N.V. Feoktistova*, A.M. Mardanova**, G.F. Hadieva, M.R. Sharipova

Kazan Federal University, Kazan, 420008 Russia

E-mail: *nfeoktis@mail.ru, **mardanovaayslu@mail.ru

Full text PDF

Abstract

The review deals with the analysis of modern literature data on rhizosphere bacteria and their role in plant life. The structure of rhizosphere has been characterized. The role of plants as the centers of formation of microbial communities has been shown. Data on the main groups of microorganisms inhabiting the rhizosphere have been provided. The associative relationship between rhizobacteria and partner plants has been investigated. The modern concept of holobiont defined as the whole host plant organism and microorganisms associated with it has been reviewed. The role of rhizobacteria in the processes of nitrogen fixation has been discussed in detail. The mechanisms of direct stimulation of plant growth by biosynthesis of phytohormones, improvement of phosphorus and nitrogen nutrition, increase in   resistance to stress, and stimulation mediated by antagonism against pathogenic microorganisms have been analyzed. The criteria for selection of rhizobacteria for practical purposes have been discussed.

Keywords: plants, rhizosphere, PGPR bacteria, nitrogen fixation, growth stimulation, antagonism

Acknowledgments. This study was performed as part of the state program for increasing the competitiveness of Kazan Federal University among the world's leading centers of science and education and funded in part by the subsidy allocated to Kazan Federal University for the state assignment in the sphere of scientific activities (project no. 14-83).

Figure captions

Fig. 1. The schematic view of rhizosphere [26].

References

  1. Dobrovol'skaya T.G. The Structure of Bacterial Communities of Soils. Moscow, Akademkniga, 2002. 282 p. (In Russian)
  2. Umarov M.M., Kurakov A.V., Stepanov A.L. Microbiological Transformation of Nitrogen in Soil. Moscow, GEOS, 2007, 137 p. (In Russian)
  3. Zvyagintsev D.G., Bab'eva I.L., Zenova G.M. Biology of Soils. Moscow, Izd. Mosk. Univ., 2005. 445 p. (In Russian)
  4. Ivanov V.P. Plant Exudates and Their Role in the Life of Phytocenoses. Moscow, Nauka, 1973. 193 p. (In Russian)
  5. Lynch J.M. The rhizosphere – form and function. Appl. Soil Ecol., 1994, vol. 1, no. 3, pp. 193–198. doi: 10.1016/0929-1393(94)90010-8.
  6. Umarov M.M. Associative Nitrogen Fixation. Moscow, Izd. Mosk. Univ., 1986. 133 p. (In Russian)
  7. Döbereiner J. Nitrogen-fixing bacteria in the rhizosphere. The Biology of Nitrogen Fixation. Quispel A. (Ed.). Amsterdam, North-Holland Pub. Co, 1974, pp. 86–120.
  8. Kameneva S.V., Muromets E.M. Genetic control of processes of bacterial interactions with plants in associations. Genetika, 1999, vol. 35, no. 11, pp. 1480–1494. (In Russian)
  9. Zvyagintsev D.G., Dobrovol'skaya T.G., Lysak L.V. Plants as centers for development of bacterial communities of soils. Zh. Obshch. Biol., 1993, vol. 54, no. 2, pp. 183–199. (In Russian)
  10. Bulgarelli D., Schlaeppi K., Spaepen S., Ver Loren van Themaat E., Schulze-Lefert P. Structure and function of bacterial microbiota of plants. Annu. Rev. Plant Biol., 2013, vol. 64, pp. 807–838. doi: 10.1146/annurev-arplant-050312-120106.
  11. Bezzubenkova O.E., Yukhlimova M.N., Nesterova N.I. Microflora of the rhizosphere and rhizoplane and its influence on the plant organism. Estestv. Tekh. Nauki, 2012, vol. 4, pp. 99–102. (In Russian)
  12. Beneduzi A., Ambrosini A., Passaglia L.M.P. Plant-growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet. Mol. Biol., 2012, vol. 35, suppl. 4, pp. 1044–1051.
  13. Balandreau J. Microbiology of the association. Can. J. Microbiol., 1983, vol. 29, no. 8, pp. 851–859. doi: 10.1139/m83-138.
  14. Dobereiner J. Dinitrogen fixation in rhizosphere and phyllospere associations. Inorganic Plant Nutrition. Berlin etc., Springer-Verlag, 1983, pp. 330–350.
  15. Bukharin O.V., Lobakova E.S., Nemtseva N.V., Cherkasov S.V. Associative Symbiosis. Yekaterinburg, Izd. Ural. Otd. Ross. Akad. Nauk, 2006. 264 p. (In Russian)
  16. Zilber-Rosenberg I., Rosenberg E. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev., 2008, vol. 32, no. 5, pp. 723–735. doi: 10.1111/j.1574-6976.2008.00123.x.
  17. Vandenkoornhuyse P., Quaiser A., Duhamel M., Le Van A., Dufresne A. The importance of the microbiome of plant holobiont. New Phytol., 2015, vol. 206, no. 4, pp. 1196–1206. doi: 10.1111/nph.13312.
  18. Schlaeppi K., Bulgarelli D. The plant microbiome at work. Mol. Plant-Microbe Interact., 2015, vol. 28, no. 3, pp. 212–217. doi: 10.1094/MPMI-10-14-0334-FI.
  19. Berg G., Rybakova D., Grube M., Koberl M. The plant microbiome explored: implications for experimental botany. J. Exp. Bot., 2016, vol. 67, no. 4, pp. 995–1002. doi: 10.1093/jxb/erv466.
  20. Chapparo J.M., Badri D.V., Bakker M.G., Sugiyama A., Manter D.K., Vivanco J.M. Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with soil microbial functions. PloS One, 2013, vol. 8, no. 8, p. 55731. doi: 10.1371/journal.pone.0055731.
  21. Djordjevic M.A., Mond-Radzman N.A., Imin N. Small-peptide signals that control root nodule number, development, and symbiosis. J. Exp Bot., 2015, vol. 66, no. 17, pp. 5171–5181. doi: 10.1093/jxb/erv357.
  22. Isobe K., Ohte N. Ecological perspectives on microbes involved in N-cycling. Microbes Environ., 2014, vol. 29, no. 1, pp. 4–16. doi: 10.1264/jsme2.ME13159.
  23. Klopper J.W., Lifshitz R., Zablotowicz R.M. Free-living bacterial inocula for enhancing crop productivity. Trends Biotechnol., 1989, vol. 7, no. 2, pp. 39–43. doi: 10.1016/0167-7799(89)90057-7.
  24. Babu N., Jogaiah S., Ito S., Nagaraj K., Tran L. Improvement of growth, fruit weight and early blight disease protection of tomato plants by rhizosphere bacteria is correlated with their beneficial traits and induced biosynthesis of antioxidant peroxidase and polyphenol oxidase. Plant Sci., 2015, vol. 231, pp. 62–73. doi: 10.1016/j.plantsci.2014.11.006.
  25. Mishke I.V. Microbial Phytohormones in Crop Production. Riga, Zinatne, 1988. 151 p. (In Russian)
  26. McNear Jr. D.H. The rhizosphere – roots, soil and everything in between. Nat. Educ. Knowl., 2013, vol. 4, no. 3, p. 1.
  27. Rajkumar M., Vara Prasad M.N., Freitas H., Ae N. Biotechnological applications of serpentine soil bacteria for phytoremediation of trace metals. Crit. Rev. Biotechnol., 2009, vol. 29, no. 2, pp. 120–130. doi: 10.1080/07388550902913772.
  28. Couillerot O., Ramírez-Trujillo A., Walker V., von Felten A., Jansa J., Maurhofer M., Défago G., Prigent-Combaret C., Comte G., Caballero-Mellado J., Moënne-Loccoz Y. Comparison of prominent Azospirillum strains in Azospirillum-Pseudomonas-Glomus consortia for promotion of maize growth. Appl. Microbiol. Biotechnol., 2013, vol. 9, no. 7, pp. 4639–4649. doi: 10.1007/s00253-012-4249-z.
  29. Chowdhury S.P., Hartmann A., Gao X-W., Borriss R. Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42 – a review. Front. Microbiol., 2015, vol. 6, art. 780, pp. 1–11. doi: 10.3389/fmicb.2015.00780.
  30. Fahad S., Hussain S., Bano A., Saud S., Hassan S., Shan D., Khan F.A., Khan F., Chen Y., Wu C., Tabassum M.A., Chun M.X., Afzal M., Jan A., Jan M.T., Huang J. Potential role of phytohormones and plant growth-promoting rhizobacteria in abiotic stresses: consequences for changing environment. Environ. Sci. Pollut. Res. Int., 2015, vol. 22, no. 7, pp. 4907–4921. doi: 10.1007/s11356-014-3754-2.
  31. Morgun V.V., Kots S.Ya., Kyrychenko E.V. Growth promoting rhizobacteria and their use in practice. Fiziol. Biokhim. Kul't. Rast., 2009, vol. 41, no. 3, pp. 187–207. (In Russian)
  32. Shaposhnikov A.I., Belimov A.A., Kravchenko L.V., Vivanco D.M. Interaction of rhizosphere bacteria with plants: mechanisms of formation and factors of efficiency in associative symbiosis (review). S-kh. Biol., 2011, no. 3, pp. 16–22. (In Russian)
  33. Lankina E.P., Khizhnyak S.V., Kulizhskiy S.P. The prospects of using psychrophilic and psychrotolerant bacteria mixed cultures for biological protection of plants from diseases. Vestn. KrasGAU, 2013, no. 4, pp. 101–105. (In Russian)
  34. Afzal M., Khan Q., Sessitsch A. Endophytic bacteria: prospects and applications for the phytoremediation of organic pollutants. Chemosphere, 2014, vol. 117, pp. 232–242. doi: 10.1016/ j.chemosphere.2014.06.078.
  35. Koul V., Adholeya A., Kochar M. Sphere of influence of indole acid and nitric oxide in bacteria. J. Basic Microbiol., 2015, vol. 55, no. 5, pp. 543–553. doi: 10.1002/jobm.201400224.
  36. Duca D., Lory J., Patten C.L., Rose D., Glick B.R. Indole-3-acetic acid in plant-microbe interactions. Antonie Van Leeuwenhoek, 2014, vol. 106, no. 1, pp. 85–125. doi: 10.1007/s10482-013-0095-y.
  37. Panhwar Q.A., Naher U.A., Jusop S., Othman R., Latif Md.A., Ismail M.R. Biochemical and molecular characterization of potential phosphate-solubilizing bacteria in acid sulfate soil and their beneficial effects on rice growth. PLoS One, 2014, vol. 9, no. 10, art. e97241. doi: 10.1371/journal.pone.0097241.
  38. Sharma S.B., Sayyed R.Z., Trivedi M.H., Gobi T.A. Phosphate solubilizing microbes: sustainable approach for managing phoaphorus deficiency in agricultural soils. SpringerPlus, 2013, vol. 2, art. 587, pp. 1–14. doi: 10.1186/2193-1801-2-587.
  39. Turner T.R., James E.K., Poole P.S. The plant microbiome. Genome Biol., 2013, vol. 14, no. 6, art. 209, pp. 1–10. doi: 10.1186/gb-2013-14-6-209.
  40. Ullah A., Mushtag H., Ali H., Munis M.F., Javed M.T., Chaudhary H.J. Diazotrophs-assisted phytoremediation of heavy metals: a novel approach. Environ. Sci. Pollut. Res. Int., 2015, vol. 22, no. 4, pp. 2505–2514. doi: 10.1007/s11356-014-3699-5.

  41. Maksimov I.V., Abizgil'dina R.R., Pusenkova L.I. Plant growth promoting rhizobacteria as alternative to chemical crop protectiors from pathogens. Appl. Biochem. Microbiol., 2011, vol. 47, no. 4, pp. 333–345. doi: 10.1134/S0003683811040090.
  42. Haas D., Defago G. Biological control of soil-borne pathogens by fluorescent pseudomonas. Nat. Rev. Microbiol., 2005, vol. 3, no. 4, pp. 307–319.
  43. Crowley D.E. Microbial Siderophores in the Plant Rhizospheric. Iron nutrition in plants and rhizospheric microorganisms. Barton L.L., Abadia J. (Eds.). Dordrecht, Springer, 2006, pp. 169–198.
  44. Baysal Ö., Lai D., Xu H., Siragusa M., Çalişkan M., Carimi F., Teixeira da Silva J.A., Tör A. A proteomic approach provides new insights into the control of soil-borne plant pathogens by Bacillus species. PLoS One, 2013, vol. 8, no. 1, art. e53182, pp. 1–12. doi: 10.1371/journal.pone.0053182.
  45. Choudhary D.K., Johri B.N. Interactions of Bacillus spp. and plants – with special reference to induced systemic resistance (ISR). Microbiol. Res., 2009, vol. 164, no. 5, pp. 493–513. doi: 10.1016/j.micres.2008.08.007.
  46. Wu L., Wu H-J., Qiao J., Gao X., Borriss R. Novel routes for improving biocontrol activity of bacillus based bioinoculants. Front. Microbiol., 2015, vol. 6, art. 1395, pp. 1–13. doi: 10.3389/fmicb.2015.01395.
  47. Dietel K., Beator B., Budiharjo A., Fan B., Borriss R. Bacterial traits involved in colonization of Arabidopsis thaliana roots by Bacillus amyloliquefaciens FZB42. Plant Pathol. J., 2013, vol. 29, no. 1, pp. 59–66. doi:10.5423/PPJ.OA.10.2012.0155.
  48. Nikitina V.E., Ponomareva E.G., Alen'kina S.A. Lectins at the cellular surfaces of azospirillae and their role in the associative relations with plants. Molekulyarnye osnovy vzaimootnoshenii assotsiativnykh mikroorganizmov s rasteniyami [Molecular Basics of Relations between Associative Microorganisms and Plants]. Moscow, Kolos, 2005, pp. 70–97. (In Russian)
  49. Weert S., Bloemberg G. Rhizosphere Competence and the Role of Root Colonization in Biocontrol. Plant-associated bacteria. Gnanamanickam S. (Ed.). Houten, The Netherlands, Springer, 2006, pp. 317–333.
  50. Krzyzanowska D., Obuchowski M., Bikowski M., Rychlowski M., Jafra S. Colonization of potato rhizosphere by GFP-tagged Bacillus subtilis MB73/2, Pseudomonas sp. P482 and Ochrobactrum sp. A44 shown on large sections of roots using enrichment sample preparation and confocal laser scanning microscopy. Sensors (Basel), 2012, vol. 12, no. 12, pp. 17608–17619. doi: 10.3390/s121217608.

For citation: Feoktistova N.V., Mardanova A.M., Hadieva G.F., Sharipova M.R. Rhizosphere bacteria. Uchenye Zapiski Kazanskogo Universiteta. Seriya Estestvennye Nauki, 2016, vol. 158, no. 2, pp. 207–224. (In Russian)


The content is available under the license Creative Commons Attribution 4.0 License.