Harnessing the potential of endophytes: Sustainable solutions for enhancing forage crop resilience and soil fertility

Asma Mahjoub; Wiem Mnafgui; Nourhene Maiza; Nour Ressaissi; Ndiko Ludidi; Mounawer Badri

doi:10.56027/JOASD.232023

Authors

Asma Mahjoub
Wiem Mnafgui
Nourhene Maiza
Nour Ressaissi
Ndiko Ludidi
Mounawer Badri

DOI:

https://doi.org/10.56027/JOASD.232023

Keywords:

Abiotic and biotic stresses, endophytic bacteria, fodder crops, PGP

Abstract

Environmental changes pose significant challenges to sustainable agriculture, adversely affecting crop production and soil fertility. Factors such as drought, salinity, pathogens, and soil type exert their influence on the behavior of fodder crops by altering their morphological, biochemical, and molecular mechanisms, ultimately leading to reduced yields and productivity. Consequently, there is a pressing need to develop mitigation strategies aimed at enhancing the tolerance of forage crops to both biotic and abiotic stresses, addressing a critical challenge in sustaining their growth.

In recent times, the use of biofertilizers has emerged as an environmentally friendly alternative to chemical fertilizers, holding promise for sustainable horticultural, agricultural, and forestry production systems. Notably, endophytic microorganisms play a pivotal role in promoting plant growth through direct or indirect mechanisms. Additionally, endophytic bacteria actively regulate gene expression responsible for the production of antioxidant enzymes, various phytohormones, siderophores, and ROS scavenging enzymes, all of which contribute to supporting the growth of host plants even in extreme environments. Consequently, there is a growing focus on understanding and validating the mechanisms through which beneficial plant endophytes interact to combat both biotic and abiotic stresses.

This review emphasizes the potential of endophytes as biofertilizers, biocontrol agents, and contributors to the mitigation of abiotic and biotic stresses, all of which play crucial roles in maintaining the development of forage crops and soil fertility.

References

Assuero, S.G., Matthew, C., Kemp, P.D., Latch, G.C.M., Barker, D.J., & Haslett, S.J. (2000). Morphological and physiological effects of water deficit and endophyte infection on contrasting tall fescue cultivars. New Zealand Journal of Agricultural Research 43, 49–61.

https://doi.org/10.1080/0028823 3.2000.9513408.

Bambharolia, R.P., Selvakumar, G., Sharma, R., Yadav, S. K., Gupta, A., Yadav, S. K., & Sahay, H. (2020). Endophytic microbes: a novel source for plant growth-promoting traits. Microbial endophytes. Prospects for Sustainable Agriculture 161-184. https://doi.org/ 10.1016/B978-0-12-818772-3.00007-2.

Baltruschat, H., Fodor, J., Harrach, B. D., Niemczyk, E., Barna, B., Gullner, G., Janeczko, A., Kogel, K.H., Schäfer, P., Schwarczinger, I., Zuccaro, A., & Skoczowski, A. (2008). Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytologist 180(2), 501-510. https://doi.org/10.1111/j.1469-8137.2008.02583.x.

Chaudhary, P., & Sharma, A. (2019). Response of nanogypsum on the performance of plant growth promotory bacteria recovered from nanocompound infested agriculture field. Environment and Ecology 37, 363–372. http://www.environmentandecology.com.

Chiellini, C., Maida, I., Emiliani, G., Mengoni, A., Mocali, S., Fabiani, A., et al. (2014). Endophytic and rhizospheric bacterial communities isolated from the medicinal plants Echinacea purpurea and Echinacea angustifolia. International Microbiology 17, 165–174. https://doi.org /10.2436/20.1501.01.219.

Chowdhary, K., & Kaushik, N. (2015). Fungal endophyte diversity and bioactivity in the

Indian medicinal plant Ocimum sanctum Linn. PLoS ONE 10(11): e0141444. https://doi.org/10.1371/journal.pone.0141444.

Clarridge, J.E. (2004) Impact of 16S rRNA gene sequence analysis for identi-

fication of bacteria on clinical microbiology and infectious diseases.

Clinical Microbiology Review 17, 840–62.

Compant, S., Duffy, B., Nowak J, Cl, C & Barka, E.A. (2005a). Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Applied and Environmental Microbiology 71, 4951–4959. https://doi.org/10.1128/AEM.71.9.4951-4959.2005.

Chen, Z., Jin, Y., Yao, X., Chen,T., Wei;X., Li,C., White, J. F.,& Nan, Z. (2020). Fungal Endophyte Improves Survival of Lolium perennein Low Fertility Soils by Increasing Root Growth, Metabolic Activity and Absorption of Nutrients. Plant Soil 452, 185–206.https://doi.org/10.1007/s11104-020-04556-7.

Chen, X., Li, M., Liu, C., Ma, J., Wang, X., Wu, B., & Jiang, X. (2020). Exploration of Endophytes from Alfalfa (Medicago sativa L.) as Biocontrol Agents. Genetic Genomics 1 (1), 2-8. http://dx.doi.org/10.31487/j.GG.2020.01.01.

Croce, P., De Luca, A., Mocioni, M., Volterrani, M., & Beard, J.B. (2001). Warm-season turfgrass species and cultivar characterizations for a Mediterranean climate. The International Turfgrass Society Research Journal 9, 855–859. https://www.researchgate.net/publication/285806183.

Drancourt, D., Berger, P., & Raoult, D. (2004). Systematic 16S rRNA gene sequenc-

ing of atypical clinical isolates identified 27 new bacterial species as-

sociated with humans. Journal of Clinical Microbiology 42, 2197–202.

Enazy, A.A., Barakah, F., Aloud, S., & Usman, A., (2018). Effect of phosphogypsum application and bacteria co-inoculation on biochemical properties and nutrient availability to maize plants in a saline soil. Archives of Agronomy and Soil Science 64(10). https://doi.org/10.1080/03650340.2018.1437909.

Egamberdieva, D., Wirth, S.J., Shurigin, V.V., Hashem, A., & Abd_Allah, E.F. (2017). Endophytic bacteria improve plant growth, symbiotic performance of chickpea (Cicer arietinum L.) and induce suppression of root rot caused by Fusarium solani under salt stress. Frontiers in Microbiology 8, 1887. https://doi.org/10.3389/fmicb.2017.01887.

FAO (2020). Last updated on November 22, 13:50

Glick, B.R. (2012). Plant growth-promoting bacteria: mechanisms and applications. Scientifica 15. https://doi.org/10.6064/2012/963401

Garcia‑Latorre, C., Rodrigo, S., Santamaria, O. (2021). Effect of fungal endophytes on plant growth and nutrient uptake in Trifolium subterraneum and Poa pratensis as affected by plant host specificity. Mycological Progress 20, 1217–1231. https://doi.org/10.1007/s11557-021-01732-6

Hodge, A. (2004). The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162, 9–24. https://doi.org/10.1111/j.1469-8137.2004.01015.x.Hall, S.L., McCulley, R.L., Barney, R.J., & Phillips, T.D. (2014). Does fungal endophyte infection improve tall fescue’s growth response to fire and water limitation? PLoS One 9, e86904. https://doi.org/10.1371/journal.pone.0086904

Hahn, H., McManus, M. T., Warnstorff, K., Monahan, B. J., Young, C. A., Davies, E., Tapper, B. A., Scott, B. (2008). Notyphodium fungal endophytes confer physiological protection to perennial ryegrass (Lolium perenne L.) subjected to a water deficit. Environmental and Experimental Botany 63 (1–3), 183-199. https://doi.org/10.1016/j.envexpbot.2007.10.021

Irankhah, S., Ganjeali, A., Mashreghi, M., & Lari, Z., (2021). Mixed inoculum of rhizobacteria and arbuscular mycorrhizal fungus enhance diosgenin contain and phosphorus uptake in fenugreek under drought stress. Rhizosphere 18, 100338. https://doi.org/10.1016/j.rhisph.2021.100338

Ignatova, L., Kistaubayeva, A., Brazhnikova, Y., Omirbekova, A., Mukasheva, T., Savitskaya, I., Karpenyuk,T., Goncharova, A., Egamberdieva,D., Sokolov, A. (2021). Characterization of cadmium-tolerant endophytic fungi isolated from soybean (Glycine max) and barley (Hordeum vulgare). Heliyon 7. e08240

https://doi.org/10.1016/j.heliyon.2021.e08240.

Kandel, S. L., Firrincieli, A., Joubert, P. M., Okubara, P.A., Leston, N D., & McGeorge, K.M. (2017a). An in vitro study of bio-control and plant growth promotion potential of salicaceae endophytes. Frontiers in Microbiology 8, 386 https://doi.org/10.3389/fmicb.2017.00386.

Kang, S.-M., Radhakrishnan, R., Khan, A.L., Kim, M.J., Park, J.M., Kim, B.R., Shin, D.H., Lee, I.J. (2014). Gibberellin secreting rhizobacterium, Pseudomonas putida H-2-3 modulates the hormonal and stress physiology of soybean to improve the plant growth under saline and drought conditions. Plant Physiology and Biochemistry 84, 115–124 https://doi.org/10.1016/j.plaphy.2014.09.001

Khalil, M. N., Tahir, M. N., Abbas, Q., Hussain, M. A., Ali, A., Akram, W., & Afzal, M. (2021). Endophytes: potential growth-promoting agents for sustainable agriculture. Journal of Plant Growth Regulation 40(2), 541-557. 1 https://doi.org/ 0.1007/s00344-020-10147-0.

Khan, A.L., Hamayun, M., Kim, Y.H., Kang, S.M., & Lee, I.J. (2011). Ameliorative symbiosis of endophyte (Penicillium funiculosum LHL06) under salt stress elevated plant growth of Glycine max L. Plant Physiology and Biochemistry, 49(8), 852-861. https://doi.org/10.1016/j.plaphy.2011.03.005.

Khalaf, E.M., & Raizada, M.N. (2018). Bacterial seed endophytes of domesticated cucurbits antagonize fungal and oomycete pathogens including powdery mildew. Frontiers in Microbiology 9, 42. https://doi.org/ 10.3389/fmicb.2018.00042

Larran, S., Monaco, C., & Alippi, H.E. (2001). Endophytic fungi in leaves of Lycopersicon esculentum Mill. The World Journal of Microbiology & Biotechnology Biotechnol 17, 181–184. https://doi.org/10.1023/A:1016670000288.

Li, L., Chang, M., Zhang, Y., & Wang, X. (2019). Diversity and potential biotechnological applications of endophytic bacteria isolated from medicinal plants. Symbiosis 77(3), 171-180.https://doi.org/10.1007/s13199-019-00602-2.

Maqbool, S., Amna, A., Mehmood, S., Suhaib, M., Sultan, T., & Munis, M.F.H. (2021). Interaction of acc deaminase and antioxidant enzymes to induce drought tolerance in Enterobacter cloacae 2wc2 inoculated maize genotypes. Pakistan Journal of Botany 53, 893–903. https://doi.org/ 10.30848/PJB2021-3(28).

Mei, C., & Flinn, B. S. (2010). The use of beneficial microbial endophytes for plant

biomass and stress tolerance improvement. Recent Patents on Biotechnology 4(1), 81-95. https://doi.org/10.2174/187220810790069523.

Mercado-Blanco, J., Rodrıguez-Jurado, D., Hervas, A.M., & Jimenez-Dıaz, R. (2004). Suppression of Verticillium wilt in olive planting stocks by

root-associated fluorescent Pseudomonas spp. Biological Control 30, 474–486.

https://doi.org/10.1016/j.biocontrol.2004.02.002.

Mahadik, S., & Kumudini, B.S. (2020). Enhancement of salinity stress tolerance and plant growth in finger millet using fluorescent pseudomonads. Rhizosphere 15, 100226. https://doi.org/10.1016/j.rhisph.2020.100226.

Mousa, W.K., Schwan, A.L. & Raizada, M.N. (2016). Characterization of Antifungal Natural Products isolated from endophyticfungi of Finger Millet (Eleusine coracana). Molecules 21, 1171. https://doi.org/10.3390/molecules21091171.

Noori, F., Etesami, H., Zarini, Hamid, N.N., Khoshkholgh-Sima, A., Salekdeh, G. H., & Alishahi, F. (2018). Mining alfalfa (Medicago sativa L.) nodules for salinity tolerant non-rhizobial bacteria to improve growth of alfalfa under salinity stress. Ecotoxicology and Environmental Safety 162(30), 129-138. https://doi.org/10.1016/j.ecoenv.2018.06.092

Nagabhyru, P., Dinkins, R.D., Wood, C.L., Charles, Bacon, W., & Schardl. C.L. (2013). Tall fescue endophyte effects on tolerance to water-deficit stress. Plant Biology 13:127. http://www.biomedcentral.com/1471-2229/13/127.

Naseem, H., & Bano, A. (2014). Role of plant growth-promoting rhizobacteria and their exopolysaccharide in drought tolerance of maize. Journal of Plant Interactions 9 (1), 689–701. http://dx.doi.org/10.1080/17429145.2014.

Pereira, E., de Aldana, B.R.V., San Emeterio, L., & Zabalgogeazcoa, I. (2019). A Survey of Culturable Fungal Endophytes fromFestuca rubra subsp. pruinosa, a Grass from Marine Cliffs, Reveals a Core Microbiome. Frontiers in Microbiology 9 - https://doi.org/10.3389/fmicb.2018.03321.

Rodríguez, H., & Fraga, R. (1999). Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnology advances 17(4-5), 319-339. https://doi.org/10.1016/S0734-9750(99)00014-2.

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

Ren, A.Z., GAO, Y.B., & Zhou F., (2007). Response of Neotyphodium lolii-infected perennial ryegrass to phosphorus deficiency. Plant soil environ 53(3), 113–119.

https://doi.org/10.17221/2225-PSE

Slama, H.B., Cherif-Silini, H., Chenari Bouket, A., Qader, M., Silini, A., Yahiaoui, B., Alenezi, F.N., Luptakova, L., Triki, M.A., Vallat, A., Oszako, T., Rateb, M.E., & Belbahri, L. (2019). Screening for Fusarium antagonistic bacteria from contrasting niches designated the endophyte Bacillus halotolerans as plant warden against Fusarium. Frontiers in Microbiology 9, 32-36. https://doi.org/10.3389/fmicb.2018.03236.

Sharma, A., Kaushik, N., Sharma, A., Bajaj, A., Rasane, M., Shouche, Y.S., Marzouk, T., & Djébali, N. (2021). Screening of tomato seed bacterial endophytes for antifungal activity reveals lipopeptide producing Bacillus siamensis strain NKIT9 as a potential bio-control agent. Frontiers in Microbiology 12, 1228.

Timmusk, S., Behers, L., Muthoni, J., Muraya, A., & Aronsson. A.C. (2017). Perspectives and Challenges of Microbial Application for Crop Improvement. Frontiers in Plant Science 8, 49. https://doi.org/10.3389/fpls.2017.00049

Tyagi, J., Varma, A., & Pudake, R.N. (2017). Evaluation of comparative effects of arbuscular mycorrhiza (Rhizophagus intraradices) and endophyte (Piriformospora indica) association with finger millet (Eleusine coracana) under drought stress. European Journal of Soil Biology 81, 1-10. https://doi.org/10.1016/j.ejsobi.2017.05.007

Umapathi, M., Chandrasekhar, C.N., Senthil, A., Kalaiselvi, T., Santhi, R., & Ravikesavan, R. (2021). Enhancement of sorghum (Sorghumbicolor (L.) Moench) growth performance by plant-growth promotin endophytes. International Journal of Ecology and Environmental Sciences 3(1), 388-394. https://www.researchgate.net/publication/349881551

Venuprasad, R., Lafitte, H.R., & Atlin, G.N. (2007). Response to direct selection for grain yield under drought stress in rice. Crop Science. 47, 285–293. https://doi.org/10.2135/cropsci2006.03.0181

Vardharajula, S., Ali, S. Z., Grover, M., Reddy, G., & Bandi, V. (2011). Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes, and antioxidant status of maize under drought stress. Journal of Plant Interactions 6(1) 1742-9145 https://doi.org/10.1080/17429145.2010.

Vurukonda, S.S., Vardharajula, S., Shrivastava, M., & SkZ, A. (2016). Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiological Research 184, 13–24. https://doi.org/10.1016/j.micres.2015.12.003.

Waller, F., Achatz, B., Baltruschat, H., Fodor, J., Becker, K., Fischer, M., Heier, T., Hückelhoven, R., Neumann, C., Wettstein, D.V., 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 Sciences 102(38), 13386-13391. https://doi.org/10.1073/pnas.0504423102.

Wang, Y., Luo, Y., Tian, P., Peng, Hao. & Feng, J. (2021). Preliminary evaluation of the of Festuca sinensis infected by Epichloë sinensis. Journal of Phytopatology. 169, (10).623-629. https://doi.org/10.1111/jph.13033.

Yang, R., Liu, P., & Ye, W. (2017). Illumina-based analysis of endophytic bacterial

diversity of tree peony (Paeonia Sect. Moutan) roots and leaves. Brazilian Journal of Microbiology 48, 695–705. https://doi /10.1016/j.bjm.2017.02.009.

Yarte, M. E., Gismondi, M. I., Llorente, B. E., and Larraburu, E. E. (2020). Isolation of endophytic bacteria from the medicinal, forestal and ornamental tree Handroanthus impetiginosus. Environmental Technology 43(8), 1129-1139. https://doi.org/10.1080/09593330.2020.1818833.

Żurek, G., Wiewióra, B., Rybka, K., & Prokopiuk, K. (2022). Different response of perennial ryegrass—Epichloë endophyte symbiota to the elevated concentration of heavy metals in soil. Journal of Applied Genetics 63, 47–59. https://doi.org/10.1007/s13353-021-00661-0.