Response and interaction of Bradyrhizobium japonicum and arbuscular mycorrhizal fungi in the soybean rhizosphere

Abstract

Regulatory response and interaction of Bradyrhizobium and arbuscular mycorrhizal fungi (AMF) play a vital role in rhizospheric soil processes and productivity of soybean (Glycine max L.). Nitrogen (N) and phosphorus (P) are essential nutrients for plant growth and productivity, the synergistic interaction(s) of AMF and Bradyrhizobium along with rhizospheric beneficial microorganisms stimulate soybean growth and development through enhanced mineral nutrient acquisition (N and P) and improved rhizosphere environment. Such interactions are crucial, especially under low-input eco-friendly agricultural cropping systems, which rely on biological processes rather than agrochemicals to maintain soil quality, sustainability, and productivity. Furthermore, enhancement of N-fixation by root nodules along with AMF-mediated synergism improves plant P nutrition and uptake, and proliferation of phosphate-solubilizing fungi. However, the genetic and/or allelic diversity among native strains, their genes/enzymes and many environmental factors (e.g., soil organic matter, fertilizers, light, temperature, soil moisture, and biotic interactors) affect the interactions between AMF and Bradyrhizobium. New information is available regarding the genetic composition of elite soybean inoculant strains in maximizing symbiotic performance, N-fixing capabilities and depending on N and P status the host-mediated regulation of root architecture. Overall, for sustainable soybean production systems, a deeper understanding of the interaction effects of Bradyrhizobium and AMF co-inoculation are expected in the future, so that optimized combinations of microorganisms can be applied as effective soil inoculants for plant growth promotion and fitness. The objective of this review is to offer insights into the mechanistic interactions of AMF and Bradyrhizobium and rhizopheric soil health, and elucidate the role of environmental factors in regulating growth, development and sustainable soybean productivity.

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References

  1. Adesemoye AO, Kloeppe JW (2009) Plant-microbe interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85:1–12

    CAS  PubMed  Article  Google Scholar 

  2. Aibara I, Miwa K (2014) Strategies for optimization of mineral nutrient transport in plants: multilevel regulation of nutrient-dependent dynamics of root architecture and transporter activity. Plant Cell Physiol 55:2027–2036

    CAS  PubMed  Article  Google Scholar 

  3. Almeida JPF, Hartwig UA, Frehner M et al (2000) Evidence that P deficiency induces N feedback regulation of symbiotic N2 fixation in white clover (Trifolium repens L.). J Exp Bot 51:1289–1297

    CAS  PubMed  Google Scholar 

  4. Aranjuelo I, Arrese-Igor C, Molero G (2014) Nodule performance within a changing environmental context. J Plant Physiol 171:1076–1090

    CAS  PubMed  Article  Google Scholar 

  5. Artursson V, Jansson JK (2003) Use of bromodeoxyuridine immunocapture to identify active bacteria associated with arbuscular mycorrhizal hyphae. Appl Environ Microbiol 69:6208–6215

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  6. Ashoka P, Meena RS, Kumar S et al (2017) Green nanotechnology is a key for eco-friendly agriculture. J Clean Prod 142:4440–4441

    Article  Google Scholar 

  7. Atkinson D, Watson CA (2000) The beneficial rhizosphere: a dynamic entity. Appl Soil Ecol 15:99–104

    Article  Google Scholar 

  8. Auge RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  9. Ballhorn DJ, Schadler M, Elias JD et al (2016) Friend or foe—light availability determines the relationship between mycorrhizal fungi, rhizobia and Lima Bean (Phaseolus lunatus L.). PLoS One 11:e0154116

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  10. Bandyopadhyay P, Bhuyan SK, Yadava PK et al (2017) Emergence of plant and rhizospheric microbiota as stable interactomes. Protoplasma 254:617–626

    PubMed  Article  Google Scholar 

  11. Barea JM, Azcon R, Azcon-Aguilar C (2002) Mycorrhizosphere interactions to improve plant fitness and soil quality. Antonie Van Leeuwenhoek 81:343–351

    CAS  PubMed  Article  Google Scholar 

  12. Barea JM, Werner D, Azcon-Aguilar C et al (2005) Interactions of arbuscular mycorrhiza and nitrogen fixing symbiosis in sustainable agriculture. In: Werner D, Newton WE (eds) Agriculture, forestry, ecology and the environment. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  13. Barrett G, Campbell CD, Fitter AH et al (2011) The arbuscular mycorrhizal fungus Glomus hoi can capture and transfer nitrogen from organic patches to its associated host plant at low temperature. Appl Soil Ecol 48:102–105

    Article  Google Scholar 

  14. Behm JE, Kiers ET (2014) A phenotypic plasticity framework for assessing intraspecific variation in arbuscular mycorrhizal fungal traits. J Ecol. 102:315–327

    Article  Google Scholar 

  15. Bellieny-Rabelo D, Oliveira AE, Venancio TM (2013) Impact of whole-genome and tandem duplications in the expansion and functional Diversification of the FBox family in legumes (Fabaceae). PLoS ONE 8:e55127

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. Benjamin JG, Nielsen DC (2006) Water deficit effects on root distribution of soybean, field pea and chickpea. Field Crops Res 97:248–253

    Article  Google Scholar 

  17. Berruti A, Lumini E, Ballestrini R et al (2015) Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front Microbiol 6:1559

    PubMed  Google Scholar 

  18. Bianciotto V, Bonfante P (2002) Arbuscular mycorrhizal fungi: a specialized niche for rhizospheric and endocellular bacteria. Antonie Van Leeuwenhoek 81:365–371

    CAS  PubMed  Article  Google Scholar 

  19. Bonneau L, Huguet S, Wipf D et al (2013) Combined phosphate and nitrogen limitation generates a nutrient stress transcriptome favorable for arbuscular mycorrhizal symbiosis in Medicago truncatula. New Phytol 199:188–202

    CAS  PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

  21. Cely MVT, de Oliveira AG, de Freitas DF et al (2016) Inoculant of arbuscular mycorrhizal fungi (Rhizophagus clarus) increase yield of soybean and cotton under field conditions. Front Microbiol 7:720

    PubMed  PubMed Central  Article  Google Scholar 

  22. Chagnon PL, Bainard LD (2015) Using molecular biology to study mycorrhizal fungal community ecology: limits and perspectives. Plant Signal Behav 10:e1046668

    PubMed  PubMed Central  Google Scholar 

  23. Chang C, Nasir F, Ma L et al (2017) Molecular communication and nutrient transfer of arbuscular mycorrhizal fungi, symbiotic nitrogen-fixing bacteria, and host plant in tripartite symbiosis. In: Sulieman S, Tran LS (eds) Legume nitrogen fixation in soils with low phosphorus availability. Springer, Cham

    Google Scholar 

  24. Chebrolu KK, Fristschi FB, Ye S et al (2016) Impact of heat stress during seed development on soybean seed metabolome. Metabolomics 12:28

    Article  CAS  Google Scholar 

  25. Clough TJ, Condron LM, Kammann C et al (2013) A review of biochar and soil nitrogen dynamics. Agronomy 2:275–293

    Article  CAS  Google Scholar 

  26. Corradi C, Brachmann A (2017) Fungal mating in the most widespread plant symbionts?. Trends Plant Sci 22:175–183

    CAS  PubMed  Article  Google Scholar 

  27. Coskan A, Gok M, Onac I et al (2003) The effects of rhizobium and mycorrhiza interactions on N2-fixation, biomass and P uptake. J Cukurova Uni Facul Agri 18:35–44

    Google Scholar 

  28. Coskan A, Gok M, Erol H et al (2010) Humic + fulvic acid as a bio-stimulator on biological nitrogen fixation. 9. Symposiums des Verband deutsch-türkischer Agrarund Naturwissenschaftler (VDTAN). Marz, Mustafa Kemal Univ. Hatay, Turkey, pp 22–27

    Google Scholar 

  29. Delamuta JRM, Ribeiro RA, Menna P et al (2012) Multilocus sequence analysis (MLSA) of Bradyrhizobium strains: revealing high diversity of tropical diazotrophic symbiotic bacteria. Braz J Microbiol. 43: 698–10

  30. Dijkstra FA, Cheng W (2007) Moisture modulates rhizosphere effects on C decomposition in two different soil types. Soil Biol Biochem 39:2264–2274

    CAS  Article  Google Scholar 

  31. Ding X, Zhang S, Wang R et al (2016) AM fungi and rhizobium regulate nodule growth, phosphorous (P) uptake, and soluble sugar concentration of soybeans experiencing P deficiency. J Pant Nutr 39:1917–1925

    Google Scholar 

  32. Dogan K, Gok M, Coskan A (2010) Effects of bacteria inoculation and iron application on biomass, yield and nitrogen contents in Cukurova region. 5th National Plant Nutrition and Fertilization Congress, Izmir, 15–17 September 2010

  33. Dube KG (2011) Effect of organic manures, biofertilizers and growth regulators in alone and combination treatments on the growth of leaves in Stevia rebaudiana Bertoni. Asiatic J Biotech Resour 2:403–413

    Google Scholar 

  34. Friberg S (2001) Distribution and diversity of arbuscular mycorrhizal fungi in traditional agriculture on the Niger inland delta, Mali, West Africa. CBM’s Skriftserie 3:53–80

    Google Scholar 

  35. Fu X (2016) New insights into plant nutrient signaling and adaptation to fluctuating environments. J Genet Genom 43:621–622

    Article  Google Scholar 

  36. Gadkar V, David-Schwartz R, Kunit T et al (2001) Arbuscular mycorrhiza fungi colonization factors involved in host recogination. Plant Physiol 127:1493–1499

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  37. Gahoonia TS, Nielsen NE (2004) Root traits as tools for creating phosphorus efficient crop varieties. Plant Soil 260:47–57

    Article  Google Scholar 

  38. Gao X, Lu X, Wu M et al (2012) Co-Inoculation with rhizobia and AMF inhibited soybean red crown rot: from field study to plant defense-related gene expression analysis. PLoS ONE 7:e33977

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  39. Garbeva P, Veen JAV, Elsas JDV (2004) Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Ann Rev Phytopathol 42:243–270

    CAS  Article  Google Scholar 

  40. Garnett T, Conn V, Kaiser B (2009) Root based approaches to improving nitrogen use efficiency in plants. Plant Cell Environ 32:1272–1283

    CAS  PubMed  Article  Google Scholar 

  41. Gavrin A, Chiasson D, Ovchinnikova E et al (2016) VAMP721a and VAMP721d are important for pectin dynamics and release of bacteria in soybean nodules. New Phytol 210:1011–1021

    CAS  PubMed  Article  Google Scholar 

  42. Genre A, Russo G (2016) Does a common pathway transduce symbiotic signals in plant–microbe interactions? Front Plant Sci 7:96

    PubMed  PubMed Central  Article  Google Scholar 

  43. Giri B, Mukerji KG (2004) Mycorrhizal inoculants alleviate salt stress in Sesbania aegyptiaca and Sesbania grandiflora under field conditions: Evidence for reduced sodium and improved magnesium uptake. Mycorrhiza 14:307–312

    PubMed  Article  Google Scholar 

  44. Gobbato E, Marsh JF, Vernie T et al (2012) A GRAS-type transcription factor with a specific function in mycorrhizal signaling. Curr Biol 22:2236–2241

    CAS  PubMed  Article  Google Scholar 

  45. Graham PH, Vance CP (2000) Nitrogen fixation in perspective: an overview of research and extension needs. Field Crop Res 65:93–106

    Article  Google Scholar 

  46. Hardarson G, Atkins C (2003) Optimizing biological N2 fixation by legumes in farming systems. Plant Soil 252:41–54

    CAS  Article  Google Scholar 

  47. Hartmann A, Rothballer M, Schmid M (2008) Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil 312:7

    CAS  Article  Google Scholar 

  48. Herman DJ, Johnson KK, Jaeger CH et al (2006) Root influence on nitrogen mineralization and nitrification in Avena barbata rhizosphere soil. Soil Sci Soc America J 70:1504–1511

    CAS  Article  Google Scholar 

  49. Hill GT, Mitkowski NA, Aldrich-Wolfe L et al (2000) Methods for assessing the composition and diversity of soil microbial communities. Appl Soil Microbe 15:25–36

    Article  Google Scholar 

  50. Hirsch PR, Mauchline TM (2012) Who’s who in the plant root microbiome?. Nature Biotechnol 30:961–962

    CAS  Article  Google Scholar 

  51. Hocking PJ (2001) Organic acids exuded from roots in phosphorus uptake and aluminium tolerance of plants in acid soils. Adv Agron 74:63–97

    CAS  Article  Google Scholar 

  52. Houlton BZ, Wang YP, Vitousek PM et al (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature. 454:327–330

    CAS  PubMed  Article  Google Scholar 

  53. Ibiang YB, Mitsumoto H, Sakamoto K (2017) Bradyrhizobia and arbuscular mycorrhizal fungi modulate manganese, iron, phosphorus, and polyphenols in soybean (Glycine max (L.) Merr.) under excess zinc. Environ Exp Bot 137:1–13

    CAS  Article  Google Scholar 

  54. Igiehon NO, Babalola OO (2017) Biofertilizers and sustainable agriculture: exploring arbuscular mycorrhizal fungi. Appl Microbiol Biotechnol 101:4871–4881

    CAS  PubMed  Article  Google Scholar 

  55. Isler E, Coskan A (2009) Effect of different bacterium (Bradyrhizobium japonicum) inoculation techniques on biological nitrogen fixation and yield of soybean. Tarim Bilimleri Dergisi 15:324–331

    Article  Google Scholar 

  56. Itakura M, Saeki K, Omuri H et al (2009) Genomic comparison of Bradyrhizobium japonicum strains with different symbiotic nitrogen-fixing capabilities and other Bradyrhizobiaceae members. The ISME J 3:326–339

    CAS  PubMed  Article  Google Scholar 

  57. Ivanov S, Federova EE, Limpens E et al (2012) Rhizobium–legume symbiosis shares an exocytotic pathway required for arbuscule formation. Proc Natl Acad Sci USA 109:8316–8321

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  58. Jakobsen I, Gazey C, Abbott IK (2001) Phosphate transport by communities of arbuscular mycorrhizal fungi in intact soil cores. New Phytol 149:95–103

    CAS  Article  Google Scholar 

  59. Jiang Y, Wang W, Xie Q et al (2017) Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 1172–1175

  60. Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48:1–13

    CAS  PubMed  Article  Google Scholar 

  61. Johnson D, Martin F, Cairney JWG et al (2012) The importance of individuals: intraspecific diversity of mycorrhizal plants and fungi in ecosystems. New Phytol 194:614–628

    PubMed  Article  Google Scholar 

  62. Joshi R, Wani SH, Singh B et al (2016) Transcription factors and plants response to drought stress: current understanding and future directions. Front Plant Sci 7:1029

    PubMed  PubMed Central  Article  Google Scholar 

  63. Keerio MI (2001) Nitrogenase activity of soybean root nodules inhibited after heat stress. Online J Biol Sci 1:297–300

    Google Scholar 

  64. Kennedy AC, Smith KL (2001) Soil microbial diversity and the sustainability of agricultural soil. Plant Soil 170:75–86

    Article  Google Scholar 

  65. Kiers ET, Denison RF (2008) Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annu Rev Ecol Evol Syst 39:215–236

    Article  Google Scholar 

  66. Kiers ET, Duhamel M, Beesetty Y et al (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882

    CAS  PubMed  Article  Google Scholar 

  67. Kikuchi Y, Hijikata N, Ohtomo R et al (2016) Aquaporin-mediated long-distance polyphosphate translocation directed towards the host in arbuscular mycorrhizal symbiosis: application of virus-induced gene silencing. New Phytol 211:1202–1208

    CAS  PubMed  Article  Google Scholar 

  68. Konvalinkova T, Jansa J (2016) Lights off for arbuscular mycorrhiza: on its symbiotic functioning under light deprivation. Front Plant Sci 7:782

    PubMed  PubMed Central  Article  Google Scholar 

  69. Krishnapriya V, Pandey R (2016) Root exudation index: screening organic acid exudation and phosphorus acquisition efficiency in soybean genotypes. Crop Pasture Sci 67:1096–1109

    CAS  Google Scholar 

  70. Kuklinsky-Sobral J, Araújo WL, Mendes R et al (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol l 6:1244–1251

    CAS  Article  Google Scholar 

  71. Latef AAHA, Chaoxing H (2011) Arbuscular mycorrhizal influence on growth, photosynthetic pigments, osmotic adjustment and oxidative stress in tomato plants subjected to low-temperature stress. Acta Phys Plantarum 33:1217–1225

    Article  CAS  Google Scholar 

  72. Lenoir I, Fontaine J, Sahraoui ALH (2016) Arbuscular mycorrhizal fungal responses to abiotic stresses: a review. Phytochemistry 123:4–15

    CAS  PubMed  Article  Google Scholar 

  73. Li B, Li YY, Wu HM et al (2016) Root exudates drive interspecific facilitation by enhancing nodulation and N2 fixation. Proc Natl Acad Sci USA 113:6496–6501

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  74. Liu ZL, Li YJ, Hou HY (2013) Differences in the arbuscular mycorrhizal fungi-improved rice resistance to allow temperature at two N levels: aspects of N and C metabolism on the plant side. Plant Phys Bioch 7:87–95

    Article  CAS  Google Scholar 

  75. Liu Z, Li Y, Ma L et al (2015) Coordinated regulation of arbuscular mycorrhizal fungi and soybean MAPK pathway genes improved mycorrhizal soybean drought tolerance. Mol Plant Microbe Interact 28:408–419

    PubMed  Article  CAS  Google Scholar 

  76. Luginbuehl LH, Menard GN, Kurup S et al (2017) Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science 356:1175–1178

    CAS  PubMed  Article  Google Scholar 

  77. Ma Y, Oliveira RS, Freitas H et al (2016) Biochemical and molecular mechanisms of plant-microbe-metal interactions: relevance for phytoremediation. Front Plant Sci 7:918

    PubMed  PubMed Central  Google Scholar 

  78. Marzban Z, Faryabi E, Torabian S (2017) Effects of arbuscular mycorrhizal fungi and Rhizobium on ion content and root characteristics of green bean and maize under intercropping. Acta agriculturae Slovenica 109:79–88

    Article  Google Scholar 

  79. Massalha H, Korenblum E, Tholl D et al (2017) Small molecules below-ground: the role of specialized metabolites in the rhizosphere. Plant J 90:788–807

    CAS  PubMed  Article  Google Scholar 

  80. Meena RS (2013a) Response to different nutrient sources on green gram (Vigna radiata L.) productivity. Indian J Ecol 40:353–31555

  81. Meena RS (2013b) Resources conservation agriculture—a review. Ann Biol 29:301–306

    Google Scholar 

  82. Meena RS, Yadav RS (2014) Phonological performance of groundnut varieties under sowing environments in hyper arid zone of Rajasthan, India. J Appl Nat Sci 6:344–348

    CAS  Google Scholar 

  83. Meena RS, Dhaka Y, Bohra JS et al (2015a) Influence of bioinorganic combinations on yield, quality and economics of mung bean. Am J Exp Agri 8:159–166

    Google Scholar 

  84. Meena RS, Yadav RS, Meena H et al (2015b) Towards the current need to enhance legume productivity and soil sustainability worldwide: a book review. J Clean Prod 104:513–515

    Article  Google Scholar 

  85. Meena RS, Gogoi N, Kumar S (2017) Alarming issues on agricultural crop production and environmental stresses. J Clean Prod 142:3357–3359

    Article  Google Scholar 

  86. Meng L, Zhang A, Wang F et al (2015) Arbuscular mycorrhizal fungi and rhizobium facilitate nitrogen uptake and transfer in soybean/maize intercropping system. Front Plant Sci 6:339

    PubMed  PubMed Central  Google Scholar 

  87. Millar NS, Bennet AE (2016) Stressed out symbiotes: hypotheses for the influence of abiotic stress on arbuscular mycorrhizal fungi. Oecologia 182:625–641

    PubMed  PubMed Central  Article  Google Scholar 

  88. Miransari M, Bahrami HA, Rejali F et al (2008) Using arbuscular mycorrhiza to alleviate the stress of soil compaction on wheat (Triticum aestivum L.) growth. Soil Biol Biochem 40:1197–1106

    CAS  Article  Google Scholar 

  89. Monier B, Peta V, Mensah J, Bücking H (2017) Inter- and intraspecific fungal diversity in the arbuscular mycorrhizal symbiosis. In: Varma A, Prasad R, Tuteja N (eds) Mycorrhiza—function, diversity, state of the art. Springer, Cham

    Google Scholar 

  90. Mutava RN, Prince SJK, Syed NH et al (2015) Understanding abiotic stress tolerance mechanisms in soybean: a comparative evaluation of soybean response to drought and flooding stress. Plant Physiol Biochem 86:109–120

    CAS  PubMed  Article  Google Scholar 

  91. Nardi S, Concheri G, Pizzegelho D et al (2000) Soil organic matter mobilization by root exudates. Chemosphere 41:653–658

    CAS  PubMed  Article  Google Scholar 

  92. Nouri E, Breullin-Sessoms F, Feller U et al (2014) Phosphorus and nitrogen regulate arbuscular mycorrhizal symbiosis in Petunia hybrida. PLoS ONE 9(3):e90841

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  93. O’Brian MR, Vance CP, VandenBosch KA (2009) Legume focus: model species sequenced, mutagenesis approaches extended, and debut of a new model. Plant Physiol 151:969

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  94. Omirou M, Fasoula DA, Ioannides IM (2016) Bradyrhizobium inoculation alters indigenous AMF community assemblages and interacts positively with AMF inoculum to improve cowpea performance. Appl Soil Ecol 108:381–389

    Article  Google Scholar 

  95. Opik M, Davison J (2016) Uniting species- and community-oriented approaches to understand arbuscular mycorrhizal fungal diversity. Fungal Ecol. 24:106–113

    Article  Google Scholar 

  96. Ordonez YM, Fernandez BR, Lara LS et al (2016) Bacteria with phosphate solubilizing capacity alter mycorrhizal fungal growth both inside and outside the root and in the presence of native microbial communities. PLoS ONE 11:e0154438

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  97. Ossler JN, Zielinski CA, Heath KD (2015) Tripartite mutualism: Facilitation or trade-off s between rhizobial and mycorrhizal symbionts of legume hosts. Am J Bot 102:1332–1341

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  99. Parsons R, Stanforth A, Raven JA et al (1993) Nodule growth and activity may be regulated by a feedback mechanism involving phloem nitrogen. Plant Cell Environ. 16: 125 – 36

  100. Penuelas J, Poulter B, Sardans J et al (2013) Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe. Nat Commun 4:2934

    PubMed  Google Scholar 

  101. Perez-Jaramillo JE, Mendes R, Raaijmakers JM (2016) Impact of plant domestication on rhizosphere microbiome assembly and functions. Plant Mol Biol. 90: 635 – 44

  102. Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274:37–49

    CAS  Article  Google Scholar 

  103. Rascovan N, Carbonetto B, Perrig D et al (2016) Integrated analysis of root microbiomes of soybean and wheat from agricultural fields. Sci Rep 6:28084

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  104. Read DJ (1992) The mycorrhizal mycelium. In: Allen MF (ed) Mycorrhizal functioning: an integrative plant-fungal process. Chapman and Hall, New York, pp 102–133

    Google Scholar 

  105. Remigi P, Zhu J, Young JPW et al (2016) Symbiosis within symbiosis: evolving nitrogen-fixing legume symbionts. Trends Microbiol 24:63–75

    CAS  PubMed  Article  Google Scholar 

  106. Rogers ED. Benfey PN (2015) Regulation of plant root system architecture: implications for crop advancement. Curr Opin Biotechnol 32:93–98

    CAS  PubMed  Article  Google Scholar 

  107. Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 152:569–572

    Google Scholar 

  108. Ruiz-Lozano JM, Collados C, Barea JM et al (2001) Arbuscular mycorrhizal symbiosis can alleviate drought-induced nodule senescence in soybean plants. New Phytol 151:493–502

    CAS  Article  Google Scholar 

  109. Sadowsky MJ (2005) Soil stress factors influencing symbiotic nitrogen fixation. Werner D, Newton WE (eds), Nitrogen fixation in agriculture, forestry, ecology, and the environment. Springer, Dordrecht, pp 89–112

    Google Scholar 

  110. Saito M (2000) Symbiotic exchange of nutrients in arbuscular mycorrhizas: transport and transfer of phosphorus. In Kapulnik Y, Douds DD, Jr (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, Dordrecht, pp 85–106

    Google Scholar 

  111. Saito M, Kato T, Saito M (1994) Effects of low temperature and shade on relationships between nodulation, vesicular-arbuscular mycorrhizal infection, and shoot growth of soybeans. Biol Fertil Soils 17:206–211

    Article  Google Scholar 

  112. Sanders IR, Rodriguez A (2016) Aligning molecular studies of mycorrhizal fungal diversity with ecologically important levels of diversity in ecosystems. The ISME J 10:2780–2786

    PubMed  Article  Google Scholar 

  113. Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340

    CAS  PubMed  Article  Google Scholar 

  114. Schlaeppi K, Bender SF, Mascher F et al (2016) High-resolution community profiling of arbuscular mycorrhizal fungi. New Phytol 212:780–791

    CAS  PubMed  Article  Google Scholar 

  115. Schmidt MWI, Torn MS, Abiven S et al (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56

    CAS  PubMed  Article  Google Scholar 

  116. Schmutz J, Cannon SB, Schlueter J et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    CAS  PubMed  Article  Google Scholar 

  117. Shahzad T, Chenu C, Genet P et al (2015) Contribution of exudates, arbuscular mycorrhizal fungi and litter depositions to the rhizosphere priming effect induced by grassland species. Soil Biol Biochem 80:146–155

    CAS  Article  Google Scholar 

  118. Simpson MJ, Simpson AJ (2017) NMR of soil organic matter. Encyclopedia of Spectroscopy and Spectrometry (3rd edn). Elsevier, Amsterdam, pp 170–174

    Google Scholar 

  119. Singh BK, Munro S, Potts JM et al (2007) Influence of grass species and soil type on rhizosphere microbial community structure in grassland soils. Appl Soil Ecol 36:147–155

    Article  Google Scholar 

  120. Sinnathamby S, Douglas-Mankin KR, Craige C (2017) Field-scale calibration of crop-yield parameters in the soil and waterassessment tool (SWAT). Agric Water Manag 180:61–69

    Article  Google Scholar 

  121. Siqueira AF, Ormeno-Orillo E, Souza RC et al (2014) Comparative genomics of Bradyrhizobium japonicum CPAC 15 and Bradyrhizobium diazoefficiens CPAC 7: elite model strains for understanding symbiotic performance with soybean. BMC Genom 15:420

    Article  CAS  Google Scholar 

  122. Smalla K, Wieland G, Buchner A et al (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  123. Stougaard J (2000) Regulators and regulation of legume root nodule development. Plant Physiol 124:531–540

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  124. Sun HY, Deng SP, Raun WR (2004) Bacterial community structure and diversity in a century-old manuretreated agroecosystem. Appl Environ Microbiol 70:5868–5874

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  125. Sylvia D, Fuhrmann J, Hartel P et al (2005) Principles and applications of soil microbiology. Pearson, New Jersey

    Google Scholar 

  126. Tan Z, Hurek T, Vinuesa P et al (2001) Specific detection of Bradyrhizobium and Rhizobium strains colonizing rice (Oryza sativa) roots by 16S-23S ribosomal DNA intergenic spacer-targeted PCR. Appl Environ Microbiol 67:3655–3664

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  127. Tilman D, Cassman KG, Matson PA et al (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  129. Uzokwe VNE, Asafo-Adjei B, Fawole I et al (2017) Generation mean analysis of phosphorus-use efficiency in freely nodulating soybean crosses grown in low-phosphorus soil. Plant Breeding 136:139–146

    CAS  Article  Google Scholar 

  130. van Overbeek LS, Saikkonen K (2016) Impact of bacterial–fungal interactions on the colonization of the endosphere. Trends Plant Sci 21:230–242

    PubMed  Article  CAS  Google Scholar 

  131. van der Wal A, de Boer W (2017) Dinner in the dark: illuminating drivers of soil organic matter decomposition. Soil Biol Biochem 105:45–48

    Article  CAS  Google Scholar 

  132. van der Heijden MGA, Wiemken A, Sanders IR (2003) Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plants. New Phytol 157:569–578

    Article  Google Scholar 

  133. Vijayakumar V, Liebisch G, Buer B et al (2016) Integrated multi-omics analysis supports role of lysophosphatidylcholine and related glycerophospholipids in the Lotus japonicusGlomus intraradices mycorrhizal symbiosis. Plant Cell Environ 39:393–315

    CAS  PubMed  Article  Google Scholar 

  134. Vogelsang KM, Reynolds HL, Bever JD (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 172:554–562

    PubMed  Article  Google Scholar 

  135. Wang X, Pan Q, Chen F et al (2011) Effects of co-inoculation with arbuscular mycorrhizal fungi and rhizobia on soybean growth as related to root architecture and availability of N and P. Mycorrhiza 21:173–181,

    PubMed  Article  CAS  Google Scholar 

  136. Wang X, Khodadadi E, Fakheri B et al (2017) Organ-specific proteomics of soybean seedlings under flooding and drought stresses. J Proteom 162:62–72

    CAS  Article  Google Scholar 

  137. Willis A, Rodrigues BF, Harris PJC (2013) The ecology of arbuscular mycorrhizal fungi. CRC Crit Rev Plant Sci 32:1–20

    Article  Google Scholar 

  138. Wittwer RA, Dorn B, Jossi W et al (2017) Cover crops support ecological intensification of arable cropping systems. Sci Rep 7:41911

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  139. Xue L, Cui H, Buer B et al (2015) Network of GRAS transcription factors involved in the control of arbuscule development in Lotus japonicus. Plant Physiol 167:854–871

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  140. Young JWP (2015) Genome diversity in arbuscular mycorrhizal fungi. Curr Opin Plant Biol 26:113–119

    CAS  PubMed  Article  Google Scholar 

  141. Young ND, Bharti AK (2012) Genome-enabled insights into legume biology. Annu Rev Plant Biol 63:283–305

    CAS  PubMed  Article  Google Scholar 

  142. Zgadzaj R, Garrido-Oter R, Jensen DB et al (2016) Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities. Proc Natl Acad Sci USA 113:E7996–E8005

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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Acknowledgements

We gratefully acknowledge Prof. Rattan Lal, School of Environment and Natural Resources, The Ohio State University for helpful discussions, suggestions and critical reading of the manuscript. We thank Dr. Veena Devi Ganeshan, Department of Plant Pathology, The Ohio State University for help in conceptualizing the figure on soybean rhizosphere.

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Correspondence to Ram Swaroop Meena or Vinod Vijayakumar.

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Meena, R.S., Vijayakumar, V., Yadav, G.S. et al. Response and interaction of Bradyrhizobium japonicum and arbuscular mycorrhizal fungi in the soybean rhizosphere. Plant Growth Regul 84, 207–223 (2018). https://doi.org/10.1007/s10725-017-0334-8

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Keywords

  • Biofertilizer
  • Biotic and abiotic interactors
  • Co-inoculation
  • Environmental factors
  • Rhizosphere
  • Soybean productivity
  • Symbiotic interactions