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Mutually beneficial legume symbioses with soil microbes and their potential for plant production

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Abstract

Legumes develop different mutually beneficial symbioses with soil microbes, such as arbuscular mycorrhizal (AM) fungi, nodule bacteria and plant growth promoting bacteria. Symbioses supply the plants with nutrients (predominantly with nitrogen and phosphorus), protect them from pathogens and abiotic stresses and improve soil microbial biodiversity and fertility. The synergistic activity of beneficial soil microbes (BSM) on the plants has great importance for the use of multi-component symbiotic systems in low-input sustainable environmentally-friendly agrotechnologies. However, the complex nature of the AM symbiosis when in a multi-component symbiosis (plant-fungus-bacteria) creates complications for the fungus to produce AM fungal propagules and poses questions (a) about the effectiveness of the fungus per se in interactions with the plants, without associates, and (b) about the necessity of using sterile/axenic conditions for the production of the AM fungi based inoculants because of any mixing and competition by microbes from the inoculants with the local soil microbial consortia. The legume genes controlling interactions with BSM (including genes responsible for effectiveness of such interactions) should be considered as a united genetic system. The plant genome is more stable than that of microbes and therefore crop plants should select beneficial microbes and control the effectiveness of the whole plant-microbe system in the field for the benefit of the crop and therefore of human beings. There is clearly a need to breed legume crops with improved performance under sustainable conditions involving interactions with BSM and optimising the use of agrochemicals.

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References

  • Akhtar MS, Siddiqui ZA (2008) Arbuscular mycorrhizal fungi as potential bioprotectants against plant pathogens. In: Siddiqu ZA et al (eds) Mycorrhizae: sustainable agriculture and forestry. Springer, Dordrecht, pp 61–97

    Chapter  Google Scholar 

  • Akhtemova GA, Pershina EV, Pinaev AG, Andronov EE, Shtark OY, Chebotar VK, Kiprushkina EI, Abdurashitov SF, Borisov AY, Gianninazzi-Pearson V, Tikhonovich IA (2010a) Pattern of bacterial consortium formation in the waste of sugar production from sugar beat. Russ J Sugar (Sakhar) 10:2–7 (in Russian)

    Google Scholar 

  • Akhtemova GA, Shtark OY, Pershina EV, Pinaev AG, Andronov EE, Borisov AY, Tikhonovich IA (2010b) Creation of new multi-component microbial bio-preparations for sustainable agriculture. In: Kunakh VA (ed) Factors of experimental evolution of organisms. Logos, Kiev, pp 210–214, in Russian

    Google Scholar 

  • Andronov EE, Petrova SN, Chizhevskaya EP, Korostik EV, Akhtemova GA, Pinaev AG (2009) Influence of introducing the genetically modified strain Sinorhizobium meliloti ACH-5 on the structure of the soil microbial community. Russ J Microbiol 78(4):474–482

    CAS  Google Scholar 

  • Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R (1998) Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: effect on radishes (Raphanus sativus L.). Plant Soil 204:57–67

    Article  CAS  Google Scholar 

  • Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10

    Article  PubMed  CAS  Google Scholar 

  • Baas-Becking LGM (1934) Geobiologie of inleiding tot de milieukunde. WP Van Stockum & Zoon, The Hague

    Google Scholar 

  • Bakker PAHM, Raaijmakers JM, Bloemberg G, Höfte M, Lemanceau P, Cooke M (2007) New perspectives and approaches in plant growth-promoting rhizobacteria research. Foreword. Eur J Plant Pathol 119:241–242, well Publishing, Ltd

    Article  Google Scholar 

  • Balachandar D, Raja P, Kumar K, Sundaram SP (2007) Non-rhizobial nodulation in legumes. Biotechnol Mol Biol Rev 2:49–57

    Google Scholar 

  • Balestrini R, Gomez-Ariza J, Lanfranco L, Bonfante P (2007) Laser microdissection reveals that transcripts for five plant and one fungal phosphate transporter genes are contemporaneously present in arbusculated cells. Mol Plant Microbe Interact 20:1055–1062

    Article  PubMed  CAS  Google Scholar 

  • Banba M, Gutjahr C, Miyao A, Hirochika H, Paszkowski U, Kouchi H, Imaizumi-Anraku H (2008) Divergence of evolutionary ways among common Sym genes: CASTOR and CCaMK show functional conservation between two symbiosis systems and constitute the root of a common signaling pathway. Plant Cell Physiol 49(11):1659–1671

    Article  PubMed  CAS  Google Scholar 

  • Barea JM, Pozo MJ, Azcon R, Azcon-Aguilar C (2005) Microbial cooperation in the rhizosphere. J Exp Bot 56:1761–1778

    Article  PubMed  CAS  Google Scholar 

  • Bennett AE, Bever JD, Bowers MD (2009) Arbuscular mycorrhizal fungal species suppress inducible plant responses and alter defensive strategies following herbivory. Oecologia 160:711–719

    Google Scholar 

  • Berg G, Hallmann J (2006) Control of plant pathogenic fungi with bacterial endophytes. In: Schulz B, Boyle S, Sieber T (eds) Microbial root endophytes. Springer, pp 53–70

  • Bianciotto V, Lumini E, Bonfante P, Vandamme P (2003) ‘Candidatus Glomeribacter gigasporarum’ gen. nov., sp. nov., an endosymbiont of arbuscular mycorrhizal fungi. Int J Syst Evol Microbiol 53:121–124

    Article  PubMed  CAS  Google Scholar 

  • Bianciotto V, Genre A, Jargeat P, Lumini E, Becard G, Bonfante P (2004) Vertical transmission of endobacteria in the arbuscular mycorrhizal fungus Gigaspora margarita through generation of vegetative spores. Appl Environ Microbiol 70:3600–3608

    Article  PubMed  CAS  Google Scholar 

  • Bloemberg G, Lugtenberg BJJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 4:343–350

    Article  PubMed  CAS  Google Scholar 

  • Bonfante P, Balestrini R, Genre A, Lanfranco L (2009) Establishment and functioning of arbuscular mycorrhizas. In: Deising H (ed) The Mycota V. Plant relationship, 2nd edn. Springer, Berlin/Heidelberg, pp 259–274

    Google Scholar 

  • Borisov AY, Tsyganov VЕ, Shtark OY, Jacobi LM, Naumkina TS, Serdyuk VP, Vishnyakova MA (2002) In: Tikhonovich IA, Vishnyakova MA (eds) The catalogue of world-wide collection. Issue 728. Pea (Symbiotic effectiveness). VIR, Saint Petersburg

    Google Scholar 

  • Borisov AY, Shtark OY, Danilova TN, Tsyganov VE, Naumkina TS (2004) Effectiviness of combined inoculation of field peas with arbuscular mycorrhizal fungi and nodule bacteria. Russ Agric Sci 4:5–7, Doklady Rossiiskoi Akademii Sel’skohozyaistvennykh Nauk

    Google Scholar 

  • Borisov AY, Danilova TN, Shtark OY, Solovov II, Kazakov AE, Naumkina TS, Vasilchikov AG, Chebotar VK, Tikhonovich IA (2008) Tripartite symbiotic system of pea (Pisum sativum L.): applications in sustainable agriculture. In: Dakora FD, Chimphango BM, Valentine AJ, Elmerich C, Newton WE (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. Springer Science and Business Media BV, Berlin/Heidelberg, pp 15–17

    Google Scholar 

  • Brewin NJ (2004) Plant cell wall remodeling in the Rhizobium-legume symbiosis. Crit Rev Plant Sci 23:1–24

    Article  CAS  Google Scholar 

  • Brockwell J, Bottomley PJ, Thies JE (1995) Manipulation of rhizobia microflora for improving legume productivity and soil fertility: a critical assessment. Plant Soil 174:143–180

    Article  CAS  Google Scholar 

  • Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304

    Article  Google Scholar 

  • Catford JG, Staehelin C, Lerat S, Piché Y, Vierheilig H (2003) Suppression of arbuscular mycorrhizal colonization and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with Nod factors. J Exp Bot 54(386):1481–1487

    Article  PubMed  CAS  Google Scholar 

  • Catoira R, Galera C, de Billy F, Penmetsa RV, Journet EP, Maillet F, Rosenberg C, Cook D, Gough C, Denarie J (2000) Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell 12:1647–1665

    Google Scholar 

  • Chabaud M, Genre A, Sieberer BJ, Faccio A, Fournier J, Novero M, Barker DG, Bonfante P (2011) Arbuscular mycorrhizal hyphopodia and germinated spore exudates trigger Ca2+ spiking in the legume and nonlegume root epidermis. New Phytol 189:347–355

    Article  PubMed  CAS  Google Scholar 

  • Chebotar VK, Kazakov AE, Erofeev SV, Danilova TN, Naumkina TS, Shtark OY, Tikhonovich IA, Borisov AY (2008) Method of production of complex microbial fertilizer. Patent No 2318784

  • Committee on Metagenomics: Challenges and Functional Applications, National Research Council (2007) The new science of metagenomics. Revealing the secrets of our microbial planet. The National Academies Press, Washington, http://www.nap.edu/catalog/11902.html

    Google Scholar 

  • Currie AF, Murray PJ, Gange AC (2011) Is a specialist root-feeding insect affected by arbuscular mycorrhizal fungi? Appl Soil Ecol 47:77–83

    Article  Google Scholar 

  • D’Haeze W, Holsters M (2002) Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12:79–105

    Article  Google Scholar 

  • Daniel R (2005) The metagenomics of soil. Nat rev 3:470–478. doi:10.1038/nrmicro1160

    Article  CAS  Google Scholar 

  • De Bary A (1879) A die erscheinung der symbiose. Von Karl J Trubner, Strassburg

    Google Scholar 

  • Dilworth MJ, James EK, Sprent JI, Newton WE (eds) (2008) Nitrogen-fixing leguminous symbioses. Springer, Dordrecht

    Google Scholar 

  • Douds DD Jr, Nagahashi G, Pfeffer PE, Kayser WM, Reider C (2005) On-farm production and utilization of arbuscular mycorrhizal fungus inoculum. Can J Plant Sci 85:15–21. doi:10.4141/P03-168

    Article  Google Scholar 

  • Douds DD Jr, Nagahashi G, Pfeffer PE, Reider C, Kayser WM (2006) On-farm production of AM fungus inoculum in mixtures of compost and vermiculite. Bioresour Technol 97:809–818. doi:10.1016/j.biortech.2005.04.015

    Article  PubMed  CAS  Google Scholar 

  • Douds DD Jr, Nagahashi G, Hepperly PR (2010) On-farm production of inoculum of indigenous arbuscular mycorrhizal fungi and assessment of diluents of compost for inoculum production. Bioresour Technol 101(7):2326–2330

    Article  PubMed  CAS  Google Scholar 

  • Duijff BJ, Gianinazzi-Pearson V, Lemanceau P (1997) Involvement of the outer membrane lipopolysaccharides in the endophytic colonization of tomato roots by biocontrol Pseudomonas fluorescens strain WCS417r. New Phytol 135:325–334

    Article  CAS  Google Scholar 

  • Elkocaa E, Kantara F, Sahinb F (2007) Influence of nitrogen fixing and phosphorus solubilizing bacteria on the nodulation, plant growth, and yield of chickpea. J Plant Nutr 31(1):157–171

    Article  CAS  Google Scholar 

  • Fournier J, Timmers ACJ, Sieberer BJ, Jauneau A, Chabaud M, Barker DG (2008) Mechanism of infection thread elongation in root hairs of Medicago truncatula and dynamic interplay with associated rhizobial colonization. Plant Physiol 148:1985–1995

    Article  PubMed  CAS  Google Scholar 

  • Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36

    Article  PubMed  CAS  Google Scholar 

  • Galvan GA, Burger-Meijer K, Kuiper TW, Kik C, Scholten OE (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. (Online) http://orgprints.org/view/projects/int_ conf_qlif2007.html

  • Garbaye J (1994) Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210

    Article  Google Scholar 

  • Gaur A, Adholeya A (2002) Arbuscular-mycorrhizal inoculation of five tropical fodder crops and inoculum production in marginal soil amended with organic matter. Biol Fertil Soils 35:214–218. doi:10.1007/s00374-002-0457-5

    Article  CAS  Google Scholar 

  • Genre A, Bonfante P (2005) Building a mycorrhiza cell: how to reach compatibility between plants and arbuscular mycorrhizal fungi. J Plant Interact 1:3–13

    Article  CAS  Google Scholar 

  • Genre A, Bonfante P (2010) The making of symbiotic cells in arbuscular mycorrhizal roots. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, Dordrecht, pp 57–81

    Chapter  Google Scholar 

  • Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17:3489–3499

    Article  PubMed  CAS  Google Scholar 

  • Gentili F, Jumpponen A (2006) Potential and possible uses of bacterial and fungal biofertilizers. In: Rai MK (ed) Handbook of microbial biofertilizers. Haworth Press, Technology & Engineering, New York, pp 1–28

    Google Scholar 

  • Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41(2):109–117. doi:10.1139/m95-015

    Article  CAS  Google Scholar 

  • Glick BR (2007) Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur J Plant Pathol 119:329–339

    Article  CAS  Google Scholar 

  • Graham PH, Hungria M, Tlusty B (2004) Breeding for better nitrogen fixation in grain legumes: where do the rhizobia fit in? Crop Manag (Online). doi:10.1094/CM-2004-0301-02-RV

  • Guether M, Neuhauser B, Balestrini R, Dynowski M, Ludewig U, Bonfante P (2009) A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol 150:73–83

    Article  PubMed  CAS  Google Scholar 

  • Haas D, Defago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol AOP. doi:10.1038/nrmicro1129, accessed 10 March 2005

  • Hallmann J, Berg G (2006) Spectrum and population dynamics of bacterial root endophytes. In: Schulz B, Boyle S, Sieber T (eds) Microbial root endophytes. Springer, pp. 15–32

  • Hawkins HJ, Johansen A, George E (2000) Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226:275–285

    Article  CAS  Google Scholar 

  • Herridge D, Rose I (2000) Breeding for enhanced nitrogen fixation in crop legumes. Field Crop Res 65:229–248

    Article  Google Scholar 

  • Hildebrandt U, Ouziad F, Marner FJ, 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 254:258–267

    Article  PubMed  CAS  Google Scholar 

  • Hirsch AM (1992) Developmental biology of legume nodulation. New Phytol 122:211–237

    Article  Google Scholar 

  • Hirsch AM, Lum MR, Downie JA (2001) What makes the rhizobia-legume symbiosis so special? Plant Physiol 127:1484–1492

    Article  PubMed  CAS  Google Scholar 

  • Hossain MS, Mårtensson A (2008) Potential use of Rhizobium spp. to improve fitness of nonnitrogen-fixing plants. Acta Agric Scand Sect B Plant Soil Sci 58(4):352–358

    Google Scholar 

  • Howieson JG, Yates RJ, Foster KJ, Real D, Besier RB (2008) Prospects for the future uses of legumes. In: Dilworth MJ, James EK, Sprent JI, Newton WE (eds) Springer Science+Business Media BV, pp 363–394

  • Ibrahim KK, Arunachalam V, Rao PSK, Tilak KVBR (1995) Seasonal response of groundnut genotypes to arbuscular mycorrhiza – Bradyrhizobium inoculation. Microbiol Res 150:218–224

    Article  Google Scholar 

  • Ijdo M, Cranenbrouck S, Declerck S (2011) Methods for large-scale production of AM fungi: past, present, and future. Mycorrhiza 21:1–16

    Article  PubMed  CAS  Google Scholar 

  • Jacobi LM, Kukalev AS, Ushakov KV, Tsyganov VE, Provorov NA, Borisov AY, Tikhonovich I (1999) Genetic variability of garden pea (Pisum sativum L.) for symbiotic capacities. Pisum Genet 31:44–45

    Google Scholar 

  • James EK (2000) Nitrogen fixation in endophytic and associative symbiosis. Field Crop Res 65(2–3):197–209

    Article  Google Scholar 

  • Kempel A, Schmidt AK, Brandl R, Schadler M (2010) Support from the underground: induced plant resistance depends on arbuscular mycorrhizal fungi. Funct Ecol 24:293–300

    Article  Google Scholar 

  • Kennedy IR, Choudhury ATMA, Kecskes ML (2004) Nonsymbiotic bacterial diazotrophs in crop-farming systems: can their potential for plant growth promotion be better exploited? Soil Biol Biochem 36:1229–1244

    Article  CAS  Google Scholar 

  • Kloepper JW, Ryu CM (2006) Bacterial endophytes as elicitors of induced systemic resistance. In: Schulz B, Boyle S, Sieber T (eds) Microbial root endophytes. Springer, Berlin, pp 33–52

    Chapter  Google Scholar 

  • Koricheva J, Gange AC, Jones T (2009) Effects of mycorrhizal fungi on insect herbivores: a metaanalysis. Ecology 90:2088–2097

    Article  PubMed  Google Scholar 

  • Kosuta S, Chabaud M, Lougnon G, Gough C, Denarie J, Barker DG, Becard G (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol 131:952–962

    Article  PubMed  CAS  Google Scholar 

  • Krüger M, Stockinger H, Krüger C, Schüβler A (2009) DNA-based species level detection of Glomeromycota: one PCR primer set for all arbuscular mycorrhizal fungi. New Phytol 183:212–223

    Article  PubMed  CAS  Google Scholar 

  • Krüger M, Krer C, Walker C, Stockinger H, Schüβler A (2012) Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 193:970–984

    Article  PubMed  Google Scholar 

  • Küster H, Vieweg MF, Manthey K, Baier MC, Hohnjec N, Perlick AM (2007) Identification andexpression regulation of symbiotically activated legume genes. Phytochemistry 68:8–18

    Article  PubMed  CAS  Google Scholar 

  • Labutova NM, Polyakov AI, Lyakh VA, Gordon VL (2004) Influence of inoculation with nodule bacteria and endomycorrhizal fungus Glomus intraradices on yield and seed protein and oil content of different soybean cultivars. Russ Agric Sci 4(2):2–4, Doklady Rossiiskoi Akademii Sel’skohozyaistvennykh Nauk

    Google Scholar 

  • Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (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 50:529–544

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Pedrosa A, Gonzalez-Guerrero M, Valderas A, Azcon-Aguilar C, Ferrol N (2006) GintAMTi encodes a functional high-affinity ammonium transporter that is expressed in the extraradical mycelium of Glomus intraradices. Fungal Genet Biol 43:102–110

    Article  PubMed  CAS  Google Scholar 

  • MacLean AM, Finan T, Sadowsky MJ (2007) Genomes of the symbiotic nitrogen-fixing bacteria of legumes. Plant Physiol 144:615–622

    Article  PubMed  CAS  Google Scholar 

  • Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Bécard G, Dénarié J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469(7328):58–63

    Article  PubMed  CAS  Google Scholar 

  • Markmann K, Parniske M (2009) Evolution of root endosymbiosis with bacteria: how novel are nodules? Trends Plant Sci 14:77–86

    Article  PubMed  CAS  Google Scholar 

  • Minerdi D, Bianciotto V, Bonfante P (2002) Endosymbiotic bacteria in mycorrhizal fungi: from their morphology to genomic sequences. Plant Soil 244:211–219

    Article  CAS  Google Scholar 

  • Nielsen JS, Joner EJ, Declerck S, Olsson S, Jakobsen I (2002) Phospho-imaging as a tool for visualization and noninvasive measurement of P transport dynamics in arbuscular mycorrhizas. New Phytol 154:809–820

    Article  CAS  Google Scholar 

  • Oldroyd GED, Downie JA (2006) Nuclear calcium changes at the core of symbiosis signalling. Curr Opin Plant Biol 9:351–357

    Article  PubMed  CAS  Google Scholar 

  • Ovtsyna AO, Staehelin C (2005) Bacterial signals required for the Rhizobium-legume symbiosis. Recent Res Develop Microbiol 7:631–648

    Google Scholar 

  • Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775

    Article  PubMed  CAS  Google Scholar 

  • Pawlowski K, Bisseling T (1996) Rhizobial and actinorhizal symbioses: what are the shared features? Plant Cell 8:1899–1913

    PubMed  CAS  Google Scholar 

  • Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118:10–15

    Article  PubMed  CAS  Google Scholar 

  • Pozo MJ, Jung SC, López-Ráez JA, Azcón-Aguilar C (2010) Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: the role of plant defence mechanisms. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, Dordrecht, pp 193–208

    Chapter  Google Scholar 

  • Prévost D, Antoun H (2005) Potential use of Rhizobium as PGPR with non-legumes. Abstracts from the 2005 Inoculant Forum, March 17–18, Saskatoon, Saskatchewan, Canada

  • Provorov NA (1998) Coevolution of rhizobia with legumes: facts and hypotheses. Symbiosis 24:337–367

    Google Scholar 

  • Provorov NA, Tikhonovich IA (2003) Genetic resources for improving nitrogen fixation in legume-rhizobia symbiosis. Genet Resour Crop Evol 50:89–99

    Article  CAS  Google Scholar 

  • Provorov NA, Vorobyov NI (2010) In: Tikhonovich IA (ed) Evolutionary genetics of plant-microbe symbioses. Nova, NY

    Google Scholar 

  • Provorov NA, Vorobyov NI, Andronov EE (2008) Macro- and microevolution of bacteria in symbiotic systems. Russ J Genet 44(1):6–20

    Article  CAS  Google Scholar 

  • Provorov NA, Shtark OY, Zhukov VA, Borisov AY, Tikhonovich IA (2010) Developmental genetics of plant-microbe symbioses. Nova, NY, USA

    Google Scholar 

  • Quilambo OA (2003) The vesicular-arbuscular mycorrhizal symbiosis. African J Biotechnol 2:539–546

    CAS  Google Scholar 

  • Rai MK (ed) (2006) Handbook of microbial biofertilizers. Haworth Press, Technology & Engineering

  • Rambelli A (1973) The rhizosphere of mycorrhizae. In: Marks GL, Koslowski TT (eds) Ectomycorrhizae. Academic, New York, pp 299–343

    Google Scholar 

  • Remans R, Croonenborghs A, Gutierrez RT, Michiels J, Vanderleyden J (2007) Effects of plant growth-promoting rhizobacteria on nodulation of Phaseolus vulgaris L. are dependent on plant P nutrition. In: Bakker PAHM, Raaijmakers JM, Bloemberg G, Höfte M, Lemanceau P, Cooke BM (eds) New perspectives and approaches in plant growth-promoting rhizobacteria research. Springer, Netherlands, pp 341–351

    Chapter  Google Scholar 

  • Rengel Z (2002) Breeding for better symbiosis. Plant Soil 245:147–162

    Article  CAS  Google Scholar 

  • Requena N, Jimenez J, Toro M, Barea JM (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 136:667–677

    Article  Google Scholar 

  • Requena N, Perez-Solis E, Azcуn-Aguilar C, Jeffries P, Barea JM (2001) Management of indigenous plant-microbe symbioses aids restoration of desertified ecosystems. Appl Environ Microbiol 67(2):495–498

    Article  PubMed  CAS  Google Scholar 

  • Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339

    Article  CAS  Google Scholar 

  • Rillig MC (2004) Arbuscular mycorrhizae, glomalin and soil aggregation. Can J Soil Sci 84:355–363

    Article  Google Scholar 

  • Roth LE, Stacey G (1989) Bacterium release into host cells of nitrogen-fixing soybean nodules: the symbiosome membrane comes from three sources. Eur J Cell Biol 49:13–23

    PubMed  CAS  Google Scholar 

  • Rufyikiri G, Declerck S, Thiry Y (2004) Comparison of 233U and 33P uptake and translocation by the arbuscular mycorrhizal fungus Glomus intraradices in root organ culture conditions. Mycorrhiza 14:203–207

    Article  PubMed  Google Scholar 

  • Ruiz-Lozano JM, Aroca R (2010) Host response to osmotic stresses: stomatal behaviour and water use efficiency of arbuscular mycorrhizal plants. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, Dordrecht, pp 239–256

    Chapter  Google Scholar 

  • Sabannavara SJ, Lakshmana HC (2011) Synergistic interactions among Azotobacter, Pseudomonas, and arbuscular mycorrhizal fungi on two varieties of Sesamum indicum L. Commun Soil Sci Plan 42(17):2122–2133

    Article  CAS  Google Scholar 

  • Sanchez L, Weidmann S, Brechenmacher L, Batoux M, van Tuinen D, Lemanceau P, Gianinazzi S, Gianinazzi-Pearson V (2004) Common gene expression in Medicago truncatula roots in response to Pseudomonas fluorescens colonization, mycorrhiza development and nodulation. New Phytol 161:855–863

    Article  CAS  Google Scholar 

  • Sanchez L, Weidmann S, Arnould C, Bernard AR, Gianinazzi S, Gianinazzi-Pearson V (2005) Pseudomonas fluorescens and Glomus mosseae trigger DMI3-dependent activation of genes related to a signal transduction pathway in roots of Medicago truncatula. Plant Physiol 139:1065–1077

    Article  PubMed  CAS  Google Scholar 

  • Sandhu HS, Gupta VVSR, Wratten SD (2010) Evaluating the economic and social impact of soil microbes. In: Dixon GR, Tilston EL (eds) Soil microbiology and sustainable crop production. Springer, Dordrecht, pp 399–417

    Chapter  Google Scholar 

  • Schultze M, Kondorosi A (1998) Regulation of symbiotic root nodule development. Annu Rev Genet 32:33–57

    Article  PubMed  CAS  Google Scholar 

  • Schulz B, Boyle S, Sieber T (2006) What are endophytes? In: Schulz B, Boyle S, Sieber T (eds) Microbial root endophytes. Springer, Dordrecht, pp 1–14

    Chapter  Google Scholar 

  • Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Schweiger P, Jakobsen I (2000) Laboratory and field methods for measurement of hyphal uptake of nutrients in soil. Plant Soil 226:237–244

    Article  CAS  Google Scholar 

  • Sessitsch A, Howieson JG, Perret X, Antoun H, Martinez-Romero E (2002) Advances in Rhizobium research. Crit Rev Plant Sci 21:323–378

    Article  CAS  Google Scholar 

  • Shtark OY, Danilova TN, Naumkina TS, Vasilchikov AG, Chebotar VK, Kazakov AE, Zhernakov AI, Nemankin TA, Prilepskaya NA, Borisov AY, Tikhonovich IA (2006) Analysis of pea (Pisum sativum L.) source material for breeding of cultivars with high symbiotic potential and choice of criteria for its evaluation. Ecol genet (Ekologicheskaja genetika) 4(2):22–28, In Russian

    Google Scholar 

  • Shtark OY, Borisov AY, Zhukov VA, Provorov NA, Tikhonovich IA (2010) Intimate associations of beneficial soil microbes with the host plants. In: Dixon GR, Tilston EL (eds) Soil microbiology and sustainable crop production. Springer, Dordrecht, pp 119–196

    Chapter  Google Scholar 

  • Shtark O, Provorov N, Mikić A, Borisov A, Ćupina B, Tikhonovich I (2011) Legume root symbioses: natural history and prospects for improvement. Ratarstvo I Povrtarstvo (Field Veg Crops Res) 48:291–304

    Article  Google Scholar 

  • Siddiqui ZA (2006) PGPR: prospective biocontrol agents of plant pathogens. In: Siddiqui ZA (ed) PGPR: Biocontrol and biofertilization. Springer, Printed in the Netherlands, pp 111–142

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London

    Google Scholar 

  • Spaink HP (1995) The molecular basis of infection and nodulation by Rhizobia: the ins and outs of sympathogenesis. Ann Rev Phytopathol 33:345–368

    Article  CAS  Google Scholar 

  • Spaink HP, Kondorosi A, Hooykaas PJJ (eds) (1998) The Rhizobiaceae. Molecular biology of model plant-associated bacteria. Kluwer Acad Publ, Dordrecht, Boston, London

    Google Scholar 

  • Sprent JI (2001) Nodulation in legumes. Cromwell Press Ltd, Kew, Royal Botanical Gardens

    Google Scholar 

  • Sprent JI (2007) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytol 174:11–25

    Article  PubMed  CAS  Google Scholar 

  • Sprent JI, James EK (2007) Legume evolution: where do nodules and mycorrhizas fit in? Plant Physiol 144:575–581

    Article  PubMed  CAS  Google Scholar 

  • Staehelin C, Xie ZP, Illana A, Vierheilig H (2011) Long-distance transport of signals during symbiosis: are nodule formation and mycorrhization autoregulated in a similar way? Plant Signal Behav 6(3):372–377

    Article  PubMed  CAS  Google Scholar 

  • Steenhoudt O, Vanderleyden J (2000) Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24(4):487–506

    Article  PubMed  CAS  Google Scholar 

  • Stockinger H, Walker C, Schüßler A (2009) ‘Glomus intraradices DAOM197198’, a model fungus in arbuscular mycorrhizal research, is not Glomus intraradices. New Phytol 183:1176–1187. doi:10.1111/j.1469-8137.2009.02874.x

    Article  PubMed  Google Scholar 

  • Sturz AV, Christie BR, Nowak J (2000) Bacterial endophytes: potential role in developing sustainable systems of crop production. Cr Rev Plant Sci 19(1):1–30

    Article  Google Scholar 

  • Suominen L, Roos C, Lortet G, Paulin L, Lindström K (2001) Identification nd structure of the rhizobium galegae common nodulation genes: evidence for horizontal gene transfer. Mol Biol Evol 18:907–916

    Article  PubMed  CAS  Google Scholar 

  • Terefework Z, Lortet G, Souminen L, Lindström K (2000) Molecular evolution of interactions between rhizobia and their legume hosts. In: Procaryotic nitrogen fixation: a model system for analysis of a biological process. Horizon Sci Press, Wymondham, pp 187–206

    Google Scholar 

  • Tikhonovich IA, Provorov NA (2007) Cooperation of plants and microorganisms: getting closer to the genetic construction of sustainable agro-systems. Biotechnol J 2(7):833–848

    Article  PubMed  CAS  Google Scholar 

  • Tilak KVBR, 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 57:67–71

    Article  CAS  Google Scholar 

  • Timmers ACJ, Vallotton P, Heym C, Menzel D (2007) Microtubule dynamics in root hairs of Medicago truncatula. Eur J Cell Biol 86:69–83

    Article  PubMed  CAS  Google Scholar 

  • Toljander JF, Lindahl BD, Paul LR, Elfstrand M, Finlay RD (2007) Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiol Ecol 61:295–304

    Article  PubMed  CAS  Google Scholar 

  • Tsigie A, Tilak KVBR, Saxena AK (2011) Field response of legumes to inoculation with plant growth-promoting rhizobacteria. Biol Fertil Soils 47(8):971–974

    Article  Google Scholar 

  • Tsyganov VE, Voroshilova VA, Priefer UB, Borisov AY, Tikhonovich IA (2002) Genetic dissection of the initiation of the infection process and nodule tissue development in the Rhizobium-pea (Pisum sativum L.) symbiosis. Ann Bot 89:357–366

    Article  PubMed  CAS  Google Scholar 

  • Turnau K, Ryszka P, Wojtczak G (2010) Metal tolerant mycorrhizal plants: a review from the perspective on industrial waste in temperate region. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, Dordrecht, pp 257–279

    Chapter  Google Scholar 

  • Vallad E, Goodman RM (2004) Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Sci 44:1920–1934

    Article  Google Scholar 

  • Van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254

    Article  CAS  Google Scholar 

  • Van Overbeek LS, van Vuurde J, van Elsas JD (2006) Application of molecular fingerprinting techniques to explore the diversity of bacterial endophytic communities. In: Schulz B, Boyle S, Sieber T (eds) Microbial root endophytes. Springer, pp 337–354

  • Vance CP (2001) Symbiotic nitrogen fixation and phosphorous acquisition. Plant nutrition in the world of declining renewable resources. Plant Physiol 127:390–397

    Article  PubMed  CAS  Google Scholar 

  • Vance CP, Heichel GH (1991) Carbon in N2 fixation: limitation or exquisite adaptation? Annu Rev Plant Physiol 42:373–392

    Article  CAS  Google Scholar 

  • Vavilov NI (1951) The origin, variation, immunity and breeding of cultivated plants. Chronica Bot 13(1/6):1–364

    Google Scholar 

  • Vavilov NI (1987) Breeding as Science. Theoretical bases of breeding. Moscow, pp 28–39

  • Vessey JK, Buss TJ (2002) Bacillus cereus UW85 inoculation effects on growth, nodulation, and N accumulation in grain legumes: controlled-environment studies. Can J Plant Sci 82(2):282–290

    Article  Google Scholar 

  • Xavier IJ, Holloway G, Leggett M (2004) Development of rhizobial inoculant formulations. Crop Manag (Online). doi:10.1094/CM-2004-0301-06-RV

  • Zavalin AA, Kozhemyakov AP (2010) New technologies of production and use of complex biological preparations. Khimizdat, St. Petersburg, in Russian

    Google Scholar 

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Acknowledgments

We thank Dr. Margarita A. Vishnyakova (N.I. Vavilov All-Russia Research Institute of Plant Industry, St-Petersburg, Russian Federation), Dr. Tatiana S. Naumkina (All-Russia Institute of Legumes and Groat Crops, Orel, Russian Federation) and Dr. Vladimir K. Chebotar (“Bisolbi-Inter” Ltd., St-Petersburg, Russian Federation) for the long-term collaboration in the fields of legume breeding and development of microbial inoculants. This work was supported by the grants of President of the Russian Federation (337.2012.4), RFBR (10-04-01146, 12-04-01687, 12-04-32126, 13-04-01702, 13-04-01703), Russian Ministry of Science and Education (Agreement No. 8056).

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  1. All-Russia Research Institute for Agricultural Microbiology, Podbelsky Sh. 3, St.-Petersburg, Pushkin, 196608, Russia

    Oksana Y. Shtark, Alexey Y. Borisov, Vladimir A. Zhukov & Igor A. Tikhonovich

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  1. Oksana Y. Shtark
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  2. Alexey Y. Borisov
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  3. Vladimir A. Zhukov
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  4. Igor A. Tikhonovich
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Correspondence to Oksana Y. Shtark.

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Shtark, O.Y., Borisov, A.Y., Zhukov, V.A. et al. Mutually beneficial legume symbioses with soil microbes and their potential for plant production. Symbiosis 58, 51–62 (2012). https://doi.org/10.1007/s13199-013-0226-2

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