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Annual Review of Plant Biology

Volume 74, 2023

Phyllosphere Microbiome

Abstract

The aboveground parts of terrestrial plants are colonized by a variety of microbes that collectively constitute the phyllosphere microbiota. Decades of pioneering work using individual phyllosphere microbes, including commensals and pathogens, have provided foundational knowledge about how individual microbes adapt to the phyllosphere environment and their role in providing biological control against pathogens. Recent studies have revealed a more complete repertoire of phyllosphere microbiota across plant taxa and how plants respond to and regulate the level and composition of phyllosphere microbiota. Importantly, the development of several gnotobiotic systems is allowing causative and mechanistic studies to determine the contributions of microbiota to phyllosphere health and productivity. New insights into how the phyllosphere carries out key biological processes, including photosynthesis, biomass accumulation, reproduction, and defense against biotic and abiotic insults, in either the presence or absence of a normal microbiota could unleash novel plant- and microbiota-based technologies to improve agriculturally relevant traits of crop plants.

Keyword(s): dysbiosis, endophyte, epiphyte, gut microbiome, phytobiome, plant immunity
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2023-05-22
2024-04-28
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Literature Cited

  1. 1.
    Abanda-Nkpwatt D, Musch M, Tschiersch J, Boettner M, Schwab W. 2006. Molecular interaction between Methylobacterium extorquens and seedlings: growth promotion, methanol consumption, and localization of the methanol emission site. J. Exp. Bot. 57:4025–32
     [Google Scholar]
  2. 2.
    Abdelfattah A, Freilich S, Bartuv R, Zhimo VY, Kumar A et al. 2021. Global analysis of the apple fruit microbiome: Are all apples the same?. Environ. Microbiol. 23:6038–55
     [Google Scholar]
  3. 3.
    Abdelfattah A, Whitehead SR, Macarisin D, Liu J, Burchard E et al. 2020. Effect of washing, waxing and low-temperature storage on the postharvest microbiome of apple. Microorganisms 8:944
     [Google Scholar]
  4. 4.
    Agler MT, Ruhe J, Kroll S, Morhenn C, Kim S-T et al. 2016. Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLOS Biol 14:e1002352Provides evidence for the existence of microbial hubs, which transmit the effects of host and environmental factors on the overall Arabidopsis phyllosphere microbiome structure.
     [Google Scholar]
  5. 5.
    Alagarasan G, Aswathy KS, Madhaiyan M. 2017. Shoot the message, not the messenger—combating pathogenic virulence in plants by inhibiting quorum sensing mediated signaling molecules. Front. Plant Sci. 8:556
     [Google Scholar]
  6. 6.
    Alcaraz LD, Peimbert M, Barajas HR, Dorantes-Acosta AE, Bowman JL, Arteaga-Vázquez MA. 2018. Marchantia liverworts as a proxy to plants’ basal microbiomes. Sci. Rep. 8:12712
     [Google Scholar]
  7. 7.
    Almario J, Mahmoudi M, Kroll S, Agler M, Placzek A et al. 2022. The leaf microbiome of Arabidopsis displays reproducible dynamics and patterns throughout the growing season. mBio 13:e02825-21
     [Google Scholar]
  8. 8.
    Arun KD, Sabarinathan KG, Gomathy M, Kannan R, Balachandar D. 2020. Mitigation of drought stress in rice crop with plant growth-promoting abiotic stress-tolerant rice phyllosphere bacteria. J. Basic Microbiol. 60:768–86
     [Google Scholar]
  9. 9.
    Bai Y, Müller DB, Srinivas G, Garrido-Oter R, Potthoff E et al. 2015. Functional overlap of the Arabidopsis leaf and root microbiota. Nature 528:364–69Characterized a comprehensive At-SPHERE bacterial culture collection from Arabidopsis roots and leaves, facilitating mechanistic studies in Arabidopsis microbiome research.
     [Google Scholar]
  10. 10.
    Barge EG, Leopold DR, Peay KG, Newcombe G, Busby PE. 2019. Differentiating spatial from environmental effects on foliar fungal communities of Populus trichocarpa. J. Biogeogr. 46:2001–11
     [Google Scholar]
  11. 11.
    Bar-On YM, Phillips R, Milo R 2018. The biomass distribution on Earth. PNAS 115:6506–11
     [Google Scholar]
  12. 12.
    Bashir I, War AF, Rafiq I, Reshi ZA, Rashid I, Shouche YS. 2022. Phyllosphere microbiome: diversity and functions. Microbiol. Res. 254:126888
     [Google Scholar]
  13. 13.
    Beck M, Wyrsch I, Strutt J, Wimalasekera R, Webb A et al. 2014. Expression patterns of FLAGELLIN SENSING 2 map to bacterial entry sites in plant shoots and roots. J. Exp. Bot. 65:6487–98
     [Google Scholar]
  14. 14.
    Bell-Dereske LP, Evans SE 2021. Contributions of environmental and maternal transmission to the assembly of leaf fungal endophyte communities. Proc. R. Soc. B 288:20210621
     [Google Scholar]
  15. 15.
    Bentley BL. 1987. Nitrogen fixation by epiphylls in a tropical rainforest. Ann. Missouri Bot. Gard. 74:234–41
     [Google Scholar]
  16. 16.
    Benucci GMN, Burnard D, Shepherd LD, Bonito G, Munkacsi AB. 2020. Evidence for co-evolutionary history of early diverging Lycopodiaceae plants with fungi. Front. Microbiol. 10:2944
     [Google Scholar]
  17. 17.
    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]
  18. 18.
    Berens ML, Wolinska KW, Spaepen S, Ziegler J, Nobori T et al. 2019. Balancing trade-offs between biotic and abiotic stress responses through leaf age-dependent variation in stress hormone cross-talk. PNAS 116:2364–73
     [Google Scholar]
  19. 19.
    Berg A, Danielsson Å, Svensson BH. 2013. Transfer of fixed-N from N2-fixing cyanobacteria associated with the moss Sphagnum riparium results in enhanced growth of the moss. Plant Soil 362:271–78
     [Google Scholar]
  20. 20.
    Berger CN, Sodha SV, Shaw RK, Griffin PM, Pink D et al. 2010. Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ. Microbiol. 12:2385–97
     [Google Scholar]
  21. 21.
    Bernal P, Allsopp LP, Filloux A, Llamas MA. 2017. The Pseudomonas putida T6SS is a plant warden against phytopathogens. ISME J 11:972–87
     [Google Scholar]
  22. 22.
    Blattman SB, Jiang W, Oikonomou P, Tavazoie S. 2020. Prokaryotic single-cell RNA sequencing by in situ combinatorial indexing. Nat. Microbiol. 5:1192–201
     [Google Scholar]
  23. 23.
    Bodenhausen N, Horton MW, Bergelson J. 2013. Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLOS ONE 8:e56329
     [Google Scholar]
  24. 24.
    Boivin S, Fonouni-Farde C, Frugier F. 2016. How auxin and cytokinin phytohormones modulate root microbe interactions. Front. Plant Sci. 7:1240
     [Google Scholar]
  25. 25.
    Bonanomi G, Antignani V, Pane C, Scala E. 2007. Suppression of soilborne fungal diseases with organic amendments. J. Plant Pathol. 89:311–24
     [Google Scholar]
  26. 26.
    Bouchard R, Peñaloza-Bojacá G, Toupin S, Guadalupe Y, Gudiño J et al. 2020. Contrasting bacteriome of the hornwort Leiosporoceros dussii in two nearby sites with emphasis on the hornwort-cyanobacterial symbiosis. Symbiosis 81:39–52
     [Google Scholar]
  27. 27.
    Brandl MT, Mandrell RE. 2002. Fitness of Salmonella enterica serovar Thompson in the cilantro phyllosphere. Appl. Environ. Microbiol. 68:3614–21
     [Google Scholar]
  28. 28.
    Bringel F, Couée I. 2015. Pivotal roles of phyllosphere microorganisms at the interface between plant functioning and atmospheric trace gas dynamics. Front. Microbiol. 6:486
     [Google Scholar]
  29. 29.
    Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Droge 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]
  30. 30.
    Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P. 2013. Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64:807–38
     [Google Scholar]
  31. 31.
    Büttner D, He SY. 2009. Type III protein secretion in plant pathogenic bacteria. Plant Physiol 150:1656–64
     [Google Scholar]
  32. 32.
    Carrell AA, Frank AC. 2014. Pinus flexilis and Picea engelmannii share a simple and consistent needle endophyte microbiota with a potential role in nitrogen fixation. Front. Microbiol. 5:333
     [Google Scholar]
  33. 33.
    Chang WS, van de Mortel M, Nielsen L, de Guzman GN, Li XH, Halverson LJ. 2007. Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water-limiting conditions. J. Bacteriol. 189:8290–99
     [Google Scholar]
  34. 34.
    Chen T, Nomura K, Wang X, Sohrabi R, Xu J et al. 2020. A plant genetic network for preventing dysbiosis in the phyllosphere. Nature 580:653–57Showed a causal relationship for microbiota-mediated dysbiosis and reported several components of a genetic framework for controlling microbiota homeostasis in Arabidopsis.
     [Google Scholar]
  35. 35.
    Clay K. 1988. Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69:10–16
     [Google Scholar]
  36. 36.
    Clay K, Schardl C. 2002. Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am. Nat. 160:S99–127
     [Google Scholar]
  37. 37.
    Colaianni NR, Parys K, Lee H-S, Conway JM, Kim NH et al. 2021. A complex immune response to flagellin epitope variation in commensal communities. Cell Host Microbe 29:635–49. E9 Showed an important correlation between immune-evading microbiota flg22 epitope variants and their ability to dominate host colonization in healthy plants.
     [Google Scholar]
  38. 38.
    Cooley MB, Miller WG, Mandrell RE. 2003. Colonization of Arabidopsis thaliana with Salmonella enterica and enterohemorrhagic Escherichia coli O157:H7 and competition by Enterobacter asburiae. Appl. Environ. Microb. 69:4915–26
     [Google Scholar]
  39. 39.
    Darby HM, Stone AG, Dick RP. 2006. Compost and manure mediated impacts on soilborne pathogens and soil quality. Soil Sci. Soc. Am. J. 70:347–58
     [Google Scholar]
  40. 40.
    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
     [Google Scholar]
  41. 41.
    Dong S, Ma W. 2021. How to win a tug-of-war: the adaptive evolution of Phytophthora effectors. Curr. Opin. Plant Biol. 62:102027
     [Google Scholar]
  42. 42.
    Dudenhöffer JH, Scheu S, Jousset A. 2016. Systemic enrichment of antifungal traits in the rhizosphere microbiome after pathogen attack. J. Ecol. 104:1566–75
     [Google Scholar]
  43. 43.
    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.e14
     [Google Scholar]
  44. 44.
    Eichmann R, Richards L, Schafer P. 2021. Hormones as go-betweens in plant microbiome assembly. Plant J 105:518–41
     [Google Scholar]
  45. 45.
    Elbert W, Weber B, Burrows S, Steinkamp J, Budel B et al. 2012. Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat. Geosci. 5:459–62
     [Google Scholar]
  46. 46.
    Fan SP, Miao LY, Li HD, Lin AH, Song FJ, Zhang P. 2020. Illumina-based analysis yields new insights into the diversity and composition of endophytic fungi in cultivated Huperzia serrata. PLOS ONE 15:e0242258
     [Google Scholar]
  47. 47.
    Finkel OM, Salas-González I, Castrillo G, Conway JM, Law TF et al. 2020. A single bacterial genus maintains root growth in a complex microbiome. Nature 587:103–8
     [Google Scholar]
  48. 48.
    Finkel OM, Salas-González I, Castrillo G, Spaepen S, Law TF et al. 2019. The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response. PLOS Biol 17:e3000534
     [Google Scholar]
  49. 49.
    Forero-Junco LM, Alanin KWS, Djurhuus AM, Kot W, Gobbi A, Hansen LH. 2022. Bacteriophages roam the wheat phyllosphere. Viruses 14:244
     [Google Scholar]
  50. 50.
    Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H et al. 2006. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat. Genet. 38:953–56
     [Google Scholar]
  51. 51.
    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
     [Google Scholar]
  52. 52.
    Gao C, Montoya L, Xu L, Madera M, Hollingsworth J et al. 2020. Fungal community assembly in drought-stressed sorghum shows stochasticity, selection, and universal ecological dynamics. Nat. Commun. 11:34
     [Google Scholar]
  53. 53.
    Gentzel I, Giese L, Ekanayake G, Mikhail K, Zhao W et al. 2022. Dynamic nutrient acquisition from a hydrated apoplast supports biotrophic proliferation of a bacterial pathogen of maize. Cell Host Microbe 30:502–17.e4
     [Google Scholar]
  54. 54.
    Giraldo MC, Dagdas YF, Gupta YK, Mentlak TA, Yi M et al. 2013. Two distinct secretion systems facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae. Nat. Commun. 4:1996
     [Google Scholar]
  55. 55.
    Grady KL, Sorensen JW, Stopnisek N, Guittar J, Shade A. 2019. Assembly and seasonality of core phyllosphere microbiota on perennial biofuel crops. Nat. Commun. 10:4135
     [Google Scholar]
  56. 56.
    Granér G, Persson P, Meijer J, Alström S. 2003. A study on microbial diversity in different cultivars of Brassica napus in relation to its wilt pathogen, Verticillium longisporum. FEMS Microbiol. Lett. 224:269–76
     [Google Scholar]
  57. 57.
    Gu G, Hu J, Cevallos-Cevallos JM, Richardson SM, Bartz JA, van Bruggen AH. 2011. Internal colonization of Salmonella enterica serovar Typhimurium in tomato plants. PLOS ONE 6:e27340
     [Google Scholar]
  58. 58.
    Hardoim PR, Hardoim CCP, van Overbeek LS, van Elsas JD. 2012. Dynamics of seed-borne rice endophytes on early plant growth stages. PLOS ONE 7:e30438
     [Google Scholar]
  59. 59.
    Hauben L, Moore ERB, Vauterin L, Steenackers M, Mergaert J et al. 1998. Phylogenetic position of phytopathogens within the Enterobacteriaceae. Syst. Appl. Microbiol. 21:384–97
     [Google Scholar]
  60. 60.
    He Z, Webster S, He SY. 2022. Growth–defense trade-offs in plants. Curr. Biol. 32:R634–39
     [Google Scholar]
  61. 61.
    Helfrich EJN, Vogel CM, Ueoka R, Schäfer 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]
  62. 62.
    Hirano SS, Upper CD. 2000. Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae—a pathogen, ice nucleus, and epiphyte. Microbiol. Mol. Biol. Rev. 64:624–53
     [Google Scholar]
  63. 63.
    Ho BT, Dong TG, Mekalanos JJ. 2014. A view to a kill: the bacterial type VI secretion system. Cell Host Microbe 15:9–21
     [Google Scholar]
  64. 64.
    Hodgson S, de Cates C, Hodgson J, Morley NJ, Sutton BC, Gange AC. 2014. Vertical transmission of fungal endophytes is widespread in forbs. Ecol. Evol. 4:1199–208
     [Google Scholar]
  65. 65.
    Holland MA 2011. Nitrogen: give and take from phylloplane microbes. Ecological Aspects of Nitrogen Metabolism in Plants JC Polacco, CD Todd 215–30. Chichester, UK: Wiley
     [Google Scholar]
  66. 66.
    Hu Y, Ding Y, Cai B, Qin X, Wu J et al. 2022. Bacterial effectors manipulate plant abscisic acid signaling for creation of an aqueous apoplast. Cell Host Microbe 30:518–29.e6
     [Google Scholar]
  67. 67.
    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
     [Google Scholar]
  68. 68.
    Inoue Y, Vy TTP, Yoshida K, Asano H, Mitsuoka C et al. 2017. Evolution of the wheat blast fungus through functional losses in a host specificity determinant. Science 357:80–83
     [Google Scholar]
  69. 69.
    Iqbal N, Khan NA, Ferrante A, Trivellini A, Francini A, Khan MIR. 2017. Ethylene role in plant growth, development and senescence: interaction with other phytohormones. Front. Plant Sci. 8:475
     [Google Scholar]
  70. 70.
    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
     [Google Scholar]
  71. 71.
    Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:323–29
     [Google Scholar]
  72. 72.
    Joyner DC, Lindow SE. 2000. Heterogeneity of iron bioavailability on plants assessed with a whole-cell GFP-based bacterial biosensor. Microbiology 146:2435–45
     [Google Scholar]
  73. 73.
    Jumpponen A, Jones KL. 2009. Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere. New Phytol 184:438–48
     [Google Scholar]
  74. 74.
    Junker RR, Keller A. 2015. Microhabitat heterogeneity across leaves and flower organs promotes bacterial diversity. FEMS Microbiol. Ecol. 91:fiv097
     [Google Scholar]
  75. 75.
    Junker RR, Tholl D. 2013. Volatile organic compound mediated interactions at the plant-microbe interface. J. Chem. Ecol. 39:810–25
     [Google Scholar]
  76. 76.
    Karasov TL, Almario J, Friedemann C, Ding W, Giolai M et al. 2018. Arabidopsis thaliana and Pseudomonas pathogens exhibit stable associations over evolutionary timescales. Cell Host Microbe 24:168–79.e4
     [Google Scholar]
  77. 77.
    Karasov TL, Neumann M, Duque-Jaramillo A, Kersten S, Bezrukov I et al. 2020. The relationship between microbial population size and disease in the Arabidopsis thaliana phyllosphere. bioRxiv 828814. https://doi.org/10.1101/828814
    [Google Scholar]
  78. 78.
    Kim D-R, Cho G, Jeon C-W, Weller DM, Thomashow LS et al. 2019. A mutualistic interaction between Streptomyces bacteria, strawberry plants and pollinating bees. Nat. Commun. 10:4802Reported beneficial Streptomyces movement from root to flower via vascular bundles and from flower to flower mediated by pollinators.
     [Google Scholar]
  79. 79.
    Klarenberg IJ, Keuschnig C, Russi Colmenares AJ, Warshan D, Jungblut AD et al. 2021. Long-term warming effects on the microbiome and nifH gene abundance of a common moss species in sub-Arctic tundra. New Phytol. 234:2044–56Provided evidence for the negative impact of climate change on the moss phyllosphere microbiome (e.g., reduction of diazotrophic bacteria).
     [Google Scholar]
  80. 80.
    Knack JJ, Wilcox LW, Delaux P-M, Ané J-M, Piotrowski MJ et al. 2015. Microbiomes of streptophyte algae and bryophytes suggest that a functional suite of microbiota fostered plant colonization of land. Int. J. Plant Sci. 176:405–20
     [Google Scholar]
  81. 81.
    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]
  82. 82.
    Kolton M, Weston DJ, Mayali X, Weber PK, McFarlane KJ et al. 2022. Defining the Sphagnum core microbiome across the North American continent reveals a central role for diazotrophic methanotrophs in the nitrogen and carbon cycles of boreal peatland ecosystems. mBio 13:e03714-21
     [Google Scholar]
  83. 83.
    Kremer JM, Sohrabi R, Paasch BC, Rhodes D, Thireault C et al. 2021. Peat-based gnotobiotic plant growth systems for Arabidopsis microbiome research. Nat. Protoc. 16:2450–70
     [Google Scholar]
  84. 84.
    Kroupitski Y, Pinto R, Brandl MT, Belausov E, Sela S 2009. Interactions of Salmonella enterica with lettuce leaves. J. Appl. Microbiol. 106:1876–85
     [Google Scholar]
  85. 85.
    Kuchina A, Brettner LM, Paleologu L, Roco CM, Rosenberg AB et al. 2021. Microbial single-cell RNA sequencing by split-pool barcoding. Science 371:6531
     [Google Scholar]
  86. 86.
    Kumar M, Kumar A, Sahu KP, Patel A, Reddy B et al. 2021. Deciphering core-microbiome of rice leaf endosphere: revelation by metagenomic and microbiological analysis of aromatic and non-aromatic genotypes grown in three geographical zones. Microbiol. Res. 246:126704
     [Google Scholar]
  87. 87.
    Laforest-Lapointe I, Messier C, Kembel SW. 2016. Host species identity, site and time drive temperate tree phyllosphere bacterial community structure. Microbiome 4:27
     [Google Scholar]
  88. 88.
    Lanver D, Tollot M, Schweizer G, Lo Presti L, Reissmann S et al. 2017. Ustilago maydis effectors and their impact on virulence. Nat. Rev. Microbiol. 15:409–21
     [Google Scholar]
  89. 89.
    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
     [Google Scholar]
  90. 90.
    Leveau JHJ, Lindow SE. 2001. Appetite of an epiphyte: quantitative monitoring of bacterial sugar consumption in the phyllosphere. PNAS 98:3446–53
     [Google Scholar]
  91. 91.
    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]
  92. 92.
    Li M, Hong L, Ye W, Wang Z, Shen H 2022. Phyllosphere bacterial and fungal communities vary with host species identity, plant traits and seasonality in a subtropical forest. Environ. Microbiome 17:29
     [Google Scholar]
  93. 93.
    Liber JA, Minier DH, Stouffer-Hopkins A, Van Wyk J, Longley R, Bonito G. 2022. Maple and hickory leaf litter fungal communities reflect pre-senescent leaf communities. PeerJ 10:e12701
     [Google Scholar]
  94. 94.
    Lidstrom ME, Chistoserdova L. 2002. Plants in the pink: cytokinin production by Methylobacterium. J. Bacteriol. 184:1818
     [Google Scholar]
  95. 95.
    Lindow SE. 1983. The role of bacterial ice nucleation in frost injury to plants. Annu. Rev. Phytopathol. 21:363–84
     [Google Scholar]
  96. 96.
    Lindow SE, Andersen G, Beattie GA. 1993. Characteristics of insertional mutants of Pseudomonas syringae with reduced epiphytic fitness. Appl. Environ. Microbiol. 59:1593–601
     [Google Scholar]
  97. 97.
    Lindow SE, Arny DC, Upper CD. 1978. Distribution of ice nucleation-active bacteria on plants in nature. Appl. Environ. Microbiol. 36:831–38
     [Google Scholar]
  98. 98.
    Lindow SE, Brandl MT. 2003. Microbiology of the phyllosphere. Appl. Environ. Microbiol. 69:1875–83
     [Google Scholar]
  99. 99.
    Lindow SE, Desurmont C, Elkins R, McGourty G, Clark E, Brandl MT 1998. Occurrence of indole-3-acetic acid-producing bacteria on pear trees and their association with fruit russet. Phytopathology 88:1149–57
     [Google Scholar]
  100. 100.
    Lindow SE, Hirano SS, Barchet WR, Arny DC, Upper CD. 1982. Relationship between ice nucleation frequency of bacteria and frost injury. Plant Physiol 70:1090–93
     [Google Scholar]
  101. 101.
    Lindow SE, Panopoulos NJ, McFarland BL. 1989. Genetic engineering of bacteria from managed and natural habitats. Science 244:1300–7
     [Google Scholar]
  102. 102.
    Liu F, Zhang JH, Zhang LJ, Diao MQ, Ling PX, Wang FS. 2021. Correlation between the synthesis of pullulan and melanin in Aureobasidium pullulans. Int. J. Biol. Macromol. 177:252–60
     [Google Scholar]
  103. 103.
    Liu W, Liu J, Triplett L, Leach J, Wang G-L. 2014. Novel insights into rice innate immunity against bacterial and fungal pathogens. Annu. Rev. Phytopathol. 52:213–41
     [Google Scholar]
  104. 104.
    Lo Presti L, Lanver D, Schweizer G, Tanaka S, Liang L et al. 2015. Fungal effectors and plant susceptibility. Annu. Rev. Plant Biol. 66:513–45
     [Google Scholar]
  105. 105.
    Longley R, Noel ZA, Benucci GMN, Chilvers MI, Trail F, Bonito G. 2020. Crop management impacts the soybean (Glycine max) microbiome. Front. Microbiol. 11:1116
     [Google Scholar]
  106. 106.
    Lozupone C, Faust K, Raes J, Faith JJ, Frank DN et al. 2012. Identifying genomic and metabolic features that can underline early successional and opportunistic lifestyles of human gut symbionts. Genome Res 22:1974–84
     [Google Scholar]
  107. 107.
    Ludwig N, Reissmann S, Schipper K, Gonzalez C, Assmann D et al. 2021. A cell surface-exposed protein complex with an essential virulence function in Ustilago maydis. Nat. Microbiol. 6:722–30
     [Google Scholar]
  108. 108.
    Lundberg DS, Pramoj Na Ayutthaya P, Strauß A, Shirsekar G, Lo W-S et al. 2021. Host-associated microbe PCR (hamPCR) enables convenient measurement of both microbial load and community composition. eLife 10:e66186
     [Google Scholar]
  109. 109.
    Ma A, Lv D, Zhuang X, Zhuang G. 2013. Quorum quenching in culturable phyllosphere bacteria from tobacco. Int. J. Mol. Sci. 14:14607–19
     [Google Scholar]
  110. 110.
    Ma KW, Ordon J, Schulze-Lefert P. 2022. Gnotobiotic plant systems for reconstitution and functional studies of the root microbiota. Curr. Protoc. 2:e362
     [Google Scholar]
  111. 111.
    Maier BA, Kiefer P, Field CM, Hemmerle L, Bortfeld-Miller M et al. 2021. A general non-self response as part of plant immunity. Nat. Plants 7:696–705Found expression of a core set of Arabidopsis genes and production of tryptophan-derived defense metabolites in response to microbiota bacterial members.
     [Google Scholar]
  112. 112.
    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
     [Google Scholar]
  113. 113.
    Manirajan BA, Ratering S, Rusch V, Schwiertz A, Geissler-Plaum R et al. 2016. Bacterial microbiota associated with flower pollen is influenced by pollination type, and shows a high degree of diversity and species-specificity. Environ. Microbiol. 18:5161–74
     [Google Scholar]
  114. 114.
    Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M et al. 2012. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol. Plant Pathol. 13:614–29
     [Google Scholar]
  115. 115.
    Marks RA, Smith JJ, Cronk Q, McLetchie DN. 2018. Variation in the bacteriome of the tropical liverwort, Marchantia inflexa, between the sexes and across habitats. Symbiosis 75:93–101
     [Google Scholar]
  116. 116.
    Masachis S, Segorbe D, Turrá D, Leon-Ruiz M, Fürst U et al. 2016. A fungal pathogen secretes plant alkalinizing peptides to increase infection. Nat. Microbiol. 1:16043
     [Google Scholar]
  117. 117.
    McCoy AG, Roth MG, Shay R, Noel ZA, Jayawardana MA et al. 2019. Identification of fungal communities within the tar spot complex of corn in Michigan via next-generation sequencing. Phytobiomes J 3:235–43
     [Google Scholar]
  118. 118.
    Miebach M, Schlechter RO, Clemens J, Jameson PE, Remus-Emsermann MNP. 2020. Litterbox—a gnotobiotic zeolite-clay system to investigate Arabidopsis–microbe interactions. Microorganisms 8:464
     [Google Scholar]
  119. 119.
    Mitter B, Pfaffenbichler N, Flavell R, Compant S, Antonielli L et al. 2017. A new approach to modify plant microbiomes and traits by introducing beneficial bacteria at flowering into progeny seeds. Front. Microbiol. 8:11
     [Google Scholar]
  120. 120.
    Monier J-M, Lindow SE. 2003. Differential survival of solitary and aggregated bacterial cells promotes aggregate formation on leaf surfaces. PNAS 100:15977–82
     [Google Scholar]
  121. 121.
    Moreira JCF, Brum M, de Almeida LC, Barrera-Berdugo S, de Souza AA et al. 2021. Asymbiotic nitrogen fixation in the phyllosphere of the Amazon forest: changing nitrogen cycle paradigms. Sci. Total Environ. 773:145066
     [Google Scholar]
  122. 122.
    Morella NM, Gomez AL, Wang G, Leung MS, Koskella B. 2018. The impact of bacteriophages on phyllosphere bacterial abundance and composition. Mol. Ecol. 27:2025–38
     [Google Scholar]
  123. 123.
    Morris MM, Frixione NJ, Burkert AC, Dinsdale EA, Vannette RL. 2020. Microbial abundance, composition, and function in nectar are shaped by flower visitor identity. FEMS Microbiol. Ecol. 96:fiaa003
     [Google Scholar]
  124. 124.
    Nadeem SM, Zahir ZA, Naveed M, Ashraf M. 2010. Microbial ACC-deaminase: prospects and applications for inducing salt tolerance in plants. Crit Rev. Plant Sci. 29:360–93
     [Google Scholar]
  125. 125.
    Nelson EB. 2018. The seed microbiome: origins, interactions, and impacts. Plant Soil 422:7–34
     [Google Scholar]
  126. 126.
    Nelson JM, Hauser DA, Li F-W. 2021. The diversity and community structure of symbiotic cyanobacteria in hornworts inferred from long-read amplicon sequencing. Am. J. Bot. 108:1731–44
     [Google Scholar]
  127. 127.
    Nelson JM, Shaw AJ. 2019. Exploring the natural microbiome of the model liverwort: fungal endophyte diversity in Marchantia polymorpha L. Symbiosis 78:45–59
     [Google Scholar]
  128. 128.
    Nemecek-Marshall M, MacDonald RC, Franzen JJ, Wojciechowski CL, Fall R. 1995. Methanol emission from leaves (enzymatic detection of gas-phase methanol and relation of methanol fluxes to stomatal conductance and leaf development). Plant Physiol 108:1359–68
     [Google Scholar]
  129. 129.
    Nobori T, Cao Y, Entila F, Dahms E, Tsuda Y et al. 2022. Dissecting the cotranscriptome landscape of plants and their microbiota. EMBO Rep 23:e55380Conducted a transcriptomic study of multiple Arabidopsis leaf microbiota strains showing enriched expression of microbiota genes putatively associated with bacterial adaptation to plant tissues.
     [Google Scholar]
  130. 130.
    Nobori T, Velasquez AC, Wu J, Kvitko BH, Kremer JM et al. 2018. Transcriptome landscape of a bacterial pathogen under plant immunity. PNAS 115:E3055–64
     [Google Scholar]
  131. 131.
    One Thousand Plant Transcript. Initiat 2019. One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574:679–85
     [Google Scholar]
  132. 132.
    Paasch BC, He SY. 2021. Toward understanding microbiota homeostasis in the plant kingdom. PLOS Pathog 17:e1009472
     [Google Scholar]
  133. 133.
    Paez-Espino D, Eloe-Fadrosh EA, Pavlopoulos GA, Thomas AD, Huntemann M et al. 2016. Uncovering Earth's virome. Nature 536:425–30
     [Google Scholar]
  134. 134.
    Peng Z, Oliveira-Garcia E, Lin G, Hu Y, Dalby M et al. 2019. Effector gene reshuffling involves dispensable mini-chromosomes in the wheat blast fungus. PLOS Genet 15:e1008272
     [Google Scholar]
  135. 135.
    Penuelas J, Staudt M. 2010. BVOCs and global change. Trends Plant Sci 15:133–44
     [Google Scholar]
  136. 136.
    Petlewski AR. 2020. Exploring Lycopodiaceae endophytes, Dendrolycopodium systematics, and the future of fern model systems. MS Thesis Cornell Univ. Ithaca, NY:
     [Google Scholar]
  137. 137.
    Pfeilmeier S, Petti GC, Bortfeld-Miller M, Daniel B, Field CM et al. 2021. The plant NADPH oxidase RBOHD is required for microbiota homeostasis in leaves. Nat. Microbiol. 6:852–64Reported evidence for a role of Arabidopsis RBOHD/F in controlling leaf microbiota homeostasis.
     [Google Scholar]
  138. 138.
    Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM. 2014. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52:347–75
     [Google Scholar]
  139. 139.
    Pozo MI, Lachance M-A, Herrera CM. 2012. Nectar yeasts of two southern Spanish plants: the roles of immigration and physiological traits in community assembly. FEMS Microbiol. Ecol. 80:281–93
     [Google Scholar]
  140. 140.
    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
     [Google Scholar]
  141. 141.
    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
     [Google Scholar]
  142. 142.
    Rico L, Ogaya R, Terradas J, Peñuelas J. 2014. Community structures of N2-fixing bacteria associated with the phyllosphere of a Holm oak forest and their response to drought. Plant Biol 16:586–93
     [Google Scholar]
  143. 143.
    Rolfe SA, Griffiths J, Ton J. 2019. Crying out for help with root exudates: adaptive mechanisms by which stressed plants assemble health-promoting soil microbiomes. Curr. Opin. Microbiol. 49:73–82
     [Google Scholar]
  144. 144.
    Roussin-Léveillée C, Lajeunesse G, St-Amand M, Veerapen VP, Silva-Martins G et al. 2022. Evolutionarily conserved bacterial effectors hijack abscisic acid signaling to induce an aqueous environment in the apoplast. Cell Host Microbe 30:489–501.e4
     [Google Scholar]
  145. 145.
    Roy D, Melotto M. 2019. Stomatal response and human pathogen persistence in leafy greens under preharvest and postharvest environmental conditions. Postharvest Biol. Technol. 148:76–82
     [Google Scholar]
  146. 146.
    Sah SK, Reddy KR, Li J. 2016. Abscisic acid and abiotic stress tolerance in crop plants. Front. Plant. Sci. 7:571
     [Google Scholar]
  147. 147.
    Santos-Medellín C, Edwards J, Liechty Z, Nguyen B, Sundaresan V. 2017. Drought stress results in a compartment-specific restructuring of the rice root-associated microbiomes. mBio 8:e00764-17
     [Google Scholar]
  148. 148.
    Saravanakumar D, Samiyappan R. 2007. ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J. Appl. Microbiol. 102:1283–92
     [Google Scholar]
  149. 149.
    Sarver J, Schultz E, Apigo A, Gernandt DS, Salas-Lizana R, Oono R. 2022. Deep sequencing across multiple host species tests pine-endophyte specificity. Am. J. Bot. 109:83–98
     [Google Scholar]
  150. 150.
    Satjarak A, Golinski GK, Trest MT, Graham LE. 2022. Microbiome and related structural features of Earth's most archaic plant indicate early plant symbiosis attributes. Sci. Rep. 12:6423
     [Google Scholar]
  151. 151.
    Savory EA, Fuller SL, Weisberg AJ, Thomas WJ, Gordon MI et al. 2017. Evolutionary transitions between beneficial and phytopathogenic Rhodococcus challenge disease management. eLife 6:e30925
     [Google Scholar]
  152. 152.
    Schierstaedt J, Grosch R, Schikora A. 2020. Agricultural production systems can serve as reservoir for human pathogens. FEMS Microbiol. Lett. 366:fnaa016
     [Google Scholar]
  153. 153.
    Seo KH, Frank JF. 1999. Attachment of Escherichia coli O157:H7 to lettuce leaf surface and bacterial viability in response to chlorine treatment as demonstrated by using confocal scanning laser microscopy. J. Food Prot. 62:3–9
     [Google Scholar]
  154. 154.
    Shade A, McManus PS, Handelsman J. 2013. Unexpected diversity during community succession in the apple flower microbiome. mBio 4:e00602–12
     [Google Scholar]
  155. 155.
    Sharma S, Kashyap PL, Sharma A 2021. Plant virome: current understanding, mechanisms, and role in phytobiome. Microbiomes and Plant Health MK Solanki, PL Kashyap, RA Ansari, B Kumari 53–81. London: Academic
     [Google Scholar]
  156. 156.
    Song L, Xie K. 2020. Engineering CRISPR/Cas9 to mitigate abundant host contamination for 16S rRNA gene-based amplicon sequencing. Microbiome 8:80
     [Google Scholar]
  157. 157.
    Song Y, Wilson AJ, Zhang X-C, Thoms D, Sohrabi R et al. 2021. FERONIA restricts Pseudomonas in the rhizosphere microbiome via regulation of reactive oxygen species. Nat. Plants 7:644–54
     [Google Scholar]
  158. 158.
    Spaepen S, Vanderleyden J, Remans R. 2007. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. Rev. 31:425–48
     [Google Scholar]
  159. 159.
    Stukenbrock EH, Christiansen FB, Hansen TT, Dutheil JY, Schierup MH. 2012. Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species. PNAS 109:10954–59
     [Google Scholar]
  160. 160.
    Su D, Yang L, Shi X, Ma X, Zhou X et al. 2021. Large-scale phylogenomic analyses reveal the monophyly of bryophytes and neoproterozoic origin of land plants. Mol. Biol. Evol. 38:3332–44
     [Google Scholar]
  161. 161.
    Sullivan BW, Smith WK, Townsend AR, Nasto MK, Reed SC et al. 2014. Spatially robust estimates of biological nitrogen (N) fixation imply substantial human alteration of the tropical N cycle. PNAS 111:8101–6
     [Google Scholar]
  162. 162.
    Teixeira PJPL, Colaianni NR, Law TF, Conway JM, Gilbert S et al. 2021. Specific modulation of the root immune system by a community of commensal bacteria. PNAS 118:e2100678118
     [Google Scholar]
  163. 163.
    Thynne E, Saur IML, Simbaqueba J, Ogilvie HA, Gonzalez-Cendales Y et al. 2017. Fungal phytopathogens encode functional homologues of plant rapid alkalinization factor (RALF) peptides. Mol. Plant Pathol. 18:811–24
     [Google Scholar]
  164. 164.
    Toruño TY, Stergiopoulos I, Coaker G. 2016. Plant-pathogen effectors: cellular probes interfering with plant defenses in spatial and temporal manners. Annu. Rev. Phytopathol. 54:419–41
     [Google Scholar]
  165. 165.
    Traveset A. 1998. Effect of seed passage through vertebrate frugivores' guts on germination: a review. Perspect. Plant Ecol. Evol. Syst. 1:151–90
     [Google Scholar]
  166. 166.
    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]
  167. 167.
    Tuomi T, Ilvesoksa J, Laakso S, Rosenqvist H. 1993. Interaction of abscisic acid and indole-3-acetic acid-producing fungi with Salix leaves. J. Plant Growth Regul. 12:149–56
     [Google Scholar]
  168. 168.
    Tyler HL, Triplett EW. 2008. Plants as a habitat for beneficial and/or human pathogenic bacteria. Annu. Rev. Phytopathol. 46:53–73
     [Google Scholar]
  169. 169.
    van Bruggen AHC, Goss EM, Havelaar A, van Diepeningen AD, Finckh MR, Morris JG Jr. 2019. One Health—cycling of diverse microbial communities as a connecting force for soil, plant, animal, human and ecosystem health. Sci. Total Environ. 664:927–37
     [Google Scholar]
  170. 170.
    Vannette RL. 2020. The floral microbiome: plant, pollinator, and microbial perspectives. Annu. Rev. Ecol. Evol. Syst. 51:363–86
     [Google Scholar]
  171. 171.
    Vannier N, Agler M, Hacquard S. 2019. Microbiota-mediated disease resistance in plants. PLOS Pathog 15:e1007740
     [Google Scholar]
  172. 172.
    Velásquez AC, Huguet-Tapia JC, He SY. 2022. Shared in planta population and transcriptomic features of nonpathogenic members of endophytic phyllosphere microbiota. PNAS 119:e2114460119Conducted long-term population and transcriptomic analyses providing evidence for common adaptive strategies among commensals and disarmed bacterial pathogens in the leaf apoplast.
     [Google Scholar]
  173. 173.
    Venkatachalam S, Ranjan K, Prasanna R, Ramakrishnan B, Thapa S, Kanchan A. 2016. Diversity and functional traits of culturable microbiome members, including cyanobacteria in the rice phyllosphere. Plant Biol 18:627–37
     [Google Scholar]
  174. 174.
    Viterbo A, Landau U, Kim S, Chernin L, Chet I 2010. Characterization of ACC deaminase from the biocontrol and plant growth-promoting agent Trichoderma asperellum T203. FEMS Microbiol. Lett. 305:42–48
     [Google Scholar]
  175. 175.
    Vogel CM, Potthoff DB, Schäfer M, Barandun N, Vorholt JA. 2021. Protective role of the Arabidopsis leaf microbiota against a bacterial pathogen. Nat. Microbiol. 6:1537–48
     [Google Scholar]
  176. 176.
    von Arx M, Moore A, Davidowitz G, Arnold AE. 2019. Diversity and distribution of microbial communities in floral nectar of two night-blooming plants of the Sonoran Desert. PLOS ONE 14:e0225309
     [Google Scholar]
  177. 177.
    von Bodman SB, Bauer WD, Coplin DL. 2003. Quorum sensing in plant-pathogenic bacteria. Annu. Rev. Phytopathol. 41:455–82
     [Google Scholar]
  178. 178.
    Vorholt JA. 2012. Microbial life in the phyllosphere. Nat. Rev. Microbiol. 10:828–40
     [Google Scholar]
  179. 179.
    Wahdan SFM, Tanunchai B, Wu Y-T, Sansupa C, Schädler M et al. 2021. Deciphering Trifolium pratense L. holobiont reveals a microbiome resilient to future climate changes. MicrobiologyOpen 10:e1217
     [Google Scholar]
  180. 180.
    Wang Y, Pruitt RN, Nürnberger T, Wang Y. 2022. Evasion of plant immunity by microbial pathogens. Nat. Rev. Microbiol. 20:449–64
     [Google Scholar]
  181. 181.
    Wang Y, Wang Y. 2018. Phytophthora sojae effectors orchestrate warfare with host immunity. Curr. Opin. Microbiol. 46:7–13
     [Google Scholar]
  182. 182.
    Whipps JM, Hand P, Pink D, Bending GD. 2008. Phyllosphere microbiology with special reference to diversity and plant genotype. J. Appl. Microbiol. 105:1744–55
     [Google Scholar]
  183. 183.
    Wolinska KW, Vannier N, Thiergart T, Pickel B, Gremmen S et al. 2021. Tryptophan metabolism and bacterial commensals prevent fungal dysbiosis in Arabidopsis roots. PNAS 118:e2111521118
     [Google Scholar]
  184. 184.
    Wright KM, Crozier L, Marshall J, Merget B, Holmes A, Holden NJ. 2017. Differences in internalization and growth of Escherichia coli O157:H7 within the apoplast of edible plants, spinach and lettuce, compared with the model species Nicotiana benthamiana. Microbiol. Biotechnol. 10:555–69
     [Google Scholar]
  185. 185.
    Xin XF, Kvitko B, He SY. 2018. Pseudomonas syringae: what it takes to be a pathogen. Nat. Rev. Microbiol. 16:316–28
     [Google Scholar]
  186. 186.
    Xin XF, Nomura K, Aung K, Velasquez AC, Yao J et al. 2016. Bacteria establish an aqueous living space in plants crucial for virulence. Nature 539:524–29
     [Google Scholar]
  187. 187.
    Yang CH, Crowley DE, Borneman J, Keen NT. 2001. Microbial phyllosphere populations are more complex than previously realized. PNAS 98:3889–94
     [Google Scholar]
  188. 188.
    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]
  189. 189.
    Yao H, Sun X, He C, Maitra P, Li X-C, Guo L-D. 2019. Phyllosphere epiphytic and endophytic fungal community and network structures differ in a tropical mangrove ecosystem. Microbiome 7:57
     [Google Scholar]
  190. 190.
    Yu K, Liu Y, Tichelaar R, Savant N, Lagendijk E et al. 2019. Rhizosphere-associated Pseudomonas suppress local root immune responses by gluconic acid-mediated lowering of environmental pH. Curr. Biol. 29:3913–20.e4
     [Google Scholar]
  191. 191.
    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:E425–34Presented a transcriptomic analysis of Pseudomonas syringae during the epiphytic and endophytic phases in bean leaves.
     [Google Scholar]
  192. 192.
    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
     [Google Scholar]
  193. 193.
    Zengler K, Hofmockel K, Baliga NS, Behie SW, Bernstein HC et al. 2019. EcoFABs: advancing microbiome science through standardized fabricated ecosystems. Nat. Methods 16:567–71
     [Google Scholar]
  194. 194.
    Zhang X, Peng H, Zhu S, Xing J, Li X et al. 2020. Nematode-encoded RALF peptide mimics facilitate parasitism of plants through the FERONIA receptor kinase. Mol. Plant 13:1434–54
     [Google Scholar]
  195. 195.
    Zheng W, Zhao S, Yin Y, Zhang H, Needham DM et al. 2022. High-throughput, single-microbe genomics with strain resolution, applied to a human gut microbiome. Science 376:eabm1483
     [Google Scholar]
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Phyllosphere Microbiome
Annual Review of Plant Biology 74, 539 (2023); https://doi.org/10.1146/annurev-arplant-102820-032704
/content/journals/10.1146/annurev-arplant-102820-032704
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