Advertisement

Exploiting rhizosphere microbial cooperation for developing sustainable agriculture strategies

  • Yoann Besset-Manzoni
  • Laura Rieusset
  • Pierre Joly
  • Gilles Comte
  • Claire Prigent-Combaret
Chemistry, Activity and Impact of Plant Biocontrol products

Abstract

The rhizosphere hosts a considerable microbial community. Among that community, bacteria called plant growth-promoting rhizobacteria (PGPR) can promote plant growth and defense against diseases using diverse distinct plant-beneficial functions. Crop inoculation with PGPR could allow to reduce the use of pesticides and fertilizers in agrosystems. However, microbial crop protection and growth stimulation would be more efficient if cooperation between rhizosphere bacterial populations was taken into account when developing biocontrol agents and biostimulants. Rhizospheric bacteria live in multi-species biofilms formed all along the root surface or sometimes inside the plants (i.e., endophyte). PGPR cooperate with their host plants and also with other microbial populations inside biofilms. These interactions are mediated by a large diversity of microbial metabolites and physical signals that trigger cell–cell communication and appropriate responses. A better understanding of bacterial behavior and microbial cooperation in the rhizosphere could allow for a more successful use of bacteria in sustainable agriculture. This review presents an ecological view of microbial cooperation in agrosystems and lays the emphasis on the main microbial metabolites involved in microbial cooperation, plant health protection, and plant growth stimulation. Eco-friendly inoculant consortia that will foster microbe–microbe and microbe–plant cooperation can be developed to promote crop growth and restore biodiversity and functions lost in agrosystems.

Keywords

Rhizosphere Microbial cooperation Microbial consortium Microbial metabolites Biocontrol Sustainable agriculture Cell–cell communication Quorum sensing 

Notes

Acknowledgements

Yoann Besset-Manzoni was supported by a CIFRE Ph.D grant from the Association Nationale de la Recherche et de la Technologie. Laura Rieusset received a Ph.D fellowship from the French Ministère de l’Enseignement Supérieur et de la Recherche. We thank A. Buchwalter for English proofreading of this paper. This study was supported by the SymbioMaize ANR project (ANR-12-JSV7-0014-01).

Author contribution

Yoann Besset-Manzoni and Laura Rieusset equally contributed to this work as first co-authors. Laura Rieusset designed the figures and tables. All authors participated in writing the manuscript and approved the final version.

References

  1. Alavi P, Müller H, Cardinale M, Zachow C, Sánchez MB, Martínez JL, Berg G (2013) The DSF quorum sensing system controls the positive influence of Stenotrophomonas maltophilia on plants. PLoS One 8(7):e67103CrossRefGoogle Scholar
  2. Allocati N, Masulli M, Di Ilio C, De Laurenzi V (2015) Die for the community: an overview of programmed cell death in bacteria. Cell Death Dis 6:e1609CrossRefGoogle Scholar
  3. Audrain B, Farag MA, Ryu CM, Ghigo JM (2015) Role of bacterial volatile compounds in bacterial biology. FEMS Microbiol Rev 39(2):222–233.  https://doi.org/10.1093/femsre/fuu013CrossRefGoogle Scholar
  4. Bailly A, Groenhagen U, Schulz S, Geisler M, Eberl L, Weisskopf L (2014) The inter-kingdom volatile signal indole promotes root development by interfering with auxin signalling. Plant J 80(5):758–771.  https://doi.org/10.1111/tpj.12666CrossRefGoogle Scholar
  5. Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134(1):307–319.  https://doi.org/10.1104/pp.103.028712CrossRefGoogle Scholar
  6. Barbey C, Crépin A, Bergeau D, Ouchiha A, Mijouin L, Taupin L, Orange N, Feuilloley M, Dufour A, Burini JF, Latour X (2013) In planta biocontrol of Pectobacterium atrosepticum by Rhodococcus erythropolis involves silencing of pathogen communication by the rhodococcal gamma-lactone catabolic pathway. PLoS One 8(6):e66642.  https://doi.org/10.1371/journal.pone.0066642CrossRefGoogle Scholar
  7. Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515(7528):505–511CrossRefGoogle Scholar
  8. Barra PJ, Inostroza NG, Acuña JJ, Mora ML, Crowley DE, Jorquera MA (2016) Formulation of bacterial consortia from avocado (Persea americana Mill.) and their effect on growth, biomass and superoxide dismutase activity of wheat seedlings under salt stress. Appl Soil Ecol 102:80–91CrossRefGoogle Scholar
  9. Barraud N, Storey MV, Moore ZP, Webb JS, Rice SA, Kjelleberg S (2009) Nitric oxide-mediated dispersal in single- and multi-species biofilms of clinically and industrially relevant microorganisms. Microb Biotechnol 2(3):370–378.  https://doi.org/10.1111/j.1751-7915.2009.00098.xCrossRefGoogle Scholar
  10. Barrios E (2007) Soil biota, ecosystem services and land productivity. Ecol Econ 64(2):269–285.  https://doi.org/10.1016/j.ecolecon.2007.03.004CrossRefGoogle Scholar
  11. Belimov AA, Kojemiakov AP, Chuvarliyeva CV (1995) Interaction between barley and mixed cultures of nitrogen fixing and phosphate-solubilizing bacteria. Plant Soil 173(1):29–37CrossRefGoogle Scholar
  12. Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17(8):478–486.  https://doi.org/10.1016/j.tplants.2012.04.001CrossRefGoogle Scholar
  13. Berg G, Grube M, Schloter M, Smalla K (2014) Unraveling the plant microbiome: looking back and future perspectives. Front Microbiol 5:148Google Scholar
  14. Berry C, Fernando WGD, Loewen PC, de Kievit TR (2010) Lipopeptides are essential for Pseudomonas sp. DF41 biocontrol of Sclerotinia sclerotiorum. Biol Control 55(3):211–218.  https://doi.org/10.1016/j.biocontrol.2010.09.011CrossRefGoogle Scholar
  15. Bianchi FJJA, Booij CJH, Tscharntke T (2006) Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Pro R Soc Lond B Biol Sci 273(1595):1715–1727.  https://doi.org/10.1098/rspb.2006.3530CrossRefGoogle Scholar
  16. Blom D, Fabbri C, Connor EC, Schiestl FP, Klauser DR, Boller T, Weisskopf L (2011) Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ Microbiol 13(11):3047–3058CrossRefGoogle Scholar
  17. Bottini R, Cassán F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65(5):497–503CrossRefGoogle Scholar
  18. Brameyer S, Kresovic D, Bode HB, Heermann R (2015) Dialkylresorcinols as bacterial signaling molecules. Proc Nat Acad Sci 112(2):572–577.  https://doi.org/10.1073/pnas.1417685112CrossRefGoogle Scholar
  19. Brazelton JN, Pfeufer EE, Sweat TA, Gardener BBM, Coenen C (2008) 2,4-Diacetylphloroglucinol alters plant root development. Mol Plant-Microbe Interact 21(10):1349–1358CrossRefGoogle Scholar
  20. Brenner K, You L, Arnold FH (2008) Engineering microbial consortia: a new frontier in synthetic biology. Trends Biotechnol 26(9):483–489CrossRefGoogle Scholar
  21. Burdman S, Okon Y, Jurkevitch E (2000) Surface characteristics of Azospirillum brasilense in relation to cell aggregation and attachment to plant roots. Crit Rev Microbiol 26(2):91–110.  https://doi.org/10.1080/10408410091154200CrossRefGoogle Scholar
  22. Calvo P, Nelson L, Kloepper JW (2014) Agricultural uses of plant biostimulants. Plant Soil 383(1–2):3–41CrossRefGoogle Scholar
  23. Cardinale BJ, Harvey CT, Gross K, Ives AR (2003) Biodiversity and biocontrol: emergent impacts of a multi-enemy assemblage on pest suppression and crop yield in an agroecosystem. Ecol Lett 6(9):857–865CrossRefGoogle Scholar
  24. Chaucheyras-Durand F, Durand H (2010) Probiotics in animal nutrition and health. Benef Microbes 1(1):3–9.  https://doi.org/10.3920/BM2008.1002CrossRefGoogle Scholar
  25. Chin-A-Woeng T, Bloemberg G, van der Bij A, van der Drift K, Schripsema J, Kroon B, Lugtenberg B (1998) Biocontrol by phenazine-1-carboxamide-producing Pseudomonas chlororaphis PCL1391 of tomato root rot caused by Fusarium oxysporum f. sp. radicis-lycopersici. Mol Plant-Microbe Interact 11(11):1069–1077.  https://doi.org/10.1094/MPMI.1998.11.11.1069CrossRefGoogle Scholar
  26. Chin-A-Woeng TF, Bloemberg GV, Mulders IH, Dekkers LC, Lugtenberg BJ (2000) Root colonization by phenazine-1-carboxamide-producing bacterium Pseudomonas chlororaphis PCL1391 is essential for biocontrol of tomato foot and root rot. Mol Plant-Microbe Interact 13(12):1340–1345CrossRefGoogle Scholar
  27. Cirou A, Diallo S, Kurt C, Latour X, Faure D (2007) Growth promotion of quorum-quenching bacteria in the rhizosphere of Solanum tuberosum. Environ Microbiol 9(6):1511–1522.  https://doi.org/10.1111/j.1462-2920.2007.01270.xCrossRefGoogle Scholar
  28. Combes-Meynet E, Pothier JF, Moënne-Loccoz Y, Prigent-Combaret C (2011) The Pseudomonas secondary metabolite 2,4-diacetylphloroglucinol is a signal inducing rhizoplane expression of Azospirillum genes involved in plant-growth promotion. Mol Plant-Microbe Interact 24(2):271–284.  https://doi.org/10.1094/MPMI-07-10-0148CrossRefGoogle Scholar
  29. Cordovez V, Carrion VJ, Etalo DW, Mumm R, Zhu H, van Wezel GP, Raaijmakers JM (2015) Diversity and functions of volatile organic compounds produced by Streptomyces from a disease-suppressive soil. Front Microbiol 6:1–13CrossRefGoogle Scholar
  30. Costa E, Pérez J, Kreft J-U (2006) Why is metabolic labour divided in nitrification? Trends Microbiol 14(5):213–219.  https://doi.org/10.1016/j.tim.2006.03.006CrossRefGoogle Scholar
  31. Couillerot O, Prigent-Combaret C, Caballero-Mellado J, Moënne-Loccoz Y (2009) Pseudomonas fluorescens and closely-related fluorescent pseudomonads as biocontrol agents of soil-borne phytopathogens. Lett Appl Microbiol 48(5):505–512.  https://doi.org/10.1111/j.1472-765X.2009.02566.xCrossRefGoogle Scholar
  32. Couillerot O, Combes-Meynet E, Pothier JF, Bellvert F, Challita E, Poirier M-A, Rohr R, Comte G, Moënne-Loccoz Y, Prigent-Combaret C (2011) Role of the antimicrobial compound 2,4-diacetylphloroglucinol in the impact of biocontrol Pseudomonas fluorescens F113 on Azospirillum brasilense phytostimulators. Microbiol 157(6):1694–1705.  https://doi.org/10.1099/mic.0.043943-0CrossRefGoogle Scholar
  33. Cox TJ (2014). The acoustic emissions produced by Escherichia coli during the growth cycle. Theses and Dissertations - Animal and Food Sciences. 33. University of Kentucky. https://uknowledge.uky.edu/animalsci_etds/33
  34. Crespi BJ (2001) The evolution of social behavior in microorganisms. Trends Ecol Evol 16(4):178–183.  https://doi.org/10.1016/S0169-5347(01)02115-2CrossRefGoogle Scholar
  35. Crowder DW, Jabbour R (2014) Relationships between biodiversity and biological control in agroecosystems: current status and future challenges. Biol Control 75:8–17CrossRefGoogle Scholar
  36. Damore JA, Gore J (2012) Understanding microbial cooperation. J Theor Biol 299:31–41.  https://doi.org/10.1016/j.jtbi.2011.03.008CrossRefGoogle Scholar
  37. De Bruijn I, De Kock MJD, Yang M, De Waard P, Van Beek TA, Raaijmakers JM (2007) Genome-based discovery, structure prediction and functional analysis of cyclic lipopeptide antibiotics in Pseudomonas species. Mol Microbiol 63(2):417–428.  https://doi.org/10.1111/j.1365-2958.2006.05525.xCrossRefGoogle Scholar
  38. De Bruijn I, De Kock MJD, De Waard P, Van Beek TA, Raaijmakers JM (2008) Massetolide A biosynthesis in Pseudomonas fluorescens. J Bacteriol 190(8):2777–2789.  https://doi.org/10.1128/JB.01563-07CrossRefGoogle Scholar
  39. de Werra P, Huser A, Tabacchi R, Keel C, Maurhofer M (2011) Plant-and microbe-derived compounds affect the expression of genes encoding antifungal compounds in a pseudomonad with biocontrol activity. Appl Environ Microbiol 77(8):2807–2812.  https://doi.org/10.1128/AEM.01760-10
  40. Debois D, Hamze K, Guérineau V, Le Caër JP, Holland IB, Lopes P, Laprévote O (2008) In situ localisation and quantification of surfactins in a Bacillus subtilis swarming community by imaging mass spectrometry. Proteomics 8(18):3682–3691CrossRefGoogle Scholar
  41. Delaplace P, Delory BM, Baudson C, Mendaluk-Saunier de Cazenave M, Spaepen S, Varin S, Brostaux Y, du Jardin P (2015) Influence of rhizobacterial volatiles on the root system architecture and the production and allocation of biomass in the model grass Brachypodium distachyon (L.) P. Beauv. BMC Plant Biol 15(1):195CrossRefGoogle Scholar
  42. Denison RF (2000) Legume sanctions and the evolution of symbiotic cooperation by Rhizobia. Am Nat 156(6):567–576.  https://doi.org/10.1086/316994CrossRefGoogle Scholar
  43. Dessaux Y, Grandclément C, Faure D (2016) Engineering the rhizosphere. Trends Plant Sci 21(3):266–278CrossRefGoogle Scholar
  44. Deveau A, Labbé J (2016) Mycorrhiza helper bacteria. In: Martin F (ed) Molecular mycorrhizal symbiosis. John Wiley and Sons, Hoboken, New Jersey, USA, pp 437–450.  https://doi.org/10.1002/9781118951446.ch24CrossRefGoogle Scholar
  45. Di Palma AA, Pereyra CM, Moreno Ramirez L, Xiqui Vázquez ML, Baca BE, Pereyra MA, Lamattina L, Creus CM (2013) Denitrification-derived nitric oxide modulates biofilm formation in Azospirillum brasilense. FEMS Microbiol Lett 338(1):77–85CrossRefGoogle Scholar
  46. Dodd IC, Zinovkina NY, Safronova VI, Belimov AA (2010) Rhizobacterial mediation of plant hormone status. Ann Appl Biol 157(3):361–379CrossRefGoogle Scholar
  47. Dong YH, Wang LH, JL X, Zhang HB, Zhang XF, Zhang LH (2001) Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411(6839):813–817.  https://doi.org/10.1038/35081101CrossRefGoogle Scholar
  48. Drogue B, Sanguin H, Borland S, Prigent-Combaret C, Wisniewski-Dyé F (2014) Genome wide profiling of Azospirillum lipoferum 4B gene expression during interaction with rice roots. FEMS Microbiol Ecol 87(2):543–555.  https://doi.org/10.1111/1574-6941.12244CrossRefGoogle Scholar
  49. Dubey GP, Ben-Yehuda S (2011) Intercellular nanotubes mediate bacterial communication. Cell 144(4):590–600.  https://doi.org/10.1016/j.cell.2011.01.015CrossRefGoogle Scholar
  50. du Jardin P (2012) The science of plant biostimulants - a bibliographic analysis, Ad hoc study report. European Commission, Brussels, p 37Google Scholar
  51. Durner J, Klessig DF (1999) Nitric oxide as a signal in plants. Curr Opin Plant Biol 2(5):369–374CrossRefGoogle Scholar
  52. Egamberdieva D (2013) The role of phytohormone producing bacteria in alleviating salt stress in crop plants. In: Miransari M (ed) Stress and Plant Biotechnology. Studium Press LLC, Houston, pp 21–39Google Scholar
  53. Elias S, Banin E (2012) Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev 36(5):990–1004.  https://doi.org/10.1111/j.1574-6976.2012.00325.xCrossRefGoogle Scholar
  54. Faure D, Vereecke D, Leveau JHJ (2009) Molecular communication in the rhizosphere. Plant Soil 321(1–2):279–303CrossRefGoogle Scholar
  55. Finlay RD, Clemmensen KE (2017) Chapter 23—immobilization of carbon in mycorrhizal mycelial biomass and secretions. In: Johnson NC, Gehring C, Jansa J (eds) Mycorrhizal mediation of soil: fertility, structure, and carbon storage. Elsevier, Amsterdam, pp 413–440Google Scholar
  56. Flemming HC, Neu TR, Wozniak DJ (2007) The EPS matrix: the “house of biofilm cells”. J Bacteriol 189(22):7945–7947.  https://doi.org/10.1128/JB.00858-07CrossRefGoogle Scholar
  57. Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S (2016) Biofilms: an emergent form of bacterial life. Nat Rev Microbiol 14(9):563–575.  https://doi.org/10.1038/nrmicro.2016.94CrossRefGoogle Scholar
  58. Frey-Klett P, Burlinson P, Deveau A, Barret M, Tarkka M, Sarniguet A (2011) Bacterial-fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiol Mol Biol Rev 75(4):583–609CrossRefGoogle Scholar
  59. Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur J Plant Pathol 119(3):329–339.  https://doi.org/10.1007/s10658-007-9162-4CrossRefGoogle Scholar
  60. Grandclément C, Tannières M, Moréra S, Dessaux Y, Faure D (2016) Quorum quenching: role in nature and applied developments. FEMS Microbiol Rev 40(1):86–116.  https://doi.org/10.1093/femsre/fuv038CrossRefGoogle Scholar
  61. Haas D, Keel C (2003) Regulation of antibiotic production in root-colonizing Peudomonas spp. and relevance for biological control of plant disease. Annu Rev Phytopathol 41:117–153CrossRefGoogle Scholar
  62. Haichar FZ, Santaella C, Heulin T, Achouak W (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80.  https://doi.org/10.1016/j.soilbio.2014.06.017CrossRefGoogle Scholar
  63. Hartmann A, Rothballer M (2017) Role of quorum sensing signals of rhizobacteria for plant growth promotion. In: Mehnaz S (ed) Rhizotrophs: plant growth promotion to bioremediation. Microorganisms for sustainability, 2nd edn. Springer, SingaporeGoogle Scholar
  64. Hidalgo-Romano B, Gollihar J, Brown SA, Whiteley M, Valenzuela E, Kaplan HB, McLean RJC (2014) Indole inhibition of N-acylated homoserine lactone-mediated quorum signalling is widespread in Gram-negative bacteria. Microbiol (United Kingdom) 160:2464–2473Google Scholar
  65. Hirakawa H, Tomita H (2013) Interference of bacterial cell-to-cell communication: a new concept of antimicrobial chemotherapy breaks antibiotic resistance. Front Microbiol 4:114CrossRefGoogle Scholar
  66. Hogan DA, Vik Å, Kolter R (2004) A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol Microbiol 54(5):1212–1223CrossRefGoogle Scholar
  67. Humphries J, Xiong L, Liu J, Prindle A, Yuan F, Arjes HA, Tsimring L, Süel GM (2017) Species-independent attraction to biofilms through electrical signaling. Cell 168(1-2):200–209.  https://doi.org/10.1016/j.cell.2016.12.014CrossRefGoogle Scholar
  68. Jacobsen CS, Hjelmsø MH (2014) Agricultural soils, pesticides and microbial diversity. Curr Opin Biotechnol 27:15–20.  https://doi.org/10.1016/j.copbio.2013.09.003CrossRefGoogle Scholar
  69. Jakobi M, Winkelmann G, Kaiser D, Kempler C, Jung G, Berg G, Bahl H (1996) Maltophilin: a new antifungal compound produced by Stenotrophomonas maltophilia R3089. J Antibiotics 49(11):1101–1104CrossRefGoogle Scholar
  70. Johnsen K, Jacobsen CS, Torsvik V, Sørensen J (2001) Pesticide effects on bacterial diversity in agricultural soils—a review. Biol Fertil Soil 33(6):443–453.  https://doi.org/10.1007/s003740100351CrossRefGoogle Scholar
  71. Jousset A, Bonkowski M (2010) The model predator Acanthamoeba castellanii induces the production of 2,4, DAPG by the biocontrol strain Pseudomonas fluorescens Q2-87. Soil Biol Biochem 42(9):1647–1649.  https://doi.org/10.1016/j.soilbio.2010.05.018CrossRefGoogle Scholar
  72. Jousset A, Rochat L, Scheu S, Bonkowski M, Keel C (2010) Predator-prey chemical warfare determines the expression of biocontrol genes by rhizosphere-associated Pseudomonas fluorescens. App Environ Microbiol 76(15):5263–5268CrossRefGoogle Scholar
  73. Kaiser C, Kilburn MR, Clode PL, Fuchslueger L, Koranda M, Cliff JB, Solaiman ZM, Murphy DV (2015) Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytol 205(4):1537–1551.  https://doi.org/10.1111/nph.13138CrossRefGoogle Scholar
  74. Kennedy TA, Naeem S, Howe KM, Knops JMH, Tilman D, Reich P (2002) Biodiversity as a barrier to ecological invasion. Nature 417(6889):636–638.  https://doi.org/10.1038/nature00776CrossRefGoogle Scholar
  75. Keohane CE, Steele AD, Wuest WM (2015) The rhizosphere microbiome: a playground for natural product chemists. Synlett 26(20):2739–2744CrossRefGoogle Scholar
  76. Kiers ET, Rousseau RA, West SA, Denison RF (2003) Host sanctions and the legume–rhizobium mutualism. Nature 425:78–81CrossRefGoogle Scholar
  77. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bucking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333(6044):880–882.  https://doi.org/10.1126/science.1208473CrossRefGoogle Scholar
  78. Kim K, Yim W, Trivedi P, Madhaiyan M, Boruah HPD, Islam MR, Lee G, Sa T (2010) Synergistic effects of inoculating arbuscular mycorrhizal fungi and Methylobacterium oryzae strains on growth and nutrient uptake of red pepper (Capsicum annuum L.) Plant Soil 327(1–2):429–440.  https://doi.org/10.1007/s11104-009-0072-4CrossRefGoogle Scholar
  79. Kreft JU (2004) Biofilms promote altruism. Microbiology 150(8):2751–2760.  https://doi.org/10.1099/mic.0.26829-0CrossRefGoogle Scholar
  80. Kuiper I, Lagendijk EL, Pickford R, Derrick JP, Lamers GEM, Thomas-Oates JE, Bloemberg GV (2004) Characterization of two Pseudomonas putida lipopeptide biosurfactants, putisolvin I and II, which inhibit biofilm formation and break down existing biofilms. Mol Microbiol 51(1):97–113CrossRefGoogle Scholar
  81. Kumar H, Dubey RC, Maheshwari DK (2011) Effect of plant growth promoting rhizobia on seed germination, growth promotion and suppression of Fusarium wilt of fenugreek (Trigonella foenum-graecum L.) Crop Prot 30(11):1396–1403CrossRefGoogle Scholar
  82. Lambrecht M, Okon Y, Broek AV, Vanderleyden J (2000) Indole-3-acetic acid: a reciprocal signalling molecule in bacteria–plant interactions. Trends Microbiol 8(7):298–300CrossRefGoogle Scholar
  83. Lareen A, Burton F, Schäfer P (2016) Plant root–microbe communication in shaping root microbiomes. Plant Mol Biol 90(6):575–587.  https://doi.org/10.1007/s11103-015-0417-8CrossRefGoogle Scholar
  84. Larsen J, Cornejo P, Barea JM (2009) Interactions between the arbuscular mycorrhizal fungus Glomus intraradices and the plant growth promoting rhizobacteria Paenibacillus polymyxa and P. macerans in the mycorrhizosphere of Cucumis sativus. Soil Biol Biochem 41(2):286–292.  https://doi.org/10.1016/j.soilbio.2008.10.029CrossRefGoogle Scholar
  85. LaSarre B, Federle MJ (2013) Exploiting Quorum Sensing to confuse bacterial pathogens. Microbiol Mol Biol Rev 77(1):73–111Google Scholar
  86. Le Mire G, Luan Nguyen M, Fassotte B, du Jardin P, Verheggen F, Delaplace P, Haissam Jijakli M (2016) Implementing plant biostimulants and biocontrol strategies in the agroecological management of cultivated ecosystems. A review. Biotechnol Agron Soc Environ 20(S1):299–313Google Scholar
  87. Lee JH, Lee J (2010) Indole as an intercellular signal in microbial communities. FEMS Microbiol Rev 34(4):426–444.  https://doi.org/10.1111/j.1574-6976.2009.00204.xCrossRefGoogle Scholar
  88. Lee JH, Wood TK, Lee J (2015) Roles of indole as an interspecies and interkingdom signaling molecule. Trends Microbiol 23(11):707–718CrossRefGoogle Scholar
  89. Leimar O, Hammerstein P (2010) Cooperation for direct fitness benefits. Philos Trans R Soc B Biol Sci 365(1553):2619–2626CrossRefGoogle Scholar
  90. Liao J, Huang H, Meusnier I, Adreit H, Ducasse A, Bonnot F, Pan L, He X, Kroj T, Fournier E, Tharreau D, Gladieux P, Morel J-B (2016) Pathogen effectors and plant immunity determine specialization of the blast fungus to rice subspecies. elife 5:e19377CrossRefGoogle Scholar
  91. Lucas JA, Ramos Solano B, Montes F, Ojeda J, Megias M, Gutierrez Mañero FJ (2009) Use of two PGPR strains in the integrated management of blast disease in rice (Oryza sativa) in Southern Spain. Field Crops Res 114(3):404–410CrossRefGoogle Scholar
  92. Maddula VSRK, Pierson EA, Pierson LS (2008) Altering the ratio of phenazines in Pseudomonas chlororaphis (aureofaciens) strain 30-84: effects on biofilm formation and pathogen inhibition. J Bacteriol 190(8):2759–2766CrossRefGoogle Scholar
  93. Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anolles G, Rolfe BG, Bauer WD (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Nat Acad Scie USA 100(3):1444–1449.  https://doi.org/10.1073/pnas.262672599CrossRefGoogle Scholar
  94. Matsuhashi M, Pankrushina AN, Takeuchi S, Ohshima H, Miyoi H, Endoh K, Murayama K, Watanabe H, Endo S, Tobi M, Mano Y, Hyodo M, Kobayashi T, Kaneko T, Otani S, Yoshimura S, Harata A, Sawada T (1998) Production of sound waves by bacterial cells and the response of bacterial cells to sound. J Gen Appl Microbiol 44(1):49–55.  https://doi.org/10.2323/jgam.44.49CrossRefGoogle Scholar
  95. Mavrodi DV, Blankenfeldt W, Thomashow LS (2006) Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annu Rev Phytopathol 44:417–445CrossRefGoogle Scholar
  96. Morris JJ, Lenski RE, Zinser ER (2012) The black queen hypothesis: evolution of dependencies through adaptive gene loss. MBio 3(2):e00036–e00012CrossRefGoogle Scholar
  97. Nadeem SM, Naveed M, Zahir ZA, Asghar HN (2013) Plant–microbe interactions for sustainable agriculture: fundamentals and recent advances. In: Arora NK (ed) Plant microbe symbiosis: fundamentals and advances. Springer India, New Delhi, pp 51–103.  https://doi.org/10.1007/978-81-322-1287-4_2CrossRefGoogle Scholar
  98. Nadell CD, Drescher K, Foster KR (2016) Spatial structure, cooperation and competition in biofilms. Nat Rev Microbiol 14(9):589–600CrossRefGoogle Scholar
  99. Nakamura Y, Yamamoto N, Kino Y, Yamamoto N, Kamei S, Mori H, Kurokawa K, Nakashima N (2016) Establishment of a multi-species biofilm model and metatranscriptomic analysis of biofilm and planktonic cell communities. Appl Microbiol Biotechnol 100(16):7263–7279.  https://doi.org/10.1007/s00253-016-7532-6CrossRefGoogle Scholar
  100. Nettles R, Watkins J, Ricks K, Boyer M, Licht M, Atwood LW, Peoples M, Smith RG, Mortensen DA, Koide RT (2016) Influence of pesticide seed treatments on rhizosphere fungal and bacterial communities and leaf fungal endophyte communities in maize and soybean. Appl Soil Ecol 102:61–69.  https://doi.org/10.1016/j.apsoil.2016.02.008CrossRefGoogle Scholar
  101. Norris V, Hyland GJ (1997) Do bacteria sing? Sonic intercellular communication between bacteria may reflect electromagnetic intracellular communication involving coherent collective vibrational modes that could integrate enzyme activities and gene expression. Mol Microbiol 24(4):879–880.  https://doi.org/10.1046/j.1365-2958.1997.3951756.xCrossRefGoogle Scholar
  102. Nowak MA (2006) Five rules for the evolution of cooperation. Science 314(5805):1560–1563CrossRefGoogle Scholar
  103. Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16(3):115–125.  https://doi.org/10.1016/j.tim.2007.12.009CrossRefGoogle Scholar
  104. Ortíz-castro R, Martínez-trujillo M, López-bucio J (2008) N-acyl-l-homoserine lactones: a class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. Plant Cell Environ 31(10):1497–1509.  https://doi.org/10.1111/j.1365-3040.2008.01863.xCrossRefGoogle Scholar
  105. Pérez-Montaño F, Alías-Villegas C, Bellogín RA, del Cerro P, Espuny MR, Jiménez-Guerrero I, López-Baena FJ, Ollero FJ, Cubo T (2014) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Res 169(5–6):325–336CrossRefGoogle Scholar
  106. Phelan VV, Liu W-T, Pogliano K, Dorrestein PC (2012) Microbial metabolic exchange—the chemotype-to-phenotype link. Nature Chem Biol 8(1):26–35.  https://doi.org/10.1038/nchembio.739CrossRefGoogle Scholar
  107. Pierson LS (2000) Expanding the club: engineering plants to talk to bacteria. Trends Plant Sci 5(3):89–91Google Scholar
  108. Price-Whelan A, Dietrich LEP, Newman DK (2006) Rethinking “secondary” metabolism: physiological roles for phenazine antibiotics. Nature Chem Biol 2(2):71–78CrossRefGoogle Scholar
  109. Prigent-Combaret C, Vidal O, Dorel C, Lejeune P (1999) Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J Bacteriol 181(19):5993–6002Google Scholar
  110. Prigent-Combaret C, Prensier G, Le Thi TT, Vidal O, Lejeune P, Dorel C (2000) Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. Environ Microbiol 2(4):450–464.  https://doi.org/10.1046/j.1462-2920.2000.00128.xCrossRefGoogle Scholar
  111. Prigent-Combaret C, Zghidi-Abouzid O, Effantin G, Lejeune P, Reverchon S, Nasser W (2012) The nucleoid-associated protein Fis directly modulates the synthesis of cellulose, an essential component of pellicle-biofilms in the phytopathogenic bacterium Dickeya dadantii. Mol Microbiol 86(1):172–186.  https://doi.org/10.1111/j.1365-2958.2012.08182.xCrossRefGoogle Scholar
  112. Prindle A, Liu J, Asally M, Ly S, Garcia-Ojalvo J, Süel GM (2015) Ion channels enable electrical communication in bacterial communities. Nature 527(7576):59–63.  https://doi.org/10.1038/nature15709CrossRefGoogle Scholar
  113. Raaijmakers JM, Mazzola M (2012) Diversity and natural functions of antibiotics produced by beneficial and plant pathogenic bacteria. Annu Rev Phytopathol 50:403–424CrossRefGoogle Scholar
  114. Raaijmakers JM, de Bruijn I, de Kock MJD (2006) Cyclic lipopeptide production by plant-associated Pseudomonas spp.: diversity, activity, biosynthesis, and regulation. Mol Plant-Microbe Interact 19(7):699–710.  https://doi.org/10.1094/MPMI-19-0699CrossRefGoogle Scholar
  115. Raaijmakers JM, de Bruijn I, Nybroe O, Ongena M (2010) Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev 34(6):1037–1062.  https://doi.org/10.1111/j.1574-6976.2010.00221.xCrossRefGoogle Scholar
  116. Ratnieks F, Wenseleers T (2008) Altruism in insect societies and beyond: voluntary or enforced? Trends Ecol Evol 23(1):45–52.  https://doi.org/10.1016/j.tree.2007.09.013CrossRefGoogle Scholar
  117. Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435(7045):1098–1101CrossRefGoogle Scholar
  118. Reyes-Pérez A, María del Carmen Vargas M, Hernández M, Aguirre-von-Wobeser E, Pérez-Rueda E, Encarnacion S (2016) Transcriptomic analysis of the process of biofilm formation in Rhizobium etli CFN42. Arch Microbiol 198(9):847–860.  https://doi.org/10.1007/s00203-016-1241-5CrossRefGoogle Scholar
  119. Riedlinger J, Schrey SD, Tarkka MT, Hampp R, Kapur M, Fiedler HP (2006) Auxofuran, a novel metabolite that stimulates the growth of fly agaric, is produced by the mycorrhiza helper bacterium Streptomyces strain AcH 505. Appl Environ Microbiol 72(5):3550–3557.  https://doi.org/10.1128/AEM.72.5.3550-3557.2006CrossRefGoogle Scholar
  120. Roongsawang N, Hase Ki, Haruki M, Imanaka T, Morikawa M, Kanaya S (2003) Cloning and characterization of the gene cluster encoding arthrofactin synthetase from Pseudomonas sp. MIS38. Chem Biol 10(9):869–880Google Scholar
  121. Rosenberg E, Zilber-Rosenberg I (2016) Microbes drive evolution of animals and plants: the hologenome concept. MBio 7(2):e01395CrossRefGoogle Scholar
  122. Rosier A, Bishnoi U, Lakshmanan V, Sherrier DJ, Bais HP (2016) A perspective on inter-kingdom signaling in plant-beneficial microbe interactions. Plant Mol Biol 90(6):537–548.  https://doi.org/10.1007/s11103-016-0433-3CrossRefGoogle Scholar
  123. Rudresh DL, Shivaprakash MK, Prasad RD (2005) Effect of combined application of Rhizobium, phosphate solubilizing bacterium and Trichoderma spp. on growth, nutrient uptake and yield of chickpea (Cicer aritenium L.) Appl Soil Ecol 28(2):139–146CrossRefGoogle Scholar
  124. Ryu C-M (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134(3):1017–1026CrossRefGoogle Scholar
  125. Ryu C-M, Farag M, Hu C-H, Reddy MS, Wei H-X, Paré PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Nat Acad Sci U S A 100(8):4927–4932.  https://doi.org/10.1073/pnas.0730845100CrossRefGoogle Scholar
  126. Ryu CM, Choi HK, Lee CH, Murphy JF, Lee JK, Kloepper JW (2013) Modulation of quorum sensing in acyl-homoserine lactone-producing or -degrading tobacco plants leads to alteration of induced systemic resistance elicited by the rhizobacterium Serratia marcescens 90–166. Plant Pathol J 29(2):182–192.  https://doi.org/10.5423/PPJ.SI.11.2012.0173CrossRefGoogle Scholar
  127. Sabra W, Dietz D, Tjahjasari D, Zeng A-P (2010) Biosystems analysis and engineering of microbial consortia for industrial biotechnology. Eng Life Sci 10(5):407–421.  https://doi.org/10.1002/elsc.201000111CrossRefGoogle Scholar
  128. Santoro AE (2016) The do-it-all nitrifier. Science 351(6271):342–343.  https://doi.org/10.1126/science.aad9839CrossRefGoogle Scholar
  129. Sarma BK, Yadav SK, Singh S, Singh HB (2015) Microbial consortium-mediated plant defense against phytopathogens: readdressing for enhancing efficacy. Soil Biol Biochem 87:25–33CrossRefGoogle Scholar
  130. Sarvaiya N, Kothari V (2015) Effect of audible sound in form of music on microbial growth and production of certain important metabolites. Microbiol 84(2):227–235.  https://doi.org/10.1134/S0026261715020125CrossRefGoogle Scholar
  131. Schmidt R, Cordovez V, de Boer W, Raaijmakers J, Garbeva P (2015) Volatile affairs in microbial interactions. ISME J 9(11):1–7CrossRefGoogle Scholar
  132. Schnider-Keel U, Seematter A, Maurhofer M, Blumer C, Duffy B, Gigot-Bonnefoy C, Keel C (2000) Autoinduction of 2,4-diacetylphloroglucinol biosynthesis in the biocontrol agent Pseudomonas fluorescens CHA0 and repression by the bacterial metabolites salicylate and pyoluteorin. J Bacteriol 182(5):1215–1225.  https://doi.org/10.1128/JB.182.5.1215-1225.2000CrossRefGoogle Scholar
  133. Schuhegger R, Ihring A, Gantner S, Bahnweg G, Knappe C, Vogg G, Hutzler P, Schmid M, Van Breusegem F, Eberl L, Hartmann A, Langebartels C (2006) Induction of systemic resistance in tomato by N-acyl-l-homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ 29(5):909–918CrossRefGoogle Scholar
  134. Sharma S, Gupta R, Dugar G, Srivastava AK (2012) Impact of application of biofertilizers on soil structure and resident microbial community structure and function. In: Maheshwari D (ed) Bacteria in agrobiology: plant probiotics. Springer, Berlin, Heidelberg, pp 65–77.  https://doi.org/10.1007/978-3-642-27515-9_4CrossRefGoogle Scholar
  135. Shong J, Jimenez Diaz MR, Collins CH (2012) Towards synthetic microbial consortia for bioprocessing. Curr Opin Biotechnol 23(5):798–802.  https://doi.org/10.1016/j.copbio.2012.02.001CrossRefGoogle Scholar
  136. Singh S, Kapoor KK (1999) Inoculation with phosphate-solubilizing microorganisms and a vesicular-arbuscular mycorrhizal fungus improves dry matter yield and nutrient uptake by wheat grown in a sandy soil. Biol Fertil Soil 28(2):139–144CrossRefGoogle Scholar
  137. Singh S, Gupta R, Sharma S (2015) Effects of chemical and biological pesticides on plant growth parameters and rhizospheric bacterial community structure in Vigna radiata. J Hazard Mater 291:102–110CrossRefGoogle Scholar
  138. Smith J (2001) The social evolution of bacterial pathogenesis. Proc R Soc Lond B Biol Sci 268(1462):61–69.  https://doi.org/10.1098/rspb.2000.1330CrossRefGoogle Scholar
  139. Smith RP (2011) Design principles and applications of engineered microbial consortia. Acta Hortic 905:63–69CrossRefGoogle Scholar
  140. Smyth EM, McCarthy J, Nevin R, Khan MR, Dow JM, O’Gara F, Doohan FM (2011) In vitro analyses are not reliable predictors of the plant growth promotion capability of bacteria; a Pseudomonas fluorescens strain that promotes the growth and yield of wheat. J Appl Microbiol 111(3):683–692CrossRefGoogle Scholar
  141. Solanki MK, Singh RK, Srivastava S, Kumar S, Kashyap PL, Srivastava AK (2015) Characterization of antagonistic-potential of two Bacillus strains and their biocontrol activity against Rhizoctonia solani in tomato. J Basic Microb 55(1):82–90.  https://doi.org/10.1002/jobm.201300528CrossRefGoogle Scholar
  142. Srinivasan K, Mathivanan N (2009) Biological control of sunflower necrosis virus disease with powder and liquid formulations of plant growth promoting microbial consortia under field conditions. Biol Control 51(3):395–402.  https://doi.org/10.1016/j.biocontrol.2009.07.013CrossRefGoogle Scholar
  143. Supaphol S, Panichsakpatana S, Trakulnaleamsai S, Tungkananuruk N, Roughjanajirapa P, O’Donnell AG (2006) The selection of mixed microbial inocula in environmental biotechnology: example using petroleum contaminated tropical soils. J Microbiol Meth 65(3):432–441CrossRefGoogle Scholar
  144. Tanouchi Y, Smith R, You L (2012) Engineering microbial systems to explore ecological and evolutionary dynamics. Curr Opin Biotechnol 23(5):791–797.  https://doi.org/10.1016/j.copbio.2012.01.006CrossRefGoogle Scholar
  145. Thomashow LS (2016) Induced systemic resistance: a delicate balance. Environ Microbiol Rep 8(5):560–563.  https://doi.org/10.1111/1758-2229.12474CrossRefGoogle Scholar
  146. Thomashow LS, Weller DM (1988) Role of a phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. tritici. J Bacteriol 170(8):3499–3508CrossRefGoogle Scholar
  147. Thomashow LS, Bonsall RF, Weller DM (1997) Antibiotic production by soil and rhizosphere microbes in situ. Man Environ Microbiol 509:1–24Google Scholar
  148. Thompson HM (1996) Interactions between pesticides; a review of reported effects and their implications for wildlife risk assessment. Ecotoxicol Lond Engl 5(2):59–81.  https://doi.org/10.1007/BF00119047CrossRefGoogle Scholar
  149. Tran H, Ficke A, Asiimwe T, Höfte M, Raaijmakers JM (2007) Role of the cyclic lipopeptide massetolide A in biological control of Phytophthora infestans and in colonization of tomato plants by Pseudomonas fluorescens. New Phytol 175(4):731–742.  https://doi.org/10.1111/j.1469-8137.2007.02138.xCrossRefGoogle Scholar
  150. Traxler MF, Kolter R (2015) Natural products in soil microbe interactions and evolution. Nat Prod Rep 32(7):956–970.  https://doi.org/10.1039/C5NP00013KCrossRefGoogle Scholar
  151. Vacheron J, Desbrosses G, Bouffaud ML, Touraine B, Moënne-Loccoz Y, Muller D, Legendre L, Wisniewski-Dyé F, Prigent-Combaret C (2013) Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4:356CrossRefGoogle Scholar
  152. Vacheron J, Renoud S, Muller D, Babalola OO, Prigent-Combaret C (2015) Alleviation of abiotic and biotic stresses in plants by Azospirillum. In: Cassan FD, Okon Y, Creus C (eds) Handbook for Azospirillum: technical issues and protocols. Springer, Berlin, Heidelberg, pp 333–365Google Scholar
  153. Vacheron J, Moënne-Loccoz Y, Dubost A, Gonçalves-Martins M, Muller D, Prigent-Combaret C (2016) Fluorescent Pseudomonas strains with only few plant-beneficial properties are favored in the maize rhizosphere. Front Plant Sci 7:1212CrossRefGoogle Scholar
  154. Van Der Heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11(3):296–310.  https://doi.org/10.1111/j.1461-0248.2007.01139.xCrossRefGoogle Scholar
  155. Venkataraman A, Rosenbaum MA, Werner JJ, Winans SC, Angenent LT (2014) Metabolite transfer with the fermentation product 2,3-butanediol enhances virulence by Pseudomonas aeruginosa. ISME J 8(6):1210–1220.  https://doi.org/10.1038/ismej.2013.232CrossRefGoogle Scholar
  156. Venturi V, Fuqua C (2013) Chemical signaling between plants and plant-pathogenic bacteria. Annu Rev Phytopathol 51(1):17–37.  https://doi.org/10.1146/annurev-phyto-082712-102239CrossRefGoogle Scholar
  157. Venturi V, Keel C (2016) Signaling in the rhizosphere. Trends Plant Sci 21(3):187–198.  https://doi.org/10.1016/j.tplants.2016.01.005CrossRefGoogle Scholar
  158. Vurukonda SSK, Vardharajula S, Shrivastava M, SkZ A (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184(Supplement C):13–24CrossRefGoogle Scholar
  159. Wang C-J, Yang W, Wang C, Gu C, Niu D-D, Liu H-X, Wang Y-P, Guo J-H (2012) Induction of drought tolerance in cucumber plants by a consortium of three plant growth-promoting rhizobacterium strains. PLoS One 7(12):e52565.  https://doi.org/10.1371/journal.pone.0052565CrossRefGoogle Scholar
  160. Wang HH, Mee MT, Church GM (2013) Chapter 17 - Applications of engineered synthetic ecosystems. In: Zhao H (ed) Synthetic biology: tools and applications. Elsevier, pp 317–325Google Scholar
  161. Ward BB (2013) Nitrification. In: Scott AE (ed) Reference module in earth systems and environmental sciences. Elsevier Amsterdam, The Netherlands.  https://doi.org/10.1016/B978-0-12-409548-9.00697-7Google Scholar
  162. Waters CM, Bassler BL (2005) Quorum sensing: communication in bacteria. Annu Rev Cell Dev Biol 21(1):319–346CrossRefGoogle Scholar
  163. Watnick P, Kolter R (2000) Biofilm, city of microbes. J Bacteriol 182(10):2675–2679CrossRefGoogle Scholar
  164. Weidner S, Latz E, Agaras BC, Valverde C, Jousset A (2016) Protozoa stimulate the plant beneficial activity of rhizospheric pseudomonads. Plant Soil 410:509–515CrossRefGoogle Scholar
  165. West SA, Cooper GA (2016) Division of labour in microorganisms: an evolutionary perspective. Nat Rev Microbiol. 14(11):716–723CrossRefGoogle Scholar
  166. West SA, Griffin AS, Gardner A, Diggle SP (2006) Social evolution theory for microorganisms. Nat Rev Microbiol 4(8):597–607.  https://doi.org/10.1038/nrmicro1461CrossRefGoogle Scholar
  167. West SA, Diggle SP, Buckling A, Gardner A, Griffin AS (2007a) The social lives of microbes. Annu Rev Ecol Evol Syst 38(1):53–77.  https://doi.org/10.1146/annurev.ecolsys.38.091206.095740CrossRefGoogle Scholar
  168. West SA, Griffin AS, Gardner A (2007b) Evolutionary explanations for cooperation. Curr Biol 17(16):R661–R672CrossRefGoogle Scholar
  169. Wu SC, Cao ZH, Li ZG, Cheung KC, Wong MH (2005) Effects of biofertilizer containing N-fixer, P and K solubilizers and AM fungi on maize growth: a greenhouse trial. Geoderma 125(1):155–166CrossRefGoogle Scholar
  170. Zaidi A, Khan MS, Aamil M (2004) Bioassociative effect of rhizospheric microorganisms on growth, yield, and nutrient uptake of greengram. J Plant Nutr 27(4):601–612CrossRefGoogle Scholar
  171. Zhang C, Sheng C, Wang W, Hu H, Peng H, Zhang X (2015) Identification of the lomofungin biosynthesis gene cluster and associated flavin-dependent monooxygenase gene in Streptomyces lomondensis S015. PLoS One 10(8):1–15Google Scholar
  172. Zhang L, Xu M, Liu Y, Zhang F, Hodge A, Feng G (2016) Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. New Phytol 210(3):1022–1032.  https://doi.org/10.1111/nph.13838CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Yoann Besset-Manzoni
    • 1
    • 2
  • Laura Rieusset
    • 1
  • Pierre Joly
    • 2
  • Gilles Comte
    • 1
  • Claire Prigent-Combaret
    • 1
  1. 1.UMR Ecologie Microbienne, CNRS, INRA, VetAgro Sup, UCBL, Université de LyonVilleurbanne cedexFrance
  2. 2.BiovitisSaint Etienne-de-ChomeilFrance

Personalised recommendations