1932

Abstract

Microorganisms colonizing plant surfaces and internal tissues provide a number of life-support functions for their host. Despite increasing recognition of the vast functional capabilities of the plant microbiome, our understanding of the ecology and evolution of the taxonomically hyperdiverse microbial communities is limited. Here, we review current knowledge of plant genotypic and phenotypic traits as well as allogenic and autogenic factors that shape microbiome composition and functions. We give specific emphasis to the impact of plant domestication on microbiome assembly and how insights into microbiomes of wild plant relatives and native habitats can contribute to reinstate or enrich for microorganisms with beneficial effects on plant growth, development, and health. Finally, we introduce new concepts and perspectives in plant microbiome research, in particular how community ecology theory can provide a mechanistic framework to unravel the interplay of distinct ecological processes—i.e., selection, dispersal, drift, diversification—that structure the plant microbiome.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-090817-062524
2019-09-08
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/73/1/annurev-micro-090817-062524.html?itemId=/content/journals/10.1146/annurev-micro-090817-062524&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Adame-Alvarez RM, Mendiola-Soto J, Heil M 2014. Order of arrival shifts endophyte-pathogen interactions in bean from resistance induction to disease facilitation. FEMS Microbiol. Lett. 355:100–7
    [Google Scholar]
  2. 2. 
    Aira M, Gómez-Brandón M, Cristina Lazcano C, Bååth E, Domínguez J 2010. Plant genotype strongly modifies the structure and growth of maize rhizosphere microbial communities. Soil Biol. Biochem. 42:2276–81
    [Google Scholar]
  3. 3. 
    Badri DV, Quintana N, El Kassis EG, Kim HK, Choi YH et al. 2009. An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota. Plant Physiol 151:2006–17Pioneering work on the impact of changes in rhizosphere chemistry on microbiome assembly.
    [Google Scholar]
  4. 4. 
    Bai Y, Muller DB, Srinivas G, Garrido-Oter R, Potthoff E et al. 2015. Functional overlap of the Arabidopsis leaf and root microbiota. Nature 528:364–69Defined bacterial communities and gnotobiotic plant system to study bacterial community establishment and functions.
    [Google Scholar]
  5. 5. 
    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. 57:233–66Comprehensive review on the role of root exudates in plant-plant and plant-microbe interactions.
    [Google Scholar]
  6. 6. 
    Bakker PAHM, Pieterse CMJ, de Jonge R, Berendsen RL 2018. The soil-borne legacy. Cell 172:1178–80
    [Google Scholar]
  7. 7. 
    Beckers B, Op De Beeck M, Weyens N, Van Acker R, Van Montagu M et al. 2016. Lignin engineering in field-grown poplar trees affects the endosphere bacterial microbiome. PNAS 113:2312–17
    [Google Scholar]
  8. 8. 
    Berendsen RL, Vismans G, Yu K, Song Y, de Jonge R et al. 2018. Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME J 12:1496–507
    [Google Scholar]
  9. 9. 
    Berg G, Koberl M, Rybakova D, Muller H, Grosch R, Smalla K 2017. Plant microbial diversity is suggested as the key to future biocontrol and health trends. FEMS Microbiol. Ecol. 93: https://doi.org/10.1093/femsec/fix050
    [Crossref] [Google Scholar]
  10. 10. 
    Berg G, Raaijmakers JM. 2018. Saving seed microbiomes. ISME J 12:1167–70
    [Google Scholar]
  11. 11. 
    Bitocchi E, Bellucci E, Giardini A, Rau D, Rodriguez M et al. 2013. Molecular analysis of the parallel domestication of the common bean (Phaseolus vulgaris) in Mesoamerica and the Andes. New Phytol 197:300–13
    [Google Scholar]
  12. 12. 
    Blaser MJ. 2017. The theory of disappearing microbiota and the epidemics of chronic diseases. Nat. Rev. Immunol. 17:461–63
    [Google Scholar]
  13. 13. 
    Bodenhausen N, Bortfeld-Miller M, Ackermann M, Vorholt JA 2014. A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. PLOS Genet 10:e1004283
    [Google Scholar]
  14. 14. 
    Boles BR, Thoendel M, Singh PK 2004. Self-generated diversity produces “insurance effects” in biofilm communities. PNAS 101:16630–35
    [Google Scholar]
  15. 15. 
    Brown P, Saa S. 2015. Biostimulants in agriculture. Front. Plant Sci. 6:671
    [Google Scholar]
  16. 16. 
    Brusetti L, Francia P, Bertolini C, Pagliuca A, Borin S et al. 2004. Bacterial communities associated with the rhizosphere of transgenic Bt 176 maize (Zea mays) and its non transgenic counterpart. Plant Soil 266:11–21
    [Google Scholar]
  17. 17. 
    Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J et al. 2015. Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392–403
    [Google Scholar]
  18. 18. 
    Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N et al. 2012. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95
    [Google Scholar]
  19. 19. 
    Cardinale M, Grube M, Erlacher A, Quehenberger J, Berg G 2015. Bacterial networks and co-occurrence relationships in the lettuce root microbiota. Environ. Microbiol. 17:239–52
    [Google Scholar]
  20. 20. 
    Carrión VJ, Cordovez V, Tyc O, Etalo DW, de Bruijn I et al. 2018. Involvement of Burkholderiaceae and sulfurous volatiles in disease-suppressive soils. ISME J 12:2307–21
    [Google Scholar]
  21. 21. 
    Carvalhais LC, Dennis PG, Badri DV, Kidd BN, Vivanco JM, Schenk PM 2015. Linking jasmonic acid signaling, root exudates, and rhizosphere microbiomes. Mol. Plant Microbe Interact. 28:1049–58
    [Google Scholar]
  22. 22. 
    Cha J-Y, Han S, Hong H-J, Cho H, Kim D et al. 2016. Microbial and biochemical basis of a Fusarium wilt-suppressive soil. ISME J 10:119–29
    [Google Scholar]
  23. 23. 
    Chaparro JM, Badri DV, Vivanco JM 2014. Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803
    [Google Scholar]
  24. 24. 
    Chapelle E, Mendes R, Bakker PA, Raaijmakers JM 2016. Fungal invasion of the rhizosphere microbiome. ISME J 10:265–68
    [Google Scholar]
  25. 25. 
    Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, Gross S, Clingenpeel S et al. 2016. Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol 209:798–811
    [Google Scholar]
  26. 26. 
    Cordovez V, Carrion VJ, Etalo DW, Mumm R, Zhu H et al. 2015. Diversity and functions of volatile organic compounds produced by Streptomyces from a disease-suppressive soil. Front. Microbiol. 6:1081
    [Google Scholar]
  27. 27. 
    Crits-Christoph A, Diamond S, Butterfield CN, Thomas BC, Banfield JF 2018. Novel soil bacteria possess diverse genes for secondary metabolite biosynthesis. Nature 558:440–44
    [Google Scholar]
  28. 28. 
    Di Giovanni GD, Watrud LS, Seidler RJ, Widmer F 1999. Comparison of parental and transgenic alfalfa rhizosphere bacterial communities using Biolog GN metabolic fingerprinting and enterobacterial repetitive intergenic consensus sequence-PCR (ERIC-PCR). Microb. Ecol. 37:129–39
    [Google Scholar]
  29. 29. 
    Dicke M. 2009. Behavioural and community ecology of plants that cry for help. Plant Cell Environ 32:654–65
    [Google Scholar]
  30. 30. 
    Dini-Andreote F, Andreote FD, Araujo WL, Trevors JT, van Elsas JD 2012. Bacterial genomes: habitat specificity and uncharted organisms. Microb. Ecol. 64:1–7
    [Google Scholar]
  31. 31. 
    Doebley JF, Gaut BS, Smith BD 2006. The molecular genetics of crop domestication. Cell 127:1309–21
    [Google Scholar]
  32. 32. 
    Doornbos RF, van Loon LC, Bakker PAHM 2012. Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere: a review. Agron. Sustain. Dev. 32:227–43
    [Google Scholar]
  33. 33. 
    Dunfield KE, Germida JJ. 2001. Diversity of bacterial communities in the rhizosphere and root interior of field-grown genetically modified Brassica napus. FEMS Microbiol. Ecol 38:1–9
    [Google Scholar]
  34. 34. 
    Durán P, Thiergart T, Garrido-Oter R, Agler M, Kemen E et al. 2018. Microbial interkingdom interactions in roots promote Arabidopsis survival. Cell 175:973–83
    [Google Scholar]
  35. 35. 
    Edwards J, Johnson C, Santos-Medellin C, Lurie E, Podishetty NK et al. 2015. Structure, variation, and assembly of the root-associated microbiomes of rice. PNAS 112:E911–20A multistep model underlying microbiome assembly in different root compartments.
    [Google Scholar]
  36. 36. 
    Etalo DW, Jeon JS, Raaijmakers JM 2018. Modulation of plant chemistry by beneficial root microbiota. Nat. Prod. Rep. 35:398–409
    [Google Scholar]
  37. 37. 
    Fukami T. 2015. Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu. Rev. Ecol. Evol. Syst. 46:1–23
    [Google Scholar]
  38. 38. 
    Giauque H, Connor EW, Hawkes CV 2019. Endophyte traits relevant to stress tolerance, resource use and habitat of origin predict effects on host plants. New Phytol 221:2239–49
    [Google Scholar]
  39. 39. 
    Gibbons SM, Scholz M, Hutchison AL, Dinner AR, Gilbert JA, Coleman ML 2016. Disturbance regimes predictably alter diversity in an ecologically complex bacterial system. mBio 7:e01372–16
    [Google Scholar]
  40. 40. 
    Giovannoni SJ, Cameron Thrash J, Temperton B 2014. Implications of streamlining theory for microbial ecology. ISME J 8:1553–65
    [Google Scholar]
  41. 41. 
    Gómez Expósito R, de Bruijn I, Postma J, Raaijmakers JM 2017. Current insights into the role of rhizosphere bacteria in disease suppressive soils. Front. Microbiol. 8:2529
    [Google Scholar]
  42. 42. 
    Grube M, Cardinale M, de Castro JV Jr, Muller H, Berg G 2009. Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME J 3:1105–15
    [Google Scholar]
  43. 43. 
    Hacquard S, Garrido-Oter R, Gonzalez A, Spaepen S, Ackermann G et al. 2015. Microbiota and most nutrition across plant and animal kingdoms. Cell Host Microbe 17:603–16
    [Google Scholar]
  44. 44. 
    Haichar FZ, Marol C, Berge O, Rangel-Castro JI, Prosser JI et al. 2008. Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221
    [Google Scholar]
  45. 45. 
    Hardoim PR, Hardoim CC, van Overbeek LS, van Elsas JD 2012. Dynamics of seed-borne rice endophytes on early plant growth stages. PLOS ONE 7:e30438
    [Google Scholar]
  46. 46. 
    Hardoim PR, van Overbeek LS, Berg G, Pirttila AM, Compant S et al. 2015. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol. Mol. Biol. Rev. 79:293–320Thorough review on the evolution and ecology of plant-endophyte interactions.
    [Google Scholar]
  47. 47. 
    Hardoim PR, van Overbeek LS, Elsas JD 2008. Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–71
    [Google Scholar]
  48. 48. 
    Haudry A, Cenci A, Ravel C, Bataillon T, Brunel D et al. 2007. Grinding up wheat: a massive loss of nucleotide diversity since domestication. Mol. Biol. Evol. 24:1506–17
    [Google Scholar]
  49. 49. 
    Hein JW, Wolfe GV, Blee KA 2008. Comparison of rhizosphere bacterial communities in Arabidopsis thaliana mutants for systemic acquired resistance. Microb. Ecol. 55:333–43
    [Google Scholar]
  50. 50. 
    Helfrich EJN, Vogel CM, Ueoka R, Schafer M, Ryffel F et al. 2018. Bipartite interactions, antibiotic production and biosynthetic potential of the Arabidopsis leaf microbiome. Nat. Microbiol. 3:909–19
    [Google Scholar]
  51. 51. 
    Herrera Paredes S, Gao T, Law TF, Finkel OM, Mucyn T et al. 2018. Design of synthetic bacterial communities for predictable plant phenotypes. PLOS Biol 16:e2003962A method for predicting causality between microbiome composition and host phenotypes.
    [Google Scholar]
  52. 52. 
    Horton MW, Bodenhausen N, Beilsmith K, Meng D, Muegge BD et al. 2014. Genome-wide association study of Arabidopsis thaliana leaf microbial community. Nat. Commun. 5:5320
    [Google Scholar]
  53. 53. 
    Hu L, Robert CAM, Cadot S, Zhang X, Ye M et al. 2018. Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat. Commun. 9:2738
    [Google Scholar]
  54. 54. 
    Huang X-F, Chaparro JM, Reardon KF, Zhang R, Shen Q, Vivanco JM 2014. Rhizosphere interactions: root exudates, microbes, and microbial communities. Botany 92:267–75
    [Google Scholar]
  55. 55. 
    Jousset A, Rochat L, Lanoue A, Bonkowski M, Keel C, Scheu S 2011. Plants respond to pathogen infection by enhancing the antifungal gene expression of root-associated bacteria. Mol. Plant Microbe Interact. 24:352–58
    [Google Scholar]
  56. 56. 
    Kiers ET, Hutton MG, Denison RF 2007. Human selection and the relaxation of legume defences against ineffective rhizobia. Proc. Biol. Sci. 274:3119–26
    [Google Scholar]
  57. 57. 
    Kim DR, Jeon CW, Shin JH, Weller DM, Thomashow L, Kwak YS 2019. Function and distribution of a lantipeptide in strawberry Fusarium wilt disease-suppressive soils. Mol. Plant Microbe Interact. 32:306–12
    [Google Scholar]
  58. 58. 
    Kim JJ, Sundin GW. 2000. Regulation of the rulAB mutagenic DNA repair operon of Pseudomonas syringae by UV-B (290 to 320 nanometers) radiation and analysis of rulAB-mediated mutability in vitro and in planta. J. Bacteriol. 182:6137–44
    [Google Scholar]
  59. 59. 
    Klassen JL. 2018. Defining microbiome function. Nat. Microbiol. 3:864–69
    [Google Scholar]
  60. 60. 
    Knapp DG, Németh JB, Barry K, Hainaut M, Henrissat B et al. 2018. Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi. Sci. Rep. 8:6321
    [Google Scholar]
  61. 61. 
    Knief C, Delmotte N, Chaffron S, Stark M, Innerebner G et al. 2012. Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J 6:1378–90
    [Google Scholar]
  62. 62. 
    Kniskern JM, Traw MB, Bergelson J 2007. Salicylic acid and jasmonic acid signaling defense pathways reduce natural bacterial diversity on Arabidopsis thaliana. Mol. Plant Microbe Interact 20:1512–22
    [Google Scholar]
  63. 63. 
    Kong HG, Kim BK, Song GC, Lee S, Ryu C-M 2016. Aboveground whitefly infestation-mediated reshaping of the root microbiota. Front. Microbiol. 7:1314
    [Google Scholar]
  64. 64. 
    Koziol L, Schultz PA, House GL, Bauer JT, Middleton EL, Bever JD 2018. The plant microbiome and native plant restoration: the example of native mycorrhizal fungi. BioScience 68:996–1006
    [Google Scholar]
  65. 65. 
    Kwak M-J, Kong HG, Choi K, Kwon S-K, Song JY et al. 2018. Rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nat. Biotechnol 36:1100–9. Correction. 2018. Nat. Biotechnol 36:1117
    [Google Scholar]
  66. 66. 
    Lauber CL, Ramirez KS, Aanderud Z, Lennon J, Fierer N 2013. Temporal variability in soil microbial communities across land-use types. ISME J 7:1641–50
    [Google Scholar]
  67. 67. 
    Lebeis SL, Paredes SH, Lundberg DS, Breakfield N, Gehring J et al. 2015. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349:860–64
    [Google Scholar]
  68. 68. 
    Lee B, Lee S, Ryu CM 2012. Foliar aphid feeding recruits rhizosphere bacteria and primes plant immunity against pathogenic and non-pathogenic bacteria in pepper. Ann. Bot. 110:281–90
    [Google Scholar]
  69. 69. 
    Leff JW, Lynch RC, Kane NC, Fierer N 2017. Plant domestication and the assembly of bacterial and fungal communities associated with strains of the common sunflower, Helianthus annuus. New Phytol. 214:412–23
    [Google Scholar]
  70. 70. 
    Legay N, Baxendale C, Grigulis K, Krainer U, Kastl E et al. 2014. Contribution of above- and below-ground plant traits to the structure and function of grassland soil microbial communities. Ann. Bot. 114:1011–21
    [Google Scholar]
  71. 71. 
    Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM et al. 2004. The metacommunity concept: a framework for multi-scale community ecology. Ecol. Lett. 7:601–13
    [Google Scholar]
  72. 72. 
    Lennon JT, Jones SE. 2011. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat. Rev. Microbiol. 9:119
    [Google Scholar]
  73. 73. 
    Leveau JH, Lindow SE. 2001. Appetite of an epiphyte: quantitative monitoring of bacterial sugar consumption in the phyllosphere. PNAS 98:3446–53
    [Google Scholar]
  74. 74. 
    Levy A, Salas Gonzalez I, Mittelviefhaus M, Clingenpeel S, Herrera Paredes S et al. 2018. Genomic features of bacterial adaptation to plants. Nat. Genet. 50:138–50
    [Google Scholar]
  75. 75. 
    Lilley AK, Hails RS, Cory JS, Bailey MJ 1997. The dispersal and establishment of pseudomonad populations in the phyllosphere of sugar beet by phytophagous caterpillars. FEMS Microbiol. Ecol. 24:151–57
    [Google Scholar]
  76. 76. 
    Lindemann SR, Bernstein HC, Song H-S, Fredrickson JK, Fields MW et al. 2016. Engineering microbial consortia for controllable outputs. ISME J 10:2077
    [Google Scholar]
  77. 77. 
    Lindow SE, Brandl MT. 2003. Microbiology of the phyllosphere. Appl. Environ. Microbiol. 69:1875–83
    [Google Scholar]
  78. 78. 
    Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J et al. 2012. Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90
    [Google Scholar]
  79. 79. 
    Maldonado-Gomez MX, Martinez I, Bottacini F, O'Callaghan A, Ventura M et al. 2016. Stable engraftment of Bifidobacterium longum AH1206 in the human gut depends on individualized features of the resident microbiome. Cell Host Microbe 20:515–26
    [Google Scholar]
  80. 80. 
    Matos A, Kerkhof L, Garland JL 2005. Effects of microbial community diversity on the survival of Pseudomonas aeruginosa in the wheat rhizosphere. Microb. Ecol. 49:257–64
    [Google Scholar]
  81. 81. 
    McCutcheon JP, Moran NA. 2011. Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10:13–26
    [Google Scholar]
  82. 82. 
    Mendes LW, de Lima Brossi MJ, Kuramae EE, Tsai SM 2015. Land-use system shapes soil bacterial communities in Southeastern Amazon region. Appl. Soil Ecol. 95:151–60
    [Google Scholar]
  83. 83. 
    Mendes LW, Raaijmakers JM, de Hollander M, Mendes R, Tsai SM 2018. Influence of resistance breeding in common bean on rhizosphere microbiome composition and function. ISME J 12:212–24
    [Google Scholar]
  84. 84. 
    Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M et al. 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–100
    [Google Scholar]
  85. 85. 
    Mendes R, Raaijmakers JM. 2015. Cross-kingdom similarities in microbiome functions. ISME J 9:1905–7
    [Google Scholar]
  86. 86. 
    Michelsen CF, Watrous J, Glaring MA, Kersten R, Koyama N et al. 2015. Nonribosomal peptides, key biocontrol components for Pseudomonas fluorescens In5, isolated from a Greenlandic suppressive soil. mBio 6:e00079
    [Google Scholar]
  87. 87. 
    Mommer L, Cotton TEA, Raaijmakers JM, Termorshuizen AJ, van Ruijven J et al. 2018. Lost in diversity: the interactions between soil-borne fungi, biodiversity and plant productivity. New Phytol 218:542–53
    [Google Scholar]
  88. 88. 
    Mutch LA, Young JP. 2004. Diversity and specificity of Rhizobium leguminosarum biovar viciae on wild and cultivated legumes. Mol. Ecol. 13:2435–44
    [Google Scholar]
  89. 89. 
    Neal AL, Ton J. 2013. Systemic defense priming by Pseudomonas putida KT2440 in maize depends on benzoxazinoid exudation from the roots. Plant Signal. Behav. 8:e22655
    [Google Scholar]
  90. 90. 
    Nemergut DR, Schmidt SK, Fukami T, O'Neill SP, Bilinski TM et al. 2013. Patterns and processes of microbial community assembly. Microbiol. Mol. Biol. Rev. 77:342–56
    [Google Scholar]
  91. 91. 
    Niu B, Paulson JN, Zheng X, Kolter R 2017. Simplified and representative bacterial community of maize roots. PNAS 114:E2450–59Development of a minimum effective bacterial consortium capable of antagonizing a fungal pathogen.
    [Google Scholar]
  92. 92. 
    Oyserman BO, Medema MH, Raaijmakers JM 2018. Road MAPs to engineer host microbiomes. Curr. Opin. Microbiol. 43:46–54
    [Google Scholar]
  93. 93. 
    Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG et al. 2013. Diversity and heritability of the maize rhizosphere microbiome under field conditions. PNAS 110:6548–53
    [Google Scholar]
  94. 94. 
    Pérez-Jaramillo JE, Carrión VJ, Bosse M, Ferrao LFV, de Hollander M et al. 2017. Linking rhizosphere microbiome composition of wild and domesticated Phaseolus vulgaris to genotypic and root phenotypic traits. ISME J 11:2244–57
    [Google Scholar]
  95. 95. 
    Pérez-Jaramillo JE, Carrión VJ, de Hollander M, Raaijmakers JM 2018. The wild side of plant microbiomes. Microbiome 6:143
    [Google Scholar]
  96. 96. 
    Pérez-Jaramillo JE, Mendes R, Raaijmakers JM 2016. Impact of plant domestication on rhizosphere microbiome assembly and functions. Plant Mol. Biol. 90:635–44
    [Google Scholar]
  97. 97. 
    Pinto-Carbó M, Sieber S, Dessein S, Wicker T, Verstraete B et al. 2016. Evidence of horizontal gene transfer between obligate leaf nodule symbionts. ISME J 10:2092–105
    [Google Scholar]
  98. 98. 
    Poudel R, Jumpponen A, Schlatter DC, Paulitz TC, Gardener BB et al. 2016. Microbiome networks: a systems framework for identifying candidate microbial assemblages for disease management. Phytopathology 106:1083–96
    [Google Scholar]
  99. 99. 
    Purugganan MD, Fuller DQ. 2009. The nature of selection during plant domestication. Nature 457:843
    [Google Scholar]
  100. 100. 
    Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB et al. 2013. Plant–soil feedbacks: the past, the present and future challenges. J. Ecol. 101:265–76
    [Google Scholar]
  101. 101. 
    Qiao Q, Wang F, Zhang J, Chen Y, Zhang C et al. 2017. The variation in the rhizosphere microbiome of cotton with soil type, genotype and developmental stage. Sci. Rep. 7:3940
    [Google Scholar]
  102. 102. 
    Ramirez KS, Craine JM, Fierer N 2012. Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob. Change Biol. 18:1918–27
    [Google Scholar]
  103. 103. 
    Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S et al. 2005. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732
    [Google Scholar]
  104. 104. 
    Reinhold-Hurek B, Hurek T. 2011. Living inside plants: bacterial endophytes. Curr. Opin. Plant Biol. 14:435–43
    [Google Scholar]
  105. 105. 
    Rillig MC, Muller LAH, Lehmann A 2017. Soil aggregates as massively concurrent evolutionary incubators. ISME J 11:1943
    [Google Scholar]
  106. 106. 
    Rodrigues JLM, Pellizari VH, Mueller R, Baek K, Jesus EC et al. 2013. Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. PNAS 110:988–93
    [Google Scholar]
  107. 107. 
    Rudrappa T, Czymmek KJ, Pare PW, Bais HP 2008. Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–56Links a specific root exudate to the recruitment of beneficial bacteria.
    [Google Scholar]
  108. 108. 
    Santhanam R, Luu VT, Weinhold A, Goldberg J, Oh Y, Baldwin IT 2015. Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping. PNAS 112:E5013–20
    [Google Scholar]
  109. 109. 
    Santoyo G, Moreno-Hagelsieb G, Orozco-Mosqueda MC, Glick BR 2016. Plant growth-promoting bacterial endophytes. Microbiol. Res. 183:92–99
    [Google Scholar]
  110. 110. 
    Schlaeppi K, Dombrowski N, Oter RG, Ver Loren van Themaat E, Schulze-Lefert P 2014. Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. PNAS 111:585–92
    [Google Scholar]
  111. 111. 
    Schlatter D, Kinkel L, Thomashow L, Weller D, Paulitz T 2017. Disease suppressive soils: new insights from the soil microbiome. Phytopathology 107:1284–97
    [Google Scholar]
  112. 112. 
    Schlemper TR, Leite MFA, Lucheta AR, Shimels M, Bouwmeester HJ et al. 2017. Rhizobacterial community structure differences among sorghum cultivars in different growth stages and soils. FEMS Microbiol. Ecol. 93: https://doi.org/10.1093/femsec/fix096
    [Crossref] [Google Scholar]
  113. 113. 
    Schulz-Bohm K, Gerards S, Hundscheid M, Melenhorst J, de Boer W, Garbeva P 2018. Calling from distance: attraction of soil bacteria by plant root volatiles. ISME J 12:1252–62
    [Google Scholar]
  114. 114. 
    Sessitsch A, Brader G, Pfaffenbichler N, Gusenbauer D, Mitter B 2018. The contribution of plant microbiota to economy growth. Microb. Biotechnol. 11:801–5
    [Google Scholar]
  115. 115. 
    Sessitsch A, Hardoim P, Doring J, Weilharter A, Krause A et al. 2012. Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol. Plant Microbe Interact. 25:28–36
    [Google Scholar]
  116. 116. 
    Shade A, Jacques MA, Barret M 2017. Ecological patterns of seed microbiome diversity, transmission, and assembly. Curr. Opin. Microbiol. 37:15–22
    [Google Scholar]
  117. 117. 
    Stringlis IA, Yu K, Feussner K, de Jonge R, Van Bentum S et al. 2018. MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. PNAS 115:E5213–22
    [Google Scholar]
  118. 118. 
    Szoboszlay M, Lambers J, Chappell J, Kupper JV, Moe LA, McNear DH 2015. Comparison of root system architecture and rhizosphere microbial communities of Balsas teosinte and domesticated corn cultivars. Soil Biol. Biochem. 80:34–44
    [Google Scholar]
  119. 119. 
    Thijs S, Sillen W, Weyens N, Vangronsveld J 2017. Phytoremediation: state-of-the-art and a key role for the plant microbiome in future trends and research prospects. Int. J. Phytoremediat. 19:23–38
    [Google Scholar]
  120. 120. 
    Toju H, Vannette RL, Gauthier M-PL, Dhami MK, Fukami T 2018. Priority effects can persist across floral generations in nectar microbial metacommunities. Oikos 127:345–52
    [Google Scholar]
  121. 121. 
    Truyens S, Weyens N, Cuypers A, Vangronsveld J 2015. Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ. Microbiol. Rep. 7:40–50
    [Google Scholar]
  122. 122. 
    Turner TR, James EK, Poole PS 2013. The plant microbiome. Genome Biol 14:209
    [Google Scholar]
  123. 123. 
    Vacher C, Hampe A, Porté AJ, Sauer U, Compant S, Morris CE 2016. The phyllosphere: microbial jungle at the plant-climate interface. Annu. Rev. Ecol. Evol. Syst. 47:1–24
    [Google Scholar]
  124. 124. 
    van Dam NM, Heil M 2011. Multitrophic interactions below and above ground: en route to the next level. J. Ecol. 99:77–88
    [Google Scholar]
  125. 125. 
    van der Meij A, Willemse J, Schneijderberg MA, Geurts R, Raaijmakers JM, van Wezel GP 2018. Inter- and intracellular colonization of Arabidopsis roots by endophytic actinobacteria and the impact of plant hormones on their antimicrobial activity. Antonie Van Leeuwenhoek 111:679–90
    [Google Scholar]
  126. 126. 
    van der Voort M, Meijer H, Schmidt Y, Watrous J, Dekkers E et al. 2015. Genome mining and metabolic profiling of the rhizosphere bacterium Pseudomonas sp. SH-C52 for antimicrobial compounds. Front. Microbiol. 6:693
    [Google Scholar]
  127. 127. 
    van Elsas JD, Chiurazzi M, Mallon CA, Elhottovā D, Krištůfek V, Salles JF 2012. Microbial diversity determines the invasion of soil by a bacterial pathogen. PNAS 109:1159–64
    [Google Scholar]
  128. 128. 
    Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A 2015. The importance of the microbiome of the plant holobiont. New Phytol 206:1196–206
    [Google Scholar]
  129. 129. 
    Velivelli SLS, Sessitsch A, Prestwich BD 2014. The role of microbial inoculants in integrated crop management systems. Potato Res 57:291–309
    [Google Scholar]
  130. 130. 
    Vellend M. 2010. Conceptual synthesis in community ecology. Q. Rev. Biol. 85:183–206Conceptual basis of the ecological processes and mechanisms mediating community assembly.
    [Google Scholar]
  131. 131. 
    Vellend M. 2016. The Theory of Ecological Communities Princeton, NJ: Princeton Univ. Press
  132. 132. 
    Vorholt JA. 2012. Microbial life in the phyllosphere. Nat. Rev. Microbiol. 10:828–40
    [Google Scholar]
  133. 133. 
    Vorholt JA, Vogel C, Carlstrom CI, Muller DB 2017. Establishing causality: opportunities of synthetic communities for plant microbiome research. Cell Host Microbe 22:142–55
    [Google Scholar]
  134. 134. 
    Wagner MR, Lundberg DS, Del Rio TG, Tringe SG, Dangl JL, Mitchell-Olds T 2016. Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat. Commun. 7:12151
    [Google Scholar]
  135. 135. 
    Watrous J, Roach P, Alexandrov T, Heath BS, Yang JY et al. 2012. Mass spectral molecular networking of living microbial colonies. PNAS 109:E1743–52
    [Google Scholar]
  136. 136. 
    Weese DJ, Heath KD, Dentinger BTM, Lau JA 2015. Long-term nitrogen addition causes the evolution of less-cooperative mutualists. Evolution 69:631–42
    [Google Scholar]
  137. 137. 
    Weinert N, Meincke R, Gottwald C, Heuer H, Gomes NC et al. 2009. Rhizosphere communities of genetically modified zeaxanthin-accumulating potato plants and their parent cultivar differ less than those of different potato cultivars. Appl. Environ. Microbiol. 75:3859–65
    [Google Scholar]
  138. 138. 
    Weller DM. 1988. Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu. Rev. Phytopathol. 26:379–407
    [Google Scholar]
  139. 139. 
    Werner GD, Kiers ET. 2015. Order of arrival structures arbuscular mycorrhizal colonization of plants. New Phytol 205:1515–24
    [Google Scholar]
  140. 140. 
    Wolińska A, Kuźniar A, Zielenkiewicz U, Izak D, Szafranek-Nakonieczna A et al. 2017. Bacteroidetes as a sensitive biological indicator of agricultural soil usage revealed by a culture-independent approach. Appl. Soil Ecol. 119:128–37
    [Google Scholar]
  141. 141. 
    Wouters FC, Blanchette B, Gershenzon J, Vassão DG 2016. Plant defense and herbivore counter-defense: benzoxazinoids and insect herbivores. Phytochem. Rev. 15:1127–51
    [Google Scholar]
  142. 142. 
    Wubs ER, van der Putten WH, Bosch M, Bezemer TM 2016. Soil inoculation steers restoration of terrestrial ecosystems. Nat. Plants 2:16107
    [Google Scholar]
  143. 143. 
    Xu X-H, Su Z-Z, Wang C, Kubicek CP, Feng X-X et al. 2014. The rice endophyte Harpophora oryzae genome reveals evolution from a pathogen to a mutualistic endophyte. Sci. Rep. 4:5783
    [Google Scholar]
  144. 144. 
    Yang G, Wagg C, Veresoglou SD, Hempel S, Rillig MC 2018. How soil biota drive ecosystem stability. Trends Plant Sci 23:1057–67
    [Google Scholar]
  145. 145. 
    Yang JW, Yi H-S, Kim H, Lee B, Lee S 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
    [Google Scholar]
  146. 146. 
    Yeoh YK, Dennis PG, Paungfoo-Lonhienne C, Weber L, Brackin R et al. 2017. Evolutionary conservation of a core root microbiome across plant phyla along a tropical soil chronosequence. Nat. Commun. 8:215
    [Google Scholar]
  147. 147. 
    Yuan J, Zhao J, Wen T, Zhao M, Li R et al. 2018. Root exudates drive the soil-borne legacy of aboveground pathogen infection. Microbiome 6:156
    [Google Scholar]
  148. 148. 
    Zachow C, Muller H, Tilcher R, Berg G 2014. Differences between the rhizosphere microbiome of Beta vulgaris ssp. maritima—ancestor of all beet crops—and modern sugar beets. Front. Microbiol. 5:415
    [Google Scholar]
  149. 149. 
    Zhalnina K, Louie KB, Hao Z, Mansoori N, da Rocha UN et al. 2018. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat. Microbiol. 3:470–80
    [Google Scholar]
  150. 150. 
    Zhou J, Ning D. 2017. Stochastic community assembly: Does it matter in microbial ecology?. Microbiol. Mol. Biol. Rev. 81:e00002–17
    [Google Scholar]
/content/journals/10.1146/annurev-micro-090817-062524
Loading
/content/journals/10.1146/annurev-micro-090817-062524
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error