doi: 10.15389/agrobiology.2018.5.977eng

UDC 633.34:579.64:631.847.211:631.811

Supported financially by Russian Science Foundation (grant 16-16-00080 for characterization of bacterial inoculum and biologicals, grant 14-16-00137 for field trials, grant 17-76-10039 for plant chemical composition assay) and Russian Foundation for Basic Research (grant 15-04-09023 for nodulation and nitrogen fixation study). Strain deposition was fulfilled within the frame of FANO Russia Program of development and inventory of bio resources



Yu.V. Beregovaya1, I.L. Tychinskaya1, S.N. Petrova1, N.V. Parahin1,
J.V. Puhalsky2, N.M. Makarova2, A.I. Shaposhnikov2, A.A. Belimov2

1Parakhin Orel State Agrarian University, 69, ul. Generala Rodina, Orel, 302019 Russia, e-mail,,
2All-Russian Research Institute for Agricultural Microbiology, Federal Agency for Scientific Organizations, 3, sh. Podbel’skogo, St. Petersburg, 196608 Russia, e-mail,,, (✉ corresponding author)

Beregovaya Yu.V.
Tychinskaya I.L.
Petrova S.N.
Puhalsky J.V.
Makarova N.M.
Shaposhnikov A.I.
Belimov A.A.
The authors declare no conflict of interests

Received November 29, 2017


Stimulation of nitrogen-fixing symbiosis by is an important mechanism of interaction between rhizobacteria and leguminous plants. At the same time, little is known about intraspecific (varietal) variability of leguminous when responding to inoculation with rhizobacteria. Our recent model studies of hydroponic soybean seedlings showed that rhizobacteria Pseudomonas oryzihabitans Ep4 can better stimulate growth and colonize the roots of Nice Mecha and Swapa soybean plants when compared to Bara variety. The purpose of this work was to study the variety-specific responses of soybeans plants to inoculation with rhizosphere bacteria (rhizobacteria) producing auxins and containing 1-aminocyclopropane-1-carboxylate (ACC) deaminase at various levels of plant mineral nutrition under agrocenosis conditions. The subject plants were three early ripening soybean Glycine max (L.) Merr. varieties of the northern ecotypes Nice Mecha, Swapa and Bara. Rhizobacterial strains Pseudomonas oryzihabitans Ep4 and Variovorax paradoxus 3-P4 were used for inoculation. Biopreparation rizotorfin containing a nodule bacterium Bradyrhizobium japonicum strain 634b was used for the formation of nitrogen-fixing symbiosis. Three-year field experiments were conducted in 2013-2015 years in the northernmost area of soybean cultivation (Orel region) on a dark gray forest medium-loamy soil. Mineral fertilizer ‘diamofoska’ was applied 7 days before sowing. Two mineral nutrition levels of N30P81K81 and N44P116K116 were used. In all treatments with rhizotorfin there was an increase in nodule biomass and nodule number, except the treatment of cultivar Bara at N30P81K81. In using lower mineral nutrition with risotorphin, the strain Ps. oryzihabitans Ep4 increased number (by 140 %) and weigh (by 176 %) of nodules and nitrogen-fixing activity (by 69 %) of Swapa plants at flowering. At a higher mineral nutrition the influence of Ps. oryzihabitans Ep4 on the legume-rhizobia symbiosis manifested by the increased nodule number on Swapa roots (by 55 %) and nitrogen-fixing activity of Bara variety (by 205 %), whereas the strain V. paradoxus 3-P4 increased nitrogen fixation of Nice Mecha (by 231 %) and Bara (by 205 %). The positive effects of both rhizobacterial strains on the plant growth at the flowering stage, as well as on the content of nutrients (Mg, Ca, B, Fe, Zn and Mo) in leaves were more pronounced on varieties Nice Mecha and Swapa at lower and/or higher mineral nutrition. At N30P81K81 the increase of shoot biomass at the flowering stage in cultivars Nice Mecha and Swapa was obtained after inoculation with mono-cultures of the studied rhizobacteria and after combination of rhizobacteria with rhizotorfin as well. However cultivar Bara has a positive response to mono-inoculation with rhizotorfin. At N44P116K116 a combined inoculation of cultivar Bara with rhizotorfin and strain Ps. oryzihabitans Ep4, as well as cultivar Nice Mecha with rhizotorfin and strain V. paradoxus 3-P4, was significantly more efficient as compared to mono-inoculation with rhizotorfin. As a rule, the positive effects of both rhizobacterial strains on plant growth at flowering, as well as on the content of nutrient elements (Mg, Ca, B, Fe, Zn and Mo) in leaves, were more pronounced on cultivars Nice Mecha and Swapa at a lower and/or a higher level of mineral nutrition. The maximum effect of rhizobacteria on seed yield and seed quality (protein and fat content) is also obtained by inoculation of varieties Nice Mecha and Swapa. However, variety Bara has the highest response to mineral fertilizers. The differences found between soybean varieties in the response to inoculation with plant growth-promoting rhizobacteria indicate a higher degree of integration between associative microorganisms and varieties Nice Mecha and Swapa compared to variety Bara. The results of this study indicate the promise for creating plant-microbe systems that combine a high degree of symbiotrophy and assimilation of nutrients from fertilizers and soil.

Keywords: Glycine max, Pseudomonas, Variovorax, intraspecies variability, mineral nutrition, rhizosphere, symbiotic nitrogen fixation, phytohormones, agrocenosis.


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