Rhizosphere Interactions: Life Below Ground

  • Kalaivani K. NadarajahEmail author


The interface between roots and soil is a region with high interaction among a myriad of organisms that affect biogeochemical cycles, plant growth, and stress tolerance. Similarly chemical compounds secreted within the rhizosphere act as attractants to microorganisms. Due to its dynamic nature and complexity, understanding rhizospheric biology and activity is essential in ensuring improved plant function and productivity within an ecosystem. Sustainable agricultural practices are dependent on studies conducted with regards to plant–microbe interactions in the rhizosphere. This chapter is an exposition of rhizospheric interactions spanning the chemistry of exudates and signals that contribute towards the complexity of the rhizosphere. The information derived from recent studies and the utilization of current technological platforms will enable us to explore and gather more information at the plant and microbiome level.


Root Exudate Switch Grass Quorum Sense Rosmarinic Acid Diffusible Signaling Factor 
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.


  1. Akiyama K, Matsuzaki K-I, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435(7043):824–827. doi: 10.1038/nature03608, PMID: 15944706PubMedCrossRefGoogle Scholar
  2. Argueso CT, Hansen M, Kieber JJ (2007) Regulation of ethylene biosynthesis. J Plant Growth Regul 26(2):92–105. doi: 10.1007/s00344-007-0013-5 CrossRefGoogle Scholar
  3. Arshad M, Shaharoona B, Mahmood T (2008) Inoculation with Pseudomonas spp. containing ACC-deaminase partially eliminates the effects of drought stress on growth, yield, and ripening of pea (Pisum sativum L.). Pedosphere 18(5):611–620. doi: 10.1016/S1002-0160(08)60055-7 CrossRefGoogle Scholar
  4. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32(6):666–681. doi: 10.1111/j.1365-3040.2009.01926.x, PMID: 19143988PubMedCrossRefGoogle Scholar
  5. Badri DV, Loyola-Vargas VM, Broeckling CD et al (2008) Altered profile of secondary metabolites in the root exudates of Arabidopsis ATP-binding cassette transporter mutants. Plant Physiol 146(2):762–771PubMedPubMedCentralCrossRefGoogle Scholar
  6. Badri DV, Quintana N, El Kassis EG et al (2009a) An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota. Plant Physiol 151(4):2006–2017. doi: 10.1104/pp.109.147462, PMID: 19854857PubMedPubMedCentralCrossRefGoogle Scholar
  7. Badri DV, Weir TL, van der Lelie D et al (2009b) Rhizosphere chemical dialogues: plant–microbe interactions. Curr Opin Biotechnol 20(6):642–650. doi: 10.1016/j.copbio.2009.09.014, PMID: 19875278PubMedCrossRefGoogle Scholar
  8. Badri DV, Chaparro JM, Zhang R et al (2013a) Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288(7):4502–4512. doi: 10.1074/jbc.M112.433300, PMID: 23293028PubMedPubMedCentralCrossRefGoogle Scholar
  9. Badri DV, Zolla G, Bakker MG et al (2013b) Potential impact of soil microbiomes on the leaf metabolome and on herbivore feeding behavior. New Phytol 198(1):264–273. doi: 10.1111/nph.12124, PMID: 23347044PubMedCrossRefGoogle Scholar
  10. Bais HP, Walker TS, Schweizer HP et al (2002) Root specific elicitation and antimicrobial activity of rosmarinic acid in hairy root cultures of sweet basil (Ocimum basilicum L.). Plant Physiol Biochem 40:983–995CrossRefGoogle Scholar
  11. Bais HP, Weir TL, Perry LG et al (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57(1):233–266. doi: 10.1146/annurev.arplant.57.032905.105159, PMID: 16669762PubMedCrossRefGoogle Scholar
  12. Bakker M, Manter D, Sheflin A et al (2012) Harnessing the rhizosphere microbiome through plant breeding and agricultural management. Plant Soil 360(1–2):1–13. doi: 10.1007/s11104-012-1361-x CrossRefGoogle Scholar
  13. Bakker PAHM, Berendsen RL, Doornbos RF et al (2013) The rhizosphere revisited: root microbiomics. Front Plant Sci 4(165). doi: 10.3389/fpls.2013.00165
  14. Battey NH, Blackbourn HD (1993) The control of exocytosis in plant cells. New Phytol 125:307–308CrossRefGoogle Scholar
  15. Bednarek P, Osbourn A (2009) Plant-microbe interactions: chemical diversity in plant defense. Science 324:746–748. doi: 10.1126/science.1171661 PubMedCrossRefGoogle Scholar
  16. Behie SW, Zelisko PM, Bidochka MJ (2012) Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science 336(6088):1576–1577. doi: 10.1126/science.1222289, PMID: 22723421PubMedCrossRefGoogle Scholar
  17. Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17(8):478–486. doi: 10.1016/j.tplants.2012.04.001, PMID: 22564542PubMedCrossRefGoogle Scholar
  18. Brakhage AA, Schroeckh V (2011) Fungal secondary metabolites – strategies to activate silent gene clusters. Fungal Genet Biol 48:15–22. doi: 10.1016/j.fgb.2010.04.004 PubMedCrossRefGoogle Scholar
  19. Buttner M (2007) The monosaccharide transporter (−like) gene family in Arabidopsis. FEBS Letters 581:2318–2324PubMedCrossRefGoogle Scholar
  20. Cai T, Cai W, Zhang J et al (2009) Host legume-exuded antimetabolites optimize the symbiotic rhizosphere. Mol Microbiol 73(3):507–517. doi: 10.1111/j.1365-2958.2009.06790.x, PMID: 19602148PubMedCrossRefGoogle Scholar
  21. Cannesan MA, Durand C, Burel C et al (2012) Effect of Arabinogalactan Proteins from the root caps of pea and Brassica napus on Aphanomyces euteiches zoospore chemotaxis and germination. Plant Physiol 159(4):1658–1670. doi: 10.1104/pp.112.198507, PMID: 22645070PubMedPubMedCentralCrossRefGoogle Scholar
  22. Chaparro JM, Badri DV, Bakker MG et al (2013a) Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with soil microbial functions. PloS ONE 8(2):e55731. doi: 10.1371/journal.pone.0055731, PMID: 23383346PubMedPubMedCentralCrossRefGoogle Scholar
  23. Chaparro JM, Badri DV, Vivanco JM (2013b) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8(4):790–803. doi: 10.1038/ismej.2013.196 PubMedPubMedCentralCrossRefGoogle Scholar
  24. Charmont S, Jamet E, Pont-Lezica R et al (2005) Proteomic analysis of secreted proteins from Arabidopsis thaliana seedlings: improved recovery following removal of phenolic compounds. Phytochemistry 66(4):453–461. doi: 10.1016/j.phytochem.2004.12.013, PMID: 15694452PubMedCrossRefGoogle Scholar
  25. Chevrot R, Rosen R, Haudecoeur E et al (2006) GABA controls the level of quorum-sensing signal in Agrobacterium tumefaciens. Proc Natl Acad Sci USA 103:7460–7464. doi: 10.1073/pnas.0600313103 PubMedPubMedCentralCrossRefGoogle Scholar
  26. Choi O, Kim JG, Joeng Y et al (2008) Pyrroloquinoline quinine is a plant growth promotion factor by Pseudomonas fluorescens B16. Plant Physiol 146:657–668PubMedPubMedCentralCrossRefGoogle Scholar
  27. Colangelo EP, Guerinot ML (2006) Put the metal to the petal: metal uptake and transport throughout plants. Curr Opin Plant Biol 9:322–330PubMedCrossRefGoogle Scholar
  28. Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42(5):669–678. doi: 10.1016/j.soilbio.2009.11.024 CrossRefGoogle Scholar
  29. Coronado C, Zuanazzi J, Sallaud C et al (1995) Alfalfa root flavonoid production is nitrogen regulated. Plant Physiol 108(2):533–542. doi: 10.1104/pp.108.2.533, PMID: 12228491PubMedPubMedCentralCrossRefGoogle Scholar
  30. Czarnota MA, Paul RN, Weston LA et al (2003) Anatomy of sorgoleone-secreting root hairs of Sorghum species. Int J Plant Sci 164:861–866CrossRefGoogle Scholar
  31. Daniels R, De Vos DE, Desair J et al (2002) The cin quorum sensing locus of Rhizobium etli CNPAF512 affects growth and symbiotic nitrogen fixation. J Biol Chem 277(1):462–468. doi: 10.1074/jbc.M106655200 PubMedCrossRefGoogle Scholar
  32. De Hoff P, Brill L, Hirsch A (2009) Plant lectins: the ties that bind in root symbiosis and plant defense. Mol Genet Genomics 282(1):1–15. doi: 10.1007/s00438-009-0460-8 PubMedPubMedCentralCrossRefGoogle Scholar
  33. de Weert S, Vermeiren H, Mulders IHM et al (2002) Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens. Mol Plant Microbe In 15(11):1173–1180. doi: 10.1094/MPMI.2002.15.11.1173, PMID: 12423023CrossRefGoogle Scholar
  34. De-la-Peña C, Lei Z, Watson BS et al (2008) Root – microbe communication through protein secretion. J Biol Chem 283(37):25247–25255. doi: 10.1074/jbc.M801967200, PMID: 18635546PubMedCrossRefGoogle Scholar
  35. De-la-Peña C, Badri DV, Lei Z et al (2010) Root secretion of defense-related proteins is development-dependent and correlated with flowering time. J Biol Chem 285(40):30654–30665. doi: 10.1074/jbc.M110.119040, PMID: 20682788PubMedPubMedCentralCrossRefGoogle Scholar
  36. Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in determining the structure of rhizosphere bacterial communities? FEMS Microbiol Ecol 72:313–327PubMedCrossRefGoogle Scholar
  37. Elad Y, Barak R, Chet I et al (2008) Ultra structural studies of the interaction between Trichoderma spp. and plant pathogenic fungi. J Phytopathol 107:168–175. doi: 10.1111/j.1439-0434.1983.tb00064.x CrossRefGoogle Scholar
  38. Fan TWM, Lane AN, Shenkar M et al (2001) Comprehensive chemical profiling of gramineous plant root exudates using high-resolution NMR and MS. Phytochem 57:209–221CrossRefGoogle Scholar
  39. Fang W, St. Leger RJ (2010) Mrt, a gene unique to fungi, encodes an oligosaccharide transporter and facilitates rhizosphere competency in Metarhizium robertsii. Plant Physiol 154(3):1549–1557. doi: 10.1104/pp.110.163014, PMID: 20837701PubMedPubMedCentralCrossRefGoogle Scholar
  40. Fellbaum CR, Gachomo EW, Beesetty Y et al (2012) Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci 109(7):2666–2671. doi: 10.1073/pnas.1118650109, PMID: 22308426PubMedPubMedCentralCrossRefGoogle Scholar
  41. Field B, Jordan F, Osbourn A (2006) First encounters – deployment of defence-related natural products by plants. New Phytol 172:193–207PubMedCrossRefGoogle Scholar
  42. Furukawa J, Yamaji N, Wang H et al (2007) An aluminum-activated citrate transporter in barley. Plant Cell Physiol 48(8):1081–1091. doi: 10.1093/pcp/pcm091, PMID: 17634181PubMedCrossRefGoogle Scholar
  43. Gao M, Teplitski M, Robinson JB et al (2003) Production of substances by Medicago truncatula that affect bacterial quorum sensing. Mol Plant Microbe In 16(9):827–834. doi: 10.1094/MPMI.2003.16.9.827 CrossRefGoogle Scholar
  44. Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251(1):1–7. doi: 10.1016/j.femsle.2005.07.030, PMID: 16099604PubMedCrossRefGoogle Scholar
  45. Grotewold E (2004) The challenges of moving chemicals within and out of cells: insights into the transport of plant natural products. Planta 219:906–909PubMedCrossRefGoogle Scholar
  46. Guiñazú L, Andrés J, Del Papa M et al (2010) Response of alfalfa (Medicago sativa L.) to single and mixed inoculation with phosphate-solubilizing bacteria and Sinorhizobium meliloti. Biol Fertil Soils 46(2):85–190. doi: 10.1007/s00374-009-0408-5 CrossRefGoogle Scholar
  47. Hamer U, Marschner B (2005) Priming effects in different soil types induced by fructose, alanine, oxalic acid and catechol additions. Soil Biol and Biochem 37:445. doi: 10.1016/j.soilbio.2004.07.037 CrossRefGoogle Scholar
  48. Hartmann A, Rothballer M, Schmid M (2008) Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil 312(1–2):7–14. doi: 10.1007/s11104-007-9514-z CrossRefGoogle Scholar
  49. Haudecoeur E, Planamente S, Cirou A et al (2009) Proline antagonizes GABA-induced quenching of quorum-sensing in Agrobacterium tumefaciens. Proc Natl Acad Sci USA 106:14587–14592. doi: 10.1073/pnas.0808005106 PubMedPubMedCentralCrossRefGoogle Scholar
  50. Hirner A, Ladwig F, Stransky H et al (2006) Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. The Plant Cell 18:1931–1946PubMedPubMedCentralCrossRefGoogle Scholar
  51. Hoffmeister D, Keller NP (2007) Natural products of filamentous fungi: enzymes, genes, and their regulation. Nat Prod Rep 24:393–416. doi: 10.1128/EC.5.4.613-619.2006 PubMedCrossRefGoogle Scholar
  52. Hogan DA (2006) Talking to themselves: autoregulation and quorum sensing in fungi. Eukaryot Cell 5(4):613–619. doi: 10.1128/EC.5.4.613-619.2006 PubMedPubMedCentralCrossRefGoogle Scholar
  53. Horiuchi J-I, Prithiviraj B, Bais H et al (2005) Soil nematodes mediate positive interactions between legume plants and rhizobium bacteria. Planta 222(5):848–857. doi: 10.1007/s00425-005-0025-y, PMID: 16025342PubMedCrossRefGoogle Scholar
  54. Huang XF, Chaparro JM, Reardon KF et al (2014) Rhizosphere interactions: root exudates, microbes, and microbial communities. Botany 92:267–275. CrossRefGoogle Scholar
  55. Ishimaru Y, Kakei Y, Shimo H et al (2011) A rice phenolic efflux transporter is essential for solubilizing precipitated apoplasmic iron in the plant stele. J Biol Chem 286(28):24649–24655. doi: 10.1074/jbc.M111.221168, PMID:21602276PubMedPubMedCentralCrossRefGoogle Scholar
  56. Jansson JK, Neufeld JD, Moran MA et al (2011) Omics for understanding microbial functional dynamics. Environ Microbiol 14(1):1–3. doi: 10.1111/j.1462-2920.2011.02518.x PubMedCrossRefGoogle Scholar
  57. Jones KM, Sharopova N, Lohar DP et al (2008) Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant. Proc Natl Acad Sci USA 105(2):704–709. doi: 10.1073/pnas.0709338105 PubMedPubMedCentralCrossRefGoogle Scholar
  58. Juan Z, Subramanian S, Zhang Y et al (2007) Flavone Synthases from Medicago truncatula are flavanone-2-hydroxylases and are important for nodulation. Plant Physiol 144:741–751CrossRefGoogle Scholar
  59. Kardol P, Cornips NJ, van Kempen MML et al (2007) Microbe-mediated plant–soil feedback causes historical contingency effects in plant community assembly. Ecol Monogr 77:147–162CrossRefGoogle Scholar
  60. Kiers ET, Duhamel M, Beesetty Y et al (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333(6044):880–882. doi: 10.1126/science.1208473, PMID: 21836016PubMedCrossRefGoogle Scholar
  61. Kim SA, Guerinot ML (2007) Mining iron: iron uptake and transport in plants. FEBS Letters 581(12):2273–2280. doi: 10.1016/j.febslet.2007.04.043 PubMedCrossRefGoogle Scholar
  62. Kim JG, Park BK, Kim SU et al (2006) Bases of biocontrol: sequence predicts synthesis and mode of action of agrocin 84, the Trojan Horse antibiotic that controls crown gall. Proc Natl Acad Sci USA 103(23):8846–8851PubMedPubMedCentralCrossRefGoogle Scholar
  63. Klepek YS, Geiger D, Stadler R et al (2005) Arabidopsis polyol transporters, a new member of the monosaccharide transporter-like superfamily, mediates H + −symport of numerous substrates including myo-inositol, glycerol and ribose. The Plant Cell 17:204–218PubMedPubMedCentralCrossRefGoogle Scholar
  64. Kobae Y, Sekino T, Yoshioka H et al (2006) Loss ofAtPDR8, a plasma membrane ABC transporter of Arabidopsis thaliana, causes hypersensitive cell death upon pathogen infection. Plant Cell Physiol 47:309–318PubMedCrossRefGoogle Scholar
  65. Kumar R, Bhatia R, Kukreja K et al (2007) Establishment of Azotobacter on plant roots: chemotactic response, development and analysis of root exudates of cotton (Gossypium hirsutum L.) and wheat (Triticum aestivum L.). J Basic Microbiol 47:436–439PubMedCrossRefGoogle Scholar
  66. Kuzyakov Y (2002) Review: factors affecting rhizosphere priming effects. J Plant Nutr Soil Sc 165(4):382–396CrossRefGoogle Scholar
  67. Lambrecht M, Okon Y, Vande BA et al (2000) Indole-3-acetic acid: a reciprocal signalling molecule in bacteria-plant interactions. Trends Microbiol 8:298–300PubMedCrossRefGoogle Scholar
  68. Lee YH, Foster J, Chen J et al (2007) AAP1 transports uncharged amino acids into roots of Arabidopsis. The Plant Journal 50:305–319PubMedCrossRefGoogle Scholar
  69. Leyval C, Berthelin J (1993) Rhizodeposition and net release of soluble organic compounds by pine and beech seedlings inoculated with rhizobacteria and ectomycorrhizal fungi. Biol Fertil Soils 15(4):259–267. doi: 10.1007/bf00337210 CrossRefGoogle Scholar
  70. Ling N, Zhang W, Wang D et al (2013) Root exudates from grafted-root watermelon showed a certain contribution in inhibiting Fusarium oxysporum f. sp. niveum. PloS ONE 8(5):e63383. doi: 10.1371/journal.pone.0063383 PubMedPubMedCentralCrossRefGoogle Scholar
  71. Liu J, Magalhaes JV, Shaff J et al (2009) Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J 57(3):389–399. doi: 10.1111/j.1365-313X.2008.03696.x, PMID:1882642PubMedCrossRefGoogle Scholar
  72. Ma JF, Yamaji N (2008) Functions and transport of silicon in plants. Cell Mol Life Sci 65:3049–3057PubMedCrossRefGoogle Scholar
  73. Magalhaes JV, Liu J, Guimarães CT et al (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet 39(9):1156–1161. doi: 10.1038/ng2074, PMID: 17721535PubMedCrossRefGoogle Scholar
  74. Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40(4):923–940. doi: 10.2135/cropsci2000.404923x CrossRefGoogle Scholar
  75. Marschner H (1995) Mineral nutrition of higher plants. Academic, LondonGoogle Scholar
  76. Mathesius U, Watt M (2010) Rhizosphere signals for plant-microbe interactions: implications for field-grown plants. In: Lüttge UE, Beyschlag W (eds) Progress in botany, vol 72. Springer, Berlin, pp 125–161. doi: 10.1007/978-3-642-13145-5_5 Google Scholar
  77. Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42(6):565–572. doi: 10.1016/j.plaphy.2004.05.009, PMID: 15246071PubMedCrossRefGoogle Scholar
  78. Meier IC, Avis PG, Phillips RP (2013) Fungal communities influence root exudation rates in pine seedlings. FEMS Microbiol Ecol 83(3):585–595. doi: 10.1111/1574-6941.12016, PMID: 23013386PubMedCrossRefGoogle Scholar
  79. Mendes R, Kruijt M, de Bruijn I et al (2011) Deciphering the rhizosphere microbiome for disease suppressive bacteria. Science 332(6033):1097–1100. doi: 10.1126/science.1203980, PMID: 21551032PubMedCrossRefGoogle Scholar
  80. Mercado-Blanco J, Bakker P (2007) Interactions between plants and beneficial Pseudomonas spp.: exploiting bacterial traits for crop protection. Antonie van Leeuwenhoek 92(4):367–389. doi: 10.1007/s10482-007-9167-1 PubMedCrossRefGoogle Scholar
  81. Morandi D, Bailey J, Gianinazzi-Pearson V (1984) Isoflavonoid accumulation in soybean roots infected with vesicular-arbuscular mycorrhizal fungi. Physiol Plant Pathol 24(3):357–364. doi: 10.1016/0048-4059(84)90009-2 CrossRefGoogle Scholar
  82. Mukerji KG, Manoharachary C, Singh J (2006) Microbial activity in the rhizospere, vol 7. Springer Science & Business Media, New YorkCrossRefGoogle Scholar
  83. Murray JD, Karas BJ, Sato S et al (2007) A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315:101–104PubMedCrossRefGoogle Scholar
  84. Nadarajah K (2016) Induced systemic resistance in rice. In: Choudhary KD, Varma A (eds) Microbial-mediated induced systemic resistance in plants. Springer, Singapore, pp 103–124. doi: 10.1007/978-981-10-0388-2_7 CrossRefGoogle Scholar
  85. Naher UA, Othman R, Mohd Saud H et al (2008) Effect of inoculation on root exudates carbon sugar and amino acids production of different rice varieties. Res J Microbiol 3(9):580–587CrossRefGoogle Scholar
  86. Narasimhan K, Basheer C, Bajic VB et al (2003) Enhancement of Plant–microbe interactions using a rhizosphere metabolomics-driven approach and its application in the removal of polychlorinated biphenyls. Plant Physiol 132(1):146–153. doi: 10.1104/pp.102.016295, PMID: 12746520PubMedPubMedCentralCrossRefGoogle Scholar
  87. Neal AL, Ahmad S, Gordon-Weeks R et al (2012) Benzoxazinoids in root exudates of maize attract Pseudomonas putida to the rhizosphere. PloS ONE 7(4):e35498. doi: 10.1371/journal.pone.0035498, PMID: 22545111PubMedPubMedCentralCrossRefGoogle Scholar
  88. Newton AC, Fitt BDL, Atkins SD et al (2010) Pathogenesis, parasitism and mutualism in the trophic space of microbe–plant interactions. Trends Microbiol 18(8):365–373. doi: 10.1016/j.tim.2010.06.002, PMID: 20598545PubMedCrossRefGoogle Scholar
  89. Nguema-Ona E, Vicré-Gibouin M, Cannesan M-A et al (2013) Arabinogalactan proteins in root–microbe interactions. Trends Plant Sci 18(8):440–449. doi: 10.1016/j.tplants.2013.03.006, PMID: 23623239PubMedCrossRefGoogle Scholar
  90. Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agronomoie 23:375–396CrossRefGoogle Scholar
  91. Nihorimbere V, Ongena M, Smargiassi M et al (2011) Beneficial effect of the rhizosphere microbial community for plant growth and health. Biotechnol Agron Soc 15:327–337Google Scholar
  92. Novas MV, Iannone LJ, Godeas AM et al (2011) Evidence for leaf endophyte regulation of root symbionts: effect of Neotyphodium endophytes on the pre-infective state of mycorrhizal fungi. Symbiosis 55(1):19–28. doi: 10.1007/s13199-011-0140-4 CrossRefGoogle Scholar
  93. Nozoye T, Nagasaka S, Kobayashi T et al (2011) Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J Biol Chem 286(7):5446–5454. doi: 10.1074/jbc.M110.180026 PubMedCrossRefGoogle Scholar
  94. Oba H, Tawaraya K, Wagatsuma T (2002) Inhibition of pre-symbiotic hyphal growth of arbuscular mycorrhizal fungus Gigaspora margarita by root exudates of Lupinus spp. Soil Sci Plant Nutr 48(1):117–120. doi: 10.1080/00380768.2002.10409180 CrossRefGoogle Scholar
  95. Okon Y, Itzigsohn R (1995) The development of Azospirillum as a commercial inoculant for improving crop yields. Biotechnol Adv 13:415–424PubMedCrossRefGoogle Scholar
  96. Ortiz-Castro R, Contreras-Cornejo HA, Macias-Rodriguez L et al (2009) The role of microbial signals in plant growth and development. Plant Signal Behav 4:701–712PubMedPubMedCentralCrossRefGoogle Scholar
  97. Parmar N (1995) Interactions of rhizosphere bacteria with Cicer-Rhizobium symbiosis. CCS Haryana Agricultural University, HisarGoogle Scholar
  98. Parmar N, Dadarwal KR (1997) Rhizobacteria from rhizosphere and rhizoplane of chick pea (Cicer arietinum L.). Indian J Microbiol 37:205–210Google Scholar
  99. Paterson E, Sim A, Standing D et al (2006) Root exudation from Hordeum vulgare in response to localized nitrate supply. J Exp Bot 57:2413–2420PubMedCrossRefGoogle Scholar
  100. Phillips DA, Fox TC, King MD et al (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136(1):2887–2894. PubMedPubMedCentralCrossRefGoogle Scholar
  101. Pineros MA, Magalhaes JV, Alves VMC et al (2002) The physiology and biophysics of an aluminum tolerance regulation and function of root exudates mechanism based on root citrate exudation in maize. Plant Physiol 129:1194–1206PubMedPubMedCentralCrossRefGoogle Scholar
  102. Poysti NJ, Loewen ED, Wang Z et al (2007) Sinorhizobium meliloti pSymB carries genes necessary for arabinose transport and catabolism. Microbiol 153(3):727–736. doi: 10.1099/mic.0.29148-0 CrossRefGoogle Scholar
  103. Raaijmakers J, Paulitz T, Steinberg C et al (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321(1–2):341–361. doi: 10.1007/s11104-008-9568-6 CrossRefGoogle Scholar
  104. Raaijmakers JM, de Bruijn I, Nybroe O et al (2010) Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev 34(6):1037–1062. doi: 10.1111/j.1574-6976.2010.00221.x PubMedCrossRefGoogle Scholar
  105. Ramos-González MI, Campos MJ, Ramos JL (2005) Analysis of Pseudomonas putida KT2440 gene expression in the maize rhizosphere: in vivo expression technology capture and identification of root-activated promoters. J Bacteriol 187(12):4033–4041. doi: 10.1128/JB.187.12.4033-4041.2005 PubMedPubMedCentralCrossRefGoogle Scholar
  106. Requena N, Perez-Solis E, Azcon-Aguilar C et al (2001) Management of indigenous plant-microbe symbioses aids restoration of desertified ecosystems. Appl Environ Microbiol 67:495–498PubMedPubMedCentralCrossRefGoogle Scholar
  107. Rokhzadi A, Asgharzadeh A, Darvish F et al (2008) Influence of plant growth promoting rhizobacteria on dry matter accumulation of chickpea (Cicer arietinum L) under field conditions. JAES 3(2):253–257Google Scholar
  108. Ryan PR, Tyerman SD, Sasaki T et al (2011) Identification of aluminium-resistance genes in plants provides an opportunity for enhancing the acid-soil tolerance of crop species. J Exp Bot 62:9–20PubMedCrossRefGoogle Scholar
  109. Ryu CM, Farag MA, Hu CH et al (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiology 134:1–10CrossRefGoogle Scholar
  110. Saharan B, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res LSMR-21:1–30Google Scholar
  111. Sanchez-Contreras M, Bauer WD, Gao M et al (2007) Quorum-sensing regulation in rhizobia and its role in symbiotic interactions with legumes. Philos Trans R Soc Lond B 362(1483):1149–1163. doi: 10.1098/rstb.2007.2041 CrossRefGoogle Scholar
  112. Sanders D, Bethke P (2000) Membrane transport. In: Buchanan BB, Gruisham W, Jones RL (eds) Biochemistry and molecular biology of plants. ASPP, Rockville, pp 110–158Google Scholar
  113. Santi C, Bogusz D, Franche C (2013) Biological nitrogen fixation in non-legume plants. Annals of Botany 111:743–767. doi: 10.1093/aob/mct048 PubMedPubMedCentralCrossRefGoogle Scholar
  114. Schnitzer SA, Klironomos JN, HilleRisLambers J et al (2011) Soil microbes drive the classic plant diversity-productivity pattern. Ecology 92(2):296–303PubMedCrossRefGoogle Scholar
  115. Sidler M, Hassa P, Hasan S et al (1998) Involvement of an ABC transporter in a developmental pathway regulating hypocotyl cell elongation in the light. Plant Cell 10:1623–1636PubMedPubMedCentralCrossRefGoogle Scholar
  116. Siegrid S, Lendzemo V, Langer I et al (2007) Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecule 12:1290–1306CrossRefGoogle Scholar
  117. Simons M, Permentier HP, de Weger LA et al (1997) Amino acid synthesis is necessary for tomato root colonization by Pseudomonas fluorescens strain WCS365. Mol Plant Microbe Interac 10(1):102–106. doi: CrossRefGoogle Scholar
  118. Snyder BA, Leite B, Hipskind J et al (1991) Accumulation of sorghum phytoalexins induced by Colletotrichum graminicola at the infection site. Physiol Mol Plant P 39:463–470CrossRefGoogle Scholar
  119. Stearns JC, Woody OZ, McConkey BJ et al (2012) Effects of bacterial ACC deaminase on Brassica napus gene expression. Mol Plant Microbe Interac 25(5):668–676. doi: 10.1094/MPMI-08-11-0213, PMID: 22352713CrossRefGoogle Scholar
  120. Steenhoudt O, Vanderleyden J (2000) Azospirillum, a free living nitrogen fixing bacterium closely associated with grasses. FEMS Microbiol Lett 24:506Google Scholar
  121. Stein M, Dittgen J, Sanchez-Rodriguez C et al (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. The Plant Cell 18:731–746PubMedPubMedCentralCrossRefGoogle Scholar
  122. Svennerstam H, Ganeteg U, Bellini C et al (2007) Comprehensive screening of Arabidopsis mutants suggests the lysine histidine transporter 1 to be involved in plant uptake of amino acids. Plant Physiol 143:1853–1860PubMedPubMedCentralCrossRefGoogle Scholar
  123. Taddei P, Tugnoli V, Bottura G et al (2002) Vibrational, 1H-NMR spectroscopic, and thermal characterization of gladiolus root exudates in relation to Fusarium oxysporum f. sp. gladioli resistance. Biopolymers 67(6):428–439. doi: 10.1002/bip.10170 PubMedCrossRefGoogle Scholar
  124. 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(6):637–648. doi: PubMedCrossRefGoogle Scholar
  125. Teplitski M, Chen H, Rajamani S et al (2004) Chlamydomonas reinhardtii secretes compounds that mimic bacterial signals and interfere with quorum sensing regulation in bacteria. Plant Physiol 134(1):137–146. doi: 10.1104/pp.103.029918, PMID: 14671013PubMedPubMedCentralCrossRefGoogle Scholar
  126. Tirichine L, Sandal N, Madsen LH et al (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315:104–107PubMedCrossRefGoogle Scholar
  127. Uren NC (2000) Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil–plant interface. Marcel Dekker, Inc., New York, pp 19–40Google Scholar
  128. Urich T, Lanzén A, Qi J et al (2008) Simultaneous assessment of soil microbial community structure and function through analysis of the meta-transcriptome. PloS One 3(6):e2527. doi: PubMedPubMedCentralCrossRefGoogle Scholar
  129. Vicré M, Santaella C, Blanchet S et al (2005) Root border-like cells of Arabidopsis. Microscopical characterization and role in the interaction with rhizobacteria. Plant Physiol 138(2):998–1008. doi: 10.1104/pp.104.051813 PubMedPubMedCentralCrossRefGoogle Scholar
  130. Walker TS, Bais HP, Grotewold E et al (2003) Root exudation and rhizosphere biology. Plant Physiol 132(1):44–51. doi: PubMedPubMedCentralCrossRefGoogle Scholar
  131. Weir TL, Park S-W, Vivanco JM (2004) Biochemical and physiological mechanisms mediated by allelochemicals. Curr Opin Plant Biol 7(4):472–479. doi: 10.1016/j.pbi.2004.05.007 PubMedCrossRefGoogle Scholar
  132. Weston LA, Ryan PR, Watt M (2012) Mechanisms for cellular transport and release of allelochemicals from plant roots into the rhizosphere. J Exp Bot 63:3445–3454. doi: 10.1093/jxb/ers054, PMID: 22378954PubMedCrossRefGoogle Scholar
  133. Winkel-Shirley B (2001) Flavonoid biosynthesis: a colorful model for genetics, biochemistry, cell biology and biotechnology. Plant Physiol 126:485–493PubMedPubMedCentralCrossRefGoogle Scholar
  134. Wu X-G, Duan H-M, Tian T et al (2010) Effect of the hfq gene on 2,4-diacetylphloroglucinol production and the PcoI/PcoR quorum-sensing system in Pseudomonas fluorescens 2P24. FEMS Microbiol Lett 309(1):16–24. doi: 10.1111/j.1574-6968.2010.02009.x PubMedGoogle Scholar
  135. Xie F, Williams A, Edwards A et al (2012) A plant arabinogalactan like glycoprotein promotes a novel type of polar surface attachment by Rhizobium leguminosarum. Mol Plant–Microbe Interact 25(2):250–258. doi: 10.1094/MPMI-08-11-0211, PMID: 21995765PubMedCrossRefGoogle Scholar
  136. Yadegari M, Rahmani HA, Noormohammadi G et al (2008) Evaluation of bean (Phaseolus vulgaris) seeds inoculation with Rhizobium phaseoli and plant growth promoting rhizobacteria on yield and yield components. Pak J Biol Sci 11:1935–1939PubMedCrossRefGoogle Scholar
  137. Yoneyama K, Xie X, Sekimoto H et al (2008) Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytol 179(2):484–494. doi: 10.1111/j.1469-8137.2008.02462.x PubMedCrossRefGoogle Scholar
  138. Zahran HH (1999) Rhizobium–legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63(4):968–989, PMID: 10585971PubMedPubMedCentralGoogle Scholar
  139. Zhang J, Subramanian S, Stacey G et al (2009) Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti. Plant J 57(1):171–183. doi: 10.1111/j.1365-313X.2008.03676.x PubMedCrossRefGoogle Scholar
  140. Zhuang X, Gao J, Ma A et al (2013) Bioactive molecules in soil ecosystems: masters of the underground. Int J Mol Sci 14(5):8841–8868. doi: 10.3390/ijms14058841 PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2016

Authors and Affiliations

  1. 1.School of Environmental and Natural Resource Sciences, Faculty of Science and TechnologyUniversiti Kebangsaan MalaysiaBangiMalaysia

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