The Plant Microbiota: Systems-Level Insights and Perspectives

Annual Review of Genetics

Volumn 50, Issue , 2016, Pages 211-234

  Müller, Daniel B ^a   Vogel, Christine ^a   Bai, Yang ^b,c   Vorholt, Julia A ^a  

^a ETH ZURICH   (Switzerland)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^c INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

Arabidopsis; Bacterial community; Commensal; Gnotobiotic; Microbiome; Plant protection

Indexed keywords

ADAPTATION; ARABIDOPSIS; BACTERIAL COLONIZATION; ECOSYSTEM; ENVIRONMENTAL FACTOR; GENOTYPE; GNOTOBIOTICS; MICROBIAL COMMUNITY; MICROFLORA; NONHUMAN; ORGANISMAL INTERACTION; PHENOTYPE; PHYLOGENY; PLANT GENETICS; PLANT LEAF; PLANT ROOT; PRIORITY JOURNAL; REVIEW; MICROBIAL CONSORTIUM; MICROBIOLOGY; PLANT;

ADAPTATION, BIOLOGICAL; ARABIDOPSIS; ECOSYSTEM; MICROBIAL CONSORTIA; MICROBIOTA; PHYLOGENY; PLANT ROOTS; PLANTS;

EID: 85000578269     PISSN: 00664197     EISSN: 15452948     Source Type: Book Series    
DOI: 10.1146/annurev-genet-120215-034952     Document Type: Review

References (159)

1. Agler MT, Ruhe J, Kroll S, Morhenn C, Kim ST, et al. 2016. Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLOS Biol. 14:e1002352
2. 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 soilmicrobiota. Plant Physiol. 151:2006-17
3. Badri DV, Zolla G, Bakker MG, Manter DK, Vivanco JM. 2013. Potential impact of soil microbiomes on the leaf metabolome and on herbivore feeding behavior. New Phytol. 198:264-73
4. Bai Y, Müller DB, Srinivas G, Garrido-Oter R, Potthoff E, et al. 2015. Functional overlap of the Arabidopsis leaf and root microbiota. Nature 528:364-69
5. Bailly A, Groenhagen U, Schulz S, Geisler M, Eberl L,Weisskopf L. 2014. The inter-kingdom volatile signal indole promotes root development by interfering with auxin signalling. Plant J. 80:758-71
6. Balsanelli E, Tuleski TR, de Baura VA, YatesMG, Chubatsu LS, et al. 2013. Maize root lectins mediate the interaction with Herbaspirillum seropedicae via N-acetyl glucosamine residues of lipopolysaccharides. PLOS ONE 8:e77001
7. Bell TH, Joly S, Pitre FE, Yergeau E. 2014. Increasing phytoremediation efficiency and reliability using novel omics approaches. Trends Biotechnol. 32:271-80
8. Berendsen RL, Pieterse CMJ, Bakker PAHM. 2012. The rhizosphere microbiome and plant health. Trends Plant Sci. 17:478-86
9. Berg G. 2009. Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl. Microbiol. Biotechnol. 84:11-18
10. Berg G, Smalla K. 2009. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol. Ecol. 68:1-13
11. Bodenhausen N, Bortfeld-MillerM, Ackermann M, Vorholt JA. 2014. A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. PLOS Genet. 10:e1004283
12. Bodenhausen N, Horton MW, Bergelson J. 2013. Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLOS ONE 8:e56329
13. Bogino P, Abod A, Nievas F, Giordano W. 2013. Water-limiting conditions alter the structure and biofilm-forming ability of bacterial multispecies communities in the alfalfa rhizosphere. PLOS ONE 8:e79614
14. Bohm M, Hurek T, Reinhold-Hurek B. 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
15. Bonito G, Reynolds H, Robeson MS, Nelson J, Hodkinson BP, et al. 2014. Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants. Mol. Ecol. 23:3356-70
16. Bouasria A, Mustafa T, De Bello F, Zinger L, Lemperiere G, 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
17. Bulgarelli D, Garrido-Oter R, Muench PC,Weiman A, Droege J, et al. 2015. Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392-403
18. Bulgarelli D, Rott M, Schlaeppi K, Loren Themaat E, Ahmadinejad N, et al. 2012. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91-95
19. Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-LefertP. 2013. Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64:807-38
20. Burch AY, Zeisler V, Yokota K, Schreiber L, Lindow SE. 2014. The hygroscopic biosurfactant syringafactin produced by Pseudomonas syringae enhances fitness on leaf surfaces during fluctuating humidity. Environ. Microbiol. 16:2086-98
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
22. Chaparro JM, Badri DV, Vivanco JM. 2014. Rhizosphere microbiome assemblage is affected by plant development. ISME J. 8:790-803
23. Chapelle E, Mendes R, Bakker PA, Raaijmakers JM. 2016. Fungal invasion of the rhizosphere microbiome. ISME J. 10:265-68
24. Chi F, Shen SH, Cheng HP, Jing YX, Yanni YG, Dazzo FB. 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
25. Chowdhury SP, Dietel K, Raendler M, Schmid M, JungeH, 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
26. Cook DE, Mesarich CH, Thomma BPHJ. 2015. Understanding plant immunity as a surveillance system to detect invasion. Annu. Rev. Phytopathol. 53:541-63
27. Copeland JK, Yuan L, Layeghifard M, Wang PW, Guttman DS. 2015. Seasonal community succession of the phyllosphere microbiome. Mol. Plant-Microbe Interact. 28:274-85
28. Dangl JL, Horvath DM, Staskawicz BJ. 2013. Pivoting the plant immune system from dissection to deployment. Science 341:746-751
29. Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, et al. 2009. Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. PNAS 106:16428-33
30. Dematheis F, Zimmerling U, Flocco C, Kurtz B, Vidal S, 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
31. Dodd IC, Perez-Alfocea F. 2012. Microbial amelioration of crop salinity stress. J. Exp. Bot. 63:3415-28
32. 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:E911-20
33. Eichorst SA, Strasser F,Woyke T, Schintlmeister A, Wagner M, Woebken D. 2015. Advancements in the application ofNanoSIMS and Raman microspectroscopy to investigate the activity of microbial cells in soils. FEMS Microbiol. Ecol. 91:fiv106
34. Ercolani GL. 1991. Distribution of epiphytic bacteria on olive leaves and the influence of leaf age and sampling time. Microb. Ecol. 21:35-48
35. Erlacher A, Cardinale M, Grosch R, Grube M, Berg G. 2014. The impact of the pathogen Rhizoctonia solani and its beneficial counterpart Bacillus amyloliquefaciens on the indigenous lettuce microbiome. Front. Microbiol. 5:175
36. Fall R, Benson AA. 1996. Leaf methanol: the simplest natural product from plants. Trends Plant Sci. 1:296-301
37. Finkel OM, Burch AY, Lindow SE, Post AF, Belkin S. 2011. Geographical location determines the population structure in phyllosphere microbial communities of a salt-excreting desert tree. Appl. Environ. Microbiol. 77:7647-55
38. Francez-Charlot A, Kaczmarczyk A, Fischer HM, Vorholt JA. 2015. The general stress response in Alphaproteobacteria. Trends Microbiol. 23:164-71
39. Fürnkranz M, Wanek W, Richter A, Abell G, Rasche F, Sessitsch A. 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
40. Gans J, Wolinsky M, Dunbar J. 2005. Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309:1387-90
41. Glick BR. 2014. Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol. Res. 169:30-39
42. Gourion B, Rossignol M, Vorholt JA. 2006. A proteomic study of Methylobacterium extorquens reveals a response regulator essential for epiphytic growth. PNAS 103:13186-91
43. Haas D, Defago G. 2005. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat. Rev. Microbiol. 3:307-19
44. Hacquard S, Garrido-Oter R, Gonzalez A, Spaepen S, Ackermann G, et al. 2015. Microbiota and host nutrition across plant and animal kingdoms. Cell Host Microbe 17:603-16
45. Hacquard S, Kracher B, Hiruma K,Münch PC, Garrido-Oter R, et al. 2016. Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi. Nat. Commun. 7:11362
46. Haichar FE, Heulin T, Guyonnet JP, Achouak W. 2016. Stable isotope probing of carbon flow in the plant holobiont. Curr. Opin. Biotechnol. 41:9-13
47. Handelsman J, Rondon MR, Brady SF, Clardy J, Goodman RM. 1998. Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem. Biol. 5:R245-49
48. Haney CH, Samuel BS, Bush J, Ausubel FM. 2015. Associations with rhizosphere bacteria can confer an adaptive advantage to plants. Nat. Plants 1:15051
49. 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
50. Hiruma K, Gerlach N, Sacristán S, Nakano RT, Hacquard S, et al. 2016. Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status-dependent. Cell 165:464-74
51. HortonMW,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
52. Hsu CC, Dorrestein PC. 2015. Visualizing life with ambient mass spectrometry. Curr. Opin. Biotechnol. 31:24-34
53. HuangWE, Ferguson A, Singer AC, Lawson K, Thompson IP, 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
54. Ikeda S, Anda M, Inaba S, Eda S, Sato S, 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
55. Inceoglu O, Al-Soud WA, Salles JF, Semenov AV, van Elsas JD. 2011. Comparative analysis of bacterial communities in a potato field as determined by pyrosequencing. PLOS ONE 6:e23321
56. Inceoglu O, Salles JF, van Elsas JD. 2012. Soil and cultivar type shape the bacterial community in the potato rhizosphere. Microb. Ecol. 63:460-70
57. Innerebner G, Knief C, Vorholt JA. 2011. Protection of Arabidopsis thaliana against leaf-pathogenic Pseudomonas syringae by Sphingomonas strains in a controlled model system. Appl. Environ. Microbiol. 77:3202-10
58. Johnston-Monje D, Mousa WK, Lazarovits G, Raizada MN. 2014. Impact of swapping soils on the endophytic bacterial communities of pre-domesticated, ancient and modern maize. BMC Plant Biol. 14:233
59. Kaczmarczyk A, Campagne S, Danza F, Metzger LC, Vorholt JA, Francez-Charlot A. 2011. Role of Sphingomonas sp. strain Fr1 PhyR-NepR-σEcfG cascade in general stress response and identification of a negative regulator . PhyR. J. Bacteriol. 193:6629-38
60. Kadivar H, Stapleton AE. 2003. Ultraviolet radiation altersmaize phyllosphere bacterial diversity. Microb. Ecol. 45:353-61
61. Kavamura VN, Taketani RG, Lanconi MD, Andreote FD, Mendes R, de Melo IS. 2013. Water regime influences bulk soil and rhizosphere of Cereus jamacaru bacterial communities in the Brazilian Caatinga biome. PLOS ONE 8:e73606
62. Kembel SW,O'ConnorTK, Arnold HK,Hubbell SP,Wright SJ, Green JL. 2014. Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. PNAS 111:13715-20
63. Kemen E. 2014. Microbe-microbe interactions determine oomycete and fungal host colonization. Curr. Opin. Plant Biol. 20:75-81
64. 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
65. Knief C, Ramette A, Frances L, Alonso-Blanco C, Vorholt JA. 2010. Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere. ISME J. 4:719-28
66. 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
67. Kolton M, Frenkel O, Elad Y, Cytryn E. 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
68. Laforest-Lapointe I,Messier C, Kembel SW. 2016. Host species identity, site and time drive temperate tree phyllosphere bacterial community structure. Microbiome 4:27
69. Lau JA, Lennon JT. 2012. Rapid responses of soil microorganisms improve plant fitness in novel environments. PNAS 109:14058-62
70. 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
71. Lee B, Lee S, Ryu C-M. 2012. Foliar aphid feeding recruits rhizosphere bacteria and primes plant immunity against pathogenic and non-pathogenic bacteria in pepper. Ann. Bot. 110:281-90
72. Li X, Rui J, Xiong J, Li J, He Z, et al. 2014. Functional potential of soil microbial communities in the maize rhizosphere. PLOS ONE 9:e112609
73. Lindow SE, Brandl MT. 2003. Microbiology of the phyllosphere. Appl. Environ. Microbiol. 69:1875-83
74. Lindow SE, Leveau JH. 2002. Phyllosphere microbiology. Curr. Opin. Biotechnol. 13:238-43
75. Lu Y, Conrad R. 2005. In situ stable isotope probing of methanogenic archaea in the rice rhizosphere. Science 309:1088-90
76. Lugtenberg B, Kamilova F. 2009. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63:541-56
77. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, et al. 2012. Defining the core Arabidopsis thaliana root microbiome. Nature 488:86-90
78. Maignien L, DeForce EA, Chafee ME, Eren AM, Simmons SL. 2014. Ecological succession and stochastic variation in the assembly of Arabidopsis thaliana phyllosphere communities. mBio 5:e00682-13
79. Manching HC, Balint-Kurti PJ, Stapleton AE. 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
80. Mendes LW, Kuramae EE, Navarrete AA, van Veen JA, Tsai SM. 2014. Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J. 8:1577-87
81. Mendes R, Garbeva P, Raaijmakers JM. 2013. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol. Rev. 37:634-63
82. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der VoortM, et al. 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097-100
83. Mondy S, Lenglet A, Beury-Cirou A, Libanga C, Ratet P, 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
84. Moran NA, Sloan DB. 2015. The hologenome concept: helpful or hollow? PLOS Biol. 13:e1002311
85. Mueller UG, Sachs JL. 2015. Engineering microbiomes to improve plant and animal health. Trends Microbiol. 23:606-17
86. Mushegian AA, EbertD. 2016. Rethinking "mutualism" in diverse host-symbiont communities. BioEssays 38:100-8
87. Neal AL, Ahmad S, Gordon-Weeks R, Ton J. 2012. Benzoxazinoids in root exudates of maize attract Pseudomonas putida to the rhizosphere. PLOS ONE 7:e35498
88. Ofek-Lalzar M, Sela N, Goldman-Voronov M, Green SJ, Hadar Y, Minz D. 2014. Niche and hostassociated functional signatures of the root surface microbiome. Nat. Commun. 5:4950
89. Oh YM, Kim M, Lee-Cruz L, Lai-Hoe A, Go R, et al. 2012. Distinctive bacterial communities in the rhizoplane of four tropical tree species. Microb. Ecol. 64:1018-27
90. OldroydGED,Murray JD, Poole PS, Downie JA. 2011. The rules of engagement in the legume-rhizobial symbiosis. Annu. Rev. Genet. 45:119-44
91. Ottesen AR, Gonzalez Pena A, White JR, Pettengill JB, Li C, et al. 2013. Baseline survey of the anatomical microbial ecology of an important food plant: Solanum lycopersicum (tomato). BMC Microbiol. 13:114
92. Panke-Buisse K, Poole AC, Goodrich JK, Ley RE, Kao-Kniffin J. 2015. Selection on soil microbiomes reveals reproducible impacts on plant function. ISME J. 9:980-89
93. Parniske M. 2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6:763-75
94. 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
95. Pieterse CMJ, ZamioudisC, Berendsen RL,WellerDM, Van Wees SCM, Bakker PAHM.2014. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52:347-75
96. Pilon-Smits E. 2005. Phytoremediation. Annu. Rev. Plant Biol. 56:15-39
97. Raaijmakers JM,Mazzola M. 2012. Diversity and natural functions of antibiotics produced by beneficial and plant pathogenic bacteria. Annu. Rev. Phytopathol. 50:403-24
98. Raes J, Bork P. 2008. Molecular eco-systems biology: towards an understanding of community function. Nat. Rev. Microbiol. 6:693-99
99. Raghavendra AKH,NewcombeG. 2013. The contribution of foliar endophytes to quantitative resistance to Melampsora rust. New Phytol. 197:909-18
100. Ramirez-Puebla ST, Servin-Garciduenas LE, Jimenez-Marin B, Bolanos LM, Rosenblueth M, et al. 2013. Gut and root microbiota commonalities. Appl. Environ. Microbiol. 79:2-9
101. Rastogi G, Sbodio A, Tech JJ, Suslow TV, Coaker GL, Leveau JHJ. 2012. Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J. 6:1812-22
102. Redford AJ, Bowers RM, Knight R, Linhart Y, Fierer N. 2010. The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ. Microbiol. 12:2885-93
103. Reinhold-Hurek B, BüngerW, Burbano CS, Sabale M, HurekT. 2015. Roots shaping theirmicrobiome: global hotspots for microbial activity. Annu. Rev. Phytopathol. 53:403-24
104. Reisberg EE, Hildebrandt U, Riederer M, Hentschel U. 2013. Distinct phyllosphere bacterial communities on Arabidopsis wax mutant leaves. PLOS ONE 8:e78613
105. Remus-EmsermannMN, Lücker S,MüllerDB, PotthoffE,DaimsH,Vorholt JA. 2014. Spatial distribution analyses of natural phyllosphere-colonizing bacteria on Arabidopsis thaliana revealed by fluorescence in situ hybridization. Environ. Microbiol. 16:2329-40
106. Ritpitakphong U, Falquet L, Vimoltust A, Berger A, Metraux JP, L'Haridon F. 2016. The microbiome of the leaf surface of Arabidopsis protects against a fungal pathogen. New Phytol. 210:1033-43
107. Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, 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
108. Rudrappa T, Czymmek KJ, Pare PW, Bais HP. 2008. Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol. 148:1547-56
109. Ryffel F, Helfrich EJ, Kiefer P, Peyriga L, Portais JC, et al. 2016. Metabolic footprint of epiphytic bacteria on Arabidopsis thaliana leaves. ISME J. 10:632-43
110. Ryu CM. 2015. Against friend and foe: type 6 effectors in plant-associated bacteria. J. Microbiol. 53:201-8
111. Scheublin TR,Deusch S,Moreno-Forero SK,Müller JA, van der Meer JR, Leveau JHJ. 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
112. Schlaeppi K, Bulgarelli D. 2015. The plant microbiome at work. Mol. Plant-Microbe Interact. 28:212-17
113. Schlaeppi K, Dombrowski N, Oter RG, van Themaat EVL, Schulze-Lefert P. 2014. Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. PNAS 111:585-92
114. 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
115. Shade A, McManus PS, Handelsman J. 2013. Unexpected diversity during community succession in the apple flower microbiome. mBio 4:e00602-12
116. Shakya M, Gottel N, Castro H, Yang ZK, Gunter L, 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
117. Sheibani-Tezerji R, Rattei T, Sessitsch A, Trognitz F, Mitter B. 2015. Transcriptome profiling of the endophyte Burkholderia phytofirmans PsJN indicates sensing of the plant environment and drought stress. mBio 6:e00621-15
118. Shi S, Nuccio E, Herman DJ, Rijkers R, Estera K, et al. 2015. Successional trajectories of rhizosphere bacterial communities over consecutive seasons. mBio 6:e00746-15
119. Smith SE, Smith FA. 2011. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu. Rev. Plant Biol. 62:227-50
120. Spaepen S, Bossuyt S, Engelen K, Marchal K, Vanderleyden J. 2014. Phenotypical and molecular responses of Arabidopsis thaliana roots as a result of inoculationwith the auxin-producing bacterium Azospirillum brasilense. New Phytol. 201:850-61
121. Spaepen S, Vanderleyden J, Remans R. 2007. Indole-3-acetic acid in microbial andmicroorganism-plant signaling. FEMS Microbiol. Rev. 31:425-48
122. Stiefel P, Zambelli T, Vorholt JA. 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
123. Stockwell VO, Johnson KB, Sugar D, Loper JE. 2011. Mechanistically compatible mixtures of bacterial antagonists improve biological control of fire blight of pear. Phytopathology 101:113-23
124. Suda W, Nagasaki A, Shishido M. 2009. Powdery mildew-infection changes bacterial community composition in the phyllosphere. Microbes Environ. 24:217-23
125. Sugiyama A, Ueda Y, ZushiT,TakaseH, YazakiK. 2014. Changes in the bacterial community of soybean rhizospheres during growth in the field. PLOS ONE 9:e100709
126. Sy A, Timmers AC, Knief C, Vorholt JA. 2005. Methylotrophic metabolism is advantageous for Methylobacterium extorquens during colonization of Medicago truncatula under competitive conditions. Appl. Environ. Microbiol. 71:7245-52
127. Thebault E, Fontaine C. 2010. Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329:853-56
128. TheisKR, Dheilly NM, Klassen JL, BruckerRM, Baines JF, et al. 2016. Getting the hologenome concept right: an eco-evolutionary framework for hosts and their microbiomes. mSystems 1:e00028-16
129. Thijs S, Sillen W, Rineau F, Weyens N, Vangronsveld J. 2016. Towards an enhanced understanding of plant-microbiome interactions to improve phytoremediation: engineering the metaorganism. Front Microbiol. 7:341
130. Thompson IP, Bailey MJ, Fenlon JS, Fermor TR, Lilley AK, 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
131. Tkacz A, Poole P. 2015. Role of root microbiota in plant productivity. J. Exp. Bot. 66:2167-75
132. Turner TR, James EK, Poole PS. 2013. The plant microbiome. Genome Biol. 14:209
133. Turner TR, Ramakrishnan K, Walshaw J, Heavens D, Alston M, et al. 2013. Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J. 7:2248-58
134. UdvardiM, Poole PS. 2013. Transport and metabolism in legume-rhizobia symbioses. Annu. Rev. Plant Biol. 64:781-805
135. Urquiaga S, Xavier RP, de Morais RF, Batista RB, Schultz N, 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
136. van Mortel JE, Vos RCH, Dekkers E, Pineda A, Guillod L, et al. 2012. Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol. 160:2173-88
137. Vandenkoornhuyse P,Mahe S, Ineson P, Staddon P, Ostle N, et al. 2007. Active root-inhabiting microbes identified by rapid incorporation of plant-derived carbon into RNA. PNAS 104:16970-75
138. 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
139. van der HeijdenMG, Bruin S, Luckerhoff L, van Logtestijn RS, Schlaeppi K. 2016. A widespread plantfungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment. ISME J. 10:389-99
140. van Elsas JD, Chiurazzi M, Mallon CA, Elhottova D, Kristufek V, Salles JF. 2012. Microbial diversity determines the invasion of soil by a bacterial pathogen. PNAS 109:1159-64
141. VogelC, Bodenhausen N, GruissemW,Vorholt JA. 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
142. Vogel C, Innerebner G, Zingg J, Guder J, Vorholt JA. 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
143. Vorholt JA. 2012. Microbial life in the phyllosphere. Nat. Rev. Microbiol. 10:828-40
144. Wagner MR, Lundberg DS, Coleman-Derr D, Tringe SG, Dangl JL, Mitchell-Olds T. 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
145. Wei Z, Yang T, Friman V-P, Xu Y, Shen Q, Jousset A. 2015. Trophic network architecture of rootassociated bacterial communities determines pathogen invasion and plant health. Nat. Commun. 6:8413
146. Weston DJ, Pelletier DA, Morrell-Falvey JL, Tschaplinski TJ, Jawdy SS, 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
147. White LJ, Jothibasu K, Reese RN, Broezel VS, Subramanian S. 2015. Spatio temporal influence of isoflavonoids on bacterial diversity in the soybean rhizosphere. Mol. Plant-Microbe Interact. 28:22-29
148. Williams TR, MarcoML. 2014. Phyllosphere microbiota composition and microbial community transplantation on lettuce plants grown indoors. mBio 5:e01564-14
149. Williams TR, Moyne AL, Harris LJ, Marco ML. 2013. Season, irrigation, leaf age, and Escherichia coli inoculation influence the bacterial diversity in the lettuce phyllosphere. PLOS ONE 8:e68642
150. Yang J, Kloepper JW, Ryu CM. 2009. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 14:1-4
151. Yang JW, Yi HS, 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
152. Yeoh YK, Paungfoo-Lonhienne C, Dennis PG, Robinson N, Ragan MA, et al. 2016. The core root microbiome of sugarcanes cultivated under varying nitrogen fertilizer application. Environ. Microbiol. 18:1338-51
153. Yu X, Lund SP, Scott RA, Greenwald JW, Records AH, et al. 2013. Transcriptional responses of Pseudomonas syringae to growth in epiphytic versus apoplastic leaf sites. PNAS 110:E425-34
154. Zamioudis C, Korteland J, Van Pelt JA, van HamersveldM, Dombrowski N, 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
155. ZamioudisC,Mastranesti P, Dhonukshe P, Blilou I, PieterseCMJ. 2013. Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiol. 162:304-18
156. Zancarini A,Mougel C, Voisin AS, Prudent M, SalonC,Munier-Jolain N. 2012. Soil nitrogen availability and plant genotype modify the nutrition strategies of M. truncatula and the associated rhizosphere microbial communities. PLOS ONE 7:e47096
157. Zarraonaindia I, Owens SM,Weisenhorn P, West K, Hampton-Marcell J, et al. 2015. The soil microbiome influences grapevine-associated microbiota. mBio 6:e02527-14
158. Zhang HM, Sun Y, Xie XT, Kim MS, Dowd SE, Pare PW. 2009. A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J. 58:568-77
159. Zipfel C. 2014. Plant pattern-recognition receptors. Trends Immunol. 35:345-351