Microbial Endophytes: A Hidden Plant Resident, Application and Their Role in Abiotic Stress Management in Plants

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Authors

  • Division of Microbial Technology, CSIR - National Botanical Research Institute, Rana Pratap Marg, Lucknow – 226001, Uttar Pradesh ,IN
  • IIRC-3, Plant-Microbe Interaction and Molecular Immunology Laboratory, Department of Biosciences, Faculty of Sciences, Integral University, Lucknow – 226006, Uttar Pradesh ,IN
  • IIRC-3, Plant-Microbe Interaction and Molecular Immunology Laboratory, Department of Biosciences, Faculty of Sciences, Integral University, Lucknow – 226006, Uttar Pradesh ,IN
  • Division of Microbial Technology, CSIR - National Botanical Research Institute, Rana Pratap Marg, Lucknow – 226001, Uttar Pradesh ,IN
  • Division of Microbial Technology, CSIR - National Botanical Research Institute, Rana Pratap Marg, Lucknow – 226001, Uttar Pradesh ,IN
  • Division of Microbial Technology, CSIR - National Botanical Research Institute, Rana Pratap Marg, Lucknow – 226001, Uttar Pradesh ,IN

DOI:

https://doi.org/10.18311/jeoh/2022/30619

Keywords:

Defense Management, Endophytes, Environmental Stress
Plant-Microbe-Interaction

Abstract

Microbial communities in nature involve complex interactions with several biotic and abiotic components. An endo-symbiotic association is one in which one organism lives within the host plant for at least a part of its life. It is often obligate and does not create visible disease and has been reported to exist for at least 400 million years. Beneficial endophytes promote plant nutrient uptake, host plant growth, reduce disease severity, inhibit plant pathogens and improve tolerance to environmental stresses. Stresses like salinity, alkalinity, drought, global warming, temperature and pollution will increase in prominence and endophytes are predicted to play a significant role and offer eco-friendly techniques to increase productivity under such conditions. There also exists the potential for genetic modification of endophytes to impart additional stress tolerance traits in hosts. The present review discusses the beneficial effect of fungal and bacterial endophytes, emphasizing improving crop productivity under abiotic stress conditions. The review also discusses the various aspects of physiological and molecular mechanisms determining the interaction and stress tolerance, enhancing plant functions and productivity.

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Published

2022-09-30

How to Cite

Fatima, T., Sharma, S., Bano, A., Srivastava, D., Verma, I., & Singh, P. C. (2022). Microbial Endophytes: A Hidden Plant Resident, Application and Their Role in Abiotic Stress Management in Plants. Journal of Ecophysiology and Occupational Health, 22(3), 127–140. https://doi.org/10.18311/jeoh/2022/30619
Received 2022-07-06
Accepted 2022-09-12
Published 2022-09-30

 

References

Rusty R, Regina Redman R. More than 400 million years of evolution and some plants still can’t make it on their own: Plant stress tolerance via fungal symbiosis. Journal of Experimental Botany. 2008; 59(5):1109–14. PMid: 18267941. https://doi.org/10.1093/ jxb/erm342 DOI: https://doi.org/10.1093/jxb/erm342

Chaturvedi H, Singh V, Gupta G. Potential of bacterial endophytes as plant growth promoting factors. J Plant Pathol Microbiol. 2016; 7(9):1–6. DOI: https://doi.org/10.4172/2157-7471.1000376

Lata R, Chowdhury S, Gond SK, White JF. Induction of abiotic stress tolerance in plants by endophytic microbes. Letters in Applied Microbiology. 2018; 66(4):258–76. PMid: 29359344. https://doi.org/10.1111/lam.12855 DOI: https://doi.org/10.1111/lam.12855

Michael K, Taylor TN, Hass H, Kerp H, Dotzler N, Hermsen EJ. Fungal endophytes in a 400-million-yr-old land plant: Infection pathways, spatial distribution, and host responses. New Phytologist. 2007; 174(3):648–57. PMid: 17447919. https://doi. org/10.1111/j.1469-8137.2007.02008.x DOI: https://doi.org/10.1111/j.1469-8137.2007.02008.x

Gunatilaka A, Leslie A. Natural products from plant-associated microorganisms: Distribution, structural diversity, bioactivity and implications of their occurrence. Journal of Natural Products. 2006; 69(3):509–26. PMid: 16562864 PMCid: PMC3362121. https://doi.org/10.1021/np058128n DOI: https://doi.org/10.1021/np058128n

Gustavo S, Moreno-Hagelsieb G, Orozco-Mosqueda MDC, Glick BR. Plant growth-promoting bacterial endophytes. Microbiological Research. 2016; 183:92–9. PMid: 26805622. https://doi.org/10.1016/j.micres.2015.11.008 7. Khare E, Mishra J, Arora, NK. Multifaceted interactions between endophytes and plant: Developments and prospects. Frontiers in Microbiology. 2018; 9:2732. DOI: https://doi.org/10.1016/j.micres.2015.11.008

Daniya E, Arthikala MK, Melappa G, Santoyo G. Alternaria Species: Endophytic fungi as alternative sources of bioactive compounds. Italian Journal of Mycology. 2018; 47(1):40–54. https://doi.org/10.6092/issn.2531-7342/8468

Fadiji AE, Babalola OO. Elucidating mechanisms of endophytes used in plant protection and other bioactivities with multifunctional prospects. Frontiers in Bioengineering and Biotechnology. (2020). 8, 467. PMid: 32500068 PMCid: PMC7242734. https:// doi.org/10.3389/fbioe.2020.00467 DOI: https://doi.org/10.3389/fbioe.2020.00467

Dubey A, Malla MA, Kumar A, Dayanandan S, Khan ML. Plants endophytes: Unveiling hidden agenda for bioprospecting toward sustainable agriculture. Critical Reviews in Biotechnology. 2020; 40(8):1210–31. PMid: 32862700. https://doi.org/10.1080/073885 51.2020.1808584 DOI: https://doi.org/10.1080/07388551.2020.1808584

Faegheh E, Harighi B. Isolation and identification of endophytic bacteria with plant growth promoting activity and biocontrol potential from wild pistachio trees. Plant Pathology Journal. 2018; 34(3):208–17. PMid: 29887777 PMCid: PMC5985647. https://doi.org/10.5423/PPJ.OA.07.2017.0158 DOI: https://doi.org/10.5423/PPJ.OA.07.2017.0158

Brunetti C, Saleem AR, Della Rocca G, Emiliani G, De Carlo A, Balestrini R, Centritto, M. Effects of plant growth-promoting rhizobacteria strains producing ACC deaminase on photosynthesis, isoprene emission, ethylene formation and growth of Mucuna pruriens (L.) DC. in response to water deficit. Journal of Biotechnology. 2021; 331:53–62. PMid: 33727083. https://doi. org/10.1016/j.jbiotec.2021.03.008 DOI: https://doi.org/10.1016/j.jbiotec.2021.03.008

Zandalinas SI, Balfagón, Gómez-Cadenas A, Mittler, R. Responses of plants to climate change: Metabolic changes during abiotic stress combination in plants. Journal of Experimental Botany. 2022; 73(11):3339–54. PMid: 35192700. https://doi. org/10.1093/jxb/erac073 DOI: https://doi.org/10.1093/jxb/erac073

Adeleke BS, Babalola OO. The plant endosphere-hidden treasures: A review of fungal endophytes. Biotechnology and Genetic Engineering Reviews. 2021; 37(2):154–77. PMid: 34666635. https://doi.org/10.1080/02648725.2021.1991714 DOI: https://doi.org/10.1080/02648725.2021.1991714

Chao Z, Wang J, Liu G, Song Z, Fang L. Impact of soil leachate on microbial biomass and diversity affected by plant diversity. Plant and Soil. 2019; 439(1-2):505–23. https://doi.org/10.1007/s11104- 019-04032-x. DOI: https://doi.org/10.1007/s11104-019-04032-x

Deyett E, Rolshausen PE. Endophytic microbial assemblage in grapevine. FEMS Microbiology Ecology. 2020; 96(5):fiaa053. DOI: https://doi.org/10.1093/femsec/fiaa053

Materatski P, Varanda C, Carvalho T, Dias AB, Campos MD, Rei F, Félix MDR. Spatial and temporal variation of fungal endophytic richness and diversity associated to the phyllosphere of olive cultivars. Fungal Biology. 2019; 123(1):66–76. PMid: 30654959. https://doi.org/10.1016/j.funbio.2018.11.004. DOI: https://doi.org/10.1016/j.funbio.2018.11.004

Dhayanithy G, Kamalraj S, Jayabaskaran C. Diversity and biological activities of endophytic fungi associated with catharanthus roseus. BMC Microbiology. 2019. PMid: 30665368 PMCid: PMC6341747. https://doi.org/10.1186/s12866-019-1386-x. DOI: https://doi.org/10.1186/s12866-019-1386-x

Daru BH, Bowman EA, Pfister DH, A. Elizabeth Arnold AE. A novel proof of concept for capturing the diversity of endophytic fungi preserved in herbarium specimens. Philosophical Transactions of the Royal Society B: Biological Sciences. 2019; 374. PMid: 30455213 PMCid: PMC6282087. https://doi. org/10.1098/rstb.2017.0395 DOI: https://doi.org/10.1098/rstb.2017.0395

Jiang M, Wang Z, Li X, Liu S, Song F, Liu F. Relationship between endophytic microbial diversity and grain quality in wheat exposed to multi-generational CO2 elevation. Science of The Total Environment. 2021; 776:146029. PMid: 33652312. https:// doi.org/10.1016/j.scitotenv.2021.146029 DOI: https://doi.org/10.1016/j.scitotenv.2021.146029

Enquahone S, van Marle G, Simachew A. Plant growth-promoting characteristics of halotolerant endophytic bacteria isolated from Sporobolus spicatus (Vahr) Kunth and Cyperus laevigatus L. of Ethiopian rift valley lakes. Archives of Microbiology. 2022; 204(7):1–15. PMid: 35723754. https://doi.org/10.1007/s00203- 022-03021-6 DOI: https://doi.org/10.1007/s00203-022-03021-6

Shah S, Shah B, Sharma R, Rekadwad B, Shouche YS, Sharma J, Pant B. Colonization with non-mycorrhizal culturable endophytic fungi enhances orchid growth and indole acetic acid production. BMC Microbiology. 2022; 22(1):1–13. PMid: 35418028 PMCid: PMC9006483. https://doi.org/10.1186/s12866-022-02507-z DOI: https://doi.org/10.1186/s12866-022-02507-z

Yavad U, Bano N, Bag S, Srivastava S, Singh PC. An insight into the endophytic bacterial community of tomato after spray application of Propiconazole and Bacillus subtilis Strain NBRI-W9. Microbiology Spectrum. Accepted. 2022.

Li JL, Sun X, Zheng Y, Lü PP, Wang YL, Guo LD. Diversity and community of culturable endophytic fungi from stems and roots of desert halophytes in northwest China. MycoKeys. 2020; 62:75. PMid: 32076383 PMCid: PMC7010840. https://doi.org/10.3897/ mycokeys.62.38923 DOI: https://doi.org/10.3897/mycokeys.62.38923.figure2

Wolfe ER, Ballhorn DJ. Do foliar endophytes matter in litter decomposition? Microorganisms. 2020; 8(3):446. PMid: 32245270 PMCid: PMC7143956. https://doi.org/10.3390/microorganisms8030446 DOI: https://doi.org/10.3390/microorganisms8030446

Verma SK, Gond SK, Mishra A, Sharma VK, Kumar J, Singh DK, Kharwar RN. Fungal endophytes representing diverse habitats and their role in plant protection. In Developments in Fungal Biology and Applied Mycology. 2017; 135–57. Springer, Singapore. DOI: https://doi.org/10.1007/978-981-10-4768-8_9

McCargo PD, Iannone LJ, Soria M, Novas MV. Diversity of foliar endophytes in a dioecious wild grass and their interaction with the systemic Epichloë. Fungal Ecology. 2020; 47:100945. https:// doi.org/10.1016/j.funeco.2020.100945 DOI: https://doi.org/10.1016/j.funeco.2020.100945

Mishra S, Bhattacharjee A, Sharma S. An ecological insight into the multifaceted world of plant-endophyte association. Critical Reviews in Plant Sciences. 2021; 40(2):127–46. https://doi.org/10 .1080/07352689.2021.1901044 DOI: https://doi.org/10.1080/07352689.2021.1901044

Santangelo JS, Kotanen PM. Nonsystemic fungal endophytes increase survival but reduce tolerance to simulated herbivory in subarctic Festuca rubra. Ecosphere. 2016; 7(5):e01260. DOI: https://doi.org/10.1002/ecs2.1260

Bamisile BS, Senyo Akutse K, Dash CK, Qasim M, Ramos Aguila LC, Ashraf HJ, Wang L. Effects of seedling age on colonization patterns of Citrus limon plants by endophytic Beauveria bassiana and Metarhizium anisopliae and their influence on seedlings growth. Journal of Fungi. 2020; 6(1):29. PMid: 32106557 PMCid: PMC7151192. https://doi.org/10.3390/jof6010029 DOI: https://doi.org/10.3390/jof6010029

Tiwari S, Gupta SC, Chauhan PS, Lata, C. An OsNAM gene plays important role in root rhizobacteria interaction in transgenic Arabidopsis through abiotic stress and phytohormone crosstalk. Plant Cell Reports. 2021; 40(1):143–55. PMid: 33084964. https:// doi.org/10.1007/s00299-020-02620-1 DOI: https://doi.org/10.1007/s00299-020-02620-1

dos Santos TB, Ribas AF, de Souza SGH, Budzinski IGF, Domingues DS. Physiological responses to drought, salinity, and heat stress in plants: A review. Stresses. 2022; 2(1):113–35. DOI: https://doi.org/10.3390/stresses2010009

Waller F, Beate A, Helmut B, József F, Katja B, Marina F, Tobias H, et al. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102(38):13386–91. PMid: 16174735 PMCid: PMC1224632. https://doi.org/10.1073/pnas.0504423102 DOI: https://doi.org/10.1073/pnas.0504423102

Khan, Abdul Latif, Muhammad Hamayun, Muhammad Waqas, Sang Mo Kang, Yoon Ha Kim, Duk Hwan Kim, and In Jung Lee. “Exophiala Sp.LHL08 Association Gives Heat Stress Tolerance by Avoiding Oxidative Damage to Cucumber Plants.” Biology and Fertility of Soils. 2012.https://doi.org/10.1007/s00374-011- 0649-y DOI: https://doi.org/10.1007/s00374-011-0649-y

Khan AL, Muhammad H, Yoon HK, Sang MK, In JLee. Ameliorative symbiosis of endophyte (Penicillium funiculosum LHL06) under salt stress elevated plant growth of glycine Max L. Plant Physiology and Biochemistry. 2011; 49(8):852–61. PMid: 21458283. https://doi.org/10.1016/j.plaphy.2011.03.005 DOI: https://doi.org/10.1016/j.plaphy.2011.03.005

Khan AL, Muhammad H, Yoon HK, Sang MK, Joon HL, In JLee. Gibberellins producing endophytic Aspergillus fumigatus Sp. LHO2 influenced endogenous phytohormonal levels, isoflavonoids production and plant growth in salinity stress. Process Biochemistry. 2011; 46(2):440–7. https://doi.org/10.1016/j. procbio.2010.09.013 DOI: https://doi.org/10.1016/j.procbio.2010.09.013

Tripathi RD, Srivastava S, Mishra S, Singh N, Tuli R, Gupta DK, Maathuis FJM. Arsenic hazards: Strategies for tolerance and remediation by plants. Trends in Biotechnology. 2007; 25(4):158–68. PMid: 17306392. https://doi.org/10.1016/j.tibtech.2007.02.003 DOI: https://doi.org/10.1016/j.tibtech.2007.02.003

Arriagada C, Aranda E, Sampedro I, Garcia-Romera I, Ocampo JA. Contribution of the saprobic fungi trametes versicolor and Trichoderma harzianum and the Arbuscular mycorrhizal fungi Glomus deserticola and G. claroideum to arsenic tolerance of Eucalyptus globulus. Bioresource Technology. 2009; 100(24):6250–7. PMid: 19648001. https://doi.org/10.1016/j. biortech.2009.07.010 DOI: https://doi.org/10.1016/j.biortech.2009.07.010

Ali AH, Usama R, El-Zayat S, El-Sayed MA. The role of the endophytic fungus, thermomyces lanuginosus on mitigation of heat stress to its host desert plant Cullen plicata. Biologia Futura. 2019; 70(1):1–7. PMid: 34554436. https://doi. org/10.1556/019.70.2019.01 DOI: https://doi.org/10.1556/019.70.2019.01

Vita PD, Taranto F. Durum wheat (Triticum turgidum sp. durum) breeding to meet the challenge of climate change. In Advances in plant breeding strategies: Cereals. Springer, Cham. 2019; 471- 524. https://doi.org/10.1007/978-3-030-23108-8_13 DOI: https://doi.org/10.1007/978-3-030-23108-8_13

Redman RS, Yong OK, Woodward CJDA, Greer C, Espino L, Doty SL, Rodriguez RJ. “Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: A strategy for mitigating impacts of climate change.” PLoS ONE. 2011; 6(7):e14823. PMid: 21750695 PMCid: PMC3130040. https://doi.org/10.1371/journal. pone.0014823 DOI: https://doi.org/10.1371/journal.pone.0014823

Xu FJ, Song SL, Ma CY, Zhang W, Sun K, Tang MJ, Xie XG, Fan KK, Dai CC. Endophytic fungus improves peanut drought resistance by reassembling the root-dwelling community of Arbuscular mycorrhizal fungi. Fungal Ecology. 2020; 48:100993. https://doi.org/10.1016/j.funeco.2020.100993 DOI: https://doi.org/10.1016/j.funeco.2020.100993

Vijayabharathi R, Arumugam S, Subramaniam G. A renaissance in plant growth-promoting and biocontrol agents by endophytes. In Microbial Inoculants in Sustainable Agricultural Productivity: Vol. 1: Research Perspectives. 2016. https://doi.org/10.1007/978- 81-322-2647-5_3

Singh PC, Shukla D, Touseef F, Nautiyal CS, Johri JK. Biological control of fusarium sp. NBRI-PMSF12 pathogenic to cultivated betelvine by Bacillus Sp. NBRI-W9, a Potential Biological Control Agent. Journal of Plant Growth Regulation. 2017; 36(1):106–17. https://doi.org/10.1007/s00344-016-9623-0 DOI: https://doi.org/10.1007/s00344-016-9623-0

Hardoim, PR, Hardoim CCP, van Overbeek LS, van Elsas JD. Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS ONE. 2012; 7(2):e30438. PMid: 22363438 PMCid: PMC3281832. https://doi.org/10.1371/journal.pone.0030438 DOI: https://doi.org/10.1371/journal.pone.0030438

Sgroy V, Fabricio C, Masciarelli O, Del Papa MF, Lagares A, Luna V. Isolation and characterization of endophytic Plant Growth- Promoting (PGPB) or Stress Homeostasis-Regulating (PSHB) Bacteria associated to the halophyte Prosopis strombulifera. Applied Microbiology and Biotechnology. 2009; 85(2):371–81. PMid: 19655138. https://doi.org/10.1007/s00253-009-2116-3 DOI: https://doi.org/10.1007/s00253-009-2116-3

Zhang YF, Lin YH, Zhao JC, Wen HZ, Qing YW, Meng Q, Xia FS. Characterization of lead-resistant and ACC deaminaseproducing endophytic bacteria and their potential in promoting lead accumulation of rape. Journal of Hazardous Materials. 2011; 186(2-3):1720–5. PMid: 21227577. https://doi.org/10.1016/j. jhazmat.2010.12.069 DOI: https://doi.org/10.1016/j.jhazmat.2010.12.069

Dudeja SS, Giri R, Saini R, Suneja-Madan P, Kothe E. Interaction of endophytic microbes with legumes. Journal of Basic Microbiology. 2012; 52(3):248–60. PMid: 21953403. https://doi. org/10.1002/jobm.201100063 DOI: https://doi.org/10.1002/jobm.201100063

Khan N, Ali S, Shahid M, Mustafa A, Sayyed RZ, Curá JA. Insights into the interactions among roots, rhizosphere and rhizobacteria for improving plant growth and tolerance to abiotic stresses: A review. Cells. 2021; 10(6):1551. PMid: 34205352 PMCid: PMC8234610. https://doi.org/10.3390/cells10061551 50. Jayakumar A, Padmakumar P, Nair IC, Radhakrishnan EK. Drought tolerant bacterial endophytes with potential plant probiotic effects from Ananas comosus. Biologia. 2020; 75(10):1769–78. https://doi.org/10.2478/s11756-020-00483-1 DOI: https://doi.org/10.2478/s11756-020-00483-1

Dasgupta MG, Burragoni S, Amrutha S, Muthupandi M, Parveen ABM, Sivakumar V, Ulaganathan, K. Diversity of bacterial endophyte in Eucalyptus clones and their implications in water stress tolerance. Microbiological Research. 2020; 241:126579. PMid:32861101 https://doi.org/10.1016/j.micres.2020.126579 DOI: https://doi.org/10.1016/j.micres.2020.126579

Ziarovská J, Medo J, Kyseľ M, Zamiešková L, Kačániová M. Endophytic bacterial microbiome diversity in early developmental stage plant tissues of wheat varieties. Plants. 2020; 9(2):266. PMid: 32085509 PMCid: PMC7076375. https://doi.org/10.3390/ plants9020266 DOI: https://doi.org/10.3390/plants9020266

Yang L, Schroder P, Vestergaard G, Schloter M, Radl V. Response of barley plants to drought might be associated with the recruiting of soil-borne endophytes. Microorganisms. 2020; 8(9):1414. PMid: 32937884 PMCid: PMC7565417. https://doi.org/10.3390/ microorganisms8091414 DOI: https://doi.org/10.3390/microorganisms8091414

Goswami M, Suresh DEKA. Plant growth-promoting rhizobacteria- alleviators of abiotic stresses in soil: A review. Pedosphere. 2020; 30(1):40–61. DOI: https://doi.org/10.1016/S1002-0160(19)60839-8

Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MAK. Stressinduced morphogenic responses: growing out of trouble? Trends in Plant Science. 2007; 12(3):98–105. PMid: 17287141. https:// doi.org/10.1016/j.tplants.2007.01.004 DOI: https://doi.org/10.1016/j.tplants.2007.01.004

Waqas, M, Khan AL, Kamran M, Hamayun M, Kang SM, Kim YH, Lee IJ. Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules. 2012; 17(9):10753–73. PMid: 22960869 PMCid: PMC6268353. https://doi.org/10.3390/molecules170910754 DOI: https://doi.org/10.3390/molecules170910754

Merzaeva OV, Shirokikh IG. The production of auxins by the endophytic bacteria of winter rye. Applied Biochemistry and Microbiology. 2010. https://doi.org/10.1134/S0003683810010072 DOI: https://doi.org/10.1134/S0003683810010072

Chandra D, Srivastava R, Glick BR, Sharma AK. Rhizobacteria producing ACC deaminase mitigate water-stress response in finger millet (Eleusine coracana (L.) Gaertn.). Biotech, 2020; 10(2):1–15. PMid: 32030334 PMCid: PMC6979641. https://doi. org/10.1007/s13205-019-2046-4 DOI: https://doi.org/10.1007/s13205-019-2046-4

Soni R, Sarita K. Yadav SK, Rajput AS. ACC-deaminase Producing Rhizobacteria: Prospects and application as stress busters for stressed agriculture. 2018; 161–75. https://doi.org/10.1007/978- 981-10-7146-1_9 DOI: https://doi.org/10.1007/978-981-10-7146-1_9

Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ. Mycorrhiza-induced resistance and priming of plant defenses. Journal of Chemical Ecology. 2012; 38:651–64. PMid: 22623151. https://doi.org/10.1007/s10886-012-0134-6 DOI: https://doi.org/10.1007/s10886-012-0134-6

Smirnoff N. Smallwood MF, Calvert CM, Bowles DJ, Eds. 1999. Plant responses to environmental stress. 224 Pp. Oxford: Bios Scientific Publishers. 2000£70 (Hardback). https://doi. org/10.1006/anbo.2000.1110 DOI: https://doi.org/10.1006/anbo.2000.1110

Torres, MS, White JF, Zhang X, Hinton DM, Bacon CW. Endophyte-mediated adjustments in host morphology and physiology and effects on host fitness traits in grasses. Fungal Ecology. 2012; 5(3):322–30. https://doi.org/10.1016/j.funeco.2011.05.006 DOI: https://doi.org/10.1016/j.funeco.2011.05.006

Kumar M, Sharma R, Jogawat A, Singh P, Dua M, Johri AK, Gill SS, et al. Piriformospora indica, a root endophytic fungus, enhances abiotic stress tolerance of the host plant. In Improving Crop Resistance to Abiotic Stress. 2012. https://doi. org/10.1002/9783527632930.ch24 DOI: https://doi.org/10.1002/9783527632930.ch24

Saddique, MAB, Ali Z, Khan AS, Rana IA, Shamsi IH. Inoculation with the endophyte piriformospora indica significantly affects mechanisms involved in osmotic stress in rice. Rice. 2018; 11:34. PMid: 29799607 PMCid: PMC5968016. https://doi.org/10.1186/ s12284-018-0226-1 DOI: https://doi.org/10.1186/s12284-018-0226-1

Helmut B, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G, Janeczko A, et al. Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytologist. 2008; 180(2):501–10. PMid: 18681935, https://doi.org/10.1111/j.1469-8137.2008.02583.x DOI: https://doi.org/10.1111/j.1469-8137.2008.02583.x

Hanhong B, Sicher RC, Kim MS, Kim SH, Strem MD, Melnick RL, Bailey BA. The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in theobroma cacao. Journal of Experimental Botany. 2009; 60(11):3279–95. PMid: 19564160 PMCid: PMC2718224. https://doi.org/10.1093/jxb/erp165 DOI: https://doi.org/10.1093/jxb/erp165

Xuemei L, Bu N, Li Y, Ma L, Xin S, Zhang L. Growth, photosynthesis and antioxidant responses of endophyte infected and non-infected rice under lead stress conditions. Journal of Hazardous Materials. 2012; 213-214:55–61. PMid: 22356744. https://doi.org/10.1016/j.jhazmat.2012.01.052 DOI: https://doi.org/10.1016/j.jhazmat.2012.01.052

Lastochkin O, Garshina D, Ivanov S, Yuldashev R, Khafizova R, Allagulova C, Fedorova K, Avalbaev A, Maslennikova D, Bosacchi M. Seed priming with endophytic Bacillus subtilis modulates physiological responses of two different Triticum aestivum L. Cultivars under drought stress. Plants. 2020; 9(12):1810. PMid: 33371269 PMCid: PMC7766295. https://doi.org/10.3390/ plants9121810 DOI: https://doi.org/10.3390/plants9121810

Bilal S, Shahzad R, Imran M, Jan R, Ki, KM, Lee IJ. Synergistic association of endophytic fungi enhances Glycine max L. resilience to combined abiotic stresses: Heavy metals, high temperature and drought stress. Industrial Crops and Products. 2020; 143:111931. DOI: https://doi.org/10.1016/j.indcrop.2019.111931

Raheem S, Khan AL, Bilal S, Asaf S, Lee IN. What is there in seeds? Vertically transmitted endophytic resources for sustainable improvement in plant growth. Frontiers in Plant Science. 2018. PMid: 29410675 PMCid: PMC5787091. https://doi. org/10.3389/fpls.2018.00024

Molina-Montenegro MA, Acuna-Rodríguez I.S., Torres-Díaz C, Gundel PE, Dreye, I. Antarctic root endophytes improve physiological performance and yield in crops under salt stress by enhanced energy production and Na+ sequestration. Scientific Reports. 2020; 10(1):1-10. PMid: 32242034 PMCid: PMC7118072. https://doi.org/10.1038/s41598-020-62544-4 DOI: https://doi.org/10.1038/s41598-020-62544-4

Liang L, Li L, Wang X, Zhu P, Wu H, Qi S. Plant growth-promoting endophyte Piriformospora indica alleviates salinity stress in Medicago truncatula. Plant Physiology and Biochemistry. 2017; 119:211–23. PMid: 28898746. https://doi.org/10.1016/j.plaphy. 2017.08.029 DOI: https://doi.org/10.1016/j.plaphy.2017.08.029

Ying M, Rajkumar M, Moreno A, Zhang C, Freitas H. Serpentine endophytic bacterium Pseudomonas azotoformans ASS1 accelerates phytoremediation of soil metals under drought stress. Chemosphere. 2017; 185:75–85. PMid: 28686889. https://doi. org/10.1016/j.chemosphere.2017.06.135 DOI: https://doi.org/10.1016/j.chemosphere.2017.06.135

Chen C, Kaiyun X, Hao L, Juanli C, Xihui S, Yao W, Lei Z. Pantoea Alhagi, a novel endophytic bacterium with ability to improve growth and drought tolerance in wheat. Scientific Reports. 2017; 7:41564. PMid: 28128318 PMCid: PMC5269684. https://doi. org/10.1038/srep41564 75. Fatemeh H, Mosaddeghi MR, Dexter AR. Effect of the fungus Piriformospora indica on physiological characteristics and root morphology of wheat under combined drought and mechanical stresses. Plant Physiology and Biochemistry. 2017; 118:107–20. PMid: 28624682. https://doi.org/10.1016/j.plaphy.2017.06.005 DOI: https://doi.org/10.1016/j.plaphy.2017.06.005

Muhammad I, Ali N, Jan G, Jan FG, Ur Rahman I, Iqbal A, Hamayun M. IAA producing fungal endophyte Penicillium roqueforti thom., enhances stress tolerance and nutrients uptake in wheat plants grown on heavy metal contaminated soils.PLoS ONE. 2018; 13(11): e0208150. PMid: 30496253 PMCid: PMC6264496. https://doi.org/10.1371/journal.pone.0208150 DOI: https://doi.org/10.1371/journal.pone.0208150

Yu Y, Teng Z, Mou Z, Lv Y, Li T, Chen S, Zhao D, Zhao Z. Melatonin confers heavy metal-induced tolerance by alleviating oxidative stress and reducing the heavy metal accumulation in Exophiala pisciphila, a Dark Septate Endophyte (DSE). BMC Microbiology. 2021; 21(1):1–11. DOI: https://doi.org/10.1186/s12866-021-02098-1

Somayeh E, Alikhani HA, Pourbabaei AA, Etesami H, Zadeh BM, Sarmadian F. Improved growth and nutrient acquisition of wheat genotypes in phosphorus deficient soils by plant growthpromoting rhizospheric and endophytic bacteria. Soil Science and Plant Nutrition. 2018; 64(6):719–27. https://doi.org/10.108 0/00380768.2018.1510284 DOI: https://doi.org/10.1080/00380768.2018.1510284

Hamayun IM, Hussain A, Iqbal A, Khan SA, Lee IJ. Endophytic fungus Aspergillus japonicus mediates host plant growth under normal and heat stress conditions. BioMed Research International. 2018; 2018: 7696831. PMid: 30627568 PMCid: PMC6304497. https://doi.org/10.1155/2018/7696831 80. Tiryaki D, İhsan A, Okkeş A. Psychrotolerant bacteria isolated from the leaf apoplast of cold-adapted wild plants improve the cold resistance of bean (Phaseolus vulgaris L.) under low temperature. Cryobiology. 2019; 86:111–9. PMid: 30419217. https:// doi.org/10.1016/j.cryobiol.2018.11.001.

Mohamad OAA, Liu YH, Li L, Ma JB, Huang Y, Gao L, Fang BZ, Wang S, El-Baz AF, Jiang HC, Li, WJ. Synergistic plant-microbe interactions between endophytic actinobacteria and their role in plant growth promotion and biological control of cotton under salt stress. Microorganisms. 2022; 10(5):867. PMid: 35630312 PMCid: PMC9143301. https://doi.org/10.3390/microorganisms10050867 DOI: https://doi.org/10.3390/microorganisms10050867

Zhou L, Li C, White JF, Johnson RD. Synergism between calcium nitrate applications and fungal endophytes to increase sugar concentration in Festuca sinensis under cold stress. Peer J. 2021; 9:e10568. PMid: 35070512 PMCid: PMC8759379. https://doi. org/10.7717/peerj.10568 DOI: https://doi.org/10.7717/peerj.10568

MacIá-Vicente JG, Rosso LC, Ciancio A, Jansson HB, Lopez- Llorca LV. Colonisation of barley roots by Endophytic Fusarium equiseti and Pochonia chlamydosporia: Effects on plant growth and disease. Annals of Applied Biology. 2009; 155(3):391–401. https://doi.org/10.1111/j.1744-7348.2009.00352.x. DOI: https://doi.org/10.1111/j.1744-7348.2009.00352.x

Morales-Cedeño LR, del Carmen Orozco-Mosqueda M, Loeza- Lara PD, Parra-Cota FI, de Los Santos-Villalobos S, Santoyo G. Plant growth-promoting bacterial endophytes as biocontrol agents of pre-and post-harvest diseases: Fundamentals, methods of application and future perspectives. Microbiological Research. 2020; 242:126612. PMid: 33059112. https://doi.org/10.1016/j. micres.2020.126612 DOI: https://doi.org/10.1016/j.micres.2020.126612

Trivedi G, Patel P, Saraf M. Synergistic effect of endophytic selenobacteria on biofortification and growth of Glycine max under drought stress. South African Journal of Botany. 2020; 134:27– 35. https://doi.org/10.1016/j.sajb.2019.10.001 DOI: https://doi.org/10.1016/j.sajb.2019.10.001

Jaber LR, Enkerli J. Fungal entomopathogens as endophytes: Can they promote plant growth? Biocontrol Science and Technology. 2017; 27(1):28–41. https://doi.org/10.1080/09583157.2016. 1243227 DOI: https://doi.org/10.1080/09583157.2016.1243227

Jaber LR, Araj SE. Interactions among endophytic fungal entomopathogens (Ascomycota:Hypocreales), the green peach aphid myzus persicae sulzer (Homoptera:Aphididae) and the Aphid Endoparasitoid Aphidius Colemani Viereck (Hymenoptera:Braconidae). Biological Control. 2018; 116:53– 61. https://doi.org/10.1016/j.biocontrol.2017.04.005 DOI: https://doi.org/10.1016/j.biocontrol.2017.04.005

Kushwaha P, Kashyap PL, Kuppusamy P, Srivastava AK, Tiwari RK. Functional characterization of endophytic bacilli from pearl millet (Pennisetum glaucum) and their possible role in multiple stress tolerance. Plant Biosystems. 2019; 154(4):503–14. https:// doi.org/10.1080/11263504.2019.1651773 DOI: https://doi.org/10.1080/11263504.2019.1651773

Jaber LR, Salem NM. Endophytic colonisation of squash by the fungal entomopathogen Beauveria bassiana (Ascomycota:Hypocreales) for managing zucchini yellow mosaic virus in cucurbits. Biocontrol Science and Technology. 2014; 224(10):1096–109. https://doi.org/10.1080/09583157.2014.9233 79 DOI: https://doi.org/10.1080/09583157.2014.923379

Flonc B, Barberchec, M, Ahmad, I. Observations on the Relationships between Endophytic Metarhizium robertsii, Spodoptera frugiperda (Lepidoptera:Noctuidae) and Maize. Pathogens. 2021; 10(6):713. PMid: 34200234 PMCid: PMC8230249.https://doi.org/10.3390/pathogens10060713 DOI: https://doi.org/10.3390/pathogens10060713

Passari AK, Upadhyaya K, Singh G, Abdel-Azeem AM, Thankappan S, Uthandi S, Singh BP. Enhancement of disease resistance, growth potential and photosynthesis in tomato (Solanum lycopersicum) by inoculation with an endophytic actinobacterium, Streptomyces thermocarboxydus strain BPSAC147. PloS one. 2019; 14(7):e0219014. PMid: 31269087 PMCid: PMC6608948. https://doi.org/10.1371/journal.pone.0219014 DOI: https://doi.org/10.1371/journal.pone.0219014

Greenfield M, Gómez-Jiménez MI, Ortiz V, Vega FE, Kramer M, Parsa S. Beauveria bassiana and metarhizium anisopliae endophytically colonize cassava roots following soil drench inoculation. Biological Control. 2016; 95:40–8. PMid: 27103778 PMCid: PMC4825668. https://doi.org/10.1016/j.biocontrol. 2016.01.002 DOI: https://doi.org/10.1016/j.biocontrol.2016.01.002

Wei QY, Li YY, Xu C, Wu YX, Zhang YR, Liu H. Endophytic colonization by Beauveria bassiana increases the resistance of tomatoes against Bemisia tabaci. Arthropod-Plant Interactions. 2020; 14(3):289–300. https://doi.org/10.1007/s11829-020- 09746-9 DOI: https://doi.org/10.1007/s11829-020-09746-9

Rondot Y, Reineke A. Endophytic Beauveria bassiana in grapevine vitis vinifera (L.) reduces infestation with piercingsucking insects. Biological Control. 2018; 116:82–9. https://doi. org/10.1016/j.biocontrol.2016.10.006 DOI: https://doi.org/10.1016/j.biocontrol.2016.10.006

Wang GF, Meng JF, Tian T, Xiao XQ, Zhang B, Xiao YN. Endophytic Bacillus velezensis strain B‐36 is a potential biocontrol agent against lotus rot caused by Fusarium oxysporum. Journal of Applied Microbiology. 2020; 128(4):1153–62. PMid: 31808212 PMCid: PMC7079251. https://doi.org/10.1111/jam.14542 DOI: https://doi.org/10.1111/jam.14542

Akello J, Thomas D, Clifford SG, Coyne D, Nakavuma J, Paparu P. Beauveria bassiana (Balsamo) Vuillemin as an Endophyte in tissue culture banana (Musa Spp.). Journal of Invertebrate Pathology. 2007; 96(1):34–42. PMid: 17391694. https://doi. org/10.1016/j.jip.2007.02.004 DOI: https://doi.org/10.1016/j.jip.2007.02.004

Qayyum MA, Waqas W, Muhammad JA, Shahbaz TS, Dunlap CA. Infection of Helicoverpa armigera by endophytic Beauveria bassiana colonizing tomato plants. Biological Control. 2015; 90:200–7. https://doi.org/10.1016/j.biocontrol.2015.04.005 DOI: https://doi.org/10.1016/j.biocontrol.2015.04.005

Allegrucci N, Velazquez M., Russo ML, Vianna MF, Abarca C, Scorsetti AC. Establishment of the entomopathogenic fungus Beauveria bassiana as an endophyte in Capsicum annuum and its effects on the aphid pest Myzus persicae (Homoptera:Aphididae). Revista de Biología Tropical. 2020; 68(4):1084–94. https://doi. org/10.15517/rbt.v68i4.41218 DOI: https://doi.org/10.15517/rbt.v68i4.41218

Muvea AM, Meyhofer R, Subramanian S, Poehling HM, Ekesi S, Maniania NK. Colonization of onions by endophytic fungi and their impacts on the biology of Thrips tabaci. PLoS ONE. 2014; 9(9):e108242. PMid: 25254657 PMCid: PMC4177896. https:// doi.org/10.1371/journal.pone.0108242 DOI: https://doi.org/10.1371/journal.pone.0108242

Win KT, Fukuyo T, Keiki O, Yoshinari Ohwaki Y. The ACC deaminase expressing endophyte pseudomonas spp. enhances NaCl stress tolerance by reducing stress-related ethylene production, resulting in improved growth, photosynthetic performance and ionic balance in tomato plants. Plant Physiology and Biochemistry. 2018; 127:599–607. PMid: 29730579. https://doi. org/10.1016/j.plaphy.2018.04.038 DOI: https://doi.org/10.1016/j.plaphy.2018.04.038

Jaber LR. Grapevine leaf tissue colonization by the fungal entomopathogen Beauveria bassiana L. and its effect against downy mildew. BioControl. 2015; 60(1):103–12. https://doi.org/10.1007/ s10526-014-9618-3 DOI: https://doi.org/10.1007/s10526-014-9618-3

Tefera T, Vidal S. Effect of inoculation method and plant growth medium on endophytic colonization of sorghum by the entomopathogenic fungus Beauveria bassiana. BioControl. 2009; 54:663–9. https://doi.org/10.1007/s10526-009-9216-y DOI: https://doi.org/10.1007/s10526-009-9216-y

Russo ML, Pelizza SA, Cabello MN, Stenglein SA, Scorsetti AC. Endophytic colonisation of tobacco, corn, wheat and soybeans by the fungal entomopathogen Beauveria bassiana (Ascomycota, Hypocreales). Biocontrol Science and Technology. 2015; 25(4):475–80. https://doi.org/10.1080/09583157.2014.982511 DOI: https://doi.org/10.1080/09583157.2014.982511

Jin M, Yang C, Wei L, Cui L, Osei R, Cai F, Ma T, Wang Y. Transcriptome analysis of Stipa purpurea interacted with endophytic Bacillus subtilis in response to temperature and ultraviolet stress. Plant Growth Regulation. 2022 Jun; 22:1–4. https://doi. org/10.1007/s10725-022-00849-2 DOI: https://doi.org/10.1007/s10725-022-00849-2

Zhang JX, Chen ZT, Meng XL, Mu GY, Hu WB, Zhao J, Nie GX. Gene cloning, expression, and characterization of a novel β-Mannanase from the Endophyte Paenibacillus Sp. CH-3. Biotechnology and Applied Biochemistry. 2017; 64(4):471–81. PMid: 27222362. https://doi.org/10.1002/bab.1510 DOI: https://doi.org/10.1002/bab.1510

Pamphile JA, da Rocha CLMSC, Azevedo JL. Co-transformation of a tropical maize endophytic isolate of Fusarium verticillioides (Synonym F. Moniliforme) with GusA and Nia Genes. Genetics and Molecular Biology. 2004; 27:253–8. https://doi.org/10.1590/ S1415-47572004000200021 DOI: https://doi.org/10.1590/S1415-47572004000200021

Sawsan Abd E, Abdel Razik ES, Al-Surhanee AA, Al-Sarraj F, Daigham GE, Mahfouz AY. Enhanced Production, Cloning, and Expression of a Xylanase Gene from Endophytic Fungal Strain Trichoderma harzianum kj831197.1: Unveiling the In Vitro Anti- Fungal Activity against Phytopathogenic Fungi. Journal of Fungi. 2022: 8(5):447.