Биоконтрольные свойства ризобий в отношении вредных организмов: механизмы действия, спектр активности, эффективность (обзор)

Исследование проводили с целью поиска и анализа данных о биоконтрольных свойствах ризобий и эффективности их применения при подавлении возбудителей заболеваний. Проанализированы 118 источников за 1984–2024 гг. из баз Scopus, Web of Science и российского индекса научного цитирования по ключевым словам: биологический контроль, биоконтроль ризобий, болезни растений, антагонистическая активность ризобий, антифунгальная активность, бактерицидная активность, нематицидная активность, производство антибиотиков и ферментов, бактериоцины, индуцированная системная резистентность, ризобии в защите растений. Ризобии часто показывают высокую или среднюю эффективность в биоконтроле как на бобовых, так и небобовых культурах при сдерживании развития фитопатогенных грибов и бактерий, а также фитопаразитических нематод. Ризобии могут осуществлять прямой или опосредованный биоконтроль. Прямое воздействие заключается в непосредственном подавлении вредных организмов благодаря синтезу широкого спектра соединений, включая бактериоцины, сидерофоры, гидролитические ферменты. Обнаружено свойство ризобий нарушать чувство кворума фитопатогенных бактерий, снижая их патогенность и вредоносность. Прямой антагонизм, исследуемый в двойных культурах in vitro, может не проявляться, тогда как использование тех же штаммов ризобий на растениях может эффективно снижать заболеваемость путем опосредованного действия в системе ризобии-растение-вредный агент. Такой биоконтроль подразумевает запуск экспрессии защитных генов растений и индукцию системной устойчивости растений, что приводит к синтезу фитогормонов, фитоалексинов и защитных ферментов, ответственных за снижение заболеваемости. Комбинация азотфиксирующих ризобий с другими PGPR-агентами позволяет повысить продуктивность бобовых культур благодаря расширению спектра полезных функций микроорганизмов, включая усвоение питательных веществ и защиту от болезней. Использование возможностей клубеньковых бактерий контролировать вредные организмы позволит идентифицировать максимально эффективные природные штаммы и расширить потенциальную функциональность уже разработанных коммерческих инокулянтов.

1. Bacterial and fungal biocontrol agents for plant disease protection: Journey from lab to field, current status, challenges, and global perspectives / M. Ayaz, C.-H. Li, Q. Ali, et al. // Molecules. 2023 Vol. 28 Article 6735 URL: https://www.mdpi.com/1420-3049/28/18/6735 (дата обращения: 30.05.2024).

2. Legume bioactive compounds: Influence of rhizobial inoculation / L. R. Silva, C. Bento, A. C. Goncalves, et al. // AIMS Microbiol. 2017 Vol. 3 No. 2 P. 267–278. doi: 10.3934/microbiol.2017.2.267.

3. O’Callaghan M., Ballard R. A., Wright D. Soil microbial inoculants for sustainable agriculture: Limitations and opportunities // Soil Use and Management. 2022 Vol. 38 P. 1340–1369. doi: 10.1111/sum.12811.

4. Induced systemic resistance-like responses elicited by rhizobia / M. L. Tonelli, M. S. Figueredo, J. Rodriguez, et al. // Plant and Soil. 2020 Vol. 448 P. 1–14. URL: https://link.springer.com/article/10.1007/s11104-020-04423-5 (дата обращения: 15.05.2024).

5. Bacteria as biological control agents of plant diseases / A. Bonaterra, E. Badosa, N. Daranas, et al. // Microorganisms. 2022 Vol. 10 No. 9 Article 1759 URL: https://www.mdpi.com/2076-2607/10/9/1759 (дата обращения: 26.01.2024).

6. Plant growth promoting rhizobia: challenges and opportunities / S. Gopalakrishnan, A. Sathya, R. Vijayabharathi, et al. // 3 Biotech. 2015 Vol. 5 P. 355–377. doi: 10.1007/s13205-014-0241-x.

7. Major biological control strategies for plant pathogens / M. A. Pandit, J. Kumar, S. Gulati, et al. // Pathogens. 2022 Vol. 11 No. 2 Article 273 URL: https://www.mdpi.com/2076-0817/11/2/273 (дата обращения: 11.02.2024).

8. Kohl J., Kolnaar R., Ravensberg W. J. Mode of action of microbial biological control agents against plant diseases: Relevance beyond efficacy // Front. Plant Sci. 2019 Vol. 10 Article 845 URL: https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2019.00845/full (дата обращения: 15.03.2024).

9. Koul B., Chopra M., Lamba S. Microorganisms as biocontrol agents for sustainable agriculture // Relationship between microbes and the environment for sustainable ecosystem services. Elsevier, 2022 377 p. doi: 10.1016/B978-0-323-89938-3.00003-7.

10. Tabande L., Naseri B. How strongly is rhizobial nodulation associated with bean cropping system? // Journal of Plant Protection Research. 2020 Vol. 60 No. 2 P. 176–184. doi: 10.24425/jppr.2020.133307.

11. Rhizobia: a promising source of plant growth-promoting molecules and their non-legume interactions: examining applications and mechanisms / S. Fahde, S. Boughribil, B. Sijilmassi, et al. // Agriculture. 2023 Vol. 13 Article 1279 URL: https://www.mdpi.com/2077-0472/13/7/1279 (дата обращения: 11.02.2024).

12. Kebede E. Competency of rhizobial inoculation in sustainable agricultural production and biocontrol of plant diseases // Front. Sustain. Food Syst. 2021 Vol. 5 Article 728014 URL: https://www.frontiersin.org/journals/sustainable-food-systems/articles/10.3389/fsufs.2021.728014/full (дата обращения: 06.03.2024).

13. Biological control of plant pathogens: A global perspective / R. Lahlali, S. Ezrari, N. Radouane, et al. // Microorganisms. 2022 Vol. 10 No. 3 Article 596 URL: https://www.mdpi.com/2076-2607/10/3/596 (дата обращения: 07.03.2024).

14. Timofeeva A. M., Galyamova M. R., Sedykh S. E. Bacterial siderophores: Classification, biosynthesis, perspectives of use in agriculture // Plants. 2022 Vol. 11 No. 22 Article 3065 URL: https://www.mdpi.com/2223-7747/11/22/3065 (дата обращения: 22.03.2024).

15. Potential of rhizobia in improving nitrogen fixation and yields of legumes / Y. Mabrouk, I. Hemissi, I. B. Salem, et al. // Symbiosis. InTech. 2018 URL: https://www.intechopen.com/chapters/59280 (дата обращения: 22.03.2024). doi: 10.5772/intechopen.73495.

16. Characterization of soybean chitinase genes induced by rhizobacteria involved in the defense against Fusarium oxysporum / J.-Y. Chen, H. Sang, M. I. Chilvers, et al. // Front. Plant Sci. 2024 Vol. 15 Article 1341181 URL: https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2024.1341181/full (дата обращения: 25.04.2024).

17. Goyal R. K., Habtewold J. Z. Evaluation of legume–rhizobial symbiotic interactions beyond nitrogen fixation that help the host survival and diversification in hostile environments // Microorganisms. 2023 Vol. 11 Article 1454 URL: https://www.mdpi.com/2076-2607/11/6/1454 (дата обращения: 21.02.2024).

18. Biocontrol of three severe diseases in soybean / S.-F. Yu, C.-L. Wang, Y.-F. Hu, et al. // Agriculture. 2022 Vol. 12 No. 9 Article 1391 URL: https://www.mdpi.com/2077-0472/12/9/1391 (дата обращения: 23.02.2024).

19. Lipopolysaccharides of Rhizobium etli strain G12 act in potato roots as an inducing agent of systemic resistance to infection by the cyst nematode Globodera pallida / M. Reitz, K. Rudolph, I. Schroder, et al. // Applied and Environmental Microbiology. 2000 Vol. 66 No. 8 P. 3515–3518. doi: 10.1128/AEM.66.8.3515-3518.2000.

20. Diaz-Valle A., Lopez-Calleja A. C., Alvarez-Venegas R. Enhancement of pathogen resistance in common bean plants by inoculation with Rhizobium etli // Front. Plant Sci. 2019 Vol. 10 Article 1317 URL: https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2019.01317/full (дата обращения: 07.03.2024).

21. Rhizobia protect their legume hosts against soil-borne microbial antagonists in a host-genotype-dependent manner / C. N. Jack, K. J. Wozniak, S. S. Porter, et al. // Rhizosphere. 2019 Vol. 9 P. 47–55. doi: 10.1016/j.rhisph.2018.11.005.

22. Lindstrom K., Mousavi S. A. Effectiveness of nitrogen fixation in rhizobia // Microb Biotechnol. 2020 Vol. 13 No. 5 P. 1314–1335. doi: 10.1111/1751-7915.13517.

23. Effect of inoculation by Moroccan rock phosphate-solubilizing rhizobia, versus phosphorus fertilization, on the growth and the phosphorus uptake BY Vicia faba / T. Maghraoui, N. Bechtaoui, A. Galiana, et al. // Pakistan Journal of Agricultural Sciences. 2016 Vol. 53 P. 817–826. doi: 10.21162/PAKJAS/16.3461.

24. Seasonal changes in the abundance Fusarium proliferatium, microbial endophytes and nutrient levels in the roots of hybrid bamboo Bambusa pervariabilis × Dendrocalamopsis grandis / L. Li, Y. Wang, C. Yu, et al. // Front. Plant Sci. 2023 Vol. 14 Article 1185449 URL: https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2023.1185449/full (дата обращения: 21.01.2024).

25. Grobelak A., Hiller J. Bacterial siderophores promote plant growth: Screening of catechol and hydroxamate siderophores // Int J Phytoremediation. 2017 Vol. 19 No. 9 P. 825–833. doi: 10.1080/15226514.2017.1290581.

26. Rhizobia as a source of plant growth-promoting molecules: Potential applications and possible operational mechanisms / S. K. Jaiswal, M. Mohammed, F. Y. I. Ibny, et al. // Front. Sustain. Food Syst. 2021 Vol. 4 Article 619676 URL: https://www.frontiersin.org/journals/sustainable-food-systems/articles/10.3389/fsufs.2020.619676/full (дата обращения: 27.01.2024).

27. Hydroxamate siderophores secreted by plant endophytic Pseudomonas putida elicit defense against blast disease in rice incited by Magnaporthe oryzae / M. Ashajyothi, S. Velmurugan, A. Kundu, et al. // Lett Appl Microbiol. 2023 Vol. 76 No. 12 Article ovad139. URL: https://academic.oup.com/lambio/article-abstract/76/12/ovad139/7471614?redirectedFrom=fulltext (дата обращения: 03.02.2024).

28. Wilt disease management and enhancement of growth and yield of Cajanus cajan (L) var. Manak by bacterial combinations amended with chemical fertilizer / H. Kumar, V. K. Bajpai, R. C. Dubey, et al. // Crop Prot. 2010 Vol. 29 No. 6 P. 591–598. doi: 10.1016/j.cropro.2010.01.002.

29. Sinorhizobium spp inoculation alleviates the effect of Fusarium oxysporum on Medicago truncatula plants by increasing antioxidant capacity and sucrose accumulation / M. Batnini, M. Lopez-Gomez, F. Palma, et al. // Applied Soil Ecology. 2020 Vol. 150 Article 103458 URL: https://www.sciencedirect.com/science/article/abs/pii/S092913931930486X (дата обращения: 03.02.2024).

30. Characterization of rhizobia isolated from leguminous plants and their impact on the growth of ICCV 2 variety of chickpea (Cicer arietinum L.) / M. I. Mir, B. K. Kumar, S. Gopalakrishnan, et al. // Heliyon. 2021 Vol. 7 No. 11 Article e08321 URL: https://www.sciencedirect.com/science/article/pii/S2405844021024245 (дата обращения: 09.02.2024).

31. Pathogen biocontrol using plant growth-promoting bacteria (PGPR): Role of bacterial diversity / H. Wang, R. Liu, M. P. You,et al. // Microorganisms. 2021 Vol. 9 No. 9 Article 1988 URL: https://www.mdpi.com/2076-2607/9/9/1988 (дата обращения: 11.02.2024).

32. Post translational modifications of Trifolitoxin: A blue fluorescent peptide antibiotic / B. J. Lethbridge, R. E. Asenstorfer, L. S. Bailey, et al. // J Antibiot. 2022 Vol. 75 P. 125–135. doi: 10.1038/s41429-021-00497-0.

33. Robleto E. A., Borneman J., Triplett E. W. Effects of bacterial antibiotic production on rhizosphere microbial communities from a culture-independent perspective // Appl Environ Microbiol. 1998 Vol. 64 No. 12 P. 5020–5022. doi: 10.1128/AEM.64.12.5020- 5022.1998.

34. Complete genome sequences of two Rhizobium strains producing azol(in)e-modified antibiotics / D. Y. Travin, D. Sutormin, P. Mergaert, et al. // Microbiology Resource Announcements. 2022 Vol. 11 No. 11 Article e00722-22. URL: https://hal.science/hal-03833088 (дата обращения: 14.04.2024).

35. Cooperation, competition, and specialized metabolism in a simplified root nodule microbiome / B. L. Hansen, R. D. C. Pessotti, M. S. Fischer, et al. // MBio. 2020 Vol. 11 No. 4 Article e01917-20. URL: https://journals.asm.org/doi/10.1128/mbio.01917-20 (дата обращения: 14.04.2024).

36. Naamala J., Jaiswal S. K., Dakora F. D. Antibiotics resistance in Rhizobium: Type, process, mechanism and benefit for agriculture // Curr Microbiol. 2016 Vol. 72 No. 6 P. 804–816. doi: 10.1007/s00284-016-1005-0.

37. Сорокина А. И., Якименко М. В., Бегун С. А. Чувствительность штаммов, выделенных из дальневосточных природных популяций ризобий, к антибактериальным препаратам // Аграрная наука. 2023 Т. 366 № 1 С. 70–75. doi: 10.32634/0869-8155-2023-366-1-70-75.

38. Potential of rhizobia as plant growth-promoting rhizobacteria / L. K. Vargas, C. G. Volpiano, B. B. Lisboa, et al. // Microbes for Legume Improvement. 2017 P. 153–174. doi: 10.1007/978-3-319-59174-2_7.

39. Rhizospheric forest bacteria / N. V. Feoktistova, A. M. Mardanova, G. F. Hadieva, et al. // Scientist. Zapp. Kazan. UN-Ta. Ser. Natural. science. 2016 Vol. 158 P. 207–224.

40. Maan P. K., Garcha S., Walia G. S. Prevalence of bacteriocinogenic Rhizobium spp. in mungbean (Vigna radiata) // Legume Research. 2018 Vol. 42 No. 4 P. 557–564. doi: 10.18805/LR-3884.

41. Emerging applications of bacteriocins as antimicrobials, anticancer drugs, and modulators of the gastrointestinal microbiota / C. Cesa-Luna, J. M. Alatorre-Cruz, R. Carreno-Lopez, et al. // Pol J Microbiol. 2021 Vol. 70 No. 2 P. 143–159. doi: 10.33073/pjm-2021-020.

42. Bacteriocin-mediated inhibition of some common pathogens by wild and mutant Lactobacillus species and in vitro amplification of bacteriocin encoding genes / A. Ahsan, B. Mazhar, M. K. Khan, et al. // ADMET DMPK. 2022 Vol. 10 No. 1 P. 75–87. doi: 10.5599/admet.1053.

43. Bacteriocin-like substance inhibits potato soft rot caused by Erwinia carotovora / F. Cladera-Olivera, G. R. Caron, A. S. Motta, et al. // Can J Microbiol. 2006 Vol. 52 P. 533–539. doi: 10.1139/w05-159.

44. Mourad K., Hafida K. Properties of bacteriocin like substances produced by Rhizobium sp. ORN83 and ORN24 strains previously isolated in saline soils of Algeria // Ecologia mediterranea. 2009 Vol. 35 No. 1 P. 91–98.

45. Selection and characterization of inhibitor agents (bacteriocin like) produced by rhizobial strains associated to Medicago in western Algeria / A. Warda, B.-h. Zoubida, B. Z. Faiza, et al. // Int J Agric Crop Sci. 2014 Vol. 7 No. 7 P. 393–401.

46. Rhizobium etli USDA9032 engineered to produce a phenazine antibiotic inhibits the growth of fungal pathogens but is impaired in symbiotic performance / H. B. Krishnan, B. R. Kang, H. A. Krishnan, et al. // Appl Environ Microbiol. 2007 Vol. 73 No. 1 P. 327–330. doi: 10.1128/AEM.02027-06.

47. Paraburkholderia sabiae uses one type VI secretion system (T6SS-1) as a powerful weapon against notorious plant pathogens / S. Hug, B. Heiniger, K. Bolli, et al. // Microbiol Spectr. 2023 Vol. 11 No. 4 Article e01622-23. URL: https://journals.asm.org/doi/10.1128/spectrum.01622-23 (дата обращения: 15.03.2024).

48. Navarro-Monserrat E. D., Taylor C. G. T6SS: A key to Pseudomonas’s success in biocontrol? // Microorganisms. 2023 Vol. 11 Article 2718 URL: https://www.mdpi.com/2076-2607/11/11/2718 (дата обращения: 01.02.2024).

49. Functional exploration of the bacterial type VI secretion system in mutualism: Azorhizobium caulinodans ORS571-Sesbania rostrata as a research model / H. H. Lin, H. M. Huang, M. Yu, et al. // Mol Plant Microbe Interact. 2018 Vol. 31 No. 8 P. 856–867. doi: 10.1094/MPMI-01-18-0026-R.

50. Type VI secretion system in pathogenic Escherichia coli: Structure, role in virulence, and acquisition / F. Navarro-Garcia, F. Ruiz-Perez, A. Cataldi, et al. // Front. Microbiol. 2019 Vol. 10 Article 1965 URL: https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2019.01965/full (дата обращения: 09.06.2024).

51. Clemens D. L., Lee B. Y., Horwitz M. A. The Francisella type VI secretion system // Front Cell Infect Microbiol. 2018 Vol. 8 Article 121 URL: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5924787/ (дата обращения: 10.06.2024).

52. The T6SS-dependent effector Re78 of Rhizobium etli Mim1 benefits bacterial competition / B. F. S. De Sousa, L. Domingo-Serrano, A. Salinero-Lanzarote, et al. // Biology. 2023 Vol. 12 Article 678 URL: https://www.mdpi.com/2079-7737/12/5/678 (дата обращения: 14.06.2024).

53. Bernal P., Llamas M. A., Filloux A. Type VI secretion systems in plant-associated bacteria // Environ Microbiol. 2018 Vol. 20 No. 1 P. 1–15. doi: 10.1111/1462-2920.13956.

54. Yin R., Cheng J., Lin J. The role of the type VI secretion system in the stress resistance of plant-associated bacteria // Stress Biology. 2024 Vol. 4 Article 16 URL: https://link.springer.com/article/10.1007/s44154-024-00151-3 (дата обращения: 19.05.2024).

55. Biofertilizers as substitute to commercial agrochemicals / C. Bhattacharyya, R. Roy, P. Tribedi, et al. // Agrochemicals detection, treatment and remediation. Butterworth-Heinemann, 2020 p. 263–290. URL: https://www.sciencedirect.com/science/article/abs/pii/B9780081030172000118#preview-section-abstract (дата обращения: 19.05.2024). doi: 10.1016/b978-0-08-103017-2.00011-8.

56. Das K., Prasanna R., Saxena A. K. Rhizobia: A potential biocontrol agent for soilborne fungal pathogens // Folia Microbiol (Praha). 2017 Vol. 62 No. 5 P. 425–435. doi: 10.1007/s12223-017-0513-z.

57. Rijavec T., Lapanje A. Hydrogen cyanide in the rhizosphere: Not suppressing plant pathogens, but rather regulating availability of phosphate // Front. Microbiol. 2016 Vol. 7 Article 1785 URL: https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2016.01785/full (дата обращения: 20.03.2024).

58. Mahmoudi E., Tabatabaei B. E. S., Venturi V. Virulence attenuation of Pectobacterium carotovorum using N-acyl-homo-serine lactone degrading bacteria isolated from potato rhizosphere // The Plant Pathology Journal. 2011 Vol. 27 P. 242–248. doi: 10.5423/PPJ.2011.27.3.242.

59. Strain identification and quorum sensing inhibition characterization of marine-derived Rhizobium sp. NAO1 / H. Chang, J. Zhou, X. Zhu, et al. // Royal Society Open Science. 2017 Vol. 4 No. 3 Article 170025 URL: https://royalsocietypublishing.org/doi/abs/10.1098/rsos.170025 (дата обращения: 21.03.2024).

60. Inheritance of rhizobitoxine induced chlorosis in soybean / K. O. Robinson, J. W. Burton, E. W. Taliercio, et al. // Crop Sci- ence. 2020 Vol. 60 P. 3027–3034. doi: 10.1002/csc2.20193.

61. The proportion of soil-borne fungal pathogens increases with elevated organic carbon in agricultural soils / S. Du, P. Trivedi, Z. Wei, et al. // mSystems. 2022 Vol. 7 No. 2 Article e01337-21. URL: https://journals.asm.org/doi/10.1128/msystems.01337-21 (дата обращения: 22.03.2024).

62. Advances in the control of phytopathogenic fungi that infect crops through their root system / J. J. R. Coque, J. M. Alvarez-Perez, R. Cobos, et al. // Adv Appl Microbiol. 2020 Vol. 111 P. 123–170. doi: 10.1016/bs.aambs.2020.01.003.

63. Ehteshamul-Haque S., Ghaffar A. Use of rhizobia in the control of root rot diseases of sunflower, okra, soybean and mung-bean // Journal of Phytopathology. 1993 Vol. 138 No. 2 P. 157–163. doi: 10.1111/j.1439-0434.1993.tb01372.x.

64. Rhizosphere competent Mesorhizobium loti MP6 induces root hair curling, inhibits Sclerotinia sclerotiorum and enhances growth of Indian mustard (Brassica campestris) / S. Chandra, K. Choure, R. C. Dubey, et al. // Brazilian Journal of Microbiology. 2007 Vol. 38 No. 1 P. 124–130. doi: 10.1590/s1517-83822007000100026.

65. Tewari S., Sharma S. Rhizobial-metabolite based biocontrol of fusarium wilt in pigeon pea // Microbial Pathogenesis. 2020 Vol. 147 Article 104278 URL: https://www.sciencedirect.com/science/article/abs/pii/S0882401020306446?via%3Dihub (дата обращения: 20.04.2024).

66. Effect of some Rhizobium strains on fenugreek growth and biological control of sclerotinia stem rot of fenugreek caused by Sclerotinia trifoliorum / I. Hemissi, A. Hachana, M. Sonia, et al. // Acta Scientific Agriculture. 2021 Vol. 5 No. 5 P. 37–45. doi: 10.31080/ASAG.2021.05.0982.

67. Mohamed A., Hagaggi N. Biological control of root rot disease and growth promotion in fenugreek (Trigonella foenum-graecum L.) mediated by microbial antagonism // Egyptian Journal of Botany. 2021 Vol. 61 No. 1 P. 241–253. doi: 10.21608/ ejbo.2020.40834.1546.

68. Role of rhizobia in suppressing the root diseases of soybean under soil amendment / G. Parveen, R. Noreen, H. A. Shafique, et al. // Planta Daninha. 2019 Vol. 37 Article e019172336. URL: https://www.scielo.br/j/pd/a/wG4dVnpvdMxBYrrCygkpVLG/?lang=en (дата обращения: 26.03.2024).

69. Abdel-Lateif K. S, Abd El-Ghany E. M. Characterization of Rhizobium isolates as biocontrol agents against Fusarium solani and Macrophomina phaseolin // Sabrao Journal of Breeding and Genetics. 2023 Vol. 55 No. 1 P. 146–155. doi: 10.54910/ sabrao2023.55.1.14.

70. Rhizoctonia solani affecting micropropagated Garnem (Prunus amygdalus x Prunus persica) rootstock – characterization and biocontrol with Rhizobia / N. Jemai, S. Gargouri, I. Hemissi, et al. // J Plant Pathol. 2021 Vol. 103 P. 207–215. doi: 10.1007/s42161-020-00712-1.

71. Efficiency assessment of combinations between Rhizobium leguminosarum and Trichoderma spp. for controlling of pea (Pisum sativum L.) damping-off disease / H. Ketta, N. El-Khateeb, M. Saleh, et al. // Egypt J. Phytopathol. 2021 Vol. 49 No. 1 URL: https://ejp.journals.ekb.eg/article_139637.html (дата обращения: 26.03.2024). doi: 10.21608/ejp.2020.43495.1007.

72. Ganesan S., Kuppusamy R. G., Sekar R. Integrated management of stem rot disease (Sclerotium rolfsii) of groundnut (Arachis hypogaea L.) using Rhizobium and Trichoderma harzianum (ITCC-4572) // Turk J Agric For. 2007 Vol. 31 No. 2 P. 103–108.

73. Interrelationships between Bacillus sp. CHEP5 and Bradyrhizobium sp. SEMIA6144 in the induced systemic resistance against Sclerotium rolfsii and symbiosis on peanut plants / M. S. Figueredo, M. L. Tonelli, T. Taurian, et al. // J Biosci. 2014 Vol. 39 No. 5 P. 877–885. doi: 10.1007/s12038-014-9470-8.

74. Co-inoculation with rhizobia and AMF inhibited soybean red crown rot: from field study to plant defense-related gene expression analysis / X. Gao, X. Lu, M. Wu, et al. // PloS one. 2012 Vol. 7 No. 3 Article e33977. URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0033977 (дата обращения: 28.03.2024).

75. Sinorhizobium Meliloti can protect Medicago Truncatula from infection by Phoma Medicaginis / M. Mrabet, E. Abdellatif, K. Zribi, et al. // Phytopathologia Mediterranea. 2011 Vol. 50 No. 2 P. 183–191. http://www.jstor.org/stable/26458692.

76. Azizpour N., Rouhrazi K. Isolation and characterization of rhizosphere bacteria for the biocontrol of the Ascochyta rabiei in Iran // Adv. Plants Agric. Res. 2016 Vol. 3 P. 121–125. doi: 10.15406/apar.2016.03.00104.

77. Rhizobia for biological control of plant diseases / C. G. Volpiano, B. B. Lisboa, C. E. Granada, et al. // Microbiome in Plant Health and Disease. Singapore: Springer, 2019 P. 315–336. doi: 10.1007/978-981-13-8495-0_14.

78. Order of microbial succession affects rhizobia-mediated biocontrol efforts against Phytophthora root rot / J. M. Plett, J. Solomon, F. Snijders, et al. // Microbiological Research. 2021 Vol. 242 Article 126628 URL: https://www.sciencedirect.com/science/article/pii/S0944501320304961?via%3Dihub (дата обращения: 01.04.2024).

79. Chao W.-L. Antagonistic activity of Rhizobium spp. against beneficial and plant pathogenic fungi // Letters in Applied Microbiology. 1990 Vol. 10 No. 5 P. 213–215. doi: 10.1111/j.1472-765x.1990.tb01336.x.

80. Harnessing the biocontrol potential of Bradyrhizobium japonicum FCBP-SB-406 to manage charcoal rot of soybean with increased yield response for the development of sustainable agriculture / U. Khalid, Z.-e.-H. Aftab, T. Anjum, et al. // Microorganisms. 2024 Vol. 12 Article 304 URL: https://www.mdpi.com/2076-2607/12/2/304 (дата обращения: 02.04.2024).

81. Schizotrophic Sclerotinia sclerotiorum-mediated root and rhizosphere microbiome alterations activate growth and disease resistance in wheat / B. Tian, Z. Qu, M. A. Mehmood, et al. // Microbiol Spectr. 2023 Vol. 11 No. 3 Article e00981-23. URL: https:// journals.asm.org/doi/10.1128/spectrum.00981-23 (дата обращения: 03.04.2024).

82. Exploring a rhizobium to fix nitrogen in non-leguminous plants by using a tumor-formation root pathogen / Y. Zhao, L. Gao, Z. Gao, et al. // Phytopathol Res. 2022 Vol. 4 Article 48 URL: https://phytopatholres.biomedcentral.com/articles/10.1186/s42483-022-00154-w (дата обращения: 04.04.2024).

83. Development of Mesorhizobium ciceri-based biofilms and analyses of their antifungal and plant growth promoting activity in chickpea challenged by Fusarium wilt / K. Das, M. V. S. Rajawat, A. K. Saxena, et al. // Indian J Microbiol. 2017 Vol. 57 No. 1 P. 48–59. doi: 10.1007/s12088-016-0610-8.

84. Huynh T., Navi S. S., Yang X. B. Biocontrol potential of Bradyrhizobium japonicum against soybean sudden death syndrome in irrigated and non-irrigated fields // Fungal diversity, ecology and control management. Singapore: Springer, 2022 p. 439–454. doi: 10.1007/978-981-16-8877-5_21.

85. Soybean sudden death syndrome causal agent Fusarium brasiliense present in Michigan / J. Wang, H. Sang, J. L. Jacobs, et al. // Plant Dis. 2019 Vol. 103 No. 6 P. 1234–1243. doi: 10.1094/PDIS-08-18-1332-RE.

86. Temesgen D., Assefa F. Inoculation of native symbiotic effective Sinorhizobium spp. enhanced soybean [Glycine max (L.) Merr.] grain yield in Ethiopia // Environ Syst Res. 2020 Vol. 9 Article 38 URL: https://environmentalsystemsresearch.springeropen.com/articles/10.1186/s40068-020-00205-1 (дата обращения: 04.04.2024).

87. Anusuya D., Sullia S. B. The antibiotic effect of culture filtrates of some soil fungi on rhizobial growth in cultures // Plant and Soil. 1984 Vol. 77 P. 387–390. doi: 10.1007/bf02182942.

88. Induction of resistance in common bean by Rhizobium leguminosarum bv. phaseoli and decrease of common bacterial blight / E. Osdaghi, M. Shams-Bakhsh, A. Alizadeh, et al. // Phytopathol Mediterr. 2011 Vol. 50 No. 1 P. 45−54.

89. «Государственный каталог пестицидов и агрохимикатов по состоянию на 14 мая 2024 г.» URL: https://mcx.gov.ru/ministry/departments/departament-rastenievodstva-mekhanizatsii-khimizatsii-i-zashchity-rasteniy/industry-information/info-gosudarstvennaya-usluga-po-gosudarstvennoy-registratsii-pestitsidov-i-agrokhimikatov/ (дата обращения: 15.05.2024).

90. Symbiotic effectiveness and bacteriocin production by Rhizobium leguminosarum bv. viceae isolated from agricultural soils in Spain / B. Rodelas, J. Gonzalez-Lopez, V. Salmeron, et al. // Applied Soil Ecology. 1998 Vol. 8 P. 51–60. doi: 10.1016/s0929-1393(97)00066-8.

91. Chattopadhyay P., Banerjee G., Handique P. J. Use of an abscisic acid-producing Bradyrhizobium japonicum isolate as biocontrol agent against bacterial wilt disease caused by Ralstonia solanacearum // J Plant Dis Prot. 2022 Vol. 129 P. 869–879. doi: 10.1007/s41348-022-00604-9.

92. The beneficial endophytic microbes enhanced tobacco defense system to resist bacterial wilt disease / J. Tao, M. Gu, S. Yu, et al. // Chem. Biol. Technol. Agric. 2024 Vol. 11 Article 21 URL: https://chembioagro.springeropen.com/articles/10.1186/s40538-024-00542-8 (дата обращения: 09.04.2024).

93. Rhizobia suppress the root knot nematode and root rotting fungi on mungbean / F. Hafiza, U. Faizah, S. Hafiza, et al. // Int. J. Biol. Res. 2017 Vol. 5 No. 2 P. 71–75.

94. Role of mungbean root nodule associated fluorescent Pseudomonas and rhizobia in suppressing the root rotting fungi and root knot nematodes in chickpea (Cicer arietinum L) / R. Noreen, A. Shafique, S. E. Haque, et al. // Pakistan Journal of Botany. 2016 Vol. 48 No. 5 P. 2139–2145.

95. A farmer friendly and economic IPM strategy to combat root-knot nematodes infesting lentil / R. Rizvi, R. Ali Ansari, G. Zehra, et al. // Cogent Food & Agriculture. 2015 Vol. 1 No. 1 Article 1053214 URL: https://www.tandfonline.com/doi/full/10.1080/23311932.2015.1053214 (дата обращения: 01.02.2024).

96. White root rot disease suppression in rubber plant with microbial co-inoculants and silicon addition / I. Shabbir, M. Y. Abd Samad, R. Othman, et al. // Rhizosphere. 2020 Vol. 15 Article 100221 URL: https://www.sciencedirect.com/science/article/abs/pii/S2452219820301336 (дата обращения: 26.02.2024).

97. iTRAQ-based proteomic analysis reveals the role of the biological control agent, Sinorhizobium fredii strain Sneb183, in enhancing soybean resistance against the soybean cyst nematode / Y. Wang, R. Yang, Y. Feng, et al. // Front Plant Sci. 2020 Vol. 11 Article 597819 URL: https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2020.597819/full (дата обращения: 26.02.2024).

98. A synthesis of functional contributions of rhizobacteria to growth promotion in diverse crops / S. Brambilla, M. Stritzler, G. Soto, et al. // Rhizosphere. 2022 Vol. 24 Article 100611 URL: https://www.sciencedirect.com/science/article/abs/pii/S2452219822001410 (дата обращения: 16.02.2024).

99. Neelipally R. T. K. R., Anoruo A. O., Nelson S. Effect of co-inoculation of Bradyrhizobium and Trichoderma on growth, development, and yield of Arachis hypogaea L. (peanut) // Agronomy. 2020 Vol. 10 Article 1415 URL: https://www.mdpi.com/2073-4395/10/9/1415 (дата обращения: 18.02.2024).

100. Coinoculation of soybean plants with Bradyrhizobium japonicum and Trichoderma harzianum: Coexistence of both microbes and relief of nitrate inhibition of nodulation / E. T. Iturralde, M. C. Stocco, A. Faura, et al. // Biotechnology Reports. 2020 Vol. 26 Article e00461. URL: https://www.sciencedirect.com/science/article/pii/S2215017X19303790 (дата обращения: 19.02.2024).

101. Effects of Bradyrhizobium co-inoculated with Bacillus and Paenibacillus on the structure and functional genes of soybean rhizobacteria community / P. Xing, Y. Zhao, D. Guan, et al. // Genes. 2022 Vol. 13 No. 11 Article 1922 URL: https://www.mdpi.com/2073-4425/13/11/1922 (дата обращения: 21.02.2024).

102. Co-inoculation of Bradyrhizobium spp. and Bacillus sp. on tarwi (Lupinus mutabilis Sweet) in the high Andean region of Peru / M. Monroy-Guerrero, M. Memenza-Zegarra, N. Taco, et al. // Agronomy. 2022 Vol. 12 Article 2132 URL: https://www.mdpi.com/2073-4395/12/9/2132 (дата обращения: 21.05.2024).

103. Microorganisms and biotic interactions / Y. Moenne-Loccoz, P. Mavingui, C. Combes, et al. // Environmental Microbiology: Fundamentals and Applications / J. C. Bertrand, P. Caumette, P. Lebaron, et al. Dordrecht: Springer, 2014 P. 395–444. doi: 10.1007/978-94-017-9118-2_11.

104. Xiao K., Kinkel L. L., Samac D. A. Biological control of Phytophthora root rots on alfalfa and soybean with Streptomyces // Biological Control. 2002 Vol. 23 No. 3 P. 285–295. doi: 10.1006/bcon.2001.1015.

105. Microbial seed coating: An attractive tool for sustainable agriculture / A. Paravar, R. Piri, H. Balouchi, et al. // Biotechnol Rep (Amst). 2023 Vol. 37 Article e0078. URL: https://www.sciencedirect.com/science/article/pii/S2215017X23000012 (дата обращения: 01.06.2024).

106. Masciarelli O., Llanes A., Luna V. A new PGPR co-inoculated with Bradyrhizobium japonicum enhances soybean nodulation // Microbiological Research. 2014 Vol. 169 No. 7–8. P. 609–615. doi: 10.1016/j.micres.2013.10.001.

107. Chickpea (Cicer arietinum L.) as model legume for decoding the co-existence of Pseudomonas fluorescens and Mesorhizobium sp. as bio-fertilizer under diverse agro-climatic zones / S. Nagpal, P. Sharma, A. Sirari, et al. // Microbiol Res. 2021 Vol. 247 Article 126720 URL: https://www.sciencedirect.com/science/article/pii/S0944501321000264?via%3Dihub (дата обращения: 03.06.2024).

108. Improving yield and health of legume crops via co-inoculation with rhizobia and Trichoderma: A global meta-analysis / J. Z. Barbosa, M. Hungria, S. A. Prior, et al. // Applied Soil Ecology. 2022 Vol. 176 Article 104493 URL: https://www.sciencedirect.com/science/article/abs/pii/S0929139322001093 (дата обращения: 09.06.2024).

109. Dual inoculation of alfalfa (Medicago sativa L.) with Funnelliformis mosseae and Sinorhizobium medicae can reduce Fusarium wilt / X. Wang, T. Ding, Y. Li, et al. // J Appl Microbiol. 2020 Vol. 129 P. 665–679. doi: 10.1111/jam.14645.

110. Rosier A. Interactions of the plant growth promoting rhizobacterium Bacillus subtilis UD1022 with Medicago root microbes. Thesis. Delaware. 2022 231 p. URL: https://udspace.udel.edu/handle/19716/32274 (дата обращения: 09.03.2024).

111. Посевные площади Российской Федерации в 2023 году: Федеральная служба государственной статистики. URL: https://rosstat.gov.ru/storage/mediabank/Posev_2023.xlsx (дата обращения: 05.07.2024).

112. Баранов В. Ф., Махонин В. Л. О биологической защите агрофитоценозов сои от вредных организмов // Масличные культуры. Научно-технический бюллетень Всероссийского научно-исследовательского института масличных культур. 2014 № 1 С. 152–164.

113. Борзенкова Г. А. Оптимизация технологии предпосевного протравливания и возможность его сочетания с инокуляцией для защиты сои от семенной инфекции // Зернобобовые и крупяные культуры. 2014 Т. 9 № 1 С. 22–30.

114. Ростостимулирующая активность клубеньковых бактерий Rhizobium leguminosarum, выделенных из бобовых растений Южного Урала / Л. Р. Хакимова, Э. Р. Сербаева, А. М. Лавина и др. // Вестник ОГУ. 2017 Т. 209 № 9 С. 96–99.

115. Анализ эффектов совместной инокуляции грибами арбускулярной микоризы и ризобиями на рост и развитие растений гороха Pisum sativum L. / И. В. Леппянен, О. Ю. Штарк, О. А. Павлова и др. // Сельскохозяйственная биология. 2021 Т. 56 № 3 С. 475–486. doi: 10.15389/agrobiology.2021.3.475rus.

116. Продуктивность бобово-ризобиального комплекса под влиянием ростстимулирующих штаммов микроорганизмов / Л. Ф. Миннебаев, Е. В. Кузина, Г. Ф. Рафикова и др. // Сельскохозяйственная биология. 2019 Т. 54 № 3 С. 481–493. doi: 10.15389/agrobiology.2019.3.481rus.

117. Эффективность азотфиксирующего симбиоза гуара (Cyamopsis tetragonoloba) со штаммами Bradyrhizobium retamae RCAM05275 и Ensifer aridi RCAM05276 в вегетационном опыте / П. С. Ульянич, А. А. Белимов, И. Г. Кузнецова и др. // Сельскохозяйственная биология. 2022 Т. 57 № 3 С. 555–565. doi: 10.15389/agrobiology.2022.3.555rus.

118. Распространенность способности подавления роста родственных штаммов у ризобий / Ал. Х. Баймиев, А. А. Владимирова, Р. Т. Матниязов и др. // Микробиология. 2023 T. 92 № 6 С. 625–630. doi: 10.31857/S0026365623600311.