1932

Abstract

Plants do not grow as axenic organisms in nature, but host a diverse community of microorganisms, termed the plant microbiota. There is an increasing awareness that the plant microbiota plays a role in plant growth and can provide protection from invading pathogens. Apart from intense research on crop plants, is emerging as a valuable model system to investigate the drivers shaping stable bacterial communities on leaves and roots and as a tool to decipher the intricate relationship among the host and its colonizing microorganisms. Gnotobiotic experimental systems help establish causal relationships between plant and microbiota genotypes and phenotypes and test hypotheses on biotic and abiotic perturbations in a systematic way. We highlight major recent findings in plant microbiota research using comparative community profiling and omics analyses, and discuss these approaches in light of community establishment and beneficial traits like nutrient acquisition and plant health.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-120215-034952
2016-11-23
2024-04-13
Loading full text...

Full text loading...

/deliver/fulltext/genet/50/1/annurev-genet-120215-034952.html?itemId=/content/journals/10.1146/annurev-genet-120215-034952&mimeType=html&fmt=ahah

Literature Cited

  1. Agler MT, Ruhe J, Kroll S, Morhenn C, Kim ST. 1.  et al. 2016. Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLOS Biol 14:e1002352 [Google Scholar]
  2. Badri DV, Quintana N, El Kassis EG, Kim HK, Choi YH. 2.  et al. 2009. An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota. Plant Physiol 151:2006–17 [Google Scholar]
  3. Badri DV, Zolla G, Bakker MG, Manter DK, Vivanco JM. 3.  2013. Potential impact of soil microbiomes on the leaf metabolome and on herbivore feeding behavior. New Phytol 198:264–73 [Google Scholar]
  4. Bai Y, Müller DB, Srinivas G, Garrido-Oter R, Potthoff E. 4.  et al. 2015. Functional overlap of the Arabidopsis leaf and root microbiota. Nature 528:364–69 [Google Scholar]
  5. Bailly A, Groenhagen U, Schulz S, Geisler M, Eberl L, Weisskopf L. 5.  2014. The inter-kingdom volatile signal indole promotes root development by interfering with auxin signalling. Plant J 80:758–71 [Google Scholar]
  6. Balsanelli E, Tuleski TR, de Baura VA, Yates MG, Chubatsu LS. 6.  et al. 2013. Maize root lectins mediate the interaction with Herbaspirillum seropedicae via N-acetyl glucosamine residues of lipopolysaccharides. PLOS ONE 8:e77001 [Google Scholar]
  7. Bell TH, Joly S, Pitre FE, Yergeau E. 7.  2014. Increasing phytoremediation efficiency and reliability using novel omics approaches. Trends Biotechnol 32:271–80 [Google Scholar]
  8. Berendsen RL, Pieterse CMJ, Bakker PAHM. 8.  2012. The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–86 [Google Scholar]
  9. Berg G. 9.  2009. Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl. Microbiol. Biotechnol. 84:11–18 [Google Scholar]
  10. Berg G, Smalla K. 10.  2009. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol. Ecol. 68:1–13 [Google Scholar]
  11. Bodenhausen N, Bortfeld-Miller M, Ackermann M, Vorholt JA. 11.  2014. A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. PLOS Genet 10:e1004283 [Google Scholar]
  12. Bodenhausen N, Horton MW, Bergelson J. 12.  2013. Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLOS ONE 8:e56329 [Google Scholar]
  13. Bogino P, Abod A, Nievas F, Giordano W. 13.  2013. Water-limiting conditions alter the structure and biofilm-forming ability of bacterial multispecies communities in the alfalfa rhizosphere. PLOS ONE 8:e79614 [Google Scholar]
  14. Bohm M, Hurek T, Reinhold-Hurek B. 14.  2007. Twitching motility is essential for endophytic rice colonization by the N2-fixing endophyte Azoarcus sp. strain BH72. Mol. Plant-Microbe Interact. 20:526–33 [Google Scholar]
  15. Bonito G, Reynolds H, Robeson MS, Nelson J, Hodkinson BP. 15.  et al. 2014. Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants. Mol. Ecol. 23:3356–70 [Google Scholar]
  16. Bouasria A, Mustafa T, De Bello F, Zinger L, Lemperiere G. 16.  et al. 2012. Changes in root-associated microbial communities are determined by species-specific plant growth responses to stress and disturbance. Eur. J. Soil Biol. 52:59–66 [Google Scholar]
  17. Bulgarelli D, Garrido-Oter R, Muench PC, Weiman A, Droege J. 17.  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. Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N. 18.  et al. 2012. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95 [Google Scholar]
  19. Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P. 19.  2013. Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64:807–38 [Google Scholar]
  20. Burch AY, Zeisler V, Yokota K, Schreiber L, Lindow SE. 20.  2014. The hygroscopic biosurfactant syringafactin produced by Pseudomonas syringae enhances fitness on leaf surfaces during fluctuating humidity. Environ. Microbiol. 16:2086–98 [Google Scholar]
  21. Carvalhais LC, Dennis PG, Badri DV, Kidd BN, Vivanco JM, Schenk PM. 21.  2015. Linking jasmonic acid signaling, root exudates, and rhizosphere microbiomes. Mol. Plant-Microbe Interact. 28:1049–58 [Google Scholar]
  22. Chaparro JM, Badri DV, Vivanco JM. 22.  2014. Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803 [Google Scholar]
  23. Chapelle E, Mendes R, Bakker PA, Raaijmakers JM. 23.  2016. Fungal invasion of the rhizosphere microbiome. ISME J 10:265–68 [Google Scholar]
  24. Chi F, Shen SH, Cheng HP, Jing YX, Yanni YG, Dazzo FB. 24.  2005. Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Appl. Environ. Microbiol. 71:7271–78 [Google Scholar]
  25. Chowdhury SP, Dietel K, Raendler M, Schmid M, Junge H. 25.  et al. 2013. Effects of Bacillus amyloliquefaciens FZB42 on lettuce growth and health under pathogen pressure and its impact on the rhizosphere bacterial community. PLOS ONE 8:e68818 [Google Scholar]
  26. Cook DE, Mesarich CH, Thomma BPHJ. 26.  2015. Understanding plant immunity as a surveillance system to detect invasion. Annu. Rev. Phytopathol. 53:541–63 [Google Scholar]
  27. Copeland JK, Yuan L, Layeghifard M, Wang PW, Guttman DS. 27.  2015. Seasonal community succession of the phyllosphere microbiome. Mol. Plant-Microbe Interact. 28:274–85 [Google Scholar]
  28. Dangl JL, Horvath DM, Staskawicz BJ. 28.  2013. Pivoting the plant immune system from dissection to deployment. Science 341:746–751 [Google Scholar]
  29. Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B. 29.  et al. 2009. Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. PNAS 106:16428–33 [Google Scholar]
  30. Dematheis F, Zimmerling U, Flocco C, Kurtz B, Vidal S. 30.  et al. 2012. Multitrophic interaction in the rhizosphere of maize: root feeding of Western Corn Rootworm larvae alters the microbial community composition. PLOS ONE 7:e37288 [Google Scholar]
  31. Dodd IC, Perez-Alfocea F. 31.  2012. Microbial amelioration of crop salinity stress. J. Exp. Bot. 63:3415–28 [Google Scholar]
  32. Edwards J, Johnson C, Santos-Medellin C, Lurie E, Podishetty NK. 32.  et al. 2015. Structure, variation, and assembly of the root-associated microbiomes of rice. PNAS 112:E911–20 [Google Scholar]
  33. Eichorst SA, Strasser F, Woyke T, Schintlmeister A, Wagner M, Woebken D. 33.  2015. Advancements in the application of NanoSIMS and Raman microspectroscopy to investigate the activity of microbial cells in soils. FEMS Microbiol. Ecol. 91:fiv106 [Google Scholar]
  34. Ercolani GL. 34.  1991. Distribution of epiphytic bacteria on olive leaves and the influence of leaf age and sampling time. Microb. Ecol. 21:35–48 [Google Scholar]
  35. Erlacher A, Cardinale M, Grosch R, Grube M, Berg G. 35.  2014. The impact of the pathogen Rhizoctonia solani and its beneficial counterpart Bacillus amyloliquefaciens on the indigenous lettuce microbiome. Front. Microbiol. 5:175 [Google Scholar]
  36. Fall R, Benson AA. 36.  1996. Leaf methanol: the simplest natural product from plants. Trends Plant Sci. 1:296–301 [Google Scholar]
  37. Finkel OM, Burch AY, Lindow SE, Post AF, Belkin S. 37.  2011. Geographical location determines the population structure in phyllosphere microbial communities of a salt-excreting desert tree. Appl. Environ. Microbiol. 77:7647–55 [Google Scholar]
  38. Francez-Charlot A, Kaczmarczyk A, Fischer HM, Vorholt JA. 38.  2015. The general stress response in Alphaproteobacteria. Trends Microbiol 23:164–71 [Google Scholar]
  39. Fürnkranz M, Wanek W, Richter A, Abell G, Rasche F, Sessitsch A. 39.  2008. Nitrogen fixation by phyllosphere bacteria associated with higher plants and their colonizing epiphytes of a tropical lowland rainforest of Costa Rica. ISME J 2:561–70 [Google Scholar]
  40. Gans J, Wolinsky M, Dunbar J. 40.  2005. Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309:1387–90 [Google Scholar]
  41. Glick BR. 41.  2014. Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol. Res. 169:30–39 [Google Scholar]
  42. Gourion B, Rossignol M, Vorholt JA. 42.  2006. A proteomic study of Methylobacterium extorquens reveals a response regulator essential for epiphytic growth. PNAS 103:13186–91 [Google Scholar]
  43. Haas D, Defago G. 43.  2005. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat. Rev. Microbiol. 3:307–19 [Google Scholar]
  44. Hacquard S, Garrido-Oter R, Gonzalez A, Spaepen S, Ackermann G. 44.  et al. 2015. Microbiota and host nutrition across plant and animal kingdoms. Cell Host Microbe 17:603–16 [Google Scholar]
  45. Hacquard S, Kracher B, Hiruma K, Münch PC, Garrido-Oter R. 45.  et al. 2016. Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi. Nat. Commun. 7:11362 [Google Scholar]
  46. Haichar FE, Heulin T, Guyonnet JP, Achouak W. 46.  2016. Stable isotope probing of carbon flow in the plant holobiont. Curr. Opin. Biotechnol. 41:9–13 [Google Scholar]
  47. Handelsman J, Rondon MR, Brady SF, Clardy J, Goodman RM. 47.  1998. Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem. Biol. 5:R245–49 [Google Scholar]
  48. Haney CH, Samuel BS, Bush J, Ausubel FM. 48.  2015. Associations with rhizosphere bacteria can confer an adaptive advantage to plants. Nat. Plants 1:15051 [Google Scholar]
  49. Hardoim PR, Hardoim CC, van Overbeek LS, van Elsas JD. 49.  2012. Dynamics of seed-borne rice endophytes on early plant growth stages. PLOS ONE 7:e30438 [Google Scholar]
  50. Hiruma K, Gerlach N, Sacristán S, Nakano RT, Hacquard S. 50.  et al. 2016. Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status-dependent. Cell 165:464–74 [Google Scholar]
  51. Horton MW, Bodenhausen N, Beilsmith K, Meng D, Muegge BD. 51.  et al. 2014. Genome-wide association study of Arabidopsis thaliana leaf microbial community. Nat. Commun. 5:5320 [Google Scholar]
  52. Hsu CC, Dorrestein PC. 52.  2015. Visualizing life with ambient mass spectrometry. Curr. Opin. Biotechnol. 31:24–34 [Google Scholar]
  53. Huang WE, Ferguson A, Singer AC, Lawson K, Thompson IP. 53.  et al. 2009. Resolving genetic functions within microbial populations: in situ analyses using rRNA and mRNA stable isotope probing coupled with single-cell Raman-fluorescence in situ hybridization. Appl. Environ. Microbiol. 75:234–41 [Google Scholar]
  54. Ikeda S, Anda M, Inaba S, Eda S, Sato S. 54.  et al. 2011. Autoregulation of nodulation interferes with impacts of nitrogen fertilization levels on the leaf-associated bacterial community in soybeans. Appl. Environ. Microbiol. 77:1973–80 [Google Scholar]
  55. Inceoglu O, Al-Soud WA, Salles JF, Semenov AV, van Elsas JD. 55.  2011. Comparative analysis of bacterial communities in a potato field as determined by pyrosequencing. PLOS ONE 6:e23321 [Google Scholar]
  56. Inceoglu O, Salles JF, van Elsas JD. 56.  2012. Soil and cultivar type shape the bacterial community in the potato rhizosphere. Microb. Ecol. 63:460–70 [Google Scholar]
  57. Innerebner G, Knief C, Vorholt JA. 57.  2011. Protection of Arabidopsis thaliana against leaf-pathogenic Pseudomonas syringae by Sphingomonas strains in a controlled model system. Appl. Environ. Microbiol. 77:3202–10 [Google Scholar]
  58. Johnston-Monje D, Mousa WK, Lazarovits G, Raizada MN. 58.  2014. Impact of swapping soils on the endophytic bacterial communities of pre-domesticated, ancient and modern maize. BMC Plant Biol 14:233 [Google Scholar]
  59. Kaczmarczyk A, Campagne S, Danza F, Metzger LC, Vorholt JA, Francez-Charlot A. 59.  2011. Role of Sphingomonas sp. strain Fr1 PhyR-NepR-σEcfG cascade in general stress response and identification of a negative regulator of PhyR. J. Bacteriol. 193:6629–38 [Google Scholar]
  60. Kadivar H, Stapleton AE. 60.  2003. Ultraviolet radiation alters maize phyllosphere bacterial diversity. Microb. Ecol. 45:353–61 [Google Scholar]
  61. Kavamura VN, Taketani RG, Lanconi MD, Andreote FD, Mendes R, de Melo IS. 61.  2013. Water regime influences bulk soil and rhizosphere of Cereus jamacaru bacterial communities in the Brazilian Caatinga biome. PLOS ONE 8:e73606 [Google Scholar]
  62. Kembel SW, O'Connor TK, Arnold HK, Hubbell SP, Wright SJ, Green JL. 62.  2014. Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. PNAS 111:13715–20 [Google Scholar]
  63. Kemen E. 63.  2014. Microbe-microbe interactions determine oomycete and fungal host colonization. Curr. Opin. Plant Biol. 20:75–81 [Google Scholar]
  64. Knief C, Delmotte N, Chaffron S, Stark M, Innerebner G. 64.  et al. 2012. Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J 6:1378–90 [Google Scholar]
  65. Knief C, Ramette A, Frances L, Alonso-Blanco C, Vorholt JA. 65.  2010. Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere. ISME J. 4:719–28 [Google Scholar]
  66. Kniskern JM, Traw MB, Bergelson J. 66.  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]
  67. Kolton M, Frenkel O, Elad Y, Cytryn E. 67.  2014. Potential role of flavobacterial gliding-motility and type IX secretion system complex in root colonization and plant defense. Mol. Plant-Microbe Interact. 27:1005–13 [Google Scholar]
  68. Laforest-Lapointe I, Messier C, Kembel SW. 68.  2016. Host species identity, site and time drive temperate tree phyllosphere bacterial community structure. Microbiome 4:27 [Google Scholar]
  69. Lau JA, Lennon JT. 69.  2012. Rapid responses of soil microorganisms improve plant fitness in novel environments. PNAS 109:14058–62 [Google Scholar]
  70. Lebeis SL, Paredes SH, Lundberg DS, Breakfield N, Gehring J. 70.  et al. 2015. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349:860–64 [Google Scholar]
  71. Lee B, Lee S, Ryu C-M. 71.  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]
  72. Li X, Rui J, Xiong J, Li J, He Z. 72.  et al. 2014. Functional potential of soil microbial communities in the maize rhizosphere. PLOS ONE 9:e112609 [Google Scholar]
  73. Lindow SE, Brandl MT. 73.  2003. Microbiology of the phyllosphere. Appl. Environ. Microbiol. 69:1875–83 [Google Scholar]
  74. Lindow SE, Leveau JH. 74.  2002. Phyllosphere microbiology. Curr. Opin. Biotechnol. 13:238–43 [Google Scholar]
  75. Lu Y, Conrad R. 75.  2005. In situ stable isotope probing of methanogenic archaea in the rice rhizosphere. Science 309:1088–90 [Google Scholar]
  76. Lugtenberg B, Kamilova F. 76.  2009. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63:541–56 [Google Scholar]
  77. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J. 77.  et al. 2012. Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90 [Google Scholar]
  78. Maignien L, DeForce EA, Chafee ME, Eren AM, Simmons SL. 78.  2014. Ecological succession and stochastic variation in the assembly of Arabidopsis thaliana phyllosphere communities. mBio 5:e00682–13 [Google Scholar]
  79. Manching HC, Balint-Kurti PJ, Stapleton AE. 79.  2014. Southern leaf blight disease severity is correlated with decreased maize leaf epiphytic bacterial species richness and the phyllosphere bacterial diversity decline is enhanced by nitrogen fertilization. Front. Plant Sci. 5:403 [Google Scholar]
  80. Mendes LW, Kuramae EE, Navarrete AA, van Veen JA, Tsai SM. 80.  2014. Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J 8:1577–87 [Google Scholar]
  81. Mendes R, Garbeva P, Raaijmakers JM. 81.  2013. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol. Rev. 37:634–63 [Google Scholar]
  82. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M. 82.  et al. 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–100 [Google Scholar]
  83. Mondy S, Lenglet A, Beury-Cirou A, Libanga C, Ratet P. 83.  et al. 2014. An increasing opine carbon bias in artificial exudation systems and genetically modified plant rhizospheres leads to an increasing reshaping of bacterial populations. Mol. Ecol. 23:4846–61 [Google Scholar]
  84. Moran NA, Sloan DB. 84.  2015. The hologenome concept: helpful or hollow?. PLOS Biol 13:e1002311 [Google Scholar]
  85. Mueller UG, Sachs JL. 85.  2015. Engineering microbiomes to improve plant and animal health. Trends Microbiol 23:606–17 [Google Scholar]
  86. Mushegian AA, Ebert D. 86.  2016. Rethinking “mutualism” in diverse host-symbiont communities. BioEssays 38:100–8 [Google Scholar]
  87. Neal AL, Ahmad S, Gordon-Weeks R, Ton J. 87.  2012. Benzoxazinoids in root exudates of maize attract Pseudomonas putida to the rhizosphere. PLOS ONE 7:e35498 [Google Scholar]
  88. Ofek-Lalzar M, Sela N, Goldman-Voronov M, Green SJ, Hadar Y, Minz D. 88.  2014. Niche and host-associated functional signatures of the root surface microbiome. Nat. Commun. 5:4950 [Google Scholar]
  89. Oh YM, Kim M, Lee-Cruz L, Lai-Hoe A, Go R. 89.  et al. 2012. Distinctive bacterial communities in the rhizoplane of four tropical tree species. Microb. Ecol. 64:1018–27 [Google Scholar]
  90. Oldroyd GED, Murray JD, Poole PS, Downie JA. 90.  2011. The rules of engagement in the legume-rhizobial symbiosis. Annu. Rev. Genet. 45:119–44 [Google Scholar]
  91. Ottesen AR, Gonzalez Pena A, White JR, Pettengill JB, Li C. 91.  et al. 2013. Baseline survey of the anatomical microbial ecology of an important food plant: Solanum lycopersicum (tomato). BMC Microbiol 13:114 [Google Scholar]
  92. Panke-Buisse K, Poole AC, Goodrich JK, Ley RE, Kao-Kniffin J. 92.  2015. Selection on soil microbiomes reveals reproducible impacts on plant function. ISME J 9:980–89 [Google Scholar]
  93. Parniske M. 93.  2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6:763–75 [Google Scholar]
  94. Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG. 94.  et al. 2013. Diversity and heritability of the maize rhizosphere microbiome under field conditions. PNAS 110:6548–53 [Google Scholar]
  95. Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM. 95.  2014. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52:347–75 [Google Scholar]
  96. Pilon-Smits E. 96.  2005. Phytoremediation. Annu. Rev. Plant Biol. 56:15–39 [Google Scholar]
  97. Raaijmakers JM, Mazzola M. 97.  2012. Diversity and natural functions of antibiotics produced by beneficial and plant pathogenic bacteria. Annu. Rev. Phytopathol. 50:403–24 [Google Scholar]
  98. Raes J, Bork P. 98.  2008. Molecular eco-systems biology: towards an understanding of community function. Nat. Rev. Microbiol. 6:693–99 [Google Scholar]
  99. Raghavendra AKH, Newcombe G. 99.  2013. The contribution of foliar endophytes to quantitative resistance to Melampsora rust. New Phytol 197:909–18 [Google Scholar]
  100. Ramirez-Puebla ST, Servin-Garciduenas LE, Jimenez-Marin B, Bolanos LM, Rosenblueth M. 100.  et al. 2013. Gut and root microbiota commonalities. Appl. Environ. Microbiol. 79:2–9 [Google Scholar]
  101. Rastogi G, Sbodio A, Tech JJ, Suslow TV, Coaker GL, Leveau JHJ. 101.  2012. Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J 6:1812–22 [Google Scholar]
  102. Redford AJ, Bowers RM, Knight R, Linhart Y, Fierer N. 102.  2010. The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ. Microbiol. 12:2885–93 [Google Scholar]
  103. Reinhold-Hurek B, Bünger W, Burbano CS, Sabale M, Hurek T. 103.  2015. Roots shaping their microbiome: global hotspots for microbial activity. Annu. Rev. Phytopathol. 53:403–24 [Google Scholar]
  104. Reisberg EE, Hildebrandt U, Riederer M, Hentschel U. 104.  2013. Distinct phyllosphere bacterial communities on Arabidopsis wax mutant leaves. PLOS ONE 8:e78613 [Google Scholar]
  105. Remus-Emsermann MN, Lücker S, Müller DB, Potthoff E, Daims H, Vorholt JA. 105.  2014. Spatial distribution analyses of natural phyllosphere-colonizing bacteria on Arabidopsis thaliana revealed by fluorescence in situ hybridization. Environ. Microbiol. 16:2329–40 [Google Scholar]
  106. Ritpitakphong U, Falquet L, Vimoltust A, Berger A, Metraux JP, L'Haridon F. 106.  2016. The microbiome of the leaf surface of Arabidopsis protects against a fungal pathogen. New Phytol 210:1033–43 [Google Scholar]
  107. Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F. 107.  et al. 2015. Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ. Microbiol. 17:316–31 [Google Scholar]
  108. Rudrappa T, Czymmek KJ, Pare PW, Bais HP. 108.  2008. Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–56 [Google Scholar]
  109. Ryffel F, Helfrich EJ, Kiefer P, Peyriga L, Portais JC. 109.  et al. 2016. Metabolic footprint of epiphytic bacteria on Arabidopsis thaliana leaves. ISME J. 10:632–43 [Google Scholar]
  110. Ryu CM. 110.  2015. Against friend and foe: type 6 effectors in plant-associated bacteria. J. Microbiol. 53:201–8 [Google Scholar]
  111. Scheublin TR, Deusch S, Moreno-Forero SK, Müller JA, van der Meer JR, Leveau JHJ. 111.  2014. Transcriptional profiling of Gram-positive Arthrobacter in the phyllosphere: induction of pollutant degradation genes by natural plant phenolic compounds. Environ. Microbiol. 16:2212–25 [Google Scholar]
  112. Schlaeppi K, Bulgarelli D. 112.  2015. The plant microbiome at work. Mol. Plant-Microbe Interact. 28:212–17 [Google Scholar]
  113. Schlaeppi K, Dombrowski N, Oter RG, van Themaat EVL, Schulze-Lefert P. 113.  2014. Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. PNAS 111:585–92 [Google Scholar]
  114. Sessitsch A, Hardoim P, Doring J, Weilharter A, Krause A. 114.  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]
  115. Shade A, McManus PS, Handelsman J. 115.  2013. Unexpected diversity during community succession in the apple flower microbiome. mBio 4:e00602–12 [Google Scholar]
  116. Shakya M, Gottel N, Castro H, Yang ZK, Gunter L. 116.  et al. 2013. A multifactor analysis of fungal and bacterial community structure in the root microbiome of mature Populus deltoides trees. PLOS ONE 8:e76382 [Google Scholar]
  117. Sheibani-Tezerji R, Rattei T, Sessitsch A, Trognitz F, Mitter B. 117.  2015. Transcriptome profiling of the endophyte Burkholderia phytofirmans PsJN indicates sensing of the plant environment and drought stress. mBio 6:e00621–15 [Google Scholar]
  118. Shi S, Nuccio E, Herman DJ, Rijkers R, Estera K. 118.  et al. 2015. Successional trajectories of rhizosphere bacterial communities over consecutive seasons. mBio 6:e00746–15 [Google Scholar]
  119. Smith SE, Smith FA. 119.  2011. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu. Rev. Plant Biol. 62:227–50 [Google Scholar]
  120. Spaepen S, Bossuyt S, Engelen K, Marchal K, Vanderleyden J. 120.  2014. Phenotypical and molecular responses of Arabidopsis thaliana roots as a result of inoculation with the auxin-producing bacterium Azospirillum brasilense. New Phytol. 201:850–61 [Google Scholar]
  121. Spaepen S, Vanderleyden J, Remans R. 121.  2007. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. Rev. 31:425–48 [Google Scholar]
  122. Stiefel P, Zambelli T, Vorholt JA. 122.  2013. Isolation of optically targeted single bacteria by application of fluidic force microscopy to aerobic anoxygenic phototrophs from the phyllosphere. Appl. Environ. Microbiol. 79:4895–905 [Google Scholar]
  123. Stockwell VO, Johnson KB, Sugar D, Loper JE. 123.  2011. Mechanistically compatible mixtures of bacterial antagonists improve biological control of fire blight of pear. Phytopathology 101:113–23 [Google Scholar]
  124. Suda W, Nagasaki A, Shishido M. 124.  2009. Powdery mildew-infection changes bacterial community composition in the phyllosphere. Microbes Environ 24:217–23 [Google Scholar]
  125. Sugiyama A, Ueda Y, Zushi T, Takase H, Yazaki K. 125.  2014. Changes in the bacterial community of soybean rhizospheres during growth in the field. PLOS ONE 9:e100709 [Google Scholar]
  126. Sy A, Timmers AC, Knief C, Vorholt JA. 126.  2005. Methylotrophic metabolism is advantageous for Methylobacterium extorquens during colonization of Medicago truncatula under competitive conditions. Appl. Environ. Microbiol. 71:7245–52 [Google Scholar]
  127. Thebault E, Fontaine C. 127.  2010. Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329:853–56 [Google Scholar]
  128. Theis KR, Dheilly NM, Klassen JL, Brucker RM, Baines JF. 128.  et al. 2016. Getting the hologenome concept right: an eco-evolutionary framework for hosts and their microbiomes. mSystems 1:e00028–16 [Google Scholar]
  129. Thijs S, Sillen W, Rineau F, Weyens N, Vangronsveld J. 129.  2016. Towards an enhanced understanding of plant-microbiome interactions to improve phytoremediation: engineering the metaorganism. Front Microbiol 7:341 [Google Scholar]
  130. Thompson IP, Bailey MJ, Fenlon JS, Fermor TR, Lilley AK. 130.  et al. 1993. Quantitative and qualitative seasonal changes in the microbial community from the phyllosphere of sugar beet (Beta vulgaris). Plant Soil 150:177–91 [Google Scholar]
  131. Tkacz A, Poole P. 131.  2015. Role of root microbiota in plant productivity. J. Exp. Bot. 66:2167–75 [Google Scholar]
  132. Turner TR, James EK, Poole PS. 132.  2013. The plant microbiome. Genome Biol 14:209 [Google Scholar]
  133. Turner TR, Ramakrishnan K, Walshaw J, Heavens D, Alston M. 133.  et al. 2013. Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J. 7:2248–58 [Google Scholar]
  134. Udvardi M, Poole PS. 134.  2013. Transport and metabolism in legume-rhizobia symbioses. Annu. Rev. Plant Biol. 64:781–805 [Google Scholar]
  135. Urquiaga S, Xavier RP, de Morais RF, Batista RB, Schultz N. 135.  et al. 2012. Evidence from field nitrogen balance and 15N natural abundance data for the contribution of biological N2 fixation to Brazilian sugarcane varieties. Plant Soil 356:5–21 [Google Scholar]
  136. van de Mortel JE, de Vos RCH, Dekkers E, Pineda A, Guillod L. 136.  et al. 2012. Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol. 160:2173–88 [Google Scholar]
  137. Vandenkoornhuyse P, Mahe S, Ineson P, Staddon P, Ostle N. 137.  et al. 2007. Active root-inhabiting microbes identified by rapid incorporation of plant-derived carbon into RNA. PNAS 104:16970–75 [Google Scholar]
  138. Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A. 138.  2015. The importance of the microbiome of the plant holobiont. New Phytol. 206:1196–206 [Google Scholar]
  139. van der Heijden MG, Bruin S, Luckerhoff L, van Logtestijn RS, Schlaeppi K. 139.  2016. A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment. ISME J 10:389–99 [Google Scholar]
  140. van Elsas JD, Chiurazzi M, Mallon CA, Elhottova D, Kristufek V, Salles JF. 140.  2012. Microbial diversity determines the invasion of soil by a bacterial pathogen. PNAS 109:1159–64 [Google Scholar]
  141. Vogel C, Bodenhausen N, Gruissem W, Vorholt JA. 141.  2016. The Arabidopsis leaf transcriptome reveals distinct but also overlapping responses to colonization by phyllosphere commensals and pathogen infection with impact on plant health. New Phytol. 212:192–207 [Google Scholar]
  142. Vogel C, Innerebner G, Zingg J, Guder J, Vorholt JA. 142.  2012. Forward genetic in planta screen for identification of plant-protective traits of Sphingomonas sp. strain Fr1 against Pseudomonas syringae DC3000. Appl. Environ. Microbiol. 78:5529–35 [Google Scholar]
  143. Vorholt JA. 143.  2012. Microbial life in the phyllosphere. Nat. Rev. Microbiol. 10:828–40 [Google Scholar]
  144. Wagner MR, Lundberg DS, Coleman-Derr D, Tringe SG, Dangl JL, Mitchell-Olds T. 144.  2014. Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wild Arabidopsis relative. Ecol. Lett. 17:717–26 [Google Scholar]
  145. Wei Z, Yang T, Friman V-P, Xu Y, Shen Q, Jousset A. 145.  2015. Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nat. Commun. 6:8413 [Google Scholar]
  146. Weston DJ, Pelletier DA, Morrell-Falvey JL, Tschaplinski TJ, Jawdy SS. 146.  et al. 2012. Pseudomonas fluorescens induces strain-dependent and strain-independent host plant responses in defense networks, primary metabolism, photosynthesis, and fitness. Mol. Plant-Microbe Interact. 25:765–78 [Google Scholar]
  147. White LJ, Jothibasu K, Reese RN, Broezel VS, Subramanian S. 147.  2015. Spatio temporal influence of isoflavonoids on bacterial diversity in the soybean rhizosphere. Mol. Plant-Microbe Interact. 28:22–29 [Google Scholar]
  148. Williams TR, Marco ML. 148.  2014. Phyllosphere microbiota composition and microbial community transplantation on lettuce plants grown indoors. mBio 5:e01564–14 [Google Scholar]
  149. Williams TR, Moyne AL, Harris LJ, Marco ML. 149.  2013. Season, irrigation, leaf age, and Escherichia coli inoculation influence the bacterial diversity in the lettuce phyllosphere. PLOS ONE 8:e68642 [Google Scholar]
  150. Yang J, Kloepper JW, Ryu CM. 150.  2009. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4 [Google Scholar]
  151. Yang JW, Yi HS, Kim H, Lee B, Lee S. 151.  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]
  152. Yeoh YK, Paungfoo-Lonhienne C, Dennis PG, Robinson N, Ragan MA. 152.  et al. 2016. The core root microbiome of sugarcanes cultivated under varying nitrogen fertilizer application. Environ. Microbiol. 18:1338–51 [Google Scholar]
  153. Yu X, Lund SP, Scott RA, Greenwald JW, Records AH. 153.  et al. 2013. Transcriptional responses of Pseudomonas syringae to growth in epiphytic versus apoplastic leaf sites. PNAS 110:E425–34 [Google Scholar]
  154. Zamioudis C, Korteland J, Van Pelt JA, van Hamersveld M, Dombrowski N. 154.  et al. 2015. Rhizobacterial volatiles and photosynthesis-related signals coordinate MYB72 expression in Arabidopsis roots during onset of induced systemic resistance and iron-deficiency responses. Plant J 84:309–22 [Google Scholar]
  155. Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CMJ. 155.  2013. Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiol. 162:304–18 [Google Scholar]
  156. Zancarini A, Mougel C, Voisin AS, Prudent M, Salon C, Munier-Jolain N. 156.  2012. Soil nitrogen availability and plant genotype modify the nutrition strategies of M. truncatula and the associated rhizosphere microbial communities. PLOS ONE 7:e47096 [Google Scholar]
  157. Zarraonaindia I, Owens SM, Weisenhorn P, West K, Hampton-Marcell J. 157.  et al. 2015. The soil microbiome influences grapevine-associated microbiota. mBio 6:e02527–14 [Google Scholar]
  158. Zhang HM, Sun Y, Xie XT, Kim MS, Dowd SE, Pare PW. 158.  2009. A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J 58:568–77 [Google Scholar]
  159. Zipfel C. 159.  2014. Plant pattern-recognition receptors. Trends Immunol. 35:345–351 [Google Scholar]
/content/journals/10.1146/annurev-genet-120215-034952
Loading
/content/journals/10.1146/annurev-genet-120215-034952
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • 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