Endophytic community of Chaenomeles speciosa fruits: Screening for biodiversity and antifungal activity
AbstractFruit crops of the genus Chaenomeles Lindl are considered today as a superfood due to accumulation of biologically active compounds with antioxidant ability and known health-promoting properties. Successful introduction of this non-traditional culture in the steppe zone of Ukraine characterised by an unfavourable climate suggests the functioning of effective protective mechanisms in plants, including those that can be provided by the influence of endophytic microorganisms. However, there is little information about the endophytic community of Chaenomeles plants. Herein, the current study was aimed to isolate the endophytic fungi from the Ch. speciosa fruits and evaluate their biological activities against the phytopathogens. The study was carried out based on the collection of the Botanical Garden of Oles Honchar Dnipro National University (Dnipro city, Ukraine). Three media, namely PDA, MPA, and Gause’s medium were used for isolation of endophytic fungi. Colonies of isolates for identification were grown on PDA, Czapek's agar, and Czapek’s yeast autolysate media. Six fungal endophytic isolates derived from both peel and pulp of Ch. speciosa fruits have been morphologically identified using macroscopic and microscopic techniques, and assigned to the genus Penicillium (sections Chrysogena, Penicillium, Viridicata), and genus Talaromyces (section Talaromyces). Species P. expansum, P. viridicatum, and P. hirsutum were identified among the peel isolates, while P. chrysogenum, P. cyclopium, and P. purpurogenum were among the pulp isolates. Antagonistic ability of the endophytic isolates against phytopathogenic fungi was evaluated using the dual culture method. The results showed moderate to high antifungal capacity of the endophytic isolates against the phytopathogenic strains of the Fusarium genus. The growth inhibition of F. culmorum mycelium due to the influence of endophytic isolates was 51.5–81.3%, and the inhibition of the growth of F. oxysporum colonies was in the range of 68.4–86.6% as compared with control. There were no significant differences in the antagonistic ability between endophytic isolates derived from the peel and pulp of the fruit. Taken together, our findings indicated the great potential of the endophytic fungi from Ch. speciosa fruits as a source for the development of biocontrol agents and discovery of new bioactive compounds.
Abd El Aty, A. A., Mohamed, A. A., Zohair, M. M., & Soliman, A. A. F. (2020). Statistically controlled biogenesis of silver nano-size by Penicillium chrysogenum MF318506 for biomedical application. Biocatalysis and Agricultural Biotechnology, 25, 101592.
Alam, B., Lǐ, J., Gě, Q., Khan, M. A., Gōng, J., Mehmood, S., Yuán, Y., & Gǒng, W. (2021). Endophytic fungi: From symbiosis to secondary metabolite communications or vice versa? Frontiers in Plant Science, 12, 791033.
An, C., Ma, S., Shi, X., Xue, W., Liu, C., & Ding, H. (2020). Diversity and antimicrobial activity of endophytic fungi isolated from Chloranthus japonicus Sieb in Qinling Mountains, China. International Journal of Molecular Sciences, 21(17), 5958.
Baron, N. C., & Rigobelo, E. C. (2021). Endophytic fungi: A tool for plant growth promotion and sustainable agriculture. Mycology, 13(1), 39–55.
Beltran-Garcia, M. J., Martinez-Rodriguez, A., Olmos-Arriaga, I., Valdez-Salas, B., Chavez-Castrillon, Y. Y., Di Mascio, P., & White, J. F. (2021). Probiotic endophytes for more sustainable banana production. Microorganisms, 9, 1805.
Chen, Q., Yu, J. J., He, J., Feng, T., & Liu, J. K. (2022). Isobenzofuranones and isocoumarins from kiwi endophytic fungus Paraphaeosphaeria sporulosa and their antibacterial activity against Pseudomonas syringae pv. actinidiae. Phytochemistry, 195, 113050.
Chen, X., Luo, X., Fan, M., Zeng, W., Yang, C., Wu, J., Zhao, C., Zhang, Y., & Zhao, P. (2019). Endophytic fungi from the branches of Camellia taliensis (W. W. Smith) Melchior, a widely distributed wild tea plant. World Journal of Microbiology and Biotechnology, 35(7), 113.
Cui, R., Lu, X., Chen, X., Malik, W. A., Wang, D., Wang, J., Wang, S., Guo, L., Chen, C., Wang, X., Wang, X., Dai, M., & Ye, W. (2021). A novel raffinose biological pathway is observed by symbionts of cotton ≡ Verticillium dahliae to improve salt tolerance genetically on cotton. Journal of Agronomy and Crop Science, 207, 956–969.
Deng, Y., Huang, L., Zhang, C., Xie, P., Cheng, J., Wang, X., & Liu, L. (2020). Novel polysaccharide from Chaenomeles speciosa seeds: Structural characterization, α-amylase and α-glucosidase inhibitory activity evaluation. International Journal of Biological Macromolecules, 153, 755–766.
Du, W., Yao, Z., Li, J., Sun, C., Xia, J., Wang, B., Shi, D., & Ren, L. (2020). Diversity and antimicrobial activity of endophytic fungi isolated from Securinega suffruticosa in the Yellow River Delta. PloS One, 15(3), e0229589.
El Enshasy, H. A., Hanapi, S. Z., Malek, R. A., Abdelgalil, S. A., & Leng, O. M. (2019). Endophytic fungi: The desired biostimulants for essential oil production. In: Singh, B. (Ed.). Advances in endophytic fungal research. Fungal Biology. Springer, Cham.
Fan, M., Chen, X., Luo, X., Zhang, H., Liu, Y., Zhang, Y., Wu, J., Zhao, C., & Zhao, P. (2020). Diversity of endophytic fungi from the leaves of Vaccinium dunalianum. Letters in Applied Microbiology, 71(5), 479–489.
Frisvad, J. C., & Samson, R. A. (2004). Polyphasic taxonomy of Penicillium subgenus Penicillium. A guide to identification of food and air-borne terverticillate Penicillia and their mycotoxins. Studies in Mycology, 49, 1–174.
Huang, W., He, J., Nisar, M. F., Li, H., & Wan, C. (2018). Phytochemical and pharmacological properties of Chaenomeles speciosa: An edible medicinal Chinese mugua. Evidence-Based Complementary and Alternative Medicine, 2018, 9591845.
Javed, A., Shah, A. H., Hussain, A., Khan, S. A., Khan, S. A., Hamayun, M., Hassan, I., & Jan, S. A. (2019). Identification and characterization of Penicillium chrysogenum T8 as potent plant growth promoting endophytic fungi. Fresenius Environmental Bulletin, 28(6), 4896–4902.
Khan, A. L., Al-Harrasi, A., Al-Rawahi, A., Al-Farsi, Z., Al-Mamari, A., Waqas, M., Asaf, S., Elyassi, A., Mabood, F., Shin, J.-H., & Lee, I.-J. (2016). Endophytic fungi from frankincense tree improves host growth and produces extracellular enzymes and indole acetic acid. PLoS One, 1(6), e0158207.
Khan, N., Martínez-Hidalgo, P., Ice, T. A., Maymon, M., Humm, E. A., Nejat, N., Sanders, E. R., Kaplan, D., & Hirsch, A. M. (2018). Antifungal activity of Bacillus species against Fusarium and analysis of the potential mechanisms used in biocontrol. Frontiers in Microbiology, 9, 2363.
Kikowska, M., Włodarczyk, A., Rewers, M., Sliwinska, E., Studzińska-Sroka, E., Witkowska-Banaszczak, E., Stochmal, A., Żuchowski, J., Dlugaszewska, J., & Thiem, B. (2019). Micropropagation of Chaenomeles japonica: A step towards production of polyphenol-rich extracts showing antioxidant and antimicrobial activities. Molecules, 24, 1314.
Lu, Y., Chen, C., Chen, H., Zhang, J., & Chen, W. (2012). Isolation and identification of endophytic fungi from Actinidia macrosperma and investigation of their bioactivities. Evidence-Based Complementary and Alternative Medicine, 2012, 382742.
Lykholat, T., Lykholat, O., & Antonyuk, S. (2016). Immunohistochemical and biochemical analysis of mammary gland tumours of different age patients. Cytology and Genetics, 50(1), 40–51.
Lykholat, Y. V., Khromykh, N. O., Didur, O. O., Drehval, O. A., Sklyar, T. V., & Anishchenko, A. O. (2021a). Chaenomeles speciosa fruit endophytic fungi isolation and characterization of their antimicrobial activity and the secondary metabolites composition. Beni-Suef University Journal of Basic and Applied Sciences, 10, 83.
Lykholat, Y. V., Khromykh, N. O., Lykholat, T. Y., Didur, O. O., Lykholat, O. A., Legostaeva, T. V., Kabar, A. M., Sklyar, T. V., Savosko, V. M., Kovalenko, I. M., Davydov, V. R., Bielyk, Y. V., Volyanik, K. O., Onopa, A. V., Dudkina, K. A., & Grygoryuk, I. P. (2019). Industrial characteristics and consumer properties of Chaenomeles Lindl. fruits. Ukrainian Journal of Ecology, 9(3), 132–137.
Martins, F., Cameirão, C., Mina, D., Benhadi-Marín, J., Pereira, J. A., & Baptista, P. (2021). Endophytic fungal community succession in reproductive organs of two olive tree cultivars with contrasting anthracnose susceptibilities. Fungal Ecology, 49, 101003.
Mehta, P., Sharma, R., Putatunda, C., & Walia, A. (2019). Endophytic fungi: Role in phosphate solubilization. In: Singh, B. P. (Ed.). Advances in endophytic fungal research: Present status and future challenges. Springer International Publishing, Cham. Pp. 183–209.
Miao, J., Li, X., Zhao, C., Gao, X., Wang, Y., & Gao, W. (2018). Active compounds, antioxidant activity and α-glucosidase inhibitory activity of different varieties of Chaenomeles fruits. Food Chemistry, 248, 330–339.
Mishra, V. K., Passari, A. K., Chandra, P., Leo, V. V., Kumar, B., Uthandi, S., Thankappan, S., Gupta, V. K., & Singh, B. P. (2017). Determination and production of antimicrobial compounds by Aspergillus clavatonanicus strain MJ31, an endophytic fungus from Mirabilis jalapa L. using UPLC-ESI-MS/MS and TD-GC-MS analysis. PLoS One, 12(10), e0186234.
Nayak, S., Samanta, S., Sengupta, C., & Swain, S. S. (2021). Rice crop loss due to major pathogens and the potential of endophytic microbes for their control and management. Journal of Applied Biology and Biotechnology, 9(5), 166–175.
Ni, H., Kong, W.-L., Zhang, Q.-Q., & Wu, X.-Q. (2021). First report of leaf spot disease caused by Colletotrichum gloeosporioides on Chaenomeles sinensis in China. Plant Disease, 105(9), 2731.
Nicoletti, R., Di Vaio, C., & Cirillo, C. (2020). Endophytic fungi of olive tree. Microorganisms, 8(9), 1321.
Pandit, S. G., Puttananjaiah, M. H., Serva Peddha, M., & Dhale, M. A. (2020). Safety efficacy and chemical profiling of water-soluble Talaromyces purpureogenus CFRM02 pigment. Food Chemistry, 310, 125869.
Parul, Thiyam, D., Dufossé, L., & Sharma, A. K. (2020). Characterization of Talaromyces purpureogenus strain F extrolites and development of production medium for extracellular pigments enriched with antioxidant properties. Food and Bioproducts Processing, 124, 143–158.
Paul, N. C., Deng, J. X., Sang, H.-K., Choi, Y.-P., & Yu, S.-H. (2012). Distribution and antifungal activity of endophytic fungi in different growth stages of chili pepper (Capsicum annuum L.) in Korea. The Plant Pathology Journal, 28(1), 10–19.
Perrone, G., & Susca, A. (2017). Penicillium species and their associated mycotoxins. In: Moretti, A., & Susca, A. (Eds.). Mycotoxigenic fungi. Methods in molecular biology. Vol. 1542. Humana Press, New York.
Poveda, J., & Baptista, P. (2021). Filamentous fungi as biocontrol agents in olive (Olea europaea L.) diseases: Mycorrhizal and endophytic fungi. Crop Protection, 146, 105672.
Poveda, J., Abril-Urias, P., & Escobar, C. (2020). Biological control of plant-parasitic nematodes by filamentous fungi inducers of resistance: Trichoderma, mycorrhizal and endophytic fungi. Frontiers in Microbiology, 11, 992.
Poveda, J., Eugui, D., Abril-Urías, P., & Velasco, P. (2021). Endophytic fungi as direct plant growth promoters for sustainable agricultural production. Symbiosis, 85, 1–19.
Radic, N., & Strukelj, B. (2012). Endophytic fungi: The treasure chest of antibacterial substances. Phytomedicine, 19, 1270–1284.
Roy Choudhury, A., Choi, J., Walitang, D. I., Trivedi, P., Lee, Y., & Sa, T. (2021). ACC deaminase and indole acetic acid producing endophytic bacterial co-inoculation improves physiological traits of red pepper (Capsicum annum L.) under salt stress. Journal of Plant Physiology, 267, 153544.
Seepe, H. A., Nxumalo, W., & Amoo, S. O. (2021). Natural products from medicinal plants against phytopathogenic Fusarium species: Current research endeavours, challenges and prospects. Molecules, 26, 6539.
Srivastava, S., Kadooka, C., & Uchida, J. Y. (2018). Fusarium species as pathogen on orchids. Microbiological Research, 207, 188–195.
Tang, Y., Yu, X., Mi, M., Zhao, J., Wang, J., & Zhang, T. (2010). Antioxidative property and antiatherosclerotic effects of the powder processed from Chaenomeles speciosa in ApoE(–/–) mice. Journal of Food Biochemistry, 34(3), 535–548.
Tran, N. T., Miles, A. K., Dietzgen, R. G., & Drenth, A. (2019). Phyllosticta capitalensis and P. paracapitalensis are endophytic fungi that show potential to inhibit pathogenic P. citricarpa on citrus. Australasian Plant Pathology, 48, 281–296.
Tsiailanis, A. D., Pateraki, C., Kyriazou, M., Chatzigiannis, C. M., Chatziathanasiadou, M., Parisis, N., Mandala, I., Tzakos, A. G., & Koutinas, A. (2022). Chemical profiling, bioactivity evaluation and the discovery of a novel biopigment produced by Penicillium purpurogenum CBS 113139. Molecules, 27(1), 69.
Uzma, F., Mohan, C. D., Hashem, A., Konappa, N. M., Rangappa, S., Kamath, P. V., Singh, B. P., Mudili, V., Gupta, V. K., Siddaiah, C. N., Chowdappa, S., Alqarawi, A. A., & Abd Allah, E. F. (2018). Endophytic fungi-alternative sources of cytotoxic compounds: A review. Frontiers in Pharmacology, 9, 309.
Yilmaz, N., Visagie, C. M., Houbraken, J., Frisvad, J. C., & Samson R. A. (2014). Polyphasic taxonomy of the genus Talaromyces. Studies in Mycology, 78, 175–341.
Zavaleta, V., & Eyzaguirre, J. (2016). Penicillium purpurogenum produces a highly stable endo-β-(1,4)-galactanase. Applied Biochemistry and Biotechnology, 180(7), 1313–1327.
Zazharskyi, V. V., Davydenko, P. О., Kulishenko, O. М., Borovik, I. V., Brygadyrenko, V. V. (2019). Antimicrobial activity of 50 plant extracts. Biosystems Diversity, 27(2), 163–169.
Zazharskyi, V. V., Davydenko, P. О., Kulishenko, O. М., Borovik, I. V., Zazharska, N. M., & Brygadyrenko, V. V. (2020). Antibacterial and fungicidal activities of ethanol extracts of 38 species of plants. Biosystems Diversity, 28(3), 281–289.
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons «Attribution» 4.0 License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.