Investigating the effectiveness of endophytic fungi under biotic and abiotic agricultural stress conditions

Abdelhak Rhouma; Lobna Hajji-Hedfi; Okon Godwin Okon; Hasadiah Okon Bassey

doi:10.56027/JOASD.122024

Authors

Abdelhak Rhouma Regional Centre of Agricultural Research of Sidi Bouzid, CRRA, Gafsa Road Km 6, B.P. 357, 9100, Sidi Bouzid, Tunisia
Lobna Hajji-Hedfi
Okon Godwin Okon
Hasadiah Okon Bassey

DOI:

https://doi.org/10.56027/JOASD.122024

Keywords:

Biostimulant, Bioprotector, Endophytic fungi, Sustainable agriculture

Abstract

Endophytic fungi play crucial roles in promoting plant growth and enhancing stress tolerance, making them valuable allies in agriculture. This reviewer explores the advantageous roles and implications of endophytic fungi in plant stress tolerance, focusing on hormonal regulation, nutrient uptake, and their management of various abiotic and biotic stresses. Endophytic fungi influence the production of plant hormones such as auxins, cytokinins, and gibberellins; thus, contributing to enhanced growth and stress resilience. They also assist in nutrient uptake, solubilizing minerals, and fixing atmospheric nitrogen; thereby improving overall plant nutrition. This reviewer discusses the mechanism of endophytic fungi’s effectiveness in managing biotic and abiotic stresses, including; high CO₂ levels, waterlogging/drought, salinity, high temperatures, salinity, heavy metal stress as well as plant pathogens and parasitic attacks. Furthermore, the bio-control capabilities of endophytic fungi against biotic stresses are highlighted, showcasing mechanisms such as induced resistance, mycoparasitism, antibiosis, and competition. The biological activities of recently isolated compounds and associated endophytic fungi are also discussed. Thus, as research in this field progresses, harnessing the full potential of endophytic fungi holds promise for promoting resilient and sustainable agriculture in the face of changing environmental conditions.

References

Aamir, M., Krishna, K.R., Andleeb, Z., Sunil, K., Mukesh, Y., Vaishali, S., Ram, S.U. (2020). Fungal endophytes: Classification, diversity, ecological role, and their relevance in sustainable agriculture. Microbial Endophytes 1, 291-323. DOI: https://doi.org/10.1016/B978-0-12-818734-0.00012-7

Abdou, R., Shabana, S., Rateb, M.E., Terezine E. (2020). Bioactive prenylated tryptophan analogue from an endophyte of Centaurea stoebe. Natural Product Research 34, 503–510. DOI: https://doi.org/10.1080/14786419.2018.1489393

Adhikari, P., Pandey, A. (2019). Phosphate solubilization potential of endophytic fungi isolated from Taxus wallichiana Zucc. roots. Rhizosphere 9, 2–9. DOI: https://doi.org/10.1016/j.rhisph.2018.11.002

Ahmad, P. (2010). Growth and antioxidant responses in mustard (Brassica juncea L.) plants subjected to combined effect of gibberellic acid and salinity. Archives of Agronomy and Soil Science 56, 575–588. DOI: https://doi.org/10.1080/03650340903164231

Ahmed, E., Holmström, S.J. (2014). Siderophores in environmental research: Roles and applications. Microbial biotechnology 7, 196–208. DOI: https://doi.org/10.1111/1751-7915.12117

Alloush, G.A. (2004). Evidence for copper binding by extracellular root exudates of tall fescue but not perennial ryegrass infected with Neotyphodium spp. endophytes. Plant and Soil 267, 1-12. DOI: https://doi.org/10.1007/s11104-005-2575-y

Arnold, A. E., Mejia, L. C., Kyllo, D., Rojas, E. I., Maynard, Z., Robbins, N., Herre, E. A. (2003). Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences 100, 15649–15654. DOI: https://doi.org/10.1073/pnas.2533483100

Arnold, E., Maynard, Z., Gilbert, G.S., Coley, P.D., Kursar, T. A. (2000). Are tropical fungal endophytes hyperdiverse? Ecology Letters 3, 267-74. DOI: https://doi.org/10.1046/j.1461-0248.2000.00159.x

Arora, H., Sharma, A., Poczai, P., Sharma, S., Haron, F.F., Gafur, A. (2022). Plant-Derived protectants in combating soil-borne fungal infections in tomato and chilli. Journal of Fungi 8, 213. DOI: https://doi.org/10.3390/jof8020213

Asgher, M., Khan, M.I.R., Anjum, N.A., Khan, N.A. (2015). Minimising toxicity of cadmium in plants-role of plant growth regulators. Protoplasma 252, 399-413. DOI: https://doi.org/10.1007/s00709-014-0710-4

Atugala, D.M., Deshappriya, N. (2015). Effect of endophytic fungi on plant growth and blast disease incidence of two traditional rice varieties. Journal of the National Science Foundation of Sri Lanka 43, 173-187. DOI: https://doi.org/10.4038/jnsfsr.v43i2.7945

Bailey, B.A., Bae, H., Strem, M.D., Roberts, D.P., Thomas, S.E., Samuels, G.J. (2006). Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species. Planta 224, 1449–1464. DOI: https://doi.org/10.1007/s00425-006-0314-0

Baltruschat, H., Fodor, J., Harrach, B.D., Niemczyk, E., Barna, B., Gullner, G. (2008). Salt tolerance of barley induced by root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytologist 180, 501–510. DOI: https://doi.org/10.1111/j.1469-8137.2008.02583.x

Baron, N.C., Rigobelo, E.C. (2021). Endophytic fungi: a tool for plant growth promotion and sustainable agriculture. Mycology 13, 39–55. DOI: https://doi.org/10.1080/21501203.2021.1945699

Behie, S.W., Bidochka, M.J. (2014). Ubiquity of insect-derived nitrogen transfer to plants by endophytic insect-pathogenic fungi: An additional branch of the soil nitrogen cycle. Applied and Environmental Microbiology Journal 80, 1553–1560. DOI: https://doi.org/10.1128/AEM.03338-13

Benhamou, N., Gagne, S., Lequere, D., Dehbi, L. (2000). Bacterial-mediated induced resistance in cucumber: Beneficial effect of the endophytic bacterium Serratia plymuthica on the protection against infection by Pythium ultimum. Phytopathology 90, 45–56. DOI: https://doi.org/10.1094/PHYTO.2000.90.1.45

Bogati, K., Walczak, M. (2022). The impact of drought stress on soil microbial community, enzyme activities and plants. Agronomy 12(1), 189. DOI: https://doi.org/10.3390/agronomy12010189

Brundrett, M.C. (2006). Understanding the roles of multifunctional mycorrhizal and endophytic fungi. In: Microbial root endophytes; Springer: Berlin/Heidelberg, Germany, pp. 281–298. DOI: https://doi.org/10.1007/3-540-33526-9_16

Cao, R., Liu, X., Gao, K., Mendgen, K., Kang, Z., Gao, J., Dai, Y., Wang, X. (2009). Mycoparasitism of endophytic fungi isolated from reed on soilborne phytopathogenic fungi and production of cell wall-degrading enzymes in vitro. Current Microbiology 59, 584–592. DOI: https://doi.org/10.1007/s00284-009-9477-9

Card, S., Johnson, L., Teasdale, S., Caradus, J. (2016). Deciphering endophyte behaviour: The link between endophyte biology and efficacious biological control agents. FEMS Microbiology Ecology 92, 1–19. DOI: https://doi.org/10.1093/femsec/fiw114

Chamoun, R., Aliferis, K.A., Jabaji, S. (2015). Identification of signatory secondary metabolites during mycoparasitism of Rhizoctonia solani by Stachybotrys elegans. Frontiers in Microbiology 6, 353. DOI: https://doi.org/10.3389/fmicb.2015.00353

Chi, F., Shen, S.H., Cheng, H.P., Jing, Y.X., Yanni, Y.G., Dazzo, F.B. (2005). Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Applied and Environmental Microbiology Journal 71, 7271–7278. DOI: https://doi.org/10.1128/AEM.71.11.7271-7278.2005

Clarke, T.C., Shetty, K.G., Jayachandran, K., Norland, M.R. (2007). Myrothecium verrucaria– a potential biological control agent for the invasive ‘old world climbing fern’ (Lygodium microphyllum). BioControl 52, 349–411. DOI: https://doi.org/10.1007/s10526-006-9035-3

Clay, K., Holah, J. (1999). Fungal endophyte symbiosis and plant diversity in successional fields. Science 285, 1742–1745. DOI: https://doi.org/10.1126/science.285.5434.1742

Conrath, U., Pieterse, C.M.J., Mauch-Mani, B. (2002). Priming in plant–pathogen interactions. Trends in Plant Science 7, 210–216. DOI: https://doi.org/10.1016/S1360-1385(02)02244-6

Daguerre, Y., Edel-Hermann, V., Steinberg, C. (2017). Fungal Genes and Metabolites Associated with the Biocontrol of Soil-borne Plant Pathogenic Fungi. In: Mérillon, JM., Ramawat, K. (eds) Fungal Metabolites. Reference Series in Phytochemistry. Springer, Cham. https://doi.org/10.1007/978-3-319-25001-4_27 DOI: https://doi.org/10.1007/978-3-319-25001-4_27

Deketelaere, S., Tyvaert, L., Franca, S.C., Hofte, M. (2017). Desirable traits of a good biocontrol agent against Verticillium wilt. Frontiers in Microbiology 8, 1186. DOI: https://doi.org/10.3389/fmicb.2017.01186

Dipietro, A. (1995). Fungal antibiosis in biocontrol of plant disease. In: Allelopathy, ACS Symposium Series, pp. 271–279. https://doi.org/10.1021/bk-1995-0582 DOI: https://doi.org/10.1021/bk-1995-0582.ch020

Donayre, D.K.M., Dalisay, T.U. (2016). Identities, characteristics, and assemblages of dematiaceous-endophytic fungi isolated from tissues of barnyard grass weed. Philippine Journal of Science 145, 153–164.

Egamberdieva, D., Wirth, S., Alqarawi, A., Abd Allah, E.F., Hashem, A. (2017). Phytohormones and beneficial microbes. Essential components for plants to balance stress and fitness. Frontiers in Microbiology 8, 2104. DOI: https://doi.org/10.3389/fmicb.2017.02104

El-Hasan, A., Walker, J., Schone, J., Buchenaurer, H. (2009). Detection of viridiofungin A and other antifungal metabolites excreted by Trichoderma harzanium active against different plant pathogens. European Journal of Plant Pathology 124, 457–470. DOI: https://doi.org/10.1007/s10658-009-9433-3

Elhindi, K., Hendawy, S.E., Salam, E.M.A. (2016). Foliar application of potassium nitrate affects the growth and photosynthesis in coriander (Coriander sativum L.) plants under salinity. Progress in Nutrition 18, 63–73.

Franken, P. (2012). The plant strengthening root endophyte Piriformospora indica, potential application, and the biology behind it. Applied Microbiology and Biotechnology 96, 1455–1464. DOI: https://doi.org/10.1007/s00253-012-4506-1

Frattarelli, D.A., Reed, M.D., Giacoia, G.P., Aranda, J.V. (2004). Antifungals in systemic neonatal candidiasis. Drugs 64, 949-968. DOI: https://doi.org/10.2165/00003495-200464090-00003

Galani, Y.J.H., Hansen, E.M.O., Droutsas, I. (2022). Effects of combined abiotic stresses on nutrient content of European wheat and implications for nutritional security under climate change. Scientific Reports 12, 5700. DOI: https://doi.org/10.1038/s41598-022-09538-6

Gavito, M.E., Curtis, P.S., Mikkelsen, T.N., Jakobsen, I. (2000). Atmospheric CO2 and mycorrhiza effects on biomass allocation and nutrient uptake of nodulated pea (Pisum sativum L.) plants. Journal of Experimental Botany 51, 1931–1938. DOI: https://doi.org/10.1093/jexbot/51.352.1931

Gonzalez-Teuber, M., Urzua, A., Plaza, P., Bascunan-Godoy, L. (2018). Effects of root endophytic fungi on response of Chenopodium quinoa to drought stress. Plant Ecology 219, 231–240. DOI: https://doi.org/10.1007/s11258-017-0791-1

Grabka, R., Entremont, T.W., Adams, S.J., Walker, A.K., Tanney, J.B., Abbasi, P.A. (2022). Fungal endophytes and their role in agricultural plant protection against pests and pathogens. Plants 11, 384. DOI: https://doi.org/10.3390/plants11030384

Han, W.X., Li, W.Z., Li, X.F., Zhang, H., Yang, S.Z., Du, J.F., Jing, H., Cheng, C.B. (2017). Isolation and identification of endophytic fungus producing Huperzine A from Huperzia serrata. Microbiology China 44, 2153–2160.

Harrach, B.D., Baltruschat, H., Barna, B., Fodor, J., Kogel, K.H. (2013). The mutualistic fungus Piriformospora indica protects barley roots from a loss of antioxidant capacity caused by the necrotrophic pathogen Fusarium culmorum. Molecular Plant-Microbe Interactions 26, 599–605. DOI: https://doi.org/10.1094/MPMI-09-12-0216-R

Holmes, K.A., Schroers, H.J., Thomas, S.E., Evans, H.C., Samuels, G.J. (2004). Taxonomy and biocontrol potential of a new species of Trichoderma from the Amazon basin of South America. Mycological Progress 3, 199–210. DOI: https://doi.org/10.1007/s11557-006-0090-z

Hyde, K.D., Xu, J.C., Rapior, S., Jeewon, R., Lumyong, S., Niego, A.G.T., Abeywickrama, P.D., Aluthmuhandiram, J.V.S., Brahamanage, R.S., Brooks, S. (2019). The amazing potential of fungi: 50 ways we can exploit fungi industrially. Fungal Diversity 97, 141–136. DOI: https://doi.org/10.1007/s13225-019-00430-9

Idbella, M., Zotti, M., Cesarano, G., Fechtali, T., Mazzoleni, S., Bonanomi, G. (2019). Fungal endophytes affect plant response to leaf litter with contrasting chemical traits. Community. Ecology 20, 205–213. DOI: https://doi.org/10.1556/168.2019.20.2.10

Igiehon, N.O., Babalola, O.O., Cheseto, X., Torto, B. (2021). Effects of rhizobia and arbuscular mycorrhizal fungi on yield, size distribution and fatty acid of soybean seeds grown under drought stress. Microbiological Research 242, 126640. DOI: https://doi.org/10.1016/j.micres.2020.126640

Ikram, M., Niaz, A., Gul, J., Farzana, G.J., Naeem, K. (2019). Endophytic fungal diversity and their interaction with plants for agriculture sustainability under stressful condition. Recent Patents on Food, Nutrition & Agriculture 10, 1-9.

Jasinski, J.P., Payette, S. (2007). Holocene occurrence of Lophodermium piceae, a black spruce needle endophyte and possible paleoindicator of boreal forest health. Quaternary Research 67, 50-56. DOI: https://doi.org/10.1016/j.yqres.2006.07.008

Jeffries, P. (1995). Biology and ecology of mycoparasitism. Canadian Journal of Botany 73, 1284–1290. DOI: https://doi.org/10.1139/b95-389

Jin, J., Zhao, Q., Zhang, X.M., Li, W.J. (2018). Research progress on bioactive products from endophytes. Journal of Microbiology 38, 103–113.

Johnson, L.J. (2008). Iron and siderophores in fungal-host interactions. Mycological Research 112, 170–183. DOI: https://doi.org/10.1016/j.mycres.2007.11.012

Joly, F.X., Scherer-Lorenzen, M., Haettenschwiler, S. (2023). Resolving the intricate role of climate in litter decomposition. Nature Ecology & Evolution 7, 214-223. DOI: https://doi.org/10.1038/s41559-022-01948-z

Kamran, M., Imran, Q.M., Ahmed, M.B., Falak, N., Khatoon, A., Yun, B.W. (2022). Endophyte-mediated stress tolerance in plants: A sustainable strategy to enhance resilience and assist crop improvement. Cells 11, 3292. DOI: https://doi.org/10.3390/cells11203292

Katoch, M., Pull, S. (2017). Endophytic fungi associated with Monarda citriodora, an aromatic and medicinal plant and their biocontrol potential. Pharmaceutical Biology 55, 1528–1535. DOI: https://doi.org/10.1080/13880209.2017.1309054

Khan, A.L., Waqas, M., Khan, A.R., Hussain, J., Kang, S.M. (2013). Fungal endophyte Penicillium janthinellum LK5 improves growth of ABA-deficient tomato under salinity. World Journal of Microbiology and Biotechnology 29, 2133–2144. DOI: https://doi.org/10.1007/s11274-013-1378-1

Khan, N., Afroz, F., Begum, M. N., Rony, S.R., Sharmin, S., Moni, F., Hasan, C.M., Shaha, K., Sohrab, M.H. (2018). Endophytic Fusarium solani: A rich source of cytotoxic and antimicrobial napthaquinone and aza-anthraquinone derivatives. Toxicology Reports 5, 970–976. DOI: https://doi.org/10.1016/j.toxrep.2018.08.016

Khan, S.A., Hamayun M., Yoon H., Kim H.Y., Suh S.J., Hwang S.K., Kong W.S. (2008). Plant growth promotion and Penicillium citrinum. BMC Microbiology 8, 231. DOI: https://doi.org/10.1186/1471-2180-8-231

Khanam, Z., Gupta, S., Verma, A. (2020). Endophytic fungi-based biosensors for environmental contaminants- A perspective. South African Journal of Botany 132, 401–406. DOI: https://doi.org/10.1016/j.sajb.2020.08.007

Khare, E., Mishra, J., Arora, N.K. (2018). Multifaceted interactions between endophytes and plants, development and prospects. Frontiers in Microbiology 9, 2732. DOI: https://doi.org/10.3389/fmicb.2018.02732

Kim, S.H., Vujanovic, V. (2016). Relationship between mycoparasites lifestyles and biocontrol behaviors against Fusarium spp. and mycotoxins production. Applied Microbiology and Biotechnology 100, 5257–5272. DOI: https://doi.org/10.1007/s00253-016-7539-z

Kloepper, J.W., Tuzun, S., Kuc, J.A. (1992). Proposed definitions related to induced disease resistance. Biocontrol Science and Technology 2, 349–351. DOI: https://doi.org/10.1080/09583159209355251

Kohl, J., Postma, J., Nicot, P., Ruocco, M., Blum, B. (2011). Stepwise screening of microorganisms for commercial use in biological control of plant-pathogenic fungi and bacteria. Biological control 57, 1–12. DOI: https://doi.org/10.1016/j.biocontrol.2010.12.004

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. DOI: https://doi.org/10.1111/j.1469-8137.2007.02008.x

Kusari, S., Hertweck, C., Spiteller, M. (2012). Chemical ecology of endophytic fungi: origins of secondary metabolites. Chemistry & Biology 19, 792–798. DOI: https://doi.org/10.1016/j.chembiol.2012.06.004

Kushwaha, R.K., Singh, S., Pandey, S.S., Kalra, A., Babu, C.V. (2019). Fungal endophytes attune with an olide biosynthesis in Withania somnifera, prime to enhanced withanolide A content in leaves and roots. World Journal of Microbiology and Biotechnology 35, 20. DOI: https://doi.org/10.1007/s11274-019-2593-1

Lahlali, R., Hijri, M. (2010). Screening, identification and evaluation of potential biocontrol fungal endophytes against Rhizoctonia solani AG3 on potato plants. FEMS Microbiology Letters 311, 152–159. DOI: https://doi.org/10.1111/j.1574-6968.2010.02084.x

Laihonen, M., Saikkonen, K., Helander, M., Vázquez, D., Aldana, B.R. (2022). Epichloë endophyte-promoted seed pathogen increases host grass resistance against insect herbivory. Frontiers in Microbiology 12, 786619. DOI: https://doi.org/10.3389/fmicb.2021.786619

Lata, R., Chowdhury, S., Gond, S., White, J.F. (2018). Induction of abiotic stress tolerance in plants by endophytic microbes. Letters in Applied Microbiology 66, 268–276. DOI: https://doi.org/10.1111/lam.12855

Laur, J., Ramakrishnan, G.B., Labbe, C., Lefebvre, F., Spanu, P.D., Belanger, R.R. (2018). Effectors involved in fungal–fungal interaction lead to a rare phenomenon of hyperbiotrophy in the tritrophic system biocontrol agent–powdery mildew–plant. New Phytologist 217, 713–725. DOI: https://doi.org/10.1111/nph.14851

Lee, S.K., Lee, S.K., Bae, H., Seo, S.T., Lee, J.K. (2014). Effects of water stress on the endophytic fungal communities of Pinus koraiensis needles infected by Cenangium ferruginosum. Mycobiology 42, 331–338. DOI: https://doi.org/10.5941/MYCO.2014.42.4.331

Li, H.Y., Da-Qiao, W., Mi, S., Zuo-Ping, Z. (2012). Endophytes and their role in phytoremediation. Fungal Diversity 54, 11–18. DOI: https://doi.org/10.1007/s13225-012-0165-x

Liu, G.R., Huo, R.Y., Zhai, Y.N., Liu, L. (2021). New bioactive sesquiterpeniods from the plant endophytic fungus Pestalotiopsis theae. Frontiers in Microbiology 12, 641504. DOI: https://doi.org/10.3389/fmicb.2021.641504

Lugtenberg, B.J.J., Caradus, J.R., Johnson, L.J. (2016). Fungal endophytes for sustainable crop production. FEMS Microbiology Ecology 92, 194. DOI: https://doi.org/10.1093/femsec/fiw194

Ma, Y., Miroslav, V., Freitas, H. (2019). Beneficial microbes alleviate climatic stresses in plants. Frontiers in Plant Science 10, 595. DOI: https://doi.org/10.3389/fpls.2019.00595

Macia-Vicente, J.G., Rosso, L.C., Ciancio, A., Jansson, H.B., Lopez-Llorca, L.V. (2009). Colonisation of barley roots by endophytic Fusarium equiseti and Pochonia chlamydosporia: Effects on plant growth and disease. Annals of Applied Biology 155, 391–401. DOI: https://doi.org/10.1111/j.1744-7348.2009.00352.x

Malinowski, D.P., Belesky, D.P. (2016). Ecological importance of Neotyphodium sp. grass endophytes in agroecosystems. Grass and Forage Science 52, 23-28.

Mane, R.S., Paarakh, P.B., Vedamurthy, A.B. (2018). Brief review on fungal endophytes. International Journal of Secondary Metabolite 5, 288–303. DOI: https://doi.org/10.21448/ijsm.482798

Mao, Z.L., Zhang, W.H., Wu, C.Y., Feng, H., Peng, Y.H., Shahid, H., Cui, Z.N., Ding, P., Shan, T.J. (2021). Diversity and antibacterial activity of fungal endophytes from Eucalyptus exserta. BMC Microbiology 21, 155. DOI: https://doi.org/10.1186/s12866-021-02229-8

Marquez, L.M., Redman, R.S., Rodriguez, R.J., Roossinck, M.J. (2007). A virus in a fungus in a plant – three-way symbiosis required for thermal tolerance. Science 315, 513–515. DOI: https://doi.org/10.1126/science.1136237

Martinuz, A., Schouten, A., Sikora, R.A. (2012). Systemically induced resistance and microbial competitive exclusion: implications on biological control. Phytopathology 102, 260–266. DOI: https://doi.org/10.1094/PHYTO-04-11-0120

Miliute, I., Buzaite, O., Baniulis, D., Stanys, V. (2015). Bacterial endophytes in agricultural crops and their role in stress tolerance: A review. Zemdirbyste-Agriculture 102, 465–478. DOI: https://doi.org/10.13080/z-a.2015.102.060

Mohandoss, J., Suryanarayanan, T.S. (2009). Effect of fungicide treatment on foliar fungal endophyte diversity in mango. Sydowia 61, 11–24.

Mousa, W.K., Raizada, M.N. (2013). The diversity of antimicrobial secondary metabolites produced by fungal endophytes: An interdisciplinary perspective. Frontiers in Microbiology 4, 65. DOI: https://doi.org/10.3389/fmicb.2013.00065

Mueller, G.M., Bills, G.F., Foster, M.S. (2004). Biodiversity of Fungi: Inventory and Monitoring Methods. Elsevier Inc. Amsterdam, The Netherlands. https://doi.org/10.1016/B978-0-12-509551-8.X5000-4 DOI: https://doi.org/10.1016/B978-0-12-509551-8.X5000-4

Mukhtar, H., Wunderlich, R.F., Muzaffar, A., Ansari, A., Shipin, O.V., Cao, T.N.D., Lin, Y.P. (2023) Soil microbiome feedback to climate change and options for mitigation. Science of The Total Environment 882, 163412. DOI: https://doi.org/10.1016/j.scitotenv.2023.163412

Murphy, B., Fiona, R., Doohan, M., Trevor, R., Hodkinson (2018). From concept to commerce, developing a successful fungal endophyte inoculant for agricultural crops. Journal of Fungi 4, 24. DOI: https://doi.org/10.3390/jof4010024

Naseem, H., Ahsan, M., Shahid, M.A., Khan, N. (2018). Exopolysaccharides producing rhizobacteria and their role in plant growth and drought tolerance. Journal of Basic Microbiology 2018, 1–14 DOI: https://doi.org/10.1002/jobm.201800309

Nassimi, Z., Taheri, P. (2017). Endophytic fungus Piriformospora indica induced systemic resistance against rice sheath blight via affecting hydrogen peroxide and antioxidants. Biocontrol Science and Technology 27, 252–267. DOI: https://doi.org/10.1080/09583157.2016.1277690

Ngwene, B., Boukail, S., Sollner, L., Franken, P., Andrade-Linares, D.R. (2016). Phosphate utilization by the fungal root endophyte Piriformospora indica. Plant and Soil 405, 231–241. DOI: https://doi.org/10.1007/s11104-015-2779-8

Nizam, S., Qiang, X., Wawra, S., Nostadt, R., Getzke, F., Schwanke, F., Zuccaro, A. (2019). Serendipita indica E50 NT modulates extracellular nucleotide levels in the plant apoplast and affects fungal colonization. EMBO Reports 20, e47430. DOI: https://doi.org/10.15252/embr.201847430

Odelade, K.A., Babalola, O.O. (2019). Bacteria, fungi and archaea domains in rhizospheric soil and their effects in enhancing agricultural productivity. International Journal of Environmental Research and Public Health 16, 3873. DOI: https://doi.org/10.3390/ijerph16203873

Okon, O.G., Matrood, A.A., Rhouma, A., Antia, U.E. (2022). Synergistic effect of arbuscular mycorrhizal fungi and poultry manure to significantly increase proximal structure and physiological parameters of Cucurbita maxima and Telfairia occidentalis under soil salinity. Nova Biotechnologica et Chimica 21, e1170. DOI: https://doi.org/10.36547/nbc.1170

Okoye, F.B., Lu, S., Nworu, C.S., Esimone, C.O., Proksch, P., Chadlic, A., Debbaba, A. (2013). Depsidone and diaryl ether derivatives from the fun gus Corynespora cassiicola, an endophyte of Gongronema latifolium. Tetrahedron Letters 54, 4210–4214. DOI: https://doi.org/10.1016/j.tetlet.2013.05.117

Olszewski N., Sun, T.P., Gubler, F. (2012). Gibberellin signaling, biosynthesis, catabolism, and response pathways. Plant Cell 14, 561–580.

Pamphile, J.A., Azevedo, J.L. (2002). Molecular characterization of endophytic strains of Fusarium verticillioides (Fusarium moniliforme) from maize (Zea mays L). World Journal of Microbiology and Biotechnology 18, 391-396. DOI: https://doi.org/10.1023/A:1015507008786

Parfrey, L.W., Lahr, D.J., Knoll, A.H., Katz, L.A. (2011). Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proceedings of the National Academy of Sciences 108, 13624-13629. DOI: https://doi.org/10.1073/pnas.1110633108

Patchett, A., Newman, J.A. (2021). Comparison of plant metabolites in root exudates of Lolium perenne infected with different strains of the fungal endophyte Epichlo festucae var. lolii. Journal of Fungi 7, 148. DOI: https://doi.org/10.3390/jof7020148

Pereira, C.B., Oliveira, D.M., Hughes, A.F., Kohlhoff, M., Vieira, M.L. (2015). Endophytic fungal compounds active against Cryptococcus neoformans and C. gattii. Journal of Antibiotics 68, 436–444. DOI: https://doi.org/10.1038/ja.2015.11

Petrini, O. (1991). Fungal Endophytes of Tree Leaves. In: Andrews, J.H., Hirano, S.S. (eds) Microbial ecology of leaves. Brock/Springer series in contemporary bioscience. Springer, New York, NY. https://doi.org/10.1007/978-1-4612-3168-4_9 DOI: https://doi.org/10.1007/978-1-4612-3168-4_9

Raviraja, N.S., Sridhar, K.R., Barlocher F. (1996). Endophytic aquatic hyphomycetes of roots of plantation crops and ferms from India. Sydowia 48, 152-60.

Redecker, D., Kodner, R., Graham, L.E. (2000). Glomalean fungi from the Ordovician. Science 289, 1920–1921. DOI: https://doi.org/10.1126/science.289.5486.1920

Rehman, S., Akhtar, M., Abdullah, S.N.A. (2016). Plant, Soil and Microbes. Cham: Springer. https://doi.org/10.1007/978-3-319-27455-3 DOI: https://doi.org/10.1007/978-3-319-27455-3

Ripa, F.A., Cao, W., Tong, S., Sun, J.G. (2019). Assessment of plant growth promoting and abiotic stress tolerance properties of wheat endophytic fungi. BioMed Research International 2019, 1–12. DOI: https://doi.org/10.1155/2019/6105865

Rodríguez, M.C.H., Evans, H.C., de Abreu, L.M., Macedo, M., Miraine, K., Bekele, K.B. (2021). New species and records of Trichoderma isolated as mycoparasites and endophytes from cultivated and wild coffee in Africa. Scientific Reports 11, 5671. DOI: https://doi.org/10.1038/s41598-021-84111-1

Rodriguez, R.J., White, J.F., Arnold, A.E., Redman, R.S. (2009). Fungal endophytes: Diversity and functional roles. New Phytologist 182, 314–330. DOI: https://doi.org/10.1111/j.1469-8137.2009.02773.x

Rouhier, N., Koh, C.S., Gelhaye, E., Corbier, C., Favier, F., Didierjean, C. (2008). Redox based antioxidant systems in plants: biochemical and structural analyses. Biochimica et Biophysica Acta 1780, 1249–1260. DOI: https://doi.org/10.1016/j.bbagen.2007.12.007

Ryan, R.P., Germaine, K., Franks, A., Ryan, D.J., Dowling, D.N. (2008). Bacterial endophytes: Recent developments and applications. FEMS Microbiology Letters 278, 1–9. DOI: https://doi.org/10.1111/j.1574-6968.2007.00918.x

Sahar, L., Doustmorad, Z. (2018). Antiproliferative and antimicrobial activities of secondary metabolites and phylogenetic study of endophytic Trichoderma species from Vinca plants. Frontiers in Microbiology 9, 1484. DOI: https://doi.org/10.3389/fmicb.2018.01484

Sahoo, S., Sarangi, S., Kerry, R.G. (2017). Bioprospecting of endophytes for agricultural and environmental sustainability (Chapter-19) in Microbial Biotechnology. Patra, J.K. (ed.) 429–458. https://doi.org/10.1007/978-981-10-6847-8_19 DOI: https://doi.org/10.1007/978-981-10-6847-8_19

Sana, T., Siddiqui, B.S., Shahzad, S., Farooq, A.D., Siddiqui, F., Sattar, S., Begumet, S. (2019). Antiproliferative activity and characterization of metabolites of Aspergillus nidulans: An endophytic fungus from Nyctanthes arbor-tristis linn. against three human cancer cell lines. Medicinal Chemistry 15, 352–359. DOI: https://doi.org/10.2174/1573406414666180828124252

Seetharaman, P., Gnanasekar, S., Chandrasekaran, R., Chandrakasan, G., Kadarkarai, M., Sivaperumal, S. (2017). Isolation and characterization of anticancer flavone chrysin (5,7-dihydroxy flavone)-producing endophytic fungi from Passiflora incarnata L. leaves. Annals of Microbiology 67, 321–331. DOI: https://doi.org/10.1007/s13213-017-1263-5

Shiomi, H.F., Silva, H.S.A., Melo, I.S.D., Nunes, F.V., Bettiol, W. (2006). Bioprospecting endophytic bacteria for biological control of coffee leaf rust. Scientia Agricola 63(1), 32-39. DOI: https://doi.org/10.1590/S0103-90162006000100006

Singh, N., Singh, A., Dahiya, P. (2021). Plant growth-promoting endophytic fungi from different habitats and their potential applications in agriculture,” in Recent trends in Mycological Research. Fungal Biology, Yadav, A.N. (ed.) (Cham: Springer) https://doi.org/10.1007/978-3-030-60659-6_3 DOI: https://doi.org/10.1007/978-3-030-60659-6_3

Srivastava, A., Srivastava, N., Sayyed, R.Z. (2012). In vitro bio-control activity of Trichoderma species against phytopathogenic A. brassicae. International Journal of Biotechnology and Biosciences 2, 6–9.

Srivastava, A., Srivastava, N., Sayyed, R.Z. (2014). Bio-control Potential of Trichoderma Species Against Alternaria brassicae. Recent advances in biofertilizers & biofungicides (PGPR) for sustainable Agriculture. London, UK: Cambridge Scholars Press, 393–400.

Stanley, S.J. (1992). Observations on the seasonal occurrence of marine endophytic andparasitic fungi. Canadian Journal of Botany 70, 2089-2096. DOI: https://doi.org/10.1139/b92-259

Strobel, G.A., Stierle, A., Stierle, D., Hess, W.M. (1993). Taxomces andreanaea proposed new taxon for a bulbilliferous hyphomycete associated with Pacific yew. Mycotaxon 47: 71-78.

Sukmawati, D., Family, N., Hidayat, I., Sayyed, R.Z., Elsayed, E.A., Dailin, D.J. (2021). Biocontrol activity of Aureubasidium pullulans and Candida orthopsilosis isolated from tectona grandis l. phylloplane against Aspergillus sp. in post-harvested citrus fruit. Sustainability 13, 7479. DOI: https://doi.org/10.3390/su13137479

Suryanarayanan, T.S. (2013). Endophyte research: going beyond isolation and metabolite documentation. Fungal Ecology 6, 561–568. DOI: https://doi.org/10.1016/j.funeco.2013.09.007

Tang, J., Xu, L., Chen, X., Hu, S. (2009). Interaction between C4 barnyard grass and C3 upland rice under elevated CO2, impact of mycorrhizae. Acta Oecologica 35, 227–235. DOI: https://doi.org/10.1016/j.actao.2008.10.005

Thines, E., Anke, H., Weber, R. W. S. S. (2004). Fungal secondary metabolites as inhibitors of infection-related morphogenesis in phytopathogenic fungi. Mycological Research 108, 14–25. DOI: https://doi.org/10.1017/S0953756203008943

Ting, A.S.Y., Mah, S.W., Tee, C.S. (2010). Identification of volatile metabolites from fungal endophytes with biocontrol potential towards Fusarium oxysporum f. sp. cubense Race 4. American Journal of Agricultural and Biological Sciences 5, 177–182. DOI: https://doi.org/10.3844/ajabssp.2010.177.182

Tintjer, T., Rudgers, J.A. (2006). Grass herbivore interaction altered by strains of a native endophyte. New Phytologist 170, 513-21. DOI: https://doi.org/10.1111/j.1469-8137.2006.01720.x

Tuna A.L., Kaya C., Dikilitas M., Higgs D. (2008). The combined effects of gibberellic acid and salinity on some antioxidant enzyme activi ties, plant growth parameters and nutritional status in maize plants. Environmental and Experimental Botany 63, 1–9. DOI: https://doi.org/10.1016/j.envexpbot.2007.06.007

Varma, A., Kost, G., Oelmuller, R. (2013). Piriformospora indica. sebacinales and their biotechnological applications. Springer Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-33802-1 DOI: https://doi.org/10.1007/978-3-642-33802-1

Walters, D., Walsh, D., Newton, A., Lyon, G. (2005). Induced resistance for plant disease control: maximizing the efficacy of resistance elicitors. Phytopathology 95, 1368–1373. DOI: https://doi.org/10.1094/PHYTO-95-1368

Wang, J., Li, T., Liu, G.Y. (2016). Unraveling the role of dark septate endophyte (DSE) colonizing maize (Zea mays) under cadmium stress: Physiological, cytological and genic aspects. Scientific Reports 6, 22028. DOI: https://doi.org/10.1038/srep22028

Waqas, M., Khan, A. L., Lee, I.J. (2014). Bioactive chemical constituents produced by endophytes and effects on rice plant growth. Journal of Plant Interactions 9, 478–487. DOI: https://doi.org/10.1080/17429145.2013.860562

Wei, Q.Y., Li, Y.Y., Xu, C., Wu, Y.X., Zhang, Y.R., Liu, H. (2020). Endophytic colonization by Beauveria bassiana increases the resistance of tomatoes against Bemisia tabaci. Arthropod-Plant Interactions 14, 289–300. DOI: https://doi.org/10.1007/s11829-020-09746-9

Wen, J., Samuel, K.O., Shu, W., Jianchen, W., Lei, X., Yinan, R., Yanchun, H. (2022). Endophytic fungi: An effective alternative source of plant-derived bioactive compounds for pharmacological studies. Journal of Fungi 8, 205. DOI: https://doi.org/10.3390/jof8020205

Wilson, D. (1995). Endophytes- The evolution of a term and clarification of its use and definition. Oikos 73, 274–276. DOI: https://doi.org/10.2307/3545919

Xiao, X., Luo, S.L., Zeng, G.M., Wei, W.Z., Wan, Y. (2010). Biosorption of cadmium by endophytic fungus (EF) Microsphaeropsis sp. LSE10 isolated from cadmium hyperaccumulator Solanum nigrum L. Bioresource Technology 101, 1668–1674. DOI: https://doi.org/10.1016/j.biortech.2009.09.083

Yadav, A., Yadav, K. (2017). Exploring the potential of endophytes in agriculture, a mini review. Advances in Plants & Agriculture Research 6, 102–106. DOI: https://doi.org/10.15406/apar.2017.06.00221

Yang, B., Ma, H.Y., Wang, X. M., Jia, Y., Hu, J., Li, X., Dai, C.C. (2014a). Improvement of nitrogen accumulation and metabolism in rice (Oryza sativa L.) by the endophyte Phomopsis liquidambari. Plant Physiology and Biochemistry 82, 172–182. DOI: https://doi.org/10.1016/j.plaphy.2014.06.002

Yang, B., Wang, X., Ma, H., Yang, T., Jia, Y., Zhou, J., Dai, C. (2015). Fungal endophyte Phomopsis liquidambari affects nitrogen transformation processes and related microorganisms in the rice rhizosphere. Frontiers in Microbiology 6, 982. DOI: https://doi.org/10.3389/fmicb.2015.00982

Yang, H., Wang, Y., Zhang, Z., Yan, R., Zhu, D. (2014b). Whole-genome shotgun assembly and analysis of the genome of Shiraia sp. strain Slf14, a novel endophytic fungus producing huperzine A and hypocrellin A. Genome announcements 2, e00011-e00014. DOI: https://doi.org/10.1128/genomeA.00011-14

Yu, H., Zhang, L., Li, L., Zheng, C., Guo, L., Li, W., Sun, P., Qin, L. (2010). Recent developments and future prospects of antimicrobial metabolites produced by endophytes. Microbiological Research 165, 437–449. DOI: https://doi.org/10.1016/j.micres.2009.11.009

Yung, L., Sirguey, C., Azou-Barré, A., Blaudez, D. (2021). Natural fungal endophytes from Noccaea caerulescens mediate neutral to positive effects on plant biomass, mineral nutrition and Zn Phytoextraction. Frontiers in Microbiology 12, 689367. DOI: https://doi.org/10.3389/fmicb.2021.689367

Zahoor, M., Muhammad, I., Hazir, R., Muhammad, Q., Sahib, A. (2017). Alleviation of heavy metal toxicity and phytostimulation of Brassica campestris L. by endophytic Mucor sp. MHR-7. Ecotoxicology and Environmental Safety 142, 139–149. DOI: https://doi.org/10.1016/j.ecoenv.2017.04.005

Zhang, J.Y., Tao, L.Y., Liang, Y.J., Chen, L.M., Mi, Y.J., Zheng, L.S., Wang, F., She, Z.G., Lin, Y.C., To, K.K.W., Fu, L.W. (2010). Anthracenedione derivatives as anticancer agents isolated from secondary metabolites of the mangrove endophytic fungi. Marine Drugs 8, 1469–1481. DOI: https://doi.org/10.3390/md8041469