ910641
G. tormentillaeCBS 904.79Potentilla sp. (Rosaeace)SwitzerlandEU254856GU320795EU219165
G. xunwuensisCFCC 53115 *Castanopsis fissa (Fagaceae)ChinaMK432667MK578141MK578067
CFCC 53116Castanopsis fissa (Fagaceae)ChinaMK432668MK578142MK578068
G.yunnanensisSAUCC YN1659 *Castanea mollissima (Fagaceae)ChinaON753746ON759771ON759779
SAUCC YN1657Castanea mollissima (Fagaceae)ChinaON753747ON759772ON759780
SAUCC YN1641Castanea mollissima (Fagaceae)ChinaON753748ON759773ON759781
Melanconis stilbostomaCBS 109778Betula pendula (Betulaceae)AustraliaDQ323524EU221886EU219104
Notes: New species established in this study are in bold. Ex-type or ex-epitype strains are marked with “*”.
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Wang, S.; Zhang, Z.; Liu, R.; Liu, S.; Liu, X.; Zhang, X. Morphological and Phylogenetic Analyses Reveal Four New Species of Gnomoniopsis (Gnomoniaceae, Diaporthales) from China. J. Fungi 2022, 8, 770. https://doi.org/10.3390/jof8080770

AMA Style

Wang S, Zhang Z, Liu R, Liu S, Liu X, Zhang X. Morphological and Phylogenetic Analyses Reveal Four New Species of Gnomoniopsis (Gnomoniaceae, Diaporthales) from China. Journal of Fungi. 2022; 8(8):770. https://doi.org/10.3390/jof8080770

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Wang, Shi, Zhaoxue Zhang, Rongyu Liu, Shubin Liu, Xiaoyong Liu, and Xiuguo Zhang. 2022. "Morphological and Phylogenetic Analyses Reveal Four New Species of Gnomoniopsis (Gnomoniaceae, Diaporthales) from China" Journal of Fungi 8, no. 8: 770. https://doi.org/10.3390/jof8080770

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