Kuraklık Stresi Altındaki Fasulyelerde Mikoriza ve Trichoderma Tedavisinin Malondialdehit Düzeyleri ve Antioksidan Aktivitesi Üzerindeki Etkisi

Öz

Küresel sıcaklıkların artması ve kuraklık koşullarının giderek daha sık hale gelmesiyle birlikte, sürdürülebilir tarım uygulamalarını geliştirme ihtiyacı her zamankinden daha önemLi hale gelmiştir. Su kıtlığına karşı bitki direncinin artırılması, artan dünya nüfusunun gıda tedarikini güvence altına almak için hayati bir öneme sahiptir. Bu çalışmada, Arbusküler Mikoriza Fungus (AMF) ve Trichoderma harzianum'un, fasulye (Phaseolus vulgaris) bitkisinin fizyolojik tepkileri ve büyümesi üzerindeki etkileri %100 ve %50 sulama rejimLeri altında incelenmiştir. %50 sulama rejimi altında, AMF ve T. harzianum inokülasyonu, kontrol grubuna kıyasla bitki boyunda %34.5, kök uzunluğunda ise %16.79 oranında önemLi artışlar sağlamıştır. Ayrıca, su kısıtı koşullarında T. harzianum uygulanan bitkilerde klorofil a (%175), klorofil b (%194) ve toplam klorofil (%180) içeriğinde belirgin artışlar gözlemLenmiştir. AMF uygulaması, toplam karotenoid içeriğinde %18'lik bir artış sağlayarak fotosentetik pigmentlerin sürdürülebilirliğini göstermiştir. Bunun yanı sıra, her iki uygulamanın da malondialdehit (MDA) birikimini önemLi ölçüde azalttığı, kuraklık koşullarında kontrol grubuna kıyasla %46.3 oranında azalma sağladığı tespit edilmiştir. Katalaz (CAT), tam sulama altında T. harzianum uygulamasıyla %201, azaltılmış sulama altında ise AMF ile %217 artış göstermiştir, bu da bu biyostimülanların oksidatif stresi hafifletmedeki rolünü vurgulamaktadır. Temel bileşen analizi (PCA), bu tedavilerin hücresel bütünlüğü etkili bir şekilde koruduğunu ve stres toleransını artırdığını doğrulamıştır. Bu bulgular, AMF ve T. harzianum nın, kuraklığa karşı bitki direncini artırmada hayati araçlar olarak potansiyelini, kurak ve yarı kurak bölgelerde sürdürülebilir tarım için önemLi sonuçlarla birlikte ortaya koymaktadır.

Anahtar Kelimeler

• Kuraklığa tolerans
• biyostimülanlar
• oksidatif stres azaltma
• AMF
• küresel ısınma

The Impact of Mycorrhiza and Trichoderma Treatment on Malondialdehyde Levels and Antioxidant Activity in Common Beans under Drought Stress

Abstract

As global temperatures rise and drought conditions become increasingly frequent, the need to develop sustainable agricultural practices has become paramount. Enhancing crop resilience to water scarcity is essential to secure food supplies for a growing global population. This study examined the effects of Arbuscular Mycorrhizal Fungi (AMF) and Trichoderma harzianum on the physiological responses and growth of common bean (Phaseolus vulgaris) under 100% and 50% irrigation regimes. Under a 50% irrigation regime, AMF and Trichoderma harzianum inoculation led to substantial increases in plant height (34.5%) and root length (16.79%), compared to the control. Additionally, significant enhancements were observed in chlorophyll a (175%), chlorophyll b (194%), and total chlorophyll (180%) content in plants subjected to T. harzianum inoculation under water deficit. The application of AMF resulted in an 18% increase in total carotenoid content, showing its efficacy in sustaining photosynthetic pigments. Furthermore, the study revealed that both treatments significantly reduced malondialdehyde (MDA) accumulation, with reductions of 46.3% compared to the control under drought conditions. Catalase (CAT), increased by 201% with T. harzianum application under full irrigation and by 217% with AMF under reduced irrigation, highlighting the role of these biostimulants in mitigating oxidative stress. Principal component analysis (PCA) further confirmed that these treatments effectively maintained cellular integrity and enhanced stress tolerance. These findings underscore the potential of AMF and T. harzianum as vital tools in enhancing crop resilience against drought, with significant implications for sustainable agriculture in arid and semi-arid regions.

Keywords

• Drought tolerance
• biostimulants
• oxidative stress mitigation
• AMF
• global warming

References

1. Abdalla, M., & Ahmed, M. A. (2021). Arbuscular mycorrhiza symbiosis enhances water status and soil-plant hydraulic conductance under drought. Frontiers in Plant Science, 12, 722954. https://doi.org/10.3389/fpls.2021.722954
2. Abdalla, M., Bitterlich, M., Jansa, J., Püschel, D., & Ahmed, M. A. (2023). The role of arbuscular mycorrhizal symbiosis in improving plant water status under drought. Journal of Experimental Botany, 74(16), 4808-4824. https://doi.org/10.1093/jxb/erad249
3. Abdel-Salam, E., Alatar, A., & El-Sheikh, M. A. (2018). Inoculation with arbuscular mycorrhizal fungi alleviates harmful effects of drought stress on damask rose. Saudi Journal of Biological Sciences, 25(8), 1772-1780. https://doi.org/10.1016/j.sjbs.2017.10.015
4. Agbodjato, N. A., Assogba, S. A., Babalola, O. O., Koda, A. D., Aguégué, R. M., Sina, H., Dagbenonbakin, D. G., Adjanohoun, A., & Baba-Moussa, L. (2022). Formulation of biostimulants based on arbuscular mycorrhizal fungi for maize growth and yield. Frontiers in Agronomy, 4, 894489. https://doi.org/10.3389/fagro.2022.894489
5. Anjum, S. A., Xie, X. Y., Wang, L. C., Saleem, M. F., Man, C., & Lei, W. (2011). Morphological, physiological and biochemical responses of plants to drought stress. African journal of agricultural research, 6(9), 2026-2032. https://doi.org/10.5897/AJAR10.027
6. Arnon, D. I. (1949). Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology, 24(1), 1.
7. Azad, K., & Kaminskyj, S. (2016). A fungal endophyte strategy for mitigating the effect of salt and drought stress on plant growth. Symbiosis, 68, 73-78. https://doi.org/10.1007/s13199-015-0370-y
8. Bashyal, B. M., Parmar, P., Zaidi, N. W., & Aggarwal, R. (2021). Molecular programming of drought-challenged Trichoderma harzianum-bioprimed rice (Oryza sativa L.). Frontiers in Microbiology, 12, 655165. https://doi.org/10.3389/fmicb.2021.655165

9. Beauchamp, C., & Fridovich, I. (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry, 44(1), 276-287. https://doi.org/10.1016/0003-2697(71)90370-8
10. Beers, R. F., & Sizer, I. W. (1952). A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. Journal of Biological Chemistry, 195(1), 133-140.
11. Begum, N., Ahanger, M. A., & Zhang, L. (2020). AMF inoculation and phosphorus supplementation alleviates drought induced growth and photosynthetic decline in Nicotiana tabacum by up-regulating antioxidant metabolism and osmolyte accumulation. Environmental and Experimental Botany, 176, 104088. https://doi.org/10.1016/j.envexpbot.2020.104088
12. Begum, N., Ahanger, M. A., Su, Y., Lei, Y., Mustafa, N. S. A., Ahmad, P., & Zhang, L. (2019). Improved drought tolerance by AMF inoculation in maize (Zea mays) involves physiological and biochemical implications. Plants, 8(12), 579. https://doi.org/10.3390/plants8120579
13. Blair, M. W., Izquierdo, P., Astudillo, C., & Grusak, M. A. (2013). A legume biofortification quandary: Variability and genetic control of seed coat micronutrient accumulation in common beans. Frontiers in Plant Science, 4, 275. https://doi.org/10.3389/fpls.2013.00275
14. Boorboori, M. R., & Zhang, H. (2023). The mechanisms of Trichoderma species to reduce drought and salinity stress in plants. Phyton, 92(8). https://doi.org/10.32604/phyton.2023.029486
15. Canal, S. B., Bozkurt, M. A., & Yílmaz, H. (2023). Humic acid ameliorates phytoremediation, plant growth and antioxidative enzymes in forage turnip (Brassica rapa L.). Plant, Soil & Environment, 69(12). https://doi.org/10.17221/394/2023-PSE
16. Claeys, H., & Inzé, D. (2013). The agony of choice: how plants balance growth and survival under water-limiting conditions. Plant Physiology, 162(4), 1768-1779. https://doi.org/10.1104/pp.113.220921
17. Demirel, F., Kumlay, A. M., & Yıldırım, B. (2021). Bazı Ekmeklik Buğday (Triticum aestivum L.) Genotiplerinin Agromorfolojik Özellikleri Bakımından Biplot, Kümeleme ve Path Analizi Yöntemleri ile Değerlendirilmesi. Avrupa Bilim ve Teknoloji Dergisi, (23), 304-311.
18. Duc, N. H., Csintalan, Z., & Posta, K. (2018). Arbuscular mycorrhizal fungi mitigate negative effects of combined drought and heat stress on tomato plants. Plant Physiology and Biochemistry, 132, 297-307. https://doi.org/10.1016/j.plaphy.2018.09.011
19. El-Sawah, A. M., Abdel-Fattah, G. G., Holford, P., Korany, S. M., Alsherif, E. A., Abdelgawad, H., Ulhassan, Z., Josko, I., Ali, B., & Sheteiwy, M. S. (2023). Funneliformis constrictum modulates polyamine metabolism to enhance tolerance of Zea mays L. to salinity. Microbiological Research, 266, 127254. https://doi.org/10.1016/j.micres.2022.127254
20. Eshaghi Gorgi, O., Fallah, H., Niknejad, Y., & Barari Tari, D. (2022). Effect of plant growth promoting rhizobacteria (PGPR) and mycorrhizal fungi inoculations on essential oil in Melissa officinalis L. under drought stress. Biologia, 77(1), 11-20. https://doi.org/10.1007/s11756-021-00919-2
21. FAO. (2021). The impact of disasters and crises on agriculture and food security: 2021. Rome.
22. FAO. (2024). Crop production statistics. https://www.fao.org/faostat/en/.[Access date: July 14, 2024].
23. Farooq, M., Hussain, M., Wahid, A., & Siddique, K. H. M. (2012). Drought stress in plants: an overview. In M. A. Hossain, S. H. Wani, S. Bhattacharjee, D. J. Burritt, L.-S. Tran, & T. J. Close (Eds.), Plant Responses to Drought Stress: From Morphological to Molecular Features (pp. 1-33). Springer. https://doi.org/10.1007/978-3-642-32653-0_1
24. Fazeli-Nasab, B., Shahraki-Mojahed, L., Piri, R., & Sobhanizadeh, A. (2022). Trichoderma: Improving growth and tolerance to biotic and abiotic stresses in plants. In Trends of Applied Microbiology for Sustainable Economy (pp. 525-564). Academic Press. https://doi.org/10.1016/b978-0-323-91595-3.00004-5
25. Ferlian, O., Biere, A., Bonfante, P., Buscot, F., Eisenhauer, N., Fernandez, I., Hause, B., Herrmann, S., Krajinski-Barth, F., Meier, C. I., Pozo, J. M., Rasmann, S., Rilling, C. M., Tarkka, T. M., van Dam, M. N., Wagg, C., & Martinez-Medina, A. (2018). Growing research networks on mycorrhizae for mutual benefits. Trends in Plant Science, 23(11), 975-984. https://doi.org/10.1016/j.tplants.2018.08.008
26. Foyer, C. H., & Hanke, G. (2022). ROS production and signalling in chloroplasts: cornerstones and evolving concepts. The Plant Journal, 111(3), 642-661. https://doi.org/10.1111/tpj.15856
27. Gupta, A., Rico-Medina, A., & Cao, M. J. (2020). The physiology of plant responses to drought. Science Advances, 6, 3-10. https://doi.org/10.1126/science.aaz7614
28. Gupta, R., & Bar, M. (2020). Plant immunity, priming, and systemic resistance as mechanisms for Trichoderma spp. biocontrol. In Trichoderma: Host Pathogen Interactions and Applications (pp. 81-110). https://doi.org/10.1007/978-981-15-3321-1_5
29. Hashem, A., Kumar, A., Al-Dbass, A. M., Alqarawi, A. A., Al-Arjani, A. B. F., Singh, G., Farooq, M., & Abd_Allah, E. F. (2019). Arbuscular mycorrhizal fungi and biochar improves drought tolerance in chickpea. Saudi Journal of Biological Sciences, 26(3), 614-624. https://doi.org/10.1016/j.sjbs.2018.11.005
30. He, J. D., Zou, Y. N., Wu, Q. S., & Kuča, K. (2020). Mycorrhizas enhance drought tolerance of trifoliate orange by enhancing activities and gene expression of antioxidant enzymes. Scientia Horticulturae, 262, 108745. https://doi.org/10.1016/j.scienta.2019.108745
31. Hu, Y., Xie, W., & Chen, B. (2020). Arbuscular mycorrhiza improved drought tolerance of maize seedlings by altering photosystem II efficiency and the levels of key metabolites. Chemical and Biological Technologies in Agriculture, 7, 1-14. https://doi.org/10.1186/s40538-020-00186-4
32. Hussain, S., Rao, M. J., Anjum, M. A., Ejaz, S., Zakir, I., Ali, M. A., Ahmad, N., & Ahmad, S. (2019). Oxidative stress and antioxidant defense in plants under drought conditions. In Plant Abiotic Stress Tolerance: Agronomic, Molecular and Biotechnological Approaches (pp. 207-219). https://doi.org/10.1007/978-3-030-06118-0_9
33. Ilyas, M., Nisar, M., Khan, N., Hazrat, A., Khan, A. H., Hayat, K., Fahad, S., Khan, A., & Ullah, A. (2021). Drought tolerance strategies in plants: a mechanistic approach. Journal of Plant Growth Regulation, 40, 926-944. https://doi.org/10.1007/s00344-020-10174-5
34. Kaur, G., & Asthir, B. (2017). Molecular responses to drought stress in plants. Biologia Plantarum, 61, 201-209. https://doi.org/10.1007/s10535-016-0700-9
35. Kaur, S., & Kumar, P. (2020). Ameliorative effect of Trichoderma, Rhizobium and mycorrhiza on internodal length, leaf area and total soluble protein in mung bean (Vigna radiata [L.] R. Wilazek) under drought stress. Journal of Pharmacognosy and Phytochemistry, 9(4), 971-977.
36. Khatun, M., Sarkar, S., Era, F. M., Islam, A. M., Anwar, M. P., Fahad, S., Datta, R., & Islam, A. A. (2021). Drought stress in grain legumes: Effects, tolerance mechanisms and management. Agronomy, 11(12), 2374. https://doi.org/10.3390/agronomy11122374
37. Khoshmanzar, E., Aliasgharzad, N., Neyshabouri, M. R., Khoshru, B., Arzanlou, M., & Asgari Lajayer, B. (2020). Effects of Trichoderma isolates on tomato growth and inducing its tolerance to water-deficit stress. International Journal of Environmental Science and Technology, 17, 869-878. https://doi.org/10.1007/s13762-019-02405-4
38. Lephatsi, M., Nephali, L., Meyer, V., Piater, L. A., Buthelezi, N., Dubery, I. A., Opperman, H., Brand, M., Huyser, J., & Tugizimana, F. (2022). Molecular mechanisms associated with microbial biostimulant-mediated growth enhancement, priming and drought stress tolerance in maize plants. Scientific Reports, 12(1), 10450. https://doi.org/10.1038/s41598-022-14570-7
39. Li, J., Meng, B., Chai, H., Yang, X., Song, W., Li, S., Lu, A., Zhang, T., & Sun, W. (2019). Arbuscular mycorrhizal fungi alleviate drought stress in C3 (Leymus chinensis) and C4 (Hemarthria altissima) grasses via altering antioxidant enzyme activities and photosynthesis. Frontiers in Plant Science, 10, 499. https://doi.org/10.3389/fpls.2019.00499
40. Malhi, G. S., Kaur, M., & Kaushik, P. (2021). Impact of climate change on agriculture and its mitigation strategies: A review. Sustainability, 13(3), 1318. https://doi.org/10.3390/su13031318
41. Mashabela, M. D., Masamba, P., & Kappo, A. P. (2023). Applications of metabolomics for the elucidation of abiotic stress tolerance in plants: A special focus on osmotic stress and heavy metal toxicity. Plants, 12(2), 269. https://doi.org/10.3390/plants12020269
42. Mathur, S., Tomar, R. S., & Jajoo, A. (2019). Arbuscular mycorrhizal fungi (AMF) protects photosynthetic apparatus of wheat under drought stress. Photosynthesis Research, 139, 227-238. https://doi.org/10.1007/s11120-018-0538-4
43. Meddich, A., Ait Rahou, Y., Boutasknit, A., Ait-El-Mokhtar, M., Fakhech, A., Lahbouki, S., Benaffari, W., Ben-Laouane, R., & Wahbi, S. (2022). Role of mycorrhizal fungi in improving the tolerance of melon (Cucumis melo) under two water deficit partial root drying and regulated deficit irrigation. Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology, 156(2), 469-479. https://doi.org/10.1080/11263504.2021.1881644
44. Mona, S. A., Hashem, A., Abd_Allah, E. F., Alqarawi, A. A., Soliman, D. W. K., Wirth, S., & Egamberdieva, D. (2017). Increased resistance of drought by Trichoderma harzianum fungal treatment correlates with increased secondary metabolites and proline content. Journal of Integrative Agriculture, 16(8), 1751-1757. https://doi.org/10.1016/S2095-3119(17)61695-2
45. Musaddaq, S., Khaliq, A., Aslam, Z., & Murtaza, G. (2021). Antioxidants enhanced drought tolerance and productivity of maize under semiarid environments. Pakistan Journal of Agricultural Sciences, 58(3). https://doi.org/10.21162/PAKJAS/21.649
46. Nahrawy, S. E., Elbagory, M., & Omara, A. E. D. (2020). Biocompatibility effect of Bradyrhizobium japonicum and Trichoderma strains on growth, nodulation and physiological traits of soybean (Glycine max L.) under water deficit conditions. Journal of Advances in Microbiology, 20(11), 52-66. https://doi.org/10.9734/jamb/2020/v20i1130300
47. Nanjundappa, A., Bagyaraj, D. J., Saxena, A. K., Kumar, M., & Chakdar, H. (2019). Interaction between arbuscular mycorrhizal fungi and Bacillus spp. in soil enhancing growth of crop plants. Fungal Biology and Biotechnology, 6(1), 23. https://doi.org/10.1186/s40694-019-0086-5
48. Özel, S. D., Gökkuş, A., & Alatürk, F. (2016). Farklı sulama seviyelerinin macar fiği (Vicia pannonica Crantz.) ve yem bezelyesinin (Pisum arvense L.) gelişimine etkileri. Alinteri Journal of Agriculture Science, 30(1), 46-52.
49. Öztürk, M., Türkyılmaz Ünal, B., García-Caparrós, P., Khursheed, A., Gul, A., & Hasanuzzaman, M. (2021). Osmoregulation and its actions during the drought stress in plants. Physiologia Plantarum, 172(2), 1321-1335. https://doi.org/10.1111/ppl.13297
50. Pandey, V., Ansari, M. W., Tula, S., Yadav, S., Sahoo, R. K., Shukla, N., Bains, G., Badal, S., Chandra, S., Gaur, A. K., Kumar, A., Shukla, A., Kumar, J., & Tuteja, N. (2016). Dose-dependent response of Trichoderma harzianum in improving drought tolerance in rice genotypes. Planta, 243, 1251-1264. https://doi.org/10.1007/s00425-016-2482-x
51. Pavithra, D., & Yapa, N. (2018). Arbuscular mycorrhizal fungi inoculation enhances drought stress tolerance of plants. Groundwater for Sustainable Development, 7, 490-494. https://doi.org/10.1016/j.gsd.2018.03.005
52. Poveda, J., Hermosa, R., Monte, E., & Nicolás, C. (2019). Trichoderma harzianum favours the access of arbuscular mycorrhizal fungi to non-host Brassicaceae roots and increases plant productivity. Scientific Reports, 9(1), 11650. https://doi.org/10.1038/s41598-019-48269-z
53. Prasad, P. V. V., Staggenborg, S. A., & Ristic, Z. (2011). Impact of drought and/or heat stress on physiological, developmental, growth, and yield processes of crop plants. Agronomy Journal, 103, 137-144. https://doi.org/10.2134/advagricsystmodel1.c11
54. Rosales, M. A., Ocampo, E., Rodríguez-Valentín, R., Olvera-Carrillo, Y., Acosta-Gallegos, J., & Covarrubias, A. A. (2012). Physiological analysis of common bean (Phaseolus vulgaris L.) cultivars uncovers characteristics related to terminal drought resistance. Plant Physiology and Biochemistry, 56, 24-34. https://doi.org/10.1016/j.plaphy.2012.04.007
55. Sairam, R. K., & Saxena, D. C. (2000). Oxidative stress and antioxidants in wheat genotypes: Possible mechanism of water stress tolerance. Journal of Agronomy and Crop Science, 184(1), 55-61. https://doi.org/10.1046/j.1439-037x.2000.00358.x
56. Saxena, B., Sharma, K., Kapoor, R., Wu, Q. S., & Giri, B. (2022). Insights into the molecular aspects of salt stress tolerance in mycorrhizal plants. World Journal of Microbiology and Biotechnology, 38(12), 253. https://doi.org/10.1007/s11274-022-03440-z
57. Shankar, V., Tayang, A., & Evelin, H. (2024). Mechanisms of Arbuscular Mycorrhizal Fungi-Induced Drought Stress Amelioration in Plants. In Arbuscular Mycorrhizal Fungi and Higher Plants: Fundamentals and Applications (pp. 149-175). Springer Nature Singapore. https://doi.org/10.1007/978-981-99-8220-2_7
58. Sheteiwy, M. S., Ali, D. F. I., Xiong, Y. C., Brestic, M., Skalicky, M., Hamoud, Y. A., Ulhassan, Z., Shaghaleh, H., AbdElgawad, H., Farooq, M., Sharma, A., & El-Sawah, A. M. (2021). Physiological and biochemical responses of soybean plants inoculated with arbuscular mycorrhizal fungi and Bradyrhizobium under drought stress. BMC Plant Biology, 21, 1-21. https://doi.org/10.1186/s12870-021-02949-z
59. Shukla, N., Awasthi, R. P., Rawat, L., & Kumar, J. (2012). Biochemical and physiological responses of rice (Oryza sativa L.) as influenced by Trichoderma harzianum under drought stress. Plant Physiology and Biochemistry, 54, 78-88. https://doi.org/10.1016/j.plaphy.2012.02.001
60. Shukla, N., Awasthi, R. P., Rawat, L., & Kumar, J. (2015). Seed biopriming with drought tolerant isolates of Trichoderma harzianum promote growth and drought tolerance in Triticum aestivum. Annals of Applied Biology, 166(2), 171-182. https://doi.org/10.1111/aab.12160
61. Singh, D. P., Singh, V., Gupta, V. K., Shukla, R., Prabha, R., Sarma, B. K., & Patel, J. S. (2020). Microbial inoculation in rice regulates antioxidative reactions and defense related genes to mitigate drought stress. Scientific Reports, 10(1), 4818. https://doi.org/10.1038/s41598-020-61140-w
62. Soares, C., Carvalho, M. E. A., Azevedo, R. A., & Fidalgo, F. (2019). Plants facing oxidative challenges—A little help from the antioxidant networks. Environmental and Experimental Botany, 161, 4-25. https://doi.org/10.1016/j.envexpbot.2018.12.009
63. Sofo, A., Scopa, A., Nuzzaci, M., & Vitti, A. (2015). Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. International Journal of Molecular Sciences, 16(6), 13561-13578. https://doi.org/10.3390/ijms160613561
64. Spinoso-Castillo, J. L., Moreno-Hernández, M. D. R., Mancilla-Álvarez, E., Sánchez-Segura, L., Sánchez-Páez, R., & Bello-Bello, J. J. (2023). Arbuscular mycorrhizal symbiosis improves ex vitro acclimatization of sugarcane plantlets (Saccharum spp.) under drought stress conditions. Plants, 12(3), 687. https://doi.org/10.3390/plants12030687
65. Sun, W., & Shahrajabian, M. H. (2023). The application of arbuscular mycorrhizal fungi as microbial biostimulant, sustainable approaches in modern agriculture. Plants, 12(17), 3101. https://doi.org/10.3390/plants12173101
66. Türkoğlu, A., Bolouri, P., Haliloğlu, K., Eren, B., Demirel, F., Işık, M. İ., Piokutowska, M.,Wojciechowski, T., & Niedbała, G. (2023). Modeling callus induction and regeneration in hypocotyl explant of fodder pea (Pisum sativum var. arvense L.) using machine learning algorithm method. Agronomy, 13(11), 2835. https://doi.org/10.3390/agronomy13112835
67. Wahab, A., Abdi, G., Saleem, M. H., Ali, B., Ullah, S., Shah, W., Muntaz, S., Yasin, G., Muresan, C. C., & Marc, R. A. (2022). Plants’ physio-biochemical and phyto-hormonal responses to alleviate the adverse effects of drought stress: A comprehensive review. Plants, 11(13), 1620. https://doi.org/10.3390/plants11131620
68. Wei, T., Simko, V., Levy, M., Xie, Y., Jin, Y., & ZemLa, J. (2017). Package ‘corrplot’. Statistician, 56, e24.
69. WHO (World Health Organization). (2023). The State of Food Security and Nutrition in the World 2023: Urbanization, agrifood systems transformation and healthy diets across the rural–urban continuum (Vol. 2023). Food & Agriculture Org.
70. Wickham, H. (2016). Programming with ggplot2. In ggplot2: Elegant Graphics for Data Analysis (pp. 241–253). Springer International Publishing.
71. Wu, Q. S., & Zou, Y. N. (2017). Arbuscular mycorrhizal fungi and tolerance of drought stress in plants. In Arbuscular Mycorrhizas and Stress Tolerance of Plants (pp. 25-41). https://doi.org/10.1007/978-981-10-4115-0_2
72. Yan, Y., Mao, Q., Wang, Y., Zhao, J., Fu, Y., Yang, Z., Peng, X., Zhang, M., Bai, B., Liu, A., Chen, S., & Ahammed, G. J. (2021). Trichoderma harzianum induces resistance to root-knot nematodes by increasing secondary metabolite synthesis and defense-related enzyme activity in Solanum lycopersicum L. Biological Control, 158, 104609. https://doi.org/10.1016/j.biocontrol.2021.104609
73. Yang, X., Lu, M., Wang, Y., Wang, Y., Liu, Z., & Chen, S. (2021). Response mechanism of plants to drought stress. Horticulturae, 7(3), 50. https://doi.org/10.3390/horticulturae7030050
74. Yeken, Z., M. (2023). Fasulye bitkisindeki bazi transkripsiyon faktörlerin abiyotik stres etmenlerine karşı tepkileri. A. Yılmaz & H. Yılmaz (eds), Bitkilerde stres direncini arttırma yöntemleri (ss. 19-55). İksad Publishing House.
75. Yılmaz, A., Yılmaz, H., Soydemir, H. E., & Çiftçi, V. (2022). Soya (Glycine max L.)’da PGPR ve AMF uygulamalarının verim özellikleri ve protein içeriğine etkisi. Uluslararası Tarım ve Yaban Hayatı Bilimleri Dergisi, 8(1), 108-118.
76. Yilmaz, A., Yildirim, E., Yilmaz, H., Soydemir, H. E., Güler, E., Ciftci, V., & Yaman, M. (2023). Use of arbuscular mycorrhizal fungi for boosting antioxidant enzyme metabolism and mitigating saline stress in Sweet Basil (Ocimum basilicum L.). Sustainability, 15(7), 5982. https://doi.org/10.3390/su15075982
77. Yilmaz, H., & Kulaz, H. (2019). The effects of plant growth promoting rhizobacteria on antioxidant activity in chickpea (Cicer arietinum L.) under salt stress. Legume Research - An International Journal, 42(1), 72-76. https://doi.org/10.18805/LR-435
78. Yilmaz, H., Özer, G., Baloch, F. S., Çiftçi, V., Chung, Y. S., & Sun, H. J. (2023). Genome-wide identification and expression analysis of MTP (Metal ion transport proteins) genes in the common bean. Plants, 12(18), 3218. https://doi.org/10.3390/plants12183218
79. Zehra, A., Meena, M., Dubey, M. K., Aamir, M., & Upadhyay, R. S. (2017). Synergistic effects of plant defense elicitors and Trichoderma harzianum on enhanced induction of antioxidant defense system in tomato against Fusarium wilt disease. Botanical Studies, 58, 1-14. https://doi.org/10.1186/s40529-017-0198-2
80. Zhang, H. Y., Xie, B. T., Duan, W. X., Dong, S. X., Wang, B. Q., Zhang, L. M., & Shi, C. Y. (2018). Effects of drought stress at different growth stages on photosynthetic efficiency and water consumption characteristics in sweet potato. Ying Yong Sheng Tai Xue Bao = The Journal of Applied Ecology, 29(6), 1943-1850. https://doi.org/10.13287/j.1001-9332.201806.024
81. Zhang, Z., Zhang, J., Xu, G., Zhou, L., & Li, Y. (2019). Arbuscular mycorrhizal fungi improve the growth and drought tolerance of Zenia insignis seedlings under drought stress. New Forests, 50(4), 593-604. https://doi.org/10.1007/s11056-018-9681-1