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Going back to the roots: the microbial ecology of the rhizosphere

Key Points

  • The rhizosphere microbiome is important for plant growth, nutrition and health in agro-ecosystems, but it also directly and/or indirectly affects the composition, biomass and functioning of plant communities in natural ecosystems.

  • The phylum Proteobacteria is the dominant bacterial phylum encountered in the rhizosphere, but fungi such as those in the phyla Ascomycota and Glomeromycota are also an integral component of the rhizosphere microbiome.

  • Soil properties and plant species are the main drivers of the microbial community composition and structure in the rhizosphere.

  • Multitrophic interactions in the rhizosphere, as well as their influence on above-ground communities of herbivores, carnivores, mutualists and symbionts, can be beneficial to plant growth.

  • Integrating our knowledge from both agricultural and natural ecosystems, from single plants and multispecies plant communities, and from below-ground and above-ground multitrophic interactions holds great promise to further improve the sustainability of crop production.

Abstract

The rhizosphere is the interface between plant roots and soil where interactions among a myriad of microorganisms and invertebrates affect biogeochemical cycling, plant growth and tolerance to biotic and abiotic stress. The rhizosphere is intriguingly complex and dynamic, and understanding its ecology and evolution is key to enhancing plant productivity and ecosystem functioning. Novel insights into key factors and evolutionary processes shaping the rhizosphere microbiome will greatly benefit from integrating reductionist and systems-based approaches in both agricultural and natural ecosystems. Here, we discuss recent developments in rhizosphere research in relation to assessing the contribution of the micro- and macroflora to sustainable agriculture, nature conservation, the development of bio-energy crops and the mitigation of climate change.

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Figure 1: Microorganisms in the rhizosphere.
Figure 2: The rhizosphere.
Figure 3: The composition of the bacterial community in the rhizosphere.
Figure 4: Root-induced changes in the rhizosphere.

References

  1. 1

    Berendsen, R., Pieterse, C. & Bakker, P. The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478–486 (2012).

    CAS  PubMed  Google Scholar 

  2. 2

    Mendes, R. et al. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332, 1097–1100 (2011). This paper describes a metataxonomic analysis of naturally disease-suppressive soil to identify consortia of rhizosphere bacteria that protect plants from fungal infections.

    CAS  PubMed  Google Scholar 

  3. 3

    Bonfante, P. & Anca, I. A. Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu. Rev. Microbiol. 63, 363–383 (2009).

    CAS  PubMed  Google Scholar 

  4. 4

    Kardol, P., Cornips, N. J., van Kempen, M. M. L., Bakx-Schotman, J. M. T. & van der Putten, W. H. Microbe-mediated plant–soil feedback causes historical contingency effects in plant community assembly. Ecol. Monogr. 77, 147–162 (2007).

    Google Scholar 

  5. 5

    Schnitzer, S. A. et al. Soil microbes drive the classic plant diversity–productivity pattern. Ecology 92, 296–303 (2011).

    PubMed  Google Scholar 

  6. 6

    Bennett, A. E. & Bever, J. D. Mycorrhizal species differentially alter plant growth and response to herbivory. Ecology 88, 210–218 (2007).

    PubMed  Google Scholar 

  7. 7

    Hol, W. H. G. et al. Reduction of rare soil microbes modifies plant–herbivore interactions. Ecol. Lett. 13, 292–301 (2010).

    PubMed  Google Scholar 

  8. 8

    Behie, S. W., Zelisko, P. M. & Bidochka, M. J. Endophytic insect–parasitic fungi translocate nitrogen directly from insects to plants. Science 336, 1576–1577 (2012).

    CAS  PubMed  Google Scholar 

  9. 9

    Vannette, R. L. & Rasmann, S. Arbuscular mycorrhizal fungi mediate below-ground plant–herbivore interactions: a phylogenetic study. Funct. Ecol. 26, 1033–1042 (2012).

    Google Scholar 

  10. 10

    Bever, J. D., Platt, T. G. & Morton, E. R. Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Annu. Rev. Microbiol. 66, 265–283 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. 11

    Pineda, A., Zheng, S. J., van Loon, J. J. A., Pieterse, C. M. J. & Dicke, M. Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci. 15, 507–514 (2010).

    CAS  PubMed  Google Scholar 

  12. 12

    Bulgarelli, D. et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91–95 (2012). A report describing the structure of the microbial community colonizing A. thaliana roots, as analysed using next-generation sequencing and catalysed reporter deposition fluorescence in situ hybridization approaches.

    CAS  Google Scholar 

  13. 13

    Lundberg, D. S. et al. Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86–93 (2012). A paper describing the application of a metagenomics approach to the analysis of the microbiomes of more than 600 A. thaliana plants.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. 14

    Prosser, J. I., Rangel-Castro, J. I. & Killham, K. Studying plant–microbe interactions using stable isotope technologies. Curr. Opin. Biotechnol. 17, 98–102 (2006).

    CAS  PubMed  Google Scholar 

  15. 15

    Mommer, L., Wagemaker, C., de Kroon, H. & Ouborg, N. Unravelling below-ground plant distributions: a real-time polymerase chain reaction method for quantifying species proportions in mixed root samples. Mol. Ecol. Res. 8, 947–953 (2008).

    CAS  Google Scholar 

  16. 16

    Kesanakurti, P. et al. Spatial patterns of plant diversity below-ground as revealed by DNA barcoding. Mol. Ecol. 20, 1289–1302 (2011).

    PubMed  Google Scholar 

  17. 17

    Reinhart, K., Tytgat, T., Van der Putten, W. & Clay, K. Virulence of soil-borne pathogens and invasion by Prunus serotina. New Phytol. 186, 484–495 (2010).

    PubMed  Google Scholar 

  18. 18

    Whitham, T. G. et al. A framework for community and ecosystem genetics: from genes to ecosystems. Nature Rev. Genet. 7, 510–523 (2006).

    CAS  PubMed  Google Scholar 

  19. 19

    Schweitzer, J. et al. Plant–soil–microorganism interactions: heritable relationship between plant genotype and associated soil microorganisms. Ecology 8, 773–781 (2008).

    Google Scholar 

  20. 20

    Lau, J. A. & Lennon, J. T. Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc. Natl Acad. Sci. USA 109, 14058–14062 (2012).

    CAS  PubMed  Google Scholar 

  21. 21

    Bever, J., Broadhurst, L. & Thrall, P. Microbial phylotype composition and diversity predicts plant productivity and plant–soil feedbacks. Ecol. Lett. 16, 164–174 (2013).

    Google Scholar 

  22. 22

    Ayres, E. et al. Home-field advantage accelerates leaf litter decomposition in forests. Soil Biol. Biochem. 41, 606–610 (2009).

    CAS  Google Scholar 

  23. 23

    Piskiewicz, A. M., Duyts, H., Berg, M. P., Costa, S. R. & van der Putten, W. H. Soil microorganisms control plant ectoparasitic nematodes in natural coastal foredunes. Oecologia 152, 505–514 (2007).

    PubMed  PubMed Central  Google Scholar 

  24. 24

    Kulmatiski, A., Beard, K. H. & Heavilin, J. Plant–soil feedbacks provide an additional explanation for diversity–productivity relationships. Proc. Biol. Sci. 279, 3020–3026 (2012). A model (based on empirical data) that explains how overyielding in mixed plant communities can be explained by a net reduction of negative interactions between plants and (rhizosphere) soil biota.

    PubMed  PubMed Central  Google Scholar 

  25. 25

    Costa, R. et al. Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiol. Ecol. 56, 236–249 (2006).

    CAS  PubMed  Google Scholar 

  26. 26

    Dias, A. C. F. et al. Potato cultivar type affects the structure of ammonia oxidizer communities in field soil under potato beyond the rhizosphere. Soil Biol. Biochem. 50, 85–95 (2012).

    CAS  Google Scholar 

  27. 27

    Garbeva, P., van Elsas, J. D. & van Veen, J. A. Rhizosphere microbial community and its response to plant species and soil history. Plant Soil 302, 19–32 (2008).

    CAS  Google Scholar 

  28. 28

    Smalla, K. et al. 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 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. 29

    Teixeira, L. et al. Bacterial diversity in rhizosphere soil from Antarctic vascular plants of Admiralty Bay, maritime Antarctica. ISME J. 4, 989–1001 (2010).

    PubMed  Google Scholar 

  30. 30

    DeAngelis, K. M. et al. Selective progressive response of soil microbial community to wild oat roots. ISME J. 3, 168–178 (2009).

    CAS  PubMed  Google Scholar 

  31. 31

    Gomes, N. C. M. et al. Bacterial diversity of the rhizosphere of maize (Zea mays) grown in tropical soil studied by temperature gradient gel electrophoresis. Plant Soil 232, 167–180 (2001).

    CAS  Google Scholar 

  32. 32

    Sharma, S., Aneja, M. K., Mayer, J., Munch, J. C. & Schloter, M. Characterization of bacterial community structure in rhizosphere soil of grain legumes. Microb. Ecol. 49, 407–415 (2005).

    CAS  PubMed  Google Scholar 

  33. 33

    Peiffer, J. et al. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc. Natl Acad. Sci. USA 110, 6548–6553 (2013).

    CAS  PubMed  Google Scholar 

  34. 34

    Uroz, S., Buee, M., Murat, C., Frey-Klett, P. & Martin, F. Pyrosequencing reveals a contrasted bacterial diversity between oak rhizosphere and surrounding soil. Environ. Microbiol. Rep. 2, 281–288 (2010).

    CAS  PubMed  Google Scholar 

  35. 35

    Vandenkoornhuyse, P. et al. Active root-inhabiting microbes identified by rapid incorporation of plant-derived carbon into RNA. Proc. Natl Acad. Sci. 104, 16970–16975 (2007).

    CAS  PubMed  Google Scholar 

  36. 36

    Hannula, S. E., Boschker, H. T. S., de Boer, W. & van Veen, J. A. 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. New Phytol. 194, 784–799 (2012).

    CAS  PubMed  Google Scholar 

  37. 37

    Berg, G. & Smalla, K. Plant species and soil types cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol. Ecol. 68, 1–13 (2009).

    CAS  Google Scholar 

  38. 38

    de Ridder-Duine, A. S. et al. 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 (2005).

    CAS  Google Scholar 

  39. 39

    Santos-Gonzalez, J. C., Nallanchakravarthula, S., Alstrom, S. & Finlay, R. D. Soil, but not cultivar, shapes the structure of arbuscular mycorrhizal fungal assemblages associated with strawberry. Microb. Ecol. 62, 25–35 (2011).

    PubMed  Google Scholar 

  40. 40

    Andrew, D. R. et al. Abiotic factors shape microbial diversity in Sonoran desert soils. Appl. Environ. Microbiol. 78, 7527–7537 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. 41

    Inceoglu, O., Salles, J. F. & van Elsas, J. D. Soil and cultivar type shape the bacterial community in the potato rhizosphere. Microb. Ecol. 63, 460–470 (2012).

    CAS  PubMed  Google Scholar 

  42. 42

    Lennon, J. & Jones, S. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nature Rev. Microbiol. 9, 119–130 (2011).

    CAS  Google Scholar 

  43. 43

    Fierer, N. & Jackson, R. B. The diversity and biogeography of soil bacterial communities. Proc. Natl Acad. Sci. USA 103, 626–631 (2006).

    CAS  PubMed  Google Scholar 

  44. 44

    Kowalchuk, G. B., Buma, D. S., De Boer, W., Klinkhamer, P. & van Veen, J. A. Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Antonie Van Leeuwenhoek 81, 509–520 (2002).

    PubMed  Google Scholar 

  45. 45

    Bergsma-Vlami, M., Prins, M. E. & Raaijmakers, J. M. Influence of plant species on population dynamics, genotypic diversity and antibiotic production in the rhizosphere by indigenous Pseudomonas spp. FEMS Microbiol. Ecol. 52, 59–69 (2005).

    CAS  PubMed  Google Scholar 

  46. 46

    Pivato, B. et al. Medicago species affect the community composition of arbuscular mycorrhizal fungi associated with roots. New Phytol. 176, 197–210 (2007).

    CAS  PubMed  Google Scholar 

  47. 47

    Haichar, F. E. et al. Plant host habitat and root exudates shape soil bacterial community structure. ISME J. 2, 1221–1230 (2008).

    CAS  PubMed  Google Scholar 

  48. 48

    Bressan, M. et al. Exogenous glucosinolate produced by Arabidopsis thaliana has an impact on microbes in the rhizosphere and plant roots. ISME J. 3, 1243–1257 (2009).

    CAS  PubMed  Google Scholar 

  49. 49

    Ladygina, N. & Hedlund, K. Plant species influence microbial diversity and carbon allocation in the rhizosphere. Soil Biol. Biochem. 42, 162–168 (2010).

    CAS  Google Scholar 

  50. 50

    Callaway, R. M. et al. Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89, 1043–1055 (2008).

    PubMed  Google Scholar 

  51. 51

    Guo, Z.-Y., Kong, C.-H., Wang, J.-G. & Wang, Y.-F. Rhizosphere isoflavones (daidzein and genistein) levels and their relation to the microbial community structure of mono-cropped soybean soil in field and controlled conditions. Soil Biol. Biochem. 43, 2257–2264 (2011).

    CAS  Google Scholar 

  52. 52

    Hassan, S. & Mathesius, U. The role of flavonoids in root–rhizosphere signalling: opportunities and challenges for improving plant–microbe interactions. J. Exp. Bot. 63, 3429–3444 (2012).

    CAS  PubMed  Google Scholar 

  53. 53

    Mathesius, U. et al. Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc. Natl Acad. Sci. USA 100, 1444–1449 (2003).

    CAS  PubMed  Google Scholar 

  54. 54

    Morris, P., Bone, E. & Tyler, B. Chemotropic and contact responses of Phytophthora sojae hyphae to soybean isoflavonoids and artificial substrates. Plant Physiol. 117, 1171–1178 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. 55

    Perez-Montano, F. et al. Nodulation-gene-inducing flavonoids increase overall production of autoinducers and expression of N-acyl homoserine lactone synthesis genes in rhizobia. Res. Microbiol. 162, 715–723 (2011).

    CAS  PubMed  Google Scholar 

  56. 56

    Kowalchuk, G., Hol, W. & van Veen, J. Rhizosphere fungal communities are influenced by Senecio jacobaea pyrrolizidine alkaloid content and composition. Soil Biol. Biochem. 38, 2852–2859 (2006).

    CAS  Google Scholar 

  57. 57

    Mazzola, M., Funnell, D. L. & Raaijmakers, J. M. Wheat cultivar-specific selection of 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas species from resident soil populations. Microb. Ecol. 48, 338–348 (2004).

    CAS  PubMed  Google Scholar 

  58. 58

    Yao, H. Y. & Wu, F. Z. Soil microbial community structure in cucumber rhizosphere of different resistance cultivars to fusarium wilt. FEMS Microbiol. Ecol. 72, 456–463 (2010).

    CAS  PubMed  Google Scholar 

  59. 59

    Hardoim, P. R. et al. Rice root-associated bacteria: insights into community structures across 10 cultivars. FEMS Microbiol. Ecol. 77, 154–164 (2012).

    Google Scholar 

  60. 60

    Bouffaud, M.-L. et al. Is diversification history of maize influencing selection of soil bacteria by roots? Mol. Ecol. 21, 195–206 (2012).

    PubMed  Google Scholar 

  61. 61

    Weinert, N. et al. 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 (2011).

    CAS  PubMed  Google Scholar 

  62. 62

    Germida, J. & Siciliano, J. Taxonomic diversity of baceria associated with the roots of modern, recent and ancient wheat cultivars. Biol. Fertil. Soils 33, 410–415 (2001).

    Google Scholar 

  63. 63

    Smith, K. P., Handelsman, J. & Goodman, R. M. Genetic basis in plants for interactions with disease-suppressive bacteria. Proc. Natl Acad. Sci. USA 96, 4786–4790 (1999).

    CAS  PubMed  Google Scholar 

  64. 64

    Nelson, E. Microbial dynamics and interactions in the spermosphere. Annu. Rev. Phytopathol. 42, 271–309 (2004).

    CAS  PubMed  Google Scholar 

  65. 65

    Lugtenberg, B. & Kamilova, F. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63, 541–556 (2009).

    CAS  PubMed  Google Scholar 

  66. 66

    Hardoim, P. R., Hardoim, C. C. P., van Overbeek, L. S. & van Elsas, J. D. Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS ONE 7, e30438 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. 67

    Normander, B. & Prosser, J. I. Bacterial origin and community composition in the barley phytosphere as a function of habitat and presowing conditions. Appl. Environ. Microbiol. 66, 4372–4377 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. 68

    Johnston-Monje, D. & Raizada, M. N. Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS ONE 6, e20396 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. 69

    Hausmann, N. & Hawkes, C. Plant neighborhood control of arbuscular mycorrhizal community composition. New Phytol. 183, 1188–1200 (2009).

    PubMed  Google Scholar 

  70. 70

    De Deyn, G. B., Raaijmakers, C. E., van Ruijven, J., Berendse, F. & van der Putten, W. H. Plant species identity and diversity effects on different trophic levels of nematodes in the soil food web. Oikos 106, 576–586 (2004).

    Google Scholar 

  71. 71

    Bezemer, T. M. et al. Divergent composition but similar function of soil food webs of individual plants: plant species and community effects. Ecology 91, 3027–3036 (2010).

    CAS  PubMed  Google Scholar 

  72. 72

    Bakker, M., Bradeen, J. & Kinkel, L. L. Effects of plant host species and plant community richness on streptomycete community structure. FEMS Microbiol. Ecol. 83, 596–606 (2012).

    PubMed  Google Scholar 

  73. 73

    van Overbeek, L. & van Elsas, J. D. Effects of plant genotype and growth stage on the structure of bacterial communities associated with potato (Solanum tuberosum L.). FEMS Microbiol. Ecol. 64, 283–296 (2008).

    CAS  PubMed  Google Scholar 

  74. 74

    Inceoglu, O., Salles, J. F., van Overbeek, L. & van Elsas, J. D. Effects of plant genotype and growth stage on the β-proteobacterial communities associated with different potato cultivars in two fields. Appl. Environ. Microbiol. 76, 3675–3684 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  75. 75

    Dumbrell, A. et al. Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing. New Phytol. 190, 794–804 (2011).

    CAS  PubMed  Google Scholar 

  76. 76

    Mougel, C. et al. Dynamic of the genetic structure of bacterial and fungal communities at different developmental stages of Medicago truncatula Gaertn. cv. Jemalong line J5. New Phytol. 170, 165–175 (2006).

    CAS  PubMed  Google Scholar 

  77. 77

    Folman, L. B., Postma, J. & Van Veen, J. A. Ecophysiological characterization of rhizosphere bacterial communities at different root locations and plant developmental stages of cucumber grown on rockwool. Microb. Ecol. 42, 586–597 (2001).

    CAS  PubMed  Google Scholar 

  78. 78

    Oldroyd, G. E. D. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nature Rev. Microbiol. 11, 252–263 (2013).

    CAS  Google Scholar 

  79. 79

    Ruyter-Spira, C., Al-Babili, S., van der Krol, S. & Bouwmeester, H. The biology of strigolactones. Trends Plant Sci. 18, 72–83 (2013).

    CAS  PubMed  Google Scholar 

  80. 80

    Schnee, C. et al. The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc. Natl Acad. Sci. USA 103, 1129–1134 (2006).

    CAS  PubMed  Google Scholar 

  81. 81

    Bouwmeester, H. J., Roux, C., Lopez-Raez, J. A. & Becard, G. Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci. 12, 224–230 (2007).

    CAS  PubMed  Google Scholar 

  82. 82

    Rasmann, S. et al. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434, 732–737 (2005).

    CAS  PubMed  Google Scholar 

  83. 83

    Macfarlane, S. Molecular determinants of the transmission of plant viruses by nematodes. Mol. Plant. Pathol. 4, 211–215 (2003).

    CAS  PubMed  Google Scholar 

  84. 84

    Cho, H. B. & Winans, S. C. VirA and VirG activate the Ti plasmid repABC operon, elevating plasmid copy number in response to wound-released chemical signals. Proc. Natl Acad. Sci. USA 102, 14843–14848 (2005).

    CAS  PubMed  Google Scholar 

  85. 85

    Wu, H.-S. et al. Effects of vanillic acid on the growth and development of Fusarium oxysporum f. sp niveum. Allelopathy J. 22, 111–121 (2008).

    Google Scholar 

  86. 86

    van West, P. et al. Oomycete plant pathogens use electric fields to target roots. Mol. Plant Microbe Interact. 15, 790–798 (2002).

    CAS  PubMed  Google Scholar 

  87. 87

    Wang, E. T. et al. A common signaling process that promotes mycorrhizal and momycete colonization of plants. Curr. Biol. 22, 2242–2246 (2012).

    CAS  PubMed  Google Scholar 

  88. 88

    Ercolin, F. & Reinhardt, D. Successful joint ventures of plants: arbuscular mycorrhiza and beyond. Trends Plant Sci. 16, 356–362 (2011).

    CAS  PubMed  Google Scholar 

  89. 89

    Govindarajulu, M. et al. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435, 819–823 (2005).

    CAS  PubMed  Google Scholar 

  90. 90

    Gange, A. C. Species-specific responses of a root- and shoot-feeding insect to arbuscular mycorrhizal colonization of its host plant. New Phytol. 150, 611–618 (2001).

    Google Scholar 

  91. 91

    Jones, K. M., Kobayashi, H., Davies, B. W., Taga, M. E. & Walker, G. C. How rhizobial symbionts invade plants: the SinorhizobiumMedicago model. Nature Rev. Microbiol. 5, 619–633 (2007).

    CAS  Google Scholar 

  92. 92

    Masson-Boivin, C., Giraud, E., Perret, X. & Batut, J. Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends Microbiol. 17, 458–466 (2009).

    CAS  PubMed  Google Scholar 

  93. 93

    Bever, J. D. et al. Rooting theories of plant community ecology in microbial interactions. Trends Ecol. Evol. 25, 468–478 (2010).

    PubMed  PubMed Central  Google Scholar 

  94. 94

    Maillet, F. et al. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469, 58–63 (2011).

    CAS  PubMed  Google Scholar 

  95. 95

    Yehuda, Z., Shenker, M., Hadar, Y. & Chen, Y. N. Remedy of chlorosis induced by iron deficiency in plants with the fungal siderophore rhizoferrin. J. Plant Nutr. 23, 1991–2006 (2000).

    CAS  Google Scholar 

  96. 96

    Vansuyt, G., Robin, A., Briat, J. F., Curie, C. & Lemanceau, P. Iron acquisition from Fe-pyoverdine by Arabidopsis thaliana. Mol. Plant Microbe Interact. 20, 441–447 (2007).

    CAS  PubMed  Google Scholar 

  97. 97

    Cook, R. J. et al. Molecular mechanisms of defence by rhizobacteria against root disease. Proc. Natl Acad. Sci. USA 92, 4197–4201 (1995). A founding paper on strategies for the genetic analysis of mechanisms of soil-borne-disease suppression by rhizobacteria.

    CAS  PubMed  Google Scholar 

  98. 98

    Haas, D. & Defago, G. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature Rev. Microbiol. 3, 307–319 (2005).

    CAS  Google Scholar 

  99. 99

    Raaijmakers, J. M. & Mazzola, M. Diversity and natural functions of antibiotics produced by beneficial and plant pathogenic bacteria. Annu. Rev. Phytopath. 50, 403–424 (2012).

    CAS  Google Scholar 

  100. 100

    Davies, J., Spiegelman, G. B. & Yim, G. The world of subinhibitory antibiotic concentrations. Curr. Opin. Microbiol. 9, 445–453 (2006).

    CAS  PubMed  Google Scholar 

  101. 101

    Romero, D., Traxler, M. F., Lopez, D. & Kolter, R. Antibiotics as signal molecules. Chem. Rev. 111, 5492–5505 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  102. 102

    Yim, G., Wang, H. H. & Davies, J. Antibiotics as signalling molecules. Phil. Trans. R. Soc. B 362, 1195–1200 (2007).

    CAS  PubMed  Google Scholar 

  103. 103

    Deveau, A. et al. 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, 560–568 (2010).

    CAS  PubMed  Google Scholar 

  104. 104

    Founoune, H. et al. Mycorrhiza helper bacteria stimulated ectomycorrhizal symbiosis of Acacia holosericea with Pisolithus alba. New Phytol. 153, 81–89 (2002).

    Google Scholar 

  105. 105

    Pivato, B., Gamalero, E., Lemanceau, P. & Berta, G. Colonization of adventitious roots of Medicago truncatula by Pseudomonas fluorescens C7R12 as affected by arbuscular mycorrhiza. FEMS Microbiol. Lett. 289, 173–180 (2008).

    CAS  PubMed  Google Scholar 

  106. 106

    Offre, P. et al. Identification of bacterial groups preferentially associated with mycorrhizal roots of Medicago truncatula. Appl. Environ. Microbiol. 73, 913–921 (2007).

    CAS  PubMed  Google Scholar 

  107. 107

    Scheublin, T. R., Sanders, I. R., Keel, C. & van der Meer, J. R. Characterisation of microbial communities colonising the hyphal surfaces of arbuscular mycorrhizal fungi. ISME J. 4, 752–763 (2010).

    PubMed  Google Scholar 

  108. 108

    Wardle, D. A. et al. Ecological linkages between aboveground and belowground biota. Science 304, 1629–1633 (2004).

    CAS  PubMed  Google Scholar 

  109. 109

    van der Heijden, M. G. A. et al. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 69–72 (1998).

    CAS  Google Scholar 

  110. 110

    Laakso, J. & Setala, H. Sensitivity of primary production to changes in the architecture of belowground food webs. Oikos 87, 57–64 (1999).

    Google Scholar 

  111. 111

    Wagg, C., Jansa, J., Schmid, B. & van der Heijden, M. G. A. Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol. Lett. 14, 1001–1009 (2011).

    PubMed  Google Scholar 

  112. 112

    Soler Gamborena, R., Bezemer, T. M., van der Putten, W. H., Vet, L. E. M. & Harvey, J. A. Root herbivore effects on aboveground herbivore, parasitoid and hyperparasitoid performance via changes in plant quality. J. Anim. Ecol. 74, 1121–1134 (2005).

    Google Scholar 

  113. 113

    Staley, J. T., Mortimer, S. R., Morecroft, M. D., Brown, V. K. & Masters, G. J. Summer drought alters plant-mediated competition between foliar- and root-feeding insect. Glob. Change Biol. 13, 866–877 (2007).

    Google Scholar 

  114. 114

    Zamioudis, C. & Pieterse, C. M. J. Modulation of host immunity by beneficial microbes. Mol. Plant Microbe Interact. 25, 139–150 (2012).

    CAS  PubMed  Google Scholar 

  115. 115

    de Roman, M. et al. Elicitation of foliar resistance mechanisms transiently impairs root association with arbuscular mycorrhizal fungi. J. Ecol. 99, 36–45 (2011).

    CAS  Google Scholar 

  116. 116

    Kostenko, O., van de Voorde, T. F. J., Mulder, P. P. J., van der Putten, W. H. & Bezemer, T. M. Legacy effects of aboveground–belowground interactions. Ecol. Lett. 15, 813–821 (2012).

    PubMed  Google Scholar 

  117. 117

    Conrath, U. et al. Priming: getting ready for battle. Mol. Plant Microbe Interact. 19, 1062–1071 (2006).

    CAS  PubMed  Google Scholar 

  118. 118

    Joosten, L., Mulder, P. P. J., Klinkhamer, P. G. L. & van Veen, J. A. Soil-borne microorganisms and soil-type affect pyrrolizidine alkaloids in Jacobaea vulgaris. Plant Soil 325, 133–143 (2009).

    CAS  Google Scholar 

  119. 119

    van de Mortel, J. E. et al. Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol. 160, 2173–2188 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  120. 120

    Fontaine, S. et al. Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450, 277–280 (2007).

    CAS  Google Scholar 

  121. 121

    Clemmensen, K. E. et al. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339, 1615–1618 (2013).

    CAS  PubMed  Google Scholar 

  122. 122

    Philippot, L., Hallin, S., Borjesson, G. & Baggs, E. M. Biochemical cycling in the rhizosphere having an impact on global change. Plant Soil 321, 61–81 (2009).

    CAS  Google Scholar 

  123. 123

    Henry, S. et al. Disentangling the rhizosphere effect on nitrate reducers and denitrifiers: insight into the role of root exudates. Environ. Microbiol. 10, 3082–3092 (2008).

    CAS  PubMed  Google Scholar 

  124. 124

    Philippot, L. & Hallin, S. Towards food, feed and energy crops mitigating climate change. Trends Plant Sci. 16, 476–480 (2011).

    CAS  PubMed  Google Scholar 

  125. 125

    Hawkes, C., Wren, I., Herman, D. & Firestone, M. K. Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol. Lett. 8, 976–985 (2005).

    Google Scholar 

  126. 126

    Subbarao, G. V. et al. Evidence for biological nitrification inhibition in Brachiaria pastures. Proc. Natl Acad. Sci. USA 106, 17302–17307 (2009).

    CAS  PubMed  Google Scholar 

  127. 127

    Aanderud, Z. T. & Bledsoe, C. S. Preferences for 15N-ammonium, 15N-nitrate, and 15N-glycine differ among dominant exotic and subordinate native grasses from a California oak woodland. Environ. Exp. Bot. 65, 205–209 (2009).

    CAS  Google Scholar 

  128. 128

    Lee, M., Flory, S. & Phillips, R. Positive feedbacks to growth of an invasive grass through alteration of nitrogen cycling. Oecologia 170, 457–465 (2012).

    PubMed  Google Scholar 

  129. 129

    Rossiter-Rachor, N. et al. Invasive Andropogon gayanus (gamba grass) is an ecosystem transformer of nitrogen relations in Australian savanna Ecol. Appl. 19, 1546–1560 (2009).

    CAS  PubMed  Google Scholar 

  130. 130

    Boudsocq, S. et al. Plant preference for ammonium versus nitrate: a neglected determinant of ecosystem functioning? Am. Nat. 180, 60–69 (2012).

    CAS  PubMed  Google Scholar 

  131. 131

    Wardle, D. A., Nicholson, K. S., Ahmed, M. & Rahman, A. Interference effects of the invasive plant Carduus nutans L. against the nitrogen-fixation ability of Trifolium repens L. Plant Soil 163, 287–297 (1994).

    CAS  Google Scholar 

  132. 132

    Dassonville, N., Guillaumaud, N., Piola, F., Meerts, P. & Poly, F. Niche construction by the invasive Asian knotweeds (species complex Fallopia): impact on activity, abundance and community structure of denitrifiers and nitrifiers. Biol. Invas. 13, 1115–1133 (2011).

    Google Scholar 

  133. 133

    Kardol, P. & Wardle, D. A. How understanding aboveground–belowground linkages can assist restoration ecology. Trends Ecol. Evol. 25, 670–679 (2012).

    Google Scholar 

  134. 134

    Grman, E. & Suding, K. N. Within-year soil legacies contribute to strong priority effects of exotics on native California grassland communities. Restor. Ecol. 18, 664–670 (2010). A keystone paper showing that the effects of plant growth can be 'memorized' by soils because the plants can change biotic and abiotic soil properties such that the performance of subsequent plant species can be promoted or reduced. These specific effects on subsequent plant species might change the priorities of one plant species over another and thus change plant community composition and functioning.

    Google Scholar 

  135. 135

    de Vries, F. T. et al. Land use alters the resistance and resilience of soil food webs to drought. Nature Clim. Chang. 2, 276–280 (2012). This article provides experimental evidence showing that soils with a high proportion of fungi are more resistant and resilient to drought stress.

    Google Scholar 

  136. 136

    Kulmatiski, A., Beard, K. H. & Stark, J. M. Soil history as a primary control on plant invasion in abandoned agricultural fields. J. Appl. Ecol. 43, 868–876 (2006).

    Google Scholar 

  137. 137

    Yelenik, S. G. & Levine, J. M. Native shrub reestablishment in exotic annual grasslands: do ecosystem processes recover? Ecol. Appl. 20, 716–727 (2010).

    CAS  PubMed  Google Scholar 

  138. 138

    Haase, S., Philippot, L., Neumann, G., Marhan, S. & Kandeler, E. Local response of bacterial densities and enzyme activities to elevated atmospheric CO2 and different N supply in the rhizosphere of Phaseolus vulgaris L. Soil Biol. Biochem. 40, 1225–1234 (2008).

    CAS  Google Scholar 

  139. 139

    Stevnbak, K. et al. Interactions between above- and belowground organisms modified in climate change experiments. Nature Clim. Change 2, 805–808 (2012).

    CAS  Google Scholar 

  140. 140

    Drigo, B. et al. Impacts of 3 years of elevated atmospheric CO2 on rhizosphere carbon flow and microbial community dynamics. Glob. Change Biol. 19, 621–636 (2013).

    Google Scholar 

  141. 141

    Dong, Y. H. et al. Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411, 813–817 (2001).

    CAS  PubMed  Google Scholar 

  142. 142

    Lorenc-Kukula, K., Jafra, S., Oszmianski, J. & Szopa, J. Ectopic expression of anthocyanin 5-O-glucosyltransferase in potato tuber causes increased resistance to bacteria. J. Agr. Food Chem. 53, 272–281 (2005).

    CAS  Google Scholar 

  143. 143

    Zeller, S. L., Kalinina, O. & Schmid, B. Costs of resistance to fungal pathogens in genetically modified wheat. J. Plant Ecol. 6, 92–100 (2012).

    Google Scholar 

  144. 144

    Adler, P. R., Del Grosso, S. J. & Parton, W. J. Life-cycle assessment of net greenhouse-gas flux for bioenergy cropping systems. Ecol. Appl. 17, 675–691 (2007).

    PubMed  Google Scholar 

  145. 145

    Tilman, D. et al. Beneficial biofuels — the food, energy, and environment trilemma. Science 325, 270–271 (2009).

    CAS  PubMed  Google Scholar 

  146. 146

    Jesus, E. C. et al. Bacterial communities in the rhizosphere of biofuel crops grown on marginal lands as evaluated by 16S rRNA gene pyrosequences. Bioenergy Res. 3, 20–27 (2010).

    Google Scholar 

  147. 147

    Lambers, H., Mougel, C., Jaillard, B. & Hinsinger, P. Plant–microbe–soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321, 83–115 (2009).

    CAS  Google Scholar 

  148. 148

    Turner, T., James, E. & Poole, P. The plant microbiome. Genome Biol. 14, 209 (2013).

    PubMed  PubMed Central  Google Scholar 

  149. 149

    Babikova, Z. et al. Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecol. Lett. 16, 835–843 (2013).

    PubMed  Google Scholar 

  150. 150

    Bissett, A., Brown, M. V., Siciliano, S. D. & Thrall, P. H. Microbial community responses to anthropogenically induced environmental change: towards a systems approach. Ecol. Lett. 16, 128–139 (2013).

    PubMed  Google Scholar 

  151. 151

    Jones, D., Nguyen, C. & Finlay, D. R. Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant Soil 321, 5–33 (2009).

    CAS  Google Scholar 

  152. 152

    Bais, H., Weir, T., Perry, L., Gilroy, S. & Vivanco, J. The role of root exudates in rhizosphere interactions with plants and other organisms. Annu. Rev. Plant Biol. 57, 233–266 (2006).

    CAS  PubMed  Google Scholar 

  153. 153

    Bru, D. et al. Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale. ISME J. 5, 532–542 (2011).

    CAS  Google Scholar 

  154. 154

    Hinsinger, P., Bengough, A. G., Vetterlein, D. & Young, I. M. Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321, 117–152 (2009).

    CAS  Google Scholar 

  155. 155

    Tsednee, M., Mak, Y. W., Chen, Y. R. & Yeh, K. C. A sensitive LC-ESI-Q-TOF-MS method reveals novel phytosiderophores and phytosiderophore–iron complexes in barley. New Phytol. 195, 951–961 (2012).

    CAS  PubMed  Google Scholar 

  156. 156

    McNear, D. H. Jr. The rhizosphere — roots, soil and everything in between. Nature Education Knowledge 4, 1 (2013).

    Google Scholar 

  157. 157

    Lakshmann, V. et al. Microbe-associated molecular patterns-triggered root responses mediate beneficial rhizobacterial recruitment in Arabidopsis. Plant Physiol. 160, 1642–1661 (2012).

    Google Scholar 

  158. 158

    Parniske, M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Rev. Microbiol. 6, 763–775 (2008).

    CAS  Google Scholar 

  159. 159

    Blossfeld, S., Gansert, D., Thiele, B., Kuhn, A. & Lösch, R. The dynamics of oxygen concentration, pH value, and organic acids in the rhizosphere of Juncus spp. Soil Biol. Biochem. 43, 1186–1197 (2011).

    CAS  Google Scholar 

  160. 160

    Blossfeld, S., Schreiber, C. M., Liebsch, G., Kuhn, A. J. & Hinsinger, P. Quantitative imaging of rhizosphere pH and CO2 dynamics with planar optodes. Ann. Bot. 112, 267–276 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  161. 161

    Spohn, M., Carminati, A. & Kuzyakov, Y. Soil zymography — a novel in situ method for mapping distribution of enzyme activity in soil. Soil Biol. Biochem. 58, 275–280 (2013).

    CAS  Google Scholar 

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Acknowledgements

The authors thank A. Spor for comments on the manuscript and for his help, together with M. van der Voort, on figure 3. This work was supported by the European Commission through the Ecological Function and Biodiversity Indicators in European Soils (EcoFINDERS) project (FP7-264465). The contribution by J.M.R. was funded, in part, by the Dutch BE-Basic Program and by the Ecogenomics Innovation Center (ECOLINC) of the Netherlands Genomics Initiative.

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Glossary

Mycorrhizal fungi

Fungi that form a mutualistic, symbiotic association with a plant.

r-strategists

Organisms that thrive in unstable or fluctuating environments where resources are abundant, unlike K-strategists, which are more competitive in stable environments with limited resources.

Microbial seed bank

A reservoir of dormant microorganisms.

Cultivar

A variety of plant that has been selected for specific traits.

Endophytic bacteria

Bacteria that live inside plant tissue without causing negative effects.

Amensalism

An association between two different species that is detrimental to individuals of one species but not to those of the other. The secretion of chemical compounds by one species, thus damaging or killing the other species, is the most common mechanism of amensalism.

Phyllosphere

The above-ground parts of plants, mostly the leaves.

Denitrification

A microbial anaerobic respiratory pathway that consists of the sequential reduction of soluble nitrate and nitrite to the nitrogen gases NO, N2O and N2.

Nitrification

A two-step aerobic process consisting of the oxidation of ammonia to nitrite, which is carried out by the ammonia-oxidizing betaproteobacteria and thaumarchaeotes, and the subsequent conversion of nitrite to nitrate, which is carried out by nitrite-oxidizing bacteria.

Ecological engineering

The application of ecological principles for sustainable management of ecosystems, including preservation, restoration and creation, to integrate human society with its natural environment for the benefit of both.

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Philippot, L., Raaijmakers, J., Lemanceau, P. et al. Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11, 789–799 (2013). https://doi.org/10.1038/nrmicro3109

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