Laboratory of rhizospheric microflora №1

Laboratory of rhizospheric microflora №1

LABORATORY OF RHIZOSPHERE MICROFLORA

BELIMOV ANDREY ALEKSEEVICH

Head of the Laboratory, Chief Researcher, Doctor of Biological Sciences

Phone: +7 812 4705100

Е-mail: belimov@arriam.ru

 

The Laboratory of Rhizosphere Microflora was established in 2001 on the basis of the group of rhizosphere microbiology of the Laboratory of Biotechnology and the laboratory of soil Mycology. Since its establishment, the laboratory has been headed by Doctor of Biological Sciences Lev Vitalievich Kravchenko, who was one of the leading scientists in the field of studying ecochemical and biological rhizosphere processes of interaction of microorganisms with plants.

 

THE MAIN AREA OF RESEARCH

 

1. Ecochemical integration of rhizosphere microorganisms with plants

Development of methods for obtaining and analyzing the qualitative and quantitative composition of root exudates. Selection and study of bacteria with a high ability to colonize the rhizosphere, antimicrobial and ACC deaminase activity, production and/or transformation of phytohormones and other biologically active substances. Investigation the role of root exudates, phytohormones and microbial metabolites in plant-microbial interactions by gas and liquid chromatography and mass spectrometry.

  

2. Adaptation and functioning of plant-microbe systems in unfavorable soil and climatic conditions

Selection and detailed characterization of rhizosphere and nodule bacteria resistant to abiotic stresses. Investigation the mechanisms of plant resistance and the anti-stress effects of microorganisms on plants in conditions of soil pollution with heavy metals, drought, extreme temperatures, nutrient deficiency and increased soil acidity. Disclosure of the adaptive potential of plant-microbe systems for their effective functioning in stressful conditions and using in agrobiotechnology. Application of microbiological, physiological, biochemical, physico-chemical and chromato-mass spectrometric methods for disclosure mechanisms of plant-microbe interactions under stressful conditions.

 

  

 

 

3. Biocontrol of phytopathogenic fungi by rhizosphere bacteria

Investigation the ecology of soil phytopathogenic fungi in different agroecological conditions. The use of microbiological, immunological and molecular methods to study the development and features of colonization by phytopathogenic fungi of the rhizosphere and roots of host plants. The study of the control functions of rhizosphere bacteria, such as competition for food sources, production of antibiotics and inhibitors, induction of systemic resistance of plants. Development of microbiological methods for biocontrol of phytopathogens and reducing the incidence of agricultural plants.

 

  

 

 

4. Genetics of specialized cells in cyanobacteria

Investigation the mechanisms of regulation, formation and differentiation of heterocysts that perform aerobic nitrogen fixation in cyanobacteria. The study of regulatory genes controlling different stages of heterocyst differentiation and determining the effectiveness of nitrogen fixation by free-living and symbiotic cyanobacteria.

 

 

Staff

CURRENT PROJECTS AND GRANTS

2024-2026 – "To study the role of associative rhizobacteria in the modulation of the phytohormone salicylic acid in barley and pea plants" (State assignment).

2024-2026 – "The role of microbial destructors and producers of abscisic acid in the resistance of agricultural plants to biotic and abiotic stress factors". RGNF grant (24-16-00166).

2020-2025 – "Studying the genetic resources of beneficial soil microorganisms of the Arctic regions of Russia in connection with climate change and prospects for expanding the range of agricultural land to the North." RGNF grant (20-76-10042).

2020-2024 - Subsidy with the support of the Ministry of Education and Science of the Russian Federation for the creation and development of a world-class scientific center "Agrotechnologies of the Future" (075-15-2022-320 dated 04/20/2022).

2024-2026 - "The role of microorganisms-destructors and producers of abscisic acid in the resistance of agricultural plants to biotic and abiotic stress factors." RGNF grant (24-16-00166).

 

COMPLETED PROJECTS AND GRANTS

2021-2023 - Subsidy with the support of the Ministry of Education and Science of the Russian Federation for the implementation of the project: "Mobilization of genetic resources of microorganisms on the basis of the Departmental collection of useful microorganisms for agricultural purposes (VKSM) at the ARRIAM using the network principle of organization" (075-15-2021-1055 dated 09/28/2021).

2022-2023 – "Dependence of resistance to fusarium root rot of barley of different genotypes on the intensity of plant protective reactions and the influence of rhizosphere microbiomes." RSF grant (22-26-00341).

2019-2023 - "Mechanisms of adaptation of seed peas (Pisum sativum L.) and its symbiosis with microorganisms to cadmium, mercury and aluminum: toxicity, transport and interactions of elements." RSF grant (19-16-00097).

2017-2019 - "Creation of new guar varieties using marker-mediated selection methods for import substitution in the oil, gas and food industries." Subsidy from the Ministry of Education and Science of the Russian Federation (14.604.21.0168).

2017-2023 - "Destruction of the phytohormone of abscisic acid by rhizospheric bacteria: biochemical pathway, molecular mechanism and bioprotective significance". RFF grant (17-14-01363).

2016-2020 - "The study of the formation of the specificity of plant-microbial interaction using relict legumes and its relationship with the productivity of symbiosis" Grant RSF (16-16-00080).

 

BASIC PUBLICATIONS 2012-2023

1. Karlov D.S., Bolsiyanova O.D., Lashchinsky N.N., Belimov A.A. Study of the relationships between agrochemical soil parameters and the species composition of plants in some areas of the Lena River delta, Northern Yakutia. Problems of the Arctic and Antarctic. 2023;69(2):228-243. https://doi.org/10.30758/0555-2648-2023-69-2-228-243.

2. Belimov A.A., Shaposhnikov A.I., Azarova T.S., Yuzikhin O.S., Sekste E.A., Safronova V.I., Tikhonovich I.A. Aluminum-immobilizing rhizobacteria modulate root exudation and nutrient uptake and increase aluminum tolerance of pea mutant E107 (brz). Plants, 2023, 12, 2334. https://doi.org/10.3390/plants12122334.

3. Shaposhnikov A., Yuzikhin O., Syrova D., Karlov D., Sazanova A., Azarova T., Sekste E., Safronova V., Belimov A. Beneficial aluminium immobilizing microorganisms inhabiting the rhizosphere of pea. Biological Communications, 2023. 68(2): 74–85. https://doi.org/10.21638/spbu03.2023.202.

4. Boykova I., Yuzikhin O., Novikova I., Ulianich P., Eliseev I.,Shaposhnikov A., Yakimov A., Belimov A. StrainStreptomycesP-56 produces nonactin and possesses insecticidal, acaricidal, antimicrobial and plant growth-promoting traits. Microorganisms, 2023, 11, 764. https://doi.org/10.3390/ microorganisms11030764.

5. Guro P., Ulianich P., Shaposhnikov A., Yuzikhin O., Karlov D., Sazanova A., Safronova V., Belimov A. Draft genome sequence of the bacteriumCupriavidusstrain D39, inhabiting the rhizosphere of pea plants (Pisum sativumL.). Microbiology Resource Announcements, 2023, 12(4): e0135422. doi: 10.1128/mra.01354-22.

6. Safronova V.; Sazanova A.; Belimov A.; Guro P.; Kuznetsova I.; Karlov D.; Chirak E.; Yuzikhin O.; Verkhozina A.; Afonin A.; Tikhonovich I. Synergy between rhizobial co-microsymbionts leads to an increase in the efficiency of plant–microbe interactions. Microorganisms, 2023, 11, 1206. https://doi.org/10.3390/ microorganisms11051206.

7. Kolesnikov L.E., Belimov A.A., Hassan B.A., Kolesnikova Yu.R., Kiselev M.V., Minakov D.S. The optimization of grain crops’ phytosanitary condition with associative rhizobacteria application. Russian Agricultural Sciences, 2023, Vol. 49, No. 2, pp. 164–171. DOI:10.3103/s1068367423020088.

8. Kolesnikov L.E., Hassan B.A., Belimov A.A., Orlova A.G., Minakov D.S., Kolesnikova Yu.R. Application of associative rhizobacteria for increasing the soft wheat productivity and reducing the diseases harmfulness. Indian Journal of Agricultural Research, 2023, AF-776, 1-7. Doi: 10.18805/IJARe.AF-766.

9. Shaposhnikov A.I., Belimov A.A., Azarova T.S. T. S. Azarova, O. K. Strunnikova, N. A. Vishnevskaya, N. I. Vorobyov, O. S. Yuzikhin & I. A. Tikhonovich. The relationship between the composition of root exudates and the efficiency of interaction of wheat plants with microorganisms. Applied Biochemistry and Microbiology, 2023, 59, 330–343.https://doi.org/10.1134/S000368382303016X.

10. Alekhina I.A., Belimov A.A., Karlov D.S. Search for arctic leguminous plants and their bacterial symbionts in the Lena delta and on the Putorana plateau. Russian Polar Research. 2023, No. 1, pp. 16-19.

11. Belimov A.A., Sazanova A.L., Ulianich P.S., Yuzikhin O.S., Guroa P.V., Shaposhnikov A.I., Sokolova D.V., Safronova V.I. Cross-nodulation and symbiosis efficiency of rhizobia isolated from nodules ofCyamopsis tetragonolobaonVigna unguiculataandGlycine max. Russian Journal of Plant Physiology, 2023, 70:182. DOI: 10.1134/S1021443723601878.

12. Guro P, Ulianich P, Belimov A, Sazanova A, Kuznetsova I, Vishnyakova M, Safronova V. Draft Genome Sequence of Guar (Cyamopsis tetragonoloba) Microsymbiont Rhizobium sp. Strain RCAM05973. Microbiol. Resour. Announc. 2023;12(6):e0007123. doi: 10.1128/mra.00071-23.

13. Yuzikhin O.S., Shaposhnikov A.I., Konnova T.A., Syrova D.S., Hamo H., Ermekkaliev T.S.; Shevchenko V.P., Shevchenko K.V., Gogoleva N.E., Nizhnikov A.A., Safronova V.I., Kamnev A.A., Belimov A.A., Gogolev Y.V. Isolation and Characterization of 1-Hydroxy-2,6,6-trimethyl-4-oxo-2-cyclohexene-1-acetic acid, a metabolite in bacterial transformation of abscisic acid. Biomolecules, 2022, 12, 1508. doi:10.3390/biom12101508.

14. Karlov D., Sazanova A., Guro P., Kuznetsova I., Verkhozina A., Belimov A., Safronova V. Genetic diversity of rhizobial strains isolated from the relict legumesGueldenstaedtia monophyllaandvernagrowing in the republics of Altai and Buryatia (Russia). Biological Communications, 2022, 67(3), 141–151. doi:10.21638/spbu03.2022.301.

15. Kichko, A.A., Gladkov, G.V., Ulianich, P.S., Safronova, V.I., Pinaev, A.G., Sekste, E.A., Belimov, A.A., Andronov, E.E. Water stress, cadmium, and plant genotype modulate the rhizosphere microbiome ofPisum sativumPlants,2022,11, 3013. https://doi.org/10.3390/plants11223013.

16. Brazhnikova Y.V., Shaposhnikov A.I., Sazanova A.L., Belimov A.A., Mukasheva T.D., Ignatova L.V. Phosphate mobilization by culturable fungi and their capacity to increase soil p availability and promote barley growth. Current Microbiology, 2022, 79(8), 240. doi: 10.1007/s00284-022-02926-1. PMID: 35792979.

17. Belimov A.A., Shaposhnikov A.I., Azarova T.S., Syrova D.S., Kitaeva A.B., Ulyanich P.S., Yuzikhin O.S., Sekste E.A., Safronova V.I., Vishnyakova M.A., Tsyganov V.E., Tikhonovich I.A. Rhizobacteria mitigate the negative effect of aluminum on pea growth by immobilizing the toxicant and modulating root exudation.Plants,2022, 11(18), 2416, doi:10.3390/plants11182416.

18. Sazanova A., Safronova V., Belimov A., Gogolev Y., Chirak E., Karlov D., Kuznetsova I., Kuzmina L., Tikhonovich I. Complete genome sequence ofRhizobiumstrain RCAM05350 from Shulgan-Tash karst cave. Microbiology Resource Announcements. 2022, 11(10), e0056922. doi: 10.1128/mra.00569-22.

19. Belimov A.A., Ulianich P.S., Syrova D.S., Shaposhnikov A.I., Safronova V.I., Dodd I.C. Modulation of tomato root architecture and root hair traits byPseudomonas brassicacearumandVariovorax paradoxuscontaining 1-aminocyclopropane-1-carboxylate deaminase. Biologia Plantarum, 2022, 66. 228-239. Doi:10.32615/bp.2022.025.

20. Syrova, D.S., Shaposhnikov, A.I., Yuzikhin, O.S., Belimov A.A. Destruction and transformation of phytohormones by microorganisms. Applied Biochemistry and Microbiology, 2022, 58, 1–18 DOI: 10.1134/S0003683822010094.

21. Ulianich P.S., Belimov A.A., Kuznetsova I.G., Sazanova A.L., Yuzikhin O.S., Laktionov Yu.V., Karlov D.S., Vishnyakova M.A., Safronova V.I. Efficiency of nitrogen-fixing symbiosis of guar (Cyamopsis tetragonoloba) with strains ofBradyrhizobium retamaeRCAM05275 andEnsifer aridiRCAM05276 in a vegetative experiment. Agricultural Biology, 2022, V. 57, №3, с. 555-565. doi: 10.15389/agrobiology.2022.3.555eng.

22. Yermekkaliyev T.S., Gogoleva N.E., Gogolev Yu.V., Konnova T.A., Shevchenko V.P., Nagaev I.Yu., Shaposhnikov A.I., Shevchenko K.V., Belimov A.A., Syrova D.S., Yuzikhin O.S., Myasoedov N.F. Metabolism by rhizobacteria of abscisic acid deuterated in the cyclohexene part // Pharmaceutical Chemistry Journal 2021. V. 55. P. 745–749. DOI: 10.1007/s11094-021-02487-w.

23. Jin K., Li H., Li X., Li H., Dodd I.C., Belimov A.A., Davies W.J., Shen J. Rhizosphere bacteria containing ACC deaminase decrease root ethylene emission and improve maize root growth with localized nutrient supply. Food and Energy Security, 2021, 10, 2, 275-284. https://doi.org/10.1002/fes3.278.

24. Yuzikhin O.S., Gogoleva N.E., Shaposhnikov A.I., Konnova T.A., Osipova E.V., Syrova D.S., Ermakova E.S., Shevchenko V.P., Nagaev I.Yu., Shevchenko K.V., Myasoedov N.F., Safronova V.I., Shavarda A.L., Nizhnikov A.A., Belimov A.A., Gogolev Yu.V. Rhizosphere bacteriumRhodococcussp.P1Y metabolizes abscisic acid to form dehydrovomifoliol // Biomolecules. 2021. V. 11. Article 345. DOI: 10.3390/biom11030345.

25. Karlov D., Sazanova A., Kuznetsova I., Tikhomirova N., Popova Z., Osledkin Y., Demidov N., Belimov A., Safronova V.Rhizobial isolates in active layer samples of permafrost soil of Spitsbergen, Arctic// Biological communications. 2021. V. 66. № 1. P. 73–82. DOI: 10.21638/spbu03.2021.109.

26. Khudyakov I., Gladkov G., Elhai J. Inactivation of three RG(S/T)GR pentapeptide-containing negative regulators of HetR results in lethal differentiation ofAnabaenaPCC 7120. Life (Basel), 2020, V. 4; 10(12):326. DOI: 10.3390/life10120326.

27. Zhou Y., Xu X., Wei Y., Cheng Y., Guo Y., Khudyakov I., Liu F., He P., Song Z., Li Z., Gao Y., Ang E.L., Zhao H., Zhang Y., Zhao S. A widespread pathway for substitution of adenine by diaminopurine in phage genomes. Science 2021, 372, (6541):512-516. DOI: 10.1126/science.abe4882.

28. Kolesnikov L.E., Belimov A.A., Kudryavtseva E.Y., Hassan B.A., Kolesnikova Yu.R. Identification of the effectiveness of associative rhizobacteria in spring wheat cultivation // Agronomy Research. 2021. V. 19. № 3, 1530–1544. DOI: 10.15159/AR.21.145.

29. Safronova V, Sazanova A, Kuznetsova I, Belimov A, Guro P, Karlov D, Yuzikhin O, Chirak E, Verkhozina A, Afonin A, Andronov E, Tikhonovich I. Increasing the legume–rhizobia symbiotic efficiency due to the synergy between commercial strains and strains isolated from relict symbiotic systems //Agronomy.V. 11. № 7. Article 1398. DOI: 10.3390/agronomy11071398.

30. Teijeiro G.R., Belimov A.A., Dodd, I.C. Microbial inoculum development for amelioration of crop drought stress: a case study ofVariovorax paradoxus5C-2. New Biotechnology, 2020, 56, 103-113. https://doi.org/10.1016/j.nbt.2019.12.006.

31. Kargapolova K.Yu., Burygin G.L., Tkachenko O.V., Evseeva N.V., Pukhalskiy Y.V. Belimov A.A. Effectiveness of inoculation of in vitro‑grown potato microplants with rhizosphere bacteria of the genusAzospirillum. Plant Cell, Tissue and Organ Culture, 2020, 141, 351–359. https://doi.org/10.1007/s11240-020-01791-9

32. Zverev A.O., Pershina E.V., Shapkin V.M., Kichko A.K., Mitrofanova O.P., Kobylyanskii V.D., Yuzikhin O.S., Belimov A.A., Andronov E.E. Molecular analysis of the rhizosphere microbial communities from gramineous plants grown on contrasting soils. Microbiology, 2020, 89, 231–241. https://doi.org/10.1134/S002626172001018X.

33. Petrova S.N., Andronov E.E., Belimov A.A. Beregovaya Yu.V., Denshchikov V.A., Minakov D.L. Prokaryotic community structure in the rapeseed (Brassica napusL.) rhizosphere depending on addition of 1-aminocyclopropane-1-carboxylate-utilizing bacteria. Microbiology, 2020, 89, 115–121. https://doi.org/10.1134/S0026261720010117.

34. Belimov A.A., Shaposhnikov A.I., Azarova T.S., Makarova N.M., Safronova V.I., Litvinskiy V.A., Nosikov V.V., Zavalin A.A., Tikhonovich I.A. Microbial Consortium of PGPR, rhizobia and arbuscular mycorrhizal fungus makes pea mutant SGECdtcomparable with Indian mustard in cadmium tolerance and accumulation. Plants, 2020, 9, 975. doi:10.3390/plants9080975.

35. Belimov A.A., Shaposhnikov A.I., Syrova D.S., Kichko A.A., Guro P.V., Yuzikhin O.S., Azarova T.S., Sazanova A.L., Sekste E.A., Litvinskiy V.A., Nosikov V.V., Zavalin A.A., Andronov E.E., Safronova V.I. The role of symbiotic microorganisms, nutrient uptake and rhizosphere bacterial community in response of pea (Pisum sativum) genotypes to elevated Al concentrations in soil. Plants, 2020, 9(12), 1801. Doi:10.3390/plants9121801.

36. Belimov A.A., Dodd I.C., Safronova V.I., Dietz K.-J. Leaf nutrient homeostasis and maintenance of photosynthesis integrity contribute to better adaptation of the pea mutant SGECdtto toxic cadmium. Biologia Plantarum, 2020, 64: 447-453. DOI: 10.32615/bp.2020.061.

37. Tsyganov V.E., Tsyganova A.V., Gorshkov A.P., Seliverstova E.V., Kim V.E., Chizhevskaya E.P., Belimov A.A., Serova T.A., Ivanova K.A., Kulaeva O.A., Kusakin P.G., Kitaeva A.B., Tikhonovich I.A. Efficacy of a plant-microbe system:Pisum sativum(L.) cadmium-tolerant mutant and rhizobium leguminosarum strains, expressing pea metallothionein genesPsMT1andPsMT2, for cadmium phytoremediation. Frontiers in Microbiology, 2020, 11:15. doi: 10.3389/fmicb.2020.00015.

38. Safronova VI, Guro PV, Sazanova AL, Kuznetsova IG, Belimov AA, Yakubov VV, Chirak ER, Afonin AМ, Gogolev YV, Andronov EE, Tikhonovich IA. Rhizobial microsymbionts of KamchatkaOxytropisspecies possess genes of the type III and VI secretion systems, which can affect the development of symbiosis. Molecular Plant Microbe Interactions, 2020, 33, №10, 1232-1241. doi: 10.1094/MPMI-05-20-0114-R.

39. Belimov A.A., Zinovkina N.Y., Safronova V.I., Litvinsky V.A., Nosikov V.V., Zavalin A.A., Tikhonovich I.A. Rhizobial ACC deaminase contributes to efficient symbiosis with pea (Pisum sativum) under single and combined cadmium and water deficit stress. Environmental and Experimental Botany, 2019, 167, 103859, https://doi.org/10.1016/j.envexpbot.2019.103859.

40. Gogoleva N., Nikolaichik Y., Ismailov T., Gorshkov V.Y., Safronova V.I., Belimov A., Gogolev Y. Complete genome sequence of the abscisic acid-utilizing strainNovosphingobiumP6W. 3 Biotech, 2019, 9:94, DOI:10.1007/s13205-019-1625-8.

41. Gogoleva N.E., Nikolaichik Y., Ismailov T., Khlopko Yu.A., Dmitrieva S.A., Konnova T.A., Ermekkaliev T.S., Safronova V.I., Belimov A.A., Gogolev Yu.V. Complete genome sequence of the abscisic acid-metabolizing rhizobacteriumRhodococcusstrain P1Y. Microbiology Resource Announcements, 2019, 8(15) e01591-18, DOI: 10.1128/MRA.01591-18.

42. Syrova D.S., Shaposhnikov A.I., Makarova N.M., Gagkaeva T.Y., Khrapalova I.A., Emelyanov V.V., Gogolev Y.V., Gannibal Ph.B., Belimov A.A. The ability of some species of phytopathogenic fungi to produce abscisic acid. Mycology and Phytopathology, 2019, 53, №5, 301–310. DOI: 1134/S0026364819050064.

43. Safronova V., Belimov A., Sazanova A., Chirak E., Kuznetsova I., Andronov E. Pinaev A., Tsyganova A., Seliverstova E., Kitaeva A., Tsyganov V. and Tikhonovich I. Two broad host range rhizobial strains isolated from relict legumes have various complementary effects on symbiotic parameters of co-inoculated plants. Frontiers in Microbiology 10:514. doi: 10.3389/fmicb.2019.00514.

44. Sazanova A.L., Safronova V.I., Kuznetsova I.G., Karlov D.S., Belimov A.A., Andronov E.E., Chirak E.R., Popova J.P., Verkhozina A.V., Willems A., Tikhonovich I.A.Bosea caraganaenov. a new species of slow-growing rhizobia isolated from root nodules of the relict speciesCaragana jubata(Pall.) Poir. originating from Mongolia. Int. J. Syst. Evol. Microbiol., 2019, 69(9), 2687-2695. doi: 10.1099/ijsem.0.003509.

45. Karlov D.S., Sazanova A.L., Kuznetsova I.G., Safronova V.I., Tikhomirova N.Yu., Popova Zh.P., Osledkin Yu.S., Verkhozina A.V., Belimov A.A. Genetic diversity of microsymbionts of thermopsis lanceolate (Thermopsis lanceolata), growing in Mongolia. Ecological genetics. 2019, Vol. 17, №1, 43-51.

46. Shaposhnikov A.I., Vishnevskaya N.A., Shakhnazarova V.Yu., Belimov A.A., Strunnikova O.K. The role of barley root exudates as a food source in the relationship betweenFusarium culmorumandPseudomonas fluorescens. Mycology and Phytopathology. 2019, 53, 5, 311-318. DOI: 10.1134 / S0026364819050052.

47. Kimeklis A.K., Chirak E.R., Kuznetsova I.G., Sazanova A.L., Safronova V.I., Belimov A.A., Onishchuk O.P., Kurchak O.N., Aksenova Т.S., Pinaev A.G., Andronov E.E., Provorov N.A. Rhizobia Isolated from the relict legumeVavilovia formosarepresent a genetically specific group withinRhizobium leguminosarumbiovarviciae.Genes,2019,10,https://doi.org/10.3390/genes10120990.

48. Chirak E.R., Kimeklis A.K., Karasev E.S., Kopat V.V., Safronova V.I., Belimov A.A., Aksenova T.S., Kabilov M.R., Provorov N.A., Andronov E.E. Search for ancestral features in genomes ofRhizobium leguminosarumViciaestrains isolated from the relict legumeVavilovia formosa.Genes,2019,10,990. https://doi.org/10.3390/genes10120990.

49. Elhai J., Khudyakov I. Ancient association of cyanobacterial multicellularity with the regulator HetR and an RGSGR pentapeptide‐containing protein (PatX). Molecular Microbiology, 2018, 110, №6, 931-954.

50. Belimov A.A., Malkov N.V., Puhalsky J.V., Tsyganov V.E., Bodyagina K.B., Safronova V.I., Dietz K.-J., Tikhonovich I.A. The crucial role of roots in increased Cd-tolerance and Cd-accumulation in the pea (Pisum sativum) mutant SGECdt. Biologia Plantarum, 2018, 62(3), 543-550.

51. Shevchenko V.P., Nagaev I.Yu., Shaposhnikov A.I., Shevchenko K.V., Belimov A.A., Batasheva S.N., Gogoleva N.E., Gogolev Yu.V., Myasoedov N.F. Synthesis and testing of abscisic acid with predominant replacement of protium atoms by tritium in the cyclohexene moiety. Doklady Chemistry, 2018, 483(3), Part 1, 268–271.

52. Kimeklis A.K., Kuznetsova I.G., Sazanova A.L., Safronova V.I., Belimov A.A., Onishchuk O.P., Kurchak O.N., Aksenova T.S., Pinaev A.G., Andronov E.E., Provorov N.A., Musaev A.M. Divergent evolution of symbiotic bacteria: rhizobia of the relic legumeVavilovia formosaform an isolated group withinRhizobium leguminosarumbv.viciae.Russian Journal of Genetics. 2018. Т. 54. № 7. С. 866-870.

53. Raheem A., Shaposhnikov A., Belimov A.A., Dodd I.C., Ali B. Auxin production by rhizobacteria was associated with improved yield of wheat (Triticum aestivum) under drought stress. Archives of Agronomy and Soil Science , 2018 , 64 , 4, 574-587.

54. Safronova V.I., Sazanova A.L., Kuznetsova I.G., Belimov A.A., Andronov E.E., Chirak E.R., Popova J.P., Tikhonovich I.A., Verkhozina A.V., Willems A.Phyllobacterium zundukensenov., a novel species of rhizobia isolated from root nodules of the legume speciesOxytropis triphylla(pall.) Pers. International Journal of Systematic and Evolutionary Microbiology. 2018, 1644-1651.

55. Safronova V.I., Belimov A.A., Sazanova A.L., Chirak E.R., Kuznetsova I.G., Andronov E.E., Puhalsky J.V., Tikhonovich I.A., Verkhozina A.V. Taxonomically different co-microsymbionts of a relict legume,Oxytropis popoviana, have complementary sets of symbiotic genes and together increase the efficiency of plant nodulation. Molecular Plant-Microbe Interactions. 2018, 31(8), 833-841.

56. Mironicheva A., Gogoleva N., Nikolaichik Y., Khlopko Y., Safronova V.I., Ermekkaliev T., Belimov A.A., Gogolev Y. Genetic and physiological characteristics of the abscisic acid metabolizing rhizobacteria. FEBS Open Bio. 2018, 8, S1, 471.

57. Ismailov T., Gogoleva N., Mironichewa A., Balkin A., Belimov A.A., Kovtunov Y., Gogolev Y. Transcriptome analysis of the abscisic acid metabolizing rhizobacteria. FEBS Open Bio . 2018, 8, S 1, 471.

58. Beregovaya Yu.V., Tychinskaya I.L., Petrova S.N., Parahin N.V., Puhalsky J.V., Makarova N.M., Shaposhnikov A.I., Belimov A.A. Cultivar specificity of the rhizobacterial effects on nitrogen-fixing symbiosis and mineral nutrition of soybean under agrocenosis conditions. Agricultural Biology, 2018, 53, № 5, 977-993. doi: 10.15389/agrobiology.2018.5.977eng.

59. Leppyanen I.V., Shakhnazarova V.Y., Shtark O.Y., Vishnevskaya N.A., Tikhonovich I.A., Dolgikh E . Receptor-like kinase LYK9 inPisum sativumL. is the CERK1-like receptor that controls both plant immunity and AM symbiosis development. International Journal of Molecular Sciences, 201 8, 19, 8 .

60. Strunnikova O., Vishnevskaya N., Shakhnazarova V., Lentsman N. Development of two strains ofFusarium culmorumwith a different aggressiveness in the soil and on the roots of barley of two genotypes. European Journal of Plant Pathology, 2018,. 151, 579-592.

61. Kuzmicheva Y.V., Shaposhnikov A.I., Petrova S.N., Makarova N.M., Tychinskaya I.L., Puhalsky J.V., Parahin N.V., Tikhonovich I.A., Belimov A.A. Variety specific relationships between effects of rhizobacteria on root exudation, growth and nutrient uptake of soybean. Plant and Soil , 2017, 419, 83-96.

62. Kopat V.V., Chirak E.R., Kimeklis A.K., Safronova V.I., Belimov A.A., Kabilov M.R., Andronov E.E., Provorov N.A. Evolution offixNOQPgenes encoding cytochrome oxidase with high affinity to oxygen in Rhizobia and related bacteria. Russian Journal of Genetics, 2017, 53(7), 766–774. DOI: 10.1134/S1022795417070067.

63. Safronova V., Belimov A., Sazanova A., Kuznetsova I., Popova J., Andronov E., Verkhozina A., Tikhonovich I. Does the Miocene-Pliocene relict legumeOxytropis triphyllaform nitrogen-fixing nodules with a combination of bacterial strains? International Journal of Environmental Studies , 2017, 74:5, 706-714.

64. Safronova V., Belimov A., Andronov E., Popova J., Tikhomirova N., Orlova O., Verkhozina A., Chimitov D., Tikhonovich I. Method for obtaining root nodules of the Baikal relict legumes in laboratory pot experiments. International Journal of Environmental Studies , 2017, 74:5, 700-705 .

65. Puhalsky Ya.V., Vishnyakova M.A., Loskutov S.I., Semenova E.V., Sekste E.A., Shaposhnikov A.I., Belimov A.A., Tikhonovich I.A. Pea (Pisum sativumL.) cultivars with low accumulation of heavy metals from contaminated soil. Agricultural Biology, 2017, 52, 3, 597-606. Doi: 10.15389/agrobiology.2017.3.597eng.

66. Safronova V.I., Kuznetsova I.G., Sazanova A.L., Belimov A.A., Andronov E.E., Chirak E.R., Osledkin Y.S., Onishchuk O.P., Kurchak O.N., Shaposhnikov A.I., Tikhonovich I.A., Willems A. Microvirga ossetica sp. nov., a species of rhizobia isolated from root nodules of the legume species Vicia alpestris Steven. International Journal of Systematic and Evolutionary Microbiology . 2017 , 67. № 1 , 94-100.

67. Kichigina N.E., Pukhalsky Ya.V., Shaposhnikov A.I., Azarova T.S., Makarova N.M., Loskutov S.I., Safronova V.I., Tikhonovich I.A., Vishniyakova M.A., Semenova E.V., Kosareva I.A., Belimov A.A. Aluminum exclusion from root zone and maintenance of nutrient uptake are principal mechanisms of al tolerance inPisum sativumPhysiology and Molecular Biology of Plants . 2017, 23, 4, 851–863.

68. Raheem A., Shaposhnikov A., Belimov A.A., Dodd I.C., Ali B. Auxin production by rhizobacteria was associated with improved yield of wheat (Triticum aestivum) under drought stress. Archives of Agronomy and Soil Science. 2018, 64, 4, 574-587.

69. Strunnikova O., Vishnevskaya N., Shakhnazarova V., Lentsman N. Development of two strains ofFusarium culmorumwith a different aggressiveness in the soil and on the roots of barley of two genotypes. European J ournal of Plant Pathol jgy, 2017, 151, 3, 579–592 .

70. Leppyanen I., Shakhnazarova V ., Shtark O ., Vishnevskaya N ., Tikhonovich I ., Dolgikh E . Receptor-like kinase LYK9 inPisum sativumis the CERK1-like receptor that controls both plant immunity and AM symbiosis development // International Journal of Molecular Science, 2018, 19, 8.

71. Leppanen I. V., Shakhnazarova V. Yu., Vishnevskaya N. A., Dolgikh E. A., Strunnikova O. TO . Study of the mechanisms of relationships between pea Pisum sativum and two strains of Fusarium culmorum with different aggressiveness. Mycology and phytopathology. 2017. 4: 241-248

72. Wang Q., Dodd I.C., Belimov A.A., Jiang F. Rhizosphere bacteria containing 1-aminocyclopropane-1- carboxylate deaminase increase growth and photosynthesis of pea plants under salt stress by limiting Na+Functional Plant Biology. 2016, 43, 161–172.

73. Belimov A.A., Malkov N.V., Puhalsky J.V., Safronova V.I., Tikhonovich I.A. High specificity in response of pea mutant SGECdtto toxic metals: growth and element composition. Environmental and Experimental Botany . 2016, 128, 91-98.

74. Safronova V.I., Kuznetsova I.G., Sazanova A.L., Belimov A.A., Andronov E.E., Chirak E.R., Osledkin Y.S., Onishchuk O.P., Kurchak O.N., Shaposhnikov A.I., Willems A., Tikhonovich I.A.Microvirga osseticanov. a new species of rhizobia isolated from root nodules of the legume speciesVicia alpestrisSteven originated from North Ossetia region in the Caucasus. International Journal of Systematic and Evolutionary Microbiology. 2016, 67(1), 94-100.

75. Shaposhnikov A.I., Morgunov A.I., Akin B., Makarova N.M., Belimov A.A., Tikhonovich I.A. Comparative characteristics of root systems and root exudation of synthetic, landrace and modern wheat varieties. Agricultural Biology, 2016, 51, 3, 68-78.

76. Vishnyakova M.A., Semenova E.V., Kosareva I.A., Kravchuk N.D., Loskutov S.I., Puhalskii I.V., Shaposhnikov A.I., Sazanova A.L., Belimov A.A. Method for rapid assessment of aluminum tolerance of pea (Pisum sativumL.). Sel’skokhozyaistvennaya biologiya [Agricultural Biology], 2015, V. 50, 3, 353-360.

77. Kuznetsova I.G., Sazanova A.L., Safronova V.I., Pinaev A.G., Verkhozina A.V., Tikhomirova N.Y., Osledkin Y.S., Belimov A.A. Genetic diversity among microsymbionts ofLathyrus,Vicia,OxytropisandAstragaluslegume species from Baikal region. Sel’skokhozyaistvennaya biologiya [Agricultural Biology], 2015, V. 50, 3, 345-352.

78. Belimov A., Dodd I., Safronova V., Shaposhnikov A., Azarova T., Makarova N., Davies W., Tikhonovich I. Rhizobacteria that produce auxins and contain 1-amino-cyclopropane-1-carboxylic acid deaminase decrease amino acid concentrations in the rhizosphere and improve growth and yield of well-watered and water-limited potato (Solanum tuberosum). Annals of Applied Biology, 2015, 167(1), 11-25.

79. Belimov A., Puhalsky I., Safronova V., ShaposhnikovA., Vishnyakova M., Semenova E., Zinovkina N., Makarova N., Wenzel W., Tikhonovich I. Role of plant genotype and soil conditions in symbiotic plant-microbe interactions for adaptation of plants to cadmium-polluted soils. Water Air and Soil Pollution, 2015, 226: 264.

80. Belimov A., Dodd I., Safronova V., Malkov N., Davies W., Tikhonovich I. The cadmium-tolerant pea (Pisum sativum) mutant SGECdtis more sensitive to mercury: assessing plant water relations. Journal of Experimental Botany, 2015, 66(8), 2359-2369.

81. Safronova V., Kuznetsova I., Sazanova A.,·Kimeklis A., Belimov A., Andronov E., Pinaev A., Pukhaev A., Popov K.,·Akopian J., Willems A., Tikhonovich I. Extra ‑ slow ‑ growingTardiphagastrains isolated from nodules ofVavilovia formosa(Stev.) Fed. Archives of Microbiology, 2015, 197(7), 889-898.

82. Strunnikova O.K., Vishnevskaya N.A., Ruchiy A.S., Shakhnazarova V.Yu., Vorobyov N.I., Chebotar V.K. The influence of soils with different textures on development, colonization capacity and interactions betweenFusarium culmorumandPseudomonas fluorescensin soil and on barley roots. Plant and Soil , 2015, 389, 131 - 144.

83. Kimeklis A.K., Safronova V.I., Kuznetsova I.G., Sazanova A.L., Belimov A.A., Pinaev A.G., Chizhevskaya E.P., Pukhaev A.R., Popov K. L.P., Andronov E.E., Provorov N.A. Phylogenetic analysis of strains of the genus Rhizobium isolated from nodules of Vavilovia formosa (stev.) Fed. Agricultural Biology, 2015, 50(5), 655-664.

84. Kuzmicheva Yu.V., Shaposhnikov A.I., Azarova N.S., Petrova S.N., Naumkina T.S., Borisov A.Yu., Belimov A.A., Kravchenko L.V., Parakhin N.V., Tikhonovich I.A. Composition of root exometabolites of the symbiotically effective pea cultivar triumph and its parental forms. Russian Journal of Plant Physiology, 2014, 61, 1, 112–118.

85. Belimov A.A, Dodd I.C., Safronova V.I., Dumova V.A., Shaposhnikov A.I., Ladatko A.G., Davies W.J. Abscisic acid metabolizing rhizobacteria decrease ABA concentrationsin plantaand alter plant growth. Plant Physiology and Biochemistry, 2014, 74, 84-91.

86. Safronova V.I. Kimeklis A.K., Chizhevskaya E.P., Belimov A.A., Andronov E.E., Pinaev A.G., Pukhaev A.R., Popov K.P., Tikhonovich I.A. Genetic diversity of rhizobia isolated from nodules of the relic speciesVavilovia formosa(Stev.) Fed. Antonie van Leeuwenhoek, 2014, 105, 389–399.

87. Strunnikova O.K., Vishnevskaya N.A., Ruchiy A.S., Shakhnazarova V.Y. Vorobyov N.I., Chebotar V.K. The influence of soils with different textures on development, olonization capacity and interactions betweenFusarium culmorumandPseudomonas fluorescensin soil and on barley roots.Plant and Soil, 2014, DOI 10.1007/s11104-014-2351-y.

88. Strunnikova O.K., Shakhnazarova V.Yu., Vishnevskaya N.A., Ruchiy A.S., Chizhevskaya E.P. Features of barley colonization by the soil-dwelling fungus Fusarium culmorum. Mycology and Phytopathology, 2013, 47, 3, 196–203.

89. Shcherbakov A.V., Bragina A.V., Kuzmina E.Yu., Berg K., Muntyan A.N., Makarova N.M., Malfanova N.V., Cardinale M., Berg G., Chebotar V. .K., Tikhonovich I.A. Endophytic bacteria of sphagnum mosses as promising objects of agricultural microbiology. Microbiology, 2013, 82, No. 3, 312-322.

90. Dodd I.C., Belimov A.A, Elphinstone E.D., Chen L., Teijeiro R.G., Kemp C., Fielding H., Wright H. Exploiting rhizobacteria that mediate plant hormone status. Aspects of Applied Biology 120 , 2013, 29-34.

91. Jiang F., Chen L., Belimov A.A., Shaposhnikov A.I., Gong F ., Meng X., Hartung W., Jeschke D.W., Davies W.J., Dodd I.C. Multiple impacts of the plant growth promoting rhizobacteriumVariovorax paradoxus5C-2 on nutrient and ABA relations ofPisum sativum.Journal of Experimental Botany, 2012, 63, 6421-6430.

92. Safronova V.I., Piluzza G., Zinovkina N.Y., Kimeklis A.K., Belimov A.A., Bullitta S. Relationships between pasture legumes, rhizobacteria an nodule bacteria in heavy metal polluted mine waste of SW Sardinia. Symbiosis, 2012, DOI 10.1007/k13199-012-0207-x.

93. Chen L., Dodd I.C., Theobald J.C., Belimov A.A., Davies W.J. The rhizobacteriumVariovorax paradoxus5C-2, containing ACC deaminase, promotes growth and development ofArabidopsis thalianavia an ethylene-dependent pathway. Journal of Experimental Botany. 2012. V . 64, P. 1565-1573.

94. Baymiev An. K., Ivanova E.S., Ptitzyn K.G., Belimov A.A., Safronova V.I., Baymiev Al.K. Genetic characterization of nodule bacteria of wild legumes living in the South Ural. Molecular Genetic, Microbiology and Virology, 2012, 1, 29-34.

95. Belimov A.A., Demchinskaya S.V., Safronova V.I. Reaction of pea plants on inoculation by rhizosphere 1-aminocyclopropane-1-carboxylate (ACC) utilizing bacteria in the presence of endomycorrhizal fungusGlomus intraradices. Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2012, №3, 90-97.

96. Shakhnazarova V. Yu., Feoktistova A. S., Chizhevskaya E. P., Vishnevskaya N.A., Strunnikova O.K. Optimization of the DNA extraction method for the identification and quantification ofFusarium culmorumin the roots of barley and wheat by PCR. Mycology and Phytopathology, 2012, 46, 4, 287–292.

97. Khudyakov I.Ya. Developmental genetics and symbiotic potential of cyanobacteria. Ecological genetics, 2012. X, 4, pp. 14-28.

98. Shaposhnikov A.I., Azarova T.S., Kravchenko L.V., A.A. Bazhanova, D.P. Bazhanov, O.G. Babak, N.A. Nekrashevich, A.V. Kilchevsky. Root secretions of tomato genotypes (Solanumlycopersicum L.), characterized by responsiveness to bacterization // Molecular and Applied Genetics. 2012. T. 14. S. 63-68.

99. Egamberdieva D., Kucharova Z., Davranov K, Berg G., Makarova N., Azarova T., Chebotar V., Tikhonovich I., Kamilova F., Validov S., Lugtenberg B. Bacteria able to control foot and root rot and to promote growth of cucumber in salinated soil. Biology and Fertility of Soils. 2011, 47, 197-205.

100. Safronova V.I., Piluzza G., Bullitta S., Belimov A.A. Use of legume-microbe symbioses for phytoremediation of heavy metal polluted soils: advantages and potential problems (Review). In: Handbook for Phytoremediation, Golubev I.A. (Ed.), NOVA Sci. , USA, 2011, p. 443-469.

101. Dodd I.C., Zinovkina N.Y., Safronova V.I., Belimov A.A. Rhizobacterial mediation of plant hormone status. Annals of Applied Biology, 2010, 157, 361-379. https://doi.org/10.1111/j.1744-7348.2010.00439.x. Belimov A.A., Dodd I.C., Hontzeas N., Theobald J.C., Safronova V.I., Davies W.J. Rhizosphere bacteria containing ACC deaminase increase yield of plants grown in drying soil via both local and systemic hormone signalling. New Phytologist, 2009, 181, 413-423.

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