Appressoria-Producing Sordariomycetes Taxa Associated with Jasminum Species
by
, , and
Deecksha Gomdola
1,2
,
Eric H. C. McKenzie
3,
Kevin D. Hyde
1,2,4,
Digvijayini Bundhun
1,2 and
Ruvishika S. Jayawardena
1,2,5,* 1
School of Science, Mae Fah Luang University, Chiang Rai 57100, Thailand
2
Center of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai 57100, Thailand
3
Manaaki Whenua-Landcare Research, Auckland 1072, New Zealand
4
Innovative Institute for Plant Health, Zhongkai University of Agriculture and Engineering, Guangzhou 510225, China
5
Kyung Hee University, Seoul 02447, Republic of Korea
*
Author to whom correspondence should be addressed.
Pathogens 2023, 12(12), 1407; https://doi.org/10.3390/pathogens12121407
Submission received: 3 October 2023
/
Revised: 22 November 2023
/
Accepted: 23 November 2023
/
Published: 29 November 2023
(This article belongs to the Special Issue Filamentous Fungal Pathogens: 2nd Edition)
Abstract
:Appressoria are specialized structures formed by certain phytopathogenic fungi during the early stages of the infection process. Over the years, significant advancements have been made in understanding the formation, types, and functions of appressoria. Besides being formed primarily by fungal pathogens, many studies have reported their occurrence in other life modes such as endophytes, epiphytes, and saprobes. In this study, we observed the formation of appressoria in fungal genera that have been found associated with leaf spots and, interestingly, by a saprobic species. We used morphological descriptions and illustrations, molecular phylogeny, coalescent-based Poisson tree processes (PTP) model, inter- and intra-species genetic distances based on their respective DNA markers, and Genealogical Concordance Phylogenetic Species Recognition Analysis (GCPSR) to establish a new species (Pseudoplagiostoma jasmini), a Ciliochorella sp., and a new host record (Coniella malaysiana). The Ciliochorella sp. is reported as a saprobe, while Pseudoplagiostoma jasmini and Coniella malaysiana were found to be associated with leaf spots of Jasminum species. All three taxa produce appressoria, and this is the first study that reports the formation of appressoria by a Ciliochorella sp. and a Pseudoplagiostoma sp.
1. Introduction
Appressoria are infection pegs, mostly produced by pathogenic fungi [1]. However, since these structures are also produced by endophytes, epiphytes, and saprobes, Chethana et al. [1] proposed a general definition of appressoria as “specialized cells or adhesion structures produced by fungi from which a penetration peg emerges that pierces or enters the host tissues”. Frank [2] discovered appressoria and came up with this term when he isolated the pathogen, Colletotrichum lindemuthanium, that causes diseases of beans. Based on the various shapes and sizes, appressoria can be grouped either as single-celled or multi-cellular/compound structures [3]. Single-celled appressoria are sub-divided into proto-appressoria, hyaline, and melanized appressoria. Compound appressoria are further classified as expressoria, infection cushion, and infection plaques [1,3].
Overall, in pathogenesis, appressoria are important for the successful invasion of host plants by certain pathogenic fungi. By attaching to the host, generating turgor pressure, and facilitating penetration, these structures ensure that the pathogen can overcome physical barriers and initiate infection of the plant [1,4]. The most frequently observed appressoria among several fungal species are single-celled, occurring mostly at the tip of germ tubes, sometimes formed laterally or intercalary on hyphae [1,3]. In this study, we identified three taxa isolated from Jasminum spp. that produce appressoria.
Jasminum (Oleaceae), native to tropical and warm temperate regions in Asia, Africa, and Europe, comprises around 200 species [5], several of which are also ecologically and economically important worldwide [6]. They are cultivated as ornamental plants, but they also have traditional and horticultural significance [7,8]. The leaves, stems, bark, roots, and flowers possess beneficial properties, including aphrodisiac, antiseptic, and diuretic [9]. Leaves of J. grandiflorum are used to cure odontalgia, otorrhea, otalgia, dysmenorrhea, leprosy, ulcerative stomatitis, ulcers, and wounds, among other disorders [10,11].
Several studies have reported fungi from Jasminum species. These studies include Colletotrichum jasminigenum and C. siamense on living leaves and flowers of J. sambac in Vietnam [12]; Curvularia prasadii isolated from leaves of J. sambac [13]; Dothidea kunmingensis reported from J. nudiflorum in southwestern China [14]; and Puccinia aizazii, a rust fungus, reported on J. humile from the foothills of the Himalayan ranges, Pakistan [15].
In this study, we employed a polyphasic approach to identify the three species, which resulted in one new taxon (Pseudoplagiostoma jasmini), a Ciliochorella sp., and a new host record (Coniella malaysiana). We used morphological descriptions and illustrations, molecular phylogeny, a coalescent-based Poisson tree processes (PTP) model, inter- and intra-species genetic distances based on their respective DNA markers, and Genealogical Concordance Phylogenetic Species Recognition Analysis (GCPSR). Updated phylogenetic trees comprising all species with molecular data are provided for the three genera. We also present drawings to show the variation in conidial shapes of Pseudoplagiostoma species. All three taxa belong to Sordariomycetes and were isolated from Jasminum spp. in northern Thailand. The Ciliochorella sp. is reported from dead leaves as a saprobe, while Pseudoplagiostoma jasmini and Coniella malaysiana were found to be associated with leaf spots. Single-celled hyaline appressoria were observed in these taxa. This is the first study that reports the formation of appressoria in Ciliochorella spp. and Pseudoplagiostoma spp.
2. Materials and Methods
2.1. Collection, Isolation and Morphological Analysis
Fallen leaf specimens with leaf spots and dead leaves of Jasminum spp. were collected from different sites in Chiang Mai, Thailand, in October 2019 and 2021, during the wet season. These were carried to the laboratory in paper bags. Single-spore isolation was performed as outlined by Senanayake et al. [16]. Axenic cultures were grown on malt extract agar (MEA, 50 g/L) and incubated for three to four weeks at 25 °C. Appressoria were observed after 24–48 h, forming at the tip of the germ tubes of the conidia. Free-hand sections of conidiomata were performed to examine the morphological characters of each species. Sterilized water was used as the mounting reagent to observe the different fungal features. A Motic SMZ 168 Series stereomicroscope was used to observe their morphology. Micro-morphological characters were photographed with a Canon 750D camera (Canon, Tokyo, Japan) attached to a Nikon ECLIPSE E600 compound microscope (Nikon, Tokyo, Japan). The photo-plates were assembled in Adobe Photoshop CS6 version 2020 (Adobe Systems Inc., San Jose, CA, USA), and measurements were made using Tarosoft® Image Frame Work software (v.0.97).
2.2. Material Deposition and Reference Numbers
The holotype specimens and ex-type living cultures were deposited in the Mae Fah Luang University herbarium (MFLU) and Mae Fah Luang University Culture Collection (MFLUCC), respectively. FacesofFungi “https://www.facesoffungi.org/ (accessed on 20 November 2023)” and Index Fungorum numbers are given [17,18], with the species description updated in the GMS microfungi database “https://gmsmicrofungi.org/ (accessed on 20 November 2023)” [19]. Species identification and the establishment of the new taxon were based on Chethana et al. [20], Jayawardena et al. [21], and Maharachchikumbura et al. [22].
2.3. DNA Extraction, PCR Amplification, and Sequencing
Fresh mycelia, grown and incubated at 25 °C on MEA plates for four weeks, were scraped from the margins of colonies. Genomic DNA was extracted from these mycelia by using the Forensic DNA Kit (D3396-01, OMEGA bio-tek, Inc., Winooski, VT, USA), following the guidelines of the manufacturer. The loci of internal transcribed spacer (ITS, nuclear rDNA consisting of ITS1-5.8S-ITS2) and large subunit (28S, D1–D2 domains of nuclear 28S rDNA), and the genes for beta-tubulin (β-tub), RNA polymerase 2 (Rpb2), and translation elongation factor 1α (tef-1α) were amplified using the following primers: ITS5/ITS4 for ITS [23]; LR0R/LR5 for 28S [23]; Bt2a/Bt2b for β-tub [24]; Rpb2-5F2/7CR for Rpb2 [25,26]; and EF1-728F/EF2 for tef-1α [27,28]. The polymerase chain reaction (PCR) was carried out in an Applied Biosystems C1000 TouchTM Thermal Cycler under the following conditions: Initial denaturation at 95 °C for 3 min; denaturation at 95 °C for 45 s; annealing at 55 °C for 50 s (ITS), 52 °C for 50 s (28S), 58 °C for 1 min 30 s (β-tub, Rpb2, and tef-1α); extension at 72 °C for 1 min; and final extension at 72 °C for 10 min (number of cycles = 40). The PCR mixture, totaling 25 µL, comprised 12.5 µL of Taq mix (PROMEGA GoTaq®, Green master mix, Madison, WI, USA), 1.5 µL of genomic DNA, 1 µL of the forward and reverse primer each, and 9 µL of double-distilled water.
The results of the amplification procedure were visualized using gel electrophoresis (1.7% agarose gel) by loading the resulting amplicons and DNA fluorescent loading dye (FluoroDyeTM, SMOBIO, Seoul, Republic of Korea) in the sample wells. These amplicons were purified, and DNA was sequenced at SolGent Co. (Daejeon, Republic of Korea). Consensus sequences of the forward and reverse DNA sequence data were produced using SeqMan (DNAStar, Madison, WI, USA).
Accession numbers for all sequences deposited in the NCBI GenBank database “https://submit.ncbi.nlm.nih.gov/ (accessed on 20 November 2023)” are listed (Table 1).
2.4. Phylogenetic Analyses
A BLAST search in NCBI “https://blast.ncbi.nlm.nih.gov/ (accessed on 20 November 2023)” was conducted for our sequences, and sequence data of ITS, 28S, β-tub, Rpb2, and tef-1α from related species were retrieved from GenBank (https://www.ncbi.nlm.nih.gov/ accessed on 20 November 2023) (Table 1). Sequences were aligned using MAFFT v.7 by applying the default settings (https://mafft.cbrc.jp/alignment/server/ accessed on 20 November 2023) [29] and trimmed using trimAl [30]. Individual loci were combined using BioEdit v.7.0.5.2 [31]. Phylogenetic trees were constructed using maximum likelihood (ML), maximum parsimony (MP), and Bayesian inference (BI) methods. Both single and combined gene trees were constructed to compare the topology and taxonomic placement of each taxon.
Maximum likelihood analyses (ML-IQ) were performed in the webserver (https://iqtree.cibiv.univie.ac.at/ accessed on 20 November 2023), by selecting the default parameters and 1000 ultrafast bootstrap replicates [32]. Phylogenetic Analysis Using Parsimony (PAUP) v.4.0b10 was used to compute MP analyses [33]. A heuristic search option with the addition of 1000 random sequence additions was applied. Maxtrees and bootstrap replicates were set up to 1000. Bayesian inference analysis (MrBayes on XSEDE v.3.2.7a) was performed in the CIPRES Science Gateway v.3.3 [34,35], after implementing MrModeltest to estimate the model of evolution of individual gene regions [36]. The partition model for each gene region is given (Table 2). Markov chain Monte Carlo (MCMC) sampling with four Markov chains was used to infer posterior probabilities (PP) for 1,000,000, 5,000,000, and 2,000,000 generations for Ciliochorella, Coniella, and Pseudoplagiostoma, respectively. The tree sample frequencies were set to 100. The first 20% of the total trees were discarded as “burn in” and the remaining 80% was used to calculate posterior probabilities.
FigTree v.1.4.4 was used to display the phylogenetic trees [37], and the phylograms were edited and produced in Microsoft PowerPoint (2016).
2.5. Genealogical Concordance Phylogenetic Species Recognition Analysis (GCPSR)
The GCPSR model was applied to scrutinize any significant recombination event that occurred between the new taxon and other phylogenetically closely related species [38], as inferred by a pairwise homoplasy index (Φw) (PHI) test. The analysis was performed in SplitsTree4 by applying the LogDet transformation and splits decomposition options [39,40]. The final layout of the splitsTree graphs was produced in Microsoft PowerPoint (2016).
2.6. Poisson Tree Processes (PTP)
The coalescent-based PTP model was applied to delineate species in Pseudoplagiostoma. The analysis was computed on the Web Server (https://species.h-its.org/ptp/ accessed on 20 November 2023) [41]. The model assumes that the process of speciation is marked by a branching event in the evolutionary tree of a group of organisms, which separates the ancestral lineage into two or more new lineages. The model further assumes that the number of lineages in a group evolves according to a Poisson process, with the rate of speciation being proportional to the number of lineages. The PTP analysis was based on the concatenated ITS, 28S, β-tub, and tef-1α regions. Maximum likelihood analysis prior to computing PTP was conducted on the IQ-tree Web Server. Genetic distances were calculated in MEGA-X by applying the Kimura 2-parameter substitution model and selecting the gamma distribution and pairwise deletion options.
3. Results
3.1. Sequence Alignment and Phylogenetic Analyses
The number of strains used in the phylogenetic analyses of each genus is given (Table 3). Phylogenetic analyses from single and combined gene regions support the identification of the new species (Pseudoplagiostoma jasmini), a Ciliochorella sp., and the new host record, Coniella malaysiana. The phylogenetic trees generated from ML-IQ, MP, and BI yielded similar taxonomic placements for our isolates.
The tef-1α of Pseudoplagiostoma mangiferae was excluded from the phylogenetic analyses because when we used the BLAST tool for P. mangiferae (accession number: MK084822; 100% identity; 100% query cover; e-value = 0.0), the sequence tallied with Melanconis instead of Pseudoplagiostoma.
3.2. Analysis 1: Ciliochorella
Based on the combined ITS, 28S, and β-tub sequence data of Ciliochorella, our isolate, MFLUCC 23-0239, clusters with other Ciliochorella species and forms a distinct lineage with the larger subclade in which reside C. dipterocarpi, C. mangiferae, and C. phanericola (97% ML-IQ, 96% MP, 0.88 PP) (Figure 1).
Genealogical Concordance Phylogenetic Species Recognition Analysis (GCPSR)
The LogDet transformation and splits decomposition options were selected while configuring the PHI test. The analysis yielded a threshold over 0.05 (Φw = 1.0) for the Ciliochorella sp., indicating no significant recombination event (Figure 2).
3.3. Analysis 2: Coniella
Based on the combined ITS, 28S, Rpb2, and tef-1α sequence data of Coniella, our isolate, MFLUCC 23-0240, forms a sister clade with the ex-type of C. malaysiana with 99% ML-IQ and 100% MP bootstrap support, and 1.00 PP support (Figure 3).
3.4. Analysis 3: Pseudoplagiostoma
Based on the combined ITS, 28S, β-tub, Rpb2, and tef-1α sequences of Pseudoplagiostoma, our isolate, MFLUCC 23-0044, groups with other species of Pseudoplagiostoma and forms a sister clade with P. dipterocarpicola (MFLUCC 21-0142 and MFLUCC 21-0114) with 35% ML-IQ and 32% MP bootstrap support, and 0.95 PP support (Figure 4).
3.4.1. Genealogical Concordance Phylogenetic Species Recognition Analysis (GCPSR)
The LogDet transformation and splits decomposition options were selected while configuring the PHI test. The analysis yielded a threshold over 0.05 (Φw = 0.7314) for the new species, Pseudoplagiostoma jasmini, indicating no significant recombination (Figure 5).
3.4.2. Poisson Tree Processes
The result generated from the PTP analysis (Figure 6) is congruent with the maximum likelihood phylogram that delimits Pseudoplagiostoma jasmini as a new species (Figure 4). Genetic distances of Pseudoplagiostoma jasmini compared with its phylogenetically closely related taxa are summarized in the “note” section under Pseudoplagiostoma in the “Taxonomy” section.
4. Taxonomy
4.1. Sporocadaceae Corda [as “Sporocadeae”], Icon. Fung. (Prague) 5: 34 (1842)
This family comprises saprobic, pathogenic, as well as endophytic genera that are commonly characterized by conidia that have appendages at one or both ends. Sporocadaceae has previously been subjected to multiple taxonomic re-evaluations and classifications [42,43]. Bartaliniaceae, Discosiaceae, Pestalotiopsidaceae, and Robillardaceae were previously treated as synonyms of Sporocadaceae [43,44,45].
4.1.1. Ciliochorella Syd., in Sydow & Mitter, Annls Mycol. 33(1/2): 62 (1935)
Type species—Ciliochorella mangiferae Syd.
Ciliochorella (Sporocadaceae, Amphisphaeriales, Xylariomycetidae) [42,43,46,47] was established by Sydow and Mitter [48]. There are ten species in Index Fungorum [18] and nine species in Species Fungorum [49]. Among these, only five Ciliochorella species have sequence data for one or more gene loci. Ciliochorella species comprise saprobic taxa that have been reported from India, Japan, South America, and Thailand [42,50,51,52]. Our isolate is also reported in its saprobic mode.
The genus is characterized by cylindrical, straight, or slightly curved conidia that are eu-septate, usually bearing two to three or more tubular apical appendages and a single basal appendage.
4.1.2. Ciliochorella sp. Gomdola, K.D. Hyde & Jayaward.
Saprobic on the leaves of Jasminum sp. Sexual morph: Not observed. Asexual morph: Coelomycetous. Conidiomata in cross-section 1000–1100 μm diam., 370–380 μm high ( = 1042 × 373 μm, n = 5), acervulus, semi-immersed, carbonaceous, solitary, uniloculate, black. Conidiomata wall 40–53 μm diam. ( = 46.7 μm, n = 10), consisting of several layers of pseudoparenchymatous cells of textura angularis, outer layers dark brown, inner layers pale brown to hyaline. Conidiophores indistinct, often reduced to conidiogenous cells. Conidiogenous cells phialidic, (5.2–)6.7–8.5(–9.5) × 1.9–2.8 μm ( = 7.4 × 2.4 μm, n = 10), formed from the inner-most layer of the wall, hyaline to pale brown, ampulliform, smooth-walled, proliferating enteroblastically. Conidia 11–15 × 2.4–3.8 μm ( = 12.9 × 3.3 μm, n = 50) (excluding basal cell), hyaline to pale brown, guttulate, 1-euseptate, smooth-walled, allantoid to sub-cylindrical, or sub-falcate to reniform, apex sometimes broadly obtuse, tapering towards a slightly curved base with a hyaline obconic basal cell 2.8–4.5 μm long ( = 3.6 μm, n = 30); conidia bearing 2 apical and 1 basal appendage. Appendages tubular, filiform, flexuous, apical appendages (6.5–)12.5–18.5 μm long ( = 16.5 μm, n = 50), basal appendage (2.5–)4–6.5(–8) μm long ( = 5.4 μm, n = 50). Appressorium 20 × 18.5 μm, single-celled, cordate to irregular-shaped, hyaline.
Culture characteristics: Colonies on MEA reaching approximately 20 mm diam. after 14 days of incubation at 25 °C, elevation flat, forming concentric rings with an entire margin, mycelium white.
Material examined: Thailand, Chiang Mai Province, Doi Lo district, on fallen dead leaves of Jasminum sp. (Oleaceae), 15 October 2019, D. Gomdola, DG314 (MFLU 23-0388), living culture MFLUCC 23-0239.
GenBank accession numbers: ITS = OR610581, 28S = OR610582.
Notes: Ciliochorella sp. (MFLUCC 23-0239) groups with other Ciliochorella species and forms a separate lineage with the larger subclade in which reside C. dipterocarpi, C. mangiferae, and C. phanericola (97% ML-IQ, 96% MP, 0.88 PP) (Figure 1). The conidial features match the morphological species concept of Ciliochorella. We compared the morphology of Ciliochorella sp. (MFLUCC 23-0239) with that of its phylogenetically closely related, C. phanericola. The conidial shape, color, and size of Ciliochorella sp. (MFLUCC 23-0239) and C. phanericola are mostly similar (Table 4). However, the conidia of Ciliochorella sp. (MFLUCC 23-0239) are 1-euseptate, while those of C. phanericola are 2-septate. Both the apical and basal appendages of Ciliochorella sp. (MFLUCC 23-0239) are shorter than those of C. phanericola (Table 4). The growth rate of Ciliochorella sp. (MFLUCC 23-0239) (2 cm after 14 days) is slower than that of C. phanericola (2.5 cm after 7 days), both grown on MEA and incubated at 25 °C [51]. In addition, appressoria were not observed in C. phanericola [51].
Excluding gaps in our aligned untrimmed dataset, in comparison of the inter-species genetic distance of Ciliochorella sp. (MFLUCC 23-0239) and C. phanericola, a difference of 0.34% was seen across ITS (533 nucleotides), but no difference was observed across 28S (868 nucleotides). We were unable to compare the differences across β-tub as Ciliochorella sp. (MFLUCC 23-0239) lacks sequence data for the gene region. Despite several trials using different amplification conditions, we were unable to obtain sequence data for β-tub. Therefore, coupled with morphological description and multi-locus phylogenetic analyses, a PHI test was also conducted to support the taxonomic placement of our isolate (MFLUCC 23-0239). The PHI test of the combined ITS and 28S yielded a threshold exceeding 0.05 (Φw = 1.0), suggesting that no recombination event has occurred.
Nevertheless, despite the PHI test result, we suggest establishing our isolate as Ciliochorella sp. instead of identifying it as a new species due to the lack of sequence data. Further studies focusing on the collection of more Ciliochorella taxa and providing sequence data for protein-coding gene regions (β-tub, Rpb2, tef-1α) will yield better resolution in the phylogenetic trees and contribute to proper species identification (Figure 7).
4.2. Schizoparmaceae Rossman, D.F. Farr & Castl. [as “Schizoparmeaceae”], Mycoscience 48(3): 137 (2007)
Schizoparmaceae was introduced to accommodate Schizoparme (sexual morph reported), Coniella, and Pilidiella (asexual morph reported) [53,54]. Alvarez et al. [55] revised the family and synonymized Pilidiella and Schizoparme under Coniella. Species in this family occur in tropical and temperate areas as phytopathogens as well as saprobes and endophytes [43,56].
4.2.1. Coniella Höhn., Ber. Dt. Bot. Ges. 36(7): 316 (1918)
Type species—Coniella pulchella Höhn.
Coniella (Schizoparmaceae, Diaporthales, and Diaporthomycetidae) [43,46,47] was established by Höhnel [57]. There are 64 species in Index Fungorum [18] and 58 species in Species Fungorum [49]. Of these, 42 Coniella species have sequence data for one or more gene regions. The genus is primarily characterized by erumpent, brown to black ascomata or conidiomata, and hyaline conidia that become pigmented upon maturation [58,59].
4.2.2. Coniella malaysiana L.V. Alvarez & Crous, in Alvarez, Groenewald & Crous, Stud. Mycol. 85: 21 (2016)
Index Fungorum number: IF 817823, Facesoffungi number: FoF 14882
Associated with leaf spots of Jasminum sp. Leaf spots irregular or oval to elongated, brown, surrounded by a dark brown to black margin, outermost surrounding reddish brown. Sexual morph: Not observed. Asexual morph: Coelomycetous. Conidiomata 135–140 μm diam., 100–130 μm high ( = 139 × 114 μm, n = 5), pycnidial, semi-immersed, sometimes erumpent, solitary, scattered or gregarious, uniloculate, globose to subglobose, black. Conidiomata wall 13.5–24.5(–28) μm diam. ( = 18.6 μm, n = 10), consisting of 3–4 layers of thick-walled pseudoparenchymatous cells of textura angularis, outer layers dark brown, inner layer pale brown to hyaline. Conidiophores 6.9–15 μm long ( = 11.2 μm, n = 10), straight to flexuous, cylindrical to ampulliform or oblong, hyaline, aseptate, unbranched, sometimes reduced to conidiogenous cells. Conidiogenous cells enteroblastic, phialidic, 6.9–13 × 2.1–3.4 μm ( = 10.7 × 2.6 μm, n = 10), hyaline, cylindrical or ampulliform, guttulate, smooth-walled. Conidia (7.5–)8.2–13.1 × 4–5 μm ( = 10.6 × 4.1 μm, n = 50), hyaline when immature, becoming pale to dark brown upon maturation, guttulate, aseptate, smooth, thick-walled, 0.4–1.5 μm diam. ( = 0.75 μm, n = 30), fusiform to truncate to sub-ellipsoidal, sometimes obovoid, wider in the middle, tapering towards a slightly curved apex and base, often with a prominent protruding basal hilum. Appressoria 19–23 × 9–15 μm ( = 20.9 × 12 μm, n = 2), single-celled, sub-ellipsoidal to irregular-shaped, hyaline.
Culture characteristics: Colonies on MEA reaching approximately 20 mm diam. after 7 days of incubation at 25 °C, elevation flat or raised, round with raised margin, forming concentric rings, mycelium dense and aerial, white.
Material examined: Thailand, Chiang Mai Province, Omkoi district, Yang Piang sub-district, associated with leaf spots of Jasminum sp. (Oleaceae), 16 October 2019, D. Gomdola, DG392 (MFLU 23-0389), living culture MFLUCC 23-0240.
Hosts and Distribution: Leaves of Corymbia torelliana in Malaysia [55], leaves of Jasminum sp. in Thailand (this study).
GenBank accession numbers: ITS = OR608286, 28S = OR608334, Rpb2 = OR601568 and tef-1α = OR601569.
Notes: Our collection shares similar morphological characters with those of the ex-type, C. malaysiana (CBS 141598) [55]. Our strain and C. malaysiana (CBS 141598) have hyaline to brown, aseptate conidia with guttules [55]. Conidial sizes are mostly similar (Table 5). The conidial length-to-width ratio of our isolate is 2.6, and that of C. malaysiana (CBS 141598) is 2.5. Other morphological similarities and differences between the two strains of C. malaysiana are given (Table 5).
In the phylogenetic analyses of the combined ITS, 28S, Rpb2, and tef-1α, our isolate is sister to the ex-type of C. malaysiana (99% ML-IQ, 100% MP, 1.00 PP) (Figure 3). Excluding gaps in our aligned untrimmed dataset, upon comparison of the intra-species genetic distance between our strain and the ex-type of C. malaysiana, the following differences were observed: 0.55% across ITS (553 nucleotide base pairs, bp), 0.12% across 28S (827 bp), 0.26% across Rpb2 (767 bp), but 2.4% across tef-1α (295 bp).
Based on morphology and multigene phylogenetic analyses, we identify our strain as a new host record of Coniella malaysiana, associated with leaf spots of Jasminum sp. in northern Thailand (Figure 8).
4.3. Pseudoplagiostomataceae Cheew., M.J. Wingf. & Crous [as “Pseudoplagiostomaceae”], in Cheewangkoon et al., Fungal Diversity 44: 95 (2010)
Pseudoplagiostomataceae, a monotypic family, was introduced to accommodate Pseudoplagiostoma, a genus that is morphologically similar but phylogenetically distinct to Plagiostoma [60].
4.3.1. Pseudoplagiostoma Cheew., M.J. Wingf. & Crous, in Cheewangkoon et al., Fungal Diversity 44: 96 (2010)
Type species—Pseudoplagiostoma eucalypti Cheewangkoon, M.J. Wingf. & Crous
Pseudoplagiostoma (Pseudoplagiostomataceae, Diaporthales, and Diaporthomycetidae) was established by Cheewangkoon et al. [60], with the introduction of three species: P. eucalypti, P. oldii, and P. variabile. There are 13 species in Index Fungorum [18] and nine species in Species Fungorum [49], and all 13 species have sequence data for one or more gene loci. The nomenclature of Pseudoplagiostoma reflects the morphological similarities with Plagiostoma (Gnomoniaceae, Diaporthales). Pseudoplagiostoma species have both sexual and asexual morphs [60]. Their sexual morph is characterized by perithecial, immersed, globose or elliptical ascomata, subcylindrical unitunicate asci (J-), and hyaline, ellipsoidal, and elongated ascospores, usually with a median septum and hyaline appendages at the apex and base (Figure 9). Their asexual morph consists of acervular or pycnidial conidiomata, and hyaline, smooth-walled, aseptate conidia (Figure 9) [60].
4.3.2. Pseudoplagiostoma jasmini Gomdola, K.D. Hyde & Jayaward., sp. nov.
Index Fungorum number: IF 900131, Facesoffungi number: FoF 14104
Etymology: The specific epithet refers to the host genus, Jasminum, from which the species was isolated.
Holotype: MFLU 23-0068
Associated with leaf spots of Jasminum grandiflorum. Leaf spots irregular, pale to medium brown, surrounded by a dark brown to black margin. Sexual morph: Not observed. Asexual morph: Coelomycetous. Conidiomata (145–)150–230(–240) μm diam., (135–)140–200 μm high ( = 184 × 171 μm, n = 20), pycnidial, semi-immersed, solitary, scattered, uniloculate, globose to subglobose, pale brown, surrounded with black margin. Conidiomata wall (19–)22–42(–46) μm thick ( = 28 μm, n = 15), consisting of 3–4 layers of thick-walled pseudoparenchymatous cells of textura angularis, outer layers dark brown to black, inner layers pale brown to hyaline. Conidiophores indistinct, often reduced to conidiogenous cells. Conidiogenous cells phialidic, (6.8–)7.7–13.7(–15.6) × 1.6–2.4(–3.0) μm ( = 10.7 × 2.1 μm, n = 10), hyaline, cylindrical or clavate, guttulate, smooth-walled, proliferating enteroblastically. Conidia (11.8–)14–22 × (5.2–)6.5–11 μm (( = 18.5 × 9.5 μm, n = 50), hyaline, guttulate, 0–2-septate, smooth, wall (0.5–)0.6–1.3 μm thick ( = 0.8 μm, n = 50), cylindrical to truncate or ellipsoidal, elongated, reniform, pyriform or obovoid, apex broadly obtuse, tapering towards a slightly curved base, often with a prominent protruding hilum. Appressorium 9.6 × 7.2 μm long, single-celled, sub-ellipsoidal to obovoid or subglobose or irregular-shaped, hyaline.
Culture characteristics: Colonies on MEA reaching approximately 20 mm diam. after 14 days of incubation at 25 °C, immature with white mycelium, elevation flat or raised, becoming aerial dense and olivaceous brown, filamentous with an undulate margin when aged.
Material examined: Thailand, Chiang Mai Province, Doi Inthanon National Park, Kew Mae Pan nature trail, on fallen leaves of Jasminum grandiflorum (Oleaceae), 20 October 2021, D. Gomdola, DG-PSEU (MFLU 23-0068, holotype), ex-type living culture MFLUCC 23-0044.
GenBank accession numbers: ITS = OQ786078, 28S = OQ786079, β-tub = OQ850148 and tef-1α = OQ850145.
Notes: Pseudoplagiostoma jasmini groups with other species of Pseudoplagiostoma and forms a sister clade with P. dipterocarpicola (MFLUCC 21-0142 and MFLUCC 21-0114) with 35% ML-IQ, 32% MP, and 0.95 PP support (Figure 4). The features are congruent with the morphological species concept of Pseudoplagiostoma [60].
Pseudoplagiostoma jasmini varies substantially in conidial shape (Figure 9). Conidia of P. jasmini are longer than those of P. dipterocarpicola (MFLUCC 21-0142) (Table 6). The conidial length-to-width ratio of P. jasmini is 2.0, whereas that of P. dipterocarpicola is 2.7.
Excluding gaps in our aligned untrimmed dataset, in pairwise nucleotide comparisons of P. jasmini and P. dipterocarpicola (MFLUCC 21-0142), the following differences were observed: 5.76% across ITS (543 nucleotide base pairs, bp), 1.86% across 28S (818 bp), 21.1% across β-tub (448 bp), and 43.7% across tef-1α (164 bp). The inter-species genetic distances (%) grouped according to the PTP result are provided (Table 7).
Based on the guidelines of Chethana et al. [20], Jayawardena et al. [21], and Maharachchikumbura et al. [22] for introducing new species, we describe P. jasmini as a new species. Despite its support values (35% ML-IQ, 32% MP, and 0.95 PP), we establish P. jasmini as a new taxon, considering the formation of one or two septa in the conidia, a feature lacking in all other Pseudoplagiostoma species; all Pseudoplagiostoma spp. have aseptate conidia. Besides morphology and multigene phylogenetic analyses, we included GCPSR and PTP analyses as further evidence to support the distinct species status of Pseudoplagiostoma jasmini (Figure 10).
5. Discussion
In pathology, appressoria are infection structures generated to invade plant tissues [1,4,69,70]. Basically, they are penetration pegs [1]. Appressoria are not solely confined to fungal pathogens. They also occur in endophytes [71,72], epiphytes [3,73,74], and saprobes [75]. In this study, we establish one new species (Pseudoplagiostoma jasmini), a Ciliochorella sp., and a new host record (Coniella malaysiana) that produce single-celled, irregular-shaped, hyaline appressoria. The Ciliochorella sp. is reported from dead leaves as a saprobe, while P. jasmini and C. malaysiana were found associated with leaf spots. In our study, pathogenicity tests were not performed. Therefore, the occurrence of appressoria in C. malaysiana and P. jasmini reveals their pathogenic and possibly endophytic nature. Certain fungi can switch their lifestyles from endophyte to saprobe and become pathogenic under suitable conditions [76]. We hypothesize that, under favorable circumstances, C. malaysiana, P. jasmini, and the saprobic Ciliochorella sp. may develop phytopathogenic traits and cause diseases. Given that appressoria are produced by fungi in various life modes, as mentioned above, it is of dire need to record their occurrences and diversity from different hosts.
This is the first study that reports the formation of appressoria in a Ciliochorella sp. and a Pseudoplagiostoma sp., but appressoria have previously been observed in Coniella musaiaensis [77]. The primary function of appressoria produced by endophytes is to cross from one cell to another [3]. For saprobes to obtain their nutrients, a living host is not a requisite. Thus, the formation of an appressorium in saprobic fungi is probably a result of adaptation while in their endophytic life mode [4,78,79,80].
Species delimitation is essential to developing a proper comprehension of the biology, geography, host-fungal association, and life modes of individual fungal taxa, as well as their respective roles in the ecosystem [20]. The taxonomy of certain Pseudoplagiostoma species yielded low support values when constructing the phylograms (ML-IQ, MP, PP). Despite the support values for the placement of P. jasmini, we establish the latter as a novel taxon as there are significant differences in the conidial morphology. All Pseudoplagiostoma taxa, except P. jasmini, have aseptate conidia. Apart from P. jasmini, all other species of Pseudoplagiostoma are cryptic, sharing similar morphologies such as shape, color, and size. Therefore, coupled with morphology and phylogenetic analyses, we employed the Genealogical Concordance Phylogenetic Species Recognition Analysis (GCPSR) to infer the species boundaries in Pseudoplagiostoma [38]. Furthermore, we advocate the use of the coalescent-based Poisson tree processes (PTP) model to compare the inter- and intra-species genetic distances in Pseudoplagiostoma [41].
Many Sordariomycetes taxa are demarcated based on ITS, 28S, small subunit (18S, nuclear rDNA), β-tub, tef-1α, and Rpb2 loci [43]. Only five Ciliochorella spp., but all Pseudoplagiostoma spp., have molecular data for one or more gene loci. A few Ciliochorella spp. lack sequence data for β-tub. The collection and examination of more Ciliochorella species, with the addition of more gene regions in the phylogenetic analyses, as applied in the analysis and delineation of other Sordariomycetes taxa, would lead to a better phylogenetic resolution and taxonomic placement of each species. Based on high-throughput sequencing, Baldrian et al. [81] suggested that the fungal diversity is around 6.28 million species worldwide but with only 1.08 million published species. A probable reason for the smaller number of Ciliochorella spp. and Pseudoplagiostoma spp. might be because they occur in poorly studied hosts and countries [82]. Northern Thailand is rich in fungal biodiversity [82]. Undoubtedly, further exploration of the fungal diversity in this area as well as other hotspots worldwide will reveal a higher diversity of these two and other genera [83].
Author Contributions
Conceptualization, D.G., E.H.C.M. and D.B.; formal analysis, D.G.; methodology, D.G.; software, D.G.; supervision, E.H.C.M., K.D.H. and R.S.J.; validation, D.G. and D.B.; writing—original draft, D.G.; writing—review and editing, E.H.C.M., K.D.H., D.B. and R.S.J. All authors have read and agreed to the published version of the manuscript.
Funding
This research was funded by MFU student scholarship 2020; The National Science and Technology Development Agency (NSTDA: Project No. P-19-52624), under the National Park Permission No. 0907.4/8218 and No. 0907.4/19647; National Research Council of Thailand (NRCT) (grant no. N42A650547), project entitled “Total fungal diversity in a given forest area with implications towards species numbers, chemical diversity, and biotechnology”; and the Mushroom Research Foundation (MRF).
Institutional Review Board Statement
Not applicable.
Informed Consent Statement
Not applicable.
Data Availability Statement
All data generated or analyzed during this study are included in this published article.
Acknowledgments
We thank Shaun Pennycook for suggesting and validating the nomenclature of the new species. R. S. Jayawardena thanks the Eminent scholar offered by Kyun Hee University.
Conflicts of Interest
The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.
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Figure 1.
Maximum likelihood phylogram based on the combined ITS, 28S, and β-tub matrices of Ciliochorella. Bootstrap support values (ML-IQ ≥ 80%), maximum parsimony (MP ≥ 80%), and Bayesian posterior probabilities (PP ≥ 0.80) are given above the branches or at the nodes as ML-IQ/MP/PP. Hyphen (-) indicates bootstrap support values below 80% for ML-IQ and MP, and posterior probabilities below 0.80. Allelochaeta acuta (CBS 144168 and CPC 19289) and Discosia ravennica (MFLU 18-0131) are the outgroup taxa. Ex-type and reference strains are in bold, and our isolate is in red.
Figure 1.
Maximum likelihood phylogram based on the combined ITS, 28S, and β-tub matrices of Ciliochorella. Bootstrap support values (ML-IQ ≥ 80%), maximum parsimony (MP ≥ 80%), and Bayesian posterior probabilities (PP ≥ 0.80) are given above the branches or at the nodes as ML-IQ/MP/PP. Hyphen (-) indicates bootstrap support values below 80% for ML-IQ and MP, and posterior probabilities below 0.80. Allelochaeta acuta (CBS 144168 and CPC 19289) and Discosia ravennica (MFLU 18-0131) are the outgroup taxa. Ex-type and reference strains are in bold, and our isolate is in red.
Figure 2.
Split graph derived from the PHI analysis, generated for Ciliochorella. Our isolate is in red.
Figure 2.
Split graph derived from the PHI analysis, generated for Ciliochorella. Our isolate is in red.
Figure 3.
Maximum likelihood phylogram based on the combined ITS, 28S, Rpb2, and tef-1α matrices of Coniella. Bootstrap support values (ML-IQ ≥ 80%) and maximum parsimony (MP ≥ 80%), and Bayesian posterior probabilities (PP ≥ 0.80) are given above the branches or at the nodes as ML-IQ/MP/PP. Hyphen (-) indicates bootstrap support values below 80% for ML-IQ and MP, and posterior probabilities below 0.80. Melanconiella hyperopta (CBS 132231 and CBS 131696) are selected as outgroups. Ex-type and reference strains are in bold, and our isolate is in red.
Figure 3.
Maximum likelihood phylogram based on the combined ITS, 28S, Rpb2, and tef-1α matrices of Coniella. Bootstrap support values (ML-IQ ≥ 80%) and maximum parsimony (MP ≥ 80%), and Bayesian posterior probabilities (PP ≥ 0.80) are given above the branches or at the nodes as ML-IQ/MP/PP. Hyphen (-) indicates bootstrap support values below 80% for ML-IQ and MP, and posterior probabilities below 0.80. Melanconiella hyperopta (CBS 132231 and CBS 131696) are selected as outgroups. Ex-type and reference strains are in bold, and our isolate is in red.
Figure 4.
Maximum likelihood phylogram based on the combined ITS, 28S, β-tub, Rpb2, and tef-1α matrices of Pseudoplagiostoma. Bootstrap support values (ML-IQ ≥ 30%) and maximum parsimony (MP ≥ 30%), and Bayesian posterior probabilities (PP ≥ 0.80) are given above the branches or at the nodes as ML-IQ/MP/PP. Hyphen (-) indicates bootstrap support values below 30% for ML-IQ and MP, and posterior probabilities below 0.80. Apoharknessia eucalypti (CBS 142518), A. eucalyptorum (CBS 142519), and Apoharknessia insueta (CBS 111377 and CBS 114575) are the outgroup taxa. Ex-type and reference strains are in bold, and the new taxon is in bold red.
Figure 4.
Maximum likelihood phylogram based on the combined ITS, 28S, β-tub, Rpb2, and tef-1α matrices of Pseudoplagiostoma. Bootstrap support values (ML-IQ ≥ 30%) and maximum parsimony (MP ≥ 30%), and Bayesian posterior probabilities (PP ≥ 0.80) are given above the branches or at the nodes as ML-IQ/MP/PP. Hyphen (-) indicates bootstrap support values below 30% for ML-IQ and MP, and posterior probabilities below 0.80. Apoharknessia eucalypti (CBS 142518), A. eucalyptorum (CBS 142519), and Apoharknessia insueta (CBS 111377 and CBS 114575) are the outgroup taxa. Ex-type and reference strains are in bold, and the new taxon is in bold red.
Figure 5.
Split graph derived from the PHI analysis, generated for Pseudoplagiostoma. The novel species is in bold red.
Figure 5.
Split graph derived from the PHI analysis, generated for Pseudoplagiostoma. The novel species is in bold red.
Figure 6.
Results generated from the PTP analysis of Pseudoplagiostoma. The analysis was based on the ML-IQ topologies of the concatenated ITS, 28S, β-tub, and tef-1α matrices. Groups of species are denoted by colored branches, with blue-colored branches indicating that they are different species, and red-colored branches representing different strains of the same species. Numbers near the nodes are posterior probabilities. The new taxon is given in bold red.
Figure 6.
Results generated from the PTP analysis of Pseudoplagiostoma. The analysis was based on the ML-IQ topologies of the concatenated ITS, 28S, β-tub, and tef-1α matrices. Groups of species are denoted by colored branches, with blue-colored branches indicating that they are different species, and red-colored branches representing different strains of the same species. Numbers near the nodes are posterior probabilities. The new taxon is given in bold red.
Figure 7.
Ciliochorella sp. (MFLUCC 23-0239) (a) Leaf specimen. (b) Close up of conidiomata on a leaf of Jasminum sp. (c) Section through conidioma. (d,e) Conidiomata wall. (f–i) Conidiophores, conidiogenous cells and developing conidia. (j–n) Immature and mature conidia with appendages. (o) Germinated conidium (p,q) top (left) and reverse (right) of colonies on MEA after 7 and 14 days of incubation, respectively. (r) Appressorium. Scale bars: (b) = 1 mm, (c) = 100 μm, (e,h,j–o) = 10 μm, (d,r) = 20 μm, (f,g,i) = 5 μm.
Figure 7.
Ciliochorella sp. (MFLUCC 23-0239) (a) Leaf specimen. (b) Close up of conidiomata on a leaf of Jasminum sp. (c) Section through conidioma. (d,e) Conidiomata wall. (f–i) Conidiophores, conidiogenous cells and developing conidia. (j–n) Immature and mature conidia with appendages. (o) Germinated conidium (p,q) top (left) and reverse (right) of colonies on MEA after 7 and 14 days of incubation, respectively. (r) Appressorium. Scale bars: (b) = 1 mm, (c) = 100 μm, (e,h,j–o) = 10 μm, (d,r) = 20 μm, (f,g,i) = 5 μm.
Figure 8.
Coniella malaysiana (MFLUCC 23-0240) (a) Herbarium specimen with leaf spots. (b) Close up of conidiomata on a leaf of Jasminum sp. (c) Section through a conidioma. (d) Conidioma wall. (e–h) Conidiophores, conidiogenous cells, and developing conidia. (i–l) Immature and mature conidia. (m) Germinated conidia (n) Top (upper) and reverse (lower) of colony on MEA after 5 and 14 days of incubation. (o,p) Appressoria. Scale bars: (b) = 500 μm, (c) = 50 μm, (d,e,m,o,p) = 10 μm, (f–l) = 5 μm.
Figure 8.
Coniella malaysiana (MFLUCC 23-0240) (a) Herbarium specimen with leaf spots. (b) Close up of conidiomata on a leaf of Jasminum sp. (c) Section through a conidioma. (d) Conidioma wall. (e–h) Conidiophores, conidiogenous cells, and developing conidia. (i–l) Immature and mature conidia. (m) Germinated conidia (n) Top (upper) and reverse (lower) of colony on MEA after 5 and 14 days of incubation. (o,p) Appressoria. Scale bars: (b) = 500 μm, (c) = 50 μm, (d,e,m,o,p) = 10 μm, (f–l) = 5 μm.
Figure 9.
Conidial (a,d–o) and ascospores (b,c) morphology of Pseudoplagiostoma spp. (a) P. eucalypti (asexual morph) (b,c) P. eucalypti (ascospores with apical and basal appendages) (d) P. oldii (e) P. dipterocarpi (f) P. variabile (g) P. corymbiicola (h) P. corymbiae (i) P. myracrodruonis (j) P. mangiferae (k) P. dipterocarpicola (l) P. castaneae (m) P. alsophilae (n) P. bambusae (o) P. machili. Scale bars = 15 µm. (Redrawn from Cheewangkoon et al. [60]; Crous et al. [61,62]; Suwannarach et al. [63]; Bezerra et al. [64]; Phookamsak et al. [65]; Mu et al. [66]; Tang et al. [67]; Zhang et al. [68]).
Figure 9.
Conidial (a,d–o) and ascospores (b,c) morphology of Pseudoplagiostoma spp. (a) P. eucalypti (asexual morph) (b,c) P. eucalypti (ascospores with apical and basal appendages) (d) P. oldii (e) P. dipterocarpi (f) P. variabile (g) P. corymbiicola (h) P. corymbiae (i) P. myracrodruonis (j) P. mangiferae (k) P. dipterocarpicola (l) P. castaneae (m) P. alsophilae (n) P. bambusae (o) P. machili. Scale bars = 15 µm. (Redrawn from Cheewangkoon et al. [60]; Crous et al. [61,62]; Suwannarach et al. [63]; Bezerra et al. [64]; Phookamsak et al. [65]; Mu et al. [66]; Tang et al. [67]; Zhang et al. [68]).
Figure 10.
Pseudoplagiostoma jasmini (MFLUCC 23-0044, ex-holotype) (a) Leaf of Jasminum grandiflorum with spots. (b) Appearance of conidiomata on leaves. (c) Close up of conidioma on substrate. (d) Section through a conidioma. (e–h) Conidiophores, conidiogenous cells, and developing conidia. (i–t) Conidia with guttules, septa and protruding hilum. (u–v) Top (left) and reverse (right) of colonies on MEA after 7 and 14 days of incubation, respectively. (w) Appressorium. Scale bars: (b) = 1 mm, (c) = 200 μm, (d) = 100 μm, (e–t) = 10 μm, (w) = 20 μm.
Figure 10.
Pseudoplagiostoma jasmini (MFLUCC 23-0044, ex-holotype) (a) Leaf of Jasminum grandiflorum with spots. (b) Appearance of conidiomata on leaves. (c) Close up of conidioma on substrate. (d) Section through a conidioma. (e–h) Conidiophores, conidiogenous cells, and developing conidia. (i–t) Conidia with guttules, septa and protruding hilum. (u–v) Top (left) and reverse (right) of colonies on MEA after 7 and 14 days of incubation, respectively. (w) Appressorium. Scale bars: (b) = 1 mm, (c) = 200 μm, (d) = 100 μm, (e–t) = 10 μm, (w) = 20 μm.
Table 1.
GenBank accession numbers of sequences used in the phylogenetic analyses. Ex-type and reference strains are denoted with an ‘*’. Our isolates are in blue.
Table 1.
GenBank accession numbers of sequences used in the phylogenetic analyses. Ex-type and reference strains are denoted with an ‘*’. Our isolates are in blue.
| Species | Isolate Number | ITS | 28S | β-tub | Rpb2 | tef-1α |
|---|---|---|---|---|---|---|
| Allelochaeta acuta | CBS 144168 * | MH822973 | MH823023 | MH823160 | N/A | N/A |
| Allelochaeta acuta | CPC 19289 | MH822975 | MH823025 | MH823162 | N/A | N/A |
| Apoharknessia eucalypti | CBS 142518 * | MG934432 | MN162172 | MG934505 | N/A | N/A |
| Apoharknessia eucalyptorum | CBS 142519 * | KY979752 | KY979807 | KY979919 | N/A | N/A |
| Apoharknessia insueta | CBS 111377 * | JQ706083 | AY720814 | N/A | N/A | MN271820 |
| Apoharknessia insueta | CBS 114575 | MN172402 | MN172370 | N/A | N/A | MN271821 |
| Ciliochorella castaneae | NBRC 104545 | N/A | AB433277 | N/A | N/A | N/A |
| Ciliochorella castaneae | NBRC 104546 | N/A | AB433278 | N/A | N/A | N/A |
| Ciliochorella dipterocarpi | MFLUCC 22-0132 * | OP912991 | OP912990 | OQ127637 | N/A | N/A |
| Ciliochorella dipterocarpi | MFLUCC 23-0023 | OQ657982 | OQ657981 | OQ657298 | N/A | N/A |
| Ciliochorella sp. | MFLUCC 23-0239 | OR610581 | OR610582 | N/A | N/A | N/A |
| Ciliochorella mangiferae | MFLUCC 12-0310 | KF827444 | KF827445 | KF827478 | N/A | N/A |
| Ciliochorella phanericola | MFLUCC 14-0984 * | KX789680 | KX789681 | KX789682 | N/A | N/A |
| Coniellaafricana | CBS 114133 * | AY339344 | AY339293 | N/A | KX833421 | KX833600 |
| Coniella australiensis | IMI 261318 | N/A | N/A | N/A | N/A | N/A |
| Coniella castaneicola | LGZ2 | MW672530 | MW856810 | N/A | N/A | N/A |
| Coniella crousii | NFCCI 2213 | HQ264189 | N/A | N/A | N/A | N/A |
| Coniella diospyri | CBS 145071 * | MK047439 | MK047489 | N/A | MK047543 | MK047562 |
| Coniella diplodiella | CBS 111858 * | AY339323 | KX833335 | N/A | KX833423 | KX833603 |
| Coniella diplodiella | CBS 111857 | AY339331 | AY339286 | N/A | N/A | AY339357 |
| Coniella diplodiopsis | CBS 590.84 * | AY339334 | AY339288 | N/A | N/A | AY339359 |
| Coniella diplodiopsis | CBS 10923 | AY339332 | AY339287 | N/A | KX833440 | KX833624 |
| Coniella duckerae | CBS 142045 * | KY924929 | N/A | N/A | N/A | N/A |
| Coniella erumpens | CBS 52378 * | KX833535 | KX833361 | N/A | KX833446 | KX833630 |
| Coniella eucalyptigena | CBS 139893 * | KR476725 | N/A | N/A | N/A | N/A |
| Coniella eucalyptorum | CBS 112640 * | AY339338 | AY339290 | N/A | KX833452 | KX833637 |
| Coniella eucalyptorum | CBS 114852 | KX833556 | KX833380 | N/A | KX833464 | KX833652 |
| Coniella ferreirense | CBS 224.80 * | MH861257 | MH873026 | N/A | N/A | N/A |
| Coniella fici | MFLU 18-2578 * | MW114356 | MW114417 | N/A | N/A | N/A |
| Coniella fici | MFLU 18-2579 | MW114357 | MW114418 | N/A | N/A | N/A |
| Coniella fragariae | CBS 17249 * | AY339317 | AY339282 | N/A | KX833472 | KX833663 |
| Coniella fragariae | CBS 45468 | KX833571 | KX833393 | N/A | KX833477 | KX833670 |
| Coniella fusiformis | CBS 141596 * | KX833576 | KX833397 | N/A | KX833481 | KX833674 |
| Coniella granati | CBS 132860 | KX833577 | KX833400 | N/A | KX833484 | KX833677 |
| Coniella heterospora | FMR: 15231 | LT800501 | LT800500 | N/A | LT800502 | LT800503 |
| Coniella hibisci | CBS 109757 * | KX833589 | N/A | N/A | N/A | KX833689 |
| Coniella javanica | CBS 45568 * | KX833583 | KX833403 | N/A | KX833489 | KX833683 |
| Coniella koreana | CBS 14397 | KX833584 | AF408378 | N/A | KX833490 | KX833684 |
| Coniella lanneae | CBS 141597 * | KX833585 | KX833404 | N/A | KX833491 | KX833685 |
| Coniella limoniformis | CBS 111021 * | KX833586 | KX833405 | N/A | KX833492 | KX833686 |
| Coniella lustricola | DAOMC 251731 * | MF631778 | MF631799 | N/A | MF651900 | MF651899 |
| Coniella lustricola | DAOMC 251734 | MF631781 | MF631802 | N/A | N/A | N/A |
| Coniella macrospora | CBS 52473 * | KX833587 | AY339292 | N/A | KX833493 | KX833687 |
| Coniella malaysiana | CBS 141598 * | KX833588 | KX833406 | N/A | KX833494 | KX833688 |
| Coniella malaysiana | MFLUCC 23-0240 | OR608286 | OR608334 | N/A | OR601568 | OR601569 |
| Coniella musaiaensis | AR3534 | N/A | N/A | N/A | N/A | N/A |
| Coniella nicotianae | CBS 87572 * | KX833590 | KX833407 | N/A | KX833495 | KX833690 |
| Coniella nigra | CBS 16560 * | AY339319 | KX833408 | N/A | KX833496 | KX833691 |
| Coniella obovata | CBS 111025 | AY339313 | KX833409 | N/A | KX833497 | KX833692 |
| Coniella paracastaneicola | CBS 141292 * | KX833591 | KX833410 | N/A | KX833498 | KX833693 |
| Coniella peruensis | CBS 110394 * | KJ710463 | KJ710441 | N/A | KX833499 | KX833695 |
| Coniella prostata | COAD 2597 | MZ727004 | MZ727000 | N/A | MZ772858 | MZ772860 |
| Coniella pseudodiospyri | CBS 145540 * | MK876381 | MK876422 | N/A | MK876479 | MK876493 |
| Coniella pseudodiospyri | CBS 145541 | MK876382 | MK876423 | N/A | MK876480 | MK876494 |
| Coniella pseudogranati | CBS 137980 * | KJ869132 | N/A | N/A | N/A | N/A |
| Coniella pseudokoreana | MFLU 13-0282 * | MF190146 | N/A | N/A | N/A | N/A |
| Coniella pseudostraminea | CBS 112624 * | KX833593 | KX833412 | N/A | KX833500 | KX833696 |
| Coniella quercicola | CBS 90469 * | KX833595 | KX833414 | N/A | KX833502 | KX833698 |
| Coniella solicola | CBS 76671 * | KX833597 | KX833416 | N/A | KX833505 | KX833701 |
| Coniella straminea | CBS 14922 | AY339348 | AY339296 | N/A | KX833506 | KX833704 |
| Coniella tibouchinae | CBS 131595 * | JQ281774 | KX833418 | N/A | KX833507 | JQ281778 |
| Coniella vitis | JZB 3700001 * | KX890008 | KX890083 | N/A | N/A | KX890058 |
| Coniella vitis | JZB 3700002 | KX889992 | KX890067 | N/A | N/A | KX890042 |
| Coniella wangiensis | CBS 132530 * | JX069873 | JX069857 | N/A | KX833509 | KX833705 |
| Discosia ravennica | MFLU 18-0131 * | MT376615 | MT376617 | MT393594 | N/A | N/A |
| Melanconiella hyperopta | CBS 132231 * | MH866004 | MH877448 | N/A | KX833510 | KX833706 |
| Melanconiella hyperopta | CBS 131696 | JQ926281 | N/A | N/A | N/A | N/A |
| Pseudoplagiostoma alsophilae | SAUCC WZ0451 * | OP810625 | OP810631 | OP828586 | OP828578 | OP828580 |
| Pseudoplagiostoma alsophilae | SAUCC WZ0152 | OP810626 | OP810632 | OP828587 | OP828579 | OP828581 |
| Pseudoplagiostoma bambusae | SAUCC 1206-4 * | OP810629 | OP810635 | OP828590 | N/A | OP828584 |
| Pseudoplagiostoma bambusae | SAUCC 1206-6 | OP810630 | OP810636 | OP828591 | N/A | OP828585 |
| Pseudoplagiostoma castaneae | SAUCC my0162 * | MZ156982 | MZ156985 | MZ220325 | MZ220323 | MZ220321 |
| Pseudoplagiostoma castaneae | SAUCC my0523 | MZ156983 | MZ156986 | MZ220326 | MZ220324 | MZ220322 |
| Pseudoplagiostoma corymbiae | CBS 132529 * | JX069861 | JX069845 | N/A | N/A | N/A |
| Pseudoplagiostoma corymbiicola | CBS 145052 * | MK047425 | MK047476 | MK047577 | N/A | MK047558 |
| Pseudoplagiostoma dipterocarpi | CMUETT57 * | KR994682 | KR994683 | N/A | N/A | N/A |
| Pseudoplagiostoma dipterocarpicola | MFLUCC 21-0142 * | OM228844 | OM228842 | OM219638 | N/A | OM219629 |
| Pseudoplagiostoma dipterocarpicola | MFLUCC 21-0114 | OM228843 | OM228841 | OM219637 | N/A | OM219628 |
| Pseudoplagiostoma eucalypti | CBS 124807 * | GU973512 | GU973606 | GU973575 | N/A | GU973542 |
| Pseudoplagiostoma eucalypti | CBS 116382 | GU973514 | GU973608 | GU973577 | N/A | GU973544 |
| Pseudoplagiostoma inthanonense | MFLUCC 23-0262 * | OR606510 | OR633320 | OR611920 | OR611921 | OR650831 |
| Pseudoplagiostoma jasmini sp. nov. | MFLUCC 23-0044 * | OQ786078 | OQ786079 | OQ850148 | N/A | OQ850145 |
| Pseudoplagiostoma machili | SAUCC BW0233 * | OP810627 | OP810633 | OP828588 | N/A | OP828582 |
| Pseudoplagiostoma machili | SAUCC BW0221 | OP810628 | OP810634 | OP828589 | N/A | OP828583 |
| Pseudoplagiostoma mangiferae | KUMCC 18-0197 * | MK084824 | MK084825 | MK084823 | N/A | N/A |
| Pseudoplagiostoma mangiferae | 8-1.1 | MN818665 | MN876855 | N/A | N/A | N/A |
| Pseudoplagiostoma myracrodruonis | URM 7799 * | MG870421 | MK982151 | MN019566 | MK977723 | MK982557 |
| Pseudoplagiostoma myracrodruonis | URM 8123 | MK982150 | MK982152 | MN019567 | MK977724 | MK982558 |
| Pseudoplagiostoma oldii | CBS 124808 * | GU973534 | GU973609 | GU993862 | N/A | GU973564 |
| Pseudoplagiostoma variabile | CBS 113067 * | GU973536 | GU973611 | GU993863 | N/A | GU973566 |
N/A: Not applicable.
Table 2.
Partition model selected for each locus for the Bayesian analyses.
| Model Selected under Akaike Information Criterion (AIC) | |||
|---|---|---|---|
| Gene Region (s) | Ciliochorella | Coniella | Pseudoplagiostoma |
| ITS | HKY+G | HKY+G | GTR+G |
| 28S | GTR+I | GTR+I+G | GTR+I+G |
| β-tub | GTR+I | N/A | HKY+I+G |
| Rpb2 | N/A | GTR+I+G | GTR+G |
| tef-1α | N/A | HKY+I+G | HKY+G |
N/A: Not applicable.
Table 3.
Total number of characters, ML-IQ, and MP analysis parameters.
| Ciliochorella | Coniella | Pseudoplagiostoma | ||
|---|---|---|---|---|
| Number of characters in the combined alignment | 2033 | 2975 | 2738 | |
| Partition of each locus | ITS: 1–516 28S: 517–1362 β-tub: 1363–2033 | ITS: 1–580 28S: 581–1412 Rpb2: 1413–2175 tef-1α: 2176–2493 | ITS: 1–557 28S: 558–1375 β-tub: 1376–1855 tef-1α: 1856–2162 Rpb2: 2163–2738 | |
| Number of strains used (excluding outgroups) | 7 (5 species) | 51 (42 species) | 23 (15 species) | |
| ML-IQ analysis parameters | ||||
| ML optimization likelihood value | −4043.048 | −17,415.761 | −12,799.621 | |
| ML Tree length | 0.245 | 2.503 | 1.687 | |
| Distinct alignment patterns | 140 | 916 | 874 | |
| Maximum parsimonious analysis parameters | ||||
| MP length: Tree #1 | 295 | 3407 | 2136 | |
| Constant | 1747 | 2034 | 1789 | |
| Parsimony-informative | 257 | 769 | 840 | |
| Parsimony-uninformative | 29 | 172 | 109 | |
| Tree #1 | CI | 0.997 | 0.445 | 0.678 |
| RI | 0.997 | 0.684 | 0.802 | |
| RC | 0.993 | 0.304 | 0.543 | |
| HI | 0.003 | 0.555 | 0.322 | |
Table 4.
Morphological comparison of Ciliochorella sp. (MFLUCC 23-0239) and C. phanericola.
| Species | |||
|---|---|---|---|
| Species Characters | Ciliochorella sp. MFLUCC 23-0239 (This Study) | C. phanericola MFLUCC 14-0984 [51] | |
| Conidiomata | Size | 1000–1100 μm diam., 370–380 μm high | 1000–1200 μm diam., 170–200 μm high |
| Shape and colour | Semi-immersed, carbonaceous, sometimes solitary, uniloculate, black | Semi-immersed, circular areas, carbonaceous, sometimes solitary, black | |
| Conidia | Size (μm) | 11–15 × 2.4–3.8 | 13–15 × 2.8–3.5 |
| L/W | 4.0 | 4.1 | |
| Shape | Allantoid to sub-cylindrical, or sub-falcate to reniform, apex sometimes broadly obtuse, tapering towards a slightly curved base with an obconic basal cell, smooth | Allantoid to sub-cylindrical, smooth | |
| Colour | Hyaline to pale brown | Hyaline to pale brown | |
| Septa | 1-euseptate | 2-septate | |
| Guttules | Present | Present | |
| Appendages | 2 apical, 1 basal, tubular, filiform, flexuous; apical 12.5–18.5 μm long; basal 4–6.5 μm long | 2 apical, 1 basal, tubular; apical 15–23 μm long; basal 9–11.5 μm long | |
| Appressoria | Present | Not observed | |
| Reported morph(s) | Asexual | Asexual | |
| Life style(s) | Saprobic | Pathogen or saprobic on leaf | |
| Hosts | Jasminum sp. | Phanera purpurea | |
| Gene region(s) | ITS, 28S | ITS, 28S, β-tub | |
L/W: length-to-width ratio.
Table 5.
Morphological comparison between our strain and the ex-type of Coniella malaysiana.
| Species | |||
|---|---|---|---|
| Species Characters | C. malaysiana MFLUCC 23-0240 (This Study) | C. malaysiana CBS 141598 [55] | |
| Conidiomata | Size | 135–140 μm diam., 100–130 μm high | 550 μm diam. |
| Shape and color | Semi-immersed, sometimes erumpent, solitary, scattered or gregarious, uniloculate, globose to subglobose, black | Immersed or superficial, globose to depressed, initially hyaline, becoming olivaceous to black with age | |
| Conidia | Size (μm) | 8.2–13.1 × 4–5 | 8.5–11 × 3.5–4.5 |
| L/W | 2.6 | 2.5 | |
| Shape | Smooth, thick-walled, fusiform to truncate to sub-ellipsoidal, sometimes obovoid, tapering towards a slightly curved apex and base, wider in the middle | Thick-walled, fusoid to ellipsoid, inequilateral, apex acutely rounded, widest in the middle, tapering to a truncate base | |
| Color | Hyaline when immature, becoming pale to dark brown upon maturation | Hyaline to pale brown | |
| Septa | Aseptate | Aseptate | |
| Guttules | Present | Present | |
| Appressoria | Present | Not observed | |
| Reported morph(s) | Asexual | Asexual | |
| Life style | Associated with leaf spots | Plant pathogenic | |
| Hosts | Jasminum sp. | Corymbia torelliana | |
| Gene region(s) | ITS, 28S, Rpb2, tef-1α | ITS, 28S, Rpb2, tef-1α | |
L/W: Length to width ratio.
Table 6.
Morphological comparison of Pseudoplagiostoma jasmini with P. dipterocarpicola.
| Species | |||
|---|---|---|---|
| Species Characters | P. jasmini MFLUCC 23-0044 (This Study) | P. dipterocarpicola MFLUCC 21-0142 [67] | |
| Conidiomata | Size | 150–230 μm diam., 140–200 μm high | 113–288 μm diam., 63–153 μm high |
| Shape and color | Pycnidial, semi-immersed, globose to subglobose, pale brown, surrounded with black margin | Pycnidial with pale yellow cylindrical strips of exuding conidia, subglobose, subcuticular to epidermal, unilocular, irregularly breaking through plant tissue at the center, medium to dark brown | |
| Conidia | Size (μm) | 14–22 × 6.5–11 | 9–22 × 4–7.5 |
| L/W | 2.0 | 2.7 | |
| Shape | Cylindrical to truncate or ellipsoidal, elongated, reniform, pyriform or obovoid, apex broadly obtuse, tapering towards slightly curved base | Ellipsoidal to elongated, apex broadly obtuse, straight, or slightly curved at base, often slightly narrow at middle, base tapering to flat protruding scar | |
| Color | Hyaline | Hyaline | |
| Septa | 0–2-septate | Aseptate | |
| Guttules | Present | Present | |
| Conidial wall (μm) | Smooth, 0.6–1.3 | Smooth, 0.5–1.5 | |
| Hilum | Mostly present and prominent | Present or absent | |
| Appressoria | Present | Not observed | |
| Reported morph(s) | Asexual | Asexual | |
| Life style | Associated with leaf spots | Associated with twigs and fruits | |
| Hosts | Jasminum grandiflorum | Dipterocarpus sp. | |
| Gene region(s) | ITS, 28S, β-tub, tef-1α | ITS, 28S, β-tub, tef-1α | |
L/W: Length-to-width ratio.
Table 7.
Genetic distance (%) between Pseudoplagiostoma species (grouped according to PTP results) in the concatenated ITS, 28S, β-tub, and tef-1α genetic markers.
Table 7.
Genetic distance (%) between Pseudoplagiostoma species (grouped according to PTP results) in the concatenated ITS, 28S, β-tub, and tef-1α genetic markers.
| Group 1 (%) | Group 2 (%) | Group 3 (%) | Group 4 (%) | |
|---|---|---|---|---|
| Group 1: P. machili | N/A | 5.67 | 11.0 | 12.3 |
| Group 2: P. alsophilae | 5.67 | N/A | 10.1 | 11.8 |
| Group 3: P. dipterocarpicola | 11.0 | 10.1 | N/A | 9.11 |
| Group 4: P. jasmini | 12.3 | 11.8 | 9.11 | N/A |
N/A: not applicable.
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MDPI and ACS Style
Gomdola, D.; McKenzie, E.H.C.; Hyde, K.D.; Bundhun, D.; Jayawardena, R.S. Appressoria-Producing Sordariomycetes Taxa Associated with Jasminum Species. Pathogens 2023, 12, 1407. https://doi.org/10.3390/pathogens12121407
AMA Style
Gomdola D, McKenzie EHC, Hyde KD, Bundhun D, Jayawardena RS. Appressoria-Producing Sordariomycetes Taxa Associated with Jasminum Species. Pathogens. 2023; 12(12):1407. https://doi.org/10.3390/pathogens12121407
Chicago/Turabian StyleGomdola, Deecksha, Eric H. C. McKenzie, Kevin D. Hyde, Digvijayini Bundhun, and Ruvishika S. Jayawardena. 2023. "Appressoria-Producing Sordariomycetes Taxa Associated with Jasminum Species" Pathogens 12, no. 12: 1407. https://doi.org/10.3390/pathogens12121407
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