Prospects for the use of multi-component symbiotic systems of the Legumes

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Legume-Rhizobial Symbiosis (LRS), Arbuscular Mycorrhiza (AM) and associations with Plant Growth-Promoting Bacteria (PGPB) implement nutritional and defensive functions in plant, improve soil fertility, and thus are appropriate to be used for sustainable crop production and soil restoration. Based on synergism and evolutional commonality of the symbioses, we propose a multi-component plant-microbe system with legume plant as a main component. Advances obtained from simultaneous inoculation of legumes with various beneficial microbes are summarized. Basic principles of legume breeding to improve effectiveness of interaction with a complex of the microbes along with problems and prospects for development of multi-microbial inoculants for legumes (and non-legumes) are stated.

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About the authors

Oksana Yur’yevna Shtark

All-Russia Research Institute for Agricultural Microbiology

Leading Scientist, Laboratory of Genetics of Plant-Microbe Interactions

Vladimir Aleksandrovich Zhukov

All-Russia Research Institute for Agricultural Microbiology

Head of Laboratory, Laboratory of Genetics of Plant-Microbe Interactions

Anton Sergeevich Sulima

All-Russia Research Institute for Agricultural Microbiology

PhD Student, Laboratory of Genetics of Plant-Microbe Interactions

Reena Singh

The Energy and Resources Institute (TERI)

Fellow and Area convener. Centre for Mycorrhizal Research

Tat’yana Sergeevna Naumkina

All-Russia Research Institute of Legumes and Groat Crops

Deputy Director for Science

Gul’nar Asanovna Akhtemova

All-Russia Research Institute for Agricultural Microbiology

Senior Scientist, Laboratory of Genetics of Plant-Microbe Interactions

Aleksey Yur’yevich Borisov

All-Russia Research Institute for Agricultural Microbiology

Chief Researcher, Laboratory of Technical Microbiology


  1. Akhtemova G. A., Pershina E. V., Pinaev A. G. et al. (2010) Formirovaniye struktury bakterial'nogo soobshchestva v otvalakh zavodov po pererabotke sakharnoy svekly [Pattern of bacterial consortium formation in the waste of sugar production from sugar beat]. Sakhar. V. 10: P. 2-7.
  2. Akhtemova G. A., Shtark O. Y., Pershina E. V. et al. (2011) Poisk khozyaystvenno-tsennykh mikroorganizmov dlya regional'nogo proizvodstva mnogokomponentnykh mikrobnykh preparatov [Search for agronomic microorganisms for the regional production of multicomponent microbial preparations]. In: Kunakh V. A., ed. Factors of experimental evolution of organisms. Kiev: Logos. P. 198-202.
  3. Artursson V., Finlay R. D., Jansson J. K. (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ. Microbiol. V. 8: P. 1-10.
  4. Babikova Z., Gilbert L., Bruce T. J. et al. (2013) Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecol. Lett. V. 16 (7): P. 835-843.
  5. Bakker P. A. H., Lemanceau P., Raaijmakers J. et al. (eds) (2007) New perspectives and approaches in plant growth-promoting rhizobacteria research. Springer Science & Business Media.
  6. Bardin S. D., Huang H. C., Pinto J. et al. (2004) Biological control of Pythium damping-off of pea and sugar beet by Rhizobium leguminosarum bv. viceae. Can J. Bot. V. 82 (3): P. 291-296.
  7. Barea J. M., Pozo M. J., Azcon R., Azcon-Aguilar C. (2005) Microbial cooperation in the rhizosphere. J. Exp. Botany. V. 56 (14): P. 1761-1788.
  8. Behl R. K., Ruppel S., Kothe E., Narula N. (2007) Wheat x Azotobacter x VA Mycorrhiza interactions towards plant nutrition and growth - a review. J. Appl. Bot. Food Qual. V. 81 (2): P. 95-109.
  9. Bennett A. E., Bever J. D., Bowers M. D. (2009) Arbuscular mycorrhizal fungal species suppress inducible plant responses and alter defensive strategies following herbivory. Oecologia. V. 160: P. 711-719.
  10. Bisht R., Chaturvedi S., Srivastava R. et al. (2009) Effect of arbuscular mycorrhizal fungi, Pseudomonas fluorescens and Rhizobium leguminosarum on the growth and nutrient status of Dalbergia sissoo Roxb. Tropical Ecol. V. 50 (2): P. 231-242.
  11. Bonfante P., Anca I. A. (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Ann. Rev. Microbiol. V. 63: P. 363-383.
  12. Borisov A. Y., Danilova T. N., Koroleva T. A. et al. (2004a) Pea (Pisum sativum L.) regulatory genes controlling development of nitrogen-fixing nodule and arbuscular mycorrhiza: fundamentals and application. Biologia. 59 Suppl. V. 13: P. 137-144.
  13. Borisov A. Y., Danilova T. N., Shtark O. Y. et al. (2008) Tripartite symbiotic system of pea (Pisum sativum L.): applications in sustainable agriculture. In: Dakora F. D., Chimphango B. M., Valentine A. J. et al., eds. Biological nitrogen fixation: towards poverty alleviation through sustainable agriculture. Proceedings of 15th International Congress on Nitrogen Fixation & 12th International Conference of the African Association for Biological Nitrogen Fixation. Berlin/Heidelberg. Springer Science and Business Media BV. P. 15-17.
  14. Borisov A. Y., Shtark O. Y., Danilova T. N. et al. (2004b) Effektivnost' ispol'zovaniya sovmestnoy inokulyatsii gorokha posevnogo (Pisum sativum L.) gribami arbuskulyarnoy mikorizy i kluben'kovymi bakteriyami dlya povysheniya produktivnosti rasteniy v ustoychivom ekologicheski oriyentirovannom zemledelii [Effectiviness of combined inoculation of field peas with arbuscular mycorrhizal fungi and nodule bacteria]. Doklady Rossiiskoi Akademii Sel’skohozyaistvennykh Nauk. V. 4: P. 5-7.
  15. Borisov A. Y., Tsyganov V. Е., Shtark O. Y. et al. (2002) The catalogue of world-wide collection. Issue 728. Pea (Symbiotic effectiveness). Tikhonovich I. A., Vishnyakova M. A., eds. Saint Petersburg: VIR.
  16. Bothe H. (2012) Arbuscular mycorrhiza and salt tolerance of plants. Symbiosis. V. 58 (1-3): P. 7-16.
  17. Campanelli A., Ruta C., De Mastro G., Morone-Fortunato I. (2013) The role of arbuscular mycorrhizal fungi in alleviating salt stress in Medicago sativa L. var. icon. Symbiosis. V. 59 (2): P. 65-76.
  18. Celik I., Ortas I., Kilic S. (2004) Effects of compost, mycorrhiza, manure and fertilizer on some physical properties of a Chromoxerert soil. Soil Till. Res. V. 78 (1): P. 59-67.
  19. Chebotar V. K., Kazakov A. E., Erofeev S. V. et al. (2008) Sposob polucheniya kompleksnogo mikrobiologicheskogo udobreniya [Method of production of complex microbial fertilizer]. Patent No 2318784.
  20. Currie A. F., Murray P. J., Gange A. C. (2011) Is a specialist root-feeding insect affected by arbuscular mycorrhizal fungi? Appl. Soil. Ecol. V. 47: P. 77-83.
  21. Daniel R. (2005) The metagenomics of soil. Nature Rev. V. 3: P. 470-478.
  22. De Mita S., Chantret N., Loridon K. et al. (2011) Molecular adaptation in flowering and symbiotic recognition pathways: insights from patterns of polymorphism in the legume Medicago truncatula. BMC Evol. Biol. V. 11: 229. doi: 10.1186/1471-2148-11-229. Aug. 1.
  23. Declerck S., Strullu D. G., Fortin A. (eds.) (2005) In vitro culture of mycorrhizas. Berlin Heidelberg: Springer.
  24. Dilworth M. J., James E. K., Sprent J. I., Newton W. E. (eds.) (2008) Nitrogen-fixing leguminous symbioses. Springer Science + Business Media BV.
  25. Doty S. L. (2008) Enhancing phytoremediation through the use of transgenics and endophytes. New Phytol. V. 179 (2): P. 318-333.
  26. Douds D. D. Jr., Nagahashi G., Pfeffer P. E. et al. (2005) On-farm production and utilization of arbuscular mycorrhizal fungus inoculum. Can. J. Plant. Sci. V. 85: P. 15-21. doi: 10.4141/P03-168.
  27. Duan J., Müller K. M., Charles T. C. et al. (2009) 1-aminocyclopropane-1-carboxylate (ACC) deaminase genes in rhizobia from southern Saskatchewan. Microb. Ecol. V. 57 (3): P. 423-436.
  28. Egamberdieva D., Lugtenberg B. (2014) Use of plant growth-promoting rhizobacteria to alleviate salinity stress in plants. In: Miransari M., ed. Use of microbes for the alleviation of soil stresses Volume 1. New York: Springer Science + Business Media. P. 73-96.
  29. Elkoca E., Kantar F., Sahin F. (2007) Influence of nitrogen fixing and phosphorus solubilizing bacteria on the nodulation, plant growth, and yield of chickpea. J. Plant Nutr. V. 31 (1): P. 157-171.
  30. Frey-Klett P., Garbaye J., Tarkka M. (2007) The mycorrhiza helper bacteria revisited. New Phytol. V. 176: P. 22-36.
  31. Galvan G. A., Burger-Meijer K., Kuiper T. W. et al. (2007) Breeding for improved responsiveness to arbuscular mycorrhizal fungi in onion. Proceedings of 3rd International Congress of the European Integrated Project Quality Low Input Food (QLIF) Congress. Hohenheim, Germany, March 20-23, 2007.
  32. Gamalero E., Berta G., Massa N. et al. (2008) Synergistic interactions between the ACC deaminase-producing bacterium Pseudomonas putida UW4 and the AM fungus Gigaspora rosea positively affect cucumber plant growth. FEMS Microbiol. Ecol. V. 64 (3): P. 459-467.
  33. Gamalero E., Berta G., Massa N. et al. (2010) Interactions between Pseudomonas putida UW4 and Gigaspora rosea BEG9 and their consequences for the growth of cucumber under salt-stress conditions. J. Appl. Microbiol. V. 108: P. 236-245.
  34. Gamalero E., Lingua G., Berta G., Glick B. R. (2009) Beneficial role of plant growth promoting bacteria and arbuscular mycorrhizal fungi on plant responses to heavy metal stress. Can. J. Microbiol. V. 55: P. 501-514.
  35. Gamalero E., Trotta A., Massa N. et al. (2004) Impact of two fluorescent pseudomonads and an arbuscular mycorrhizal fungus on tomato plant growth, root architecture and P acquisition. Mycorrhiza. V. 14 (3): P. 185-192.
  36. Gianinazzi S, Vosátka M (2004) Inoculum of arbuscular mycorrhizal fungi for production systems: science meets business. Can. J. Bot. V. 82: P. 1264-1271.
  37. Gorton A. J., Heath K. D., Pilet-Nayel M. L., Baranger A., Stinchcombe J. R. (2012) Mapping the genetic basis of symbiotic variation in legume-rhizobium interactions in Medicago truncatula. G3 (Bethesda). V. 2 (11): P. 1291-1303. doi: 10.1534/g3.112.003269. Nov. 1.
  38. Govindasamy V., Senthilkumar M., Magheshwaran V. et al. (2010) Bacillus and Paenibacillus spp.: Potential PGPR for sustainable agriculture. In: Maheshwari D. K., ed. Plant growth and health promoting bacteria. Berlin Heidelberg: Springer. P. 333-364.
  39. Graham P. H., Hungria M., Tlusty B. (2004) Breeding for better nitrogen fixation in grain legumes: where do the rhizobia fit in? Crop Management (Online). doi: 10.1094/CM-2004-0301-02-RV.
  40. Hage-Ahmed K., Moyses A., Voglgruber A. et al. (2013) Alterations in root exudation of intercropped tomato mediated by the arbuscular mycorrhizal fungus Glomus mosseae and the soilborne pathogen Fusarium oxysporum f. sp. Lycopersici. J. Phytopathol. V. 161 (11-12): P. 763-773.
  41. Hajnal-Jafari T., Jarak M., Đurić S., Stamenov D. (2012) Effect of co-inoculation with different groups of beneficial microorganisms on the microbiological properties of soil and yield of maize (Zea mays L.). Ratarstvo i Povrtarstvo. V. 49 (2): P. 183-188.
  42. Hartmann A., Schmid M., Van Tuinen D., Berg G. (2009) Plant-driven selection of microbes. Plant Soil. V. 321 (1-2): P. 235-257.
  43. Herridge D., Rose I. (2000) Breeding for enhanced nitrogen fixation in crop legumes. Field Crops Res. V. 65: P. 229-248.
  44. Hildebrandt U., Ouziad F., Marner F. J., Bothe H. (2006) The bacterium Paenibacillus validus stimulates growth of the arbuscular mycorrhizal fungus Glomus intraradices up to the formation of fertile spores. FEMS Microbiol. Lett. V. 254: P. 258-267.
  45. Hossain M. S., Mårtensson A. (2008) Potential use of Rhizobium spp. to improve fitness of nonnitrogen-fixing plants. Acta Agric. Scand. Section B - Plant Soil Sci. V. 58 (4): P. 352-358.
  46. Huang H. C., Erickson R. S. (2007) Effect of seed treatment with Rhizobium leguminosarum on Pythium damping-off, seedling height, root nodulation, root biomass, shoot biomass, and seed yield of pea and lentil. J. Phytopathol. V. 155 (1): P. 31-37.
  47. Ibrahim K. K., Arunachalam V., Rao P. S. K., Tilak K. V. B.R. (1995) Seasonal response of groundnut genotypes to arbuscular mycorrhiza - Bradyrhizobium inoculation. Microbiol. Res. V. 150: P. 218-224.
  48. IJdo M., Cranenbrouck S., Declerck S. (2011) Methods for large-scale production of AM fungi: past, present, and future. Mycorrhiza. V. 21: P. 1-16.
  49. Jacobi L. M., Kukalev A. S., Ushakov K. V. et al. (1999) Genetic variability of garden pea (Pisum sativum L.) for symbiotic capacities. Pisum Genet. V. 31: P. 44-45.
  50. James E. K. (2000) Nitrogen fixation in endophytic and associative symbiosis. Field Crop Res. V. 65: P. 197-209.
  51. Kempel A., Schmidt A. K., Brandl R., Schadler M. (2010) Support from the underground: induced plant resistance depends on arbuscular mycorrhizal fungi. Funct. Ecol. V. 24: P. 293-300.
  52. Kennedy I. R., Choudhury A. T. M.A., Kecskes M. L. (2004) Nonsymbiotic bacterial diazotrophs in crop-farming systems: can their potential for plant growth promotion be better exploited? Soil. Biol. Biochem. V. 36: P. 1229-1244.
  53. Koltai H., Kapulnik Y. (eds.) (2010) Arbuscular mycorrhizas: physiology and function. Dordrecht: Springer.
  54. Koricheva J., Gange A. C., Jones T. (2009) Effects of mycorrhizal fungi on insect herbivores: a metaanalysis. Ecology. V. 90: P. 2088-2097.
  55. Kuzmicheva Y. V., Shaposhnikov A. I., Azarova T. S. et al. (2014) Sostav kornevykh ekzometabolitov vysokosimbiotrofnogo sorta gorokha Triumf i yego roditel'skikh form. Fiziologiya rasteniy [The composition of the root exometabolites of highly symbiotrophic pea cv. Triumph and its parental forms]. Fiziologiya rasteniy. V. 61 (1): 121-128.
  56. Labutova N. M., Polyakov A. I., Lyakh V. A., Gordon V. L. (2004) Vliyaniye inokulyatsii kluben'kovymi bakteriyami i endomikoriznym gribom Glomus intraradices na urozhay razlichnykh sortov soi i soderzhaniye belka i masla v semenakh [Influence of inoculation with nodule bacteria and endomycorrhizal fungus Glomus intraradices on yield and seed protein and oil content of different soybean cultivars]. Doklady Rossiiskoi Akademii Sel’skohozyaistvennykh Nauk. V. 4 (2): P. 2-4.
  57. Leonforte A., Sudheesh S., Cogan N. O. et al. (2013) SNP marker discovery, linkage map construction and identification of QTLs for enhanced salinity tolerance in field pea (Pisum sativum L.). BMC Plant Biol. V. 13: 161. doi: 10.1186/1471-2229-13-161. Oct 17.
  58. Liu J., Maldonado-Mendoza I., Lopez-Meyer M. et al. (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J. V. 50: P. 529-544.
  59. Lobkov V. T., Donskaya M. V., Vasil'chikov A. G. (2011) Povysheniye effektivnosti simbioticheskikh sistem nuta (Cicer arietinum L.) [Improving the efficiency of symbiotic systems of chickpea (Cicer arietinum L.)]. Vestnik Orlovskogo Gosudarstvennogo Agrarnogo Universiteta. V. 30 (3): P. 39-43.
  60. López-López A., Rogel M. A., Ormeño-Orrillo E et al. (2010) Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Sys. Appl. Microbiol. V. 33 (6): P. 322-327.
  61. Lugtenberg B. (ed.) (2015). Principles of plant-microbe interactions. Springer International Publishing.
  62. Mäder P., Kaiser F., Adholeya A. et al. (2011) Inoculation of root microorganisms for sustainable wheat-rice and wheat-black gram rotations in India. Soil Biol. Biochem. V. 43 (3): P. 609-619.
  63. Malusá E., Sas-Paszt L., Ciesielska J. (2012) Technologies for beneficial microorganisms inocula used as biofertilizers. Sci. World J. Article ID 491206. doi: 10.1100/2012/491206.
  64. Mishra A., Prasad K., Rai G. (2010) Effect of bio-fertilizer inoculations on growth and yield of dwarf field pea. J. Agron. V. 9 (4): P. 163-168.
  65. Naumann M., Schüßler A., Bonfante P. (2010) The obligate endobacteria of arbuscular mycorrhizal fungi are ancient heritable components related to the Mollicutes. ISME J. V. 4 (7): P. 862-871.
  66. Naumkina T. S., Borisov A. Y., Shtark O. Y. et al. (2011) Ispol'zovaniye simbiozov bobovykh pri sozdanii vysokoeffektivnykh rastitel'no-mikrobnykh sistem dlya adaptivnogo rasteniyevodstva [Use of symbioses of pod-bearing plants for building of highly effective plant-microbic systems for adaptive plant growing]. Agrarnaya Rossiya. V. 3: P. 35-37.
  67. Naumkina TS, Suvorova GN, Vasil'chikov AG et al. (2012) Sozdaniye vysokoeffektivnykh rastitel'no-mikrobnykh sistem fasoli [Creation of highly effective plant-microbe systems of beans]. Zernobobovyye i Krupyanyye Kul'tury. V. 2: P. 21-26.
  68. Oldroyd G. E., Downie J. A. (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. V. 59: P. 519-546.
  69. Ormeño-Orrillo E., Hungria M., Martinez-Romero E. 2013. Dinitrogen-fixing prokaryotes. The Prokaryotes. Berlin Heidelberg: Springer. P. 427-451.
  70. Pattinson G. S., Hammill K. A., Sutton B. G., McGee P. A. (2004). Growth and survival of seedlings of native plants in an impoverished and highly disturbed soil following inoculation with arbuscular mycorrhizal fungi. Mycorrhiza. V. 14 (6): P. 339-346.
  71. Pershina E., Andronov E., Pinaev A., Provorov N. (2013) Recent advances and perspectives in metagenomic studies of soil microbial communities. In: Malik A., Grohmann E., Alves M., eds. Management of the microbial resources in the environment. Berlin: Springer: P. 141-166.
  72. Provorov N. A., Shtark O. Y. (2014) Napravlennaya evolyutsiya gribov i rasteniy v simbioticheskikh sistemakh [Directed evolution of fungi and plants in symbiotic systems]. Mikologiya i fitopatologiya. V. 48 (3): P. 151-160.
  73. Puri A., Adholeya A. (2013) A new system using Solanum tuberosum for the co-cultivation of Glomus intraradices and its potential for mass producing spores of arbuscular mycorrhizal fungi. Symbiosis. V. 59 (2): P. 87-97.
  74. Rai M. K. (ed) (2006) Handbook of microbial biofertilizers. Haworth Press Technology Engineering.
  75. Reimann S., Hauschild R., Hildebrandt U., Sikora R. A. (2008) Interrelationships between Rhizobium etli G12 and Glomus intraradices and multitrophic effects in the biological control of the root-knot nematode Meloidogyne incognita on tomato. J. Plant Dis. Protect. V. 115 (3): P. 108-113.
  76. Reinhold-Hurek B., Hurek T. (2007) Endophytic associations of Azoarcus spp. In: Associative and endophytic nitrogen-fixing bacteria and cyanobacterial associations. Springer Netherlands. P. 191-210.
  77. Remigi P., Capela D., Clerissi C. et al. (2014) Transient hypermutagenesis accelerates the evolution of legume endosymbionts following horizontal gene transfer. PLoS Biol. V. 12 (9): e1001942.
  78. Rengel Z. (2002) Breeding for better symbiosis. Plant Soil. V. 245: P. 147-162.
  79. Requena N., Jimenez J., Toro M., Barea J. M. (1997) Interactions between plant-growth-promoting rhizobacteria (PGPR), arbuscular mycorrhizal fungi and Rhizobium spp. in the rhizosphere of Anthyllis cytisoides, a model legume for revegetation in Mediterranean semi-arid ecosystems. New Phytol. V. 136: P. 667-677.
  80. Requena N., Perez-Solis E., Azcуn-Aguilar C. et al. (2001) Management of indigenous plant-microbe symbioses aids restoration of desertified ecosystems. Appl. Environ. Microbiol. V. 67 (2): 495-498.
  81. Richardson A. E., Barea J. M., McNeill A. M., Prigent-Combaret C. (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil. V. 321: P. 305-339.
  82. Rillig M. C. (2004) Arbuscular mycorrhizae, glomalin and soil aggregation. Can. J. Soil Sci. V. 84: P. 355-363.
  83. Scheublin T. R., Ridgway K. P., Young J. P. W., Van Der Heijden M. G. (2004) Nonlegumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. Appl. Environ. Microbiol. V. 70 (10): P. 6240-6246.
  84. Scheublin T. R., Sanders I. R., Keel C., van der Meer J. R. (2010) Characterisation of microbial communities colonising the hyphal surfaces of arbuscular mycorrhizal fungi. ISME J. V. 4 (6): P. 752-763.
  85. Scheublin T. R., Van Der Heijden M. G. (2006) Arbuscular mycorrhizal fungi colonize nonfixing root nodules of several legume species. New Phytol. V. 172 (4): P. 732-738.
  86. Schulz B., Boyle S., Sieber T. (eds.) (2006) Microbial root endophytes. Springer.
  87. Sessitsch A., Howieson J. G., Perret X. et al. (2002) Advances in Rhizobium research. Crit. Rev. Plant. Sci. V. 21: P. 323-378.
  88. Shcherbakov A. V., Bragina A. V., Kuzmina E. Y. et al. (2013) Endophytic bacteria of Sphagnum mosses as promising objects of agricultural microbiology. Microbiology. V. 82 (3): P. 306-315.
  89. Shiraishi A., Matsushita N., Hougetsu T. (2010) Nodulation in black locust by the Gammaproteobacteria Pseudomonas sp. and the Betaproteobacteria Burkholderia sp. Syst. Appl. Microbiol. V. 33 (5): P. 269-274.
  90. Shtark O. Y., Borisov A. Y., Zhukov V. A. et al. (2010) Intimate associations of beneficial soil microbes with the host plants. In: Dixon G. R., Tilston E. L. eds. Soil microbiology and sustainable crop production. Dordrecht: Springer. P. 119-196.
  91. Shtark O. Y., Borisov A. Y., Zhukov V. A., Tikhonovich I. A. (2012) Mutually beneficial legume symbioses with soil microbes and their potential for plant production. Symbiosis. V. 57 (3): P. 51-62.
  92. Shtark O. Y., Danilova T. N., Naumkina T. S. et al. (2006) Analiz iskhodnogo materiala gorokha posevnogo (Pisum sativum L.) dlya selektsii sortov s vysokim simbioticheskim potentsialom i vybor parametrov dlya yego otsenki [Analysis of pea (Pisum sativum L.) source material for breeding of cultivars with high symbiotic potential and choice of criteria for its evaluation]. Ekologicheskaja Genetika. V. 4 (2): P. 22-28.
  93. Siddiqui Z. A. (2006) PGPR: prospective biocontrol agents of plant pathogens. In: Siddiqui ZA, ed. PGPR: Biocontrol and biofertilization. Springer Netherlands. P. 111-142.
  94. Siddiqui Z. A., Akhtar M. S., Futai K. (eds.) (2008) Mycorrhizae: sustainable agriculture and forestry. New Delhi: Springer.
  95. Sidorova K. K., Shumnyy V. K., Glyanenko M. N. et al. (2014) Geneticheskiy potentsial mestnykh endemichnykh form gorokha Pisum sativum L. po priznakam azotfiksatsii i produktivnosti [Genetic potential of local endemic forms of the pea (Pisum sativum L.) on the basis of nitrogen fixation and productivity]. Genetika. V. 50 (1): P. 35-43.
  96. Sidorova K. K., Goncharova A. V., Goncharov P. L., Shumnyi V. K. 2012. Selektsiya kormovogo gorokha (Pisum sativum L) na povysheniye azotfiksatsii s ispol'zovaniyem simbioticheskikh mutantov [Selection of pea on rising of nitrogen fixation (Pisum sativum L) with the use of symbiotic mutants]. Sel'skokhozyaystvennaya Biologiya. N 1: P. 105-109.
  97. Smith S. E., Read D. J. (2008) Mycorrhizal Symbiosis. 3rd ed. London: Academic Press.
  98. Smýkal P., Aubert G., Burstin J. et al. (2012) Pea (Pisum sativum L.) in the genomic era. Agronomy. V. 2: P. 74-115.
  99. Sprent J. I., James E. K. (2007) Legume evolution: where do nodules and mycorrhizas fit in? Plant Physiol. V. 144: P. 575-581.
  100. Stanton-Geddes J., Paape T., Epstein B. et al. (2013) Candidate genes and genetic architecture of symbiotic and agronomic traits revealed by whole-genome, sequence-based association genetics in Medicago truncatula. PLoS One. V. 8 (5): e65688. doi: 10.1371/journal.pone.0065688. May 31.
  101. Stockinger H., Krüger M., Schüßler A. (2010) DNA barcoding of arbuscular mycorrhizal fungi. New Phytol. V. 187 (2): P. 461-474.
  102. Sturz A. V., Christie B. R., Nowak J. (2000) Bacterial endophytes: potential role in developing sustainable systems of crop production. Cr. Rev. Plant Sci. V. 19 (1): P. 1-30.
  103. Taurian T., Anzuay M. S., Ludueña L. M. et al. (2013) Effects of single and co-inoculation with native phosphate solubilising strain Pantoea sp J49 and the symbiotic nitrogen fixing bacterium Bradyrhizobium sp SEMIA 6144 on peanut (Arachis hypogaea L.) growth. Symbiosis. V. 59 (2): P. 77-85.
  104. Tikhonovich I. A., Provorov N. A. (2007) Cooperation of plants and microorganisms: getting closer to the genetic construction of sustainable agro-systems. Biotechnol. J. V. 2 (7): P. 833-848.
  105. Tilak K. V. B.R., Ranganayaki N., Manoharachari C. (2006) Synergistic effects of plant-growth promoting rhizobacteria and Rhizobium on nodulation and nitrogen fixation by pigeonpea (Cajanus cajan). Eur. J. Soil Sci. V. 57: P. 67-71.
  106. Toljander J. F., Artursson V., Paul L. R. et al. (2006) Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species. FEMS Microbiol. Lett. V. 254 (1): P. 34-40.
  107. Toljander J. F., Lindahl B. D., Paul L. R. et al. (2007) Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiol. Ecol. V. 61: P. 295-304.
  108. Tsigie A., Tilak K. V. B.R., Saxena A. K. (2011) Field response of legumes to inoculation with plant growth-promoting rhizobacteria. Biol. Fert. Soils. V. 47 (8): P. 971-974.
  109. Valdenegro M., Barea J. M., Azcón R. (2001) Influence of arbuscular-mycorrhizal fungi, Rhizobium meliloti strains and PGPR inoculation on the growth of Medicago arborea used as model legume for re-vegetation and biological reactivation in a semi-arid mediterranean area. Plant Growth Regul. V. 34 (2): P. 233-240.
  110. Vallad E., Goodman R. M. (2004) Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Sci. V. 44: P. 1920-1934.
  111. Vidal-Dominguez M. T., Azcón-Aguilar C., Barea J. M. (1994) Preferential sporulation of Glomus fasciculatum in the root nodules of herbaceous legumes. Symbiosis. V. 16: P. 65-73.
  112. Wakelin S. A., Ryder M. H. (2004) Plant growth-promoting inoculants in Australian agriculture. Crop Management. (Online). doi: 10.1094/CM-2004-0301-01-RV.
  113. Xavier I. J., Holloway G., Leggett M. (2004) Development of rhizobial inoculant formulations. Crop Management (Online). doi: 10.1094/CM-2004-0301-06-RV.
  114. Xavier L. J. C., Germida J. J. (2002) Response of lentil under controlled conditions to co-inoculation with arbuscular mycorrhizal fungi and rhizobia varying in efficacy. Soil Biol. Biochem. V. 34 (2): P. 181-188.
  115. Yang J., Kloepper J. W., Ryu C. M. (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. V. 14 (1): P. 1-4.
  116. Zavalin A. A. (2005) Biopreparaty, udobreniya i urozhay [Bio-preparations, fertilizers and harvest]. Moscow: Publishing house of All-Russian scientific-research institute of agrochemistry named by D. N. Pryanishnikov.
  117. Zavalin A. A., Kozhemyakov A. P. (eds.) (2010) Novyye tekhnologii proizvodstva i primeneniya biopreparatov kompleksnogo deystviya [New technologies of production and use of biopreparations with complex action]. St. Petersburg: Khimizdat.
  118. Zhukov V. A., Shtark O. Y., Borisov A. Y., Tikhonovich I. A. (2013) Breeding to Improve Symbiotic Effectiveness of Legumes. In: Andersen S. B., ed. Plant Breeding Methods. Rijeka, Croatia: InTech. doi: 10.5772/53003.



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