The rhizosphere revisited: Root microbiomics

Frontiers in Plant Science

Volumn 4, Issue MAY, 2013, Pages

  Bakker, Peter A H M ^a   Berendsen, Roel L ^a   Doornbos, Rogier F ^a   Wintermans, Paul C A ^a   Pieterse, Corné M J ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Arabidopsis thaliana; Extended phenotype; Microbial communities; Plant roots; Pseudomonas spp

Indexed keywords

EID: 84891605888     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00165     Document Type: Review

References (91)

1. Amann, R. I., Ludwig, W., and Schleifer, K. H. (1995). Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59, 143-169.
2. Badri, D. V., Chaparro, J. M., Manter, D. K., Martinoia, E., and Vivanco, J. M. (2012). Influence of ATP-binding cassette transporters in root exudation of phytoalexins, signals, and in disease resistance. Front. Plant Sci. 3:149. doi: 10.3389/fpls.2012.00149
3. Badri, D. V., Chaparro, J. H., Zhang, R., Shen, Q., and Vivanco, J. M. (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, 4502-4512. doi: 10.1074/jbc.M112.433300
4. Bais, H. P., Weir, T. L., Perry, L. G., Gilroy, S., and Vivanco, J. M. (2006). The role of root exudates in rhizosphere interactions with plants and other organisms. Annu. Rev. Plant Biol. 57, 233-266. doi: 10.1146/annurev.arplant.57.032905.105159
5. Barret, M., Frey-Klett, P., Guillerm-Erckelboudt, A. V., Boutin, M., Guernec, G., and Sarniguet, A. (2009). Effect of wheat roots infected with the pathogenic fungus Gaeumannomyces graminis var. tritici on gene expression of the biocontrol bacterium Pseudomonas fluorescens Pf29Arp. Mol. Plant Microbe Interact. 22, 1611-1623. doi: 10.1094/MPMI-22-12-1611
6. Berendsen, R. L., Pieterse, C. M. J., and Bakker, P. A. H. M. (2012). The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478-486. doi: 10.1016/j.tplants.2012.04.001
7. Berg, G., and Smalla, K. (2009). Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol. Ecol. 68, 1-13. doi: 10.1111/j.1574-6941.2009.00654.x
8. Bulgarelli, D., Rott, M., Schlaeppi, K., Ver Loren van Themaat, E., Ahmadinejad, N., Assenza, F., et al. (2012). Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91-95. doi: 10.1038/nature11336
9. Carvalhais, L. C., Dennis, P. G., Badri, D. V., Tyson, G. W., Vivanco, J. M., and Schenk, P. M. (2013). Activation of the jasmonic acid plant defence pathway alters the composition of columnbreak rhizosphere bacterial communities. PLoS ONE 8:e56457. doi: 10.1371/journal.pone.0056457
10. Chaparro, J. M., Badri, D. V., Bakker, M. G., Sugiyama, A., Manter, D. K., and Vivanco, J. M. (2013). Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with soil microbial functions. PLoS ONE 8:e55731. doi: 10.1371/journal.pone.0055731
11. DeCoste, N. J., Gadkar, V. J., and Filion, M. (2010). Verticillium dahliae alters Pseudomonas spp. populations and HCN gene expression in the rhizosphere of strawberry. Can. J. Microbiol. 56, 906-915. doi: 10.1139/W10-080
12. De Ridder-Duine, A. S., Kowalchuk, G. A., Klein Gunnewiek, P. J. A., Smant, W., Van Veen, J. A., and De Boer, W. (2005). Rhizosphere bacterial community composition in natural stands of Carex arenaria (sand sedge) is determined by bulk soil community composition. Soil Biol. Biochem. 37, 349-357. doi: 10.1016/j.soilbio.2004.08.005
13. Doornbos, R. F., Geraats, B. P. J., Kuramae, E. E., Van Loon, L. C., and Bakker, P. A. H. M. (2011). Effects of jasmonic acid, ethylene, and salicylic acid signaling on the rhizosphere bacterial community of Arabidopsis thaliana. Mol. Plant Microbe Interact. 24, 395-407. doi: 10.1094/MPMI-05-10-0115
14. Doornbos, R. F., Van Loon, L. C., and Bakker, P. A. H. M. (2012). Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. Agron. Sustain. Dev. 32, 227-243. doi: 10.1007/s13593-011-0028-y
15. Eshel, A., and Beeckman, T. (2013). Plant Roots: The Hidden Half, 4th Edn. Boca Raton, FL: CRC Press.
16. Fan, B., Cravalhais, L. C., Becker, A., Fedoseyenko, D., Von Wiren, N., and Borriss, R. (2012). Transcriptomic profiling of Bacillus amyloliquefaciens FZB42 in response to maize root exudates. BMC Microbiol. 12:116. doi: 10.1186/1471-2180-12-116
17. Foster, R. C., Rovira, A. D., and Cock, T. W. (1983). Ultrastructure of the Root-Soil Interface. St. Paul, MN: The American Phytopathological Society.
18. Gao, M., Teplitski, M., Robinson, J. B., and Bauer, D. W. (2003). Production of substances by Medicago truncatulathat affect bacterial quorum sensing. Mol. Plant Microbe Interact. 16, 827-834. doi: 10.1094/MPMI.2003.16.9.827
19. Garbeva, P. V., Van Elsas, J. D., and Van Veen, J. A. (2008). Rhizosphere microbial community and its response to plant species and soil history. Plant Soil 302, 19-32. doi: 10.1007/s11104-007-9432-0
20. Germida, J. J., Siciliano, S. D., De Freitas, J. R., and Seib, A. M. (1998). Diversity of root-associated bacteria associated with field-grown canola (Brassica napus L.) and wheat (Triticum aestivum L.). FEMS Microbiol. Ecol. 26, 43-50. doi: 10.1111/j.1574-6941.1998.tb01560.x
21. Glandorf, D. C. M., Peters, L. G. L., Van der Sluis, I., Bakker, P. A. H. M., and Schippers, B. (1993). Crop specificity of rhizosphere pseudomonads and the involvement of root agglutinins. Soil Biol. Biochem. 25, 981-989. doi: 10.1016/0038-0717(93)90144-Z
22. Gosalbes, M. J., Abellan, J. J., Durban, A., Perez-Cobas, A. E., Latorre, A., and Moya, A. (2012). Metagenomics of human microbiome: beyond 16s rDNA. Clin. Microbiol. Infect. Dis. 18, 47-49. doi: 10.1111/j.1469-0691.2012.03865.x
23. Grayston, S. J., Wang, S., Campbell, C. D., and Edwards, A. C. (1998). Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol. Biochem. 30, 369-378. doi: 10.1016/S0038-0717(97)00124-7
24. Haichar, F. Z., Marol, C., Berge, O., Rangel-Castro, J. I., Prosser, J. I., Balesdent, J., et al. (2008). Plant host habitat and root exudates shape soil bacterial community structure. ISME J. 2, 1221-1230. doi: 10.1038/ismej.2008.80
25. Hartmann, A., Rothballer, M., and Schmid, M. (2008). Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil 312, 7-14. doi: 10.1007/s11104-007-9514-z
26. Hartmann, A., Schmid, M., Van Tuinen, D., and Berg, G. (2009). Plant-driven selection of microbes. Plant Soil 321, 235-257. doi: 10.1007/s11104-008-9814-y
27. Hiltner, L. (1904). Uber neuere Erfahrungen und Probleme auf dem Gebiete der Bodenbakteriologie unter besonderden berucksichtigung und Brache. Arb. Dtsch. Landwirtsch. Gesellschaft 98, 59-78.
28. Hirsch, P. R., and Mauchline, T. H. (2012). Who's who in the plant root microbiome? Nat. Biotechnol. 30, 961-962. doi: 10.1038/nbt.2387
29. Hosni, T., Moretti, C., Devescovi, G., Suarez-Moreno, Z. R., Fatmi, M. B., Guarnaccia, C., et al. (2011). Sharing of quorum-sensing signals and role of interspecies communities in a bacterial plant disease. ISME J. 5, 1857-1870. doi: 10.1038/ismej.2011.65
30. Inceoglu, O., Van Overbeek, L. S., Salles, J. F., and Van Elsas, J. D. (2013). The normal operating range of bacterial communities in soil used for potato cropping. Appl. Environ. Microbiol. 79, 1160-1170. doi: 10.1128/AEM.02811-12
31. Jansson, J. K., Neufeld, J. D., Moran, M. A., and Gilbert, J. A. (2012). Omics for understanding microbial functional dynamics. Environ. Microbiol. 14, 1-3. doi: 10.1111/j.1462-2920.2011.02518.x
32. Jones, D. L., Nguyen, C., and Finlay, R. D. (2009). Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321, 5-33. doi: 10.1007/s11104-009-9925-0
33. Jousset, A., Rochat, L., Lanoue, A., Bonkowski, M., Keel, C., and Scheu, S. (2011). Plants respond to pathogen infection by enhancing the antifungal gene expression of root-associated bacteria. Mol. Plant Microbe Interact. 24, 352-358. doi: 10.1094/MPMI-09-10-0208
34. Kent, A. D., and Triplett, E. W. (2002). Microbial communities and their interactions in soil and rhizosphere ecosystems. Annu. Rev. Microbiol. 56, 211-236. doi: 10.1146/annurev.micro.56.012302.161120
35. Kirk, J. L., Klironomos, J. N., Lee, H., and Trevors, J. T. (2005). The effects of perennial ryegrass and alfalfa on microbial abundance and diversity in petroleum contaminated soil. Environ. Pollut. 133, 455-465. doi: 10.1016/j.envpol.2004.06.002
36. Koch, B., Worm, J., Jensen, L. E., Hojberg, O., and Nybroe, O. (2001). Carbon limitation induces σs-dependent gene expression in Pseudomonas fluorescens in soil. Appl. Environ. Microbiol. 67, 3363-3370. doi: 10.1128/AEM.67.8.3363-3370.2001
37. Kwak, Y. S., Bonsall, R. F., Okubara, P. A., Paulitz, T. C., Thomashow, L. S., and Weller, D. M. (2012). Factors impacting the activity of 2, 4-diacetylphloroglucinol-producing Pseudomonas fluorescens against take-all of wheat. Soil Biol. Biochem. 54, 48-56. doi: 10.1016/j.soilbio.2012.05.012
38. Kyselkova, M., Kopecky, J., Frapolli, M., Defago, G., Sagova-Mareckova, M., Grundmann, G. L., et al. (2009). Comparison of rhizobacterial community composition in soil suppressive or conducive to tobacco black root rot disease. ISME J. 3, 1127-1138. doi: 10.1038/ismej.2009.61
39. Lakshmanan, V., Kitto, S. L., Caplan, J. L., Hsueh, Y. H., Kearns, D. B., Wu, Y. S., et al. (2012). Microbe-associated molecular patterns-triggered root responses mediate beneficial rhizobacterial recruitment in Arabidopsis. Plant Physiol. 160, 1642-1661. doi: 10.1104/pp.112.200386
40. Lee, B., Lee, S., and Ryu, M. R. (2012). Foliar aphid feeding recruits rhizosphere bacteria and primes plant immunity against pathogenic and non-pathogenic bacteria in pepper. Ann. Bot. 110, 281-290. doi: 10.1093/aob/mcs055
41. Lemanceau, P., Corberand, T., Gardan, L., Latour, X., Laguerre, G., Boeufgras, J.-M., et al. (1995). Effect of two plant species, flax (Linum usitatissimum L.) and tomato (Lycopersicon esculentum Mill.), on the diversity of soilborne populations of fluorescent pseudomonads. Appl. Environ. Microbiol. 61, 1004-1012.
42. Leveau, J. H. J. (2007). The magic and menace of metagenomics: prospects for the study of plant growth-promoting rhizobacteria. Eur. J. Plant Pathol. 119, 279-300. doi: 10.1007/s10658-007-9186-9
43. Liu, F., Bian, Z., Jia, Z., Zhao, Q., and Song, S. (2012). The GCR1 and GPA1 participate in promotion of Arabidopsisprimary root elongation induced by N-acyl-homoserine lactones, the bacterial quorum-sensing signals. Mol. Plant Microbe Interact. 25, 677-683. doi: 10.1094/MPMI-10-11-0274
44. Lugtenberg, B., and Kamilova, F. (2009). Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63, 541-556. doi: 10.1146/annurev.micro.62.081307. 162918
45. Lundberg, D. S., Lebeis, S. L., Herrera Paredes, S., Yourstone, S., Gehring, J., Malfatti, S., et al. (2012). Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86-90. doi: 10.1038/nature11237
46. Marasco, R., Rolli, E., Ettoumi, B., Vigani, G., Mapelli, F., Borin, S., et al. (2012). A drought resistance-promoting microbiome is selected by root system under desert farming. PLoS ONE 7:e48479. doi: 10.1371/journal.pone.0048479
47. Mark, G. L., Dow, J. M., Kiely, P. D., Higgings, H., Haynes, J., Baysse, C., et al. (2005). Transcriptome profiling of bacterial responses to root exudates identifies genes involved in microbe-plant interactions. Proc. Natl. Acad. Sci. U.S.A. 102, 17454-17459. doi: 10.1073/pnas.0506407102
48. Mathesius, U., Mulders, S., Gao, M., Teplitski, M., Caetano-Anolles, G., Rolfe, B. G., et al. (2003). Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc. Natl. Acad. Sc. U.S.A. 100, 1444-1449. doi: 10.1073/pnas.262672599
49. Matilla, M. A., Ramos, J. L., Bakker, P. A. H. M., Doornbos, R. F., Vivanco, J. M., Badri, D. V., et al. (2010). Pseudomonas putida KT2440 causes induced systemic resistance and changes in Arabidopsis root exudation. Environ. Microbiol. Rep. 2, 381-388. doi: 10.1111/j.1758-2229.2009.00091.x
50. Mavrodi, O. V., Mavrodi, D. V., Parejko, J. A., Thomashow, L. S., and Weller, D. M. (2012). Irrigation differentially impacts populations of indigenous antibiotic-producing Pseudomonas spp. in the rhizosphere of wheat. Appl. Environ. Microbiol. 78, 3214-3220. doi: 10.1128/AEM.07968-11
51. Mazurier, S., Corberand, T., Lemanceau, P., and Raaijmakers, J. M. (2009). Phenazine antibiotics produced by fluorescent pseudomonads contribute to natural soil suppressiveness to Fusarium wilt. ISME J. 3, 977-991. doi: 10.1038/ismej.2009.33
52. Mazzola, M. (2002). Mechanisms of natural soil suppressiveness to soilborne diseases. Antonie Van Leeuwenhoek 81, 557-564. doi: 10.1023/A:1020557523557
53. Mendes, R., Kruijt, M., De Bruijn, I., Dekkers, E., Van der Voort, M., Schneider, J. H. M., et al. (2011). Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332, 1097-1100. doi: 10.1126/science.1203980
54. Micallef, S. A., Channer, S., Shiaris, M. P., and Colon-Carmona, A. (2009a). Plant age and genotype impact the progression of bacterial community succession in the Arabidopsis rhizosphere. Plant Signal. Behav. 4, 777-780. doi: 10.4161/psb.4.8.9229
55. Micallef, S. A., Shiaris, M. P., and Colon-Carmona, A. (2009b). Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. J. Exp. Bot. 60, 1729-1742. doi: 10.1093/jxb/erp053
56. Miethling, R., Wieland, G., Backhaus, H., and Tebbe, C. C. (2000). Variation in microbial rhizosphere communities in response to crop species, soil origin, and inoculation with Sinorhizobium meliloti L33. Microb. Ecol.
57. Miller, M. B., and Bassler, B. L. (2001). Quorum sensing in bacteria. Annu. Rev. Microbiol. 55, 165-199. doi: 10.1146/annurev.micro.55.1.165
58. Moree, W. J., Phelan, V. V., Wu, C.-H., Bandeira, N., Cornett, D. S., Duggan, B. M., et al. (2012). Interkingdom metabolic transformations captured by microbial imaging mass spectrometry. Proc. Natl. Acad. Sci. U.S.A. 109, 13811-13816. doi: 10.1073/pnas.1206855109
59. Neal, A. L., Ahmad, S., Gordon-Weeks, R., and Ton, J. (2012). Benzoxazinoids in root exudates of maize attract Pseudomonas putida to the rhizosphere. PLoS ONE 7:e35498. doi: 10.1371/journal.pone.0035498
60. Normander, B., and Prosser, J. I. (2000). Bacterial origin and community composition in the barley phytosphere as a function of habitat and presowing conditions. Appl. Environ. Microbiol. 66, 4372-4377. doi: 10.1128/AEM.66.10.4372-4377.2000
61. Okubara, P. A., and Bonsall, R. F. (2008). Accumulation of Pseudomonas-derived 2, 4-diacetylphloroglucinol on wheat seedling roots is influenced by host cultivar. Biol. Control 46, 322-331. doi: 10.1016/j.biocontrol.2008.03.013
62. Pechy-Tarr, M., Borel, N., Kupferschmied, P., Turner, V., Binggeli, O., Radovanovic, D., et al. (2013). Control and host-dependent activation of insect toxin expression in a root-associated biocontrol pseudomonad. Environ. Microbiol. 15, 736-750. doi: 10.1111/1462-2920.12050
63. Pierson, L. S., and Pierson, E. A. (2007). Roles of diffusible signals in communication among plant-associated bacteria. Phytopathology 97, 227-232. doi: 10.1094/PHYTO-97-2-0227
64. Raaijmakers, J. M., and Weller, D. M. (1998). Natural plant protection by 2, 4-diacetylphloroglucinol-producing Pseudomonas spp. in take-all decline soils. Mol. Plant Microbe Interact. 11, 144-152. doi: 10.1094/MPMI.1998.11.2.144
65. Rosenzweig, N., Tiedje, J. M., Quensen, J. F., Meng, Q., and Hao, J. J. (2012). Microbial communities associated with potato common scab-suppressive soil determined by pyrosequencing analyses. Plant Dis. 96, 718-725. doi: 10.1094/PDIS-07-11-0571
66. Rovira, A. D. (1969). Plant root exudates. Bot. Rev. 35, 17-34. doi: 10.1007/BF02859887
67. Rudrappa, T., Czymmek, K. J., Paré, P. W., and Bais, H. P. (2008). Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol. 148, 1547-1556. doi: 10.1104/pp.108.127613
68. Ruffner, B., Pechy-Tarr, M., Ryffel, F., Hoegger, P., Obrist, C., Rindlisbacher, A., et al. (2013). Oral insecticidal activity of plant-associated pseudomonads. Eviron. Microbiol. 15, 751-763. doi: 10.1111/j.1462-2920.2012.02884.x
69. Sanguin, H., Sarniguet, A., Gazengel, K., Moenne-Loccoz, Y., and Grundmann, G. L. (2009). Rhizosphere bacterial communities associated with disease suppressiveness stages of take-all decline in wheat monoculture. New Phytol. 184, 694-707. doi: 10.1111/j.1469-8137.2009.03010.x
70. Schenk, S. T., Stein, E., Kogel, K. H., and Schikora, A. (2012). Arabidopsis growth and defense are modulated by bacterial quorum sensing molecules. Plant Signal. Behav. 7, 178-181. doi: 10.4161/psb.18789
71. Schikora, A., Schenk, S. T., Stein, E., Molitor, A., Zuccaro, A., and Kogel, K. H. (2011). N-acyl-homoserine lactone confers resistance toward biotrophic and hemibiotrophic pathogens via altered activation of AtMPK6. Plant Physiol. 157, 1407-1418. doi: 10.1104/pp.111.180604
72. Schreiner, K., Hagn, A., Kyselkova, M., Moenne-Loccoz, Y., Welzl, G., Munch, J. C., et al. (2010). Comparison of barley succession and take-all disease as environmental factors shaping the rhizobacterial community during take-all decline. Appl. Environ. Microbiol. 76, 4703-4712. doi: 10.1128/AEM.00481-10
73. Schuhegger, R., Ihring, A., Gantner, S., Bahnweg, G., Knappe, C., Vogg, G., et al. (2006). Induction of systemic resistance in tomato by N-acyl-L-homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ. 29, 909-918. doi: 10.1111/j.1365-3040.2005.01471.x
74. Schwachtje, J., Karojet, S., Thormalen, I., Bernholz, C., Kunz, S., Brouwer, S., et al. (2011). A naturally associated rhizobacterium of Arabidopsis thaliana induces a starvation-like transcriptional response while promoting growth. PLoS ONE 6:e29382. doi: 10.1371/journal.pone.0029382
75. Smalla, K., Wieland, G., Buchner, A., Zock, A., Parzy, J., Kaiser, S., et al. (2001). Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl. Environ. Microbiol. 67, 4742-4751. doi: 10.1128/AEM.67.10.4742-4751.2001
76. Sorensen, J., Hauberg Nicolaisen, M., Ron, E., and Simonet, P. (2009). Molecular tools in rhizosphere microbiology-from single-cell to whole-community analysis. Plant Soil 321, 483-512. doi: 10.1007/s11104-009-9946-8
77. Teplitski, M., Robinson, J. B., and Bauer, W. D. (2000). Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol. Plant Microbe Interact. 13, 637-648. doi: 10.1094/MPMI.2000.13.6.637
78. Traxler, M. F., and Kolter, R. (2012). A massively spectacular view of the chemical lives of microbes. Proc. Natl. Acad. Sci. U.S.A. 109, 10128-10129. doi: 10.1073/pnas.1207725109
79. Urich, T., Lanzen, A., Qi, J., Huson, D. H., Schleper, C., and Schuster, S. C. (2008). Simultaneous assessment of soil microbial community structure and function through analysis of the meta-transcriptome. PLoS ONE 3:e2527. doi: 10.1371/journal.pone.0002527
80. Van de Mortel, J. E., De Vos, R. C. H., Dekkers, E., Pineda, A., Guillod, L., Bouwmeester, K., et al. (2012). Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol. 160, 2173-2188. doi: 10.1104/pp.112.207324
81. Van Overbeek, L. S., Van Elsas, J. D., and van Veen, J. A. (1997). Pseudomonas fluorescens Tn5-B20 mutant RA92 responds to carbon limitation in soil. FEMS Microbiol. Ecol. 24, 57-71. doi: 10.1016/S0168-6496(97)00045-7
82. Von Rad, U., Klein, I., Dobrev, P. I., Kottova, J., Zazimalova, E., Fekete, A., et al. (2008). Response of Arabidopsis thaliana to N-hexanoyl-DL-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere. Planta 229, 73-85. doi: 10.1007/s00425-008-0811-4
83. Vorholt, J. A. (2012). Microbial life in the phyllosphere. Nat. Rev. Microbiol. 10, 828-840. doi: 10.1038/nrmicro2910
84. Walker, T. S., Bais, H. P., Grotewold, E., and Vivanco, J. M. (2003). Root exudation and rhizosphere biology. Plant Physiol. 132, 44-51. doi: 10.1104/pp.102.019661
85. Watrous, J., Roach, P., Alexandrov, T., Heath, B. S., Yang, J. Y., Kersten, R. D., et al. (2012). Mass spectral molecular networking of living microbial colonies. Proc. Natl. Acad. Sci. U.S.A. 109, E1743-E1752. doi: 10.1073/pnas.1203689109
86. Weinert, N., Piceno, Y., Ding, G. C., Meincke, R., Heuer, H., Berg, G., et al. (2011). PhyloChip hybridization uncovered an enormous bacterial diversity in the rhizosphere of different potato cultivars: many common and few cultivar-dependent taxa. FEMS Microbiol. Ecol. 75, 497-506. doi: 10.1111/j.1574-6941.2010.01025.x
87. Weller, D. M., Raaijmakers, J. M., McSpadden Gardener, B. B., and Thomashow, L. S. (2002). Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu. Rev. Phytopathol. 40, 309-348. doi: 10.1146/annurev.phyto.40.030402.110010
88. Yang, J. W., Yi, H. S., Kim, H., Lee, B., Lee, S., Ghim, S. Y., et al. (2011). Whitefly infestation of pepper plants elicits defence responses against bacterial pathogens in leaves and roots and changes the below-ground microflora. J. Ecol. 99, 46-56. doi: 10.1111/j.1365-2745.2010.01756.x
89. Zamioudis, C., and Pieterse, C. M. J. (2012). Modulation of host immunity by beneficial microbes. Mol. Plant Microbe Interact. 25, 139-150. doi: 10.1094/MPMI-06-11-0179
90. Zancarini, A., Mougel, C., Voisin, A. S., Prudent, M., Salon, C., and Munier-Jolain, N. (2012). Soil nitrogen availability and plant genotype modify the nutrition strategies of M. truncatula and the associated rhizosphere microbial communities. PLoS ONE 7:e47096. doi: 10.1371/journal.pone.0047096
91. Zysko, A., Sanguin, H., Hayes, A., Wardleworth, L., Zeef, L. A. H., Sim, A., et al. (2012). Transcriptional response of Pseudomonas aeruginosa to a phosphate-deficient Lolium perenne rhizosphere. Plant Soil 359, 25-44. doi: 10.1007/s11104-011-1060-z