Plant Molecular Biology

, Volume 90, Issue 6, pp 537–548 | Cite as

A perspective on inter-kingdom signaling in plant–beneficial microbe interactions

  • Amanda Rosier
  • Usha Bishnoi
  • Venkatachalam Lakshmanan
  • D. Janine Sherrier
  • Harsh P. BaisEmail author


Recent work has shown that the rhizospheric and phyllospheric microbiomes of plants are composed of highly diverse microbial species. Though the information pertaining to the diversity of the aboveground and belowground microbes associated with plants is known, an understanding of the mechanisms by which these diverse microbes function is still in its infancy. Plants are sessile organisms, that depend upon chemical signals to interact with the microbiota. Of late, the studies related to the impact of microbes on plants have gained much traction in the research literature, supporting diverse functional roles of microbes on plant health. However, how these microbes interact as a community to confer beneficial traits to plants is still poorly understood. Recent advances in the use of “biologicals” as bio-fertilizers and biocontrol agents for sustainable agricultural practices is promising, and a fundamental understanding of how microbes in community work on plants could help this approach be more successful. This review attempts to highlight the importance of different signaling events that mediate a beneficial plant microbe interaction. Fundamental research is needed to understand how plants react to different benign microbes and how these microbes are interacting with each other. This review highlights the importance of chemical signaling, and biochemical and genetic events which determine the efficacy of benign microbes to promote the development of beneficial traits in plants.


Aboveground Belowground Microbiome Phyllosphere Rhizosphere 



H. P. B and D. J. S. acknowledge the support from BASF through a company-sponsored project to University of Delaware.

Author contribution

HPB and DJS conceived the outline of the review. AR, UB and VL wrote the individual sections of the review.


  1. Afshinnekoo E, Meydan C, Chowdhury S, Jaroudi D, Boyer C (2015) Geospatial resolution of human and bacterial diversity with city-scale metagenomics. CELS 1:72–87Google Scholar
  2. Antunes PM (2004) Determination on nutritional and signalling factors involved in the tripartite symbiosis formed by arbuscular mycorrhizal fungi, Bradyrhizobium and soybean. Ph.D. thesis, Univ. of Guelph, Guelph, ONGoogle Scholar
  3. Badri DV, Zolla G, Bakker MG, Manter DK, Vivanco JM (2013) Potential impact of soil microbiomes on the leaf metabolome and on herbivore feeding behavior. New Phytol 198:264–273PubMedCrossRefGoogle Scholar
  4. Balint-Kurti P, Simmons SJ, Blum JE, Ballaré CL, Stapleton AE (2010) Maize leaf epiphytic bacteria diversity patterns are genetically correlated with resistance to fungal pathogen infection. Mol Plant Microbe Interact 23:473–484PubMedCrossRefGoogle Scholar
  5. Ban H, Chai X, Lin Y, Zhou Y, Peng D, Zhou Y (2009) Transgenic Amorphophallus konjac expressing synthesized acyl-homoserine lactonase (aiiA) gene exhibit enhanced resistance to soft rot disease. Plant Cell Rep 28:1847–1855PubMedCrossRefGoogle Scholar
  6. Beattie GA, Lindow SE (1995) The secret life of foliar bacterial pathogens on leaves. Annu Rev Phytopathol 33:145–172PubMedCrossRefGoogle Scholar
  7. Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486PubMedCrossRefGoogle Scholar
  8. Berg G (2009) Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84:11–18PubMedCrossRefGoogle Scholar
  9. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13PubMedCrossRefGoogle Scholar
  10. Bodenhausen N, Bortfeld-Miller M, Ackermann M, Vorholt JA (2014) A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. PLoS Genet 10:e1004283PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bouffaud ML, Poirier MA, Muller D, Moënne-Loccoz Y (2014) Root microbiome relates to plant host evolution in maize and other Poaceae. Environ Microbiol 16:2804–2814PubMedCrossRefGoogle Scholar
  12. Bulgarelli D, Rott M, Schlaeppi K, van Themaat EVL, Ahmadinejad N, Assenza F et al (2012) Revealing structure and assembly cues for Arabidopsis root inhabiting bacterial microbiota. Nature 488:91–95PubMedCrossRefGoogle Scholar
  13. Carvalhais LC, Dennis PG, Badri DV, Tyson GW, Vivanco JM, Schenk PM (2013) Activation of the jasmonic acid plant defense pathway alters the composition of rhizosphere bacterial communities. PLoS One 8:e56457PubMedPubMedCentralCrossRefGoogle Scholar
  14. Carvalhais LC, Dennis PG, Schenk PM (2014) Plant defense inducers rapidly influence the diversity of bacterial communities in a potting mix. Appl Soil Ecol 84:1–5CrossRefGoogle Scholar
  15. Carvalhais LC, Dennis PG, Badri DV, Kidd BN, Vivanco JM et al (2015) Linking jasmonic acid signaling, root exudates, and rhizosphere microbiomes. Mol Plant Microbe Interact 28:1049–1058PubMedCrossRefGoogle Scholar
  16. Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48:489–499CrossRefGoogle Scholar
  17. Chernin LS (2011) Quorum-sensing signals as mediators of PGPRs’ beneficial traits. In: Maheshwari DK (ed) Bacteria in agrobiology: plant nutrient management. Springer, Berlin, pp 209–236CrossRefGoogle Scholar
  18. Christensen H, Jakobsen I (1993) Reduction of bacterial growth by a vesicular-arbuscular mycorrhizal fungus in the rhizosphere of cucumber (Cucumis sativus L.). Biol Fertil Soils 15:253–258CrossRefGoogle Scholar
  19. Combes-Meynet E, Pothier JF, Mënne-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 24:271–284PubMedCrossRefGoogle Scholar
  20. Crépin A, Barbey C, Cirou A, Tannières M, Orange N, Feuilloley M et al (2012) Biological control of pathogen communication in the rhizosphere: a novel approach applied to potato soft rot due to Pectobacterium atrosepticum. Plant Soil 358:27–37CrossRefGoogle Scholar
  21. Damiani I, Baldacci-Cresp F, Hopkins J, Andrio E, Balzergue S, Lecomte P et al (2012) Plant genes involved in harbouring symbiotic rhizobia or pathogenic nematodes. New Phytol 194:511–522PubMedCrossRefGoogle Scholar
  22. DeAngelis KM, Lindow SE, Firestone MK (2008) Bacterial quorum sensing and nitrogen cycling in rhizosphere soil. FEMS Microbiol Ecol 66:197–207PubMedCrossRefGoogle Scholar
  23. Degrassi G, Devescovi G, Solis R, Steindler L, Venturi V (2007) Oryza sativa rice plants contain molecules that activate different quorum-sensing N-acyl homoserine lactone biosensors and are sensitive to the specific AiiA lactonase. FEMS Microbiol Lett 269:213–220PubMedCrossRefGoogle Scholar
  24. Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72:313–327PubMedCrossRefGoogle Scholar
  25. Dong YH, Wang LH, Xu JL, Zhang HB, Zhang XF, Zhang LH (2001) Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411:813–817PubMedCrossRefGoogle Scholar
  26. Doornbos RF, Geraats BPJ, Kuramae EE, Van Loon LC, Bakker PAHM (2011) Effects of jasmonic acid, ethylene, and salicylic acid signaling on the rhizosphere bacterial community of Arabidopsis thaliana. Mol Plant Microbe Interact 24:395–407PubMedCrossRefGoogle Scholar
  27. Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci USA. doi: 10.1073/pnas.1414592112 Google Scholar
  28. Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259PubMedPubMedCentralCrossRefGoogle Scholar
  29. Erlacher A, Cardinale M, Grosch R, Grube M, Berg G (2014) The impact of the pathogen Rhizoctonia solani and its beneficial counterpart Bacillus amyloliquefaciens on the indigenous lettuce microbiome. Front Microbiol 5:175PubMedPubMedCentralCrossRefGoogle Scholar
  30. Felici C, Vettori L, Giraldi E, Forino LMC, Toffanin A, Tagliasacchi AM (2008) Single and co-inoculation of Bacillus subtilis and Azospirillum brasilense on Lycopersicon esculentum: effects on plant growth and rhizosphere microbial community. Appl Soil Ecol 40:260–270CrossRefGoogle Scholar
  31. Fox SL, O’Hara GW, Bräu L (2011) Enhanced nodulation and symbiotic effectiveness of Medicago truncatula when co-inoculated with Pseudomonas fluorescens WSM3457 and Ensifer (Sinorhizobium) medicae WSM419. Plant Soil 348:245–254CrossRefGoogle Scholar
  32. Franzini VI, Azcón R, Méndes FL, Aroca R (2013) Different interaction among Glomus and Rhizobium species on Phaseolus vulgaris and Zea mays plant growth, physiology and symbiotic development under moderate drought stress conditions. Plant Growth Regul 70:265–273CrossRefGoogle Scholar
  33. Gao M, Teplitski M, Robinson JB, Bauer WD (2003) Production of substances by Medicago truncatula that affect bacterial quorum sensing. Mol Plant Microbe Interact 16:827–834PubMedCrossRefGoogle Scholar
  34. Gao M, Chen H, Eberhard A, Gronquist MR, Robinson JB, Connolly M (2007) Effects of AiiA-mediated quorum quenching in Sinorhizobium meliloti on quorum-sensing signals, proteome patterns, and symbiotic interactions. Mol Plant Microbe Interact 20:843–856PubMedCrossRefGoogle Scholar
  35. Geurts R, Heidstra R, Hadri AE, Downie JA, Franssen H, Van Kammen A, Bisseling T (1997) Sym2 of pea is involved in a nodulation factor-perception mechanism that controls the infection process in the epidermis. Plant Physiol 115:351–359PubMedPubMedCentralGoogle Scholar
  36. Gilbert JA, Jansson JK, Knight R (2014) The earth microbiome project: successes and aspirations. BMC Biol 12:69PubMedPubMedCentralCrossRefGoogle Scholar
  37. Giron D, Frago E, Glevarec G, Pieterse CMJ, Dicke M (2013) Cytokinins as key regulators in plant–microbe–insect interactions: connecting plant growth and defense. Funct Ecol 27:599–609CrossRefGoogle Scholar
  38. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227PubMedCrossRefGoogle Scholar
  39. González JE, Keshavan ND (2006) Messing with bacterial quorum sensing. Microbiol Mol Biol Rev 70:859–875PubMedPubMedCentralCrossRefGoogle Scholar
  40. González JE, Reuhs BL, Walker GC (1996) Low molecular weight EPS II of Rhizobium meliloti allows nodule invasion in Medicago sativa. Proc Natl Acad Sci USA 93:8636–8641PubMedPubMedCentralCrossRefGoogle Scholar
  41. Goss MJ, de Varennes A (2002) Soil disturbance reduces the efficacy of mycorrhizal associations for early soybean growth and N2 fixation. Soil Biol Biochem 34:1167–1173CrossRefGoogle Scholar
  42. Grayston SJ, Wang SQ, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378CrossRefGoogle Scholar
  43. Gurich N, González JE (2009) Role of quorum sensing in Sinorhizobium meliloti-Alfalfa symbiosis. J Bacteriol 191:4372–4382PubMedPubMedCentralCrossRefGoogle Scholar
  44. Harris MO, Friesen TL, Xu SS, Chen MS, Giron D, Stuart JJ (2015) Pivoting from Arabidopsis to wheat to understand how agricultural plants integrate responses to biotic stress. J Exp Bot 66:513–531PubMedCrossRefGoogle Scholar
  45. Helman Y, Chernin L (2015) Silencing the mob: disrupting quorum sensing as a means to fight plant disease. Mol Plant Pathol 16:316–329PubMedCrossRefGoogle Scholar
  46. Hoang HH, Becker A, González JE (2004) The LuxR homolog ExpR, in combination with the Sin quorum sensing system, plays a central role in Sinorhizobium meliloti gene expression. J Bacteriol 186:5460–5472PubMedPubMedCentralCrossRefGoogle Scholar
  47. Hunter PJ, Hand P, Pink D, Whipps JM, Bending GD (2010) Both leaf properties and microbe-microbe interactions influence within-species variation in bacterial population diversity and structure in the lettuce (Lactuca Species) phyllosphere. Appl Environ Microbiol 76:8117–8125PubMedPubMedCentralCrossRefGoogle Scholar
  48. Ikeda S, Okubo T, Takeda N, Banba M, Sasaki K, Imaizumi-Anraku H (2011) The genotype of the calcium/calmodulin-dependent protein kinase gene (CCaMK) determines bacterial community diversity in rice roots under paddy and upland field conditions. Appl Environ Microbiol 77:4399–4405PubMedPubMedCentralCrossRefGoogle Scholar
  49. Innerebner G, Knief C, Vorholt JA (2011) Protection of Arabidopsis thaliana against leaf-pathogenic Pseudomonas syringae by Sphingomonas strains in a controlled model system. Appl Environ Microbiol 77:3202–3210PubMedPubMedCentralCrossRefGoogle Scholar
  50. Jetiyanon K, Kloepper JW (2002) Mixtures of plant growth-promoting rhizobacteria for induction of systemic resistance against multiple plant diseases. Biol Control 24:285–291CrossRefGoogle Scholar
  51. Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480CrossRefGoogle Scholar
  52. Kang Y, Shen M, Wang H, Zhao Q (2013) A possible mechanism of action of plant growth-promoting rhizobacteria (PGPR) strain Bacillus pumilus WP8 via regulation of soil bacterial community structure. J Gen Appl Microbiol 59:267–277PubMedCrossRefGoogle Scholar
  53. Kang Y, Shen M, Yang X, Cheng D, Zhao Q (2014) A plant growth-promoting rhizobacteria (PGPR) mixture does not display synergistic effects, likely by biofilm but not growth inhibition. Microbiology 83:666–673CrossRefGoogle Scholar
  54. Kembel SW, O’Connor TK, Arnold HK, Hubbell SP, Wright SJ, Green JL (2014) Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. Proc Natl Acad Sci USA 111:13715–13720PubMedPubMedCentralCrossRefGoogle Scholar
  55. Keshavan ND, Chowdhary PK, Haines DC, González JE (2005) l-Canavanine made by Medicago sativa interferes with quorum sensing in Sinorhizobium meliloti. J Bacteriol 187:8427–8436PubMedPubMedCentralCrossRefGoogle Scholar
  56. Kim K, Yim W, Trivedi P, Madhaiyan M, Deka Boruah HP, Rashedul Islam MD et al (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 327:429–440CrossRefGoogle Scholar
  57. Kowalchuk GA, Buma DS, de Boer W, Klinkhamer PGL, van Veen JA (2002) Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Anton Leeuw Int J G 81:509–520CrossRefGoogle Scholar
  58. Kumar AS, Bais HP (2012) Wired to the roots: impact of root-beneficial microbe interactions on aboveground plant physiology and protection. Plant Signal Behav 7:1598–1604PubMedPubMedCentralCrossRefGoogle Scholar
  59. Kumar AS, Lakshmanan V, Caplan JL, Powell D, Czymmek KJ, Levia DF, Bais HP (2012) Rhizobacteria Bacillus subtilis restricts foliar pathogen entry through stomata. Plant J 72:694–706PubMedCrossRefGoogle Scholar
  60. Lakshmanan V, Kitto SL, Caplan JL, Hsueh YH, Kearns DB, Wu YS et al (2012) Microbe-associated molecular patterns-triggered root responses mediate beneficial rhizobacterial recruitment in Arabidopsis. Plant Physiol 160:1642–1661PubMedPubMedCentralCrossRefGoogle Scholar
  61. Lakshmanan V, Selvaraj G, Bais HP (2014) Functional soil microbiome: belowground solutions to an aboveground problem. Plant Physiol 166:689–700PubMedPubMedCentralCrossRefGoogle Scholar
  62. Landgraf R, Schaarschmidt S, Hause B (2012) Repeated leaf wounding alters the colonization of Medicago truncatula roots by beneficial and pathogenic microorganisms. Plant, Cell Environ 35:1344–1357CrossRefGoogle Scholar
  63. Lebeis SL, Paredes SH, Lundberg DS, Breakfield N, Gehring J et al (2015) Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349:860–864PubMedCrossRefGoogle Scholar
  64. Lee B, Farag MA, Park HB, Kloepper JW, Lee SH, Ryu CM (2012a) Induced resistance by a long-chain bacterial volatile: elicitation of plant systemic defense by a C13 volatile produced by Paenibacillus polymyxa. PLoS One 7:e48744PubMedPubMedCentralCrossRefGoogle Scholar
  65. Lee BL, Lee S, Ryu CM (2012b) Foliar aphid feeding recruits rhizosphere bacteria and primes plant immunity against pathogenic and non-pathogenic bacteria in pepper. Ann Bot 110:281–290PubMedPubMedCentralCrossRefGoogle Scholar
  66. Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Prome JC, Denarie J (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 392:936–941Google Scholar
  67. Liu X, Bimerew M, Ma Y, Müller H, Ovadis M, Eberl L (2007) Quorum-sensing signaling is required for production of the antibiotic pyrrolnitrin in a rhizospheric biocontrol strain of Serratia plymuthica. FEMS Microbiol Lett 270:299–305PubMedCrossRefGoogle Scholar
  68. Lowery CA, Dickerson TJ, Janda KD (2008) Interspecies and inter-kingdom communication mediated by bacterial quorum sensing. Chem Soc Rev 37:1337–1346PubMedCrossRefGoogle Scholar
  69. Ma A, Lv D, Zhuang X, Zhuang G (2013) Quorum quenching in culturable phyllosphere bacteria from tobacco. Int J Mol Sci 14:14607–14619PubMedPubMedCentralCrossRefGoogle Scholar
  70. Marasco R, Rolli E, Ettoumi B, Vigani G, Mapelli F, Borin S (2012) A drought resistance-promoting microbiome is selected by root system under desert farming. PLoS One 7:e48479PubMedPubMedCentralCrossRefGoogle Scholar
  71. Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anolles G, Rolfe BG (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci USA 100:1444–1449PubMedPubMedCentralCrossRefGoogle Scholar
  72. Meldau S, Erb M, Baldwin IT (2012) Defense on demand: mechanisms behind optimal defence patterns. Ann Bot 110:1503–15141PubMedPubMedCentralCrossRefGoogle Scholar
  73. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100PubMedCrossRefGoogle Scholar
  74. Meyer SLF, Halbrendt JM, Carta LK, Skantar AM, Liu T, Abdelnabby HME et al (2009) Toxicity of 2,4-diacetylphloroglucinol (DAPG) to plant-parasitic and bacterial-feeding nematodes. J Nematol 41:274–280PubMedPubMedCentralGoogle Scholar
  75. Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199PubMedCrossRefGoogle Scholar
  76. Minz D, Ofek M, Hadar Y (2013) Plant rhizosphere microbial communities. In: DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: prokaryotic communities and ecophysiology. Springer, Berlin, pp 57–84Google Scholar
  77. Molina L, Constantinescu F, Michel L, Reimmann C, Duffy B, Défago G (2003) Degradation of pathogen quorum-sensing molecules by soil bacteria: a preventive and curative biological control mechanism. FEMS Microbiol Ecol 45:71–81PubMedCrossRefGoogle Scholar
  78. Morel MA, Cagide C, Minteguiaga MA, Dardanelli MS, Castro-Sowinski S (2014) The pattern of secreted molecules during the co-inoculation of alfalfa plants with Sinorhizobium meliloti and Delftia sp. strain JD2: An interaction that improves plant yield. Mol Plant Microbe Interact 28:134–142CrossRefGoogle Scholar
  79. Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie 23:375–396CrossRefGoogle Scholar
  80. Oliver KM, Degnan PH, Burke GR, Moran NA (2010) Facultative symbionts of aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55:247–266PubMedCrossRefGoogle Scholar
  81. Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci USA 110:6548–6553PubMedPubMedCentralCrossRefGoogle Scholar
  82. Pellock BJ, Teplitski M, Boinay RP, Bauer WD, Walker GC (2002) A LuxR homolog controls production of symbiotically active extracellular polysaccharide ii by Sinorhizobium meliloti. J Bacteriol 184:5067–5076PubMedPubMedCentralCrossRefGoogle Scholar
  83. Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64:180–201PubMedPubMedCentralCrossRefGoogle Scholar
  84. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799PubMedCrossRefGoogle Scholar
  85. Pierson LS, Wood DW, Pierson EA (1998) Homoserine lactone-mediated gene regulation in plant-associated bacteria. Annu Rev Phytopathol 36:207–225PubMedCrossRefGoogle Scholar
  86. Pieterse CM, Van Der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521PubMedCrossRefGoogle Scholar
  87. Prashar P, Kapoor N, Sachdeva S (2013) Rhizosphere: its structure, bacterial diversity and significance. Rev Environ Sci Biotechnol 13:63–77CrossRefGoogle Scholar
  88. Raaijmakers JM, Weller DM (1998) Natural plant protection by 2,4-diacetylphloroglucinol producing Pseudomonas spp. in take-all decline soils. Mol Plant Microbe Interact 11:144–152CrossRefGoogle Scholar
  89. Radutoiu S, Madsen LH, Madsen EB, Jurkiewicz A, Fukai E, Quistgaard EM (2007) LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J 26:3923–3935PubMedPubMedCentralCrossRefGoogle Scholar
  90. Rastogi G, Sbodio A, Tech JJ, Suslow TV, Coaker GL, Leveau JHJ (2012) Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J 6:1812–1822PubMedPubMedCentralCrossRefGoogle Scholar
  91. Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21:541–554PubMedCrossRefGoogle Scholar
  92. Rinaudi LV, Gonzalez JE (2009) The low-molecular-weight fraction of exopolysaccharide ii from sinorhizobium meliloti is a crucial determinant of biofilm formation. J Bacteriol 191:7216–7224PubMedPubMedCentralCrossRefGoogle Scholar
  93. Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343PubMedCrossRefGoogle Scholar
  94. Roh JY, Choi JY, Li MS, Jin BR, Je YH (2007) Bacillus thuringiensis as a specific, safe, and effective tool for insect pest control. J Microbiol Biotechnol 17:547–559PubMedGoogle Scholar
  95. Rudrappa T, Czymmek KJ, Paré PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–1556PubMedPubMedCentralCrossRefGoogle Scholar
  96. Rudrappa T, Biedrzycki ML, Kunjeti SG, Donofrio NM et al (2010) The rhizobacterial elicitor acetoin induces systemic resistance in Arabidopsis thaliana. Commun Integr Biol 3:130–138PubMedPubMedCentralCrossRefGoogle Scholar
  97. Ryu C-M, Murphy JF, Reddy MS, Kloepper JW (2007) A two-strain mixture of rhizobacteria elicits induction of systemic resistance against Pseudomonas syringae and Cucumber mosaic virus coupled to promotion of plant growth on Arabidopsis thaliana. J Microbiol Biotechnol 17:280–286PubMedGoogle Scholar
  98. Ryu C-M, Choi HK, Lee C-H, Murphy JF, Lee J-K, 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 29:182–192PubMedPubMedCentralCrossRefGoogle Scholar
  99. Sanchez-Contreras M, Bauer WD, Gao M, Robinson JB, Allan Downie J (2007) Quorum-sensing regulation in rhizobia and its role in symbiotic interactions with legumes. Philos Trans R Soc Lond B Biol Sci 362:1149–1163PubMedPubMedCentralCrossRefGoogle Scholar
  100. Santhanam R, Groten K, Meldau DG, Baldwin IT (2014) Analysis of plant–bacteria interactions in their native habitat: bacterial communities associated with wild tobacco are independent of endogenous JA levels and developmental stages. PLoS One 9:e94710PubMedPubMedCentralCrossRefGoogle Scholar
  101. Schenk ST, Hernández-Reyes C, Samans B, Stein E, Neumann C, Schikora M et al (2014) n-acyl-homoserine lactone primes plants for cell wall reinforcement and induces resistance to bacterial pathogens via the salicylic acid/oxylipin pathway. Plant Cell 26:2708–2723PubMedPubMedCentralCrossRefGoogle Scholar
  102. Schlaeppi K, Bulgarelli D (2015) The plant microbiome at work. Mol Plant Microbe Interact 28:212–217PubMedCrossRefGoogle Scholar
  103. Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S 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 67:4742–4751PubMedPubMedCentralCrossRefGoogle Scholar
  104. Soler R, Erb M, Kaplan I (2013) Long distance root–shoot signaling in plant–insect community interactions. Trends Plant Sci 18:149–156PubMedCrossRefGoogle Scholar
  105. Spaink HP (2000) Root nodulation and infection factors produced by rhizobial bacteria. Annu Rev Microbiol 54:257–288PubMedCrossRefGoogle Scholar
  106. Spence C, Bais H (2013) Probiotics for plants: rhizospheric microbiome and plant fitness. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere, Vols 1 and 2. Wiley, Hoboken, pp 713–721. doi: 10.1002/9781118297674.ch67
  107. Spence C, Alff E, Johnson C, Ramos C, Donofrio N, Sundaresan V (2014) Natural rice rhizospheric microbes suppress rice blast infections. BMC Plant Biol 14:130PubMedPubMedCentralCrossRefGoogle Scholar
  108. Stam JM, Kroes A, Li Y, Gols R, van Loon JJ, Poelman EH (2014) Plant interactions with multiple insect herbivores: from community to genes. Plant Biol 65:689–713CrossRefGoogle Scholar
  109. Steer J, Harris JA (2000) Shifts in the microbial community in rhizosphere and non-rhizosphere soils during the growth of Agrostis stolonifera. Soil Biol Biochem 32:869–878CrossRefGoogle Scholar
  110. Steidle A, Sigl K, Schuhegger R, Ihring A, Schmid M, Gantner S (2001) Visualization of n-acylhomoserine lactone-mediated cell-cell communication between bacteria colonizing the tomato rhizosphere. Appl Environ Microbiol 67:5761–5770PubMedPubMedCentralCrossRefGoogle Scholar
  111. Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959–962PubMedCrossRefGoogle Scholar
  112. Sugio A, Dubreuil G, Giron D, Simon JC (2015) Plant–insect interactions under bacterial influence: ecological implications and underlying mechanisms. J Exp Bot 66:467–478PubMedCrossRefGoogle Scholar
  113. Sylla J, Alsanius BW, Krüger E, Reineke A, Strohmeier S, Wohanka W (2013) Leaf microbiota of strawberries as affected by biological control agents. Phytopathol 103:1001–1011CrossRefGoogle Scholar
  114. Teplitski M, Robinson JB, Bauer WD (2000) Plants secrete substances that mimic bacterial n-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant Microbe Interact 13:637–648PubMedCrossRefGoogle Scholar
  115. Teplitski M, Chen H, Rajamani S, Gao M, Merighi M, Sayre RT (2004) Chlamydomonas reinhardtii secretes compounds that mimic bacterial signals and interfere with quorum sensing regulation in bacteria. Plant Physiol 134:137–146PubMedPubMedCentralCrossRefGoogle Scholar
  116. Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270PubMedCrossRefGoogle Scholar
  117. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI (2007) The human microbiome project. Nature 449:804–810PubMedPubMedCentralCrossRefGoogle Scholar
  118. Turner TR, James EK, Poole PS (2013) The plant microbiome. Genome Biol 14:209–219PubMedPubMedCentralCrossRefGoogle Scholar
  119. Uroz S, Dessaux Y, Oger P (2009) Quorum sensing and quorum quenching: the yin and yang of bacterial communication. Chem biochem Eur J Chem Biol 10:205–216CrossRefGoogle Scholar
  120. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T et al (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72CrossRefGoogle Scholar
  121. Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A (2015) The importance of the microbiome of the plant holobiont. New Phytol 206:1196–1206PubMedCrossRefGoogle Scholar
  122. Vandeputte OM, Kiendrebeogo M, Rasamiravaka T, Stévigny C, Duez P, Rajaonson S (2011) The flavanone naringenin reduces the production of quorum sensing-controlled virulence factors in Pseudomonas aeruginosa PAO1. Microbiol Read Engl 157:2120–2132CrossRefGoogle Scholar
  123. Venturi V, Fuqua C (2013) Chemical signaling between plants and plant-pathogenic bacteria. Annu Rev Phytopathol 51:17–37PubMedCrossRefGoogle Scholar
  124. Veselova MA, Klein S, Bass IA, Lipasova VA, Metlitskaia AZ, Ovadis MI (2008) Quorum sensing systems of regulation, synthesis of phenazine antibiotics, and antifungal (corrected) activity in rhizospheric bacterium Pseudomonas chlororaphis 449. Genetika 44:1617–1626PubMedGoogle Scholar
  125. von Bodman SB, Bauer WD, Coplin DL (2003) Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol 41:455–482CrossRefGoogle Scholar
  126. von Rad U, Klein I, Dobrev PI, Kottova J, Zazimalova E, Fekete A (2008) Response of Arabidopsis thaliana to N-hexanoyl-DL-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere. Planta 229:73–85CrossRefGoogle Scholar
  127. Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840PubMedCrossRefGoogle Scholar
  128. Walker V, Couillerot O, Felten AV, Bellvert F, Jansa J, Maurhofer M (2011) Variation of secondary metabolite levels in maize seedling roots induced by inoculation with Azospirillum, Pseudomonas and Glomus consortium under field conditions. Plant Soil 356:151–163CrossRefGoogle Scholar
  129. Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Reg 19:195–216Google Scholar
  130. Weyens N, van der Lelie D, Taghavi S, Newman L, Vangronsveld J (2009) Exploiting plant-microbe partnerships to improve biomass production and remediation. Trends Biotechnol 27:591–598PubMedCrossRefGoogle Scholar
  131. Whipps JM, Hand P, Pink D, Bending GD (2008) Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105:1744–1755PubMedCrossRefGoogle Scholar
  132. Williams TR, Marco ML (2014) Phyllosphere microbiota composition and microbial community transplantation on lettuce plants grown indoors. Mbio 5:e01564–14PubMedPubMedCentralCrossRefGoogle Scholar
  133. Wood DW, Gong F, Daykin MM, Williams P, Pierson LS (1997) N-acyl-homoserine lactone-mediated regulation of phenazine gene expression by Pseudomonas aureofaciens 30–84 in the wheat rhizosphere. J Bacteriol 179:7663–7670PubMedPubMedCentralGoogle Scholar
  134. Wu JQ, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24PubMedCrossRefGoogle Scholar
  135. Yang JW, Yi HS, Kim H, Lee B, Lee S, Ghim SY (2011) Whitefly infestation of pepper plants elicits defense responses against bacterial pathogens in leaves and roots and changes the below-ground microflora. J Ecol 99:46–56CrossRefGoogle Scholar
  136. Zeriouh H, Romero D, Garcia-Gutierrez L, Cazorla FM, de Vicente A, Perez-Garcia A (2011) The iturin-like lipopeptides are essential components in the biological control arsenal of Bacillus subtilis against bacterial diseases of cucurbits. Mol Plant Microbe Interact MPMI 24:1540–1552PubMedCrossRefGoogle Scholar
  137. Zhang L, Ruan L, Hu C, Wu H, Chen S, Yu Z, Sun M (2007) Fusion of the genes for AHL-lactonase and S-layer protein in Bacillus thuringiensis increases its ability to inhibit soft rot caused by Erwinia carotovora. Appl Microbiol Biotechnol 74:667–675PubMedCrossRefGoogle Scholar
  138. Zhang B, Bai Z, Hoefel D, Tang L, Yang Z, Zhuang G, Yang J, Zhang H (2008) Assessing the impact of the biological control agent Bacillus thuringiensis on the indigenous microbial community within the pepper plant phyllosphere. FEMS Microbiol Lett 284:102–108PubMedCrossRefGoogle Scholar
  139. Zolla G, Badri DV, Bakker MG, Manter DK, Vivanco JM (2013) Soil microbiomes vary in their ability to confer drought tolerance to Arabidopsis. Appl Soil Ecol 68:1–9CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Amanda Rosier
    • 1
    • 2
  • Usha Bishnoi
    • 1
    • 2
  • Venkatachalam Lakshmanan
    • 1
    • 2
  • D. Janine Sherrier
    • 1
    • 2
  • Harsh P. Bais
    • 1
    • 2
    Email author
  1. 1.Department of Plant and Soil SciencesUniversity of DelawareNewarkUSA
  2. 2.Delaware Biotechnology InstituteNewarkUSA

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