Advertisement

Underlying mechanism of plant–microbe crosstalk in shaping microbial ecology of the rhizosphere

  • Akansha Jain
  • Joydeep Chakraborty
  • Sampa DasEmail author
Review

Abstract

The rhizosphere is the immediate area of soil encompassing plant roots that is inhabited by a large population of microorganisms and invertebrates, making its environment highly complex. Plants attract specific soil microorganisms using root exudates from large associations of soil microorganisms. The successful establishment of plant growth-promoting rhizospheric microorganisms is the first step in defending plants from soil-borne pathogenic organisms. Understanding rhizosphere’s unique and dynamic ecology will help in improving nutrient absorption, water use efficiency, modifying soil properties, thereby, enhancing plant growth, yield and integrating disease management strategies. In recent years, in the field of plant–microbe interaction, root exudates have received considerable importance in mediating interactions with nearby plants and microorganisms. Novel discernment of key factors framing the microbial community in rhizosphere will be very crucial in achieving sustainable agriculture. This review discusses on how root exudates play a crucial role in facilitating nutrient, signal exchange in rhizosphere and modulating changes in architecture of microbial community. We focus in particular on the influence of root exudates on positive and negative plant–microbe interactions occurring in rhizosphere and point out implicit avenues for further research.

Keywords

Exudates Microbes Plant–microbe interaction Rhizosphere 

Notes

Acknowledgements

AJ is grateful to Department of Science and Technology, Govt. of India, New Delhi for financial assistance under Start-Up Research Grant (Young Scientist) Scheme (YSS/2015/000773) and under Women Scientist Scheme-A (WOS-A) (SR/WOS-A/LS-377/2018). SD acknowledges Indian National Science Academy for providing Senior Scientist Fellowship.

References

  1. Agler MT, Ruhe J, Kroll S, Morhenn C, Kim S-T, Weigel D, Kemen E (2016) Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol 14:e1002352PubMedPubMedCentralGoogle Scholar
  2. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedGoogle Scholar
  3. Almario J, Kyselková M, Kopecký J, Ságová-Marecková M, Muller D, Grundmann GL, Moënne-Loccoz Y (2013) Assessment of the relationship between geologic origin of soil, rhizobacterial community composition and soil receptivity to tobacco black root rot in Savoie region (France). Plant Soil 371:397–408Google Scholar
  4. Andersen PC, Brodbeck BV, Oden S, Shriner A, Leite B (2007) Influence of xylem fluid chemistry on planktonic growth, biofilm formation and aggregation of Xylella fastidiosa. FEMS Microbiol Lett 274:210–217PubMedGoogle Scholar
  5. Arcate JM, Karp MA, Nelson EB (2006) Diversity of Peronosporomycete (Oomycete) communities associated with the rhizosphere of different plant species. Microb Ecol 51:36–50PubMedGoogle Scholar
  6. Bacilio-Jiménez M, Aguilar-Flores S, Ventura-Zapata E, Pérez-Campos E, Bouquelet S, Zenteno E (2003) Chemical characterization of root exudates from rice (Oryza sativa) and their effects on the chemotactic response of endophytic bacteria. Plant Soil 249(2):271–277Google Scholar
  7. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32(6):666–681PubMedGoogle Scholar
  8. Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM (2013) 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 288:4502–4512PubMedPubMedCentralGoogle Scholar
  9. Baetz U, Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends Plant Sci 19:90–98PubMedGoogle Scholar
  10. Bais HP, Walker TS, Stermitz FR, Hufbauer RA, Vivanco JM (2002) Enantiomeric-dependant phytotoxic and antimicrobial activity of (±)-catechin: a rhizosecreted racemic mixture from spotted knapweed. Plant Physiol 128:1173–1179PubMedGoogle Scholar
  11. Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134:307–319PubMedPubMedCentralGoogle Scholar
  12. 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 57:233–266PubMedGoogle Scholar
  13. Banasiak J, Biala W, Staszków A, Swarcewicz B, Kepczynska E, Figlerowicz M, Jasinski M (2013) A Medicago truncatula ABC transporter belonging to subfamily G modulates the level of isoflavonoids. J Exp Bot 64:1005–1015PubMedGoogle Scholar
  14. Bardon C, Piola F, Bellvert F, Haichar FZ, Comte G, Meiffren G, Pommier T, Puijalon S, Tsafack N, Poly F (2014) Evidence for biological denitrification inhibition (BDI) by plant secondary metabolites. N Phytol 204:62Google Scholar
  15. Beckers B, Op De Beeck M, Weyens N, Boerjan W, Vangronsveld J (2017) Structural variability and niche differentiation in the rhizosphere and endosphere bacterial microbiome of field-grown poplar trees. Microbiome 5(1):25PubMedPubMedCentralGoogle Scholar
  16. Behie SW, Zelisko PM, Bidochka MJ (2012) Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science 336(6088):1576–1577PubMedGoogle Scholar
  17. Bertin C, Yang XH, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83Google Scholar
  18. Bharadwaj DP, Alström S, Lundquist PO (2012) Interactions among Glomus irregulare, arbuscular mycorrhizal spore-associated bacteria, and plant pathogens under in vitro conditions. Mycorrhiza 22:437–447PubMedGoogle Scholar
  19. Bolanos-Vasquez MC, Werner D (1997) Effect of Rhizobium tropici, R. etli, and R. leguminosarum bv. phaseoli on nod gene-inducing flavonoids in root exudates of Phaseolus vulgaris. Mol Plant-Microbe Interact 10:339–346Google Scholar
  20. Bouffaud ML, Poirier MA, Muller D, Moënne-Loccoz Y (2014) Root microbiome relates to plant host evolution in maize and other Poaceae. Environ Microbiol 16:2804–2814PubMedGoogle Scholar
  21. Boyer M, Bally R, Perrotto S, Chaintreuil C, Wisniewski-Dyé F (2008) A quorum-quenching approach to identify quorum sensing-regulated functions in Azospirillum lipoferum. Res Microbiol 159:699–708PubMedGoogle Scholar
  22. Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744PubMedGoogle Scholar
  23. Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J, Pan Y, McHardy AC, Schulze-Lefert P (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392–403PubMedPubMedCentralGoogle Scholar
  24. Cai T, Cai W, Zhang J, Zheng H, Tsou AM, Xiao L, Zhong Z, Zhu J (2009) Host legume-exuded antimetabolites optimize the symbiotic rhizosphere. Mol Microbiol 73:507–517PubMedGoogle Scholar
  25. Calvo OC, Franzaring J, Schmid I, Müller M, Brohon N, Fangmeier A (2016) Atmospheric CO2 enrichment and drought stress modify root exudation of barley. Glob Change Biol 23:1292–1304Google Scholar
  26. Casieri L, Gallardo K, Wipf D (2012) Transcriptional response of Medicago truncatula sulphate transporters to arbuscular mycorrhizal symbiosis with and without sulphur stress. Planta 235:1431–1447PubMedGoogle Scholar
  27. Catford JG, Staehelin C, Larose G, Piché Y, Vierheilig H (2006) Systemically suppressed isoflavonoids and their stimulating effects on nodulation and mycorrhization in alfalfa split-root systems. Plant Soil 285:257–266Google Scholar
  28. Chaparro JM, Badri DV, Vivanco JM (2013) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803PubMedPubMedCentralGoogle Scholar
  29. Chen YP, Rekha PD, Arun AB, Shen FT, Lai WA, Young CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34:33–41Google Scholar
  30. Chen Y, Cao S, Chai Y, Clardy J, Kolter R, Guo J, Losick R (2012) A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants. Mol Microbiol 85:418–430PubMedPubMedCentralGoogle Scholar
  31. Combes-Meynet E, Pothier JF, Moënne-Loccoz Y, Prigent-Combaret C (2011) The Pseudomonas secondary metabolite 2,4-diacetylphloroglucinol is a signal inducing rhizoplane expression of Azospirillum genes involved in plant-growth promotion. Mol Plant-Microbe Interact 24:271–284PubMedGoogle Scholar
  32. Coskun D, Britto DT, Shi W, Kronzucke HJ (2017) How plant root exudates shape the nitrogen cycle. Trends Plant Sci 22:661–673PubMedGoogle Scholar
  33. Couillerot O, Combes-Meynet E, Pothier JF, Bellvert F, Challita E, Poirier MA, Rohr R, Comte G, Moënne-Loccoz Y, Prigent-Combaret C (2011) The role of the antimicrobial compound 2,4-diacetylphloroglucinol in the impact of biocontrol Pseudomonas fluorescens F113 on Azospirillum brasilense phytostimulators. Microbiology 157:1694–1705PubMedGoogle Scholar
  34. Curlango-Rivera G, Duclos DV, Ebolo JJ, Hawes MC (2010) Transient exposure of root tips to primary and secondary metabolites: impact on root growth and production of border cells. Plant Soil 332:267–275Google Scholar
  35. D’Mello JPF (2015) Toxicology of non-protein amino acids. In: D’Mello JPF (ed) Amino acids in higher plants. CABI, Wallingford, UK, pp 507–537Google Scholar
  36. Dardanelli MS, Manyani H, Gonzalez-Barroso S, Rodriguez Carvajal MA, Gil-Serramp AM, Espuny MR, López-Baena FJ, Bellogín RA, Megías M, Ollero FJ (2010) Effect of the presence of the plant growth promoting rhizobacterium (PGPR) Chryseobacterium balustinum Aur9 and salt stress in the pattern of flavonoids exuded by soybean roots. Plant Soil 328:483–493Google Scholar
  37. de Ascensao AR, Dubery IA (2003) Soluble and wall-bound phenolics and phenolic polymers in Musa acuminata roots exposed to elicitors from Fusarium oxysporum f sp cubense. Phytochemistry 63(6):679–686PubMedGoogle Scholar
  38. de Weert S, Vermeiren H, Mulders IHM, Kuiper I, Hendrickx N, Bloemberg GV, Vanderleyden J, De Mol R, Lugtenberg BJJ (2002) Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens. Mol Plant-Microbe Interact 15:1173–1180PubMedGoogle Scholar
  39. De Maeyer K, D’Aes J, Hua GK, Perneel M, Vanhaecke L, Noppe H, Höfte M (2011) N-acylhomoserine lactone quorum-sensing signaling in antagonistic phenazine-producing Pseudomonas isolates from the red cocoyam rhizosphere. Microbiology 157:459–472PubMedGoogle Scholar
  40. Deveau A, Brulé C, Palin B, Champmartin D, Rubini P, Garbaye J, Sarniguet A, Frey-Klett P (2010) Role of fungal trehalose and bacterial thiamine in the improved survival and growth of the ectomycorrhizal fungus Laccaria bicolor S238N and the helper bacterium Pseudomonas fluorescens BBc6R8. Environ Microbiol Rep 2:560–568PubMedGoogle Scholar
  41. Dixon R, Kahn D (2004) Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2:621–631PubMedGoogle Scholar
  42. Doidy J, van Tuinen D, Lamotte O, Corneillat M, Alcaraz G, Wipf D (2012) The Medicago truncatula sucrose transporter family: characterization and implication of key members in carbon partitioning towards arbuscular mycorrhizal fungi. Mol Plant 5:1346–1358PubMedGoogle Scholar
  43. Drogue B, Combes-Meynet E, Moënne-Loccoz Y, Wisniewski-Dyé F, Prigent-Combaret C (2013) Control of the cooperation between plant growth-promoting rhizobacteria and crops by rhizosphere signals. In: Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere, vol 1 and 2. Wiley, Hoboken, pp 281–294Google Scholar
  44. Eberl L (1999) N-acyl homoserine lactone-mediated gene regulation in gram-negative bacteria. Syst Appl Microbiol 22(4):493–506PubMedGoogle Scholar
  45. Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci USA 112:E911–E920PubMedGoogle Scholar
  46. Esquivel-Cote R, Ramirez-Gama RM, Tsuzuki-Reyes G, Orozco-Segovia A, Huante P (2010) Azospirillum lipoferum strain AZm5 containing 1-aminocyclopropane-1-carboxylic acid deaminase improves early growth of tomato seedlings under nitrogen deficiency. Plant Soil 337:65–75Google Scholar
  47. Fan B, Borriss R, Bleiss W, Wu X (2012) Gram-positive rhizobacterium Bacillus amyloliquefaciens FZB42 colonizes three types of plants in different patterns. J Microbiol 50:38–44PubMedGoogle Scholar
  48. Farrar K, Bryant D, Cope-Selby N (2014) Understanding and engineering beneficial plant–microbe interactions: plant growth promotion in energy crops. Plant Biotechnol J 12(9):1193–1206PubMedPubMedCentralGoogle Scholar
  49. Frapolli M, Pothier JF, Défago G, Moënne-Loccoz Y (2012) Evolutionary history of synthesis pathway genes for phloroglucinol and cyanide antimicrobials in plant-associated fluorescent pseudomonads. Mol Phylogenet Evol 63:877–890PubMedGoogle Scholar
  50. Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275PubMedPubMedCentralGoogle Scholar
  51. Hannula SE, Boschker HTS, de Boer W, van Veen JA (2012) 13C pulse-labeling assessment of the community structure of active fungi in the rhizosphere of a genetically starch-modified potato (Solanum tuberosum) cultivar and its parental isoline. N Phytol 194:784–799Google Scholar
  52. Hierro JL, Callaway RM (2003) Allelopathy and exotic plant invasion. Plant Soil 256:25–39Google Scholar
  53. Hirsch PR, Miller AJ, Dennis PG (2013) Do root exudates exert more influence on rhizosphere bacterial community structure than other rhizodeposits? In: Bruijin FJ (ed) Molecular microbial ecology of the rhizosphere, vol 1. Wiley, Hoboken, pp 229–242Google Scholar
  54. Hutsch BW, Augustin J, Merbach W (2000) Plant rhizodeposition an important source for carbon turnover in soils. J Plant Nutr Soil Sci 165:397–407Google Scholar
  55. Idriss EE, Makarewicz O, Farouk A, Rosner K, Greiner R, Bochow H, Richter T, Borriss R (2002) Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant-growth-promoting effect. Microbiology 148:2097–2109PubMedGoogle Scholar
  56. Igiehon NO, Babalola OO (2018) Rhizosphere microbiome modulators: contributions of nitrogen fixing bacteria towards sustainable agriculture. Int J Environ Res Public Health 15(4):574.  https://doi.org/10.3390/ijerph15040574 CrossRefPubMedCentralGoogle Scholar
  57. Iven T, König S, Singh S, Braus-Stromeyer SA, Bischoff M, Tietze LF, Braus GH, Lipka V, Feussner I, Dröge-Laser W (2012) Transcriptional activation and production of tryptophan-derived secondary metabolites in Arabidopsis roots contributes to the defense against the fungal vascular pathogen Verticillium longisporum. Mol Plant 5(6):1389–1402PubMedGoogle Scholar
  58. Jain A, Singh S, Sarma BK, Singh HB (2012) Microbial consortium mediated reprogramming of defense network in pea to enhance tolerance against Sclerotinia sclerotiorum. J Appl Microbiol 112(3):537–550PubMedGoogle Scholar
  59. Jain A, Singh A, Singh BN, Singh S, Upadhyay RS, Sarma BK, Singh HB (2013a) Biotic stress management in agricultural crops using microbial consortium. In: Maheshwari DK (ed) Bacteria in agrobiology: disease management. Springer, Berlin, pp 427–448Google Scholar
  60. Jain A, Singh A, Singh S, Singh HB (2013b) Microbial consortium-induced changes in oxidative stress markers in pea plants challenged with Sclerotinia sclerotiorum. J Plant Growth Regul 32:388–398Google Scholar
  61. Jain A, Singh A, Singh S, Singh V, Singh HB (2015) Phenols enhancement effect of microbial consortium in pea plants restrains Sclerotinia sclerotiorum. Biol Control 89:23–32Google Scholar
  62. Jain A, Singh A, Singh S, Singh HB (2015) Comparative proteomics analysis in pea treated with microbial consortium of beneficial microbes reveals changes in protein network to enhance resistance against Sclerotinia sclerotiorum. J Plant Physiol 3:1. https:// doi.org/10.1016/j.jplph.2015.05.004Google Scholar
  63. Jin CW, Ye YQ, Zheng SJ (2014) An underground tale: contribution of microbial activity to plant iron acquisition via ecological processes. Ann Bot 113(1):7–18PubMedGoogle Scholar
  64. Johnston-Monje D, Raizada MN (2011) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS ONE 6:e20396PubMedPubMedCentralGoogle Scholar
  65. Jones DL (1998) Organic acids in the rhizosphere—a critical review. Plant Soil 205:25–44Google Scholar
  66. Kamoun S, Furzer O, Jones JD, Judelson HS, Ali GS, Dalio RJ, Roy SG, Schena L, Zambounis A, Panabières F, Cahill D, Ruocco M, Figueiredo A, Chen XR, Hulvey J, Stam R, Lamour K, Gijzen M, Tyler BM, Grünwald NJ, Mukhtar MS, Tomé DF, Tör M, Van Den Ackerveken G, McDowell J, Daayf F, Fry WE, Lindqvist-Kreuze H, Meijer HJ, Petre B, Ristaino J, Yoshida K, Birch PR, Govers F (2015) The top 10 oomycete pathogens in molecular plant pathology. Mol Plant Pathol 16:413–434PubMedGoogle Scholar
  67. Kang J, Park J, Choi H, Burla B, Kretzschmar T, Lee Y, Martinoia E (2011) Plant ABC transporters. Arabidopsis Book 9:e0153PubMedGoogle Scholar
  68. Kawaharada Y, Kelly S, Nielsen MW, Hjuler CT, Gysel K, Muszyński A, Carlson RW, Thygesen MB, Sandal N, Asmussen MH, Vinther M, Andersen SU, Krusell L, Thirup S, Jensen KJ, Ronson CW, Blaise M, Radutoiu S, Stougaard J (2015) Receptor-mediated exopolysaccharide perception controls bacterial infection. Nature 523(7560):308–312PubMedGoogle Scholar
  69. Koroney AS, Plasson C, Pawlak B, Sidikou R, Driouich A, Vicré-Gibouin M-B (2016) Root exudate of Solanum tuberosum is enriched in galactose-containing molecules and impacts the growth of Pectobacterium atrosepticum. Ann Bot 118(4):797–808PubMedPubMedCentralGoogle Scholar
  70. Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier JB, Reinhardt D, Bours R, Bouwmeester HJ, Martinoia E (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483:341–344PubMedGoogle Scholar
  71. Ladygina N, Hedlund K (2010) Plant species influence microbial diversity and carbon allocation in the rhizosphere. Soil Biol Biochem 42:162–168Google Scholar
  72. Lange M, Eisenhauer N, Sierra CA, Bessler H, Engels C, Griffiths RI, Mellado-Vázquez PG, Malik AA, Roy J, Scheu S, Steinbeiss S, Thomson BC, Trumbore SE, Gleixner G (2015) Plant diversity increases soil microbial activity and soil carbon storage. Nat Commun 6:6707PubMedGoogle Scholar
  73. Lanoue A, Burlat V, Henkes GJ, Koch I, Schurr U, Röse US (2010) De novo biosynthesis of defense root exudates in response to Fusarium attack in barley. N Phytol 185:577–588Google Scholar
  74. Lebeis SL, Paredes SH, Lundberg DS, Breakfield N, Gehring J, McDonald M, Malfatti S, Glavina del Rio T, Jones CD, Tringe SG, Dangl JL (2015) Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349:860–864PubMedGoogle Scholar
  75. Leigh JA, Coplin DL (1992) Exopolysaccharides in plant–bacterial interactions. Annu Rev Microbiol 46:307–346PubMedGoogle Scholar
  76. Li XL, Geoege E, Marschner H (1991) Phosphorus depletion and pH decrease at the root–soil and hyphae–soil interfaces of VAM white clover fertilized with ammonium. N Phytol 119:397–404Google Scholar
  77. Li S, Zhang N, Zhang Z, Luo J, Shen B, Zhang R, Shen Q (2013) Antagonist Bacillus subtilis HJ5 controls Verticillium wilt of cotton by root colonization and biofilm formation. Biol Fertil Soils 49:295–303Google Scholar
  78. Ling N, Raza W, Ma J, Huang Q, Shen Q (2011) Identification and role of organic acids in watermelon root exudates for recruiting Paenibacillus polymyxa SQR-21 in the rhizosphere. Eur J Soil Biol 47:374–379Google Scholar
  79. Lipton DS, Blanchar RW, Blevins DG (1987) Citrate, malate and succinate concentration in exudates from P-sufficient and P stresses Medicago sativa L seedlings. Plant Physiol 85:315–317PubMedPubMedCentralGoogle Scholar
  80. Liu X, Jia J, Popat R, Ortori CA, Li J, Diggle SP, Gao K, Cámara M (2011) Characterisation of two quorum sensing systems in the endophytic Serratia plymuthica strain G3: differential control of motility and biofilm formation according to life-style. BMC Microbiol 11:26PubMedPubMedCentralGoogle Scholar
  81. Liu F, Hewezi T, Lebeis SL, Pantalone V, Grewal PS, Staton ME (2019) Soil indigenous microbiome and plant genotypes cooperatively modify soybean rhizosphere microbiome assembly. BMC Microbiol 19: Article number: 201Google Scholar
  82. Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Bécard G, Dénarié J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–63PubMedGoogle Scholar
  83. Marschner H (1995) Mineral nutrition of higher plants. Academia, LondonGoogle Scholar
  84. Mathesius U (2009) Comparative proteomic studies of root–microbe interactions. J Proteomics 72(3):353–366PubMedGoogle Scholar
  85. Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anolles G, Rolfe BG, Bauer WD (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci USA 100:1444–1449PubMedGoogle Scholar
  86. Mishra S, Nautiyal CS (2012) Reducing the allelopathic effect of Parthenium hysterophorus L on wheat (Triticum aestivum L) by Pseudomonas putida. Plant Growth Regul 66:155–165Google Scholar
  87. Mohanram S, Kumar P (2019) Rhizosphere microbiome: revisiting the synergy of plant–microbe interactions. Ann Microbiol 69(4):307–320Google Scholar
  88. Moore JW, Herrera-Foessel S, Lan C, Schnippenkoetter W, Ayliffe M, Huerta-Espino J, Lillemo M, Viccars L, Milne R, Periyannan S, Kong X, Spielmeyer W, Talbot M, Bariana H, Patrick JW, Dodds P, Singh R, Lagudah E (2015) A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat Genet 47:1494–1498PubMedGoogle Scholar
  89. Morris PF, Bone E, Tyler BM (1998) Chemotropic and contact responses of Phytophthora sojae hyphae to soybean isoflavonoids and artificial substrates. Plant Physiol 117:1171–1178PubMedPubMedCentralGoogle Scholar
  90. Mougel C, Offre P, Ranjard L, Corberand T, Gamalero E, Robin C, Lemanceau P (2006) Dynamic of the genetic structure of bacterial and fungal communities at different developmental stages of Medicago truncatula Gaertn cv Jemalong line J5. N Phytol 170:165–175Google Scholar
  91. Mousa WK, Shearer C, Limay-Rios V, Ettinger CL, Eisen JA, Raizada MN (2016) Root-hair endophyte stacking in finger millet creates a physicochemical barrier to trap the fungal pathogen Fusarium graminearum. Nat Microbiol 1:16167PubMedGoogle Scholar
  92. Murray JD, Cousins DR, Jackson KJ, Liu C (2013) Signaling at the root surface: the role of cutin monomers in mycorrhization. Mol Plant 6:1381–1383PubMedPubMedCentralGoogle Scholar
  93. Nardi S, Concheri G, Pizzeghello D, Sturaro A, Rella R, Parvoli G (2000) Soil organic matter mobilization by root exudates. Chemosphere 41:653–658PubMedGoogle Scholar
  94. Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agronomoie 23:375–396Google Scholar
  95. Olanrewaju OS, Ayangbenro AS, Glick BR, Babalola OO (2019) Plant health: feedback effect of root exudates–rhizobiome interactions. Appl Microbiol Biotechnol 103(3):1155–1166PubMedGoogle Scholar
  96. Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263PubMedGoogle Scholar
  97. Pangesti N, Pineda A, Pieterse CM, Dicke M, van Loon JJ (2013) Two-way plant mediated interactions between root-associated microbes and insects: from ecology to mechanisms. Front Plant Sci 4:414PubMedPubMedCentralGoogle Scholar
  98. Paulsen IT, Press CM, Loper JE (2005) Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5. Nat Biotechnol 23:873–878PubMedGoogle Scholar
  99. Peiffer J, Sporb A, Korenb O, Jinb Z, Tringed SG, Dangle JL, Bucklera ES, Ley RE (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci USA 110:6548–6553PubMedGoogle Scholar
  100. Pérez-Jaramillo JE, Mendes R, Raaijmakers JM (2016) Impact of plant domestication on rhizosphere microbiome assembly and functions. Plant Mol Biol 90:635–644PubMedGoogle Scholar
  101. Peters NK, Frost JW, Long SR (1986) A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233(4767):977–980PubMedGoogle Scholar
  102. 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 11:789–799PubMedGoogle Scholar
  103. Prober SM, Leff JW, Bates ST, Borer ET, Firn J, Harpole WS, Lind EM, Seabloom EW, Adler PB, Bakker JD, Cleland EE, DeCrappeo NM, DeLorenze E, Hagenah N, Hautier Y, Hofmockel KS, Kirkman KP, Knops JM, La Pierre KJ, MacDougall AS, McCulley RL, Mitchell CE, Risch AC, Schuetz M, Stevens CJ, Williams RJ, Fierer N (2014) Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecol Lett 18:85–95PubMedGoogle Scholar
  104. Ruan Y, Kotraiah V, Straney DC (1995) Flavonoids stimulate spore germination in Fusarium solani pathogenic on legumes in a manner sensitive to inhibitors of cAMP-dependent protein kinase. Mol Plant Microb Interact 8:929–938Google Scholar
  105. Rudrappa T, Czymmek KJ, Pare PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–1556PubMedPubMedCentralGoogle Scholar
  106. Sarma BK, Singh DP, Mehta S, Singh HB (2002) Plant growth promoting rhizobacteria-elicited alterations in phenolic profile of chickpea (Cicer arietinum) infected by Sclerotium rolfsii. J Phytopathol 150:277–282Google Scholar
  107. Sasse J, Martinoia E, Northen T (2018) Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci 23:25–41PubMedGoogle Scholar
  108. Saxena A, Singh HB, Raghuwanshi R (2015) Elevation of defense network in chilli against Colletotrichum capsici by phyllospheric Trichoderma strain. J Plant Growth Regul 3:1.  https://doi.org/10.1007/s00344-015-9542-5 CrossRefGoogle Scholar
  109. Schlaeppi K, Dombrowski N, Oter RG, Loren V, van Themaat E, Schulze-Lefert P (2014) Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proc Natl Acad Sci USA 111:585–592PubMedGoogle Scholar
  110. Schmidt R, Etalo DW, de Jager V, Gerards S, Zweers H, de Boer W, Garbeva P (2016) Microbial small talk: volatiles in fungal–bacterial interactions. Front Microbiol 6:1495PubMedPubMedCentralGoogle Scholar
  111. Shakya M, Gottel N, Castro H, Yang ZK, Gunter L, Labbé J, Muchero W, Bonito G, Vilgalys R, Tuskan G, Podar M, Schadt CW (2013) A multifactor analysis of fungal and bacterial community structure in the root microbiome of mature Populus deltoides trees. PLoS ONE 8:e76382PubMedPubMedCentralGoogle Scholar
  112. Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA (2013) Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus 2:587PubMedPubMedCentralGoogle Scholar
  113. Shukla KP, Sharma S, Singh NK, Singh V, Tiwari K, Singh S (2011) Nature and role of root exudates: efficacy in bioremediation. Afr J Biotechnol 10:9717–9724Google Scholar
  114. Singh A, Jain A, Sarma BK, Upadyay BK, Singh HB (2013) Rhizosphere microbes facilitate redox homeostasis in Cicer arietinum against biotic stress. Ann Appl Biol 163:33–46Google Scholar
  115. Singh A, Jain A, Sarma BK, Upadyay BK, Singh HB (2014) Rhizosphere competent microbial consortium mediates rapid changes in phenolic profiles in chickpea during Sclerotium rolfsii infection. Microbiol Res 169:353–360PubMedGoogle Scholar
  116. Somers E, Ptacek D, Gysegom P, Srinivasan M, Vanderleyden J (2005) Azospirillum brasilense produces the auxin-like phenylacetic acid by using the key enzyme for indole-3-acetic acid biosynthesis. Appl Environ Microbiol 71:1803–1810PubMedPubMedCentralGoogle Scholar
  117. Stanley NR, Britton RA, Grossman AD, Lazazzera BA (2003) Identification of catabolite repression as a physiological regulator. J Bacteriol 185:1951–1957PubMedPubMedCentralGoogle Scholar
  118. Steinauer K, Chatzinotas A, Eisenhauer N (2016) Root exudate cocktails: the link between plant diversity and soil microorganisms? Ecol Evol 6:7387–7396PubMedPubMedCentralGoogle Scholar
  119. Stepanovic S, Dakic I, Opavski N, Jezek P, Ranin L (2003) Influence of the growth medium composition on biofilm formation by Staphylococcus sciuri. Ann Microbiol 53:63–74Google Scholar
  120. Takenaka S, Nishio Z, Nakamura Y (2003) Induction of defense reactions in sugar beet and wheat treatment with cell wall protein fractions from the mycoparasite Pythium oligandrum. Phytopathology 93:1228–1232PubMedGoogle Scholar
  121. Taketani RG, Lançoni MD, Kavamura VN, Durrer A, Andreote FD, Melo IS (2017) Dry season constrains bacterial phylogenetic diversity in a semi-arid rhizosphere system. Microb Ecol 73:153–161PubMedGoogle Scholar
  122. Thomashow LS, Weller DM (1990) Role of antibiotics and siderophores in biocontrol of take-all disease of wheat. Plant Soil 126:93–99Google Scholar
  123. Thomashow LS, Weller DM (1995) Current concepts in the use of introduced bacteria for biological disease control: mechanisms and antifungal metabolites. In: Stacey G, Keen N (eds) Plant–microbe interactions, vol 1. Chapman and Hall, New York, pp 187–235Google Scholar
  124. Turner T, James E, Poole P (2013) The plant microbiome. Genome Biol 14:209PubMedPubMedCentralGoogle Scholar
  125. Uroz S, Buee M, Murat C, Frey-Klett P, Martin F (2010) Pyrosequencing reveals a contrasted bacterial diversity between oak rhizosphere and surrounding soil. Environ Microbiol Rep 2:281–288PubMedGoogle Scholar
  126. Vacheron J, Desbrosses G, Bouffaud ML, Touraine B, Loccoz YM, Muller D, Legendre L, Wisniewski-Dyé F, Prigent-Combaret C (2013) Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4:356PubMedPubMedCentralGoogle Scholar
  127. Vandenkoornhuyse P, Mahé S, Ineson P, Staddon P, Ostle N, Cliquet JB, Francez AJ, Fitter AH, Young JPW (2007) Active root-inhabiting microbes identified by rapid incorporation of plant-derived carbon into RNA. Proc Natl Acad Sci USA 104:16970–16975PubMedGoogle Scholar
  128. Vicre M, Santaella C, Blanchet S, Gateau A, Driouich A (2005) Root border-like cells of Arabidopsis Microscopical characterization and role in the interaction with rhizobacteria. Plant Physiol 138:998–1008PubMedPubMedCentralGoogle Scholar
  129. Walder F, Brulé D, Koegel S, Wiemken A, Boller T, Courty PE (2015) Plant phosphorus acquisition in a common mycorrhizal network: regulation of phosphate transporter genes of the Pht1 family in sorghum and flax. N Phytol 205:1632–1645Google Scholar
  130. Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51PubMedPubMedCentralGoogle Scholar
  131. Wang Y, Bouwmeester K, van de Mortel JE, Shan W, Govers F (2013) A novel Arabidopsis-oomycete pathosystem: differential interactions with Phytophthora capsici reveal a role for camalexin, indole glucosinolates and salicylic acid in defence. Plant Cell Environ 36:1192–1203PubMedGoogle Scholar
  132. Weisskopf L, Heller S, Eberl L (2011) Burkholderia species are major inhabitants of white lupin cluster roots. Appl Environ Microbiol 77:7715–7720PubMedPubMedCentralGoogle Scholar
  133. Wilkens S (2015) Structure and mechanism of ABC transporters. F1000Prime Rep 7:14Google Scholar
  134. Winkelmann G (2007) Ecology of siderophores with special reference to the fungi. Biometals 20:379–392PubMedGoogle Scholar
  135. Xu H (2011) d-amino acid mitigated membrane biofouling and promoted biofilm. J Membr Sci 376:266–274Google Scholar
  136. Xu H, Kemppainen M, El Kayal W, Lee SH, Pardo AG, Cooke JEK, Zwiazek JJ (2015) Overexpression of Laccaria bicolor aquaporin JQ585595 alters root water transport properties in ectomycorrhizal white spruce (Picea glauca) seedlings. N Phytol 205:757–770Google Scholar
  137. Yamada K, Kanai M, Osakabe Y, Ohiraki H, Shinozaki K, Yamaguchi-Shinozaki K (2011) Monosaccharide absorption activity of Arabidopsis roots depends on expression profiles of transporter genes under high salinity conditions. J Biol Chem 286:43577–43586PubMedPubMedCentralGoogle Scholar
  138. Yang CH, Crowley DE, Menge JA (2001) 16S rDNA fingerprinting of rhizosphere bacterial communities associated with healthy and Phytophthora infected avocado roots. FEMS Microbiol Ecol 35:129–136PubMedGoogle Scholar
  139. Yang G, Zhou B, Zhang X, Zhang Z, Wu Y, Zhang Y, Lu S, Zou Q, Gao Y, Teng L (2016) Effects of tomato root exudates on Meloidogyne incognita. PLoS ONE 3:1.  https://doi.org/10.1371/journal.pone.0154675 CrossRefGoogle Scholar
  140. Yuan J, Zhang N, Huang Q, Raza W, Li R, Vivanco JM, Shen Q (2015) Organic acids from root exudates of banana help root colonization of PGPR strain Bacillus amyloliquefaciens NJN-6. Sci Rep 5:13438PubMedPubMedCentralGoogle Scholar
  141. Zhang N, Wang D, Liu Y, Li S, Shen Q, Zhang R (2013) Effects of different plant root exudates and their organic acid components on chemotaxis, biofilm formation and colonization by beneficial rhizosphere-associated bacterial strains. Plant Soil 374:689–700Google Scholar
  142. Zohora US, Rahman MS, Ano T (2009) Biofilm formation and lipopeptide antibiotic iturin A production in different peptone media. J Environ Sci 21(Supplement 1):S24–S27Google Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2020

Authors and Affiliations

  1. 1.Division of Plant BiologyBose Institute Centenary Campus, CIT Scheme, VII-MKankurgachi, KolkataIndia

Personalised recommendations