Фізіологія рослин і генетика 2026, том 58, № 4, 355-368, doi:

Вплив триходерми і ризобій на параметри росту та формування симбіотичного апарату в рослин люцерни за умов засолення

Михалків Л.М., Коць С.Я., Омельчук С.В., Мокрицький К.А.

Ключові слова: Medicago sativa L., Trichoderma lignorum, Sinorhizobium meliloti, growth, weight, nodules, salinity, sаlt toleranc

Фізіологія рослин і генетика
2026, том 58, № 4, 355-368

Повний текст та додаткові матеріали

Цитована література

 1. Zhou H., Shi H., Yang Y., Feng X., Chen X., Xiao F., Lin H., Guo Y. Insights into plant salt stress signaling and tolerance. J. Genet. Genom. 2024. 51 (1). Р. 16—34. https://doi.org/10.1016/j.jgg.2023.08.007

 2. Irshad A., Rehman R.N.U., Abrar M.M., Saeed Q., Sharif R., Hu T. Contribution of rhizobium-legume symbiosis in salt stress tolerance in Medicago truncatula evaluated through photosynthesis, antioxidant exymes, and compatible solutes accumulation. Sustanainability. 2021. 13(6). 3366. https://doi.org/10.3390/su13063369

 3. Коць С.Я., Михалків Л.М., Мельникова Н.М., Мокрицький К.А. Формування і функціонування симбіотичних систем люцерни з різними штамами синоризобій під впливом засолення. Тернопільські біологічні читання — Ternopil Bioscience — 2024: Матеріали Міжнар. наук.-практ. конф. (Тернопіль, 18—19 квітня 2024). Тернопіль: Вектор, 2024. C. 59—62.

 4. Zhang S., Gan Y., Xu B. Application of plant-growth-promoting fungi Trichoderma longibrachiatum T6 enhances tolerance of wheat to salt stress through improvement of antioxidative defense system and gene expression. Front. Plant Sci. 2016. 7. 1405. https://doi.org/10.3389/fpls.2016.01405

 5. Poveda J. Trichoderma parareesei favors the tolerance of rapeseed (Brassica napus L.) to salinity and drought due to a chorismate mutase. Agronomy. 2020. 10. 116. https://doi.org/10.3390/agronomy10010118

 6. Adusumilli N., Kolli S.Ch. Management of salinity stress by the application of Trichoderma. Advances in trichoderma biology for agricultural applications. Springer, 2022. Р. 303—320. https://doi.org/10.1007/978-3-030-91650-3_11

 7. Gao P., Li Y., Guo Y., Duan T. Co-inoculation of lucerne (Medicago sativa) with an AM fungus and a rhizobium reduces occurrence of spring black stem and leaf spot caused by Phoma medicaginis. Crop Pasture Sci. 2018. 69 (9). Р. 933—943. https://doi.org/ 10.1071/CP18135

 8. Gao H., Yang D., Yang L., Han S., Liu G., Tang L., Chen J., Wang D., Guo C. Co-inoculation with Sinorhizobium meliloti and Enterobacter ludwigii improves the yield, nodulation, and quality of alfalfa (Medicago sativa L.) under saline-alkali environments. Ind. Crops Prod. 2023. 199. 116818. https://doi.org/10.1016/j.indcrop.2023.116818

 9. Barbosa J.Z., Hungria M., da Silva Sena J.V., Poggere G., dos Reis A.R., CorrГa R.S. Meta-analysis reveals benefits of co-inoculation of soybean with Azospirillum brasilense and Bradyrhizobium spp. in Brazil. Appl. Soil Ecol. 2021. 163. 103913. https://doi.org/10.1016/j.apsoil.2021.103913

10. Kumar S., Pandey S., Rathore U.S., Kumar K. Multi-trait Trichoderma for improving plant health of grain legumes. Microbial Mitigation of Stress Response of Food Legumes. CRC Press, 2020. Р. 85—102. https://doi.org/10.1201/9781003028413-8

11. Nirmalkar V.К., Singh S., Tiwari R.S., Said P.P., Kaushik D.K. Field Efficacy of Trichoderma harzianum and Rhizobium against Wilt Complex of Chickpea. Int. J. Curr. Microbiol. Appl. Sci. 2017. 6 (7). Р. 1421—1429. https://doi.org/10.20546/ijcmas.2017. 607.170

12. Neelipally R.T.K.R., Anoruo A.O., Nelson S. Effect of сo-inoculation of Bradyrhizobium and Trichoderma on growth, development, and yield of Arachis hypogaea L. (Peanut). Agronomy. 2020. 10 (9). 1415. https://doi.org/10.3390/agronomy10091415

13. Poveda J., Eugui D. Combined use of Trichoderma and beneficial bacteria (mainly Bacillus and Pseudomonas): Development of microbial synergistic bio-inoculants in sustainable agriculture. Biol. Control. 2022. 176. 105100. https://doi.org/10.1016/j.biocontrol.2022.105100

14. Barbosa J.Z., Hungria M., Prior S.A., Moura M.C., Poggere G., Motta A.C.V. Improving yield and health of legume crops via co-inoculation with rhizobia and Trichoderma: A global meta-analysis. Appl. Soil Ecol. 2022. 176. 1044933. https://doi.org/10.1016/j.apsoil.2022.104493

15. Пюрко О.Є., Мусієнко М.М., Казаков Є.О., Христова Т.Є. Основи солестійкості рослин та методи її вивчення. Вісник ЗДУ. 2001, № 1. С. 1—5.

16. Tyshchenko A.V., Tyshchenko O.D., Koblay O.O. The importance of the root system in the manifestation of adaptability to abiotic stress factors. Climate-smart agriculture: science and practice. Riga, Latvia: Baltija Publishing, 2023. Р. 256—289. https://doi.org/ 10.30525/978-9934-26-389-7-14

17. Li L., Peng Z., Mao X., Wang J., Chang X., Reynolds M., Jing R. Genome-wide association study reveals genomic regions controlling root and shoot traits at late growth stages in wheat. Ann. Bot. 2019. 124. Р. 993—1006. https://doi.org/10.1093/aob/ mcz041

18. Bl«ha L. Importance of root-shoot ratio for crops production. J. Agron. Agric. Sci. 2019. 2. 12. https://doi.org/10.24966/AAS-8292/100012

19. Ѓgren G.I., Ingestad T. Root:Shoot ratio as a balance between nitrogen productivity and photosynthesis. Plant Cell Environ. 2006. 10 (7). Р. 579—586. https://doi.org/10.1111/ 1365-3040.ep11604105

20. Brooker R., Brown L.K., George T.S., Pakeman R.J., Palmer S., Ramsay L., SchШb C., Schurch N., Wilkinson M.J. Active and adaptive plasticity in a changing climate. Trends Plant Sci. 2022. 27(7). Р. 717—728. https://doi.org/10.1016/j.tplants. 2022.02.004

21. Conteras-Cornejo H.A., Macias-Rodrigues L., del-Val E., Larsen J. Ecological functions of Trichoderma spp. and their secondary metabolites in the rhizosphere: interactions with plants. FEMS Microbiol. Ecol. 2016. 92 (4). fiw036. https://doi.org/10.1093/femsec/ fiw036

22. Manganiello G., Sacco A., Ercolano M.R., Vinale F., Lanzuise S., Pascale A., Napolitano M., Lombardi N., Lorito M., Woo S.L. Modulation of tomato response to Rhizoctonia solani by Trichoderma harzianum and its secondary metabolite harzianic acid. Front. Microbiol. 2018. 9. 1966. https://doi.org/10.3389/fmicb. 2018.01966

23. Vicente I., Baroncelli R., Hermosa R., Monte E., Vannacci G., Sarrocco S. Role and genetic basis of specialised secondary metabolites in Trichoderma ecophysiology. Fungal Biol. Rev. 2022. 39. Р. 83—99. https://doi.org/10.1016/j.fbr.2021.12.004

24. Vaccaro F., Bettini P.P., Courty P-E., Mengoni A., Passeri I., Sarrocco C., Fagorzi C. Toward deciphering the molecular dialogue in the rhizomicrobiota: Transcriptomic profiling of Trichoderma in rhizobia interaction. Microbiol. Res. 2025. 297. 128180. https://doi.org/10.1016/j.micres.2025.128180

25. Mahapatra S., Das T., Das S. In vitro сompatibility study between the Rhizobium and native Trichoderma isolates from Lentil rhizospheric soil. Int. J. Curr. Microbiol. Appl. Sci. 2017. 8 (6). P. 1757—1769. https://doi.org/10.20546/ijcmas.2017.608.208

26. Vaccaro F., Passeri I., Ajijah N., Bettini P., Courty P.E., DДbiec-Andrzejewska K., Joshi N., Kowalewska ˜., Stasiuk R., MusiaУowski M., Pranaw K., Mengoni A. Genotype-by-genotype interkingdom cross-talk between symbiotic nitrogen fixing Sinorhizobium meliloti strains and Trichoderma species. Microbiol. Res. 2024. 285. 127768. https://doi.org/10.1016/j.micres.2024.127768

27. Bѕcquer C.J., Lazarovits G., Lalin I. In vitro interaction between Trichoderma harzianum and plant growth promoter rhizosphere bacteria. CJAS. 2013. 47(1). P. 97—102.

28. Maingi G. Effect of Trichoderma asperellum on growth of Rhizobium leguminosarum in vitro. G.J.B.A.H.S. 2016. 5(1). P. 43—48.

29. Scudeletti D., Crusciol C.A.C., Bossolani J.W., Moretti L.G., Momesso L., TubaФa B.S., de Castro S.G.Q., De Oliveira E.F., Hungria M. Trichoderma asperellum inoculation as a tool for attenuating drought stress in Sugarcane. Front. Plant Sci. 2021. 12. 645542. https://doi.org/10.3389/fpls.2021.645542

30. Shwerif N. Role of Trichoderma and Sinorhizobium strains for improving growth and nutritional status of alfalfa under Cd stress. IJEAB. 2018. 3(1). P. 33—48. https://doi.org/10.22161/ijeab/3.1.6

REFERENCES

 1. Zhou, H., Shi, H., Yang, Y., Feng, X., Chen, X., Xiao, F., Lin, H. & Guo, Y. (2024). Insights into plant salt stress signaling and tolerance. J. Genet. Genom., 51(1), pp. 16-34. https://doi.org/10.1016/j.jgg.2023.08.007

 2. Irshad, A., Rehman, R.N.U., Abrar, M.M., Saeed, Q., Sharif, R. & Hu, T. (2021). Contribution of rhizobium-legume symbiosis in salt stress tolerance in Medicago truncatula evaluated through photosynthesis, antioxidant exymes, and compatible solutes accumulation. Sustanainability, 13(6), 3366. https://doi.org/10.3390/su13063369

 3. Kots, S.Ya, Mykhalkiv, L.M., Melnykova, N.M. & Mokrytskyi, K.A. (2024, April). Forming and functioning of alfalfa symbiotic systems with different synorhizobium strains under influence of salinity. Materials of International Scientific and Practical Conference «Ternopilski biologichni chytannya — Ternopil Bioscience — 2024» (pp. 59-62), Ternopil [in Ukrainian].

 4. Zhang, S., Gan, Y. & Xu, B. (2016). Application of plant-growth-promoting fungi Trichoderma longibrachiatum T6 enhances tolerance of wheat to salt stress through improvement of antioxidative defense system and gene expression. Front. Plant Sci.,7, 1405. https://doi.org/10.3389/fpls.2016.01405

 5. Poveda, J. (2020). Trichoderma parareesei favors the tolerance of rapeseed (Brassica napus L.) to salinity and drought due to a chorismate mutase. Agronomy, 10, 116. https://doi.org/10.3390/agronomy10010118

 6. Adusumilli, N. & Kolli, S.Ch. (2022). Management of salinity stress by the application of Trichoderma. In: Advances in trichoderma biology for agricultural applications (pp. 303-320). Springer. https://doi.org/10.1007/978-3-030-91650-3_11

 7. Gao, P., Li, Y., Guo, Y. & Duan, T. (2018). Co-inoculation of lucerne (Medicago sativa) with an AM fungus and a rhizobium reduces occurrence of spring black stem and leaf spot caused by Phoma medicaginis. Crop Pasture Sci., 69(9), pp. 933-943. https://doi.org/10.1071/CP18135

 8. Gao, H., Yang, D., Yang, L., Han, S., Liu, G., Tang, L., Chen, J., Wang, D. & Guo, C. (2023). Co-inoculation with Sinorhizobium meliloti and Enterobacter ludwigii improves the yield, nodulation, and quality of alfalfa (Medicago sativa L.) under saline-alkali environments. Ind. Crops Prod., 199, 116818. https://doi.org/10.1016/j.indcrop.2023.116818

 9. Barbosa, J.Z., Hungria, M., da Silva Sena, J.V., Poggere, G., dos Reis, A.R. & CorrГa, R.S. (2021). Meta-analysis reveals benefits of co-inoculation of soybean with Azospirillum brasilense and Bradyrhizobium spp. in Brazil. Appl. Soil Ecol., 163, 103913. https://doi.org/10.1016/j.apsoil.2021.103913

10. Kumar, S., Pandey, S., Rathore, U.S. & Kumar, K. (2020). Multi-trait Trichoderma for improving plant health of grain legumes. In: N. Amaresan et al. (Eds.), Microbial Mitigation of Stress Response of Food Legumes. (pp. 85-102). CRC Press. https://doi.org/10.1201/9781003028413-8

11. Nirmalkar, V.К., Singh, S., Tiwari, R.S., Said, P.P. & Kaushik, D.K. (2017). Field Efficacy of Trichoderma harzianum and Rhizobium against Wilt Complex of Chickpea. Int. J. Curr. Microbiol. App. Sci., 6(7), pp. 1421-1429. https://doi.org/10.20546/ijcmas.2017.607.170

12. Neelipally, R.T.K.R., Anoruo, A.O. & Nelson, S. (2020). Effect of Co-Inoculation of Bradyrhizobium and Trichoderma on Growth, Development, and Yield of Arachis hypogaea L. (Peanut). Agronomy, 10(9), 1415. https://doi.org/10.3390/agronomy10091415

13. Poveda, J. & Eugui, D. (2022). Combined use of Trichoderma and beneficial bacteria (mainly Bacillus and Pseudomonas): Development of microbial synergistic bio-inoculants in sustainable agriculture. Biol. Control., 176, 105100. https://doi.org/10.1016/ j.biocontrol.2022.105100

14. Barbosa, J.Z., Hungria, M., Prior, S.A., Moura, M.C., Poggere, G. & Motta, A.C.V. (2022). Improving yield and health of legume crops via co-inoculation with rhizobia and Trichoderma: A global meta-analysis. Appl. Soil Ecol., 176, 1044933. https://doi.org/ 10.1016/j.apsoil.2022.104493

15. Pyurko O.Ye., Musiyenko, M.M., Kazakov, Ye.O. & Hrystova, T.Ye. (2001). Basics of salt resistance of plants and methods of its study. Bulletin of Zaporizhzhіa National University, 1, pp. 1-5 [in Ukrainian]

16. Tyshchenko, A.V., Tyshchenko, O.D. & Koblay, O.O. (2023). The importance of the root system in the manifestation of adaptability to abiotic stress factors. In: Climate-smart agriculture: science and practice (pp. 256-289). Riga, Latvia: Baltija Publishing. https://doi.org/10.30525/978-9934-26-389-7-14

17. Li, L., Peng, Z., Mao, X., Wang, J., Chang, X., Reynolds, M. & Jing, R. (2019). Genome-wide association study reveals genomic regions controlling root and shoot traits at late growth stages in wheat. Ann. Bot., 124, pp. 993-1006. https://doi.org/10.1093/ aob/mcz041

18. Bl«ha, L. (2019). Importance of root-shoot ratio for crops production. J. Agron. Agric. Sci., 2, 12. https://doi.org/10.24966/AAS-8292/100012

19. Ѓgren, G.I., Ingestad, T. (2006). Root:Shoot ratio as a balance between nitrogen productivity and photosynthesis. Plant Cell Environ., 10(7), pp. 579-586. https://doi.org/ 10.1111/1365-3040.ep11604105

20. Brooker, R., Brown, L.K., George, T.S., Pakeman, R.J., Palmer, S., Ramsay, L., SchШb, C., Schurch, N. & Wilkinson, M.J. (2022). Active and adaptive plasticity in a changing climate. Trends Plant Sci., 27(7), pp. 717-728. https://doi.org/10.1016/j.tplants. 2022.02.004

21. Conteras-Cornejo, H.A., Macias-Rodrigues, L., del-Val, E. & Larsen, J. (2016). Ecological functions of Trichoderma spp. and their secondary metabolites in the rhizosphere: interactions with plants. FEMS Microbiol. Ecol., 92(4), fiw036. https://doi.org/ 10.1093/femsec/fiw036

22. Manganiello, G., Sacco, A., Ercolano, M.R., Vinale, F., Lanzuise, S., Pascale, A., Napolitano, M., Lombardi, N., Lorito, M. & Woo, S.L. (2018). Modulation of tomato response to Rhizoctonia solani by Trichoderma harzianum and its secondary metabolite harzianic acid. Front. Microbiol., 9, 1966. https://doi.org/10.3389/fmicb.2018.01966

23. Vicente, I., Baroncelli, R., Hermosa, R., Monte, E., Vannacci, G. & Sarrocco, S. (2022). Role and genetic basis of specialised secondary metabolites in Trichoderma ecophysiology. Fungal Biol. Rev., 39, pp. 83-99. https://doi.org/10.1016/j.fbr.2021.12.004

24. Vaccaro, F., Bettini, P.P., Courty, P-E., Mengoni, A., Passeri, I., Sarrocco, C. & Fagorzi, C. (2025). Toward deciphering the molecular dialogue in the rhizomicrobiota: Transcriptomic profiling of Trichoderma in rhizobia interaction. Microbiol. Res., 297, 128180. https://doi.org/10.1016/j.micres.2025.128180

25. Mahapatra, S., Das, T. & Das, S. (2017). In vitro сompatibility ыtudy between the Rhizobium and native Trichoderma isolates from Lentil rhizospheric soil. Int. J. Curr. Microbiol. Appl. Sci., 8(6), pp. 1757-1769. https://doi.org/10.20546/ijcmas.2017.608.208

26. Vaccaro, F., Passeri, I., Ajijah, N., Bettini, P., Courty, P.E., DДbiec-Andrzejewska, K., Joshi, N., Kowalewska, ˜., Stasiuk, R., MusiaУowski, M., Pranaw, K. & Mengoni, A. (2024). Genotype-by-genotype interkingdom cross-talk between symbiotic nitrogen fixing Sinorhizobium meliloti strains and Trichoderma species. Microbiol. Res., 285, 127768. https://doi.org/10.1016/j.micres.2024.127768

27. Bѕcquer, C.J., Lazarovits, G. & Lalin, I. (2013). In vitro interaction between Trichoderma harzianum and plant growth promoter rhizosphere bacteria. CJAS, 47(1), pp. 97-102.

28. Maingi, G. (2016). Effect of Trichoderma asperellum on growth of Rhizobium leguminosarum in vitro. G.J.B.A.H.S., 5(1), pp. 43-48.

29. Scudeletti, D., Crusciol, C.A.C., Bossolani, J.W., Moretti, L.G., Momesso, L., TubaФa, B.S., de Castro, S.G.Q., De Oliveira, E.F. & Hungria, M. (2021). Trichoderma asperellum inoculation as a tool for attenuating drought stress in Sugarcane. Front. Plant Sci., 12, 645542. https://doi.org/10.3389/fpls.2021.645542

30. Shwerif, N. (2018). Role of Trichoderma and Sinorhizobium strains for improving growth and nutritional status of alfalfa under Cd stress. IJEAB, 3(1), pp. 33-48. https://doi.org/10.22161/ijeab/3.1.6