doi: 10.15389/agrobiology.2018.5.977eng

UDC 633.34:579.64:631.847.211:631.811

Acknowledgements:
Supported financially by Russian Science Foundation (grant ¹ 16-16-00080 for characterization of bacterial inoculum and biologicals, grant ¹ 14-16-00137 for field trials, grant ¹ 17-76-10039 for plant chemical composition assay) and Russian Foundation for Basic Research (grant ¹ 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

 

CULTIVAR SPECIFICITY OF THE RHIZOBACTERIAL EFFECTS
ON NITROGEN-FIXING SYMBIOSIS AND MINERAL NUTRITION
OF SOYBEAN UNDER AGROCENOSIS CONDITIONS

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 juliemons@yandex.ru, pridatko1990@mail.ru,
svet-orl@yandex.ru
;
2All-Russian Research Institute for Agricultural Microbiology, Federal Agency for Scientific Organizations, 3, sh. Podbel’skogo, St. Petersburg, 196608 Russia, e-mail jankiss88@gmail.com, nm_makarova@yahoo.com, ai-shaposhnikov@mail.ru, belimov@rambler.ru (✉ corresponding author)

ORCID:
Beregovaya Yu.V. orcid.org/0000-0001-7853-326X
Tychinskaya I.L. orcid.org/0000-0002-9805-8432
Petrova S.N. orcid.org/0000-0003-4482-3458
Puhalsky J.V. orcid.org/0000-0001-5233-3497
Makarova N.M. orcid.org/0000-0003-4781-328X
Shaposhnikov A.I. orcid.org/0000-0003-0771-5589
Belimov A.A. orcid.org/0000-0002-9936-8678
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.

 

Full article (Rus)

Full article (Eng)

 

REFERENCES

  1. Vessey J.K. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil, 2003, 255(2): 571-586 CrossRef
  2. Bashan Y., Holguin G., de-Bashan L.E. Azospirillum-plant relationships: physiological, molecular, agricultural, and environmental advances (1997-2003). Can. J. Microbiol., 2004, 50(8): 521-577 CrossRef
  3. Glick B.R., Cheng Z., Czarny J., Duan J. Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur. J. Plant Pathol., 2007, 119(3): 329-339 CrossRef
  4. Plant growth and health promoting bacteria. D.K. Maheshwari (ed.). Springer-Verlag, Berlin, Heidelberg, 2010 CrossRef
  5. Nascimento F.X., Rossi M.J., Soares C.R.F.S., McConkey B.J., Glick B.R. New insights into 1-aminocyclopropane-1-carboxylate (ACC) deaminase phylogeny, evolution and ecological significance. PLoS ONE, 2014, 9(6): e99168 CrossRef
  6. Korir H., Mungai N.W., Thuita M., Hamba Y., Masso C. Co-inoculation effect of rhizobia and plant growth promoting rhizobacteria on common bean growth in a low phosphorus soil. Front. Plant Sci., 2017, 8: 141 CrossRef
  7. Medeot D.B., Paulucci N.S., Albornoz A.I., Fumero M.V., Bueno M.A., Garcia M.B., Woelke V.R., Okon Y., Dardanelli M.S. Plant growth promoting rhizobacteria improving the legume-rhizobia symbiosis. In: Microbes for legume improvement. M.S. Khan, A. Zaidi, J. Musarrat (eds.). Springer-Verlag, Vienna, 2010: 473-494 CrossRef
  8. Pérez-Montaño F., Alías-Villegas C., Bellogín R.A., del Cerro P., Espuny M.R., Jiménez-Guerrero I., López-Baena F.J., Ollero F.J., Cubo T. Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol. Res., 2014, 169(5-6): 325-336 CrossRef
  9. Polonenko D.R., Scher F.M., Kloepper J.W., Singgleton C.A., Laliberte M., Zaleska I. Effects of roots colonizing bacteria on nodulation of soybean roots by Bradyrhizobium japonicum. Can. J. Microbiol., 1987, 33(6): 498-503 CrossRef
  10. Zhang F., Dashti N., Hynes R.K., Smith D.L. Plant growth promoting rhizobacteria and soybean [Glycine max (L.) Merr.] nodulation and nitrogen fixation at suboptimal root zone temperatures. Annals of Botany, 1996, 77(5): 453-460 CrossRef
  11. Chebotar V.K., Asis C.A., Akao S. Production of growth-promoting substances and high colonization ability of rhizobacteria enhance the nitrogen fixation of soybean when coinoculated with Bradyrhizobium japonicum. Biol. Fert. Soils, 2001, 34(6): 427-432 CrossRef
  12. Hungria M., Nogueira M., Araujo R. Co-inoculation of soybeans and common beans with rhizobia and azospirilla: strategies to improve sustainability. Biol. Fert. Soils, 2013, 49(7): 791-801 CrossRef
  13. Bai Y., D’Aoust F., Smith D.L., Driscoll B.T. Isolation of plant-growth-promoting Bacillus strains from soybean root nodules. Can. J. Microbiol., 2002, 48(3): 230-238 CrossRef
  14. Bai Y., Zhou-Xiao M., Smith D.L. Enhanced soybean plant growth resulting from coinoculation of Bacillus strains with Bradyrhizobium japonicum. Crop Sci., 2003, 43(5): 1774-1781 CrossRef
  15. Atieno M., Herrmann L., Okalebo R., Lesueur D. Efficiency of different formulations of Bradyrhizobium japonicum and effect of co-inoculation of Bacillus subtilis with two different strains of Bradyrhizobium japonicum. World J. Microbiol. Biotechnol., 2012, 28(7): 2541-2550 CrossRef
  16. Tsigie A., Tilak K.V.B.R., Anil K.S. Field response of legumes to inoculation with plant growth-promoting rhizobacteria. Biol. Fert. Soils, 2012, 47: 971-974 CrossRef
  17. Masciarelli O., Llanes A., Luna V. A new PGPR co-inoculated with Bradyrhizobium japonicum enhances soybean nodulation. Microbiol. Res., 2014, 169: 609-615 CrossRef
  18. Mishra P.K., Mishra S., Selvakumar G., Kundu S., Gupta H.S. Enhanced soybean (Glycine max L.) plant growth and nodulation by Bradyrhizobium japonicum-SB1 in presence of Bacillus thuringiensis-KR1. Acta Agr. Scand. B-S. P., 2009, 59(2): 189-196 CrossRef
  19. Diep C.N., My N.T.X., Nhu V.T.P. Isolation and characterization of endophytic bacteria in soybean root nodules. World Journal of Pharmacy and Pharmaceutical Sciences, 2016, 5(6): 222-241.
  20. Shiri-Janagard M., Raei Y., Gasemi-Golezani G., Aliasgarzad N. Influence of Bradyrhizobium japonicum and phosphate solubilizing bacteria on soybean yield at different levels of nitrogen and phosphorus. International Journal of Agronomy and Plant Production, 2012, 3(11): 544-549.
  21. 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 signaling. New Phytol., 2009, 181: 413-423 CrossRef
  22. Gamalero E., Glick B.R. Bacterial modulation of plant ethylene levels. Plant Physiol., 2015, 169: 13-22 CrossRef
  23. Nascimento F.X., Brígido C., Glick B.R., Rossi M.J. The role of rhizobial ACC deaminase in the nodulation process of leguminous plants. International Journal of Agronomy, 2016, 2016: Article ID 1369472 CrossRef
  24. Remans R., Beebe S., Blair M., Manrique G., Tovar E., Rao I., Croonenborghs A., Torres-Gutierrez R., El-Howeity M., Michiels J., Vanderleyden J. Physiological and genetic analysis of root responsiveness to auxin-producing plant growth-promoting bacteria in common bean (Phaseolus vulgaris L.). Plant Soil, 2008, 302(1-2): 149-161 CrossRef
  25. Safronova V.I., Stepanok V.V., Engqvist G.L., Alekseyev Y.V., Belimov A.A. Root-associated bacteria containing 1-aminocyclopropane-1-carboxylate deaminase improve growth and nutrient uptake by pea genotypes cultivated in cadmium supplemented soil. Biol. Fert. Soils, 2006, 42(3): 267-272 CrossRef
  26. Das S.K., Sharma K.L., Neelam S., Srinivas K. Effect of cultivars, nitrogen sources and soil types on response of sorghum (Sorghum bicolor L.) to Azospirillum inoculation. Ann. Agric. Sci., 1997, 18(3): 313-317.
  27. Saubidet M.I., Barneix A.J. Growth stimulation and nitrogen supply to wheat plants inoculated with Azospirillum brasilense. J. Plant Nutr., 1998, 21(12): 2565-2577 CrossRef
  28. Burdman S., Kigel J., Okon Y. Effects of Azospirillum brasilense on nodulation and growth of common bean (Phaseolus vulgaris L.). Soil Biol. Biochem., 1997, 29(5-6): 923-929 CrossRef
  29. Walker V., Bertrand C., Bellvert F., Mënne-Loccoz Y., Bally R., Comte G. Host plant secondary metabolite profiling shows a complex, strain-dependent response of maize to plant growth-promoting rhizobacteria of the genus Azospirillum. New Phytol.,2011, 189(2): 494-506 CrossRef
  30. Dashti N., Zhang F., Hynes R., Smith D.L. Plant growth promoting rhizobacteria accelerate nodulation and increase nitrogen fixation activity by field grown soybean [Glycine max (L.) Merr.] under short season conditions. Plant Soil, 1998, 200(2): 205-213 CrossRef
  31. 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 fungus Glomus intraradices. Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2012, 3: 90-97 CrossRef
  32. Kuzmicheva Yu.V., Shaposhnikov A.I., Azarova T.S., Petrova S.N., Naumkina T.S., Borisov A.Yu., Belimov A.A., Kravchenko L.V., Parakhin N.V., Tikhonovich I.A. Fiziologiya rastenii, 2014, 61(1): 121-128 (in Russ.).
  33. Imran A., Mirza M.S., Shah T.M., Malik K.A., Hafeez F.Y. Differential response of kabuli and desi chickpea genotypes toward inoculation with PGPR in different soils. Front. Microbiol., 2015, 6: 859 CrossRef
  34. Drogue B., Sanguin H., Chamam A., Mozar M., Llauro C., Panaud O., Prigent-Combaret C., Picault N., Wisniewski-Dye F. Plant root transcriptome profiling reveals a strain-dependent response during Azospirillum-rice cooperation. Front. Plant. Sci., 2014, 5: 607 CrossRef
  35. Okubara P.A., Kornoely J.P., Landa B.B. Rhizosphere colonization of hexaploid wheat by Pseudomonas fluorescens strains Q8rl-96 and Q2-87 is cultivar-variable and associated with changes in gross root morphology. Biol. Control, 2004, 30(2): 392-403 CrossRef
  36. Smith K.P., Goodman R.M. Host variation for interactions with beneficial plant-associated microbes. Annu. Rev. Phytopathol., 1999, 37: 473-491 CrossRef
  37. 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 Soil, 2017, 419(1-2): 83-96 CrossRef
  38. Belimov A.A., Safronova V.I., Sergeyeva T.A., Egorova T.N., Matveyeva V.A., Tsyganov V.E., Borisov A.Y., Tikhonovich I.A., Kluge C., Preisfeld A., Dietz K.J., Stepanok V.V. Characterisation of plant growth-promoting rhizobacteria isolated from polluted soils and containing 1-aminocyclopropane-1-carboxylate deaminase. Can. J. Microbiol., 2001, 47(7): 642-652 CrossRef
  39. Belimov A.A., Hontzeas N., Safronova V.I., Demchinskaya S.V., Piluzza G., Bullitta S., Glick B.R. Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol. Biochem., 2005, 37(2): 241-250 CrossRef
  40. Laktionov Yu.V., Popova T.A., Andreev O.A., Ibatullina R.P., Kozhemyakov A.P. Creating new forms of growth-stimulating microbial preparations and their performance on various cultures. Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2011, 3: 116-118 (in Russ.).
  41. Arinushkina E.V. Guidelines for the chemical analysis of soils. Moscow State University Press, Moscow, 1970.
  42. Hardy R.W.F., Bums R.C., Holsten R.D. Application of the C2H2-C2H4 assay for measurement of nitrogen fixation. Soil Biol. Biochem., 1973, 5(1): 47-82 CrossRef
  43. Preston G.M. Plant perceptions of plant growth-promoting Pseudomonas. Philos. T. Roy. Soc. B, 2004, 359(1446): 907-918 CrossRef
  44. Patten C.L., Glick B.R. Bacterial biosynthesis of indole-3-acetic acid. Can. J. Microbiol., 1996, 42(3): 207-220 CrossRef
  45. Spaepen S., Vanderleyden J., Remans R. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. Rev., 2007, 31(4): 425-448 CrossRef
  46. Badri D.V., Quintana N., El-Kassis E.G., Kim H.K., Choi Y.H., Sugiyama A., Verpoorte R., Martinoia E., Manter D.K., Vivanco J.M. An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota. Plant Physiol., 2009, 151: 2006-2017 CrossRef
  47. Saleem M., Arshad M., Hussain S., Bhatti A.S. Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J. Ind. Microbiol. Biot., 2007, 34(10): 635-648 CrossRef
  48. Krotzky A., Bergold R., Werner D. Plant characteristics limiting associative N2 fixation with two cultivars of sorghum mutants. Soil Biol. Biochem., 1988, 20(2): 157-162 CrossRef
  49. Verma J.P., Yadav J., Tiwari K.N. Enhancement of nodulation and yield of chickpea by co-inoculation of indigenous Mesorhizobium spp. and plant growth-promoting rhizobacteria in Eastern Uttar Pradesh. Commun. Soil Sci. Plan., 2012, 43(3): 605-621 CrossRef
  50. Wani P.A., Khan M.S., Zaidi A. Co-inoculation of nitrogen fixing and phosphate solubilizing bacteria to promote growth, yield and nutrient uptake in chickpea. Acta Agron. Hung., 2007, 55(3): 315-323 CrossRef
  51. Elkoca E., Turan M., Donmez M.F. Effects of single, dual and triple inoculations with Bacillus subtilis, Bacillus megaterium and Rhizobium leguminosarum bv. phaseoli on nodulation, nutrient uptake, yield and yield parameters of common bean (Phaseolus vulgaris L. cv. ‘ELKOCA-05’). J. Plant Nutr., 2010, 33(14): 2104-2119 CrossRef
  52. Figueiredo M.V.B., Martinez C.R., Burity H.A., Chanway C.P. Plant growth-promoting rhizobacteria for improving nodulation and nitrogen fixation in the common bean (Phaseolus vulgaris L.). World J. Microb. Biot., 2008, 24(7): 1187-1193 CrossRef
  53. Yadegari M., Asadi Rahmani H., Noormohammadi G., Ayneband A. Plant growth promoting rhizobacteria increase growth, yield and nitrogen fixation in Phaseolus vulgaris. J. Plant Nutr., 2010, 33(12): 1733-1743 CrossRef
  54. Tilak K.V.B.R., Ranganayaki N., Manoharachari C. Synergistic effects of plant-growth promoting rhizobacteria and Rhizobium on nodulation and nitrogen fixation by pigeon pea (Cajanus cajan). Eur. J. Soil Sci., 2006, 57(1): 67-71 CrossRef
  55. Dileep Kumar B.S., Berggren I., Mårtensson A.M. Potential for improving pea production by co-inoculation with fluorescent Pseudomonas and Rhizobium. Plant Soil, 2001, 229(1): 25-34 CrossRef
  56. Mishra P.K., Mishra S., Selvakumar G., Bisht J. K., Kundu S., Gupta H.S. Co-inoculation of Bacillus thuringeinsis-KR1 with Rhizobium leguminosarum enhances plant growth and nodulation of pea (Pisum sativum L.) and lentil (Lens culinaris L.). World J. Microb. Biot., 2009, 25(5): 753-761 CrossRef
  57. Qureshi M.A., Shakir M.A., Iqbal A., Akhtar N., Khan A. Co-inoculation of phosphate solubilizing bacteria and rhizobia for improving growth and yield of mungbean (Vigna radiata L.). J. Anim. Plant Sci., 2012, 21(3): 491-497.
  58. Guinazu L.B., Andres J.A., Del Papa M.F., Pistorio M., Rosas S.B. Response of alfalfa (Medicago sativa L.) to single and mixed inoculation with phosphate-solubilising bacteria and Sinorhizobium meliloti. Biol. Fert. Soils, 2010, 46(2): 185-190 CrossRef
  59. 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+ accumulation. Funct. Plant Biol., 2016, 43(2): 161-172.
  60. Belimov A.A., Puhalsky I.V., Safronova V.I., Shaposhnikov A.I., Vishnyakova M.A., Semenova E.V., Zinovkina N.Y., Makarova N.M., Wenzel W., Tikhonovich I.A. Role of plant genotype and soil conditions in symbiotic plant-microbe interactions for adaptation of plants to cadmium polluted soils. Water Air Soil Poll., 2015, 226(8): 1-15 CrossRef

back