Microbial Contribution to the Sustainability of Forest Ecosystems: Mechanisms of Stress Mitigation and Growth Promotion

Authors

DOI:

https://doi.org/10.61326/silvaworld.v5i2.508

Keywords:

Abiotic stress tolerance, Climate change, Forest microbiome, Mycorrhizal fungi, Phytohormones, Sustainable forest management

Abstract

Global climate change is intensifying drought, salinity, extreme temperatures, nutrient limitation, and soil degradation, thereby threatening forest regeneration, seedling establishment, and ecosystem functioning. This review synthesizes current knowledge on the contribution of forest-associated microorganisms to tree growth, resource acquisition, and stress tolerance in both coniferous and broadleaved forest species. It covers plant growth-promoting rhizobacteria, endophytic bacteria and fungi, arbuscular mycorrhizal fungi, ectomycorrhizal fungi, and microbial consortia associated with diverse forest trees, including species of Pinus, Picea, Cedrus, Pseudotsuga, Thuja, Quercus, Fagus, Populus, Betula, and Acacia. Across nursery, greenhouse, field, reciprocal-soil, and climate-gradient studies, beneficial microbial associations have been linked to improved germination, root development, nutrient and water acquisition, photosynthetic performance, seedling survival, and biomass accumulation under drought, salinity, heat, cold, nutrient deficiency, and degraded-soil conditions. These effects involve enhanced root development, nutrient mobilization, phytohormone regulation, ACC deaminase activity, antioxidant defense, osmotic adjustment, and modification of plant–soil feedbacks. However, microbial effects are not universally positive and vary according to tree genotype, microbial identity, inoculum origin, soil properties, stress intensity, and biotic interactions. Microbial consortia and climate-matched native communities may provide complementary functions, although their persistence and performance under field conditions remain variable. Overall, microbiome-informed nursery production, afforestation, and ecological restoration represent promising complementary strategies for improving forest resilience. Further multi-year field studies are needed to determine whether these benefits translate into sustained forest ecosystem functioning and climate resilience.

References

Aalipour, H., Nikbakht, A., Etemadi, N., & MacDonald, J. E. (2021). Co-inoculation of Arizona cypress with mycorrhizae and rhizobacteria affects biomass, nutrient status, water-use efficiency, and glomalin-related soil protein concentration. Urban Forestry & Urban Greening, 60, 127050. https://doi.org/10.1016/j.ufug.2021.127050

Aalipour, H., Nikbakht, A., Etemadi, N., Rejali, F., & Soleimani, M. (2020). Biochemical response and interactions between arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria during establishment and stimulating growth of Arizona cypress (Cupressus arizonica G.) under drought stress. Scientia Horticulturae, 261, 108923. https://doi.org/10.1016/j.scienta.2019.108923

Abarna, R., Jinisha Blessie, J. P., Nandana, M. S., Drisya, K. A., Chitra, N., & Anith, K. N. (2025). Unlocking the microbiome-mediated mechanism of stress resilience in plants. Plant Science Today, 12(4), 1-19. https://doi.org/10.14719/pst.9052

Abdelaal, K., AlKahtani, M., Attia, K., Hafez, Y., Király, L., & Künstler, A. (2021). The role of plant growth-promoting bacteria in alleviating the adverse effects of drought on plants. Biology, 10(6), 520. https://doi.org/10.3390/biology10060520

Abdelaal, K. A. A., Attia, K. A., Alamery, S. F., El-Afry, M. M., Ghazy, A. I., Tantawy, D. S., Al-Doss, A. A., El-Shawy, E. S. E., Abu-Elsaoud, A. M., & Hafez, Y. M. (2020a). Exogenous application of proline and salicylic acid can mitigate the injurious impacts of drought stress on barley plants associated with physiological and histological characters. Sustainability, 12(5), 1736. https://doi.org/10.3390/su12051736

Abdelaal, K. A., El-Shawy, E. A., Hafez, Y. M., Abdel-Dayem, S. M., Chidya, R. C. G., Saneoka, H., & El Sabagh, A. (2020b). Nano-Silver and non-traditional compounds mitigate the adverse effects of net blotch disease of barley in correlation with up-regulation of antioxidant enzymes. Pakistan Journal of Botany, 52(3), 1065-1072. https://doi.org/10.30848/PJB2020-3(13)

Abdelaal, K. A., Hafez, Y. M., El-Afry, M. M., Tantawy, D. S., & Alshaal, T. (2018). Effect of some osmoregulators on photosynthesis, lipid peroxidation, antioxidative capacity, and productivity of barley (Hordeum vulgare L.) under water deficit stress. Environmental Science and Pollution Research, 25(30), 30199-30211. https://doi.org/10.1007/s11356-018-3023-x

Abou-Attia, F., & El-Aziz, A. (2007). Effect of Bio and Mineral fertilization on the main insect pests and some characters of sugar beet plants. Journal of Plant Protection and Pathology, 32(2), 1471-1485. https://doi.org/10.21608/jppp.2007.219428

Acharya, B. R., Gill, S. P., Kaundal, A., & Sandhu, D. (2024). Strategies for combating plant salinity stress: The potential of plant growth-promoting microorganisms. Frontiers in Plant Science, 15, 1406913. https://doi.org/10.3389/fpls.2024.1406913

Adeleke, B. S., Chaudhary, P., Ayilara, M. S., Ojo, F. M., Erinoso, S. M., Upadhayay, V. K., Adeyemo, A. I., & Akinola, S. A. (2024). Rhizosphere microbiomes mediating abiotic stress mitigation for improved plant nutrition. Ecologies, 5(3), 375-401. https://doi.org/10.3390/ecologies5030024

Aghai, M. M., Khan, Z., Joseph, M. R., Stoda, A. M., Sher, A. W., Ettl, G. J., & Doty, S. L. (2019). The effect of microbial endophyte consortia on Pseudotsuga menziesii and Thuja plicata survival, growth, and physiology across edaphic gradients. Frontiers in Microbiology, 10, 1353. https://doi.org/10.3389/fmicb.2019.01353

Ali, M., Gul, A., Gul, A., Hasan, H., Gul, S., Fareed, A., Nadeem, M., Siddique, R., Jan, S. U., & Jamil, M. (2020). Chapter 9 - Cellular mechanisms of drought tolerance in wheat. In M. Ozturk & A. Gul (Eds.), Climate change and food security with emphasis on wheat (pp. 155-167). Academic Press. https://doi.org/10.1016/B978-0-12-819527-7.00009-1

AlKahtani, M. D. F., Hafez, Y. M., Attia, K., Rashwan, E., Al Husnain, L., AlGwaiz, H. I. M., & Abdelaal, K. A. A. (2021a). Evaluation of silicon and proline application on the oxidative machinery in drought-stressed sugar beet. Antioxidants, 10(3), 398. https://doi.org/10.3390/antiox10030398

AlKahtani, M., Hafez, Y., Attia, K., Al-Ateeq, T., Ali, M. A., Hasanuzzaman, M., & Abdelaal, K. (2021b). Bacillus thuringiensis and silicon modulate antioxidant metabolism and improve the physiological traits to confer salt tolerance in lettuce. Plants, 10(5), 1025. https://doi.org/10.3390/plants10051025

Allsup, C. M., George, I., & Lankau, R. A. (2023). Shifting microbial communities can enhance tree tolerance to changing climates. Science, 380(6647), 835-840. https://doi.org/10.1126/science.adf2027

Alvarez, M., Huygens, D., Olivares, E., Saavedra, I., Alberdi, M., & Valenzuela, E. (2009). Ectomycorrhizal fungi enhance nitrogen and phosphorus nutrition of Nothofagus dombeyi under drought conditions by regulating assimilative enzyme activities. Physiologia Plantarum, 136(4), 426-436. https://doi.org/10.1111/j.1399-3054.2009.01237.x

Ashraf, M., & Foolad, M. R. (2007). Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany, 59(2), 206-216. https://doi.org/10.1016/j.envexpbot.2005.12.006

Atik, A. (2013). Effect of different concentrations of effective microorganisms (Baikal EM1) on the root collar diameter and height growth in the seedlings of Anatolian black pine [Pinus nigra Arnold subsp. pallasiana Lamb. (Holmboe)]. Journal of Food, Agriculture & Environment, 11(2), 1300-1304.

Ayan, S., Çalışkan, E., Özel, H. B., Yer Çelik, E. N., Gülseven, O., & Yılmaz, E. (2021). Etkili mikroorganizmaların tüplü Toros sediri (Cedrus libani A. Rich.) fidanlarının morfolojik özelliklerine etkisi. Bartın Orman Fakültesi Dergisi, 23(1), 294-305. https://doi.org/10.24011/barofd.893148 (In Turkish)

Ayan, S., Çalışkan, E., Özel, H. B., Yer Çelik, E. N., Yılmaz, E., Gülseven, O., & Akın, Ş. S. (2022). The influence of effective microorganisms on physiological characteristics of containerized Taurus cedar (Cedrus libani A. Rich.) seedlings. CERNE, 28, e103018. https://doi.org/10.1590/01047760202228013018

Azizi, S., Tabari, M., Abad, A. R. F. N., Ammer, C., Guidi, L., & Bader, M. K.-F. (2022). Soil inoculation with beneficial microbes buffers negative drought effects on biomass, nutrients, and water relations of common myrtle. Frontiers in Plant Science, 13, 892826. https://doi.org/10.3389/fpls.2022.892826

Bai, Y., Müller, D. B., Srinivas, G., Garrido-Oter, R., Potthoff, E., Rott, M., Dombrowski, N., Münch, P. C., Spaepen, S., Remus-Emsermann, M., Hüttel, B., McHardy, A. C., Vorholt, J. A., & Schulze-Lefert, P. (2015). Functional overlap of the Arabidopsis leaf and root microbiota. Nature, 528(7582), 364-369. https://doi.org/10.1038/nature16192

Bastas, K. K. (2021). Impacts of climate changes on plant-beneficial microorganism Interactions. Turkish Journal of Agriculture - Food Science and Technology, 9(sp), 2594-2603. https://doi.org/10.24925/turjaf.v9isp.2594-2603.4946

Bayar, E., & Deligöz, A. (2019). Cedrus libani ve Pinus nigra subsp. pallasiana ağaçlandırma alanında kurak dönemde ağaç-su ilişkisi değişimleri. Turkish Journal of Forestry, 20(4), 317-323. https://doi.org/10.18182/tjf.598303 (In Turkish)

Begum, N., Xiao, Y., Wang, L., Li, D., Irshad, A., & Zhao, T. (2023). Arbuscular mycorrhizal fungus Rhizophagus irregularis alleviates drought stress in soybean with overexpressing the GmSPL9d gene by promoting photosynthetic apparatus and regulating the antioxidant system. Microbiological Research, 273, 127398. https://doi.org/10.1016/j.micres.2023.127398

Berendsen, R. L., Pieterse, C. M., & Bakker, P. A. (2012). The rhizosphere microbiome and plant health. Trends in Plant Science, 17(8), 478-486. https://doi.org/10.1016/j.tplants.2012.04.001

Berg, G., Grube, M., Schloter, M., & Smalla, K. (2014). Unraveling the plant microbiome: Looking back and future perspectives. Frontiers in Microbiology, 5, 148. https://doi.org/10.3389/fmicb.2014.00148

Bettegowda, R. H., Nanjundappa, A., Revanna, A., Manchegowda, H. K., Ravi, J. E., & Bagyaraj, D. J. (2021). Selected microbial consortia promotes Dalbergia sissoo growth in the large-scale nursery and wastelands in a semi-arid region in India. Journal of Forest Research, 26(6), 448-454. https://doi.org/10.1080/13416979.2021.1955439

Bois, G., Bigras, F. J., Bertrand, A., Piché, Y., Fung, M. Y. P., & Khasa, D. P. (2006). Ectomycorrhizal fungi affect the physiological responses of Picea glauca and Pinus banksiana seedlings exposed to an NaCl gradient. Tree Physiology, 26(9), 1185-1196. https://doi.org/10.1093/treephys/26.9.1185

Bonfante, P., & Genre, A. (2010). Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nature Communications, 1(1), 48. https://doi.org/10.1038/ncomms1046

Brundrett, M. C., & Tedersoo, L. (2018). Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytologist, 220(4), 1108-1115. https://doi.org/10.1111/nph.14976

Bulgarelli, D., Schlaeppi, K., Spaepen, S., Ver Loren van Themaat, E., & Schulze-Lefert, P. (2013). Structure and functions of the bacterial microbiota of plants. Annual Review of Plant Biology, 64, 807-838. https://doi.org/10.1146/annurev-arplant-050312-120106

Çakmakçı, R. (2005). Bitki gelişimini teşvik eden rizobakterilerin tarımda kullanımı. Atatürk Üniversitesi Ziraat Fakültesi Dergisi, 36(1), 97-107. (In Turkish)

Çakmakçı, R., Dönmez, M. F., & Erdoğan, Ü. (2007). The effect of plant growth promoting rhizobacteria on barley seedling growth, nutrient uptake, some soil properties, and bacterial counts. Turkish Journal of Agriculture and Forestry, 31(3), 189-199.

Chahboub, H. G., Lamhamedi, M. S., & Abrous-Belbachir, O. (2021). Implications of ectomycorrhizal inoculation for drought stress tolerance of Atlas cedar (Cedrus atlantica) seedlings. New Zealand Journal of Forestry Science, 51, 7. https://doi.org/10.33494/nzjfs512021x131x

Chen, J., Zhang, H., Zhang, X., & Tang, M. (2020a). Arbuscular mycorrhizal symbiosis mitigates oxidative injury in black locust under salt stress through modulating antioxidant defence of the plant. Environmental and Experimental Botany, 175, 104034. https://doi.org/10.1016/j.envexpbot.2020.104034

Chen, W., Meng, P., Feng, H., & Wang, C. (2020b). Effects of arbuscular mycorrhizal fungi on growth and physiological performance of Catalpa bungei C.A.Mey. under drought stress. Forests, 11(10), 1117. https://doi.org/10.3390/f11101117

Chernyad’ev, I. I. (2005). Effect of water stress on the photosynthetic apparatus of plants and the protective role of cytokinins: A review. Applied Biochemistry and Microbiology, 41(2), 115-128. https://doi.org/10.1007/s10438-005-0021-9

Compant, S., Clément, C., & Sessitsch, A. (2010). Plant growth-promoting bacteria in the rhizo-and endosphere of plants: Their role, colonization, mechanisms involved and prospects for utilization. Soil Biology and Biochemistry, 42(5), 669-678. https://doi.org/10.1016/j.soilbio.2009.11.024

Cregger, M. A., Veach, A. M., Yang, Z. K., Crouch, M. J., Vilgalys, R., Tuskan, G. A., & Schadt, C. W. (2018). The Populus holobiont: Dissecting the effects of plant niches and genotype on the microbiome. Microbiome, 6(1), 31. https://doi.org/10.1186/s40168-018-0413-8

Crowe, J. H., & Crowe, L. M. (1992). Membrane integrity in anhydrobiotic organisms: Toward a mechanism for stabilizing dry cells. In G. N. Somero, C. B. Osmond & C. L. Bolis (Eds.), Water and life: Comparative analysis of water relationships at the organismic, cellular, and molecular levels (pp. 87-103). Springer. https://doi.org/10.1007/978-3-642-76682-4_7

Danzberger, J., Hikino, K., Landhäusser, S. M., Hesse, B. D., Meyer, S., Buegger, F., Weikl, F., Grams, T. E. E., & Pritsch, K. (2025). Drought acclimation of beech seedlings depends largely on their rooting patterns and less on the fungal communities in soils. Plant and Soil, 508(1), 49-70. https://doi.org/10.1007/s11104-024-06784-7

Das, K., & Roychoudhury, A. (2014). Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Frontiers in Environmental Science, 2, 53. https://doi.org/10.3389/fenvs.2014.00053

Deligöz, A. (2011). Seasonal changes in the physiological characteristics of Anatolian black pine and the effect on seedling quality. Turkish Journal of Agriculture and Forestry, 35(1), 23-30. https://doi.org/10.3906/tar-0908-343

Deligöz, A., & Cankara, F. G. (2020). Differences in physiological and biochemical responses to summer drought of Pinus nigra subsp. pallasiana and Pinus brutia in a natural mixed stand. Journal of Forestry Research, 31(5), 1479-1487. https://doi.org/10.1007/s11676-018-00876-8

Deligöz, A., & Gür, M. (2015). Morphological, physiological and biochemical responses to drought stress of stone pine (Pinus pinea L.) seedlings. Acta Physiologiae Plantarum, 37(11), 243. https://doi.org/10.1007/s11738-015-1998-1

Diagne, N., Ndour, M., Djighaly, P. I., Ngom, D., Ngom, M. C. N., Ndong, G., Svistoonoff, S., & Cherif-Silini, H. (2020). Effect of plant growth-promoting rhizobacteria (PGPR) and arbuscular mycorrhizal fungi (AMF) on salt stress tolerance of Casuarina obesa (Miq.). Frontiers in Sustainable Food Systems, 4, 601004. https://doi.org/10.3389/fsufs.2020.601004

Dimkpa, C. O., Svatoš, A., Dabrowska, P., Schmidt, A., Boland, W., & Kothe, E. (2008). Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces spp. Chemosphere, 74(1), 19-25. https://doi.org/10.1016/j.chemosphere.2008.09.079

Dodd, I. C., Zinovkina, N. Y., Safronova, V. I., & Belimov, A. A. (2010). Rhizobacterial mediation of plant hormone status. Annals of Applied Biology, 157(3), 361-379. https://doi.org/10.1111/j.1744-7348.2010.00439.x

Domínguez-Núñez, J. A., Medina, M., Berrocal-Lobo, M., Anríquez, A., & Albanesi, A. (2015). The combined effects of Pseudomonas fluorescens CECT 844 and the black truffle co-inoculation on Pinus nigra seedlings. iForest, 8(5), 624-630. https://doi.org/10.3832/ifor1334-007

Eichmann, R., Richards, L., & Schäfer, P. (2021). Hormones as go-betweens in plant microbiome assembly. The Plant Journal, 105(2), 518-541. https://doi.org/10.1111/tpj.15135

El Sabagh, A., Islam, M. S., Hossain, A., Iqbal, M. A., Mubeen, M., Waleed, M., Reginato, M., Battaglia, M., Ahmed, S., Rehman, A., Arif, M., Athar, H.-U.-R., Ratnasekera, D., Danish, S., Raza, M. A., Rajendran, K., Mushtaq, M., Skalicky, M., Brestic, M., Soufan, W., Fahad, S., Pandey, S., Kamran, M., Datta, R., & Abdelhamid, M. T. (2022). Phytohormones as growth regulators during abiotic stress tolerance in plants. Frontiers in Agronomy, 4, 765068. https://doi.org/10.3389/fagro.2022.765068

El Sabagh, A., Abdelaal, K. A., & Barutcular, C. (2017). Impact of antioxidants supplementation on growth, yield and quality traits of canola (Brassica napus L.) under irrigation intervals in North Nile Delta of Egypt. Journal of Experimental Biology and Agricultural Sciences, 5(2), 163-172. https://doi.org/10.18006/2017.5(2).163.172

Farooq, M., Wahid, A., Kobayashi, N., Fujita, D., & Basra, S. M. A. (2009). Plant drought stress: Effects, mechanisms and management. Agronomy for Sustainable Development, 29(1), 185-212. https://doi.org/10.1051/agro:2008021

Fasciglione, G., Casanovas, E. M., Quillehauquy, V., Yommi, A. K., Goñi, M. G., Roura, S. I., & Barassi, C. A. (2015). Azospirillum inoculation effects on growth, product quality and storage life of lettuce plants grown under salt stress. Scientia Horticulturae, 195, 154-162. https://doi.org/10.1016/j.scienta.2015.09.015

Ferreira, M. J., Silva, H., & Cunha, A. (2019). Siderophore-producing rhizobacteria as a promising tool for empowering plants to cope with iron limitation in saline soils: A review. Pedosphere, 29(4), 409-420. https://doi.org/10.1016/S1002-0160(19)60810-6

Franco, J. A., Bañón, S., Vicente, M. J., Miralles, J., & Martínez-Sánchez, J. J. (2011). Root development in horticultural plants grown under abiotic stress conditions: A review. The Journal of Horticultural Science and Biotechnology, 86(6), 543-556. https://doi.org/10.1080/14620316.2011.11512802

Gahan, J., & Schmalenberger, A. (2014). The role of bacteria and mycorrhiza in plant sulfur supply. Frontiers in Plant Science, 5, 723. https://doi.org/10.3389/fpls.2014.00723

Gao, X., Luan, J., Wang, L., Li, H., Wang, Q., Wang, Z., Jin, Z., & Yu, F. (2023). Effect of the plant growth promoting rhizobacterium, Cronobacter sp. Y501, for enhancing drought tolerance in maize (Zea mays L.). Journal of Soil Science and Plant Nutrition, 23(2), 2786-2797. https://doi.org/10.1007/s42729-023-01234-2

Goodrich, J. K., Davenport, E. R., Waters, J. L., Clark, A. G., & Ley, R. E. (2016) Cross-species comparisons of host genetic associations with the microbiome. Science, 352(6285), 532-535. https://doi.org/10.1126/science.aad9379

Goswami, D., Thakker, J. N., & Dhandhukia, P. C. (2016). Portraying mechanics of plant growth promoting rhizobacteria (PGPR): A review. Cogent Food & Agriculture, 2(1), 1127500. https://doi.org/10.1080/23311932.2015.1127500

Grant, O. M. (2012). Understanding and exploiting the impact of drought stress on plant physiology. In P. Ahmad & M. N. V. Prasad (Eds.), Abiotic stress responses in plants: Metabolism, productivity and sustainability (pp. 89-104). Springer. https://doi.org/10.1007/978-1-4614-0634-1_5

Grice, E. A., & Segre, J. A. (2012). The human microbiome: Our second genome. Annual Review of Genomics and Human Genetics, 13, 151-170. https://doi.org/10.1146/annurev-genom-090711-163814

Guo, H., Huang, Z., Li, M., & Hou, Z. (2020a). Growth, ionic homeostasis, and physiological responses of cotton under different salt and alkali stresses. Scientific Reports, 10(1), 21844. https://doi.org/10.1038/s41598-020-79045-z

Guo, Q., Meng, L., Han, J., Mao, P., Tian, X., Zheng, M., & Mur, L. A. J. (2020b). SOS1 is a key systemic regulator of salt secretion and K⁺/Na⁺ homeostasis in the recretohalophyte Karelinia caspia. Environmental and Experimental Botany, 177, 104098. https://doi.org/10.1016/j.envexpbot.2020.104098

Gupta, A., Rico-Medina, A., & Caño-Delgado, A. I. (2020). The physiology of plant responses to drought. Science, 368(6488), 266-269. https://doi.org/10.1126/science.aaz7614

Hafez, Y. M., Abdelaal, K. A., Eid, M. E., & Mehiar, F. F. (2016). Morpho-physiological and biochemical responses of barley plants (Hordeum vulgare L.) against barley net blotch disease with application of non-traditional compounds and fungicides. Egyptian Journal of Biological Pest Control, 26(2), 261-268.

Han, S., Cheng, Y., Wu, G., He, X., & Zhao, G. (2024). Enhancing salt tolerance in poplar seedlings through arbuscular mycorrhizal fungi symbiosis. Plants, 13(2), 233. https://doi.org/10.3390/plants13020233

National Research Council, Board on Life Sciences, Committee on Metagenomics, & Functional Applications. (2007). The new science of metagenomics: Revealing the secrets of our microbial planet. The National Academies Press. https://doi.org/10.17226/11902

Hasan, M. K., El Sabagh, A., Sikdar, M. S., Alam, M. J., Ratnasekera, D., Barutcular, C., Abdelaal, K. A. A., & Islam, M. S. (2017). Comparative adaptable agronomic traits of blackgram and mungbean for saline lands. Plant Archives, 17(1), 589-593.

He, A., Niu, S., Yang, D., Ren, W., Zhao, L., Sun, Y., Meng, L., Zhao, Q., Paré, P. W., & Zhang, J. (2021). Two PGPR strains from the rhizosphere of Haloxylon ammodendron promoted growth and enhanced drought tolerance of ryegrass. Plant Physiology and Biochemistry, 161, 74-85. https://doi.org/10.1016/j.plaphy.2021.02.003

Huang, Y. M., Zou, Y. N., & Wu, Q. S. (2017). Alleviation of drought stress by mycorrhizas is related to increased root H2O2 efflux in trifoliate orange. Scientific Reports, 7, 42335. https://doi.org/10.1038/srep42335

Jaiswal, D. K., Verma, J. P., Prakash, S., Meena, V. S., & Meena, R. S. (2016). Potassium as an important plant nutrient in sustainable agriculture: A state of the art. In V. S. Meena, B. R. Maurya, J. P. Verma & R. S. Meena (Eds.), Potassium solubilizing microorganisms for sustainable agriculture (pp. 21-29). Springer. https://doi.org/10.1007/978-81-322-2776-2_2

Johnson, D., & Gilbert, L. (2015). Interplant signalling through hyphal networks. New Phytologist, 205(4), 1448-1453. https://doi.org/10.1111/nph.13115

Kandemir, G., Önde, S., Temel, F., & Kaya, Z. (2017). Population variation in drought resistance and its relationship with adaptive and physiological seedling traits in Turkish red pine (Pinus brutia Ten.). Turkish Journal of Biology, 41(2), 256-267. https://doi.org/10.3906/biy-1608-77

Khosravi, M., Heydari, M., Alikhani, H. A., Arani, A. M., Guidi, L., & Prévosto, B. (2025). Mitigating negative impacts of drought on oak seedlings performances through plant growth-promoting rhizobacteria. Journal of Environmental Management, 375, 124163. https://doi.org/10.1016/j.jenvman.2025.124163

Kim, S. G., Kim, S. Y., & Park, C. M. (2007). A membrane-associated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Planta, 226(3), 647-654. https://doi.org/10.1007/s00425-007-0513-3

Knief, C., Delmotte, N., Chaffron, S., Stark, M., Innerebner, G., Wassmann, R., von Mering, C., & Vorholt, J. A. (2012). Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. The ISME Journal, 6(7), 1378-1390. https://doi.org/10.1038/ismej.2011.192

Kumari, V. V., Banerjee, P., Verma, V. C., Sukumaran, S., Chandran, M. A. S., Gopinath, K. A., Venkatesh, G., Yadav, S. K., Singh, V. K., & Awasthi, N. K. (2022). Plant nutrition: An effective way to alleviate abiotic stress in agricultural crops. International Journal of Molecular Sciences, 23(15), 8519. https://doi.org/10.3390/ijms23158519

La, V. H., Lee, B. R., Zhang, Q., Park, S. H., Islam, M. T., & Kim, T. H. (2019). Salicylic acid improves drought-stress tolerance by regulating the redox status and proline metabolism in Brassica rapa. Horticulture, Environment, and Biotechnology, 60(1), 31-40. https://doi.org/10.1007/s13580-018-0099-7

Leake, J., Johnson, D., Donnelly, D., Muckle, G., Boddy, L., & Read, D. (2004). Networks of power and influence: The role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Canadian Journal of Botany, 82(8), 1016-1045. https://doi.org/10.1139/b04-060

Li, F., Zi, H., Sonne, C., & Li, X. (2023). Microbiome sustains forest ecosystem functions across hierarchical scales. Eco-Environment & Health, 2(1), 24-31. https://doi.org/10.1016/j.eehl.2023.03.001

Ma, Y., Oliveira, R. S., Freitas, H., & Zhang, C. (2016a). Biochemical and molecular mechanisms of plant-microbe-metal interactions: Relevance for phytoremediation. Frontiers in Plant Science, 7, 918. https://doi.org/10.3389/fpls.2016.00918

Ma, Y., Zhang, C., Oliveira, R. S., Freitas, H., & Luo, Y. (2016b). Bioaugmentation with endophytic bacterium E6S homologous to Achromobacter piechaudii enhances metal Rhizoaccumulation in host Sedum plumbizincicola. Frontiers in Plant Science, 7, 75. https://doi.org/10.3389/fpls.2016.00075

Mendes, R., Garbeva, P., & Raaijmakers, J. M. (2013). The rhizosphere microbiome: Significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiology Reviews, 37(5), 634-663. https://doi.org/10.1111/1574-6976.12028

Mishra, P., Mishra, J., & Arora, N. K. (2023). Biofortification revisited: Addressing the role of beneficial soil microbes for enhancing trace elements concentration in staple crops. Microbiological Research, 275, 127442. https://doi.org/10.1016/j.micres.2023.127442

Mittler, R. (2017). ROS are good. Trends in Plant Science, 22(1), 11-19. https://doi.org/10.1016/j.tplants.2016.08.002

Mohanram, S., & Kumar, P. (2019). Rhizosphere microbiome: Revisiting the synergy of plant-microbe interactions. Annals of Microbiology, 69(4), 307-320. https://doi.org/10.1007/s13213-019-01448-9

Mohanty, P., Singh, P. K., Chakraborty, D., Mishra, S., & Pattnaik, R. (2021). Insight into the role of PGPR in sustainable agriculture and environment. Frontiers in Sustainable Food Systems, 5, 667150. https://doi.org/10.3389/fsufs.2021.667150

Munns, R., & Tester, M. (2008). Mechanisms of salinity tolerance. Annual Review of Plant Biology, 59, 651-681. https://doi.org/10.1146/annurev.arplant.59.032607.092911

Nosheen, S., Ajmal, I., & Song, Y. (2021). Microbes as biofertilizers, a potential approach for sustainable crop production. Sustainability, 13(4), 1868. https://doi.org/10.3390/su13041868

Nouri, K., Nikbakht, A. M., Haghighi, M., Etemadi, N., Rahimmalek, M., & Szumny, A. (2023). Screening some pine species from North America and dried zones of western Asia for drought stress tolerance in terms of nutrients status, biochemical and physiological characteristics. Frontiers in Plant Science, 14, 1281688. https://doi.org/10.3389/fpls.2023.1281688

Novo, L. A., Mahler, C. F., & González, L. (2015). Plants to harvest rhenium: Scientific and economic viability. Environmental Chemistry Letters, 13(4), 439-445. https://doi.org/10.1007/s10311-015-0517-3

Orozco-Mosqueda, M. D. C., Rocha-Granados, M. D. C., Glick, B. R., & Santoyo, G. (2018). Microbiome engineering to improve biocontrol and plant growth-promoting mechanisms. Microbiological Research, 208, 25-31. https://doi.org/10.1016/j.micres.2018.01.005

Parke, J. L., Linderman, R. G., & Black, C. H. (1983). The role of ectomycorrhizas in drought tolerance of Douglas-fir seedlings. New Phytologist, 95(1), 83-95. https://doi.org/10.1111/j.1469-8137.1983.tb03471.x

Parlak, S., & Güner, D. (2017). Mikrobiyal gübre uygulamasının karaçam (Pinus nigra Arnold subsp. pallasiana Lamb. Holmboe) fidanlarının bazı morfolojik özelliklerine etkisi. Ormancılık Araştırma Dergisi, 4(2), 100-106. https://doi.org/10.17568/ogmoad.337884 (In Turkish)

Piveta, L. B., Roma-Burgos, N., Noldin, J. A., Viana, V. E., de Oliveira, C., Lamego, F. P., & de Avila, L. A. (2021). Molecular and physiological responses of rice and weedy rice to heat and drought stress. Agriculture, 11(1), 9. https://doi.org/10.3390/agriculture11010009

Puri, A., Padda, K. P., & Chanway, C. P. (2020). Sustaining the growth of Pinaceae trees under nutrient-limited edaphic conditions via plant-beneficial bacteria. PLOS One, 15(8), e0238055. https://doi.org/10.1371/journal.pone.0238055

Raaijmakers, J. M., Paulitz, T. C., Steinberg, C., Alabouvette, C., & Moënne-Loccoz, Y. (2009). The rhizosphere: A playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant and Soil, 321, 341-361. https://doi.org/10.1007/s11104-008-9568-6

Rahdari, P., & Hoseini, S. M. (2012). Drought stress: A review. International Journal of Agronomy and Plant Production, 3(10), 443-446.

Rashid, M. I., Mujawar, L. H., Shahzad, T., Almeelbi, T., Ismail, I. M., & Oves, M. (2016). Bacteria and fungi can contribute to nutrients bioavailability and aggregate formation in degraded soils. Microbiological Research, 183, 26-41. https://doi.org/10.1016/j.micres.2015.11.007

Rashwan, E., Alsohim, A. S., El-Gammaal, A., Hafez, Y., & Abdelaal, K. A. (2020). Foliar application of nano zink-oxide can alleviate the harmful effects of water deficit on some flax cultivars under drought conditions. Fresenius Environmental Bulletin, 29, 8889-8904.

Repáč, I., Balanda, M., Vencurik, J., Kmet’, J., Krajmerová, D., & Paule, L. (2014). Effects of substrate and ectomycorrhizal inoculation on the development of two-years-old container-grown Norway spruce (Picea abies Karst.) seedlings. iForest-Biogeosciences and Forestry, 8(4), 487-496. https://doi.org/10.3832/ifor1291-007

Rincón, A., Valladares, F., Gimeno, T. E., & Pueyo, J. J. (2008). Water stress responses of two Mediterranean tree species influenced by native soil microorganisms and inoculation with a plant growth-promoting rhizobacterium. Tree Physiology, 28(11), 1693-1701. https://doi.org/10.1093/treephys/28.11.1693

Samancıoğlu, A., & Yıldırım, E. (2015). Bitki gelişimini teşvik eden bakteri uygulamalarının bitkilerde kuraklığa toleransı artırmadaki etkileri. Mustafa Kemal Üniversitesi Ziraat Fakültesi Dergisi, 20(1), 72-79. (In Turkish)

Sanhueza, T., Hernández, I., Sagredo-Sáez, C., Villanueva-Guerrero, A., Alvarado, R., Mujica, M. I., Fuentes-Quiroz, A., Menéndez, E., Jorquera-Fontena, E., da Silva Valadares, R. B., & Herrera, H. (2024). Juvenile plant–microbe interactions modulate the adaptation and response of forest seedlings to rapid climate change. Plants, 13(2), 175. https://doi.org/10.3390/plants13020175

Santoyo, G., Moreno-Hagelsieb, G., del Carmen Orozco-Mosqueda, M., & Glick, B. R. (2016). Plant growth-promoting bacterial endophytes. Microbiological Research, 183, 92-99. https://doi.org/10.1016/j.micres.2015.11.008

Sarker, U., & Oba, S. (2018). Drought stress enhances nutritional and bioactive compounds, phenolic acids and antioxidant capacity of Amaranthus leafy vegetable. BMC Plant Biology, 18(1), 258. https://doi.org/10.1186/s12870-018-1484-1

Serraj, R., & Sinclair, T. R. (2002). Osmolyte accumulation: Can it really help increase crop yield under drought conditions? Plant, Cell & Environment, 25(2), 333-341. https://doi.org/10.1046/j.1365-3040.2002.00754.x

Sevanto, S., Gehring, C. A., Ryan, M. G., Patterson, A., Losko, A. S., Vogel, S. C., Carter, K. R., Dickman, L. T., Espy, M. A., & Kuske, C. R. (2023). Benefits of symbiotic ectomycorrhizal fungi to plant water relations depend on plant genotype in pinyon pine. Scientific Reports, 13, 14424. https://doi.org/10.1038/s41598-023-41191-5

Shahid, M., Singh, U. B., Khan, M. S., Singh, P., Kumar, R., Singh, R. N., Kumar, A., & Singh, H. V. (2023). Bacterial ACC deaminase: Insights into enzymology, biochemistry, genetics, and potential role in amelioration of environmental stress in crop plants. Frontiers in Microbiology, 14, 1132770. https://doi.org/10.3389/fmicb.2023.1132770

Sheikh, A. H., Raghuram, B., Eschen-Lippold, L., Scheel, D., Lee, J., & Sinha, A. K. (2014). Agroinfiltration by cytokinin-producing Agrobacterium sp. strain GV3101 primes defense responses in Nicotiana tabacum. Molecular Plant-Microbe Interactions, 27(11), 1175-1185. https://doi.org/10.1094/mpmi-04-14-0114-r

Shi, C.-L., Park, H.-B., Lee, J. S., Ryu, S., & Ryu, C.-M. (2010). Inhibition of primary roots and stimulation of lateral root development in Arabidopsis thaliana by the rhizobacterium Serratia marcescens 90–166 is through both auxin-dependent and-independent signaling pathways. Molecules and Cells, 29(3), 251-258. https://doi.org/10.1007/s10059-010-0032-0

Shrivastava, P., & Kumar, R. (2015). Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi Journal of Biological Sciences, 22(2), 123-131. https://doi.org/10.1016/j.sjbs.2014.12.001

Siddiqui, M. H., Al-Khaishany, M. Y., Al-Qutami, M. A., Al-Whaibi, M. H., Grover, A., Ali, H. M., Al-Whaibi, M. S., & Bukhari, N. A. (2015). Response of different genotypes of faba bean plant to drought stress. International Journal of Molecular Sciences, 16(5), 10214-10227. https://doi.org/10.3390/ijms160510214

Spence, C., & Bais, H. (2015). Role of plant growth regulators as chemical signals in plant-microbe interactions: A double edged sword. Current Opinion in Plant Biology, 27, 52-58. https://doi.org/10.1016/j.pbi.2015.05.028

Timofeeva, A. M., Galyamova, M. R., & Sedykh, S. E. (2022). Bacterial siderophores: Classification, biosynthesis, perspectives of use in agriculture. Plants, 11(22), 3065. https://doi.org/10.3390/plants11223065

Toprak, B. (2020). Early growth performance of mycorrhizae-inoculated Taurus cedar (Cedrus libani A. Rich.) seedlings in a nursery experiment conducted in inland part of Turkey. Journal of Plant Nutrition, 43(2), 165-175. https://doi.org/10.1080/01904167.2019.1656242

Tripathi, R., Aravind, T., Kumar, S., Keswani, C., Singh, S. P., Tewari, R., Tewari, A. K., Singh, K. P., & Minkina, T. (2025). Microbial phytohormones: the potential orchestrators of plant growth and defense. Discover Plants, 2(1), 180. https://doi.org/10.1007/s44372-025-00274-5

Tüfekçi, S., & Ortaş, İ. (2024). Impact of three distinct mycorrhizal species on Cedrus libani seedling development and nutrient uptake. Forest Systems, 33(2), e04. https://doi.org/10.5424/fs/2024332-20816

Turner, T. R., James, E. K., & Poole, P. S. (2013). The plant microbiome. Genome Biology, 14(6), 209. https://doi.org/10.1186/gb-2013-14-6-209

Ulrich, D. E. M., Sevanto, S., Peterson, S., Ryan, M., & Dunbar, J. (2020). Effects of soil microbes on functional traits of loblolly pine (Pinus taeda) seedling families from contrasting climates. Frontiers in Plant Science, 10, 1643. https://doi.org/10.3389/fpls.2019.01643

Uzma, M., Iqbal, A., & Hasnain, S. (2022). Drought tolerance induction and growth promotion by indole acetic acid producing Pseudomonas aeruginosa in Vigna radiata. PLOS One, 17(2), e0262932. https://doi.org/10.1371/journal.pone.0262932

Van Zelm, E., Zhang, Y., & Testerink, C. (2020). Salt tolerance mechanisms of plants. Annual Review of Plant Biology, 71(1), 403-433. https://doi.org/10.1146/annurev-arplant-050718-100005

Vasanthi, N., Saleena, L. M., & Raj, S. A. (2018). Silica solubilization potential of certain bacterial species in the presence of different silicate minerals. Silicon, 10(2), 267-275. https://doi.org/10.1007/s12633-016-9438-4

Verma, V., Ravindran, P., & Kumar, P. P. (2016). Plant hormone-mediated regulation of stress responses. BMC Plant Biology, 16(1), 86. https://doi.org/10.1186/s12870-016-0771-y

Wang, J., Zhang, H., Gao, J., Zhang, Y., Liu, Y., & Tang, M. (2021). Effects of ectomycorrhizal fungi (Suillus variegatus) on the growth, hydraulic function, and non-structural carbohydrates of Pinus tabulaeformis under drought stress. BMC Plant Biology, 21, 171. https://doi.org/10.1186/s12870-021-02945-3

Wang, J., Zhang, Y., Li, Y., Wang, X., Nan, W., Hu, Y., Zhang, H., Zhao, C., Wang, F., Li, P., Shi, H., & Bi, Y. (2015). Endophytic microbes Bacillus sp. LZR216-regulated root development is dependent on polar auxin transport in Arabidopsis seedlings. Plant Cell Reports, 34(6), 1075-1087. https://doi.org/10.1007/s00299-015-1766-0

Wang, P., Sun, X., Li, C., Wei, Z., Liang, D., & Ma, F. (2013). Long‐term exogenous application of melatonin delays drought‐induced leaf senescence in apple. Journal of Pineal Research, 54(3), 292-302. https://doi.org/10.1111/jpi.12017

Werner, S., Polle, A., & Brinkmann, N. (2016). Belowground communication: Impacts of volatile organic compounds (VOCs) from soil fungi on other soil-inhabiting organisms. Applied Microbiology and Biotechnology, 100(20), 8651-8665. https://doi.org/10.1007/s00253-016-7792-1

Xu, L., He, J., Meng, Y., Zheng, Y., Lu, B., Zhang, J., & Zhou, Y. (2024). Enhancing drought resistance in Pinus tabuliformis seedlings through root symbiotic fungi inoculation. Frontiers in Plant Science, 15, 1446437. https://doi.org/10.3389/fpls.2024.1446437

Yadav, S. K. (2010). Cold stress tolerance mechanisms in plants. A review. Agronomy for Sustainable Development, 30(3), 515-527. https://doi.org/10.1051/agro/2009050

Yavuz, Z., & Kocaçınar, F. (2025). Seasonal changes in biochemical properties of some tree species growing in humid, semi-humid, semi-arid and arid forests. Kastamonu University Journal of Forestry Faculty, 25(2), 177-187. https://doi.org/10.17475/kastorman.1787158

Zare, M., Azizi, M. H., & Bazrafshan, F. (2011). Effect of drought stress on some agronomic traits in ten barley (Hordeum vulgare) cultivars. Technical Journal of Engineering and Applied Sciences, 1(3), 57-62.

Downloads

Published

30-09-2026

Issue

Section

Review Articles