دوفصلنامه فنآوری تولیدات گیاهی

دوفصلنامه فنآوری تولیدات گیاهی

تعدیل تنش القاء شده توسط ویروس موزاییک گوجه‌فرنگی (ToMV) و بهبود شاخص‌های فیزیولوژیک و بیوشیمیایی گیاه گوجه‌فرنگی توسط قارچ Serendipita indica

نوع مقاله : مقاله پژوهشی

نویسندگان
1 دانش‌آموخته کارشناسی ارشد تولید محصولات گلخانه‌ای، گروه تولید و ژنتیک گیاهی، دانشکده کشاورزی، دانشگاه ملایر، ملایر، ایران
2 دانشیار، گروه تولید و ژنتیک گیاهی، دانشکده کشاورزی، دانشگاه ملایر، ملایر، ایران
3 استادیار، گروه تولید و ژنتیک گیاهی، دانشکده کشاورزی، دانشگاه ملایر، ملایر، ایران
10.22084/ppt.2026.32584.2185
چکیده
گوجه‌فرنگی یکی از مهم‌ترین محصولات سبزی در جهان است که تولید آن به‌طور قابل‌توجهی تحت تأثیر بیماری‌های ویروسی از جمله ویروس موزاییک گوجه‌فرنگی (Tomato mosaic virus) قرار می‌گیرد. قارچ اندوفیت Serendipita indica به دلیل توانایی در بهبود رشد و القای پاسخ‌های دفاعی در گیاهان، گزینه‌ای امیدبخش برای کاهش اثرات تنش‌های بیماری‌زا از جمله ویروس‌ها محسوب می‌شود. به‌منظور بررسی اثر قارچ S. indica بر بهبود پاسخ‌های رشدی، فیزیولوژیک و بیوشیمیایی گوجه‌فرنگی در شرایط آلودگی با ویروسToMV، آزمایشی به‌صورت فاکتوریل در قالب طرح کاملاً تصادفی در شرایط گلخانه‌ای اجرا شد. تیمارها شامل آلودگی با ویروس (شاهد و آلوده) و وضعیت تلقیح با قارچ (تلقیح‌شده و عدم تلقیح با قارچ) بودند. نشاءها در مرحله دوبرگی با سوسپانسیون اسپور قارچ تلقیح و در مرحله چهاربرگی به‌صورت مکانیکی با ویروس آلوده شدند. نتایج نشان داد که آلودگی با ویروس موجب کاهش معنی‌دار رشد، زیست‌توده، کلروفیل و محتوای نسبی آب و افزایش نشت الکترولیت، مالون‌دی‌آلدئید و پراکسید هیدروژن شد. در مقابل، تلقیح با قارچ سبب بهبود شاخص‌های رشدی و افزایش رنگدانه‌های فتوسنتزی شد و به‌طور معنی‌داری شاخص‌های تنش اکسیداتیو را کاهش داد. همچنین قارچ با افزایش فنول کل، قندهای محلول، پروتئین کل و تقویت فعالیت آنزیم‌های آنتی‌اکسیدان ظرفیت دفاعی گیاه را در شرایط شاهد و آلودگی با ویروس بهبود بخشید. به‌طورکلی، نتایج این پژوهش نشان داد که قارچ اندوفیت S. indica با تعدیل تنش اکسیداتیو و تقویت سیستم دفاعی گیاه، نقش مؤثری در افزایش تحمل گوجه‌فرنگی به آلودگی ویروسی دارد و می‌تواند به‌عنوان یک راهکار زیستی امیدبخش در مدیریت بیماری‌های ویروسی مورد استفاده قرار گیرد.
کلیدواژه‌ها
موضوعات

عنوان مقاله English

Mitigation of Tomato Mosaic Virus (ToMV)-Induced Stress and Improvement of Physiological and Biochemical Parameters in Tomato Plants by the Fungus Serendipita Indica

نویسندگان English

Sahar Fereydouni Valashjerdi 1
Mehdi Ghabooli 2
Reza Almasi 3
1 Department of Plant Production and Genetics, Faculty of Agriculture, Malayer University, Malayer, Iran
2 Department of Plant Production and Genetics, Faculty of Agriculture, Malayer University, Malayer, Iran
3 Department of Plant Production and Genetics, Faculty of Agriculture, Malayer University, Malayer, Iran
چکیده English

Introduction:
Tomato (Solanum lycopersicum L.) is one of the most important vegetable crops worldwide, widely cultivated for both fresh consumption and processing. However, its production is greatly affected by various pathogens, particularly viral diseases, which can significantly reduce plant growth, yield, and fruit quality. Among these pathogens, Tomato mosaic virus (ToMV), a member of the genus Tobamovirus, is considered one of the most important viruses infecting tomato plants. Infection with ToMV disrupts normal physiological processes, reduces photosynthetic efficiency, and induces oxidative stress through the excessive accumulation of reactive oxygen species, ultimately leading to growth inhibition and yield losses. In recent years, the use of beneficial soil microorganisms has gained considerable attention as an environmentally friendly approach to enhance plant resistance against biotic stresses. Endophytic fungi are among the most important groups of these microorganisms, as they establish mutualistic associations with host plants and can improve plant growth, nutrient uptake, and stress tolerance. Serendipita indica (formerly Piriformospora indica), a root‑colonizing endophytic fungus belonging to the order Sebacinales, is one of the most well‑studied beneficial fungi. This fungus can colonize the roots of a wide range of plant species and can be easily cultured under laboratory conditions. Numerous studies have shown that S. indica promotes plant growth by improving nutrient acquisition, enhancing photosynthetic performance, and regulating plant hormonal balance. In addition, it has been reported to increase plant tolerance to various abiotic stresses such as drought, salinity, and nutrient deficiency. Moreover, S. indica can stimulate plant defense mechanisms by enhancing antioxidant enzyme activities, promoting the accumulation of protective metabolites, and activating defense‑related pathways. Through these mechanisms, this endophytic fungus can help plants better cope with pathogen attacks. Therefore, due to its ability to promote plant growth and strengthen plant defense responses, S. indica is considered a promising biological agent for mitigating the adverse effects of plant pathogens, including viral infections in tomato.
Materials and Methods:
To investigate the effect of the endophytic fungus S. indica on improving growth, physiological, and biochemical responses of tomato under ToMV infection, a factorial experiment was conducted in a completely randomized design with five replications under greenhouse conditions. The experimental treatments included of two factors: virus infection at two levels (non‑infected control and ToMV‑infected plants) and fungal inoculation at two levels (non‑inoculated and inoculated with S. indica). Tomato seedlings were grown under controlled greenhouse conditions, and at the two‑leaf stage they were inoculated with a spore suspension of S. indica. Subsequently, at the four-leaf stage they were mechanically inoculated with the virus. Plants were then maintained under greenhouse conditions and monitored until the typical symptoms of viral infection appeared. After the appearance of symptoms, a comprehensive set of morphological, physiological, and biochemical parameters was evaluated. Growth characteristics such as shoot and root growth and biomass were measured. Physiological traits including photosynthetic pigments (chlorophyll a, chlorophyll b, and total chlorophyll) and relative water content were also determined. In addition, oxidative stress indicators, including electrolyte leakage, malondialdehyde (MDA), and hydrogen peroxide (H₂O₂), were assessed to evaluate membrane damage and oxidative injury. Furthermore, osmotic and defense‑related metabolites such as total phenolic compounds, soluble sugars, and total protein were quantified, along with the activities of major antioxidant enzymes including catalase, peroxidase, and ascorbate peroxidase. These measurements were carried out to better understand the role of S. indica in modulating plant responses to viral stress.
Results and discussion:
The results indicated that viral infection significantly impaired plant performance, leading to marked reductions in growth parameters, biomass accumulation, chlorophyll content, and relative water content. In addition, virus‑infected plants exhibited elevated levels of oxidative stress, as evidenced by increased electrolyte leakage, malondialdehyde (MDA), and hydrogen peroxide (H₂O₂) accumulation, reflecting enhanced membrane damage and cellular oxidative damage. In contrast, inoculation with the endophytic fungus S. indica markedly alleviated the detrimental effects of viral infection. Plants colonized by S. indica showed significant improvements in growth traits and biomass production, along with increased concentrations of photosynthetic pigments compared with non‑inoculated plants. Furthermore, fungal inoculation substantially reduced oxidative stress markers, including electrolyte leakage, MDA, and H₂O₂ levels. S. indica also enhanced the plant’s biochemical defense system by increasing total phenolic compounds, soluble sugars, and total protein content, while significantly stimulating the activities of key antioxidant enzymes such as catalase (CAT), peroxidase (POX), and ascorbate peroxidase (APX). Collectively, these responses indicate that S. indica strengthens the antioxidant and metabolic defense mechanisms of the plant, thereby improving its tolerance and physiological stability under both non‑infected and virus‑infected conditions.
Conclusions:
Overall, the results indicate that the endophytic fungus S. indica enhances tomato tolerance to viral infection through the modulation of oxidative stress and activation of plant defense mechanisms. Colonization by S. indica reduced the accumulation of reactive oxygen species and cellular damage while increasing antioxidant enzyme activities and protective metabolites such as phenolics, soluble sugars, and proteins. These responses improved cellular stability and supported better physiological performance under viral stress. Therefore, S. indica can be considered a promising biological agent for the management of viral diseases and for promoting sustainable agricultural practices.

کلیدواژه‌ها English

biotic stresses
biomass
tomato
endophytic fungi
Akbar, M. U., Aqeel, M., Shah, M. S., Jeelani, G., Iqbal, N., Latif, A. and Noman, A. (2023). Molecular regulation of antioxidants and secondary metabolites act in conjunction to defend plants against pathogenic infection. South African Journal of Botany, 161, 247-257. https://doi.org/10.1016/j.sajb.2023.08.028.
Almasi, R., Roumi, V., Pakbaz, S. and Sedaghatian, H. (2025). Effect of Gigaspora margarita on tomato–ToMV interaction. Genetic Engineering and Biosafety Journal, 13(2), 277-289.
Anwaar, H.A., Perveen, R., Mansha, M.Z., Aatif, H.M., Sarwar, Z.M., ud din Umar, U., Hanif, C.M.S., Sajid, M., Rehman, A.U., Alam, M.M. and Shafique, M.S. (2019). Potential of Fungal Endophytes to Antagonise puccinia Striiformis Causing Wheat Yellow Rust (preprint).
Arnon, A. N. (1949). Method of extraction of chlorophyll in the plants. Agronomy Journal, 23, 112-121.
Aseel, D. G., Rashad, Y. M. and Hammad, S. M. (2019). Arbuscular mycorrhizal fungi trigger transcriptional expression of flavonoid and chlorogenic acid biosynthetic pathways genes in tomato against Tomato Mosaic Virus. Scientific reports, 9(1), 9692.
Atkinson, N. J. and Urwin, P. E. (2012). The interaction of plant biotic and abiotic stresses: from genes to the field. Journal of Experimental Botany, 63 (10): 3523–3543. https://doi.org/10.1093/jxb/ers100
Bates, L. S., Waldren, R. A. and Teare, I. D. (1973) Rapid determination of free proline for water-stress studies. Plant and Soil, 39, 205-207. https://doi.org/10.1007/BF00018060
Batool, A., Wang, C., Xia, Y., Xiao, L., Ahmad, J., Liu, L. and Chen, C. (2025). Transcriptional profiles of endophyte Serendipita indica associated with plant growth improvement in watermelon. BMC Plant Biology, 25, 1776. https://doi.org/10.1186/s12870-025-07659-4.
Bergmeyer, H. U. (1970) Standardization of methods for estimation of enzyme activity in biological fluids. Journal of Clinical Chemistry and Clinical Biochemistry, 8, 658-660. https://cir.nii.ac.jp/crid/1570854174602617472
Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Chandran, K., Sreeja, S. J. and Johnson, J. M. (2021). Beneficial root endophytic fungus Piriformospora indica inhibits the infection of Blackeye cowpea mosaic virus in yard long bean with enhanced growth promotion. Journal of Tropical Agriculture, 59(1).
Culver, J. and Padmanabhan, M. (2007). Virus-induced disease: Altering host physiology one interaction at a time. Annual Review of Phytopathology, 45, 221–243. doi.org/10.1146/annurev.phyto.45.062806.094422
Ding, A., Ahsan, T., Han, D., Wang, C., Du, S., Wang, W. and Zhang, S. (2025). Root colonization by Serendipita indica triggers resistance against stem rot in Arachis hypogaea L. World Journal of Microbiology and Biotechnology, 41(11), 1-18. https://doi.org/10.1007/s11274-025-04604-3.
Elsharkawy, M.M., El-Okkiah, S., Elsadany, A.Y., Bedier, M.Y., Omara, R.I., Behiry, S.I., Hassan, S. and Abdelkhalek, A. (2022). Systemic resistance induction of tomato plants against tomato mosaic virus by microalgae. Egyptian Journal of Biological Pest Control, 32, 37. doi.org/10.1186/s41938-022-00538-2.
Ershadi, A., Karimi, R,. and Naderi Mahdei, K. (2016). Freezing tolerance and its relationship with soluble carbohydrates, proline and water content in 12 grapevine cultivars. Acta Physiologiae Plantarum, 38(1): 1-10. https://doi.org/10.1007/s11738-015-2021-6
Fakhro, A., Andrade-Linares, D. R., von Bargen, S., Bandte, M., Büttner, C., Grosch, R. and Franken, P. (2010). Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza, 20(3), 191-200. https://doi.org/10.1007/s00572-009-0279-5
Ghabooli, M. and Kaboosi, E. (2022). Alleviation of the adverse effects of drought stress using a desert adapted endophytic fungus and glucose in tomato. Rhizosphere, 21, 100481. https://doi.org/10.1016/j.rhisph.2022.100481
Ghabooli, M., Khatabi, B., Ahmadi, F. S., Sepehri, M., Mirzaei, M., Amirkhani, A., Jorrín-Novo, J. V. and Salekdeh, G. H. (2013) Proteomics study reveals the molecular mechanisms underlying water stress tolerance induced by Piriformospora indica in barley. Journal of Proteomics, 94, 289-301. https://doi.org/10.1016/j.jprot.2013.09.017
Ghabooli, M., Rezaei, E., Movahedi, Z. and Mohsenifard, E. (2020). Effect of Piriformospora indica inoculation on some morphophysiological parameters in licorice (Glycyrrhiza glabra L.) under drought stress. Iranian Journal of Plant Physiology, 10(4), 3379-3389. https://dx.doi.org/10.30495/ijpp.2020.677198
Hemeda, H. M. and Klein, B. P. (1990) Effects of naturally occurring antioxidants on peroxidase activity of vegetable extracts. Journal of Food Science, 55(1), 184-185. https://doi.org/10.1111/j.1365-2621.1990.tb06048.x
Huang, Y., Li, J., Nong, C., Lin, T., Fang, L., Feng, X. and Miao, L. (2024). Piriformospora indica enhances resistance to fusarium wilt in strawberry by increasing the activity of superoxide dismutase, peroxidase, and catalase, while reducing the content of malondialdehyde in the roots. Horticulturae, 10(3), 240.
Huseynova, I. M., Mirzayeva, S. M., Sultanova, N. F., Aliyeva, D. R., Mustafayev, N. S. and Aliyev, J. A. (2018). Virus-induced changes in photosynthetic parameters and peroxidase isoenzyme contents in tomato (Solanum lycopersicum L.) plants. Photosynthetica, 56(3), 841-850. https://doi.org/10.1007/s11099-017-0737-9.
Irigoyen, J., Einerich, D. and Sánchez‐Díaz, M. (1992). Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiologia Plantarum, 84(1), 55-60. https://doi.org/10.1034/j.1399-3054.1992.840109.x
Jiang, T., Hao, T., Chen, W., Li, C., Pang, S., Fu, C., Cheng, J., Zhang, C., Ghorbanpour, M. and Miao, S. (2025). Reprogrammed Plant Metabolism During Viral Infections: Mechanisms, Pathways and Implications. Molecular Plant Pathology, 26(2), e70066. https://doi.org/10.1111/mpp.70066
Kaboosi, E., Ghabooli, M. and Karimi, R. (2022). Piriformospora indica inoculants enhance flowering, yield, and physiological characteristics of tomato (Lycopersicon esculentum) in different growth phases. Iranian Journal of Plant Physiology, 12(3), 4183-4194. https://doi.org/10.30495/ijpp.2021.1923991.1302
Kaboosi, E., Ghabooli, M. and Karimi, R. (2023). Combined effect of trehalose and Serendipita indica inoculation might participate in Solanum lycopersicum induced cold tolerance. Current Microbiology, 80(7), 224. https://doi.org/10.1007/s00284-023-03326-9
Kirnak, H., Kaya, C., Tas, I. and Higgs, D. (2001). The influence of water deficit on vegetative growth, physiology, fruit yield and quality in eggplants. Bulg. Journal of Plant Physiology, 27(3-4), 34-46.
Kumar, S., Udaya Shankar, A. C., Nayaka, S. C., Lund, O. S. and Prakash, H. S. (2011). Detection of Tobacco mosaic virus and Tomato mosaic virus in pepper and tomato by multiplex RT–PCR. Letters in Applied Microbiology, 53(3), 359-363.
Kumar, M., Yadav, V., Tuteja, N. and Johri, A. K. (2009). Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology (Reading, England), 155(Pt 3), 780–790. https://doi.org/10.1099/mic.0.019869-0
Lee, Y. C., Johnson, J. M., Chien, C. T., Sun, C., Cai, D., Lou, B. and Yeh, K. W. (2011). Growth promotion of Chinese cabbage and Arabidopsis by Piriformospora indica is not stimulated by mycelium-synthesized auxin. Molecular plant-microbe interactions, 24(4), 421-431.
Li, L., Feng, Y., Qi, F. and Hao, R. (2023). Research progress of Piriformospora indica in improving plant growth and stress resistance to plant. Journal of Fungi, 9(10), 965.
Liang, S. M., Hashem, A., Fathi Abd_Allah, E. and Wu, Q. S. (2025). Transcriptomic analysis reveals potential roles of polyamine and proline metabolism in waterlogged peach roots inoculated with Funneliformis mosseae and Serendipita indica. Tree Physiology, 45(2), tpaf013.
Lin, C., Hu, W., Qin, X., Fei, Y. and Hu, D. (2025). Effects of Serendipita indica on the Morphological and Physiological Characteristics of Agrostis stolonifera L. Under Drought Stress. Agronomy, 15(1).
Llorens, E., Camañes, G., Lapeña, L. and García-Agustín, P. (2016). Priming by hexanoic acid induce activation of mevalonic and linolenic pathways and promotes the emission of plant volatiles. Frontiers in Plant Science, 7, 495. https://doi.org/10.3389/fpls.2016.00495
Miozzi, L., Catoni, M., Fiorilli, V., Mullineaux, P. M., Accotto, G.P. and Lanfranco, L. (2011). Arbuscular mycorrhizal symbiosis limits foliar transcriptional responses to viral infection and favors long-term virus accumulation. Molecular Plant-Microbe Interaction, 24, 1562–1572. doi: 10.1094/MPMI-05-11-0116
Mehri, M., Ghabooli, M. and Movahedi, Z. (2023) Contribution of Serendipita indica on growth improvement, antioxidative capacity of Dracocephalum kotschyi, and its resistance against cadmium stress. International Microbiology, 1-11. https://doi.org/10.1007/s10123-023-00339-z
Murphy, B. R., Doohan, F. M. and Hodkinson, T. R. (2014). Yield increase induced by the fungal root endophyte Piriformospora indica in barley grown at low temperature is nutrient limited. Symbiosis, 62(1), 29-39. https://doi.org/10.1007/s13199-014-0268-0
Nakano, Y. and Asada, K. (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidases in spinach chloroplasts. Plant Cell Physiology, 22, 867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Ogunwande, I.O. (2023). Measurement of Technical Efficiency and Value Addition of Hybrid Tomato Production Under Urban Homestead Farming in Southwest Nigeria. Tropentag 2023: Conference on International Research on Food Security, Natural Resource Management and Rural Development, Berlin, Germany, 20–22 September.
Pan, R., Xu, L., Wei, Q., Wu, C., Tang, W., Oelmüller, R. and Zhang, W. (2017). Piriformospora indica promotes early flowering in Arabidopsis through regulation of the photoperiod and gibberellin pathways. PLoS One, 12(12), e0189791. https://doi.org/10.1371/journal.pone.0189791
Pazarlar, S., Gumus, M. and Öztekin, G. B. (2013). The Effects of Tobacco mosaic virus Infection on Growth and Physiological Parameters in Some Pepper Varieties (Capsicum annuum L.). Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 41(2), 427–433. https://doi.org/10.15835/nbha4129008
Rahbari, A., Esmaielpour, B., Azarmi, R., Fatemi, H., Lajayer, H. M., Panahirad, S. and Vita, F. (2025). Symbiotic fungus serendipita indica as a natural bioenhancer against cadmium toxicity in chinese cabbage. Plants, 14(17), 2773.
Reinero, A. and Beachy, R.N. (1989). Reduced photosystem II activity and accumulation of viral coat protein in chloroplasts of leaves infected with tobacco mosaic virus. Plant Physiology, 89(1), 111-116.
Roylawar, P., Khandagale, K., Randive, P., Shinde, B., Murumkar, C., Ade, A., Singh, M., Gawande, S. and Morelli, M. (2021). Piriformospora indica primes onion response against stemphylium leaf blight disease. Pathogens, 10(9), 1085.
Saleem, S., Sekara, A. and Pokluda, R. (2022). Serendipita indica—A review from agricultural point of view. Plants, 11(24), 3417.
Saru, S. S. (2021). Evaluation of beneficial fungal root endophyte, Piriformospora indica for the management of Tomato leaf curl virus (Doctoral dissertation, Department of Plant Pathology, College of Agriculture, Vellayani).
Sedaghatian, H., Almasi, R., Pakbaz, S. and Roumi, V. (2024). Effects of a tripartite interaction among ToMV, tomato and Glomus fasciculatum. Genetic Engineering and Biosafety Journal, 13(1), 51-62.
Scalschi, L., Vicedo, B., Camañes, G., Fernandez-Crespo, E., Lapeña, L., González-Bosch, C. and García-Agustín, P. (2013). Hexanoic acid is a resistance inducer that protects tomato plants against Pseudomonas syringae by priming the jasmonic acid and salicylic acid pathways. Molecular Plant Pathology, 14(4), 342–355. https://doi.org/10.1111/mpp.12010
Siegel, A., Hari, V., Montgomery, I. and Kolacz, K. (1976). A messenger RNA for capsid protein isolated from tobacco mosaic virus-infected tissue. Virology, 73(2), 363-371.
Shen, G., Cao, H., Zeng, Q., Guo, X., Shao, H., Wang, H. and Zeng, L. (2025). Integrated physiological, transcriptomic, and metabolomic analysis reveals mechanism underlying the Serendipita indica-enhanced drought tolerance in tea plants. Plants, 14(7), 989.
Sofy, A. R., Sofy, M. R., Hmed, A. A., Dawoud, R. A., Alnaggar, A. E. A. M., Soliman, A. M. and El-Dougdoug, N. K. (2021). Ameliorating the adverse effects of tomato mosaic tobamovirus infecting tomato plants in Egypt by boosting immunity in tomato plants using zinc oxide nanoparticles. Molecules, 26(5), 1337.
Soosaar, J. L., Burch-Smith, T. M. and Dinesh-Kumar, S. P. (2005). Mechanisms of plant resistance to viruses. Nature Reviews Microbiology, 3(10), 789-798.
Su, Z. Z., Wang, T., Shrivastava, N., Chen, Y. Y., Liu, X., Sun, C. and Lou, B. G. (2017). Piriformospora indica promotes growth, seed yield and quality of Brassica napus L. Microbiological research, 199, 29-39. https://doi.org/10.1016/j.micres.2017.02.006.
Sun, C., Johnson, J. M., Cai, D., Sherameti, I., Oelmüller, R. and Lou, B. (2010). Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. Journal of plant physiology, 167(12), 1009–1017. https://doi.org/10.1016/j.jplph.2010.02.013
Teimory, H., Ghabooli, M., Movahedi, Z. (2021). Effects of different inoculation methods of Serendipita indica on some morphophysiological, biochemical, and yield traits of tomato under drought stress, Journal of Plant Biological Sciences, 13(2), 1-22. https://doi.org/10.22108/ijpb.2021.128853.1253 [In Persian].
Torres, M. A., Jones, J. D. and Dangl, J. L. (2006). Reactive oxygen species signaling in response to pathogens. Plant physiology, 141(2), 373-378.
Trzewik, A., Marasek-Ciolakowska, A. and Orlikowska, T. (2020). Protection of highbush blueberry plants against Phytophthora cinnamomi using Serendipita indica. Agronomy, 10(10), 1598.
Tyagi, J., Chaudhary, P., Mishra, A., Khatwani, M., Dey, S. and Varma, A. (2022). Role of endophytes in abiotic stress tolerance: with special emphasis on Serendipita indica. International Journal of Environmental Research, 16(4), 62. https://doi.org/10.1007/s41742-022-00439-0.
Velikova, V. and Loreto, F. (2005) On the relationship between isoprene emission and thermotolerance in Phragmites australis leaves exposed to high temperatures and during the recovery from a heat stress. Plant, Cell and Environment, 28(3), 318-327. https://doi.org/10.1111/j.1365-3040.2004.01314.x
Velioglu, Y., Mazza, G., Gao, L. and Oomah, B. D. (1998) Antioxidant activity and total phenolics in selected fruits, vegetables, and grain products. Journal of Agricultural and Food Chemistry, 46(10), 4113-4117. https://doi.org/10.1021/jf9801973
Wallis, C. M. and Galarneau, E. R. A. (2020). Phenolic compound induction in plant-microbe and plant-insect interactions: a meta-analysis. Frontiers in plant science, 11, 580753.
Wan, Y. X., Kapoor, R., da Silva, F. S. B., Abd-Allah, E. F., Kuča, K., Hashem, A. and Wu, Q. S. (2024). Elucidating the mechanism regarding enhanced tolerance in plants to abiotic stress by Serendipita indica. Plant Growth Regulation, 103(2), 271-281. https://doi.org/10.1007/s10725-024-01124-2.
Wang, F., Zeng, B., Sun, Z. and Zhu, C. (2009) Relationship between proline and Hg2+ induced oxidative stress in a tolerant rice mutant. Archives of Environmental Contamination and Toxicology, 56(4), 723. https://doi.org/10.1007/s007260170026
Wang, H., Zheng, J., Ren, X., Yu, T., Varma, A., Lou, B. and Zheng, X. (2015). Effects of Piriformospora indica on the growth, fruit quality and interaction with Tomato yellow leaf curl virus in tomato cultivars susceptible and resistant to TYCLV. Plant Growth Regulation, 76, 303-313. https://doi.org/10.1007/s10725-015-0025-2.
Xu, L., Wu, C., Oelmüller, R. and Zhang, W. (2018). Role of phytohormones in Piriformospora indica-induced growth promotion and stress tolerance in plan