The Complex Molecular Signaling Network in Microbe–Plant Interaction



Soil bacteria living around plants exert neutral, beneficial, or detrimental effects on plant growth and development. These effects are the result of signal exchange in which there is a mutual recognition of diffusible molecules produced by the plant and microbe partners. Understanding the molecular signaling network involved in microbe–plant interaction is a promising opportunity to improve crop productivity and agriculture sustainability. Many approaches have been used to decipher these molecular signals, and the results show that plants and microorganisms respond by inducing the expression of, and releasing, a mixture of molecules that includes flavonoids, phytohormones, pattern recognition receptors, nodulins, lectins, enzymes, lipo-chitooligosaccharides, exopolysaccharides, amino acids, fatty acids, vitamins, and volatiles.

This chapter reviews current knowledge of the diverse signaling pathways that are turned on when plants interact with beneficial microbes, with emphasis on bacteria belonging to the genera Rhizobium, Azospirillum, and Pseudomonas.


Arbuscular Mycorrhizal Fungus Root Hair Quorum Sense Plant Growth Promotion Plant Growth Promote Rhizobacteria 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



 We thank Programa de Desarrollo de las Ciencias Básicas (PEDECIBA). The work of M. Morel was supported by Agencia Nacional de Investigación e Innovación (ANII). Dr. Valerie Dee revised linguistic aspects of this manuscript.


  1. Adonizio A, Kong K, Mathee K (2008) Inhibition of quorum sensing-controlled virulence factor production in Pseudomonas aeruginosa by South Florida plant extracts. Antimicrob Agents Chemother 52:198–203PubMedCrossRefGoogle Scholar
  2. Ali B, Sabri A, Ljung K, Hasnain S (2009) Auxin production by plant associated bacteria: impact on endogenous IAA content and growth of Triticum aestivum L. Lett Appl Microbiol 48:542–547PubMedCrossRefGoogle Scholar
  3. Ariel F, Brault-Hernandez M, Laffont C, Huault E, Brault M, Plet J, Moison M, Blanchet S, Ichanté JL, Chabaud M, Carrere S, Crespi M, Chan RL, Frugiera F (2012) Two direct targets of cytokinin signaling regulate symbiotic nodulation in Medicago truncatula. Plant Cell 24:3838–3852PubMedCrossRefGoogle Scholar
  4. Arkhipova T, Prinsen E, Veselov S, Martinenko E, Melentiev A, Kudoyarova G (2007) Cytokinin producing bacteria enhance plant growth in drying soil. Plant Soil 292:305–315CrossRefGoogle Scholar
  5. Azziz G, Bajsa N, Haghjou T, Taulé C, Valverde A, Igual J, Arias A (2012) Abundance, diversity and prospecting of culturable phosphate solubilizing bacteria on soils under crop-pasture rotations in a no-tillage regime in Uruguay. Appl Soil Ecol 61:320–326CrossRefGoogle Scholar
  6. Badri D, Vivanco J (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681PubMedCrossRefGoogle Scholar
  7. Badri D, Weir T, van der Lelie D, Vivanco J (2009) Rhizosphere chemical dialogues: plant–microbe interactions. Curr Opin Biotechnol 20:642–650PubMedCrossRefGoogle Scholar
  8. Bahat-Samet E, Castro-Sowinski S, Okon Y (2004) Arabinose content of extracellular polysaccharide plays a role in cell aggregation of Azospirillum brasilense. FEMS Microbiol Lett 237:195–203PubMedCrossRefGoogle Scholar
  9. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266PubMedCrossRefGoogle Scholar
  10. Bakker P, Pieterse C, van Loon L (2007) Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97(2007):239PubMedCrossRefGoogle Scholar
  11. Bapaume L, Reinhardt D (2012) How membranes shape plant symbioses: signaling and transport in nodulation and arbuscular mycorrhiza. Front Plant Sci 3:1–29CrossRefGoogle Scholar
  12. Bashan Y, Holguin G, de-Bashan L (2004) Azospirillum-plant relationships: physiological molecular, agricultural, and environmental advances (1997–2003). Can J Microbiol 50:521–577PubMedCrossRefGoogle Scholar
  13. Batut J, Mergaert P, Masson-Boivin CM (2011) Peptide signalling in the rhizobium-legume symbiosis. Curr Opin Microbiol 14:181–187PubMedCrossRefGoogle Scholar
  14. Baudoin E, Lerner A, Mirza M, El Zemrany H, Prigent-Combaret C, Jurkevich E, Spaepen S, Vanderleyden J, Nazaret S, Okon Y, Moenne-Loccoz Y (2010) Effects of Azospirillum brasilense with genetically modified auxin biosynthesis gene ipdC upon the diversity of the indigenous microbiota of the wheat rhizosphere. Res Microbiol 161:219–226PubMedCrossRefGoogle Scholar
  15. Bazin J, Bustos-Sanmamed P, Hartmann C, Lelandais-Briere C, Crespi M (2012) Complexity of miRNA-dependent regulation in root-symbiosis. Philos Trans R Soc Lond B Biol Sci 367:1570–1579PubMedCrossRefGoogle Scholar
  16. Becker A, Fraysse N, Sharypova L (2005) Recent advances in studies on structure and symbiosis-related function of rhizobial K-antigens and lipopolysaccharide. Mol Plant Microbe Interact 18:899–905PubMedCrossRefGoogle Scholar
  17. Begum AA, Leibovitch S, Migner P, Zhang F (2001) Specific flavonoids induced nod gene expression and pre-activated nod genes of Rhizobium leguminosarum increased pea (Pisum sativum L.) and lentil (Lens culinaris L.) nodulation in controlled growth chamber environments. J Exp Bot 52:1537–1543PubMedCrossRefGoogle Scholar
  18. Bent E (2010) Induced systemic resistance mediated by plant growth-promoting rhizobacteria (PGPR) and fungi (PGPF). In: Tuzun S, Bent E (eds) Multigenic and induced systemic resistance in plants. Springer, New York, pp 225–258Google Scholar
  19. Bhattacharjee R, Singh A, Mukhopadhyay S (2008) Use of nitrogen-fixing bacteria as biofertiliser for non-legumes: prospects and challenges. Appl Microbiol Biotechnol 80:199–209PubMedCrossRefGoogle Scholar
  20. Bianco C, Defez R (2011) Soil bacteria support and protect plants against abiotic stresses. In: Shanker A (ed) Abiotic stress in plants-mechanisms and adaptations. Intech, Rijeka, pp 143–170Google Scholar
  21. Bleecker A, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18PubMedCrossRefGoogle Scholar
  22. Boiero L, Perrig D, Masciarelli O, Penna C, Cassán F, Luna V (2007) Phytohormone production by three strains of Bradyrhizobium japonicum and possible physiological and technological implications. Appl Microbiol Biotechnol 74:874–880PubMedCrossRefGoogle Scholar
  23. Bomfeti CA, Florentino LA, Guimarães AP, Gomes Cardoso P, Guerreiro MC, de Souza Moreira FM (2011) Exopolysaccharides produced by the symbiotic nitrogen-fixing bacteria of Leguminosae. Rev Bras Ciênc Solo 35:657–671CrossRefGoogle Scholar
  24. Burdman S, Volpin H, Kigel J, Kapulnik Y, Okon Y (1996) Promotion of nod gene inducers and nodulation in common bean (Phaseolus vulgaris) roots inoculated with Azospirillum brasilense Cd. Appl Environ Microbiol 62:3030–3033PubMedGoogle Scholar
  25. Burdman S, Jurkevitch E, Soria-Diaz M, Gil Serrano A, Okon Y (2000) Extracellular polysaccharide composition of Azospirillum brasilense and its relation with cell aggregation. FEMS Microbiol Lett 189:259–264PubMedCrossRefGoogle Scholar
  26. Cai T, Cai W, Zhang J, Zheng H, Tsou A, Xiao L, Zhong Z, Zhu J (2009) Host legume-exuded antimetabolites optimize the symbiotic rhizosphere. Mol Microbiol 73:507–517PubMedCrossRefGoogle Scholar
  27. Cai Z, Kastell A, Knorr D, Smetanska I (2012) Exudation: an expanding technique for continuous production and release of secondary metabolites from plant cell suspension and hairy root cultures. Plant Cell Rep. doi: 10.1007/s00299-011-1165-0 Google Scholar
  28. Cassán F, Perrig D, Sgroy V, Masciarelli O, Penna C, Luna V (2009) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Eur J Soil Biol 45:28–35CrossRefGoogle Scholar
  29. Cesco S, Mimmo T, Tonon G, Tomasi N, Pinton R, Terzano R, Neumann G, Weisskopf L, Renella G, Landi L, Nannipieri P (2012) Plant-borne flavonoids released into the rhizosphere: impact on soil bio-activities related to plant nutrition. A review. Biol Fertil Soils. doi: 10.1007/s00374-011-0653-2 Google Scholar
  30. Chalupowicz L, Barash I, Schwartz M, Aloni R, Manulis S (2006) Comparative anatomy of gall development on Gypsophila paniculata induced by bacteria with different mechanisms of pathogenicity. Planta 224:429–437PubMedCrossRefGoogle Scholar
  31. Choi J, Choi D, Lee S, Ryu C, Hwang I (2011) Cytokinins and plant immunity: old foes or new friends? Trends Plant Sci 16:388–394PubMedCrossRefGoogle Scholar
  32. Combes-Meynet E, Pothier J, 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 24:271–284PubMedCrossRefGoogle Scholar
  33. D’Antuono A, Casabuono A, Couto A, Ugalde R, Lepek V (2005) Nodule development induced by Mesorhizobium loti mutant strains affected in polysaccharide synthesis. Mol Plant Microbe Interact 18(5):446–457PubMedCrossRefGoogle Scholar
  34. D’Haeze W, Holsters M (2002) Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12:79R–105RPubMedCrossRefGoogle Scholar
  35. Dardanelli MS, Fernández de Córdoba FJ, Espuny MR, Rodriguez Carvajal MA, Soria Díaz ME, Gil Serrano AM, Okon Y, Megías M (2008) Effect of Azospirillum brasilense coinoculation with Rhizobium on Phaseolus vulgaris flavonoids and Nod factor production under salt stress. Soil Biol Biochem 40:2713–2721CrossRefGoogle Scholar
  36. Davies P (2010) The plant hormones: their nature, occurrence, and functions. In: Davies P (ed) Plant hormones. Springer, Dordrecht, pp 1–15CrossRefGoogle Scholar
  37. De la Peña C, Lei Z, Watson BS, Sumner LW, Vivanco JM (2008) Root-microbe communication through protein secretion. J Biol Chem 283:25247–25255CrossRefGoogle Scholar
  38. Deakin WJ, Broughton WJ (2009) Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat Rev Microbiol 7:312–320PubMedGoogle Scholar
  39. Ding Y, Kalo P, Yendrek C, Sun J, Liang Y, Marsh JF, Harris JM, Oldroyd GE (2008) Abscisic acid coordinates Nod Factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula. Plant Cell 20:2681–2695PubMedCrossRefGoogle Scholar
  40. Downie J (2010) The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol Rev 34:150–170PubMedCrossRefGoogle Scholar
  41. Dunn M, Puerppke S, Krishnan H (1992) The nod gene inducer genistein alters the composition and molecular mass distribution of extracellular polysaccharides produced by Rhizobium fredii USDA193. FEMS Microbiol Lett 97:107–112Google Scholar
  42. Egamberdieva D, Berg G, Lindström K, Räsänen LA (2010) Co-inoculation of Pseudomonas spp. with Rhizobium improves growth and symbiotic performance off odder galega (Galega orientalis Lam.). Eur J Soil Biol 46:269–272CrossRefGoogle Scholar
  43. Etesami H, Ali Alikhani H, Ali Akbari A (2009) Evaluation of plant growth hormones production (IAA) ability by Iranian soils Rhizobial strains and effects of superior strains application on wheat growth indexes. World Appl Sci J 6:1576–1584Google Scholar
  44. Fang Y, Hirsch AM (1998) Studying early nodulin gene ENOD40 expression and induction by nodulation factor and cytokinin in transgenic alfalfa. Plant Physiol 116:53–68PubMedCrossRefGoogle Scholar
  45. Fauvart M, Michiels J (2008) Rhizobial secreted proteins as determinants of host specificity in the Rhizobium-legume symbiosis. FEMS Microbiol Lett 285:1–9PubMedCrossRefGoogle Scholar
  46. Ferguson BJ, Beveridge CA (2009) Roles for auxin, cytokinin, and strigolactone in regulating shoot branching. Plant Physiol 149:1929–1944PubMedCrossRefGoogle Scholar
  47. Figueiredo MVB, Seldin L, de Araujo FF, Mariano RLR (2010) Plant growth promoting rhizobacteria: fundamentals and applications. In: Maheshwari D (ed) Plant growth and health promoting bacteria. Springer, Berlin/HeidelbergGoogle Scholar
  48. Fischer S, Miguel M, Mori G (2003) Effect of root exudates on the exopolysaccharide composition and the lipopolysaccharide profile of Azospirillum brasilense Cd under saline stress. FEMS Microbiol Lett 219:53–62PubMedCrossRefGoogle Scholar
  49. Fournier J, Timmers A, Sieberer B, Jauneau A, Chabaud M, Barker D (2008) Mechanism of infection thread elongation in root hairs of Medicago truncatula and dynamic interplay with associated Rhizobial colonization. Plant Physiol 148:1985–1995PubMedCrossRefGoogle Scholar
  50. Fraysse N, Jabbouri A, Treilhou M, Couderc F, Poinsot V (2002) Symbiotic conditions induce structural modifications of Sinorhizobium sp. NGR234 surface polysaccharides. Glycobiology 12:741–748PubMedCrossRefGoogle Scholar
  51. Fraysse N, Couderc F, Poinsot V (2003) Surface polysaccharide involvement in establishing the rhizobium–legume symbiosis. Eur J Biochem 270:1365–1380PubMedCrossRefGoogle Scholar
  52. Friesen M, Porter SS, Stark SC, von Wettberg EJ, Sachs JL, Martinez-Romero E (2011) Microbially mediated plant functional traits. Annu Rev Ecol Evol Syst 42:23–46CrossRefGoogle Scholar
  53. Gao M, D’Haeze W, De Rycke R, Wolucka B, Holsters M (2001) Knockout of an azorhizobial dTDP-l-rhamnose synthase affects lipopolysaccharide and extracellular polysaccharide production and disables symbiosis with Sesbania rostrata. Mol Plant Microbe Interact 14:857–866PubMedCrossRefGoogle Scholar
  54. Gao M, Teplitski M, Robinson J, Bauer W (2003) Production of substances by Medicago truncatula that affect bacterial quorum sensing. Mol Plant Microbe Interact 16:827–834PubMedCrossRefGoogle Scholar
  55. Genre A, Bonfante P (2007) Check-in procedures for plant cell entry by biotrophic microbes. Mol Plant Microbe Interact 20:1023–1030PubMedCrossRefGoogle Scholar
  56. Geurts R, Bisseling T (2002) Rhizobium Nod factor perception and signaling. Plant Cell 14:S239–S249PubMedGoogle Scholar
  57. Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117CrossRefGoogle Scholar
  58. Govindarajan M, Balandreau J, Muthukumarasamy R, Kwon S-W, Weon H-Y, Lakshminarasimhan C (2008) Effects of the inoculation of Burkholderia vietnamiensis and related endophytic diazotrophic bacteria on grain yield of rice. Microb Ecol 55:21–37PubMedCrossRefGoogle Scholar
  59. Gray E, Smith D (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes. Soil Biol Biochem 37:395–412CrossRefGoogle Scholar
  60. Guerrero-Molina MF, Winik BC, Pedraza RO (2011) More than rhizosphere colonization of strawberry plants by Azospirillum brasilense. Appl Soil Ecol. doi: 10.1016/J.APSOIL.2011.10.011 Google Scholar
  61. Gutierrez-Luna F, Lopez-Bucio J, Altamirano-Hernández J, Valencia-Cantero E, Reyes de la Cruz H, Macías-Rodríguez L (2010) Plant growth-promoting rhizobacteria modulate root-system architecture in Arabidopsis thaliana through volatile organic compound emission. Symbiosis 51:75–83CrossRefGoogle Scholar
  62. Haggag W (2007) Colonization of exopolysaccharide-producing Paenibacillus polymyxa on peanut roots for enhancing resistance against crown rot disease. Afr J Biotechnol 6:1568–1577Google Scholar
  63. Han J, Su L, Dong X, Cai Z, Sun X, Yang H, Wang Y, Song W (2005) Characterization of a novel plant growth-promoting bacteria strain Delftia tsuruhatensis HR4 both as a diazotroph and a potential biocontrol agent against various plant pathogens. Syst Appl Microbiol 28:66–76PubMedCrossRefGoogle Scholar
  64. Hartwing UA, Maxwell CA, Joseph CM, Phillips DA (1990) Chrysoeriol and luteolin released from alfalfa seeds induce nod genes in Rhizobium meliloti. Plant Physiol 92:116–122CrossRefGoogle Scholar
  65. Hassan S, Mathesius U (2012) The role of flavonoids in root–rhizosphere signalling: opportunities and challenges for improving plant–microbe interactions. J Exp Bot 63:3429–3444PubMedCrossRefGoogle Scholar
  66. Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol. doi: 10.1007/s13213-010-0117-1 Google Scholar
  67. Heckmann AB, Sandal N, Bek AS, Madsen LH, Jurkiewicz A, Nielsen MW, Tirichine L, Stougaard J (2011) Cytokinin induction of root nodule primordia in Lotus japonicus is regulated by a mechanism operating in the root cortex. Mol Plant Microbe Interact 24:1385–1395PubMedCrossRefGoogle Scholar
  68. Held M, Hossain M, Yokota K, Bonfante P, Stougaard J, Szczyglowsk K (2010) Common and not so common symbiotic entry. Trends Plant Sci 15:540–545PubMedCrossRefGoogle Scholar
  69. Ikeda S, Okubo T, Anda M, Nakashita H, Yasuda M, Sato S, Kaneko T, Tabata T, Eda S, Momiyama A, Terasawa K, Mitsui H, Minamisawa K (2010) Community- and genome-based views of plant-associated bacteria: plant–bacterial interactions in soybean and rice. Plant Cell Physiol 51:1398–1410PubMedCrossRefGoogle Scholar
  70. Jayaraman D, Forshey KL, Grimsrud PA, Ane JM (2012) Leveraging proteomics to understand plant-microbe interactions. Front Plant Sci 3:1–6CrossRefGoogle Scholar
  71. Jofre E, Lagares A, Mori G (2004) Disruption of dTDP-rhamnose biosynthesis modifies lipopolysaccharide core, exopolysaccharide production, and root colonization in Azospirillum brasilense. FEMS Microbiol Lett 231:267–275PubMedCrossRefGoogle Scholar
  72. Kapulnik Y, Okon Y, Henis Y (1985) Changes in root morphology or wheat caused by Azospirillum inoculation. Can J Microbiol 31:881–887CrossRefGoogle Scholar
  73. Keshavan N, Chowdhary P, Haines D, Gonzalez J (2005) l-Canavanine made by Medicago sativa interferes with quorum sensing in Sinorhizobium meliloti. J Bacteriol 187:8427–8436PubMedCrossRefGoogle Scholar
  74. Khakipour N, Khavazi K, Mojallali H, Pazira E, Asadirahmani H (2008) Production of auxin hormone by fluorescent Pseudomonads. Am Eurasian J Agric Environ Sci 4:687–692Google Scholar
  75. Khalid A, Sultana S, Arshad M, Mahmood S, Mahmood T, Tariq Siddique M (2011) Performance of auxin producing rhizobacteria for improving growth and yield of wheat and rice grown in rotation under field conditions. Int J Agric Appl Sci 3:44–50Google Scholar
  76. Khan GA, Declerck M, Sorin C, Hartmann C, Crespi M, Lelandais-Briere C (2011) MicroRNAs as regulators of roots development and architecture. Plant Mol Biol 77:47–58PubMedCrossRefGoogle Scholar
  77. Kiil K, Binnewies T, Willenbrock H, Kirkelund Hansen S, Yang L, Jelsbak L, Ussery D, Friis C (2008) Comparative genomics of Pseudomonas. In: Rehm B (ed) Pseudomonas. Model organism, pathogen, cell factory. Wiley-VCH, WeinheimGoogle Scholar
  78. Kinkema M, Gresshoff PM (2008) Investigation of downstream signals of the soybean autoregulation of nodulation receptor kinase GmNARK. Mol Plant Microbe Interact 21:1337–1348PubMedCrossRefGoogle Scholar
  79. Kyungseok P, Kloepper J, Ryu C (2008) Rhizobacterial exopolysaccharides elicit induced resistance on cucumber. J Microbiol Biotechnol 18:1095–1100Google Scholar
  80. Lambrecht M, Okon Y, Vande Broek A, Vanderleyden J (2000) Indole-3-acetic acid: a reciprocal signalling molecule in bacteria–plant interactions. Trends Microbiol 8:298–300PubMedCrossRefGoogle Scholar
  81. Lang K, Lindermann A, Hauser F, Göttfert M (2008) The genistein stimulon of Bradyrhizobium japonicum. Mol Genet Genomics 279:203–211PubMedCrossRefGoogle Scholar
  82. Lee H-I, Lee J-H, Park K-H, Sangurdekar D, Chang W-S (2012) Effect of soybean coumestrol on Bradyrhizobium japonicum nodulation ability, biofilm formation, and transcriptional profile. Appl Environ Microbiol 78:2896–2903PubMedCrossRefGoogle Scholar
  83. Lim J, Kim S (2009) Synergistic plant growth promotion by the indigenous auxins-producing PGPR Bacillus subtilis AH18 and Bacillus licheniformis K11. J Korean Soc Appl Biol Chem 52:531–538CrossRefGoogle Scholar
  84. Lopez-Bucio J, Campos-Cuevas J, Hernández-Calderón E, Velásquez-Becerra C, Farías-Rodríguez R, Macías-Rodríguez L, Valencia-Cantero E (2007) Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopsis thaliana. Mol Plant Microbe Interact 20:207–217PubMedCrossRefGoogle Scholar
  85. Maj D, Wielbo J, Marek-Kozaczuk M, Skorupska A (2010) Response to flavonoids as a factor influencing competitiveness and symbiotic activity of Rhizobium leguminosarum. Microbiol Res 165:50–60PubMedCrossRefGoogle Scholar
  86. Malik D, Sindhu S (2011) Production of indole acetic acid by Pseudomonas sp.: effect of coinoculation with Mesorhizobium sp. Cicer on nodulation and plant growth of chickpea (Cicer arietinum). Physiol Mol Biol Plant 17:25–32CrossRefGoogle Scholar
  87. Mandal S, Chakraborty D, Dey S (2010) Phenolic acids act as signaling molecules in plant-microbe symbioses. Plant Signal Behav 5:359–368PubMedCrossRefGoogle Scholar
  88. Masson-Boivin C, Giraud E, Perret X, Batut J (2009) Establishing nitrogen-fixing symbiosis with legumes: how many Rhizobium recipes? Trends Microbiol 17:458–466PubMedCrossRefGoogle Scholar
  89. Mathesius U (2009) Comparative proteomic studies of root-microbe interactions. J Proteomics 72:353–366PubMedCrossRefGoogle Scholar
  90. Mathis R, Van Gijsegem F, De Rycke R, D’Haeze W, Van Maelsaeke E, Anthonio E, Van Montagu M, Holsters M, Vereecke D (2005) Lipopolysaccharides as a communication signal for progression of legume endosymbiosis. Proc Natl Acad Sci USA 102:2655–2660PubMedCrossRefGoogle Scholar
  91. Maxwell CA, Hartwing UA, Joseph CM, Phillips DA (1989) A chalcone and two related flavonoids released from alfalfa roots induce nod genes of Rhizobium meliloti. Plant Physiol 91:842–847PubMedCrossRefGoogle Scholar
  92. Medeot DB, Paulicci NS, Albornoz AI, Fumero MV, Bueno MA, Garcia MB, Woelke MR, Okon Y, Dardanelli MS (2010) Plant growth promoting rhizobacteria improving the legume-rhizobia symbiosis. In: Khan MS, Zaidi A, Musarrat J (eds) Microbes for legume improvement. Springer, New York, pp 473–494CrossRefGoogle Scholar
  93. Miyazawa H, Oka-Kira E, Sato N, Takahashi H, Wu G-J, Sato S, Hayashi M, Betsuyaku S, Nakazono M, Tabata S, Harada K, Sawa S, Fukuda H, Kawaguchi M (2010) The receptor-like kinase KLAVIER mediates systemic regulation of nodulation and non-symbiotic shoot development in Lotus japonicus. Development 137:4317–4325PubMedCrossRefGoogle Scholar
  94. Morel MA, Ubalde M, Braña V, Castro-Sowinski S (2011) Delftia sp. JD2: a potential Cr(VI)-reducing agent with plant growth-promoting activity. Arch Microbiol 193:163–168CrossRefGoogle Scholar
  95. Morel M, Braña V, Castro-Sowinski S (2012) Legume crops, importance and use of bacterial inoculation to increase the production. In: Goyal A (ed) Crop plant. InTech, Rijeka, pp 217–240Google Scholar
  96. Murray JD, Karas BJ, Sato S, Tabata S, Amyot L, Szczyglowski K (2007) A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315:101–104PubMedCrossRefGoogle Scholar
  97. Oka-Kira E, Kawaguchi M (2006) Long-distance signaling to control root nodule number. Curr Opin Plant Biol 9:496–502PubMedCrossRefGoogle Scholar
  98. Okon Y, Kapulnik Y (1986) Development and function of Azospirillum-inoculated roots. Plant Soil 90:3–16CrossRefGoogle Scholar
  99. Okon Y, Labandera-Gonzalez C (1994) Agronomic applications of Azospirillum: an evaluation of 20 years worldwide field inoculation. Soil Biol Biochem 26:1591–1601CrossRefGoogle Scholar
  100. Okumoto S, Pilot G (2011) Amino acid export in plants: a missing link in nitrogen cycling. Mol Plant 4:453–463PubMedCrossRefGoogle Scholar
  101. Oldroyd GE (2007) Plant science nodules and hormones. Science 315:52–53PubMedCrossRefGoogle Scholar
  102. Oldroyd GE, Downie A (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546PubMedCrossRefGoogle Scholar
  103. Oldroyd G, Murray J, Poole P, Downie A (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45:119–144PubMedCrossRefGoogle Scholar
  104. Op den Camp R, De Mita S, Lillo A, Cao Q, Limpens E, Bisseling T, Geurts R (2011) A phylogenetic strategy based on a legume-specific whole genome duplication yields symbiotic cytokinin type-A response regulators. Plant Physiol 157:2013–2022PubMedCrossRefGoogle Scholar
  105. Ortiz-Castro R, Martinez-Trujillo M, Lopez-Bucio J (2008a) N-acyl-l-homoserine lactones: a class of bacterial quorum-sensing signals alters post-embryonic root development in Arabidopsis thaliana. Plant Cell Environ 31:1497–1509PubMedCrossRefGoogle Scholar
  106. Ortiz-Castro R, Valencia-Cantero E, Lopez-Bucio J (2008b) Plant growth promotion by Bacillus megaterium involves cytokinin signaling. Plant Signal Behav 3:263–265PubMedCrossRefGoogle Scholar
  107. Ortiz-Castro R, Contreras-Cornejo HA, Macías-Rodríguez L, Lopez-Bucio J (2009) The role of microbial signals in plant growth and development. Plant Signal Behav 4:701–712PubMedCrossRefGoogle Scholar
  108. Pallai R, Hynes RK, Verma B, Nelson LM (2012) Phytohormone production and colonization of canola (Brassica napus L.) roots by Pseudomonas fluorescens 6–8 under gnotobiotic conditions. Can J Microbiol 58:170–178PubMedCrossRefGoogle Scholar
  109. Parada M, Vinardell J, Ollero F, Hidalgo A, Gutiérrez R, Buendía-Clavería A, Lei W, Margaret I, López-Baena F, Gil-Serrano A, Rodríguez-Carvajal M, Moreno J, Ruiz-Sainz J (2006) Sinorhizobium fredii HH103 mutants affected in capsular polysaccharide (KPS) are impaired for nodulation with soybean and Cajanus cajan. Mol Plant Microbe Interact 19:43–52PubMedCrossRefGoogle Scholar
  110. Parmar N, Dadarwal K (1999) Stimulation of nitrogen fixation and induction of flavonoid-like compounds by rhizobacteria. J Appl Microbiol 86:36–44CrossRefGoogle Scholar
  111. Parmar N, Dufresne J (2011) Beneficial interactions of plant growth promoting rhizosphere microorganisms. In: Singh A et al (eds) Bioaugmentation, biostimulation and biocontrol. Springer, Berlin/Heidelberg, pp 27–42CrossRefGoogle Scholar
  112. Peck MC, Fisher RF, Long SR (2006) Diverse flavonoids stimulate NodD1 binding to nod gene promoters in Sinorhizobium meliloti. J Bacteriol 188:5417–5427PubMedCrossRefGoogle Scholar
  113. Peters NK, Frost JW, Long SR (1986) A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233:977–980PubMedCrossRefGoogle Scholar
  114. Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5:237–243PubMedCrossRefGoogle Scholar
  115. Pieterse C, Leon-Reyes A, Van der Ent S, Van Wees S (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–317PubMedCrossRefGoogle Scholar
  116. Ping L, Boland W (2004) Signals from the underground: bacteria volatiles promote growth in Arabidopsis. Trends Plant Sci 9:263–266PubMedCrossRefGoogle Scholar
  117. Popp C, Ott T (2011) Regulation of signal transduction and bacterial infection during root nodule symbiosis. Curr Opin Plant Biol 14:458–467PubMedCrossRefGoogle Scholar
  118. Quagliotto L, Azziz G, Bajsa N, Vaz P, Pérez C, Ducamp F, Cadenazzi M, Altier N, Arias A (2009) Three native Pseudomonas fluorescens strains tested under growth chamber and field conditions as biocontrol agents against damping-off in alfalfa. Biol Control 51:42–50CrossRefGoogle Scholar
  119. Qurashi A, Sabri A (2012) Bacterial exopolysaccharide and biofilm formation stimulate chickpea growth and soil aggregation under salt stress. Braz J Microbiol 43(3):1183–1191CrossRefGoogle Scholar
  120. Ramos Solano B, Barriuso J, Gutierrez Mañero J (2009) Biotechnology of the rhizosphere. In: Kirakosyan A, Kaufman PB (eds) Recent advances in plant biotechnology. Springer, Dordrecht/New York, p 137CrossRefGoogle Scholar
  121. Reis V, dos Santos Teixeira KR, Pedraza RO (2011) What is expected from the genus Azospirillum as a plant growth-promoting bacteria? In: Maheshwari DK (ed) Bacteria in agrobiology: plant growth responses. Springer, Berlin/Heidelberg, pp 123–138CrossRefGoogle Scholar
  122. Remans R, Croonenborghs A, Torres Gutierrez R, Michiels J, Vanderleyden J (2007) Effects of plant growth-promoting rhizobacteria on nodulation of Phaseolus vulgaris L. are dependent on plant nutrition. Eur J Plant Pathol 119:341–351CrossRefGoogle Scholar
  123. Remans R, Ramaekers L, Schelkens S, Hernandez G, Garcia A, Reyes J, Mendez N, Toscano V, Mulling M, Galvez L, Vanderleyden J (2008) Effect of Rhizobium-Azospirillum coinoculation on nitrogen fixation and yield of two contrasting Phaseolus vulgaris L. genotypes cultivated across different environments in Cuba. Plant Soil 312:25–37CrossRefGoogle Scholar
  124. Reuhs B, Kim J, Badgett A, Carlson R (1994) Production of cell-associated polysaccharides of Rhizobium fredii USDA205 is modulates by apigenin and host root extract. Mol Plant Microbe Interact 7:240–247PubMedCrossRefGoogle Scholar
  125. Robert-Seilaniantz A, Navarro L, Bari R, Jones JDG (2007) Pathological hormone imbalances. Curr Opin Plant Biol 10:372–379PubMedCrossRefGoogle Scholar
  126. Robledo M, Jimenez-Zurdo JI, Velazquez E et al (2008) Rhizobium cellulase CelC2 is Essentials for primary symbiotic infection of legume host roots. Proc Natl Acad Sci USA 105:7064–7069PubMedCrossRefGoogle Scholar
  127. Rodriguez-Navarro DN, Dardanelli MS, Ruíz-Saínz J (2007) Attachment of bacteria to the roots of higher plants. FEMS Microbiol Lett 272:127–136PubMedCrossRefGoogle Scholar
  128. Rosas S, Andrés J, Rovera M, Correa N (2006) Phosphate-solubilizing Pseudomonas putida can influence the rhizobia-legume symbiosis. Soil Biol Biochem 38:3502–3505CrossRefGoogle Scholar
  129. Russo DM, Williams A, Edwards A et al (2006) Proteins exported via de PrsD-PrsE type I secretion system and the acidic exopolysaccharide are involved in biofilm formation by Rhizobium leguminosarum. J Bacteriol 188:4474–4486PubMedCrossRefGoogle Scholar
  130. Ryu C, Farag M, Paré P, Kloepper J (2005) Invisible signals from the underground: bacterial volatiles elicit plant growth promotion and induce systemic resistance. Plant Pathol J 21:7–12CrossRefGoogle Scholar
  131. Saeki K (2011) Rhizobial measures to evade host defense strategies and endogenous threats to persistent symbiotic nitrogen fixation: a focus on two legume-rhizobium model systems. Cell Mol Life Sci 68:1327–1339PubMedCrossRefGoogle Scholar
  132. Schuhegger R, Ihring A, Gantner S, Bahnweg G, Knappe C, Vogg G, Hutzler H, Schmid M, Van Breusegem F, Eberl L, Hartmann A, Langebartel C (2006) Induction of systemic resistance in tomato by N-acyl-L homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ 29:909–918PubMedCrossRefGoogle Scholar
  133. Shaw L, Burns R (2003) Biodegradation of organic pollutants in the rhizosphere. Adv Appl Microbiol 53:1–60PubMedCrossRefGoogle Scholar
  134. Shaw LJ, Morris P, Hooker JE (2006) Perception and modification of plant flavonoid signals by rhizosphere microorganisms. Environ Microbiol 8:1867–1880PubMedCrossRefGoogle Scholar
  135. Silby MW, Cerdeño-Tárraga AM, Vernikos GS, Giddens SR, Jackson RW, Preston GM, Zhang XX, Moon CD, Gehring SM, Godfrey SAC, Knight CG, Malone JG, Robinson Z, Spiers AJ, Harris S, Challis GL, Yaxley AM, Harris D, Seeger K, Murphy L, Rutter S, Squares R, Quail MA, Saunders E, Mavromatis K, Brettin TS, Bentley SD, Hothersall J, Stephens E, Thomas CM, Parkhill J, Levy SB, Rainey PB, Thomson NR (2009) Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens. Genome Biol 10(5):R51PubMedCrossRefGoogle Scholar
  136. Simon SA, Meyers BC, Sherrier J (2009) MicroRNAs in the rhizobia legume symbiosis. Plant Physiol 151:1002–1008PubMedCrossRefGoogle Scholar
  137. Smit G, Swant S, Lugtenberg BJJ, Kijne JW (1992) Molecular mechanisms of attachment of Rhizobium bacteria to plant roots. Mol Microbiol 6:2897–2903PubMedCrossRefGoogle Scholar
  138. Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448PubMedCrossRefGoogle Scholar
  139. Spaepen S, Dobbelaere S, Croonenborghs A, Vanderleyden J (2008) Effects of Azospirillum brasilense indole-3-acetic acid production on inoculated wheat plants. Plant Soil 312:15–23CrossRefGoogle Scholar
  140. Stacey G, Libault M, Brechenmacher L, Wan J, May GD (2006) Genetics and functional genomics of legume nodulation. Curr Opin Plant Biol 9:110–121PubMedCrossRefGoogle Scholar
  141. Staehelin C, Xie Z-P, Illana A, Vierheiling H (2011) Long-distance transport of signals during symbiosis. Plant Signal Behav 6:372–377PubMedCrossRefGoogle Scholar
  142. Star L, Matan O, Dardanelli MS, Kapulnik Y, Burdman S, Okon Y (2012) The Vicia sativa spp. nigra-Rhizobium leguminosarum bv. viciae symbiotic interaction is improved by Azospirillum brasilense. Plant Soil 356:165–174CrossRefGoogle Scholar
  143. Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T, Toussaint JP, Vierheilig H (2007) Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12:1290–1306PubMedCrossRefGoogle Scholar
  144. Sun J, Cardoza V, Mitchell D, Bright L, Oldroyd G, Harris J (2006) Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation. Plant J 46:961–970PubMedCrossRefGoogle Scholar
  145. Sutton JM, Lea EJ, Downie JA (1994) The nodulation-signaling protein NodO from Rhizobium leguminosarum biovar viciae forms ion channels in membranes. Proc Natl Acad Sci USA 91:9990–9994PubMedCrossRefGoogle Scholar
  146. Tirichine L, Sandal N, Madsen L, Radutoiu S, Albrektsen AS, Sato S, Asamizu E, Tabata S, Stougaard J (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315:104–107PubMedCrossRefGoogle Scholar
  147. Tortora ML, Dıaz-Ricci JC, Pedraza RO (2011) Azospirillum brasilense siderophores with antifungal activity against Colletotrichum acutatum. Arch Microbiol 193:275–286PubMedCrossRefGoogle Scholar
  148. Troch E, Vanderleyden J (1996) Surface properties and motility of Rhizobium and Azospirillum in relation to plant root attachment. Microb Ecol 32:149–169PubMedCrossRefGoogle Scholar
  149. Tseng T-T, Tyler BM, Setubal JC (2009) Protein secretion systems in bacterial-host associations, and their description in the gene ontology. BMC Microbiol 9:S2PubMedCrossRefGoogle Scholar
  150. Tsuchiya Y, McCourt P (2009) Strigolactones: a new hormone with a past. Curr Opin Plant Biol 12:556–561PubMedCrossRefGoogle Scholar
  151. Tsuneda S, Aikawa H, Hayashi H, Yuasa A, Hirata A (2003) Extracellular polymeric substances responsible for bacterial adhesion onto solid surface. FEMS Microbiol Lett 223:287–292PubMedCrossRefGoogle Scholar
  152. Ubalde M, BrañaV SF, Morel M, Martínez-Rosales C, Marquez C, Castro-Sowinski S (2012) The versatility of Delftia sp. isolates as tools for bioremediation and biofertilization technologies. Curr Microbiol 64(6):597–603PubMedCrossRefGoogle Scholar
  153. Upadhyay S, Singh JS, Singh DP (2011) Exopolysaccharide-producing plant growth-promoting rhizobacteria under salinity condition. Pedosphere 21(2):214–222CrossRefGoogle Scholar
  154. Van de Velde W, Zehirov G, Szatmari A, Debreczeny M, Ishihara H, Kevei Z, Farkas A, Mikulass K, Nagy A, Tiricz H, Satiat-Jeunemaître B, Alunni B, Bourge M, Kucho K-I, Abe M, Kereszt A, Maroti G, Uchiumi T, Kondorosi E, Mergaert P (2010) Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327:1122–1126PubMedCrossRefGoogle Scholar
  155. van Noorden GE, Kerim T, Goffard N, Wiblin R, Pellerone FI, Rolfe BG, Mathesius U (2007) Overlap of proteome changes in Medicago truncatula in response to auxin and Sinorhizobium meliloti. Plant Physiol 144:1115–1131PubMedCrossRefGoogle Scholar
  156. Vandeputte O, Kiendrebeogo M, Rajaonson S, Diallo B, Mol A, El Jaziri M, Baucher M (2010) Identification of catechin as one of the factors in Pseudomonas aeruginosa PAO1 of quorum-sensing-controlled virulence bark extract that reduces the production flavonoids from Combretum albiflorum. Appl Environ Microbiol 76:243–253PubMedCrossRefGoogle Scholar
  157. Voinnet O (2008) Post-transcriptional RNA silencing in plant-microbe interactions: a touch of robustness and versatility. Curr Opin Plant Biol 11:464–470PubMedCrossRefGoogle Scholar
  158. Volpin H, Burdman S, Castro-Sowinski S, Kapulnik Y, Okon Y (1996) Inoculation with Azospirillum increased exudation of rhizobial nod-gene inducers by alfalfa roots. Mol Plant Microbe Interact 9:388–394CrossRefGoogle Scholar
  159. von Rad U, Klein I, Dobrev PI, Kottova J, Zazimalova E, Fekete A, Hartmann A, Schmitt-Kopplin P, Durner J (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
  160. Wani P, Khan MS, Zaidi A (2007) Synergistic effects of the inoculation with nitrogen-fixing and phosphate-solubilizing rhizobacteria on the performance on field-grown chickpea. J Plant Nutr Soil Sci 170:283–287CrossRefGoogle Scholar
  161. Yadegari M, Rahmani HA, Noormohammadi G, Ayneband A (2010) Plant growth promoting rhizobacteria increase growth, yield and nitrogen fixation in Phaseolus vulgaris. J Plant Nutr 33:1733–1743CrossRefGoogle Scholar
  162. Yoshimitsu Y, Tanaka K, Fukuda W, Asami T, Yoshida S, Hayashi K, Kamiya Y, Jikumaru Y, Shigeta T, Nakamura Y, Matsuo T, Okamoto S (2011) Transcription of DWARF4 plays a crucial role in auxin-regulated root elongation in addition to Brassinosteroid homeostasis in Arabidopsis thaliana. PLoS One 6(8):e23851PubMedCrossRefGoogle Scholar

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© Springer India 2013

Authors and Affiliations

  1. 1.Laboratory of Molecular MicrobiologyClemente Estable Institute of Biological ResearchMontevideoUruguay
  2. 2.Department of Biochemistry and Molecular Biology, Faculty of ScienceUniversity of the RepublicMontevideoUruguay

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