Endophytic fungi: Benefits for plants and biotechnological potential

Authors

DOI:

https://doi.org/10.33448/rsd-v11i4.27008

Keywords:

Endophytic; Mutualistic relationship; Antimicrobial resistance; Bioactive substances.

Abstract

Endophytic fungi are microorganisms that live inside plants, establishing a mutualistic relationship, where both benefit from this interaction. They require protection and nutrients from host plants, and in return fungi can contribute to host's growth and nutrient uptake. In addition, they can improve plant tolerance to abiotic and biotic stresses and increase plant resistance to insects and pests. Endophytic fungi produce bioactive compounds similar to those of the host plant. The economic exploitation of these bioactive compounds is much promising. These bioactive products are related to sustainable production systems and to the development of new substances with strong pharmacological properties such as antiviral, antifungal, anti-inflammatory, antitumor and antiparasitic, antidiabetic and immunosuppressant, including response to resistant microorganisms. This study is a descriptive review, having as aim to approach the main benefits of endophytic fungi for host plants, as well as the biotechnological application of the bioactive compounds produced by them. The prospection of endophytic in extreme environment could result in discovery of new bioactive compounds with surprising potential for biotechnology area. So, the development of new research frontiers in this issue is indispensable for the sustainable exploitation of the great benefits that these microorganisms could provide to the science.

Author Biographies

Sybelle Georgia Mesquita da Silva, Rede Nordeste de Biotecnologia

Northeast Network of Biotechnology

Breno Araújo de Melo, Rede Nordeste de Biotecnologia

Northeast Network of Biotechnology

Micheline Thais dos Santos, Universidade Federal Rural de Pernambuco

Department of Animal Morphology and Physiology

Raisa Rodrigues Santos Rios, Rede Nordeste de Biotecnologia

Northeast Network of Biotechnology

Camila Matos de Santa’Anna Santos, Universidade Federal de Alagoas

Institute of Biological and Health Sciences

Karlos Antônio Lisboa Ribeiro Júnior, Rede Nordeste de Biotecnologia

Northeast Network of Biotechnology

Fernanda Cristina de Albuquerque Maranhão, Universidade Federal de Alagoas

Institute of Biological and Health Sciences

Tania Marta Carvalho dos Santos, Universidade Federal de Alagoas

Campus of engineering and agricultural sciences

Angelina Bossi Fraga, Rede Nordeste de Biotecnologia

Northeast Network of Biotechnology

References

Aly, A. H., Debbab, A. & Proksch, P. (2011). Fungal endophytes: unique plant inhabitants with great promises. Applied Microbiology and Biotechnology, 90, 1829–1845.

Ariantari, Ni. P., Daletos, G., Mandi, A., Kurtan, T., Muller, W. E. G., Lin, W., Ancheeva, E. & Proksch, P. (2019). Expanding the chemical diversity of an endophytic fungus Bulgaria inquinans, an ascomycete associated with mistletoe, through an OSMAC approach. RSC Advances, 9, 25119–25132.

Arnold, A. E. & Lutzoni, F. (2007). Diversity and host range of foliar fungal endophytes: Are tropical leaves biodiversity hotspots? Ecology, 88(3), 541–549.

Arnold, A. E., Maynard, Z., Gilbert, G. S., Coley, P. D. & Kursar, T. A. (2000). Are tropical fungal endophytes hyperdiverse? Ecology Letters, 3(4), 267-274.

Azevedo, J. L. (1999). Botânica: uma ciência básica ou aplicada? Revista Brasileira de Botânica 22(2), 225-229.

Azevedo, J. L. (1998). Microrganismos endofíticos. Ecologia Microbiana. Jaguariúna: EMBRAPA, 117-137.

Bacon, C. W., Porter, J. K., Robbins, J. D. & Luttrell, E. S. (1977). Epichloë typhina from toxic tall fescue grasses. Applied Environmental Microbiology, 34(5), 576–581.

Bayat, F., Mirlohi, A. & Khodambashi, M. (2009). Effects of endophytic fungi on some drought tolerance mechanisms of tall fescue in a hydroponics culture. Russian Journal of Plant Physiology, 56(4), 510-516.

Bhardwaj, A., Sharma, D., Jadon, N. & Agrawal, P. K. (2015). Antimicrobial and phytochemical screening of endophytic fungi isolated from spikes of Pinus roxburghii. Archives of Clinical Microbiology, 6(3).

Bush, L. P., Wilkinson, H. H. & Schardl, C. L. (1997). Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiology, 114, 1-7.

Carvalho, J. O., Broll, V., Martinelli, A. H. S. & Lopes, F. C. (2020). Chapter 25 - Endophytic fungi: positive association with plants Editor(s): Vivek Sharma, Richa Salwan, Laith Khalil Tawfeeq Al-Ani, Molecular Aspects of Plant Beneficial Microbes in Agriculture, Academic Press, 321-332.

Chen, Y., Yang, W., Zou, G., Chen, S. & Pang, J. (2019). Bioactive polyketides from the mangrove endophytic fungi Phoma sp. SYSU-SK-7. Fitoterapia, 139.

Chowdhury, N. S., Farjana, F. & Sohrab, Md. H. (2020). Isolation, identification and pharmacological activities of endophytic fungi from Aponogeton undulatus Roxb. Pharmacology & Pharmacy, 11, 350-361.

Collado, J., Platas, G., González, I. & Peláez, F. (1999). Geographical and seasonal influences on the distribution of fungal endophythes in Quercus ilex. New Phytologist, 144, 525-532.

Cruzzi, C., Link, S., Vilani, A. & Onofre, S. B. (2011). Enzimas extracelulares produzidas por fungos endofíticos isolados de Baccharis dracunculifolia d.c. (Asteraeceae). Global Science and Technology, 4(2), 47-57.

De Zoysa, M. H. N., Rathnayake, H., Hewawasam, R. P. & Wijayaratne, W. M. D. G. B. (2019). Determination of in vitro antimicrobial activity of five Sri Lankan medicinal plants against selected human pathogenic Bacteria. International Journal of Microbiology, 1-9.

Deng, Z. & Cao, L. (2016). Fungal endophytes and their interactions with plants in phytoremediation: A review. Chemosphere, 1-7.

Dutta, D., Puzari, K. C., Gogoi, R. & Dutta, P. (2014). Endophytes: Exploitation as a tool in plant protection. Brazilian Archives of Biology and Technology, 57(5), 621-629.

Elango, D., Manikandan, V., Jayanthi, P., Velmurugan, P., Balamuralikrishnan, B., Ravi, A. V. & Shivakumar, M. S. (2020). Selection and characterization of extracellular enzyme production by an endophytic fungi Aspergillus sojae and its bio-efficacy analysis against cotton leaf worm, Spodoptera litura. Curren Plant Biology, 23, 1-9.

Elfita, Munawar, Muharni & Sudrajat, M. A. (2014). Identification of new lactone derivatives isolated from Trichoderma sp., An Endophytic Fungus of Brotowali (Tinaspora crispa). HAYATI Journal of Bioscience, 21(1), 15-20.

Estrada, C., Wcislo, W. T. & Van Bael, S. A. (2013). Symbiotic fungi alter plant chemistry that discourages leaf-cutting ants. New Phytologist, 198, 241–251.

Faeth, S. H. & Fagan, W. F. (2002). Fungal Endophytes: common host plant symbionts but uncommon mutualists. Integrative and Comparative Biology, 42, 360–368.

Farhat, H., Urooj, F., Tariq, A., Sultana, V., Ansari, M., Ahmad, V. U. & Ehteshamul-Haque, S. (2019). Evaluation of antimicrobial potential of endophytic fungi associated with healthy plants and characterization of compounds produced by endophytic Cephalosporium and Fusarium solani. Biocatalysis and Agricultural Biotechnology, 18.

Farjana, A., Zerin, N. & Kabir, M. S. (2014). Antimicrobial activity of medicinal plant leaf extracts against pathogenic bactéria. Asian Pacific Journal of Tropical Disease, 4(2), S920-S923.

Ferrara, M. A. (2006). Fungos Endofíticos. Potencial para a Produção de Substâncias Bioativas. Revista Fitos, 2(1), 73-79.

Fontana, D. C., Paula, S., Torres, A. G., Souza, V. H. M., Pascholati, S. F., Schmidt, D. & Dourado Neto, D. (2021). Endophytic fungi: biological control and induced resistance to phytopathogens and abiotic stresses. Pathogens, 10, 1-28.

Fouda, A. H., Hassan, S. E-D., Eid, A. M. & Ewais, E. E-D. (2015). Biotechnological applications of fungal endophytes associated with medicinal plant Asclepias sinaica (Bioss.). Annals of Agricultural Science, 60(1), 95-104.

Gakuubi, M. M., Munusamy, M., Liang, Z-X. & Bee Ng, S. (2021). Fungal endophytes: a promising frontier for discovery of novel bioactive compounds. Journal of Fungi, 7, 1-24.

Gamboa, M. A., Laureano, S. & Bayman, P. (2002). Measuring diversity of endophytic fungi in leaf fragments: Does size matter? Mycopathologia, 156, 41–45.

Ghaffari, M. R., Mirzaei, M., Ghabooli, M., Khatabi, B., Wu, Y., Zabet-Moghaddam, M., Mohammadi-Nejad, G., Haynes, P. A., Hajirezaei, M. R., Sepehri, M. & Salekdeh, G. H. (2019). Root endophytic fungus Piriformospora indica improves drought stress adaptation in barley by metabolic and proteomic reprogramming. Environmental and Experimental Botany, 157, 197–210.

Gomes, O. C. & Luiz, J. H. H. (2018). Endophytic fungi isolated from medicinal plants: Future prospects of bioactive natural products from Tabebuia/Handroanthus endophytes. Applied Microbiology and Biotechnology, 102, 9105–9119.

González, V. & Tello, M. L. (2011). The endophytic mycota associated with Vitis vinifera in central Spain. Fungal Diversity, 47, 29–42.

Gopane, B., Tchatchouang, C. D. K., Regnier, T., Ateba, C. N. & Manganyi, M. C. (2021). Community diversity and stress tolerance of culturable endophytic fungi from black seed (Nigella sativa L.). South African Journal of Botany, 137, 272-277.

Gouda, S., Das, G., Sem, S. K., Shin, H. S. & Patra, J. K. (2016). Endophytes: a treasure house of bioactive compounds of medicinal importance. Frontiers in Microbiology, 7, 1-8.

Gunatilaka, A. A. L. (2006). Natural products from plant-associated microorganisms: distribution, structural diversity, bioactivity, and implication of their occurrence. Journal of Natural Products, 69, 509–526.

Guo, B., Dai, J-R., Ng, S., Huang, Y., Leong, C., Ong, W. & Carté, B. K. (2000). Cytonic acids A and B: novel tridepside inhibitors of hCMV protease from the endophytic fungus Cytonaema species. Journal of Natural Products, 63, 602-604.

Gupta, S., Chaturvedi, P., Kulkarni, M. G. & Staden, J. V. (2018). A critical review on exploiting the pharmaceutical potential of plant endophytic fungi. Biotechnology Advances, 39.

Hartley, S. E. & Gange, A. C. (2009). Impacts of plant symbiotic fungi on insect herbivores: Mutualism in a multitrophic context. Annual Review of Entomology, 54, 323–342.

Higgins, K. L, Arnold, A. E, Miadlikowska, J., Sarvate, S. D, & Lutzoni, F. (2007). Phylogenetic relationships, host affinity, and geographic structure of boreal and arctic endophytes from three major plant lineages. Molecular Phylogenetics and Evolution, 42, 543–555.

Hirsch, G. & Braun, U. (1992). Communities of parasitc microfungi. In: WINTERHOFF, W (ed) Handbook of Vegetation Science, 19(1), 225-250.

Hoffman, M. T. & Arnold, A. E. (2008). Geographic locality and host identity shape fungal endophyte communities in cupressaceous trees. Mycological Research, 112, 331–344.

Howell, C. R. (2003). Mechanisms Employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Disease, 87(1), 4-10.

Hu, Z., Wu, Z., Su, Q., Li, M., Wu, S., Meng, R. & Ding, W. (2020) Metabolites with phytopathogenic fungi inhibitory activities from the mangrove endophytic fungus Botryosphaeria ramose. Bioorganic Chemistry, 104.

Hu, Y., Li, C., Kulkarni, B. A., Strobel, G., Lobkovsky, E., Torczynski, R. M. & Porco Jr, J. A. (2001). Exploring chemical diversity of epoxyquinoid natural products: synthesis and biological activity of (-)-Jesterone and related molecules. Organic Letters, 3(11), 1649-1652.

Jaber, L. R. & Ownley, B. H. (2017). Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biological Control.

Jadulco, R., Brauers, G., Edrada, R. A., Ebel, R., Wray, V., Sudarsono & Proksch, P. (2002). New metabolites from sponge-derived fungi Curvularia lunata and Cladosporium herbarum. Journal of Natural Products, 65, 730-733.

Jalgaonwala, R. E., Mohite, B. V. & Mahajan, R. T. (2010). Evaluation of endophytes for their antimicrobial activity from indigenous medicinal plants belonging to North Maharashtra region, India. International Journal of Pharmacy & Biomedical Research, 1(5), 136–141.

Jia, M., Chen, L., Xin, H. L., Zheng, C. J., Rahman, K., Han, T. & Qin, L. P. A. (2016). Friendly relationship between endophytic fungi and medicinal plants: a systematic review. Frontiers in Microbiology, 7.

Jiang, S., Qian, D-W., Yang, N-Y., Tao, J-H. & Duan J-A. (2013). Biodiversity and antimicrobial activity of endophytic fungi in Angelica sinensis. Chinese Herbal Medicines, 5(4), 264-271.

Kalyanasundaram, I., Nagamuthu, J. & Muthukumaraswamy, S. (2015). Antimicrobial activity of endophytic fungi isolated and identified from salt marsh plant in Vellar Estuary. Journal of Microbiology and Antimicrobials, 7(2), 13-20.

Kathiravan, G., Sureban, S. M., Sree, H. N., Bhuvaneshwari, V. & Kramony, E. (2013). Isolation of anticancer drug Taxol from Pestalotiopsis breviseta with apoptosis and B-Cell lymphoma protein docking studies. Journal of Basic and Clinical Pharmacy, 4(1),14-9.

Kham, A. L., Hussain, J., Al-Harrasi, A., Al-Rawahi, A. & Lee, In-J. (2013). Endophytic fungi: resource for gibberellins and crop abiotic stress resistance. Critical Reviews in Biotechnology, Early Online, 1–13.

Kham, A. L., Hamayun, M., Radhakrishnan, R., Waqas, M., Kang, S-Mo., Kim, Y-Ha., Shin, J-Ho., Choo, Y-S., Kim, J-G. & Lee, In-J. (2011a) Mutualistic association of Paecilomyces formosus LHL10 offers thermotolerance to Cucumis sativus. Antonie van Leeuwenhoek, 101, 267–279.

Kham, A. L., Hamayun, M., Ahmad, N., Waqas, M., Kang, S-Mo., Kim, Y-Ha. & Lee, In-J. (2011b). Exophiala sp. LHL08 reprograms Cucumis sativus to higher growth under abiotic stresses. Physiologia Plantarum, 143, 329–343.

Khare, E., Mishra, J. & Arora, N. K. (2018). Multifaceted interactions between endophytes and plant: developments and prospects. Frontiers in Microbiology, 9, 1-12.

Khiralla, A., Mohamed, I., Thomas, J., Mignard, B., Spina, R. & Yagi, S. (2015). A pilot study of antioxidant potential of endophytic fungi from some Sudanese medicinal plants. Asian Pacific Journal of Tropical Medicine, 8(9), 701-704.

Krings, M.; Taylor, T. N.; Hass, H.; Kerp, H.; Dotzler, N. & Hermsen. E. J. (2007). Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytologist, 174, 648–657.

Kumar, G.; Chandra, P. & Choudhary, M. (2017). Endophytic fungi: a potential source of bioactive compounds. Chemical Science Review and Letters, 6(24), 2373-2381.

Kusari, S.; Singh, S. & Jayabaskaran, C. (2014). Biotechnological potencial of plantassociated endophytic fungi: hope versus hype. Trends in biotechnology, 32(6), 297- 303.

Kusari, S.; Hertweck, C. & Spiteller, M. (2012). Chemical ecology of endophytic fungi: origins of secondary metabolites. Chemistry & Biology, 19, 792-798.

Lata, R., Chowdhury, S., Gond, S. K. & White, J. F. (2018). Induction of abiotic stress tolerance in plants by endophytic microbes. Letters Applied Microbiology, 66(4), 268-276.

Li, H., Qing, C., Zhang, Y. & Zhao, Z. (2005). Screening for endophytic fungi with antitumor and antifungal activities from Chinese medicinal plants. World Journal of Microbiology & Biotechnology, 21, 1515-1519.

Lim, S. M., Agatonovic-Kustrin, S., Lim, F. T. & Ramasamy, K. (2021). High-performance thin layer chromatography-based phytochemical and bioactivity characterisation of anticancer endophytic fungal extracts derived from marine plants. Journal of Pharmaceutical and Biomedical Analysis, 193.

Liu, Y., Kurtán, T., Mándi, A., Weber, H., Wang, C., Hartmann, R., Lin, W., Daletos, G. & Proksch, P. (2018). A novel 10-membered macrocyclic lactone from the mangrove-derived endophytic fungus Annulohypoxylon sp. Tetrahedron Letters, 59, 632-636.

Ludwig-Müller, J. (2015). Plants and endophytes: Equal partners in secondary metabolite production? Biotechnology Letters, 37(7), 1325–1334.

Luz, J. S., Silva, R. L. O., Silveira, E. B. & Cavalcante, U. M. T. (2006). Atividade enzimática de fungos endofíticos e efeito na promoção do crescimento de mudas de maracujazeiro-amarelo. Revista Caatinga, 19(2), 128-134.

Manganyi, M. C., Regnier, T., Kumar, A., Bezuidenhout, C. C. & Ateba, C. C. (2018). Biodiversity and antibacterial screening of endophytic fungi isolated from Pelargonium sidoides. South African Journal of Botany, 116, 192-199.

Milke, L., Aschenbrenner, J., Marienhagen, J. & Kallscheuer, N. (2018). Production of plant-derived polyphenols in microorganisms: Current state and perspectives. Applied Microbiology and Biotechnology, 102(4), 1575– 1585.

Mollaei, S., Khanehbarndaz, O., Gerami-Khashal, Z. & Ebadi, M. (2019). Molecular identification and phytochemical screening of endophytic fungi isolated from Lithospermum officinale L. roots: a new source of shikonin. Phytochemistry, 198, 1-7.

Moricca, S. & Ragazzi, A. (2008). Fungal endophytes in Mediterranean oak forests: a lesson from Discula quercina. Phytopathology, 98, 380–386.

Nascimento, T. L., Oki, Y., Lima, D. M. M., Almeida-Cortez, J. S., Fernandes, G. W. & Souza-Motta, C. M. (2015). Biodiversity of endophytic fungi in different leaf ages of Calotropis procera and their antimicrobial activity. Fungal Ecology, 14, 79-86.

Nath, A. & Joshi, S. R. (2015). Ultrastructural effect on mastitis pathogens by extract of endophytic fungi associated with ethnoveterinary plant, Hibiscus sabdariffa L. Journal of Microscopy and Ultrastructure, 3, 38-43.

Oita, S., Ibáñez, A., Lutzoni, F., Miadlikowska, J., Geml, J., Lewis, L. A., Hom, E. F. Y., Carbone, I., U’Ren, J. M. & Arnold, A. E. (2021). Climate and seasonality drive the richness and composition of tropical fungal endophytes at a landscape scale. Communications Biology, 4(313).

Oliveira, V. M., Sette, L. D. & Fantinatti-Garboggini, F. (2006). Preservação e Prospecção de Recursos Microbianos. MultiCiência, 7, 1-19.

Ownley, B. H., Griffin, M. R., Klingeman, W. E., Gwinn, K. D., Moulton, J. K., & Pereira, R. M. (2008). Beauveria bassiana: endophytic colonization and plant disease control. Journal of Invertebrate Pathology, 98(3), 267–270.

Pamphile, J. A., Costa, A. T., Rosseto, P., Polonio, J. C., Pereira, J. O. & Azevedo, J. L. (2017). Aplicações biotecnológicas de metabólitos secundários extraídos de fungos endofíticos: o caso do Colletotrichum sp. Revista Uningá, 53(1), 113-119.

Parthasarathy, R., Chandrika, M., Rao, H. C. Y., Kamalraj, S., Jayabaskaran, C. & Pugazhendhi, A. (2020). Molecular profiling of marine endophytic fungi from green algae: assessment of antibacterial and anticancer activities. Process Biochemistry, 96, 11-20.

Peixoto Neto, P. A. S., Azevedo, J. L. & Caetano, L. C. (2004). Microrganismos endofíticos em plantas: status atual e perspectivas. Boletin latinoamericano y del Caribe de Plantas Medicinales y Aromáticas, 3(4), 69-72.

Petrini, O. (1991). Fungal endophytes of tree leaves. In: Andrews, J.H et al. (eds) Microbial ecology of leaves. Spring-Verlag, New York, 179-197.

Pietro-Souza, W., Pereira, F. C., Mello, I. S., Stachack, F. F. F., Terezo, A. J., Cunha, C. N., White, J. F., Li, H. & Soares, M. A. (2020). Mercury resistance and bioremediation mediated by endophytic fungi. Chemosphere, 240.

Pinheiro, E. A. A., Pina, J. R. S., Feitosa, A. O., Carvalho, J. M., Borges, F. C., Marinho, P. S. B. & Marinho, A. M. R. (2017). Bioprospecting of antimicrobial activity of extracts of endophytic fungi from Bauhinia guianensis. Revista Argentina de Microbiologia, 49(1), 3-6.

Pires, I. M. O., Silva, A.V., Santos, M. G. S., Bezerra, J. D. P., Barbosa, R. N., Silva, D. C. V., Svedese, V. M., Souza-Mota, C. M. & Paiva, L. M. (2015). Potencial antibacteriano de fungos endofíticos de cactos da caatinga, uma floresta tropical seca no Nordeste do Brasil. Gaia Scientia, 9(2), 155-161.

Prodanov, C. C. & Freitas, E. C. (2013). Metodologia do trabalho científico [recurso eletrônico]: métodos e técnicas da pesquisa e do trabalho acadêmico. 2 ed. Novo Hamburgo: Feevale.

Puri, S. C., Nazir, A., Chawla, R., Arora, R., Riyaz-ul-Hasan, S., Amna, T., Ahmed, B., Verma, V., Singh, S., Sagar, R., Sharma, A., Kumar, R., Sharma, R.K. & Qazi, G.N. (2006). The endophytic fungus Trametes hirsuta as a novel alternative source of podophyllotoxin and related aryl tetralin lignans. Journal of Biotechnology, 122, 494-510.

Rajani, P., Rajasekaran, C., Vasanthakumari, M. M., Olsson, S. B. & Ravikanth, G. (2021). Inhibition of plant pathogenic fungi by endophytic Trichoderma spp. through mycoparasitism and volatile organic compounds. Microbiological Research, 242, 1-12.

Rana, K. L., Kour, D., Kaur, T., Devi, R., Negi, C., Yadav, A. N., Yadav, N., Singh, K. & Saxena, A. K. (2020). Endophytic fungi from medicinal plants: biodiversity and biotechnological applications. 11 - Endophytic fungi from medicinal plants: biodiversity and biotechnological applications, Editor(s): Ajay Kumar, Radhakrishnan E. K, Microbial Endophytes, Woodhead Publishing, 273-305.

Redecker, D., Kodner, R. & Graham, L. E. (2000). Glomalean Fungi from the Ordovician. Science, 289, 1920-1921.

Redell, P. & Gordon, V. (2000). Lessons from nature: can ecology provide new leads in the search for novel bioactive chemicals from rainforests? In S. K. Wrigley, M. A. Hayes, R. Thomas, E. J. T. Chrystal, and N. Nicholson (ed.), Biodiversity: New leads for pharmaceutical and agrochemical industries. The Royal Society of Chemistry. Cambridge, United Kingdom, 205–212.

Saikkonen, K., Faeth, S. H., Helander, M. & Sullivan, T. J. (1998). Fungal endophytes: a continuum of interactions with host plants. Annual Review of Ecology, Evolution and Systematics, 29, 319–343.

Schardl, C. L., Leuchtmann, A. & Spiering, M. J. (2004). Symbioses of grasses with seedborne fungal endophytes. Annual Review of Plant Biology, 55, 315–340.

Schulz, B., Hass, S., Junker, C., Andrée, N. & Schobert, M. (2015). Fungal endophytes are involved in multiple balanced antagonisms. Current Science, 109(1), 39-45.

Schulz, B., Römmert, A. K. & Dammann, U. (1999). The endophyte-host interaction: A balanced antagonism? Mycological Research, 103, 1275-1283.

Sieber, T. N. (2007). Endophytic fungi in forest trees: Are they mutualists? Fungal Biology Reviews, 21, 75–89.

Siqueira, V. M., Conti, R., Araújo, J. M. & Souza-Motta, C. M. (2011). Endophytic fungi from the medicinal plant Lippia sidoides Cham. and their antimicrobial activity. Symbiosis, 53, 89–95

Soares, D. A., Rosa, L. H., Silva, J. F. M. & Pimenta, R. S. (2017). A review of bioactive compounds produced by endophytic fungi associated with medicinal plants. Boletim do Museu Paraense Emílio Goeldi Ciencias Naturais, 12(3), 331-352.

Souza, B. S., Oliveira, D. R., Rocha, F. V. R., Canto, E. S., Oliveira, D. P. & Santos, T. T. (2018) Fungos endofíticos associados à planta medicinal Kalanchoe pinnata (Lam.) pers. Revista Desafios, 5(3).

Stierle, A., Strobel, G. & Stierle, D. (1993). Taxol and Taxane Production by Taxomyces andreanae, an endophytic fungus of Pacific Yew. Science, 260, 214-216.

Strobel, G. A. (2002). Rainforest endophytes and bioactive products. Critical Reviews in Biotechnology, 22(4), 315-333.

Strobel, G., Daisy, B., Castillo, U. & Harper, J. (2004). Natural Products from Endophytic Microorganisms. Journal of Natural Products, 67(2), 257–268.

Strobel, G. & Daisy, B. (2003). Bioprospecting for microbial endophytes and their natural products. Microbiology and Molecular Biology Reviews, 67(4), 491–502.

Sun, X., Ding, Q., Hyde, K. D. & Guo, L. D. (2012). Community structure and preference of endophytic fungi of three woody plants in a mixed forest. Fungal Ecology, 5, 624-632.

Sun, X., Guo, L-D. & Hyde, K. D. (2011). Community composition of endophytic fungi in Acer truncatum and their role in decomposition. Fungal Diversity, 47, 85–95.

Supratman, U., Suzuki, T., Nakamura, T., Yokoyama, Y., Harneti, D., Maharani, R., Salam, S., Abdullah, F. F., Koseki, T. & Shiono Y. (2021). New metabolites produced by endophyte Clonostachys rosea B5 - 2. Natural Products Research, 35(9),1525-1531.

Tan, R. X. & Zou, W. X. (2001). Endophytes: A rich source of functional metabolites. Natural Products Report, 18, 448-459.

Tan, Z., Hurek, T. & Reinhold-Hurek, B. (2003). Effect of N-fertilization, plant genotype and environmental conditions on nifH gene pools in roots of rice. Environmental Microbiology, 5(10), 1009–1015.

Tanvir, R., Javeed, A. & Bajwa, A. G. (2017). Endophyte bioprospecting in South Asian medicinal plants: an attractive resource for biopharmaceuticals. Applied Microbiology and Biotechnology, 101, 1831-1844.

Techaoei, S., Jirayuthcharoenkul, C., Jarmkom, K., Dumrongphuttidecha, T. & Khobjai, W. (2020). Chemical evaluation and antibacterial activity of novel bioactive compounds from endophytic fungi in Nelumbo nucifera. Saudi Journal of Biological Sciences, 27, 2883-2889.

Tonial, F., Maia, B. H. L. N. S., Gomes-Figueiredo, J. A., Sobottka, A. M., Bertol, C. D., Nepel, A., Savi, D. C., Vicente, V. A., Gomes, R. R. & Glienke, C. (2016). Influence of culturing conditions on bioprospecting and the antimicrobial potential of endophytic fungi from Schinus terebinthifolius. Current Microbiology, 72, 173-183.

Venkateswarulu, N., Shameer, S., Bramhachari, P. V. & Basha, S. K. T. (2018). Isolation and characterization of plumbagin (5-hydroxyl-2-methylnaptalene-1,4-dione) producing endophytic fungi Cladosporium delicatulum from endemic medicinal plants. Biotechnology Reports, 20.

Waller, F., Achatz, B., Baltruschat, H., Fodor, J., Becker, K., Fischer, M., Heier, T., Huckelhoven, R., Neumann, C., Wettstein, D., Franken, P. & Kogel, K. H. (2005). The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proceedings of the National Academy of Science U S A, 102, 13386.

Weber, D., Sterner, O., Anke, T., Gorzalczancy, S., Martino, V. & Acevedo, C. (2004). Phomol, a new antiinflammatory metabolite from an endophyte of the medicinal plant Erythrina crista-galli. The Journal of Antibiotic, 57(9), 559-563.

Webber, J. (1981). A natural control of Dutch elm disease. Nature, 292, 449-451.

White Junior, J. F., Belanger, F., Meyer, W., Sullivan, R. S., Bischoff, J. F. & Lewis, E. A. (2002). Clavicipitalean fungal epibionts and endophytes: development of symbiotic interactions with plants. Symbiosis, 33, 201-2013.

Wilkinson, H. H., Siegel, M. R., Blankenship, J. D., Mallory, A. C., Bush, L. P. & Schardl, C. L. (2000). Contribution of fungal Loline alkaloids to protection from aphids in a grass-endophyte mutualism. Molecular Plant-Microbe Interactions, 13(10), 1027–1033.

Wu, H., Yan, Z., Deng, Y., Wu, Z., Xu, X., Li, X., Zhou, X. & Luo, H. (2020). Endophytic fungi from the root tubers of medicinal plant Stephania dielsiana and their antimicrobial activity. Acta Ecologica Sinica, 40(5), 383-387.

Wu, Z., Chen, J., Zhang, X., Chen, Z., Li, T., She, Z., Ding, W. & Li, C. (2019). Four new isocoumarins and a new natural tryptamine with antifungal activities from a mangrove endophytic fungus Botryosphaeria ramosa L29. Marine Drugs, 17(88), 1-9.

Xu, Z-Y., Zhang, X-X., Ma, J-K., Yang, Y., Zhou, J. & Xu, J. (2020). Secondary metabolites produced by mangrove endophytic fungus Aspergillus fumigatus HQD24 with immunosuppressive activity. Biochemical Systematics and Ecology, 93, 1-4.

Yadav, M., Yadav, A. & Yadav, J. P. (2014). In vitro antioxidant activity and total phenolic content of endophytic fungi isolated from Eugenia jambolana Lam. Asian Pacific Journal of Tropical Medicine, 7, S256-S261.

Yang, L., Zou, Y. N., Tian, Z. H., Wu, Q. S. & Kuča, K. (2021). Effects of beneficial endophytic fungal inoculants on plant growth and nutrient absorption of trifoliate orange seedlings. Scientia Horticulturae, 227.

Ye, D., Li, T., Yi, Y., Zhang, X. & Zou, L. (2019). Characteristics of endophytic fungi from Polygonum hydropiper suggest potential application for P-phytoextraction. Fungal Ecology, 41, 126-136.

Zabalgogeazcoa, I. (2008). Fungal endophytes and their interaction with plant pathogens. Spanish Journal of Agricultural Research, 6 (Special issue), 138–146.

Zhang, B., Salituro, G., Szalkowski, D., Li, Z., Zhang, Y., Royo, I., Vilella, D., Díez, M. T., Pelaez, F., Ruby, C., Kendall, R. L., Mao, X., Griffin, P., Calaycay, J., Zierath, J. R., Heck, J. V., Smith, R. G. & Moller, D. E. (1999). Discovery of a small molecule insulin mimetic with antidiabetic activity in mice. Science, 284.

Downloads

Published

12/03/2022

How to Cite

SILVA, S. G. M. da .; MELO, B. A. de; SANTOS, M. T. dos; RIOS, R. R. S.; SANTOS, C. M. de S. .; JÚNIOR, K. A. L. R. .; MARANHÃO, F. C. de A.; SANTOS, T. M. C. dos; FRAGA, A. B. Endophytic fungi: Benefits for plants and biotechnological potential. Research, Society and Development, [S. l.], v. 11, n. 4, p. e9211427008, 2022. DOI: 10.33448/rsd-v11i4.27008. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/27008. Acesso em: 25 apr. 2024.

Issue

Section

Review Article