Foods and Raw Materials

2308-4057 2310-9599

121015

10.21603/2308-4057-2027-1-705

URMUKV

Review Article

Sinorhizobium and sustainable farming: Genomic approaches

https://orcid.org/0000-0002-3044-3529

Serazetdinova

Yuliya R.

Serazetdinova

Yuliya R.

serazetdinova2000@mail.ru

https://orcid.org/0000-0002-8508-3372

Kolpakova

Daria E.

Kolpakova

Daria E.

https://orcid.org/0000-0001-6362-7589

Borodina

Ekaterina E.

Borodina

Ekaterina E.

https://orcid.org/0000-0003-4988-8197

Asyakina

Lyudmila K.

Asyakina

Lyudmila K.

alk_kem@kemsu.ru

https://orcid.org/0000-0002-5630-3196

Prosekov

Alexander Yu.

Prosekov

Alexander Yu.

aprosekov@rambler.ru

доктор технических наук;

doctor of technical sciences;

https://orcid.org/0000-0001-9879-482X

Petrov

Andrey N.

Petrov

Andrey N.

Kemerovo State University Kemerovo Россия Kemerovo State University Kemerovo Russian Federation

Kemerovo State University Кемерово Россия Kemerovo State University Kemerovo Russian Federation

Russian Biotechnological University Moscow Россия Russian Biotechnological University Moscow Russian Federation

22 04 2026

15 1 238 256 14 01 2026 07 04 2026

https://jfrm.ru/en/issues/24071/24389/

Global population growth requires highly efficient and environmentally sustainable agricultural technologies that can ensure food security with minimal environmental impact. As an alternative to chemical preparations, organic farming uses biological mechanisms to provide plants with nutrients. This review systematizes the current data on the genomics of nitrogen-fixing bacteria of the genus Sinorhizobium. The review covered articles published in 1993–2025 and indexed in Scopus, MDPI, ScienceDirect, and Google Scholar. The metadata were processed in Zotero and VOSviewer. The review summarizes information about the structure of Sinorhizobium genomes, key genes, and regulatory networks involved in the formation of symbiosis with host plants. It focuses on the molecular mechanisms that determine the effectiveness of biological nitrogen fixation and transport of iron, zinc, and phosphates. The obtained genomic data may be used to develop tailored biological products capable of increasing crop yield and stress resistance by targeted modification of the rhizosphere microbiome. The latest scientific achievements and solutions demonstrate a great potential for sustainable agricultural technologies that replace chemical fertilizers with microbial communities. This approach reduces environmental risks and ensures a long-term productivity of agroecosystems, supporting climate resilience biodiversity conservation and stable agricultural development.

Organic farming Sinorhizobium symbiotic nitrogen fixation phosphorus solubilization siderophores

The research was part of State Assignment FZSR-2024-0009: Plant Growth-Promoting Bacteria as a Tool for Enhancing the Agronomic Biofortification of Wheat.

Hamad A, Tayel A. Food 2050 concept: The trends that shape the future of our food. Journal of Future Foods. 2026;6(6):1053–1066. https://doi.org/10.1016/j.jfutfo.2025.03.003

Serazetdinova YuR, Borodina EE, Fotina NV, Naik A, Mudgal G, et al. Rhizobia as complex biofertilizers for wheat: Biological nitrogen fixation and plant growth promotion. Foods and Raw Materials. 2026;14(1):214–227. https://doi.org/10.21603/2308-4057-2026-1-669

Chen X, Cui Z, Fan M, Vitousek P, Zhao M, et al. Producing more grain with lower environmental costs. Nature. 2014;514:486–489. https://doi.org/10.1038/nature13609

Yadav AK, Gurnule GG, Gour NI, There U, Choudhary VC. Micronutrients and fertilizers for improving and maintaining crop value: A review. International Journal of Environment, Agriculture and Biotechnology. 2022;7(1):125–140. https://doi.org/10.22161/ijeab.71.15

Wang H, Yang Y, Yao C, Feng Y, Wang H, et al. The correct combination and balance of macronutrients nitrogen, phosphorus and potassium promote plant yield and quality through enzymatic and antioxidant activities in potato. Journal of Plant Growth Regulation. 2024;43:4716–4734. https://doi.org/10.1007/s00344-024-11428-2

Li S, Li H, Yang J, Si Z, Zhou T, et al. Integrating water and nitrogen optimization to enhance wheat yield and macronutrients absorption under high-low seedbed cultivation. Irrigation Science. 2026;44:28. https://doi.org/10.1007/s00271-025-01056-3

Xiong C, Zhao X. Impacts of chemical fertilizer reduction on grain yield: A case study of China. PLoS One. 2024;19(3):e0298600. https://doi.org/10.1371/journal.pone.0298600

Liu Y, Liang F, Yan S, Tu T, Shi Z, et al. Optimizing fertilization strategies for low-carbon agriculture: Balancing greenhouse gas mitigation, soil health, and productivity. Results in Engineering. 2025;27:107094. https://doi.org/10.1016/j.rineng.2025.107094

Amin F, Jilani MI. Environmental, microbiological and chemical implications of fertilizers use in soils: A review. International Journal of Chemical and Biochemical Sciences. 2024;25(18):56–73.

10.

Jote CA. The impacts of using inorganic chemical fertilizers on the environment and human health. Organic & Medicinal Chemistry International Journal. 2023;13(3):555864. https://doi.org/10.19080/OMCIJ.2023.13.555864

11.

Liu H, Li S, Qiang R, Lu E, Li C, et al. Response of soil microbial community structure to phosphate fertilizer reduction and combinations of microbial fertilizer. Reduction and combinations of microbial fertilizer. Frontiers in Environmental Science. 2022;10;899727. https://doi.org/10.3389/fenvs.2022.899727

12.

Yu J, Hou P, Gao Q, Tan Q, Jiang D, et al. Optimizing nitrogen fertilizer and straw management promote root extension and nitrogen uptake to improve grain yield and nitrogen use efficiency of winter wheat (Triticum aestivum L.). Archives of Agronomy and Soil Science. 2024;70(1):1–17. https://doi.org/10.1080/03650340.2024.2316232

13.

Xu M, He R, Cui G, Wei J, Li X, et al. Understanding soil contamination in nitrogen fertilizer manufacturing: Spatial distribution, factors, and implications for environmental management. Water, Air, & Soil Pollution. 2024;235:236. https://doi.org/10.1007/s11270-024-07024-5

14.

Singh S, Singh R, Singh K, Katoch K, Zaeen A, et al. Smart fertilizer technologies: An environmental impact assessment for sustainable agriculture. Smart Agricultural Technology. 2024;8:100504. https://doi.org/10.1016/j.atech.2024.100504

15.

Faskhutdinova ER, Bogacheva NN, Borodina EE, Pozdnyakova AV, Luzyanin SL. Effect of endophytic microorganisms on growth rate of crops. Food Processing: Techniques and Technology. 2024;54(4):820–836. (In Russ.) https://doi.org/10.21603/2074-9414-2024-4-2548

16.

Yan L, Wang Y, Tumbalam P, Tengli Z, Zhang T, et al. Spatiotemporal distribution of chemical fertilizer application and manure application potential in China. Environmental Engineering Science. 2019;36(10):1337–1348. https://doi.org/10.1089/ees.2018.0486

17.

Liu C, Zhu T, Xin L. Effectiveness of agricultural technology services on fertilizer reduction in wheat production in China. Sustainability. 2025;17(7):2840. https://doi.org/10.3390/su17072840

18.

Ren Z, Zhang H, Li H, Wu Q, Huang Y, et al. Improving wheat yield, fertilizer use efficiency, and economic benefits through farmer-participation nutrient management. Sustainability. 2025;17(8):3481. https://doi.org/10.3390/su17083481

19.

Fotina NV, Serazetdinova YR, Kolpakova DE, Asyakina LK, Atuchin VV, et al. Enhancement of wheat growth by plant growth-stimulating bacteria during phytopathogenic inhibition. Biocatalysis and Agricultural Biotechnology. 2024;60:103294. https://doi.org/10.1016/j.bcab.2024.103294

20.

Serazetdinova YuR, Chekushkina DYu, Borodina EE, Kolpakova DE, Minina VI, et al. Synergistic interaction between Azotobacter and Pseudomonas bacteria in a growth-stimulating consortium. Foods and Raw Materials. 2025;13(2):376–393. http://doi.org/10.21603/2308-4057-2025-2-651

21.

Asyakina LK, Serazetdinova YuR, Frolova AS, Fotina NV, Neverova OA, et al. Antagonistic activity of extremophilic bacteria against phytopathogens in agricultural crops. Food Processing: Techniques and Technology. 2023;53(3):565–575. https://doi.org/10.21603/2074-9414-2023-3-2457

22.

Faskhutdinova ER, Fotina NV, Neverova OA, Golubtsova YuV, Mudgal G, et al. Extremophilic bacteria as biofertilizer for agricultural wheat. Foods and Raw Materials. 2024;12(2):348–360. https://doi.org/10.21603/2308-4057-2024-2-613

23.

Dhar SK, Kaur J, Singh GB, Chauhan A, Tamang J, et al. Novel Bacillus and Prestia isolates from Dwarf century plant enhance crop yield and salinity tolerance. Scientific Reports. 2024;14:14645. https://doi.org/10.1038/s41598-024-65632-x

24.

Wei X, Xie B, Wan C, Song R, Zhong W, et al. Enhancing soil health and plant growth through microbial fertilizers: Mechanisms, benefits, and sustainable agricultural practices. Agronomy. 2024;14(3):609. https://doi.org/10.3390/agronomy14030609

25.

Kaur J, Dhar SK, Chauhan A, Yadav S, Mudgal G, et al. GC-MS validated phytochemical up-leveling with in vitro-raised Sansevieria trifasciata [Prain]: The Mother in Law’s tongue gets more antibacterial. Current Plant Biology. 2023;35–36:100308. https://doi.org/10.1016/j.cpb.2023.100308

26.

Kolpakova DE, Serazetdinova YuR, Fotina NV, Zaushintsena AV, Asyakina LK, et al. Microbial biofortification of grain crops: Current state and prospects. Food Processing: Techniques and Technology. 2024;54(2):191–211. (In Russ.) https://doi.org/10.21603/2074-9414-2024-2-2500

27.

Asyakina LK, Vorob'eva EE, Proskuryakova LA, Zharko MYu. Evaluating extremophilic microorganisms in industrial regions. Foods and Raw Materials. 2023;11(1):162–171. https://doi.org/10.21603/2308-4057-2023-1-556

28.

Prosekov AYu, Vesnina AD, Lyubimova NA, Chekushkina DYu, Mikhailova ES. Consumer genomics in personalized nutrition. Food Processing: Techniques and Technology. 2025;55(2):400–415. (In Russ.) https://doi.org/10.21603/2074-9414-2025-2-2582

29.

Jiang L, Seo J, Peng Y, Jeon D, Park S, et al. Genome insights into the plant growth-promoting bacterium Saccharibacillus brassicae ATSA2T. AMB Express. 2023;13(1):9. https://doi.org/10.1186/s13568-023-01514-1

30.

Fagorzi C, Ilie A, Decorosi F, Cangioli L, Viti C, et al. Symbiotic and nonsymbiotic members of the genus Ensifer (syn. Sinorhizobium) are separated into two clades based on comparative genomics and high-throughput phenotyping. Genome Biology and Evolution. 2020;12(12):2521–2534. https://doi.org/10.1093/gbe/evaa221

31.

Lardi M, Pessi G. Functional genomics approaches to studying symbioses between legumes and nitrogen-fixing rhizobia. High-Throughput. 2018;7(2):15. https://doi.org/10.3390/ht7020015

32.

Kuzmanović N, Biondi E, Overmann J, Puławska J, Verbarg S, et al. Genomic analysis provides novel insights into diversification and taxonomy of Allorhizobium vitis (i.e. Agrobacterium vitis). BMC Genomics. 2022;23:462. https://doi.org/10.1186/s12864-022-08662-x

33.

Ferraz Helene LC, Klepa MS, Hungria M. New insights into the taxonomy of bacteria in the genomic era and a case study with Rhizobia. International Journal of Microbioljgy. 2022;2022:4623713. https://doi.org/10.1155/2022/4623713

34.

Rajkumari J, Katiyar P, Dheeman S, Pandey P, Maheshwari DK. The changing paradigm of rhizobial taxonomy and its systematic growth upto postgenomic technologies. World Journal of Microbiology and Biotechnology. 2022;38:206. https://doi.org/10.1007/s11274-022-03370-w

35.

Hassen AI, Lamprecht SC, Bopape FL. Emergence of β-rhizobia as new root nodulating bacteria in legumes and current status of the legume–rhizobium host specificity dogma. World Journal of Microbiology and Biotechnology. 2020;36:40. https://doi.org/10.1007/s11274-020-2811-x

36.

Farrand SK, van Berkum PP, Oger P. Agrobacterium is a definable genus of the family Rhizobiaceae. International Journal of Systematic and Evolutionary Microbiology. 2003;53(5):1681–1687. https://doi.org/10.1099/ijs.0.02445-0

37.

Bartoš O, Chmel M, Swierczková I. The overlooked evolutionary dynamics of 16S rRNA revises its role as the “gold standard” for bacterial species identification. Scientific Reports. 2024;14:9067. https://doi.org/10.1038/s41598-024-59667-3

38.

Rodríguez-Beltrán J, DelaFuente J, León-Sampedro R, MacLean RC, San Millán Á. Beyond horizontal gene transfer: The role of plasmids in bacterial evolution. Nature Reviews Microbiology. 2021;19:347–359. https://doi.org/10.1038/s41579-020-00497-1

39.

Kehlet-Delgado H, Montoya AP, Jensen KT, Wendlandt CE, Dexheimer C, et al. The evolutionary genomics of adaptation to stress in wild rhizobium bacteria. Proceedings of the National Academy of Sciences. 2024;121(13):e2311127121. https://doi.org/10.1073/pnas.2311127121

40.

Hassler HB, Probert B, Moore C, Lawson E, Jackson RW, et al. Phylogenies of the 16S rRNA gene and its hypervariable regions lack concordance with core genome phylogenies. Microbiome. 2022;10:104. https://doi.org/10.1186/s40168-022-01295-y

41.

Cortés-Lópeza NG, Ordóñez-Baqueraa PL, Viveros JD. Molecular tools used for metagenomic analysis. Review. Revista mexicana de ciencias pecuarias. 2020;11(4):1150–1173. https://doi.org/10.22319/rmcp.v11i4.5202

42.

Liu R, Qiao X, Shi Y, Peterson CB, Bush WS, et al. Constructing phylogenetic trees for microbiome data analysis: A mini-review. Computational and Structural Biotechnology Journal. 2024;23:3859–3868. https://doi.org/10.1016/j.csbj.2024.10.032

43.

Young JPW, Moeskjær S, Afonin A, Rahi P, Maluk M, et al. Defining the Rhizobium leguminosarum species complex. Genes. 2021;12(1):111. https://doi.org/10.3390/genes12010111

44.

diCenzo GC, Zamani M, Checcucci A, Fondi M, Griffitts JS, et al. Multidisciplinary approaches for studying rhizobium-legume symbioses. Canadian Journal of Microbiology. 2019;65(1):1–33. https://doi.org/10.1139/cjm-2018-0377

45.

Kuzmanović N, Fagorzi C, Mengoni A, Lassalle F, diCenzo GC. Taxonomy of Rhizobiaceae revisited: proposal of a new framework for genus delimitation. International Journal of Systematic and Evolutionary Microbiology. 2022;72(3):005243. https://doi.org/10.1099/ijsem.0.005243

46.

Ormeño-Orrillo E, Servín-Garcidueñas LE, Rogel MA, González V, Peralta H, et al. Taxonomy of rhizobia and agrobacteria from the Rhizobiaceae family in light of genomics. Systematic and Applied Microbiology. 2015;38(4):287–291. https://doi.org/10.1016/j.syapm.2014.12.002

47.

Chaumeil PA, Mussig AJ, Hugenholtz P, Parks D. GTDB-Tk: A toolkit to classify genomes with the genome taxonomy database. Bioinformatics. 2020;36(6):1925–1927. https://doi.org/10.1093/bioinformatics/btz848

48.

Kumar HKS, Gan HM, Tan MH, Eng WWH, Barton HA, et al. Genomic characterization of eight Ensifer strains isolated from pristine caves and a whole genome phylogeny of Ensifer (Sinorhizobium). Journal of Genomics. 2017;5:12–15. https://doi.org/10.7150/jgen.17863

49.

Chen WF, Wang ET, Ji ZJ, Zhang JJ. Recent development and new insight of diversification and symbiosis specificity of legume rhizobia: Mechanism and application. Journal of Applied Microbiology. 2021;131(2):553–563. https://doi.org/10.1111/jam.14960

50.

Poole P, Ramachandran V, Terpolilli J. Rhizobia: From saprophytes to endosymbionts. Nature Reviews Microbiology. 2018;16:291–303. https://doi.org/10.1038/nrmicro.2017.171

51.

Yang J, Lan L, Jin Y, Yu N, Wang D, et al. Mechanisms underlying legume-rhizobium symbioses. Journal of Integrative Plant Biology. 2022;64(2):244–267. https://doi.org/10.1111/jipb.13207

52.

Maróti G, Kondorosi É. Nitrogen-fixing Rhizobium-legume symbiosis: Are polyploidy and host peptide-governed symbiont differentiation general principles of endosymbiosis? Frontiers in Microbiology. 2014;5:326. https://doi.org/10.3389/fmicb.2014.00326

53.

Rutten PJ, Poole PS. Oxygen regulatory mechanisms of nitrogen fixation in rhizobia. Advances in Microbial Physiology. 2019;75:325–389. https://doi.org/10.1016/bs.ampbs.2019.08.001

54.

Mendis HC, Madzima TF, Queiroux C, Jones KM. Function of succinoglycan polysaccharide in Sinorhizobium meliloti host plant invasion depends on succinylation, not molecular weight. mBio. 2016;7(3):e00606–16. https://doi.org/10.1128/mBio.00606-16

55.

Chávez-Jacobo VM, Becerra-Rivera VA, Guerrero G, Dunn MF. The Sinorhizobium meliloti NspS-MbaA system affects biofilm formation, exopolysaccharide production and motility in response to specific polyamines. Microbiology. 2023;169(1):001293. https://doi.org/10.1099/mic.0.001293

56.

Jeong J, Kim Y, Hu Y, Jung S. Bacterial succinoglycans: Structure, physical properties, and applications. Polymers. 2022;14(2):276. https://doi.org/10.3390/polym14020276

57.

Sun H, Cui Y, Liu A, Meng D, Hu J, et al. Production and functional characterization of an extracellular galactoglucan G2 secreted by the Sinorhizobium sp. ACT002. Carbohydrate Polymers. 2026;374:124718. https://doi.org/10.1016/j.carbpol.2025.124718

58.

López-Baena FJ, Ruiz-Sainz JE, Rodríguez-Carvajal MA, Vinardell JM. Bacterial molecular signals in the Sinorhizobium fredii-soybean symbiosis. International Journal of Systematic and Evolutionary Microbiology. 2016;17(5):755. https://doi.org/10.3390/ijms17050755

59.

Wightman T, Muszyński A, Kelly SJ, Sullivan JT, Smart CJ, et al. Rhizobial secretion of truncated exopolysaccharides severely impairs the Mesorhizobium-Lotus symbiosis. Molecular Plant-Microbe Interactions. 2024;37(9):662–675. https://doi.org/10.1094/MPMI-03-24-0024-R

60.

Maillet F, Fournier J, Mendis HC, Tadege M, Wen J, et al. Sinorhizobium meliloti succinylated high-molecular-weight succinoglycan and the Medicago truncatula LysM receptor-like kinase MtLYK10 participate independently in symbiotic infection. The Plant Journal. 2020;102(2):311–326. https://doi.org/10.1111/tpj.14625

61.

Kawaharada Y, Kelly S, Nielsen MW, Hjuler CT, Gysel K, et al. Receptor-mediated exopolysaccharide perception controls bacterial infection. Nature. 2015;523:308–312. https://doi.org/10.1038/nature14611

62.

Kawaharada Y, Nielsen MW, Kelly S, James EK, Andersen KR, et al. Differential regulation of the Epr3 receptor coordinates membrane-restricted rhizobial colonization of root nodule primordia. Nature Communications. 2017;8:14534. https://doi.org/10.1038/ncomms14534

63.

Arnold MFF, Shabab M, Penterman J, Boehme KL, Griffitts JS, et al. Genome-wide sensitivity analysis of the microsymbiont Sinorhizobium meliloti to symbiotically important, defensin-like host peptides. mBio. 2017;8(4):e01060-17. https://doi.org/10.1128/mbio.01060-17

64.

Penterman J, Abo RP, de Nisco NJ, Arnold MF, Longhi R, et al. Host plant peptides elicit a transcriptional response to control the Sinorhizobium meliloti cell cycle during symbiosis. Proceedings of the National Academy of Sciences. 2014;111(9):3561–3566. https://doi.org/10.1073/pnas.1400450111

65.

Wang ET, Tian CF, Chen WF, Young JPW, Chen WX. Ecology and evolution of Rhizobia. Singapore: Springer Nature; 2019, 273 p. https://doi.org/10.1007/978-981-32-9555-1

66.

Sanjuán J. Towards the minimal nitrogen-fixing symbiotic genome. Environmental Microbiology. 2016;18(8):2292–2294. https://doi.org/10.1111/1462-2920.13261

67.

Zhao R, Liu LX, Zhang YZ, Jiao J, Cui WJ, et al. Adaptive evolution of rhizobial symbiotic compatibility mediated by co-evolved insertion sequences. The ISME Journal. 2018;12(1):101–111. https://doi.org/10.1038/ismej.2017.136

68.

Haskett TL, Terpolilli JJ, Bekuma A, O'Hara GW, Sullivan JT, et al. Assembly and transfer of tripartite integrative and conjugative genetic elements. Proceedings of the National Academy of Sciences. 2016;113(43):12268–12273. https://doi.org/10.1073/pnas.1613358113

69.

Baxter L, Roy P, Picot E, Watts J, Jones A, et al. Comparative genomics across three Ensifer species using a new complete genome sequence of the medicago symbiont Sinorhizobium (Ensifer) meliloti WSM1022. Microorganisms. 2021;9(12):2428. https://doi.org/10.3390/microorganisms9122428

70.

Pirhanov A, Bridges CM, Goodwin RA, Guo YS, Furrer J, et al. Optogenetics in Sinorhizobium meliloti enables spatial control of exopolysaccharide production and biofilm structure. ACS Synthetic Biology. 2021;10(2):345–356. https://doi.org/10.1021/acssynbio.0c00498

71.

Remigi P, Zhu J, Young JPW, Masson-Boivin C. Symbiosis within symbiosis: Evolving nitrogen-fixing legume symbionts. Trends in Microbiology. 2015;24:63–75. https://doi.org/10.1016/j.tim.2015.10.007

72.

Ling J, Wang H, Wu P, Li T, Tang Y, et al. Plant nodulation inducers enhance horizontal gene transfer of Azorhizobium caulinodans symbiosis island. Proceedings of the National Academy of Sciences. 2016;113(48):13875–13880. https://doi.org/10.1073/pnas.1615121113

73.

Liu LX, Li QQ, Zhang YZ, Hu Y, Jiao J, et al. The nitrate-reduction gene cluster components exert lineage-dependent contributions to optimization of Sinorhizobium symbiosis with soybeans. Environmental Microbiology. 2017;19(12):4926–4938. https://doi.org/10.1111/1462-2920.13948

74.

Singh P, Kumar K, Jha A, Yadava P, Pal M, et al. Global gene expression profiling under nitrogen stress identifies key genes involved in nitrogen stress adaptation in maize (Zea mays L.). Scientific Reports. 2022;12:4211. https://doi.org/10.1038/s41598-022-07709-z

75.

Wright GSA, Saeki A, Hikima T, Nishizono Y, Hisano T, et al. Architecture of the complete oxygen-sensing FixL-FixJ two-component signal transduction system. Science Signaling. 2018;11(525):eaaq0825. https://doi.org/10.1126/scisignal.aaq0825

76.

Almada JC, Bortolotti A, Porrini L, Albanesi D, Miguel V, et al. Allosteric coupling activation mechanism in histidine kinases. Scientific Reports. 2025;15:14682. https://doi.org/10.1038/s41598-025-88468-5

77.

Sun W, Shahrajabian MH. Survey on nitrogenase evolution by considering the importance of nitrogenase, its structure, and mechanism of nitrogenase. Notulae Botanicae Horti Agrobotanici Cluj-Napoca. 2024;52(1):13157. https://doi.org/10.15835/nbha52113157

78.

Bhatla SC, Lal MA. Plant physiology, development and metabolism. Singapore: Springer; 2023, 899 p. https://doi.org/10.1007/978-981-99-5736-1

79.

Day DA, Smith PMC. Iron transport across symbiotic membranes of nitrogen-fixing legumes. International Journal of Molecular Sciences. 2021;22(1):432. https://doi.org/10.3390/ijms22010432

80.

Singh RL. Principles and applications of environmental biotechnology for a sustainable future. Singapore: Springer; 2016, 487 p. https://doi.org/10.1007/978-981-10-1866-4

81.

Liu KH, Zhang B, Yang BS, Shi WT, Li YF, et al. Rhizobiales-specific RirA represses a naturally «synthetic» foreign siderophore gene cluster to maintain Sinorhizobium-legume mutualism. mBio. 2022;13(1):e02900-21. https://doi.org/10.1128/mbio.02900-21

82.

Einsle O. On the shoulders of giants-reaching for nitrogenase. Molecules. 2023;28(24):7959. https://doi.org/10.3390/molecules28247959

83.

Klebba PE, Newton SMC, Six DA, Kumar A, Yang T, et al. Iron acquisition systems of gram-negative bacterial pathogens define TonB-dependent pathways to novel antibiotics. Chemical Reviews. 2021;121(9):5193–5239. https://doi.org/10.1021/acs.chemrev.0c01005

84.

Kramer J, Özkaya Ö, Kümmerli R. Bacterial siderophores in community and host interactions. Nature Reviews Microbiology. 2020;18:152–163. https://doi.org/10.1038/s41579-019-0284-4

85.

Soto MJ, Pérez J, Muñoz-Dorado J, Contreras-Moreno FJ, Moraleda-Muñoz A. Transcriptomic response of Sinorhizobium meliloti to the predatory attack of Myxococcus xanthus. Frontiers in Microbiology. 2023;14:1213659. https://doi.org/10.3389/fmicb.2023.1213659

86.

Lynch D, O'Brien J, Welch T, Clarke P, Cuı́v PÓ, et al. Genetic organization of the region encoding regulation, biosynthesis, and transport of rhizobactin 1021, a siderophore produced by Sinorhizobium meliloti. Journal of Bacteriology. 2001;183:2576–2585. https://doi.org/10.1128/JB.183.8.2576-2585.2001

87.

Arnold E. Non-classical roles of bacterial siderophores in pathogenesis. Frontiers in Cellular and Infection Microbiology. 2024;14:1465719. https://doi.org/10.3389/fcimb.2024.1465719

88.

Ogwu MC, Patterson ME, Senchak PA. Phosphorus mining and bioavailability for plant acquisition: Environmental sustainability perspectives. Environmental Monitoring and Assessment. 2025;197:572. https://doi.org/10.1007/s10661-025-14012-7

89.

Fathi A, Mehdiniya Afra J. Plant growth and development in relation to phosphorus: A review. Bulletin of University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca. Agriculture. 2023;80(1):1–7. https://doi.org/10.15835/buasvmcn-agr:2022.0012

90.

Tian J, Ge F, Zhang D, Deng S, Liu X. Roles of phosphate solubilizing microorganisms from managing soil phosphorus deficiency to mediating biogeochemical P cycle. Biology. 2021;10(2):158. https://doi.org/10.3390/biology10020158

91.

Barnett MJ, Long SR. Novel genes and regulators that influence production of cell surface exopolysaccharides in Sinorhizobium meliloti. Journal of Bacteriology. 2018;200(3):e00501-17. https://doi.org/10.1128/JB.00501-17

92.

diCenzo GC, Sharthiya H, Nanda A, Zamani M, Finan TM. PhoU allows rapid adaptation to high phosphate concentrations by modulating PstSCAB Transport Rate in Sinorhizobium meliloti. Journal of Bacteriology. 2017;199(18):e00143-17. https://doi.org/10.1128/JB.00143-17

93.

Santos J, Cardoso P, Rocha R, Pinto R, Lopes T, et al. Phosphate-solubilizing bacteria from different genera, host plants, and climates: Influence of soil pH on plant growth and biochemistry. Land. 2025;14(10):2065. https://doi.org/10.3390/land14102065

94.

Kumar A, Kumar A, Patel H. Role of microbes in phosphorus availability and acquisition by plants. International Journal of Current Microbiology and Applied Sciences. 2018;7(5):1344–1347. https://doi.org/10.20546/ijcmas.2018.705.161

95.

Jindo K, Audette Y, Olivares FL, Canellas LP, Smith DS, et al. Biotic and abiotic effects of soil organic matter on the phytoavailable phosphorus in soils: A review. Chemical and Biological Technologies in Agriculture. 2023;10(1):29. https://doi.org/10.1186/s40538-023-00401-y

96.

Patil R, Sontakke T, Biradar A, Nalage D. Zinc: An essential trace element for human health and beyond. Food and Health. 2023;5(3):13. https://doi.org/10.53388/FH2023013

97.

Mikhaylina A, Ksibe AZ, Scanlan DJ, Blindauer CA. Bacterial zinc uptake regulator proteins and their regulons. Biochemical Society Transactions. 2018;46(4):983–1001. https://doi.org/10.1042/BST20170228

98.

Schmidt C, Schwarzenberger C, Große C, Nies DH. FurC regulates expression of zupT for the central zinc importer ZupT of Cupriavidus metallidurans. Journal of Bacteriology. 2014;196(19):3461–3471. https://doi.org/10.1128/jb.01713-14

99.

Chaoprasid P, Dokpikul T, Johnrod J, Sirirakphaisarn S, Nookabkaew S, et al. Agrobacterium tumefaciens zur regulates the high-affinity zinc uptake system TroCBA and the putative metal chaperone YciC, along with ZinT and ZnuABC, for survival under zinc-limiting conditions. Applied and Environmental Microbiology. 2016;82(12):3503–3514. https://doi.org/10.1128/AEM.00299-16

100.

Suryawati B. Zinc homeostasis mechanism and its role in bacterial virulence capacity. AIP Conference Proceedings. 2018;2021(1):070081. https://doi.org/10.1063/1.5062819

101.

Bobrov AG, Kirillina O, Fetherston JD, Miller MC, Burlison JA, et al. The Yersinia pestis siderophore, yersiniabactin, and the ZnuABC system both contribute to zinc acquisition and the development of lethal septicaemic plague in mice. Molecular Microbiology. 2014;93:759–775. https://doi.org/10.1111/mmi.12693

102.

Bellotti D, Rowińska-Żyrek M, Remelli M. Novel insights into the metal binding ability of ZinT periplasmic protein from Escherichia coli and Salmonella enterica. Dalton Transactions. 2020;49:9393–9403. https://doi.org/10.1039/D0DT01626H

103.

Lu M, Li Z, Liang J, Wei Y, Rensing C, et al. Zinc resistance mechanisms of P1B-type ATPases in Sinorhizobium meliloti CCNWSX0020. Scientific Reports. 2016;6:29355. https://doi.org/10.1038/srep29355

104.

Zhang P, Zhang B, Jiao J, Dai SQ, Chen WX, et al. Modulation of symbiotic compatibility by rhizobial zinc starvation machinery. mBio. 2020;11(1):e03193–e03119. https://doi.org/10.1128/mBio.03193-19

105.

Jiao J, Ni M, Zhang B, Zhang Z, Young JPW, et al. Coordinated regulation of core and accessory genes in the multipartite genome of Sinorhizobium fredii. PLoS Genetics. 2018;14(5):e1007428. https://doi.org/10.1371/journal.pgen.1007428

106.

Jiao J, Wu LJ, Zhang B, Hu Y, Li Y, et al. MucR is required for transcriptional activation of conserved ion transporters to support nitrogen fixation of Sinorhizobium fredii in soybean nodules. Molecular Plant-Microbe Interactions. 2016;29(5):352–361. https://doi.org/10.1094/MPMI-01-16-0019-R

107.

Samy PMA, Ramasamy A, Chinnusamy V, Kumar BS. Legumes: Physiology and molecular biology of abiotic stress tolerance. Singapore: Springer; 2023, 390 p. https://doi.org/10.1007/978-981-19-5817-5

108.

Abreu I, Saéz Á, Castro-Rodríguez R, Escudero V, Rodríguez-Haas B, et al. Medicago truncatula Zinc-Iron Permease6 provides zinc to rhizobia-infected nodule cells. Plant, Cell & Environment. 2017;40(11):2706–2719. https://doi.org/10.1111/pce.13035

109.

Ivanova E, Skalozub O. The effectiveness of the use of Sinorhizobium meliloti in the cultivation of variable alfalfa (Medicago varia Mart.). IOP Conference Series: Earth and Environmental Science. 2022;962:012017. https://doi.org/10.1088/1755-1315/962/1/012017

110.

Harris F, Dobbs J, Atkins D, Ippolito JA, Stewart JE. Soil fertility interactions with Sinorhizobium-legume symbiosis in a simulated Martian regolith; effects on nitrogen content and plant health. PLoS One. 2021;16(9):e0257053. https://doi.org/10.1371/journal.pone.0257053

111.

Kang X, Yu X, Zhang Y, Cui Y, Tu W, et al. Inoculation of Sinorhizobium saheli YH1 leads to reduced metal uptake for Leucaena leucocephala grown in mine tailings and metal-polluted soils. Frontiers in Microbiology. 2018;9:1853. https://doi.org/10.3389/fmicb.2018.01853

112.

Oves M, Qari HA, Khan MS. Sinorhizobium saheli: Advancing chromium mitigation, metal adsorption, and plant growth enhancement in heavy metal-contaminated environments. Journal of Plant Growth Regulation. 2025;44:168–187. https://doi.org/10.1007/s00344-023-11123-8

113.

Saidi S, Cherif-Silini H, Bouket AC, Silini A, Eshelli M, et al. Improvement of Medicago sativa crops productivity by the Co-inoculation of Sinorhizobium meliloti–actinobacteria under salt stress. Current Microbiology. 2021;78:1344–1357. https://doi.org/10.1007/s00284-021-02394-z

114.

Sijilmassi B, Filali-Maltouf A, Fahde S, Ennahli Y, Boughribil S, et al. In-vitro plant growth promotion of Rhizobium strains isolated from lentil root nodules under abiotic stresses. Agronomy. 2020;10(7):1006. https://doi.org/10.3390/agronomy10071006

115.

Baloglu MC, Celik Altunoglu Y, Baloglu P, Yildiz AB, Türkölmez N, et al. Gene-editing technologies and applications in legumes: Progress, evolution, and future prospects. Frontiers in Genetics. 2022;13:859437. https://doi.org/10.3389/fgene.2022.859437

116.

Wang L, Xiao Y, Wei X, Wei X, Pan J, et al. Highly efficient CRISPR-mediated base editing in Sinorhizobium meliloti. Frontiers in Microbiology. 2021;12:686008. https://doi.org/10.3389/fmicb.2021.686008

117.

Hernandez Benitez EM, Martínez Romero E, Aguirre Noyola JL, Farias Rico JA, Ledezma Tejeida D. Computational inference of Rhizobium phaseoli transcriptional regulatory network predicts transcription factors involved in nodulation. Briefings in Functional Genomics. 2025;24:elaf020. https://doi.org/10.1093/bfgp/elaf020

118.

Fan K, Xiao Z, Wang L, Cheung W L, Wong F, et al. Transcriptomes of soybean roots and nodules inoculated with Sinorhizobium fredii with NopP and NopI variants. Scientific Data. 2024;11:1146. https://doi.org/10.1038/s41597-024-03964-z

119.

Wang S, Yan J, Heal KV, Li H, Yu Y, et al. Rhizosphere microbial roles in phosphorus cycling during successive plantings of Chinese fir plantations. Forest Ecology and Management. 2024;570:122227. https://doi.org/10.1016/j.foreco.2024.122227

120.

Asyakina L, Barsukov P, Serazetdinova Y, Baturina O, Fotina N, et al. A novel fungicide consortium: is it better for wheat production and how does it affect the rhizosphere microbiome? Applied Microbiology. 2025;5(4):142. https://doi.org/10.3390/applmicrobiol5040142

121.

Serazetdinova YuR, Bogacheva NN, Karchin KV, Isachkova OA, Neverova OA, et al. Prospects for the combined use of Pseudomonas koreensis and Pseudomonas plecoglossicida for biological enrichment of plants with nitrogen. Storage and Processing of Farm Products. 2025;33(1):116–129. (In Russ.) https://doi.org/10.36107/spfp.2025.1.573

122.

Bogacheva NN, Afonina YuE, Serazetdinova YuR, Kolpakova DE, Naik A, et al. Combined use of zeolite and growth-stimulating bacteria to improve wheat growth. Food Processing: Techniques and Technology. 2025;55(3):509–520. (In Russ.) https://doi.org/10.21603/2074-9414-2025-3-2591

123.

Liu G, Wang H, Tong B, Cui Y, Vonesch SC, et al. An efficient CRISPR/Cas12e system for genome editing in Sinorhizobium meliloti. ACS Synthetic Biology. 2023;12(3):898–903. https://doi.org/10.1021/acssynbio.2c00629