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Article

Endophytic Fungi Associated with Mango Show In Vitro Antagonism against Bacterial and Fungal Pathogens

by
Er-Fu Yang
1,2,3,4,†,
Samantha C. Karunarathna
1,3,†,
Saowaluck Tibpromma
3,
Steven L. Stephenson
5,
Itthayakorn Promputtha
4,6,
Abdallah M. Elgorban
7,
Salim Al-Rejaie
8 and
Putarak Chomnunti
1,*
1
School of Science, Mae Fah Luang University, Chiang Rai 57100, Thailand
2
Master of Science Program in Applied Microbiology (International Program), Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand
3
Center for Yunnan Plateau Biological Resources Protection and Utilization, College of Biological Resource and Food Engineering, Qujing Normal University, Qujing 655011, China
4
Research Center in Bioresources for Agriculture, Industry and Medicine, Chiang Mai University, Chiang Mai 50200, Thailand
5
Department of Biological Sciences, University of Arkansas, Fayetteville, AR 72701, USA
6
Environmental Science Research Center, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand
7
Department of Botany and Microbiology, College of Science, King Saud University, Riyadh P.O. Box 145111, Saudi Arabia
8
Department of Pharmacology & Toxicology, College of Pharmacy, King Saud University, Riyadh P.O. Box 145111, Saudi Arabia
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2023, 13(1), 169; https://doi.org/10.3390/agronomy13010169
Submission received: 19 November 2022 / Revised: 24 December 2022 / Accepted: 29 December 2022 / Published: 4 January 2023
(This article belongs to the Special Issue Promoting Sustainable Agriculture through the Manipulation of Plant-Associated Microbial Communities)
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Abstract

:
Endophytic fungi live in inter-cellular spaces of healthy plant tissues without causing any apparent symptoms of diseases for the host plant. Some fungal endophytes help their plant hosts to survive under biotic and abiotic stresses. In this study, we collected healthy mango leaves at the Honghe mango plantations (Yunnan Province) in the winter. A total of 34 different fungal endophytic strains were isolated, and their phylogenetic placements were estimated based on the ITS gene. Members of genus Chaetomium were the dominant fungal endophytes (26%). Common bacterial plant pathogens (Erwinia amylovora and Pseudomonas syringae) and fungal plant pathogens (Botrytis cinerea and Penicillium digitatum) were selected to test the antagonism of the fungal endophytes isolated from mango leaves through co-cultivation in vitro assay. Three strains of Chaetomium sp. viz. KUNCC22-0749, UNCC22-10750, and KUNCC22-10752 showed great inhibition against two bacterial pathogens viz. Erwinia amylovora and Pseudomonas syringae, and Alternaria sp. KUNCC22-10760, Chaetomium sp. KUNCC22-10749, Daldinia sp. KUNCC22-10744, and Rosellinia sp. KUNCC22-10751 also showed great to moderate antagonistic effects against two fungal pathogens viz. Botrytis cinerea and Penicillium digitatum.

1. Introduction

Phytopathogenic fungi are among the dominant agents of plant diseases that result in enormous losses in yield and quality of field crops, fruits, and other edible plant materials [1]. Based on the mode of nutrition, phytopathogenic fungi are normally classified into two major groups: biotrophic and necrotrophic pathogens. Biotrophic pathogens (biotrophs) have close relationships with their hosts and are able to use living tissues to obtain nutrients, while necrotrophic pathogens (necrotrophs) kill plant tissues and obtain nutrients [2]. Fungal infections cause a wide variety of disease symptoms [3]. Green mold and associated decay caused by Penicillium digitatum is the most devastating disease in postharvest citrus fruits (oranges, tangerines, lemons, and grapefruit). About 90% of postharvest losses in citriculture have been observed to be caused by P. digitatum in arid regions and tropical subclimates [4,5]. In addition, Botrytis cinerea (teleomorph Botryotinia fuckeliana) has been reported to attack mainly more than 200 dicotyledonous plants, especially as the causal agent of grey mold or botrytis bunch rot in vineyards, causing serious economic losses worldwide [6,7,8].
Phytopathogenic bacteria are important plant pathogens widespread throughout the world [9]. Rajesh-Kannan et al. [10] estimated that about 150 bacterial species are responsible for different plant diseases, and they mainly belong to three families: Enterobacteriaceae, Pseudomonaceae, and Xantomonadaceae. Erwinia amylovora (Enterobacteriaceae), a causal agent of fire blight on a variety of host species in the Rosaceae, causes severe hazards to the production of Malus, Pyracantha, Pyrus, and Rubus [11,12,13]. Moreover, Pseudomonas syringae (Pseudomonaceae) includes 15 identified species and more than 60 pathovars [14]. Almost all Pseudomonas syringae pathovars are able to infect over 180 plant species and are exceedingly difficult to control, especially since they result in bacterial cankers on various economically significant fruits crops from genera Actinidia, Mangifera, and Prunus [15,16,17,18]. Pseudomonas syringae pv. syringae is known as the most polyphagous bacterium that has a broad host range [17,19]. Mansfield et al. [20] mentioned that both E. amylovora and P. syringae are listed among the top 10 plant pathogenic bacteria.
The word “endophyte” is derived from Greek, meaning inside or within plants [21]. Endophytic fungi live entirely within plant tissues without causing any apparent symptoms of diseases and emerge to sporulate at the plant or host-tissue senescence [22,23]. Several factors influence biological characteristics of endophytes, such as host species, host developmental stage, inoculum density, and environmental conditions, and they play a significant role in the control of plant pathogen communities [24]. Endophytic fungi help plant hosts survive under biotic and abiotic stresses, and considerable evidence has shown that some endophytic fungi have the ability to protect host plants from attacks from pathogens and insects [25] and environmental stresses [26,27]. However, the delicate relationships between most fungal endophytes and their plant hosts have still not been well understood [28,29]. In addition, the secondary metabolites produced by endophytic fungi appear to have potential as anticancer, insecticidal, antidiabetic, immunosuppressive, and biocontrol agents. Therefore, the intensive studies of endophytic fungi will be helpful in the industrial, pharmaceutical, medical, and agricultural sectors [30].
Mango-associated fungal endophytes have been poorly studied. Vieira et al. [31] isolated 22 fungal endophytic strains of Colletotrichum associated with mango in South China. Dashyal et al. [32] isolated 35 strains of endophytic fungi from the stem and leaves of 10 mango varieties. In recent years, endophytic fungi have been regarded as exciting novel sources of new bioactive compounds, with reports from a variety of hosts [33,34,35]. Nwakanma et al. [36] reported that secondary metabolites of endophytic fungi isolated from bush mango leaves have antimicrobial activities. Phytopathogenic bacteria and fungi are severe on economic crops, and chemical treatments are the most used control strategies [1,9,37,38]. However, as a result of the widespread and repeated use of certain chemical fungicides, a number of pathogenic strains have become fungicide-resistant, and fungicide residues have caused environmental pollution and harmed soil and water animals [39]. Endophytic fungi are eco-friendly and effective biocontrol agents against various bacterial and fungal pathogens [40,41], while endophytic fungi associated with mango are poorly studied. Therefore, investigating the diversity of endophytic fungi associated with mango and screening the antagonistic strains are useful for controlling fungal and bacterial pathogens in the field. The aims of this study were to investigate the endophytic fungi associated with mango and screen endophytic strains with biocontrol potentials.

2. Materials and Methods

2.1. Sampling Mango Leaves and Endophytes Isolation

Fresh and healthy mango leaves were picked from well-managed trees in the Honghe prefecture, Yunnan Province, in December 2020 (Figure 1). The local GPS and elevation information (102°50′11″ E, 23°41′01″ N, 500 ± m) was recorded, and 100 leaves were picked from different mango trees and transported to the mycology laboratory in disposable sterilized bags. Tibpromma et al. [42] was followed for the isolation of endophytic fungi. The collected leaf samples were washed with tap water, cut into small pieces, and surface sterilized in sodium hypochlorite (3%) for 1 min, followed by washing in sterilized water and 75% ethanol for 1 min. Finally, they were washed in sterile distilled water 3 times and dried in sterilized tissue papers. Four sterilized leaf pieces were inoculated to a potato dextrose agar (PDA) medium and incubated at 27 °C for 1–2 days. Once the hypha emerges from leaf tissues, the tips were picked up to new PDA plates [43]. The morphology of colonies on PDA was taken with a camera of a Huawei P40 mobile phone (Huawei, Shenzhen, China). Fungal cultures were deposited in the Kunming Institute of Botany Culture Collection, China (KUNCC).

2.2. DNA Extraction, PCR Amplification and Sequencing

After the fungi had grown for around a week on PDA plates, those cultures were used for DNA extraction. The fresh mycelia (30–50 mg) were scraped from pure fungal colonies and transferred into 1.5 mL sterilized microcentrifuge tubes. Genomic DNA was extracted by the Biospin Fungus Genomic DNA Extraction Kit–BSC14S1 (BioFlux®, Hangzhou, China), following the manufacturer’s guidelines. A part of extracted DNA was stored at 4 °C for the instant PCR amplification, and the remaining portion was kept at −20 °C for long-term storage. PCR mixture contained 12.5 µL of 2× Power Taq PCR MasterMix (mixture of EasyTaqTM DNA Polymerase, dNTPs, 8.5 µL of double-distilled water (ddH2O), optimized buffer (Beijing Bio Teke Corporation (Bio Teke), Beijing, China [44]) and 1 μL of each forward and reverse primers (10 pmol), and 2 μL of DNA templet. Using the primers ITS4/ITS5, the internal transcribed spacer (ITS) region was amplified [45]. The PCR condition of ITS genes constituted 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, 1 min at 72 °C, and a final denaturation step of 10 min at 72 °C. The PCR products were purified and sequenced at Beijing Bio Teke Corporation.

2.3. Sequence Alignment and Phylogenetic Analyses

The reverse and forward sequences were checked in BioEdit v. 7.0.9.0 [46] and assembled in the Geneious (Restricted) 9.1.2 (website: https://www.geneious.com, accessed on 20 May 2022). Each sequence was BLASTn searched in the GenBank (website: http://blast.ncbi.nlm.nih.gov/, accessed on 20 May 2022) to screen the taxa with the highest degree of similarity. The ITS sequence alignment was made in the MAFFT online server (website: www.ebi.ac.uk/Tools/mafft, accessed on 20 May 2022) [47] and minor alterations in BioEdit 7.2.3 [46], whenever necessary. TrimAL v1.2 (website: http://trimal.cgenomics.org, accessed on 20 March 2022) was used to eliminate the uninformative gaps and unclear regions in the data alignment. On the CIPRES Science Gateway v.3.3, maximum likelihood analysis (ML) was performed (website: http://www.phylo.org/portal2, accessed on 20 May 2022 [48]), selecting RAxML-HPC2 on XSEDE (8.2.12) [49] with the GTRGAMMA substitution model with 1000 bootstrap iterations. FigTree v1.4.0 was used to display phylogenetic trees [50], while Microsoft PowerPoint (Microsoft Inc., Redmond, WA, USA) was used to edit the tree and reliable bootstrap support values were inserted from ML. Newly generated sequences were deposited in GenBank.

2.4. Screening Antagonistic Endophytes by Dual Culture Assay

For screening antagonistic fungal endophytes, two bacterial (Pseudomonas syringae and Erwinia amylovora) and two fungal (Penicillium digitatum and Botrytis cinerea) plant pathogens were obtained from China General Microbiological Culture Collection Center (CGMCC) (Table 1). The 34 fungal endophytes and four phytopathogenic species were respectively inoculated in the media (fungi: potato dextrose agar (PDA), bacteria: nutrient agar (NA)) for 10 days at 27 °C to make sure all strains have the same growing age [51,52,53,54]. At 10 days, the mycelium discs of 3.0 mm diameter from both the endophytes and the phytopathogenic fungi were taken out, and the plugs were co-inoculated equidistantly in 85 mm PDA Petri dishes spaced 10 mm from the edge of the dish, while 3.0 mm width of phytopathogenic bacteria were streaked in the opposite of fungal endophytes in NA Petri dishes. All endophyte-phytopathogen antagonism tests were performed in triplicate, and the plates (triplicate) that were only inoculated with bacterial and fungal pathogens were used as the control groups. After incubating at 27 °C for 10 days, the radial growth of bacterial/fungal pathogens was measured, provided the endophytic fungi overrun the pathogens, and the measured value was obtained from the reverse side. The antagonistic property of each endophyte was expressed as percentage inhibition of radial growth of fungal pathogens and width of the bacterial streak (PIRG-P), using the formula PIRG-P(%) = [(R1 − R2)/R1] × 100%, where: PIRG-P = Percentage inhibition; R1 = The radial growth of the fungal pathogens in control plates/The width of bacterial streak; R2 = The radial growth of the fungal pathogens/The width of bacterial streak at 10 days of antagonism trials [51,52,53,54].

2.5. Statistical Analysis

The inhibition rate was analyzed using IBM-SPSS (Statistic Product and Service Solutions) Statistics for Windows, version 29. 0. (SPSS Inc., Chicago, IL, USA). Data were analyzed by the one-way ANOVA with LSD and Duncan tests at the significant level p < 0.05. All values were expressed as means of three replicates ± standard deviation (S.D.). The visual bar chart was formed in GraphPad Prism software version 9.0 (GraphPad Holdings, San Diego, CA, USA) statistical package.

3. Results

3.1. Diversity of Endophytic Fungi and Phylogenetic Analyses Based on the ITS Gene

In this study, we isolated 34 fungal endophytic strains, and their phylogenetic placements were given based on the ITS locus. The colony morphology in the PDA of each strain was exhibited beside ML (Maximum likelihood analysis) tree (Figure 2). The results show that the 34 strains belong to 3 different classes (Dothideomycetes, Pezizomycetes, and Sordariomycetes); 12 different orders (Amphisphaeriales, Botryosphaeriales, Calosphaeriales, Capnodiales, Diaporthales, Glomerellales, Hypocreales, Mycosphaerellales, Pezizales, Pleosporales, Sordariales, and Xylariales); and 20 different families. In addition, Chaetomiaceae (Chaetomium spp.) isolates showed the highest diversity, which accounts for 26% (9 strains) among all the isolates (Figure 3).

3.2. In Vitro Biocontrol Experiments

3.2.1. Effect of Endophytes on the Growth of Erwinia amylovora (CGMCC: 1.7276)

Colonies of Erwinia amylovora were observed as white colonies in NA media. Chaetomium sp. KUNCC22-10749 strain inhibited the growth of E. amylovora by forming a fast-growing plentiful aerial mycelium within a short time (Figure 4b), at an inhibition rate of 50.00 ± 1.63% (Table 2). Chaetomium sp. KUNCC22-10750 strain inhibited the growth of E. amylovora by forming a clear zone between the fungus and the bacterium (Figure 4c) at an inhibition rate of 58.49 ± 3.27% (Table 2).

3.2.2. Effect of Endophytes on the Growth of Pseudomonas syringae (CGMCC: 1.3333)

Pseudomonas syringae was visible as orange-yellow, slimy colonies in NA media. Chaetomium sp. KUNCC22-10752 strain inhibited the growth of P. syringae (Figure 4e) with an inhibition rate of 50.67 ± 2.00% (Table 2). The pathogenic strain became dry, stopped growing, and covered with the mycelium of fungal endophytes.

3.2.3. Effect of Endophytes on the Growth of Botrytis cinerea (CGMCC: 3.3790)

The cultures of Botrytis cinerea were fast-growing, pale brown at the center, and white at the margins, and reached a diameter of around 60 mm in PDA after 10 days, without sporulating. Daldinia sp. KUNCC22-10744 strain was fast-growing and overlapped Botrytis cinerea (Figure 5b) with an inhibition rate of 55.56 ± 1.73% (Table 2). Chaetomium sp. KUNCC22-10749 strain inhibited the growth of B. cinerea (Figure 5c) with an inhibition rate of 52.02 ± 2.92% (Table 2) producing abundant aerial mycelium. Alternaria sp. KUNCC22-10760 strain inhibited the growth of B. cinerea (Figure 5d) with an inhibition rate of 67.15 ± 5.88% (Table 2) and the pathogen grew slowly, and mycelium was sparse.

3.2.4. Effect of Endophytes on the Growth of Penicillium digitatum (CGMCC: 3.15410)

The cultures of Penicillium digitatum were observed to be greenish, white at the margin, and a single colony in PDA reached 35–40 mm in diameter with sporulation after 10 days. Daldinia sp. KUNCC22-10744 strain was a fast-growing and overlapped pathogen (Figure 5f) with an inhibition rate of 51.16 ± 5.59% (Table 2). Rosellinia sp. KUNCC22-10751 strain was fast-growing while pathogens grew slowly (Figure 5g) at an inhibition rate of 60.83 ± 2.88% (Table 2). Figure 6, Figure 7, Figure 8 and Figure 9 show the Inhibition rates of different fungal endophytes to GCMCC: 1.7276, GCMCC: 1.3333, GCMCC: 3.3790, and GCMCC: 3.15410.

4. Discussion

The internal transcribed spacer (ITS) sequence has been generally recognized as a fungal barcode because it is the most sequenced region of fungi and is often used for identification, phylogenetics, and systematics [56,57]. Furthermore, the 5.8S-ITS region has previously been applied to the identification of endophytic fungal genera [58,59,60,61]. In this study, 34 isolates were identified to the generic level based on combined ITS. The nine different strains of Chaetomium were shown to be the dominant group, accounting for 26% of total strains (Figure 2). Chaetomium sp. strains viz. KUNCC22-10749, KUNCC22-10750, and KUNCC22-10752 showed antagonism against bacterial pathogens in vitro, while Chaetomium sp. KUNCC22-10749 is the only strain in this group that showed antagonism against the fungal pathogen Botrytis cinerea in vitro. Chaetomium is the largest genus in the family Chaetomiaceae and encompasses more than 350 species. Recently, this has become an important research topic due to its high diversity and prominent potential capability in biocontrol. The mechanisms of biocontrol of the endophytic Chaetomium spp. mainly include antibiosis, competition for nutrients and space, mycoparasitism, and induction of defense response in plants [62,63]. Species of Chaetomium have huge potential to control plant and soil fungal pathogens [64,65,66]. For example, Chaetomium globosum has been proven as a potential antagonist of Cochliobolus sativus, Venturia inaequalis, and Pythium ultimum [67,68,69]. Chaetomium cupreum and C. globosum have been reported to control corn leaf spot disease caused by Curvularia lunata, tomato wilt disease caused by Fusarium oxysporum, sheath blight disease of rice caused by Rhizoctonia solani, and rice blast disease caused by Pyricularia oryzae [70].
In this study, one of two Daldinia sp. strains KUNCC22-10744 strain exhibited significant antagonistic properties against the fungal pathogens Botrytis cinerea and Penicillium digitatum by competing for nutrition and space. Daldinia belongs to the family Hypoxylaceae, and currently, 58 species are accepted in this genus [66]. Specific secondary metabolites are constantly found in Daldinia sp., and they often have significant biological activities [71,72]. Liarzi et al. [73] isolated endophytic Daldinia concentrica from an olive tree, and its volatile organic compounds (VOCs) demonstrated antimicrobial activity against various fungi and oomycetes.
In this study, two Alternaria strains were isolated, and the Alternaria sp. (KUNCC22-10760 strain) was found to have prominent antagonistic properties against the fungal pathogen Botrytis cinerea. Alternaria as a pathogenic fungal group often causes black spot decay on hosts (including mango) [74,75]. However, Soltani and Hosseyni Moghaddam [76] isolated endophytic Alternaria species from healthy Cupressaceae trees, and a further study found their extracted metabolites exhibited significant growth inhibitory activities against pathogenic bacteria and fungi. These endophytic Alternaria are abundant in biologically active compounds that are possible to apply in medical and agricultural fields [77].
In this study, Rosellinia sp. KUNCC22-10751 strain exhibited prominent antagonistic abilities against the fungal pathogen Botrytis cinerea. Species of Rosellinia such as Rosellinia bunodes, R. necatrix, and R. pepo often cause root rots on many cash crops and trees [78]. Despite the fact that the endophytic species of Rosellinia have been shown to have potential as biocontrol agents, this is rarely reported [79]. Nevertheless, a large number of metabolites from endophytic Rosellinia species have been investigated recently [78,80,81].

5. Conclusions

Our study contributes to the knowledge of mango-associated endophytic fungi with the potential as biocontrol agents. We isolated 34 different fungal endophytes from healthy and fresh mango leaves, and the genus Chaetomium was reported as the dominant group. In addition, three strains of Chaetomium sp. showed great in vitro inhibition against two bacterial pathogens viz. Erwinia amylovora and Pseudomonas syringae, while the strains of Alternaria sp., Chaetomium sp., Daldinia sp., and Rosellinia sp. showed great to moderate in vitro antagonistic properties against fungi pathogens viz. Botrytis cinerea and Penicillium digitatum. Therefore, future studies should especially focus on how the studies translate into in vivo action, such as inoculating those effective fungal endophytes on plant pots (Mango seedlings or Arabidopsis thaliana) that were infected by selected fungal or bacterial pathogens.

Author Contributions

Conceptualization, S.C.K. and S.T.; data curation, E.-F.Y.; formal analysis, E.-F.Y.; funding acquisition, S.C.K., S.T., S.L.S., A.M.E., S.A.-R. and P.C.; investigation, E.-F.Y., S.L.S., I.P. and P.C.; methodology, E.-F.Y.; project administration, S.C.K. and I.P.; resources, E.-F.Y., A.M.E., S.A.-R. and P.C.; supervision, S.C.K., S.T., I.P., A.M.E. and P.C.; writing—original draft, E.-F.Y.; writing—review and editing, S.C.K., S.T., S.L.S., I.P., A.M.E., S.A.-R. and P.C. All authors have read and agreed to the published version of the manuscript.

Funding

The Faculty of Science and Graduate School, Chiang Mai University. National Natural Science Foundation of China (No. NSFC 31760013, 31950410558 and 32260004). High-Level Talent Recruitment Plan of Yunnan Provinces (“Young Talents” Program). The authors extend their appreciation to the Researchers Supporting Project number (RSP2023R120), King Saud University, Riyadh, Saudi Arabia.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data related to the present study are presented in the manuscript.

Acknowledgments

S.C.K. thanks the Visiting Scholars for World Class Research Collaboration Reinventing university grant 2021 for providing visiting scholarship. The authors are grateful to the Center for Yunnan Plateau Biological Resources Protection and Utilization, College of Biological Resource and Food Engineering, Qujing Normal University for providing the resources for morphological and molecular research. Er-fu Yang and Itthayakorn Promputtha are grateful to the Faculty of Science and Graduate School, Chiang Mai University for supporting of M.Sc. scholarship. Putarak Chomnunti would like to thank the National Reserch Council of Thailand (NRCT) grant number N41A640165. Reinventing University 2021 is thanked for supporting the research assistant.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. (a,b) Mango fruits and flowers with healthy leaves in Honghe, Yunnan Province, China.
Figure 1. (a,b) Mango fruits and flowers with healthy leaves in Honghe, Yunnan Province, China.
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Figure 2. The left side shows the phylogram generated from maximum likelihood analysis based on an ITS sequence dataset. The tree is rooted with Candelariella blastidiata (LE-L11031). The ML bootstrap support values equal to or greater than 60% are shown at the nodes. Type strains are indicated in bold. The right-side images show all the endophytic fungi cultures that were grown on PDA at room temperature for two weeks and their culture collection numbers are written at the bottom of the culture image.
Figure 2. The left side shows the phylogram generated from maximum likelihood analysis based on an ITS sequence dataset. The tree is rooted with Candelariella blastidiata (LE-L11031). The ML bootstrap support values equal to or greater than 60% are shown at the nodes. Type strains are indicated in bold. The right-side images show all the endophytic fungi cultures that were grown on PDA at room temperature for two weeks and their culture collection numbers are written at the bottom of the culture image.
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Figure 3. Classification of endophytic fungi (n = 34) associated with mango leaves.
Figure 3. Classification of endophytic fungi (n = 34) associated with mango leaves.
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Figure 4. The images of two bacterial pathogens that were co-cultivated with the mango fungal endophytes on NA plates. (a,d) Control groups; (b,c,e) Endophyte-phytopathogen antagonism tests.
Figure 4. The images of two bacterial pathogens that were co-cultivated with the mango fungal endophytes on NA plates. (a,d) Control groups; (b,c,e) Endophyte-phytopathogen antagonism tests.
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Figure 5. The two fungal pathogens co-cultivated with the mango fungal endophytes on PDA plates. (a,e) Control groups; (b–d,f,g) Endophyte-phytopathogen antagonism tests.
Figure 5. The two fungal pathogens co-cultivated with the mango fungal endophytes on PDA plates. (a,e) Control groups; (b–d,f,g) Endophyte-phytopathogen antagonism tests.
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Figure 6. Inhibition rates of different fungal endophytes to bacterial pathogen Erwinia amylovora (GCMCC: 1.7276). The bars denoted by the same letter are not significantly different from each other.
Figure 6. Inhibition rates of different fungal endophytes to bacterial pathogen Erwinia amylovora (GCMCC: 1.7276). The bars denoted by the same letter are not significantly different from each other.
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Figure 7. Inhibition rates of different fungal endophytes to bacterial pathogen Pseudomonas syringae (GCMCC1.3333). The bars denoted by the same letter are not significantly different from each other.
Figure 7. Inhibition rates of different fungal endophytes to bacterial pathogen Pseudomonas syringae (GCMCC1.3333). The bars denoted by the same letter are not significantly different from each other.
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Figure 8. Inhibition rates of different fungal endophytes to fungal pathogen Botrytis cinerea (GCMCC: 3.3790). The bars denoted by the same letter are not significantly different from each other.
Figure 8. Inhibition rates of different fungal endophytes to fungal pathogen Botrytis cinerea (GCMCC: 3.3790). The bars denoted by the same letter are not significantly different from each other.
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Figure 9. Inhibition rates of different fungal endophytes to fungal pathogen Penicillium digitatum (GCMCC: 3.15410). The bars denoted by the same letter are not significantly different from each other.
Figure 9. Inhibition rates of different fungal endophytes to fungal pathogen Penicillium digitatum (GCMCC: 3.15410). The bars denoted by the same letter are not significantly different from each other.
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Table
Table 1. Bacterial and fungal pathogens from China General Microbiological Culture Collection Center (CGMCC).
Table 1. Bacterial and fungal pathogens from China General Microbiological Culture Collection Center (CGMCC).
SpeciesStrainReferences
Bacterial pathogensPseudomonas syringaeCGMCC: 1.3333[55]
Erwinia amylovoraCGMCC: 1.7276[20]
Fungal pathogensPenicillium digitatumCGMCC: 3.15410[5]
Botrytis cinereaCGMCC: 3.3790[7]
Table
Table 2. The radial growth inhibition rates of fungal and bacterial pathogens. Inhibitions equal to or greater than 50% are in black bold.
Table 2. The radial growth inhibition rates of fungal and bacterial pathogens. Inhibitions equal to or greater than 50% are in black bold.
Collection No.GeneraGenBank Accession Number (ITS)Growth Inhibition Rate (GI) of 10 Days ± SD (%)
Erwinia amylovora CGMCC: 1.7276Pseudomonas syringae CGMCC 1.3333Botrytis cinerea
CGMCC: 3.3790		Penicillium digitatum CGMCC: 3.15410
KUNCC22-10741ChaetomiumON52074418.86 ± 3.27 c–g16.00 ± 4 f–i31.54 ± 5.06 l–n17.75 ± 2.65 h–l
KUNCC22-10742PhyllostictaON52074513.20 ± 6.54 e–j8.00 ± 4 j–m39.82 ± 4.17 d–l31.34 ± 2.11 c–f
KUNCC22-10743AnnulohypoxylonON52074622.64 ± 3.27 c–e13.33 ± 2.31 g–j37.61 ± 5.82 f–m29.96 ± 6.39 c–g
KUNCC22-10744DaldiniaON5207477.54 ± 3.27 h–j2.67 ± 2.31 lm55.56 ± 1.73 b51.16 ± 5.59 b
KUNCC22-10745XylariaON5207487.54 ± 1.63 h–j18.67 ± 2.31 fg29.88 ± 2.53 mn28.58 ± 2.11 c–h
KUNCC22-10746XylariaON52074911.32 ± 8.65 f–j21.33 ± 2.31 ef40.92 ± 4.17 d–j23.05 ± 8.10 e–j
KUNCC22-10747CercosporaON5207506.60 ± 2.83 ij10.67 ± 4.62 h–k32.92 ± 3.79 j–n25.81 ± 0.80 d–i
KUNCC22-10748CladosporiumON52075113.20 ± 8.65 e–j30.67 ± 2.31 b–d33.20 ± 0.96 i–n20.29 ± 2.88 f–k
KUNCC22-10749ChaetomiumON52075250.00 ± 1.63 b29.33 ± 2.31 cd52.02 ± 2.92 bc38.25 ± 6.39 c
KUNCC22-10750ChaetomiumON52075358.49 ± 3.27 a49.33 ± 2.31 a42.58 ± 2.66 d–h34.57 ± 4.23 cd
KUNCC22-10751RoselliniaON5207549.43 ± 5.66 g–j2.00 ± 2.11 m47.55 ± 4.17 cd60.83 ± 2.88 a
KUNCC22-10752ChaetomiumON52075545.29 ± 3.27 b50.67 ± 2.00 a32.09 ± 4.97 k–n28.12 ± 2.77 c–h
KUNCC22-10753PezizaON52075624.53 ± 3.27 cd18.67 ± 6.11 fg44.24 ± 3.45 c–g6.00 ± 2.77 m
KUNCC22-10754PhaeosphaeriaON52075711.32 ± 8.65 f–j12.00 ± 4.00 g–k43.13 ± 1.26 d–h27.66 ± 2.11 c–i
KUNCC22-10755AlternariaON52075826.42 ± 5.67 c36.00 ± 4.00 bc40.37 ± 4.39 d–k17.06 ± 2.77 i–l
KUNCC22-10756FusariumON52075924.53 ± 3.27 cd17.33 ± 2.31 f–h39.27 ± 1.26 d–l16.05 ± 1.72 i–l
KUNCC22-10757ChaetomiumON52076018.87 ± 11.79 c–g7.33 ± 4.16 j–m32.09 ± 6.63 k–n33.65 ± 9.97 c–e
KUNCC22-10758ChaetomiumON52076122.64 ± 3.27 c–e22.67 ± 6.11 ef36.51 ± 6.70 g–m28.11 ± 2.4 c–h
KUNCC22-10759ChaetomiumON52076216.98 ± 6.54 c–h10.67 ± 2.31 h–k45.34 ± 3.31 c–f30.42 ± 9.81 c–g
KUNCC22-10760AlternariaON52076320.75 ± 5.67 c–f32.00 ± 4.00 b–d67.15 ± 5.88 a29.96 ± 9.71 c–g
KUNCC22-10761ChaetomiumON52076416.98 ± 3.27 c–h9.33 ± 2.31 i–l29.88 ± 2.53 mn20.74 ± 1.6 f–k
KUNCC22-10762PericoniaON5207659.43 ± 0.00 g–j26.67 ± 2.31 de40.37 ± 1.66 d–k37.8 ± 3.66 c
KUNCC22-10763PleurostomaON5207665.66 ± 3.27 ij21.33 ± 4.62 ef41.75 ± 4.25 d–i34.11 ± 6.54 cd
KUNCC22-10765PhaeosphaeriaON5207674.71 ± 1.63 j17.33 ± 2.31 f–h42.86 ± 4.61 d–h10.60 ± 8.45 k–m
KUNCC22-10766NemaniaON52076819.81 ± 5.9 c–f6.00 ± 2.00 k–m27.12 ± 4.38 n21.67 ± 8.89 f–j
KUNCC22-10767ChaetomiumON52076918.87 ± 6.54 c–g32.00 ± 4.00 b–d26.57 ± 5.06 n23.97 ± 4.99 d–j
KUNCC22-10768ArthriniumON52077014.15 ± 4.32 e–j36.67 ± 7.57 b34.58 ± 8.41 h–n31.34 ± 2.88 c–f
KUNCC22-10769CladosporiumON52077122.64 ± 3.27 c–e31.33 ± 3.06 b–d37.61 ± 3.45 f–m19.82 ± 2.77 g–k
KUNCC22-10770MonocilliumON5207727.54 ± 3.27 h–j6.00 ± 5.29 k–m38.72 ± 3.32 e–l9.68 ± 4.22 lm
KUNCC22-10771ArthriniumON52077313.2 ± 3.27 e–j3.33 ± 1.15 lm39.54 ± 0.83 d–l21.67 ± 1.60 f–j
KUNCC22-10772DaldiniaON5207744.71 ± 1.63 j10.67 ± 6.11 h–k46.45 ± 8.17 c–e21.66 ± 11.51 f–j
KUNCC22-10773PestalotiopsisON52077515.09 ± 5.66 d–i21.33 ± 2.31 ef29.88 ± 2.53 mn28.40 ± 8.16 c–h
KUNCC22-10774DiaportheON52077620.75 ± 5.67 c–f9.33 ± 2.31 i–l42.31 ± 0.48 d–h25.81 ± 2.11 d–i
KUNCC22-10775ColletotrichumON52077722.64 ± 3.27 c–e2.67 ± 2.31 lm31.54 ± 6.69 l–n14.30 ± 3.91 j–m
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Yang, E.-F.; Karunarathna, S.C.; Tibpromma, S.; Stephenson, S.L.; Promputtha, I.; Elgorban, A.M.; Al-Rejaie, S.; Chomnunti, P. Endophytic Fungi Associated with Mango Show In Vitro Antagonism against Bacterial and Fungal Pathogens. Agronomy 2023, 13, 169. https://doi.org/10.3390/agronomy13010169

AMA Style

Yang E-F, Karunarathna SC, Tibpromma S, Stephenson SL, Promputtha I, Elgorban AM, Al-Rejaie S, Chomnunti P. Endophytic Fungi Associated with Mango Show In Vitro Antagonism against Bacterial and Fungal Pathogens. Agronomy. 2023; 13(1):169. https://doi.org/10.3390/agronomy13010169

Chicago/Turabian Style

Yang, Er-Fu, Samantha C. Karunarathna, Saowaluck Tibpromma, Steven L. Stephenson, Itthayakorn Promputtha, Abdallah M. Elgorban, Salim Al-Rejaie, and Putarak Chomnunti. 2023. "Endophytic Fungi Associated with Mango Show In Vitro Antagonism against Bacterial and Fungal Pathogens" Agronomy 13, no. 1: 169. https://doi.org/10.3390/agronomy13010169

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