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Article

Taxonomy and Phylogeny of Endophytic Fungi (Chaetomiaceae) Associated with Healthy Leaves of Mangifera indica in Yunnan, China

by
Er-Fu Yang
1,2,
Samantha C. Karunarathna
1,*,
Dong-Qin Dai
1,
Alviti Kankanamalage Hasith Priyashantha
2,
Itthayakorn Promputtha
2,
Abdallah Elgorban
3 and
Saowaluck Tibpromma
1,*
1
Center for Yunnan Plateau Biological Resources Protection and Utilization, College of Biological Resource and Food Engineering, Qujing Normal University, Qujing 655011, China
2
Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand
3
Center of Excellence in Biotechnology Research (CEBR), King Saud University, Riyadh 145111, Saudi Arabia
*
Authors to whom correspondence should be addressed.
Diversity 2023, 15(10), 1094; https://doi.org/10.3390/d15101094
Submission received: 24 August 2023 / Revised: 15 September 2023 / Accepted: 25 September 2023 / Published: 20 October 2023
(This article belongs to the Special Issue The Hidden Fungal Diversity in Asia 2.0)
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Abstract

:
Mangoes belong to Mangifera (Anacardiaceae), which contains 69 species, but only Mangifera indica is popularly cultivated and commercialized. Mango is one of the most important crops grown in China’s Yunnan Province and significantly contributes to the economic security of these locals. Endophytic fungi have been recognized as beneficial microbes that improve plant growth, productivity, and survivability under environmental stress. Nevertheless, many host plant-related endophytic fungi are yet to be identified, including the mango-related species. During this study, we recognized three different fungal species in the family Chaetomiaceae derived from healthy mango (Mangifera indica) leaves based on morphological examinations coupled with multi-gene phylogenetic analysis (ITS, LSU, rpb2, and tub2). These species are Dichotomopilus funicola (KUNCC23-13347) and Humicola wallefii (KUNCC22-10759, 23-13348), derived from new hosts, and a new species of Arcopilus hongheensis (KUNCC22-10767, 23-13346).

1. Introduction

Mango is a deep-rooted, evergreen plant belonging to the genus Mangifera (Anacardiaceae), with 69 species and over 1500 verities [1,2]. Nonetheless, among them, Mangifera indica is the most commonly cultivated species in worldwide farmlands and home yards [1,2]. The cultivation of mango, particularly in China, has a history of over 1300 years, with more than 40 different varieties [3]. China was the second largest mango producing country, where 3,483,500 metric tons of fruits were harvested from 359,600 hectares plantation in 2020 [3]. Mango has been a significant source of income for rural communities in the main growing areas of Baoshan, Honghe, Huaping, Simao, and Yuanjiang in Yunnan [3,4].
Fungal endophytes are an intriguing group that resides within the intracellular and/or extracellular spaces of plant tissues without causing any adverse effects or visible disease symptoms among the hosts [5]. Endophytic fungi offer a number of benefits to plants, such as protecting hosts from abiotic (e.g., drought, high temperature, and waterlogging) and biotic (e.g., pathogens and insect pests) stresses and promoting plant growth and germination [6,7,8,9]. Moreover, owing to their numerous properties, such as anticancer, antidiabetic, biocontrol, immunosuppressive, and insecticidal potentials, endophytes are often used in agricultural, industrial, pharmaceutical, and medical sectors [10,11,12]. Even though endophytes are among the most widely studied groups of fungi, studies of mango-associated endophytes are comparatively limited. Nevertheless, according to the available studies, a considerable number of endophytes associated with mango were recognized—for example, Vieira et al. [13] isolated 22 strains of endophytic Colletotrichum from leaves, stem fragments, and mature inflorescence images of sampled mango plants. In another study, Dashyal et al. [14] recognized 35 fungal endophytes only using the stems and leaves of mango. Similarly, Yang et al. [15] isolated 34 different fungal endophytic strains from mango leaves. Further, they found that some endophytes are capable of serving as bio-control agents.
Previous diversity studies have found that Chaetomiaceae could be the dominant group of endophytic fungi present in mango leaves [15]. In this study, we isolated the Chaetomiaceae species from fresh and healthy leaves of mango. The new endophytic fungus viz. Arcopilus hongheensis, two new records of viz. Dichotomopilus funicola, and the known species viz. Humicola wallefii are described via detailed morphological comparisons and four-gene molecular phylogenetic analyses.

2. Materials and Methods

2.1. Samples Collection and Fungi Isolation

The fresh and healthy leaf samples were randomly picked from commercially cultured mango trees in Honghe Prefecture, Yunnan, China (102°50′11′′ E, 23°41′01′′ N); carefully arranged in separate polythene bags; and taken to the mycology laboratory for fungal endophyte isolation [16]. Firstly, the samples were cleaned with tap water, and each leaf was cut into several small pieces (1 × 1 cm; middle parts of leaves). The leaf pieces were surface sterilized using 3% sodium hypochlorite (NaOCl) for 2 min, followed by three repeated washings with sterilized water. Further, surface sterilization was carried out via washing with 75% ethanol (C2H6O) for 2 min and three series of washing with sterile distilled water and allowed to dry under the laminar flow cabinet. Then, the edges of the leaf pieces were trimmed, transferred onto potato dextrose agar (PDA) plates, and incubated at 27 °C for 2–15 days [17,18]. When individual hyphal tips grew out from the leaf blade, the mycelia were picked using sterilized needles, placed onto new PDA plates, and incubated at 27 °C for one month. Once endophytic fungi were sporulated in PDA, their dry cultures were deposited in the Kunming Institute of Botany, Academia Sinica (HKAS) herbarium, and the live cultures were deposited in the Kunming Institute of Botany Culture Collection (KUNCC).

2.2. Microscopic Examination

The morphology of Chaetomiaceae species was followed Wang et al. [19] and cultured on PDA media (1–3 months at 27 °C) to induce the development of ascomata. Mycelia masses, fruiting bodies, ascomatal hairs, ascomata, and ascospores were initially observed. The colony morphologies of Chaetomiaceae species were captured by measuring micro-morphological characteristics in distilled water (some asci and ascospores were strained in Lugol’s iodine solution), and slides were observed. The color codes in the manuscript followed colorhexa (http://www.colorhexa.com, accessed on 14 September 2023) [20]. The fungi micro-structure sizes were measured using the Tarosoft (R) Image Frame Work program, and color photo-plates of the micro-structures were combined using Adobe Photoshop CS3 Extended v. 10.0 (Adobe®, San Jose, CA, USA).

2.3. DNA Extraction, PCR Amplification, and Sequencing

Fungal mycelia were removed from the colonies on PDA using sterilized needles and transferred into 1.5 mL centrifugal tubes for DNA extraction. Genomic DNA extraction followed the instructions of the manufacturer of the Biospin Fungus Genomic DNA Extraction Kit-BSC14S1 (BioFlux®, Beijing Bio Teke Corporation, Beijing, China). A part of the extracted DNA was used as a template to perform Polymerase Chain Reaction (PCR), while the remaining part of the DNA solution was stored at −20 °C for long-term preservation. The PCR reaction mixture was 25 µL in total, including 8.5 µL of double-distilled water (ddH2O), 12.5 µL of 2 × Power Taq PCR Master Mix (mixture of EasyTaqTM DNA Polymerase, dNTPs, and optimized buffer; Beijing Bio Teke Corporation—Bio Teke, Beijing, China), 2 µL of DNA template, and 2 µL of forward and reverse primers. The regions of internal transcribed spacer (ITS) and large subunit ribosomal RNA (LSU) were amplified using the primers ITS4/ITS5 and LR5/LROR [21,22]. The PCR condition of ITS and LSU was created using an initial denaturation step of 3 min at 94 °C, followed by 35 cycles of 30 s at 94 °C, 50 s at 55 °C, and 1 min at 72 °C and a final denaturation step of 10 min at 72 °C [23]. The partial RNA polymerase II subunit (rpb2) region was amplified using the primers fRPB2-5F and fRPB2-7cR [24]. The PCR condition of rpb2 started with the initial denaturation at 95 °C for 3 min, followed by 35 cycles of denaturation at 95 °C for 45 s, annealing at 57 °C for 50 s, and extending 90 s at 72 °C, as well as an extension at 72 °C for 10 min [23]. The beta-tubulin (tub2) was amplified using the primers T1 and T22 [25]. The PCR condition of tub2 gene began with an initial denaturation step of 3 min at 94 °C, followed by 35 cycles of 30 s at 94 °C, 50 s at 52 °C, and 1 min at 72 °C and a final denaturation step of 10 min at 72 °C [26]. The PCR products were sent to Beijing Bio Teke Corporation (Beijing, China) for purification and sequencing.

2.4. Phylogenetic Analyses

The forward and reverse sequences were combined in Geneious (Restricted) 9.1.2 (https://www.geneious.com, accessed on 12 June 2023) and subjected to BLASTn searches in the GenBank (http://blast.ncbi.nlm.nih.gov/, accessed on 12 June 2023) [27] to select the species names, strains, and accession numbers of the most closely related genera/taxa by forming a spreadsheet of all involved species. Sequence alignments were carried out via the server version of MAFFT using default settings (http://mafft.cbrc.jp/alignment/server, accessed on 2 May 2023) [28], and we edited the beginning and end in BioEdit 7.2.3 [29]. Ambiguous and uninformative regions were removed via trimAL v1.2 (http://trimal.cgenomics.org, accessed on 12 June 2023), and sequences were manually combined using BioEdit. The alignment transformation environment (ALTER) online program was used to convert Fasta files to the PHYLIP (for ML) and NEXUS (for BI) formata [30]. Maximum likelihood analysis (ML) was carried out by selecting RAxML-HPC2 via the XSEDE (8.2.12) [31] and GTRGAMMA substitution models at 1000 bootstrap iterations via the CIPRES Science Gateway platform v.3.3 (http://www.phylo.org/portal2, accessed on 12 June 2023, [32]). Bayesian analysis was conducted via MrBayes v. 3.1.2 [31,33] in the CIPRES Science Gateway platform to evaluate posterior probabilities (PP) [34] using Markov Chain Monte Carlo sampling (MCMC). The GTR+I+G evolution model was also applied in the BI analyses. Bayesian analyses of six simultaneous Markov chains were run for 1,000,000 generations, and trees were sampled and printed to output at every 100th generation (resulting in 10,000 trees in total). Phylogenetic trees were visualized using FigTree v1.4.0 [35], and the final tree was formed via Microsoft PowerPoint 2006 version.

3. Results

3.1. Phylogenetic Results

The concatenated LSU, ITS, rpb2, and tub2 sequence datasets consisted of 83 fungal strains of genera, including Achaetomiella, Arcopilus, Collariella, Dichotomopilus, Humicola, and Pseudohumicola, with Trichocladium tomentosum (CBS 144476) and T. uniseriatum (LC3756) used as the outgroups [19,36]. The combined sequence matrix comprises a total of 83 fungal strains and 2509 characters (563 characters for LSU, 594 characters for ITS, 525 characters for rpb2, and 827 characters for tub2). A phylogenetic investigation based on maximum likelihood analysis yielded the best RAxML tree, with a final likelihood value of −27,870.158799. The matrix consisted of 1188 distinct alignment patterns with 13.04% undetermined characters or gaps. The estimated base frequencies were as follows: A = 0.227002; C = 0.285086; G = 0.282451; T = 0.205461. Substitution rates: AC = 1.108152; AG = 3.236434; AT = 1.315296; CG = 1.271850; CT = 5.563544; GT = 1.000000. Gamma distribution: shape parameter α = 1.135475. The final average standard deviation of the split frequencies at the end of entire MCMC generations was found to be 0.009914 via BI analysis. There were five newly isolated strains. KUNCC23-13347 was basal to Dichotomopilus funicola strains, with 99% via ML and 1.00 via BYPP statistical support (Figure 1); KUNCC22-10767 and KUNCC23-13346 were basal and well separated with Arcopilus navicularis (CCF 3252), with 99% via ML and 1.00 via BYPP statistical support (Figure 1); and KUNCC22-10759 and KUNCC23-13348 were grouped with H. wallefii (CBS 147.67), with 81% via ML and 0.99 via BYPP statistical support (Figure 1).

3.2. Taxonomy

  • Arcopilus X. Wei Wang, Samson & Crous, Studies in Mycology 84: 159 (2016) [36]
Index Fungorum number: IF818835
Type species: Arcopilus aureus (Chivers) X. Wei Wang & Samson, Studies in Mycology 84: 217 (2016) [36]
Notes: The genus Arcopilus was introduced by Wang et al. [36] with the type species A. aureus. The colonies of Arcopilus usually present yellowish to light orange or red, with rust exudates [36]. Currently, Arcopilus contains 13 species [19,37]. Arcopilus species are used to control phytopathogens, and are processed into bioformulates and commercial products (e.g., BIOKUPRUMTM, AgriLife corporation, Andhra Pradesh, India; and Ketomium®, GreenBiomix corporation, Ho Chi Minh, Vietnam). Many studies reported that bioactive metabolites from Arcopilus species have antibacterial, anticancer, and antivirus properties [38,39,40,41].
  • Arcopilus hongheensis E.F. Yang & Tibpromma, sp. nov.
Index Fungorum number: IF900233
Etymology: The name reflects the location “Honghe” where the holotype was collected.
Holotype: HKAS 129059
Descriptions: Endophytic on fresh and healthy Mangifera indica leaves, and colonies on PDA sporulated after three months (Figure 2). Sexual morph: Ascomata 100–140 × 80–95 µm ( x ¯ = 120 × 85 µm, n = 10), superficial, ostiolate, with ascomatal hairs, ellipsoid or subglobose. Ascomatal wall brown (#463727), membranaceous, comprised of dark-brown, thick-walled cells of textura angularis. Terminal hairs 4–6 µm wide at the base, verrucose, olivaceous (#849238) to brown (#d18e4a) in reflected light, septate, dark brown, fading and tapering towards the tips, arcuate, circinate to coiled, lateral hairs flexuous or apically incurved. Asci appeared quickly when the culture matured; they could not be seen during observation. Ascospores 10–14 × 6–8.5 µm ( x ¯ = 12 × 7.3 µm, n = 20), limoniform, verrucose, olivaceous (#849238) to brown (#d18e4a) after maturing, with a germ pore. Asexual morph: Undetermined.
Culture characteristics: Colonies growing on PDA are around 60 mm in diameter after one month. Mycelium 2–3 ( x ¯ = 2.5 µm, n = 10) µm wide, hyaline (#f2f2f2), branched, septate, smooth-walled. Colonies were observed to be effuse, circular, dense, flat, white (#e6e6e6) to yellowish (#e6e600) outwardly, entire edge, slightly striated, and pale brown at the reverse. Forming a few dark-brown fruiting bodies after three months in PDA, also produced reddish brown (#7d2020) pigments in PDA.
Material examined: China, Yunnan Province, Honghe, Menglong Village, on fresh and healthy leaves of Mangifera indica (102°50′11″ E, 23°41′01″ N, 500 m), 22 December 2020, E.F. Yang, Mg005 (HKAS 129059, holotype), ex-type living culture KUNCC22-10767, KUMCC 23-13346. GenBank numbers: KUNCC22-10767 = ITS; OR117280, LSU: OR117285; rpb2: OR119771; tub2: OR119776. KUMCC 23-13346 = ITS: OR117279; LSU: OR117284; rpb2: OR119770; tub2: OR119775.
Notes: The colonies of Arcopilus usually present yellowish to orange or red [36], and our isolates also showed reddish brown (#7d2020) in PDA, and produced limoniform to reniform, verrucose, olivaceous (#849238) to brown (#87744b) ascospores. The multi-gene analyses showed that our isolates are closely related but separated from A. navicularis (CCF 3252), with 99% via ML and 1.00 via BYPP statistical support (Figure 1). Moreover, they have different-sized ascospores (10–14 × 6–8.5 µm vs. 7.2–8.8 × 4.5–5.5 µm) and ascospores with different characteristics (broadly navicular in side view, lemon-shaped seen from above, dark brown vs. limoniform, verrucose, and olivaceous (#849238) to brown (#87744b)) [42]. Therefore, we introduced Arcopilus hongheensis as a new endophytic species on healthy mango leaves based on morphological comparisons and phylogenetic analyses.
  • Dichotomopilus X. Wei Wang, Samson & Crous, Studies in Mycology 84: 185 (2016) [36]
Index Fungorum number: IF818840
Type species: Dichotomopilus indicus (Corda) X. Wei Wang & Samson, Studies in Mycology 84: 189 (2016) [36]
Notes: The chaetomium-like genus Dichotomopilus was first established by Wang et al. [36], and to date, it contains 13 species [37]. However, the potential values of Dichotomopilus funicola were well studied, with Gu et al. [43] recently reporting that endophytic D. funicola is a good source of vitexin, which has antioxidant potential. Further, Nayak et al. [44] identified Dichotomopilus funicola as a laccase producer.
  • Dichotomopilus funicola (Cooke) X. Wei Wang & Samson, Stud. Mycol. 84: 189 (2016) [36]
Index Fungorum number: IF818841
Description: Endophytic on fresh and healthy Mangifera indica leaves, colonies on PDA sporulated after about half a month (Figure 3). Sexual morph: Ascomata 165–220 × 152–200 µm ( x ¯ = 190 × 175 µm, n = 20), superficial, ostiolate, spherical, ellipsoid to ovate. Ascomatal hairs 3–7 μm wide, seta-like at the beginning, and developed to apically branched later, erect, tapering towards tips. Ascomatal wall brown (#463727), thick-walled cells of textura intricata or epidermoidea. Asci 15–22 × 9–13 µm ( x ¯ = 18.5 × 11 µm, n = 30), fasciculate, clavate, pyriform to ovate, hyaline (#e5e5e5) to brown, with eight irregularly arranged ascospores, evanescent quickly. Ascospores 5–6.5 × 3–5 µm ( x ¯ = 5.5 × 4 µm, n = 30), olivaceous (#849238) to brown (#b0906f), bilaterally flattened, verrucose, with one apical germ pore. Asexual morph: Undetermined.
Culture characteristics: Colonies can grow on PDA, and they reached around 70 mm in diameter after one month and appeared to be white (#f2f2f2). Mycelium 1.5–4 ( x ¯ = 3 µm, n = 10) µm wide, hyaline (#f2f2f2), branched, septate, thick-walled. Obverse: flat or effuse, hyaline, lobate to the crenated edge, fertile near the margin with numerous fruiting bodies; Reverse: yellowish brown (#cdcd00), excluding reddish brown (#cc8236) at the center. Without pigments produced in PDA.
Known substratum: Isolated from dust [36]; Endophytic on pigeon pea [43]; Soil sample [44]; Isolated from fresh and healthy leaves of Mangifera indica (This study).
Known distribution: USA [36]; India [44]; China [43], this study.
Material examined: China, Yunnan Province, Honghe Menglong Village, on fresh and healthy leaves of Mangifera indica (102°50′11″ E, 23°41′01″ N, 500 m), 22 December 2020, E.F. Yang, EF22 (HKAS 129060), living culture KUNCC23-13347. GenBank numbers: ITS: OR117276, LSU: OR117281, rpb2: OR119767, tub2: OR119772.
Notes: Our isolate fits well with the concept of Dichotomopilus, as it has seta-like and apically branching ascomatal hairs and olivaceous, bilaterally flattened, and verrucose asci [36]. The multi-gene analyses showed our isolates group with Dichotomopilus funicola strains (Figure 1), and our isolate shares similar-sized ascospores with Dichotomopilus funicola (5–6.5 × 3–5 µm vs. 5–6 × 3.5–4.8 × 3–3.8 μm) [36]. Thus, we reported a new host record of Dichotomopilus funicola associated with Mangifera indica leaves based on morphology and phylogeny. Previously, D. funicola was isolated from dust and soil as a saprobic fungus [36,44] and an endophytic element on pigeon peas [43]. In this study, D. funicola was isolated as an endophytic fungus from fresh and healthy leaves of Mangifera indica.
  • Humicola Traaen, Nytt Magazin for Naturvidenskapene 52: 31 (1914) [45]
Index Fungorum number: IF8566
Type species: Humicola fuscoatra Traaen, Nytt Magazin for Naturvidenskapene 52: 33 (1914). [45]
Notes: The genus Humicola was established by Traaen [45] to be part of the type species H. fuscoatra, and it is typically regarded as an asexual genus in the Chaetomiaceae [46]. The sexual morphs of Humicola are similar to Chaetomium and chaetomium-like fungi [47]. In contrast, the asexual morphs of Humicola produce pigmented, single-celled, thick-walled conidia and lateral, terminal, or connected and poorly developed conidiophores [48]. Wang et al. [47] revised the classification of Humicola and humicola-like taxa in the Chaetomiaceae based on multi-locus phylogenic analyses and morphological examinations. Wang et al. [19] constructed the phylogenetic relationships of 20 different Humicola species. Humicola taxa are often found in compost habitats, dirt, soil, decayed plant materials, indoor spaces, and even cat fur [49,50,51]. Interestingly, some Humicola species also act as mycoparasites and have the ability to invade and colonize the hyphae or survival structures of other fungal species, e.g., H. fuscoatra isolated from Aspergillus favus sclerotia [52]. Humicola also contains thermophilic fungi that are capable of degrading complicated natural substrates, and as a result, they have the potential to be a rich source of enzymes used in biotechnological and commercial applications, such as cellulases, feruloyl esterases, pectate lyases, xylanases, and β-xylosidases [43,44,45,46,47,48,49,50,51,52,53,54,55,56].
  • Humicola wallefii (J.A. Mey & Lanneau) X. Wei Wang & Houbraken, Studies in Mycology 93: 107 (2018) [47]
Index Fungorum number: IF824452
Descriptions: Endophytic on fresh and healthy leaves of Mangifera indica. Colonies on PDA sporulated for around one month (Figure 4). Sexual morph: Ascomata 258–355 × 170–260 µm ( x ¯ = 300 × 215 µm, n = 20), superficial, ostiolate, ellipsoidal to ovoid, ascomatal hairs present buff (#f0dc82) to pale luteous (#80ff00) in reflected light. Ascomatal wall composed of brown, thick-walled cells of textura angular to irregular. Terminal hairs 2–4 μm wide near the base, and flexuous to undulate, septate, verrucose, lateral hairs straight, arcuate. Asci 33–52 × 10–15 µm ( x ¯ = 45 × 12.5 µm, n = 20), clavate, with eight biseriate ascospores. Ascospores 10–12 × 6–9 µm ( x ¯ = 11 × 8 µm, n = 20), limoniform, white (#d9d9d9) to olivaceous (#b9c194) to brown (#9aa52a) with the maturity, bilaterally flattened, umbonate at both ends, with an apical germ pore. Asexual morph: Mycelium 3–10 ( x ¯ = 4.5 µm, n = 20) µm wide, hyaline (#f2f2f2) to yellowish brown (#e6d300), and branched. Conidia 11–14.5 μm ( x ¯ = 12.5 µm, n = 30) diam., usually formed on the side of vegetative hyphae, globose to oblate, solitary, yellowish-brown (#b3a400), thick-walled, slightly verruculose.
Culture characteristics: Colonies growing on PDA reach around 40 mm in diameter after a month. Obverse: raised, circular, low dense, entire edge, white (#e6e6e6), visible numerous fruiting bodies scattered on the surface of the colonies, aerial mycelium white (#e6e6e6); Reverse: pale brown (#b0906f) to brown (#e6e600). Without pigments formed in PDA.
Known substratum: Isolated from soil [47]; isolated from fresh and healthy Mangifera indica leaves (This study).
Known Distribution: DR Congo [47]; China (This study).
Material examined: China, Yunnan Province, Honghe Menglong Village, on fresh and healthy leaves of Mangifera indica (102°50′11″ E, 23°41′01″ N, 500 m), 22 December 2020, E.F. Yang, EF24 (HKAS 129061), living culture KUNCC22-10759, KUNCC23-13348. GenBank numbers: KUNCC22-10759 = ITS: OR117278, LSU: OR117283, rpb2: OR119769, tub2: OR119774; KUNCC23-13348 = ITS: OR117277, LSU: OR117282, rpb2: OR119768, tub2: OR119773.
Notes: Our isolate produced similar conidia with the asexual genus Humicola in Chaetomiaceae, as well as similar Chaetomium-like ascospores. Our isolates share similar size asci and ascospores to those of Humicola wallefii CBS 147.67 (Asci: 50 × 7–8 µm vs. 33–52 × 10–15 µm; Ascospores: 6.5–8 × 4.5–6.5 vs. 10–12 × 6–9 µm). In the previous study, H. wallefii was isolated from the soil as a saprobic fungus [47]. The multi-gene phylogenetic tree also indicated that our isolates were closely related to the strains of Humicola wallefii (CBS 147.67) with high statistical support (Figure 1). Here, we introduced a new host and country record of Humicola wallefii based on morphology and multigene phylogeny.

4. Discussion

Based on multi-gene phylogenetic analyses and their morphological characteristics, 280 species in 50 genera belonging to the family Chaetomiaceae have been reported to date [19,36,37]. Also, the genus Chaetomium contains the largest number of species, with 192 records in the Species Fungorum [36,37]. Chaetomiaceae synthesizes many secondary metabolites with different chemical structures and shows outstanding bioactivities [57]. Species of the Chaetomiaceae are used as biological control agents for various plant diseases, as well as as bio-organic fertilizers in crop cultivation [9,15,58]. On top of that, Chaetomium species are reported as versatile weapons against various plant pathogens and act as growth promoters in maize (Zea mays), cucumbers (Cucumis sativus), and Agaricus bisporus (edible mushroom) [9,59,60,61]. Most importantly, the species in Chaetomiaceae produce industrially relevant enzymes, significantly benefiting agriculture, biotechnology, ecosystems, food production, and human health [15,62]. Those enzymes include L-methioninase, β-1,3-glucanase, laccase, dextranase, and polysaccharide mono-oxygenase and lipolytic, pectinolytic, amylolytic, chitinolytic, and proteolytic enzymes [57].
Our isolates were obtained in fresh and healthy mango leaves, and those species were probably voluntarily selected by mango hosts from soil or compost in plantations; however, this hypothesis needs to be proved via further experiments. Those isolated endophytic fungi could inoculate mango seedlings but require further testing. In addition, this study only isolated the endophytic fungi from leaf parts, as only leaves are available during the collecting time (December 2022), while endophytic fungi from roots, flowers, fruits, and stems need to be screened in future studies. We noted that the endophytic fungal diversity of plants can change with the seasons [63]; therefore, further systemic studies of endophytic fungi associated with different parts of mango and their diversity change in different seasons are necessary.
Most species of Arcopilus were previously recognized as Chaetomium until the genus Arcopilus was established by Wang et al. [36]. Based on the phylogenetic analyses (Figure 1), 13 species were accepted in this genus, including four recently introduced species [19,37,41]. Our strains (KUNCC22-10767 and KUMCC 23-13346) formed an independent group, separated from other species of Arcopilus; therefore, our isolates are considered a new species of Arcopilus. In addition, other strains, namely KUNCC23-13347 and KUNCC22-10759 (=KUNCC23-13348), were identified as Dichotomopilus funicola and Humicola wallefii, respectively, based on morphological comparisons and phylogenetic analyses. In addition, Wang et al. [19] suggested that oatmeal agar (OA) can be used as a standard medium to culture Chaetomiaceae fungi, which stimulates the production of sexual structures. Malt extract agar (MEA) and PDA are used for extrolite profiling but are not suitable for morphological studies as sexual morphs are generally poorly induced [19]. In our study, Arcopilus hongheensis also formed very low numbers of ascomata in PDA, but Dwibedi et al. [64] reported asexual structures of Arcopilus aureus to be well formed in PDA. In addition, our Dichotomopilus funicola and Humicola wallefii isolates produced a relatively high number of ascomata in PDA. Chaetomium is a well-studied group in the family Chaetomiaceae, while other genera in Chaetomiaceae have been relatively poorly studied, especially in terms of their taxonomies, metabolites, and application prospects. Chaetomiaceae fungi were previously found to be a dominant group in mango leaves [15], but this is the first study to report Arcopilus, Humicola, and Dichotomopilus (Chaetomiaceae) as being associated with mango and identify them at the species level.

Author Contributions

Conceptualization, S.C.K. and S.T.; methodology, E.-F.Y.; software, E.-F.Y.; validation, S.C.K. and S.T.; formal analysis, S.C.K., S.T. and E.-F.Y.; investigation, E.-F.Y. and A.K.H.P.; resources, S.C.K., S.T. and A.K.H.P.; writing—original draft preparation, E.-F.Y.; writing—review and editing, A.K.H.P., I.P., A.E. and E.-F.Y.; visualization, D.-Q.D., S.C.K., S.T. and E.-F.Y.; supervision, S.C.K. and S.T.; project administration, S.C.K. and S.T.; funding acquisition, S.C.K. and S.T. All authors have read and agreed to the published version of the manuscript.

Funding

Samantha C. Karunarathna and Dong-Qing Dai thank the National Natural Science Foundation of China (No. NSFC 31760013, 31950410558, 32260004), the High-Level Talent Recruitment Plan of Yunnan Province (“Young Talents” Program and “High-End Foreign Experts” Program), and the Local Colleges Applied Basic Research Projects of Yunnan Province (No. 202001BA070001-002) for their support. Erfu Yang and Itthayakorn Promputtha thank the Faculty of Science and Graduate School, Chiang Mai University, for supporting the TA/RA Ph.D. scholarship scheme. The authors extend their appreciation to the Deputyship for Research & Innovation, Ministry of Education in Saudi Arabia for funding this research work through the project no. (IFKSUOR3-299-3).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We are grateful to the Center for Yunnan Plateau Biological Resources Protection and Utilization, the College of Biological Resource and Food Engineering, Qujing Normal University, for providing the facilities used in the morphological and molecular experiments.

Conflicts of Interest

The authors declare no conflict of interest.

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Diversity 15 01094 g001
Figure 1. The phylogram of partially related genera in Chaetomiaceae constructed based on combined LSU, ITS, rpb2, and tub2 sequences. The tree is rooted with Trichocladium tomentosum (CBS 144476) and T. uniseriatum (LC3756). The BI and ML bootstrap support values are equal to or above 0.95 BYPP, and 75% are shown above the nodes’ first and second positions. Type strains are shown in bold, and newly generated strains are shown in red.
Figure 1. The phylogram of partially related genera in Chaetomiaceae constructed based on combined LSU, ITS, rpb2, and tub2 sequences. The tree is rooted with Trichocladium tomentosum (CBS 144476) and T. uniseriatum (LC3756). The BI and ML bootstrap support values are equal to or above 0.95 BYPP, and 75% are shown above the nodes’ first and second positions. Type strains are shown in bold, and newly generated strains are shown in red.
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Figure 2. Arcopilus hongheensis (HKAS 129059, holotype). (a) Colony grown on PDA (one month old); (b) Ascomata on PDA surface; (c) An ascoma; (d) Apical part of ascoma; (e) Ascomatal wall; (f–h) Immature to mature ascospores.
Figure 2. Arcopilus hongheensis (HKAS 129059, holotype). (a) Colony grown on PDA (one month old); (b) Ascomata on PDA surface; (c) An ascoma; (d) Apical part of ascoma; (e) Ascomatal wall; (f–h) Immature to mature ascospores.
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Figure 3. Dichotomopilus funicola (HKAS 129060). (a,b) Colony grown on PDA (one month old); (c,g) Close-up of ascomata; (d–f) Immature and mature ascomata; (h–j) Asci strained in Lugol’s iodine; (k,n) Branched terminal hairs; (l) Ascomatal wall; (m) Ascospores.
Figure 3. Dichotomopilus funicola (HKAS 129060). (a,b) Colony grown on PDA (one month old); (c,g) Close-up of ascomata; (d–f) Immature and mature ascomata; (h–j) Asci strained in Lugol’s iodine; (k,n) Branched terminal hairs; (l) Ascomatal wall; (m) Ascospores.
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Figure 4. Humicola wallefii (HKAS 129061): (a,b) Colonies on PDA (one month old); (c,d) Ascomata; (e) Conidia formed on hypha; (f) An ascoma; (g) Apical hairs; (h,i) Asci; (j) Ascospores; (k) Conidia with mycelium on PDA.
Figure 4. Humicola wallefii (HKAS 129061): (a,b) Colonies on PDA (one month old); (c,d) Ascomata; (e) Conidia formed on hypha; (f) An ascoma; (g) Apical hairs; (h,i) Asci; (j) Ascospores; (k) Conidia with mycelium on PDA.
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Yang, E.-F.; Karunarathna, S.C.; Dai, D.-Q.; Priyashantha, A.K.H.; Promputtha, I.; Elgorban, A.; Tibpromma, S. Taxonomy and Phylogeny of Endophytic Fungi (Chaetomiaceae) Associated with Healthy Leaves of Mangifera indica in Yunnan, China. Diversity 2023, 15, 1094. https://doi.org/10.3390/d15101094

AMA Style

Yang E-F, Karunarathna SC, Dai D-Q, Priyashantha AKH, Promputtha I, Elgorban A, Tibpromma S. Taxonomy and Phylogeny of Endophytic Fungi (Chaetomiaceae) Associated with Healthy Leaves of Mangifera indica in Yunnan, China. Diversity. 2023; 15(10):1094. https://doi.org/10.3390/d15101094

Chicago/Turabian Style

Yang, Er-Fu, Samantha C. Karunarathna, Dong-Qin Dai, Alviti Kankanamalage Hasith Priyashantha, Itthayakorn Promputtha, Abdallah Elgorban, and Saowaluck Tibpromma. 2023. "Taxonomy and Phylogeny of Endophytic Fungi (Chaetomiaceae) Associated with Healthy Leaves of Mangifera indica in Yunnan, China" Diversity 15, no. 10: 1094. https://doi.org/10.3390/d15101094

APA Style

Yang, E. -F., Karunarathna, S. C., Dai, D. -Q., Priyashantha, A. K. H., Promputtha, I., Elgorban, A., & Tibpromma, S. (2023). Taxonomy and Phylogeny of Endophytic Fungi (Chaetomiaceae) Associated with Healthy Leaves of Mangifera indica in Yunnan, China. Diversity, 15(10), 1094. https://doi.org/10.3390/d15101094

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