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Article

First Report of Colletotrichum fructicola, C. rhizophorae sp. nov. and C. thailandica sp. nov. on Mangrove in Thailand

by
Chada Norphanphoun
1,2,3 and
Kevin D. Hyde
1,2,3,*
1
Center of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai 57100, Thailand
2
School of Science, Mae Fah Luang University, Chiang Rai 57100, Thailand
3
Mushroom Research Foundation, 128 M.3 Ban Pa Deng T. Pa Pae, A. Mae Taeng, Chiang Mai 50150, Thailand
*
Author to whom correspondence should be addressed.
Pathogens 2023, 12(12), 1436; https://doi.org/10.3390/pathogens12121436
Submission received: 29 September 2023 / Revised: 27 November 2023 / Accepted: 6 December 2023 / Published: 10 December 2023
(This article belongs to the Special Issue Filamentous Fungal Pathogens: 2nd Edition)
Browse Figures
Versions Notes

Abstract

:
Colletotrichum, a genus within the phylum Ascomycota (Fungi) and family Glomerellaceae are important plant pathogens globally. In this paper, we detail four Colletotrichum species found in mangrove ecosystems. Two new species, Colletotrichum rhizophorae and C. thailandica, and a new host record for Colletotrichum fructicola were identified in Thailand. Colletotrichum tropicale was collected from Taiwan’s mangroves and is a new record for Rhizophora mucronata. These identifications were established through a combination of molecular analysis and morphological characteristics. This expanded dataset for Colletotrichum enhances our understanding of the genetic diversity within this genus and its associations with mangrove ecosystems. The findings outlined herein provide data on our exploration of mangrove pathogens in Asia.

1. Introduction

Mangroves, the coastal ecosystems where land and sea merge, have been a subject of fascination for ecologists, conservationists, and nature enthusiasts for decades. Thailand has an extensive coastline and is home to numerous mangrove forests that have not only drawn the attention of researchers but have also unveiled a lesser-known yet incredibly diverse facet of these ecosystems—the extraordinary diversity of fungi they harbor [1,2]. This introduction sets the stage for the exploration of the captivating world of Thai mangroves and their rich fungal diversity. Thailand’s mangrove forests are a critical component of its coastal biodiversity and ecological integrity. They serve as a protective buffer against erosion, tidal surges, provide invaluable breeding grounds for marine species, and contribute significantly to carbon sequestration and climate change mitigation [3]. While the spotlight is often on the charismatic fauna and flora within mangroves, the fungi inhabiting these environments have, until recently, remained less studied. Recent studies have shed light on the remarkable diversity of fungi in Thai mangroves [4,5,6,7]. These fungi exhibit unique adaptations to the harsh conditions of mangrove ecosystems, thriving in saline environments and forming intricate relationships with mangrove trees and other microorganisms [1,2]. They play pivotal roles in nutrient cycling, organic matter decomposition, and symbiotic associations, all of which are essential for the health and sustainability of mangrove ecosystems [8,9].
Colletotrichum is a genus within the phylum Ascomycota (Fungi), belonging to the order Glomerellales and family Glomerellaceae [10]. There are 1035 names in Index Fungorum (http://www.indexfungorum.org/, Access Date 18 September 2023) with the type species being Colletotrichum lineola Corda. The genus is characterized by hemibiotrophic or necrotrophic lifestyles, displaying a biotrophic phase during initial host colonization before transitioning to necrotrophic, leading to cell death [1,11]. Colletotrichum species are important plant pathogens causing anthracnose or Colletotrichum blight diseases, infecting a wide range of hosts, including fruits, vegetables, ornamental plants, and agricultural crops [12,13,14,15]. Typical symptoms of Colletotrichum infection include dark, sunken lesions with defined edges on leaves, stems, and fruits, resulting in wilting, rotting, and premature fruit drops [16,17]. Given its economic significance, Colletotrichum causes substantial losses in crop yield and quality globally, affecting major plants like mango, banana, Citrus, pepper, coffee, and strawberry [18,19,20,21]. The morphological features of Colletotrichum vary among species but generally include conidia, conidiomata, and setae [22]. Disease management involves using resistant cultivars, cultural practices, fungicides, and sanitation [23]. Molecular techniques, such as DNA sequencing of specific genes (e.g., ITS, act, β-tubulin, gapdh), evolutionary and coalescent-based methods, aid in accurate identification [24,25]. Ongoing research aims to understand pathogenic mechanisms, host specificity, and sustainable disease control strategies [26]. Some Colletotrichum species are also endophytes or latent pathogens, which means they live in plants without causing disease until the right conditions are met, including mangroves [27,28,29,30,31,32,33,34]. Colletotrichum’s prevalence and impact on mangroves have been thoroughly investigated in several studies, providing crucial data for a comprehensive understanding of its ecology and management strategies [28,35,36].
In this study, we studied the mangroves of Thailand and Taiwan to uncover the phylogenetic diversity of Colletotrichum species associated with Rhizophora apiculata and R. mucronata, respectively. The aim of this study was to identify these isolates based on phylogenetic data and morphology to confirm their novel associations in mangrove ecosystems.

2. Materials and Methods

2.1. Sampling and Examination of Specimens

Fresh leaf samples were collected in 2017 from Rhizophora apiculata in Thailand. Fresh specimens were taken to the laboratory in paper bags, examined, and described. Morphological characters of conidiomata were examined using an Olympus SZX16 stereo microscope (Olympus Corporation, Tokyo, Japan). Micromorphology was studied and photographed using a Nikon Eclipse Ni compound microscope with a Microscope Camera DS-Ri2 (Nikon Corporation, Tokyo, Japan). All image measurements were made with the Image Frame Work program v. 0.9.7 (Tarosoft ®, Nontha Buri, Thailand). Photoplates were made using Adobe Photoshop CC 2019 version 20.0.1 (Adobe Systems, San Jose, CA, USA).
The cultures were acquired using the tissue isolation technique as described in the study of Norphanphoun et al. [37]. Single hyphal tips were transferred onto 2% potato agar (PA) plates at room temperature (25 °C ± 2) throughout a one-week period: 12 hours dark and 12 hours light. The cultural features were observed and documented at intervals of 5, 7, and 14 days. The morphological characteristics of the culture were analyzed during the entire cultivation duration. In order to conduct further experiments, pure cultures were cultivated on potato dextrose agar (PDA) (HiMedia Laboratories LLC, Kennett Square, PA, USA). Dried and living cultures were deposited in the culture collection at Mae Fah Luang University (MFLUCC) and herbarium collection (MFLU), Chiang Rai, Thailand. The enumeration of Faces of Fungi (https://www.facesoffungi.org/) was conducted following the methodology outlined in Jayasiri et al. [38].

2.2. DNA Extraction, Amplification via PCR, and Sequencing

Genomic DNA was extracted from fresh fungal mycelia growing on PDA at room temperature (25 °C ± 2) for two weeks using an E.Z.N.A® Fungal DNA Mini Kit, (Omega Bio-tek, Inc., Nocross, GA, USA) following the manufacturer’s protocols. Polymerase chain reactions (PCR) were carried out using the following primer pairs: ITS1/ITS4 to amplify the internal transcribed spacer region (ITS), ACT512F/ACT738R for actin (act), GDF1/GPDHR2 for partial glyceraldehyde-3-phosphate dehydrogenase region (gapdh), T1/T2 for beta-tubulin (β-tubulin), CHS-79F/CHS-354R for chitin synthase (chs-1), CL1C/CL2C for calmodulin (cal) [39,40,41,42].
The amplification reactions were carried out using the following protocol: 25 μL reaction volume containing 1 µL of DNA template, 1 µL (20 µM stock concentration) of each forward and reverse primers, 12.5 µL of DreamTaq Green PCR Master Mix (2×) (Thermo Fisher Scientific Inc., Waltham, MA, USA), and 9.5 µL of double-distilled water (ddH2O). The PCR thermal cycling program for each locus is described in Table 1. PCR products were analyzed using 1.7% TAE agarose gels containing the 100 bp DNA Ladder RTU (Bio-Helix Co., Ltd., Taipei, Taiwan) to confirm the presence of amplicons at the expected molecular weight. The purification and sequencing of PCR products using the amplification primers specified above were conducted at SolGent Co., Ltd., located in Daejeon, Republic of Korea.

2.3. Phylogenetic Analysis

The raw readings were processed and organized into contigs using Geneious Prime® 2023.2.1 Java Version 11.0.18+10 (64-bit) software (Biomatters Inc., Boston, MA, USA). The newly generated sequences were utilized as queries to conduct a BLASTn search against the nonredundant (nr) database in GenBank (https://www.ncbi.nlm.nih.gov/; accessed on 1 September 2023). The retrieval of similar sequences was conducted, followed by the construction of numerous alignments. The GenBank taxonomy browser was utilized to verify all sequences classified as Colletotrichum in the database. BioEdit version 7.2.5 (Ibis Biosciences, Carlsbad, CA, USA) [43] was used to assign open reading frames of the protein coding sequences of actin, gapdh, β-tubulin, chs-1, and cal according to reference sequences in the GenBank database. The combined sequence data of all loci were used to perform maximum likelihood (ML) and Bayesian inference analysis (BI). The dataset consisted of 126 taxa of the Colletotrichum gloeosporioides species complex and two taxa from singleton species as outgroups, C. arecacearum strains MH0003 and MH0003-1. Outgroup sequences were selected based on preliminary analysis of the multigene phylogeny of the Colletotrichum species complex dataset. All taxa used for these analyses can be found in Table 2.
Sequences were aligned for each locus separately using the MAFFT v.7.110 online program (http://mafft.cbrc.jp/alignment/server/; accessed on 19 September 2023) [44]. TrimAl/readAl v1.2. program was used to trim ambiguously aligned positions [45]. The software BioEdit version 7.2.5 was utilized to make additional manual edits as needed [43]. The congruency of genes and their potential for combination were assessed using a partition homogeneity test (PHT) conducted using PAUP* 4.0b10 software [46]. The concatenated sequence alignments were acquired from MEGA version 7.0.14 and version 10.1.0, as reported by Kumar et al. [47] and Tamura et al. [48], respectively. Geneious Prime® 2023.2.1 was used to convert file format to Nexus BI analyses.
The data were divided into the following categories: ITS, act-exon, gapdh-exon, β-tubulin-exon, chs-1-exon, cal-exon, act-intron, gapdh-intron, β-tubulin-intron, and cal-intron. The researchers utilized the software RAxML-HPC2 on XSEDE to conduct maximum likelihood (ML) analysis, which was implemented using the CIPRES Science Gateway web server (https://www.phylo.org/portal2/; accessed on 20 November 2023) [49]. A total of 1000 bootstrap repeats were conducted in a swift manner, employing the GTRGAMMA model to simulate nucleotide evolution. The researchers conducted a Bayesian inference analysis by utilizing the Markov Chain Monte Carlo (MCMC) algorithm, which was implemented on the CIPRES Science Gateway web server. Specifically, they used MrBayes on XSEDE, as described by Miller et al. [49]. The optimal nucleotide substitution model for each partition was individually calculated using MrModeltest version 2.2 (Boston, MA, USA), as shown in Table 3 [50]. The computation of posterior probability involved the execution of two independent runs, each consisting of four chains. These runs were initiated from a randomly generated tree topology. A total of 10 million generations were executed for the given dataset. The sampling of trees occurred at regular intervals of 100 generations. According to Ronquist et al. [51], a quarter of the trees were excluded as burn-in values, while the average standard deviation of split frequencies reached convergence below 0.01.
The phylogram was generated using FigTree v1.4.3 (http://tree.bio.ed.ac.uk/software/figtree/) [52], a software tool commonly used for visualizing phylogenetic trees. The final figure was created using Adobe Illustrator CC version 23.0.1 (64-bit) and Adobe Photoshop CC version 20.0.1 release, both products developed by Adobe Systems in California, USA. The newly produced sequences in this investigation were deposited in GenBank as indicated in Table 2. The completed alignments and trees were submitted to TreeBASE.
The Genealogical Concordance Phylogenetic Species Recognition (GCPSR) model with a pairwise homoplasy index (PHI) test was used to analyze the newly generated taxon and its most phylogenetically close neighbors [53]. The PHI test was performed in SplitsTree v. 4.14.6 [54,55] with a five-locus concatenated dataset (ITS, act, gapdh, β-tubulin, chs-1, and cal) to determine the recombination level among phylogenetically closely related species. A pairwise homoplasy index below a 0.05 threshold (Φw < 0.05) indicated the presence of significant recombination in the dataset. The relationship between closely related species was visualized by constructing a split graph.

3. Results

The results of the partition homogeneity test (PHT) for the phylogenetic tree were not significant (95% level), which suggests that the individual datasets can be combined. To assess tree topology and clade support, single-locus phylogenetic trees were also generated before the combined gene tree was conducted. In this research, we introduce two novel Colletotrichum species alongside two known species.
The phylogenetic analysis utilized a comprehensive dataset encompassing six genes, including 126 strains from the Colletotrichum species in the gloeosporioides species complex and 2 singleton strains—C. arecacearum strains MH0003 and MH0003-1 sequences served as the outgroup. This dataset had a total length of 1803 characters, inclusive of alignment gaps, with the following partitions: ITS1+5.8S+ITS2 (1–593), act-exon (594–679), gapdh-exon (680–743), β-tubulin-exon (744–973), chs-1-exon (974–1197), cal-exon (1198–1569), act-intron (1570–1738), gapdh-intron (1739–1951), β-tubulin-intron (1952-2175), and cal-intron (2176–2534). Both maximum likelihood (ML) and Bayesian inference (BI) were employed for the analysis. Notably, trees generated under distinct optimality criteria exhibited congruent topologies and showed no significant differences. The highest-scoring likelihood tree for the combined dataset possessed a final likelihood value of -13,417.186937 (Figure 1). Within this tree, the new strains clustered within the gloeosporioides species complex clade, alongside other sequences identified as members of the gloeosporioides species complex. Remarkably, this species complex received robust statistical support, with 100% bootstrap support (BSML) and a posterior probability of 1.00 (PPBI).
The analysis of six genetic loci using both maximum likelihood (ML) and Bayesian inference (BI) methods resulted in a phylogenetic tree with well-supported clades, as shown in Figure 1. Within this study, we propose the recognition of two novel species, namely C. rhizophorae and C. thailandica, with robust statistical backing, signified by a high bootstrap support of 95% (BSML) and a posterior probability of 0.85 (PPBI). In terms of known species, two strains originating from mangrove habitats in Thailand (MFLUCC 17-1752 and MFLUCC 17-1753) were classified as members of the species C. fructicola, while a strain from Taiwan (NTUCC) was identified as C. tropicale. Notably, MFLUCC 17-1752 and MFLUCC 17-1753 clustered within the C. fructicola species group with substantial support: a 98% bootstrap support (BSML) and a posterior probability of 1.00 (PPBI). On the other hand, strain NTUCC was grouped within the C. tropicale species cluster, exhibiting a strong 99% bootstrap support (BSML) and a posterior probability of 1.00 (PPBI). It is noteworthy that all newly introduced strains in this study shared the same topological arrangement as the preliminary analysis of the Colletotrichum species complex.
To assess evolutionary independence, we employed the GCPSR concept on our strain dataset and its closely related taxa. The pairwise homoplasy index (PHI or Φw) is a crucial metric, and a value below 0.05 suggests the presence of substantial genetic recombination within a dataset. Figure 2 shows that our GCPSR analysis gave a PHI of 0.3688 for all closely related taxa in this study. This means that there was no significant genetic mixing between these strains and their sister taxa. Since we saw that the newly introduced species were very different from each other in terms of their phylogeny, we extended the GCPSR analysis to isolate only these new species. The results showed that the PHI value was greater than 0.05 (Φw = 1.0) for both newly taxon C. rhizophorae and C. thailandica isolates with the known species C. pandanicola. This clearly shows that these two new species have not been recombined in a significant way. This substantiates the distinct species status of all these isolates.

3.1. Colletotrichum fructicola Prihast., L. Cai and K.D. Hyde, Fungal Diversity 39: 96 (2009)

Isolated from the leaf spot that is associated with Rhizophora apiculata Blume. Asexual morph: Conidiomata pycnidial, globose, brown, superficial on PDA, releasing conidia in a yellow mass, slimy, globose, glistening mass. Conidiophores either directly formed from hyphae or from a cushion of spherical hyaline cells, septate, branched. Conidiogenous cells hyaline, cylindrical to ampulliform, straight to flask-shaped, 5–15 × 3–5 μm. Setae not observed. Conidia (9–)12.5–13(–14) × (4.7–)4–5(–5.5) μm (mean ± SD = 13 ± 0.5 × 5 ± 0.5 μm), hyaline, aseptate, smooth-walled, clavate to cylindrical, one end rounded and one end acute or both ends rounded, guttulate, granular. Sexual morph: Ascomata pycnidial, produced on WA + needle, sub-globose with ostiole, superficial, brown. Asci 30–68 × 8–14 μm, clavate to cymbiform, slightly curved, composed of pale to medium brown flattened angular cells, bitunicate, smooth-walled, 6–8-spored, with visible apical chamber, hyaline. Ascospore (14–)15–16(–19) × (4.4–)4–5(–5.3) μm (mean ± SD = 16 ± 0.5 × 5 ± 0.5 μm), hyaline, aseptate, smooth-walled, allantoid to lunate, both ends rounded, guttulate, granular.
Culture characteristics: Colonies on CMA reaching 7–8 cm diam after 7 d at room temperature (±25 °C), under light 12 h/dark 12 h, colonies rhizoid to filamentous, dense, flat or raised surface, with filiform margin, white from above and white to pale-yellow reverse, with producing grouped pycnidia. Colonies on WA with sterilized sticks, reaching 5 cm diam after 7 d at room temperature (±25 °C), under light 12 h/dark 12 h, colonies rhizoid to filamentous, dense, flat surface, with filiform margin, dark green from above and reverse, with producing pycnidia on sticks and immersed pycnidia under media.
Hosts and Distribution: Actinidia chinensis, China [56], Japan [57]; Aesculus chinensis, China [58]; Amomum villosum, China [59]; Anacardium occidentale, Brazil [60,61]; Annona spp., Brazil [62,63]; Anthurium, Sri Lanka [64]; Arachis hypogaea, China [65]; Areca catechu, China [66,67]; Atractylodes ovata, Korea [68]; Aucuba japonica, China [69], Korea [70]; Averrhoa carambola, China [71]; Bletilla striata, China [72]; Brassica spp., China [73]; Camellia chrysantha, China [74]; Camellia grijsii, China [75,76]; Camellia oleifera, China [77]; Camellia sinensis, China [67,78,79,80,81,82,83], Indonesia [42,80]; Capsicum spp., China [84,85], Thailand [86]; Carica papaya, Mexico [87]; Carya spp., China [88,89,90,91]; Cattleya spp., Brazil [92]; Ceanothus thyrsiflorus, Italy [93]; Citrus spp., China [19,94]; Coffea arabica, Thailand [32,42], China [95]; Corchorus sp., China [96,97]; Cunninghamia lanceolata, China [98,99]; Curcuma phaeocaulis, China [100]; Cyclamen sp., Italy [93]; Cymbopogon citratus, Thailand [101,102]; Dalbergia hupeana, China [103]; Dendrobium spp. China, Thailand [104,105]; Dimocarpus longan, Thailand [101]; Dioscorea spp., Nigeria [42]; Diospyros kaki, Brazil [106], China [107,108],; Eichhornia crassipes, China [109]; Eriobotrya japonica, China [110]; Eucalyptus spp., [111]; Ficus edulis, Germany [42]; Fragaria × ananassa, China [112,113,114,115,116]; Glycine max, China [117]; Hedera spp., China [100,118,119]; Hevea brasiliensis, China [120]; Hydrangea paniculate, Italy [93]; Ilex chinensis, China [100]; Illicium verum, China [121]; Juglans regia, China [122,123]; Licania tomentosa, Brazil [124]; Ligustrum lucidum, China [100]; Limonium sp., Israel [42]; Liquidambar styraciflua, Italy [93]; Liriodendron spp., China [125]; Loropetalum chinense, China [126]; Luffa cylindrica, China [127]; Macadamia ternifolia, China [128]; Magnolia garrettii, China [27]; Magnolia spp., China [129,130,131,132]; Malus domestica, USA [42,133], Brazil [42,134,135,136], Uruguay [135,137,138,139], China [140,141], Korea [142,143,144,145], Japan [146], Italy [147] and France [148]; Mangifera indica, Brazil, Mexico, Egypt, China, Korea, India [20,25,149,150,151,152,153,154,155]; Manihot esculenta, China [156], Brazil [157,158]; Morus alba, China [159]; Musa spp., China [160]; Myrica rubra, China [161]; Nephelium lappaceum, Puerto Rico [162]; Nicotiana tabacum, China [163]; Nopalea cochenillifera, Brazil [164]; Osmanthus fragrans, China [30]; Paris polyphylla, China [165,166]; Pennisetum purpureum, Thailand [102]; Persea americana, New Zealand [167], Australia [42], China [168], Israel [169], Colombia [170], Mexico [171,172]; Peucedanum praeruptorum, China [173]; Phalaenopsis sp., Brazil [92]; Phoebe sheareri, China [174]; Pouteria caimito, China [175]; Prunus persica, USA [176,177], China [178], Korea [179]; Prunus salicina, China [180,181,182]; Pyrus spp., China [42,183,184,185], and Korea [186]; Radermachera sinica, China [187]; Rhizophora apiculate, Thailand (in this study); Rubus spp., Colombia [188], China [189]; Salvia greggii, Italy [190]; Selenicereus undatus, Thailand [191]; Tetragastris panamensis, Panama [42]; Tetrapanax papyrifer, China [192]; Theobroma cacao, Panama [42]; Vitis spp., Korea [193], Brazil [194]; Zamia furfuracea, China [195]; Zingiber officinale, China [100]; Ziziphus jujuba, China [196,197,198]; Ziziphus sp., Thailand [191]; Human, China [199]; Nematodes, Worms Chordodes formosanus, China [200].
Material examined: Thailand, Chanthaburi Province, associated on leaf spot of Rhizophora apiculata, 25 April 2017, Kevin D. Hyde JT04-1, living cultures, MFLUCC 17-1752 (dried culture in MFLU 23-0476); JT04-2, living cultures, MFLUCC 17-1753 (dried culture in MFLU 23-0477).
Notes: Based on samples taken from Coffea arabica in Thailand, Prihastuti et al. [201] described Colletotrichum fructicola (Figure 3 and Figure 4). This taxon has various ecological roles, including epiphytic, endophytic, and pathogenic associations [202]. Yang et al. [203], which summarized subsequent research, showed Colletotrichum fructicola has a widespread distribution across a variety of host species. Through single and combined-gene phylogenetic analysis, our strain consistently grouped with C. fructicola, a species within the gloeosporioides species complex. This alignment was observed in both the preliminary analysis of the Colletotrichum species complex dataset and Figure 1. Furthermore, our strain exhibited morphological characteristics similar to C. fructicola, such as conidia size (in our study; 13.2 ± 0.5 × 5 ± 0.3 μm versus to 9.7–14 × 3–4.3 μm: Prihastuti et al. [201]), ascus size (in our study; 30–68 × 8–14 μm versus 30–55 × 6.5–8.5 μm: Prihastuti et al. [201]), featuring clavate to cymbiform asci, and ascospores (in our study; 16 ± 0.5 × 5 ± 0.5 μm versus to 9–14 × 3–4 μm: Prihastuti et al. [201]), which were hyaline and lunate. Consequently, we classify our strain as C. fructicola. This is the first record of an endophytic C. fructicola isolated from Rhizophora apiculata in Thailand.

3.2. Colletotrichum rhizophorae Norph. and K.D. Hyde sp. nov.

  • Index Fungorum number: IF901452; Faces of Fungi number: FoF 14890, Figure 5
  • Etymology: refers to the host from which the fungus was isolated, Rhizophora apiculata Blume.
  • Holotype: MFLU 23-0478
Isolated from an asymptomatic leaf spot of Rhizophora apiculata Blume. Sexual morph: undetermined. Asexual morph: Conidiomata pycnidial, globose, dark brown, superficial on PDA, releasing conidia in a yellow mass, slimy, globose. Conidiophores either directly formed from hyphae or from a cushion of spherical hyaline cells, septate, branched. Conidiogenous cells hyaline to pale brown, cylindrical to clavate, straight to flask-shaped, 6–19 × 2–9 μm. Setae not observed. Conidia (11.5–)12.5–13(–14.5) × (4–)4.5–5(–5.7) μm (mean ± SD = 13.1 ± 0.9 × 4.5 ± 0.3 μm), hyaline, aseptate, smooth-walled, ellipsoidal to cylindrical, one end rounded and one end acute or both ends rounded, guttulate, granular.
Culture characteristics: Colonies on PDA reaching 6–7 cm diam after 7 d at room temperature (±25 °C), under light 12 h/dark 12 h, colonies filamentous to circular, medium dense, aerial mycelium on surface flat, with irregular margin, white from above and reverse, with producing pycnidia and yellow spore mass.
Distribution: Thailand
Hosts: Rhizophora apiculata
Material examined: Thailand, Wan Yao, Khlung, Chanthaburi, asymptomatic leaf of Rhizophora apiculata, 25 April 2017, Kevin D. Hyde WYKE04AP (dried culture, MFLU 23-0478, holotype), living cultures, MFLUCC 17-1927; WYKE04AL, MFLUCC 17-1911 (dried culture MFLU 23-0479).
Notes: We introduce Colletotrichum rhizophorae as a novel species discovered within Rhizophora apiculata, a mangrove plant in Thailand (Figure 5). This classification is supported by morphological and phylogenetic evidence, as depicted in Figure 1. The phylogenetic analysis demonstrates that this new taxon closely associates with C. thailandica (Figure 1). However, notable distinctions in morphology are observed between C. rhizophorae and C. thailandica, particularly in conidia, conidiophores, and conidiogenous cells (refer to Figure 5 and Figure 6). In order to establish evolutionary independence, we applied the GCPSR concept to C. rhizophorae and its neighboring taxa. Our dataset yielded a PHI value exceeding 0.05 (Φw = 0.363), indicating the absence of significant genetic recombination between C. rhizophorae and its sister taxa, namely C. pandanicola and C. thailandica (Figure 2). Furthermore, a comparison of nucleotide sequences within ITS, act, gapdh, β-tubulin, chs-1, and SCDgle revealed discrepancies between C. thailandica and C. rhizophorae (ITS 5 bp, act 3 bp, gapdh 4 bp, β-tubulin 2 bp, chs-1 6 bp, and SCDgle 4 bp).

3.3. Colletotrichum thailandica Norph. and K.D. Hyde sp. nov.

  • Index Fungorum number: IF901453; Faces of Fungi number: FoF 14891, Figure 6
  • Etymology: refers to the country where the fungus was collected, Thailand.
  • Holotype: MFLU 23-0480
Isolated from an asymptomatic leaf spot of Rhizophora apiculata Blume. Sexual morph: undetermined. Asexual morph: Conidiomata pycnidial, globose, dark brown, superficial on PDA, releasing conidia in a yellow mass, slimy, globose, glistening mass. Conidiophores either directly formed from hyphae or from a cushion of spherical hyaline cells, septate, branched. Conidiogenous cells hyaline to pale brown, cylindrical to ampulliform, straight to flask-shaped, 6–16 × 2–5 μm. Setae about 40–85 µm long, brown to pale brown, and septate. Conidia (12.3–)13.5–15.5(–17.4) × (3.8–)4–4.5(–5.3) μm (mean ± SD = 14.7 ± 1.2 × 4 ± 0.3 μm), hyaline, aseptate, smooth-walled, clavate to cylindrical, one end rounded and one end acute or both ends rounded, guttulate, granular.
Culture characteristics: Colonies on PDA reaching 7–8 cm diam after 10 d at room temperature (±25 °C), under light 12 h/dark 12 h, colonies filamentous to circular, medium dense, aerial mycelium on surface flat or raised, with filiform margin (curled margin), fluffy, white from above and white to pale-yellow reverse, with producing pycnidia and yellow spore mass.
Distribution: Thailand.
Hosts: Rhizophora apiculate
Material examined: Thailand, Wan Yao, Khlung, Chanthaburi, asymptomatic leaf of Rhizophora apiculata, 25 April 2017, Kevin D. Hyde WYKE07AL, Living Cultures, MFLUCC 17-1924 (dried culture MFLU).
Notes: Thailand, Wan Yao, Khlung, Chanthaburi, asymptomatic leaf of Rhizophora apiculata, 25 April 2017, Kevin D. Hyde WYKE07AL (dried culture MFLU 23-0480, holotype), living cultures, MFLUCC 17-1924.
Notes: Colletotrichum thailandica is introduced here as a new species in the gloeosporioides species complex, a classification supported by both morphological (Figure 6) and phylogenetic data. The phylogenetic analysis underscores the distinctiveness of this new taxon, clearly separating it from other recognized Colletotrichum species (Figure 1).
In order to assess evolutionary autonomy, we applied the GCPSR concept to C. thailandica and its closely related taxa. Our data showed that the PHI value was higher than 0.05 (Φw = 0.363), which means that there was not much genetic mixing between C. thailandica and its closest relatives, C. pandanicola and C. rhizophorae (Figure 2). Since there was a lot of phylogenetic diversity between newly introduced species and species that had already been published, like C. pandanicola, we used GCPSR analysis on a larger dataset. The outcome revealed a PHI value surpassing 0.05 (Φw = 1.0), unequivocally indicating the absence of significant recombination for this new species. As a result, we formally introduce C. thailandica as a distinct species, isolated from Rhizophora apiculata in Thailand.

3.4. Colletotrichum tropicale E.I. Rojas, S.A. Rehner & Samuels, Mycologia 102(6): 1331 (2010)

  • Faces of Fungi number: FoF 14892, Figure 7
Isolated from the asymptomatic leaf of Rhizophora mucronata Lam. Sexual morph: undetermined. Asexual morph: Conidiomata pycnidial, globose, brown, superficial on PDA, releasing conidia in a yellow mass, slimy, globose, glistening mass. Conidiophores either directly formed from hyphae or from a cushion of spherical hyaline cells, septate, branched. Conidiogenous cells hyaline to pale brown, cylindrical to ampulliform, straight to flask-shaped, 10–20 × 3–5 μm. Conidia (12–)12.5–13(–14) × (4–)4.5–5(–5.7) μm (mean ± SD = 13.2 ± 0.5 × 5 ± 0.3 μm), hyaline, aseptate, smooth-walled, clavate to cylindrical, one end rounded and one end acute or both ends rounded, guttulate, granular.
Culture characteristics: Colonies on PDA reaching 7–8 cm diam after 14 d at room temperature (±25 °C), under light 12 h/dark 12 h, colonies filamentous to circular, medium dense, aerial mycelium on surface flat or raised, with filiform margin (curled margin), fluffy, gravy from above and dark gravy reverse, with producing pycnidia and yellow spore mass (Figure 3D).
Hosts and distribution: Anacardium, Brazil [60,61]; Annona spp., Brazil, Colombia, Panama and Cuba [63,204,205,206]; Capsicum spp., Indonesia [86] and Brazil [207]; Carica papaya, Costa Rica [208]; Cariniana legalis, Brazil [209]; Cattleya spp., Brazil [92]; Cenchrus purpureus [102]; Coffea spp., China [95]; Copernicia prunifera, Brazil [210]; Cordia alliodora, Panama [206]; endophyte Trichilia tuberculata, Panama [206]; Ficus spp., China [211,212]; Licania tomentosa, Brazil [124]; Litchi chinensis, Japan [42]; Malpighia emarginata, Japan [213]; Mangifera indica Brazil, Mexico, China [20,151,152,153,155,214]; Manihot spp., Brazil [215]; Musa spp., Brazil [216]; Myrciaria dubia, Brazil [217]; Nelumbo nucifera, China [218]; Origanum vulgare, Mexico [219]; Passiflora edulis, Brazil [220]; Persea americana, Mexico [172]; Plinia cauliflora, Japan [221]; Punica granatum, Brazil [222]; Rhizophora mucronata, Taiwan (in this study); Sauropus androgynus, China [223]; Selenicereus monacanthus, Philippines [224], Mexico [225]; Theobroma cacao, Panama [206]; Viola surinamensis, Panama [206]; Human [199].
Material examined: China, Taiwan, Tainan, Shicao, tissue isolation from asymptomatic leaves of Rhizophora mucronata, 17 July 2018, Chada Norphanphoun SCE3L-3B; living cultures, NTUCC.
Notes: Colletotrichum tropicale was documented by Rojas et al. [206] based on isolates obtained from Theobroma cacao leaves in Panama (Figure 7). This taxon has various ecological roles, including epiphytic, endophytic, and pathogenic with wide hosts and distribution [202]. The species was recorded as an endophyte in tropical regions associated with Annona muricata (Annonaceae), Cenchrus purpureus (Poaceae), Cordia aliodora (Boraginaceae), Cymbopogon citratus (Poaceae), Litchi chinensis (Sapindaceae), Nelumbo nucifera (Nelumbonaceae), Theobroma cacao (Malvaceae), Trichilia tuberculata (Meliaceae), Viola surinamensis (Myristicaceae) [42,102,206,218]. In our current study, our phylogenetic analysis clearly places our strain within the C. tropicale clade with robust support, as illustrated in Figure 1. This grouping is further substantiated by the striking similarity in conidia morphology and size, as observed in our study (13.2 ± 0.5 × 5 ± 0.3 μm) when compared to the reported values by Rojas et al. [206] in 2010 (14.1–14.8 × 5.1–5.20 μm). Consequently, we formally designate our isolate as C. tropicale, representing the first documented instance of an endophytic fungus isolated from Rhizophora mucronata in Taiwan.

4. Discussion

Colletotrichum is a pathogenic genus that affects various plant species, including mangroves [28,29,30]. It causes anthracnose, a common disease characterized by dark lesions on leaves, stems, and fruits [16]. Several studies have investigated the prevalence and impact of Colletotrichum on mangroves, providing valuable data for understanding its ecology and management strategies [28,35,36]. In this study, we focused on the examination of six strains isolated from mangrove ecosystems. Five of these strains were isolated from Rhizophora apiculata in Thailand’s mangroves, while one strain originated from Rhizophora mucronata in Taiwan. Among the isolates, Colletotrichum fructicola (MFLUCC 17-1752) was obtained from leaf spot symptoms, while the remaining strains were isolated from asymptomatic leaves. It is important to note that C. fructicola has been found to play different roles in the environment, including as an epiphyte, an endophyte, and a pathogen in a wide range of host species [203]. This suggests that the presence of Colletotrichum species in mangrove ecosystems may be more diverse than initially anticipated. These taxa can exhibit various ecological interactions, including their colonization of asymptomatic leaves. As a result, there is potential for the discovery of additional fungal species within mangrove forest zones. These newly discovered species could encompass both those commonly found in other plant species and entirely novel fungal types.
This comprehensive study employed phylogenetic analysis, morphological characterization, and the Genetic Clade–Phenetic Species Recognition (GCPSR) concept to elucidate the taxonomy and evolutionary relationships of these Colletotrichum species within the gloeosporioides species complex according to the guidelines of Chethana et al. [226] and Maharachchikumbura et al. [227]. Previously, Weir et al. [42] documented the efficacy of individual genes in discerning species within the gloeosporioides species complex. The study identified the designated barcoding gene for fungi in the gloeosporioides complex, encompassing eight genes: the internal transcribed spacer region (ITS), actin (act), glyceraldehyde-3-phosphate dehydrogenase region (gapdh), beta-tubulin (β-tubulin), chitin synthase (chs-1), calmodulin (cal), glutamine synthetase (GS), and manganese-superoxide dismutase (SOD2). However, it was observed that these genes do not consistently provide a conclusive resolution of relationships for all species within this particular species complex. In the context of C. siamense, the performance of individual genes that can distinguish species within the C. gloeosporioides species complex is notably achieved by examining cal and β-tubulin sequences. Conversely, for C. tropicale, the distinguishing genes encompass β-tubulin, act, GS, and SOD2. In the case of C. fructicola, the pertinent genes for effective differentiation are cal, chs-1, GS, and SOD2. To overcome limitations associated with gene function in species delimitation and to achieve precise identification of Colletotrichum isolates in the present study, a comprehensive approach employing six gene sequences (ITS, act, gapdh, β-tubulin, chs-1, and cal), encompassing 126 strains, and 2 singleton strains as outgroups were used to facilitate the identification of two novel species and to document a new host record from Thailand. Moreover, there is a new record of C. tropicale from Taiwan, using act, β-tubulin, and chs-1. The study encompasses multiple reference isolates of C. fructicola, C. siamense, and C. tropicale. The results of a multigene phylogenetic analysis demonstrated that the combined use of ITS, act, gapdh, β-tubulin, chs-1, and cal offered superior resolution in determining Colletotrichum species, surpassing the efficacy of single-gene analysis. This finding aligns with prior studies conducted by Prihastuti et al. [201] and Weir et al. [42]. The results provided valuable insights into the diversity and classification of Colletotrichum species. The phylogenetic analysis, utilizing both maximum likelihood (ML) and Bayesian inference (BI) methods, revealed a well-supported clustering of the new strains within the gloeosporioides species complex clade, alongside sequences previously identified as members of this complex. The robust statistical support, with 100% bootstrap support (BSML) and a posterior probability of 1.00 (PPBI), underlined the validity of the species complex classification (Figure 1). Within this complex, two novel species are formally recognized: C. rhizophorae and C. thailandica. These designations were supported by a high bootstrap support of 99% (BSML) and a posterior probability of 1.00 (PPBI), reaffirming their distinct species status. Additionally, known species, including C. fructicola and C. tropicale, were identified and validated based on their placement within the phylogenetic tree. The application of the GCPSR concept further corroborated the evolutionary independence of these species. The pairwise homoplasy index (PHI or Φw) values exceeding 0.05 indicated a lack of significant genetic recombination within the dataset, highlighting the distinctiveness of the newly proposed species. This was particularly evident in the case of C. rhizophorae and C. thailandica, as their PHI values exceeded 0.05 even when analyzed with closely related taxa. The study delved into the taxonomy of two Colletotrichum species, C. fructicola and C. tropicale, offering significant insights into their classification, morphology, and distribution.
Colletotrichum fructicola, originally described in 2009 from Coffea arabica in Thailand [201], was the subject of taxonomic reevaluation. The study consistently found that the strain under investigation clustered closely with known C. fructicola strains within the gloeosporioides species complex. This clustering was observed both in the preliminary analysis and the final phylogenetic tree, reaffirming its placement within this species complex. Furthermore, morphological similarities, including conidia size, asci size, and ascospore features, provided additional support for the classification of the strain as C. fructicola. Importantly, this study marked a significant milestone in scientific discovery by documenting the first-ever instance of an endophytic fungus isolated from R. apiculata in Thailand.
Colletotrichum tropicale, initially documented from T. cacao leaves in Panama [206], was also investigated in this study. The research employed phylogenetic analysis and examination of conidia morphology to validate the classification of the study’s isolate as C. tropicale. This confirmation represented a notable scientific contribution, as it marked the first documented instance of an endophytic fungus isolated from R. mucronata in Taiwan.
These records expand our knowledge of the geographic distribution of these fungal species. In conclusion, this research enhances our understanding of fungal diversity within mangrove ecosystems and provides valuable taxonomic and ecological insights. The combined use of molecular, morphological, and ecological data, as well as genetic recombination analysis, strengthens the credibility of the newly introduced Colletotrichum species. Overall, this research significantly contributes to our understanding of the taxonomy and evolutionary relationships within the Colletotrichum species complex. The combination of molecular, morphological, and ecological data has led to the recognition of novel species and the validation of known ones, enhancing our knowledge of these important plant-associated fungi.

Author Contributions

Conceptualization, C.N. and K.D.H.; Methodology, C.N. and K.D.H.; Software, C.N.; Formal analysis, C.N.; Resources, K.D.H.; Data curation, K.D.H.; Writing—original draft, C.N.; Writing—review & editing, K.D.H.; Supervision, K.D.H.; Project administration, K.D.H. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by The National Research Council of Thailand (NRCT) grant number N42A650547.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The completed alignments and trees were submitted to TreeBASE submission ID 31014 (http://purl.org/phylo/treebase/phylows/study/TB2:S31014?x-access-code=a44bff36f1453301a23a6c12ba2d815c&format=html accessed on 28 September 2023).

Acknowledgments

Cexpresses gratitude for the postdoctoral fellowship fund provided by Mae Fah Luang University. Kevin D. Hyde expresses gratitude to the National Research Council of Thailand (NRCT) for providing the grant titled “Total fungal Diversity in a Given Forest Area with Implications towards Species Numbers, Chemical Diversity and Biotechnology” (grant no: N42A650547).

Conflicts of Interest

The authors declare no conflict of interest.

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Pathogens 12 01436 g001aPathogens 12 01436 g001b
Figure 1. Phylogenetic tree generated from maximum likelihood analysis based on combined ITS, act-exon, gapdh-exon, β-tubulin-exon, chs-1-exon, act-intron, gapdh-intron, β-tubulin-intron sequence data. The species obtained in this study are in blue and species synonymized are in green. Ex-type taxa are in bold. Bar = 0.03, which represents the estimated number of nucleotide substitutions of site per branch.
Figure 1. Phylogenetic tree generated from maximum likelihood analysis based on combined ITS, act-exon, gapdh-exon, β-tubulin-exon, chs-1-exon, act-intron, gapdh-intron, β-tubulin-intron sequence data. The species obtained in this study are in blue and species synonymized are in green. Ex-type taxa are in bold. Bar = 0.03, which represents the estimated number of nucleotide substitutions of site per branch.
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Figure 2. The results of the pairwise homoplasy index (PHI) test for closely related species of Colletotrichum stains in this study using both LogDet transformation and splits decomposition. PHI test results (Φw) > 0.05 indicate no significant recombination within the dataset.
Figure 2. The results of the pairwise homoplasy index (PHI) test for closely related species of Colletotrichum stains in this study using both LogDet transformation and splits decomposition. PHI test results (Φw) > 0.05 indicate no significant recombination within the dataset.
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Figure 3. Colletotrichum fructicola (MFLUCC 17-1752). (A) Habitat. (B,C) Rhizophora apiculata leaf spot. (D) Culture on CMA (leaf-above, right-reverse). (E–G) Conidiomata on PDA. (H,I) Conidiogenous cells giving rise to conidia. (J–P) Conidia. Scale bars: (F) = 200 µm, (G) = 500 µm, (H–P) 10 µm.
Figure 3. Colletotrichum fructicola (MFLUCC 17-1752). (A) Habitat. (B,C) Rhizophora apiculata leaf spot. (D) Culture on CMA (leaf-above, right-reverse). (E–G) Conidiomata on PDA. (H,I) Conidiogenous cells giving rise to conidia. (J–P) Conidia. Scale bars: (F) = 200 µm, (G) = 500 µm, (H–P) 10 µm.
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Figure 4. Sexual morph of Colletotrichum fructicola (MFLUCC 17-1752). (A) Culture on WA with sterilized sticks. (B) Ascomata habitat on sterilized sticks. (C) Ascoma. (D) Ascoma peridium. (E–G) Immature and mature asci. (H) Apical ring in Melzer’s reagent. (I–M) Ascospores. Scale bars: (B) = 100 µm, (C) = 50 µm, (D–M) = 10 µm.
Figure 4. Sexual morph of Colletotrichum fructicola (MFLUCC 17-1752). (A) Culture on WA with sterilized sticks. (B) Ascomata habitat on sterilized sticks. (C) Ascoma. (D) Ascoma peridium. (E–G) Immature and mature asci. (H) Apical ring in Melzer’s reagent. (I–M) Ascospores. Scale bars: (B) = 100 µm, (C) = 50 µm, (D–M) = 10 µm.
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Figure 5. Colletotrichum rhizophorae (MFLUCC 17-1927). (A) Habitat. (B,C) Rhizophora apiculata. (D,E) Culture on PDA (leaf-above, right-reverse). (F) conidiomata on WA with sterilized sticks. (G) Conidiomata on PDA. (H,I) Conidiogenous cells giving rise to conidia. (J–P) Conidia. Scale bars: (F) = 200 µm, (G) = 500 µm, (H–P) 10 µm.
Figure 5. Colletotrichum rhizophorae (MFLUCC 17-1927). (A) Habitat. (B,C) Rhizophora apiculata. (D,E) Culture on PDA (leaf-above, right-reverse). (F) conidiomata on WA with sterilized sticks. (G) Conidiomata on PDA. (H,I) Conidiogenous cells giving rise to conidia. (J–P) Conidia. Scale bars: (F) = 200 µm, (G) = 500 µm, (H–P) 10 µm.
Pathogens 12 01436 g005
Pathogens 12 01436 g006
Figure 6. Colletotrichum thailandica (MFLUCC 17-1924). (A) Habitat. (B,C) Rhizophora apiculata. (D,E) Culture on PDA (leaf-above, right-reverse). (F,G) Conidiomata on PDA. (H) Conidiogenous cells giving rise to conidia. (I) Setae. (J–P) Conidia. Scale bars: (F) = 250 µm, (G) = 500 µm, (H–P) 10 µm.
Figure 6. Colletotrichum thailandica (MFLUCC 17-1924). (A) Habitat. (B,C) Rhizophora apiculata. (D,E) Culture on PDA (leaf-above, right-reverse). (F,G) Conidiomata on PDA. (H) Conidiogenous cells giving rise to conidia. (I) Setae. (J–P) Conidia. Scale bars: (F) = 250 µm, (G) = 500 µm, (H–P) 10 µm.
Pathogens 12 01436 g006
Pathogens 12 01436 g007
Figure 7. Colletotrichum tropicale (NCYU). (A) Habitat. (B,C) Rhizophora mucronata. (D) Culture on PDA (leaf-above, right-reverse). (E–G) Colony sporulating on PDA. (H) Conidiogenous cells giving rise to conidia. (I–M) Conidia. Scale bars: (E) = 2 mm, (F) = 100 µm, (G) = 50 µm, (H,M) = 10 µm, (J–L) = 20 µm.
Figure 7. Colletotrichum tropicale (NCYU). (A) Habitat. (B,C) Rhizophora mucronata. (D) Culture on PDA (leaf-above, right-reverse). (E–G) Colony sporulating on PDA. (H) Conidiogenous cells giving rise to conidia. (I–M) Conidia. Scale bars: (E) = 2 mm, (F) = 100 µm, (G) = 50 µm, (H,M) = 10 µm, (J–L) = 20 µm.
Pathogens 12 01436 g007
Table 1. Polymerase chain reaction (PCR) thermal cycling programs for each locus.
Table 1. Polymerase chain reaction (PCR) thermal cycling programs for each locus.
GenePrimersPCR Thermal Cycle Protocols *
ITSITS1/ITS4ID 95 °C for 5 min, 40 cycles of D at 95 °C for 45 s, A at 53 °C for 45 s, E at 72 °C for 2 min, FE at 72 °C for 10 min
actinACT512F/ACT738RID 95 °C for 3 min, 35 cycles of D at 95 °C for 30 s, A at 56 °C for 30 s, E at 72 °C for 45 s, FE at 72 °C for 1 min
gapdhGDF1/GPDHR2ID 95 °C for 5 min, 35 cycles of D at 95 °C for 30 s, A at 50 °C for 45 s, E at 72 °C for 90 s, FE at 72 °C for 7 min
β-tubulinT1/T2ID 95 °C for 3 min, 35 cycles of D at 95 °C for 30 s, A at 543 °C for 30 s, E at 72 °C for 45 s, FE at 72 °C for 1 min
chs-1CHS-79F/CHS-354RID 95 °C for 3 min, 35 cycles of D at 95 °C for 30 s, A at 59 °C for 30 s, E at 72 °C for 45 s, FE at 72 °C for 1 min
calCL1C/CL2CID 94 °C for 3 min, 40 cycles of D at 95 °C for 30 s, A at 57 °C for 80 s, E at 72 °C for 80 s, FE at 72 °C for 10 min
* ID: initial denaturation; D = denaturation; A = annealing; E = elongation; FE = final extension.
Table 2. GenBank accession numbers of the sequences used in phylogenetic analyses Figure 1.
Table 2. GenBank accession numbers of the sequences used in phylogenetic analyses Figure 1.
SpeciesStrainHostCountryAccession Numbers
ITSactgapdhβ-tubulinchs-1cal
C. aenigmaICMP 18608 TPersea americanaIsraelJX010244JX009443JX010044JX010389JX009774JX009683
C. aeschynomenesICMP 17673 TAeschynomene virginicaUSAJX010176JX009483JX009930JX010392JX009799JX009721
C. alataeICMP 17919 TDioscorea alataIndiaJX010190JX009471JX009990JX010383JX009837JX009738
C. alienumICMP 12071 TMalus domesticaNew ZealandJX010251JX009572JX010028JX010411JX009882JX009654
C. analogumCGMCC 3.16079 TAgeratina adenophoraChinaOK030860OK513599OK513663OK513629OK513559-
C. aotearoaICMP 18537 TCoprosma sp.New ZealandJX010205JX009564JX010005JX010420JX009853JX009611
C. arecacearumLC13850, MH0003 TArecaceaeChinaMZ595867MZ664165MZ664049MZ673986MZ799262MZ799238
C. arecacearumLC13851, MH0003-1ArecaceaeChinaMZ595868MZ664166MZ664050MZ673987MZ799263MZ799239
C. arecicolaCGMCC 3.19667 TAreca catechuChinaMK914635MK935374MK935455MK935498MK935541-
C. artocarpicolaMFLUCC 18-1167 TArtocarpus heterophyllusThailandMN415991MN435570MN435568MN435567MN435569-
C. asianumICMP 18580 TCoffea arabicaThailandJX010196JX009584JX010053JX010406JX009867FJ917506
C. asianumCMM4057Mangifera indicaBrazilKC329792KC533747KC517168KC517278--
C. asianumC1646Mangifera indicaTaiwan (China)MK326570MK462967MK376935-MK347247-
C. asianumTL107Mangifera indicaChinaMF039845MF039758MF040776MF039816MF039787-
C. asianumICMP 18696M. indicaAustraliaJX010192JX009576JX009915JX010384JX009753JX009723
C. asianumCMM4056Mangifera indicaBrazilKC329789KC533720KC517165KC517277--
C. australianumUMC002 TCitrus sinensisAustraliaMG572138MN442109MG572127MG572149MW091987-
C. camelliaeCGMCC 3.14925 TCamellia sinensisChinaKJ955081KJ954363KJ954782KJ955230MZ799255KJ954634
C. cangyuanenseCGMCC 3.18969 TAgeratina adenophoraChinaOK030864OK513603OK513667OK513633OK513563-
C. changpingenseSA0016 TFragaria × ananassChinaKP683152KP683093KP852469KP852490KP852449-
C. chiangmaienseMFLUCC 18-0945 TMagnolia garrettiiThailandMW346499MW655578MW548592-MW623653-
C. chrysophilumCMM4268 TMusa sp.BrazilKX094252KX093982KX094183KX094285KX094083KX094063
C. cigarroICMP 18539 TOlea europaeaAustraliaJX010230JX009523JX009966JX010434JX009800JX009635
C. clidemiaeICMP 18658 TClidemia hirtaHawaiiJX010265JX009537JX009989JX010438JX009877JX009645
C. cobbittienseBRIP 66219 TCordyline stricta × C. australisAustraliaMH087016MH094134MH094133MH094137MH094135-
C. conoidesCGMCC 3.17615 TCapsicum sp.ChinaKP890168KP890144KP890162KP890174KP890156KP890150
C. cordylinicolaICMP 18579 TCordyline fruticosaThailandJX010226JX009586JX009975JX010440JX009864HM470238
C. cycadisBRIP 71326a TCycas revolutaChinaMT439915 MT439919MT439921MT439917-
C. dimorphumCGMCC 3.16083 TAgeratina adenophoraChinaOK030867OK513606OK513670OK513636OK513566-
C. dracaenigenumMFLUCC 19-0430 TDracaena sp.ThailandMN921250MT313686MT215577-MT215575-
C. endophyticumMFLUCC 13-0418 TPennisetum purpureumThailandKC633854KF306258KC832854MZ673954MZ799261-
C. fructicolaICMP 18581 TCoffea arabicaThailandJX010165JX009501JX010033JX010405JX009866FJ917508
C. fructicolaICMP 12568Persea americanaAustraliaJX010166JX009529JX009946-JX009762JX009680
C. fructicolaICMP 17787Malus domesticaBrazilJX010164JX009439JX009958-JX009807JX009667
C. fructicolaICMP 17788Malus domesticaBrazilJX010177JX009458JX009949-JX009808JX009672
C. fructicolaIMI 345051, ICMP 17819Fragaria × ananassaCanadaJX010180JX009469JX009997-JX009820JX009668
C. fructicolaICMP 18613Limonium sinuatumIsraelJX010167JX009491JX009998JX010388JX009772JX009675
C. fructicolaICMP 18698Limonium sp.IsraelJX010168JX009585JX010052-JX009773JX009677
C. fructicolaICMP 18667Limonium sp.IsraelJX010169JX009464JX009951-JX009775JX009679
C. fructicolaICMP 18615Limonium sp.IsraelJX010170JX009511JX010016-JX009776JX009678
C. fructicolaICMP 18610Pyrus pyrifoliaJapanJX010174JX009526JX010034-JX009788JX009681
C. fructicolaICMP 18120Dioscorea alataNigeriaJX010182JX009436JX010041JX010401JX009844JX009670
C. fructicolaCBS 125395, ICMP 18645Theobroma cacaoPanamaJX010172JX009543JX009992JX010408JX009873JX009666
C. fructicolaICMP 18727Fragaria × ananassaUSAJX010179JX009565JX010035JX010394JX009812JX009682
C. fructicolaCBS 120005, ICMP 18609Fragaria × ananassaUSAJX010175JX009534JX009926-JX009792JX009673
C. fructicolaICMP 17789Malus domesticaUSAJX010178JX009451JX009914-JX009809JX009665
C. fructicolaICMP 18125Dioscorea alataNigeriaJX010183JX009468JX010009-JX009847JX009669
C. fructicolaCBS 125397 T, ICMP 18646Tetragastris panamensisPanamaJX010173JX009581JX010032JX010409JX009874JX009674
C. fructicolaCBS 238.49 T, ICMP 17921Ficus edulisGermanyJX010181JX009495JX009923JX010400JX009839JX009671
C. fructicolaMFLUCC 17-1752Rhizophora apiculataThailandOR828931OR840845OR840868OR840862OR840856OR840851
C. fructicolaMFLUCC 17-1753Rhizophora apiculataThailandOR828932OR840846OR840869OR840863OR840857OR840852
C. fructivorumCBS 133125 TVaccinium macrocarponBurlingtonJX145145MZ664126MZ664047JX145196MZ799259-
C. gloeosporioidesICMP 17821 TCitrus sinensisItalyJX010152JX009531JX010056JX010445JX009818JX009731
C. gracileCGMCC 3.16075 TAgeratina adenophoraChinaOK030868OK513607OK513671OK513637OK513567
C. grevilleaeCBS 132879 TGrevillea sp.ItalyKC297078KC296941KC297010KC297102KC296987KC296963
C. grossumCGMCC 3.17614 TChili pepperChinaKP890165KP890141KP890159KP890171KP890153KP890147
C. hebeienseMFLUCC 13-0726 TVitis viniferaChinaKF156863KF377532KF377495KF288975KF289008-
C. hederiicolaMFLU 15-0689 THedera helixItalyMN631384MN635795--MN635794-
C. hellenienseCBS 142418 TPoncirus trifoliataGreece, ArtaKY856446KY856019KY856270KY856528KY856186KY856099
C. henanenseCGMCC 3.17354 TCamellia sinensisChinaKJ955109KM023257KJ954810KJ955257MZ799256KJ954662
C. horiiICMP 10492 TDiospyros kakiJapanGQ329690JX009438GQ329681JX010450JX009752JX009604
C. hystricisCBS 142411 TCitrus hystrixItaly, CataniaKY856450KY856023KY856274KY856532KY856190KY856103
C. jiangxienseCGMCC 3.17361 TCamellia sinensisChinaKJ955149KJ954427KJ954850OK236389MZ799257KJ954701
C. kahawaeICMP 17816 TCoffea arabicaKenyaJX010231JX009452JX010012JX010444JX009813JX009642
C. makassarenseCBS 143664 TCapsicum annuumIndonesiaMH728812MH781480MH728820MH846563MH805850-
C. musaeCBS 116870 TMusa sp.USAHQ596292HQ596284HQ596299HQ596280JX009896JX009742
C. nanhuaenseCGMCC 3.18962 TAgeratina adenophoraChinaOK030870OK513609OK513673OK513639OK513569-
C. nullisetosumCGMCC 3.16080 TMangifera indicaChinaOK030872OK513611OK513675OK513641OK513571-
C. nupharicolaICMP 18187 TNuphar lutea subsp. polysepalaUSAJX010187JX009437JX009972JX010398JX009835JX009663
C. oblongisporumCGMCC 3.16074 TAgeratina adenophoraChinaOK030874-OK513677OK513643OK513573-
C. pandanicolaMFLUCC 17-0571 TPandanaceaeThailandMG646967MG646938MG646934MG646926MG646931-
C. pandanicolaMFLUCC 22-0164PandanaceaeThailandOP802369OP801689OP801724OP801744OP801706-
C. pandanicolaMFLUCC 22-0151PandanaceaeThailandOP802371OP801691OP801726OP801746OP801708-
C. pandanicolaMFLUCC 22-0159PandanaceaeThailandOP802373OP801692OP801727OP801747OP801709-
C. perseaeCBS 141365 TAvocadoIsraelKX620308KX620145KX620242KX620341MZ799260-
C. proteaeCBS 132882 TProtea sp.South AfricaKC297079KC296940KC297009KC297101KC296986KC296960
C. pseudotheobromicolaMFLUCC 18-1602 TPrunus aviumChinaMH817395MH853681MH853675MH853684MH853678-
C. psidiiICMP 19120 TPsidium sp.ItalyJX010219JX009515JX009967JX010443JX009901JX009743
C. queenslandicumICMP 1778 TCarica papayaAustraliaJX010276JX009447JX009934JX010414JX009899JX009691
C. rhexiaeCBS 133134 TRhexia virginicaSussexJX145128MZ664127MZ664046JX145179MZ799258-
C. rhizophoraeMFLUCC 17-1927 TRhizophora apiculataThailandOR828933OR840847OR840870OR840864OR840858OR840853
C. rhizophoraeMFLUCC 17-1911Rhizophora apiculataThailandOR828934OR840848OR840871OR840865OR840859OR840854
C. salsolaeICMP 19051 TSalsola tragusHungaryJX010242JX009562JX009916JX010403JX009863JX009696
C. siamenseICMP 18578 TCoffea arabicaThailandJX010171JX009518JX009924JX010404JX009865FJ917505
C. siamenseHSI-3Hymenocallis littoralisChinaOM654563OM831342OM831360OM831384OM831354-
C. siamenseICMP 12567Persea americanaAustraliaJX010250JX009541JX009940JX010387JX009761JX009697
C. siamenseDAR 76934, ICMP 18574Pistacia veraAustraliaJX010270JX009535JX010002JX010391JX009798JX009707
C. siamenseICMP 12565Persea americanaAustraliaJX010249JX009571JX009937-JX009760JX009698
C. siamenseCBS 125379, ICMP 18643Hymenocallis americanaChinaJX010258GQ856776JX010060-GQ856729GQ849451
C. siamenseICMP 18121Dioscorea rotundataNigeriaJX010245JX009460JX009942JX010402JX009845JX009715
C. siamenseICMP 18117Dioscorea rotundataNigeriaJX010266JX009574JX009954-JX009842JX009700
C. siamenseICMP 18739Carica papayaSouth AfricaJX010161JX009484JX009921-JX009794JX009716
C. siamenseICMP 18570Persea americanaSouth AfricaJX010248JX009510JX009969-JX009793JX009699
C. siamenseICMP 18569Persea americanaSouth AfricaJX010262JX009459JX009963-JX009795JX009711
C. siamenseHKUCC 10884, ICMP 18575Capsicum annuumThailandJX010256JX009455JX010059-JX009785JX009717
C. siamenseHKUCC 10881, ICMP 18618Capsicum annuumThailandJX010257JX009512JX009945-JX009786JX009718
C. siamenseICMP 18572Vitis viniferaUSAJX010160JX009487JX010061-JX009783JX009705
C. siamenseICMP 18571Fragaria × ananassaUSAJX010159JX009482JX009922-JX009782JX009710
C. siamenseICMP 17795Malus domesticaUSAJX010162JX009506JX010051JX010393JX009805JX009703
C. siamenseCBS 125378 (T), ICMP 18642Hymenocallis americanaChinaJX010278GQ856775JX010019JX010410GQ856730JX009709
C. siamenseCBS 130420 (T), ICMP 19118Jasminum sambacVietnamHM131511HM131507HM131497JX010415JX009895JX009713
C. siamenseICMP 17785Malus domesticaUSAJX010272JX009446JX010058-JX009804JX009706
C. siamenseICMP 18573Vitis viniferaUSAJX010271JX009435JX009996-JX009784JX009712
C. siamenseICMP 18118Commelina sp.NigeriaJX010163JX009505JX009941-JX009843JX009701
C. siamenseMFLUCC 22-0109PandanaceaeThailandOP740246OP744511OP744513OP744514OP744512-
C. siamenseMFLUCC 22-0135PandanaceaeThailandOP802374OP801693OP801728OP801748OP801710-
C. siamenseMFLUCC 22-0137PandanaceaeThailandOP802362OP801686OP801721OP801740OP801703-
C. siamenseMFLUCC 22-0138PandanaceaeThailandOP802366OP801688OP801723OP801742OP801705-
C. siamenseCGMCC 3.16078 TAgeratina adenophoraChinaOK030876OK513613OK513679OK513645OK513575-
C. subhenanenseCGMCC 3.16073 TAgeratina adenophoraChinaOK030883OK513618OK513684OK513647OK513581-
C. syzygiicolaMFLUCC 10-0624 TSyzygium samarangenseThailandKF242094KF157801KF242156KF254880-KF254859
C. tainanenseCBS 143666 TCapsicum annuumTaiwan (China)MH728818MH781475MH728823MH846558MH805845-
C. temperatumCBS 133122 TVaccinium macrocarponBronxJX145159MZ664125MZ664045JX145211MZ799254-
C. tengchongenseYMF 1.04950, CGMCC 3.18950 TIsoetes sinensisChinaOL842169OL981238OL981264-OL981290-
C. theobromicolaICMP 18649 TTheobroma cacaoPanamaJX010294JX009444JX010006JX010447JX009869JX009591
C. thailandicaMFLUCC 17-1924 TRhizophora apiculataThailandOR828935OR840849OR840872OR840866OR840860OR840855
C. tiICMP 4832 TCordyline sp.New ZealandJX010269JX009520JX009952JX010442JX009898JX009649
C. tropicaleICMP 18653 TTheobroma cacaoPanamaJX010264JX009489JX010007JX010407JX009870JX009719
C. tropicaleMAFF 239933, ICMP 18672Litchi chinensisJapanJX010275JX009480JX010020JX010396JX009826JX009722
C. tropicaleCBS 124943, ICMP 18651Annona muricataPanamaJX010277JX009570JX010014-JX009868JX009720
C. tropicaleNTUCCRhizophora mucronataTaiwan (China)-OR840850-OR840867OR840861-
C. viniferumCBS130643 TVitis vinifera cv. ShuijingChinaJN412804JN412795JN412798--JQ309639
C. vulgarisYMF 1.04940, CGMCC 3.18940 THippuris vulgarisChinaOL842170OL981239OL981265-OL981291-
C. wuxienseCGMCC 3.17894 TCamellia sinensisChinaKU251591KU251672KU252045KU252200KU251939KU251833
C. xanthorrhoeaeICMP 17903 TXanthorrhoea preissiiAustraliaJX010261JX009478JX009927JX010448JX009823JX009653
C. xishuangbannaenseMFLUCC 19-0107 TMagnolia liliiferaChinaMW346469MW652294MW537586-MW660832-
C. yuanjiangenseCGMCC 3.18964 TAgeratina adenophoraChinaOK030885OK513620OK513686OK513649OK513583-
C. yulongenseCFCC 50818 TVaccinium dunalianum var. urophyllumChinaMH751507MH777394MK108986MK108987MH793605MH793604
BRIP—Queensland Plant Pathology Herbarium; CBS—CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands; CFCC—China Forestry Culture Collection Center; CGMCC—China General Microbiological Culture Collection Center; ICMP—International Collection of Microorganisms from Plants; IMI—International Mycological Institute; MFLUCC—Mae Fah Luang University Culture Collection, Chiang Rai, Thailand; NTUCC—the Department of Plant Pathology and Microbiology, National Taiwan University Culture Collection. T Ex-type strains. Strains in this study are in bold.
Table 3. The best-fit nucleotide substitution model for each dataset, selected by AIC in MrModeltest. 2.2.
Table 3. The best-fit nucleotide substitution model for each dataset, selected by AIC in MrModeltest. 2.2.
GeneSubstitution Model
ITSSYM+I+G
act-exonHKY
gapdh-exonF81
β-tubulin-exonGTR+G
chs-1-exonK80+G
cal-exonSYM+G
act-intronK80+G
gapdh-intronHKY+G
β-tubulin-intronK80+G
cal-intronSYM+G
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Norphanphoun, C.; Hyde, K.D. First Report of Colletotrichum fructicola, C. rhizophorae sp. nov. and C. thailandica sp. nov. on Mangrove in Thailand. Pathogens 2023, 12, 1436. https://doi.org/10.3390/pathogens12121436

AMA Style

Norphanphoun C, Hyde KD. First Report of Colletotrichum fructicola, C. rhizophorae sp. nov. and C. thailandica sp. nov. on Mangrove in Thailand. Pathogens. 2023; 12(12):1436. https://doi.org/10.3390/pathogens12121436

Chicago/Turabian Style

Norphanphoun, Chada, and Kevin D. Hyde. 2023. "First Report of Colletotrichum fructicola, C. rhizophorae sp. nov. and C. thailandica sp. nov. on Mangrove in Thailand" Pathogens 12, no. 12: 1436. https://doi.org/10.3390/pathogens12121436

APA Style

Norphanphoun, C., & Hyde, K. D. (2023). First Report of Colletotrichum fructicola, C. rhizophorae sp. nov. and C. thailandica sp. nov. on Mangrove in Thailand. Pathogens, 12(12), 1436. https://doi.org/10.3390/pathogens12121436

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